Below I discuss briefly major characters in the order in which they will be encountered when mentioned in the characterizations. The emphasis in this section is on providing entries both to the general literature, but especially to articles where there is much information on the variation of a single character; I sometimes also give an indication of how good the sampling is - all too often it is very bad. Definitions of the characters mentioned here and of related features are provided in the Glossary. Note, however, that these characters and the "states" I use in describing the variation within them should not simply be converted into data for phylogenetic analysis. Some, for example, fruit types, may be logically connected with the nature of the gynoecium, and often, as with fruit types themselves, seedling morphology, pollen, testa and tegmen types, they may each yield a dozen or more of more or less individually varying characters. Furthermore, in these and many other characters the states we talk about may well be arbitrarily delimited. This does not mean that they are always useless, but it does mean that they do not necessarily refer to anything "real" in the world (see the Introduction for more discussion) and they are essential to enabling discussion (e.g. E. J. Edwards 2023). It should also be remembered that because the same term is used for features in two groups, it cannot be assumed that this entails a hypothesis that the structures in the two had a common evolutionary origin, i. e., that they are homologous under one definition of the term. However, if botanical terms were reformulated so as to refer only to synapomorphies (shared derived features), changes in the terms we use would be almost innumerable and botanical discourse would become nigh on impossible. Although an indication of how useful a character is systematically - i.e., how much it varies, and its general pattern of variation - may be given below, it will soon become clear that in general, even if a feature is strongly supported as being an apomorphy for a clade in one part of the tree, it will a) likely be lost in that same clade, and b) vary elsewhere (e.g. Stebbins 1951). Finally, it should be remembered that ecological and systematic definitions of characters of flowers, fruits and seeds in particular may be at odds; the definitions and circumscriptions adopted will depend on the purpose of the study, and animals like ants, for instance, are notorious for being totally unconcerned whether the seed they are about to carry off has a sarcotesta or an aril - or even if it is a seed at all. See also the Plant Ontology Consortium.
There are of course many other features mentioned in individual family characterisations. For these, general distributions may be unknown or not really of much interest because the feature is varying in a phylogenetically informative fashion only locally, although I try to provide context for these features where necessary.
I cannot emphasize enough the value of much older literature, especially that from ca 1870-1920. There one can find surveys of various aspects of plant anatomy and morphology for individual characters or for plant groups that have never been improved since, and I mention such work frequently. Of course, not all of this literature is helpful - it can be difficult to understand, one has to be careful about the names used, etc. - but in all too many cases it still provides most of the information we have. Work in which the evolution of individual organs or organ systems are discussed outside any immediate phylogenetic context, but rather from the point of view of particular a priori theories of plant morphology, are much less easy to use. Kaplan (2001a) concisely summarized the different approaches of the great practitioners in the far-from-monolithic German tradition; looking back, the meticulous and comprehensive surveys of various aspects of plant form and anatomy by Hofmeister (e.g. 1849, 1851, 1868), Nageli (1858), and de Bary (1884), and more recently von Goebel (e.g. 1932), Troll (e.g. 1969, 1971) and the like have never been equalled - and in the four volumes of Kaplan (1997) much of this and subsequent literature is synthesized (see also Kaplan 2001a, 2022). The task is to put their findings in a phylogenetic context... I have also necessarily relied much on the secondary literature, for instance, there is much information in Engler (1900-onwards) and Engler and Prantl (1887-1915; Ed. 2, 1924-onwards - cited under individual authors), Airy Shaw (1966), Hutchinson (1973), Cronquist (1981), Goldberg (1986, see also 2003), Mabberley (2017), Takhtajan (1997: beware of typographical errors!, 2009), and N. Smith et al. (2004). The meticulously-documented series of papers that make up the Generic Flora of the Southeastern United States (ed. C. E. Wood Jr.) and of course the monumental series of volumes edited by Kubitzki and others (1993a onwards) have been invaluable; contributions to these two endeavours are cited individually. Much information is summarized in Rolf Dahlgren's diagrams (e.g. Dahlgren 1975a) and is included in recent large-scale phylogenies (e.g. Hufford 1992: Rosidae; Nandi et al. 1998: all flowering plants). Zomlefer (1994) was helpful, especially early on. Information on many characters mentioned below is taken from these references and also from the general references mentioned at the beginning of each character group; this is definitely not the best method of documentation (see Introduction).
The discussion in this section is very much atomistic in that the plant is dissected into bits and pieces that are for the most part considered separately. However, one will also want to know whether a part in one species is "the same" as that in another. For basic comparisons, thinking about what you are looking at in the context of Remane's three main criteria of "homology"/similarity, i.e., special properties, position, and intermediates, is definitely the way to go (see Remane 1952; Kaplan 1997: vol. 1 ch. 1, 2022). Whether or not features are homologous in the strict sense will also depend on putting the features into a phylogenetic context. For an approach which considers the plant as a whole, with changes affecting above- and below-ground parts simultaneously, and from a topological point of view - i.e. looking at the "relationships between objects that are maintained under deformations to a structure, but not tearing" , see e.g. Li et al. (2017a: p. , 2017b, 2018 and references), and this leads to the consideration of the mathematical concept of persistent homology. See also process morphology (Kirchoff et al. 2008 and references).
Plant architecture. Hallé et al. (1978; see Guédès 1983 for a criticism) list a number of architectural models, growth patterns based on variation in a number of growth characters and to which plants may be assigned (see Hallé 2004; Millet 2012; esp. Bell & Bryan 2008; Hollender & Dardick 2015: molecular basis of architecture; Chomicki et al. 2017b: architecture in fossil plants, 12 new models; Chomicki et al. 2018: models in herbs). Plant models are rarely mentioned here except in passing since they are not often constant in taxa of any size and the general approach is usually typological; a large number of "models" could be named if the variation discussed by Hallé et al. (1978) were applied consistently. However, the individual characters that Hallé et al. (1978) discuss, e.g., ortho- and plagiotropy (the latter in particular comes in various flavours), and continuous and discontinuous (rythmic) and monopodial and sympodial growth, may be mentioned individually in the characterisations and discussions. Thinking of plant growth in terms of these variables is very helpful, much more so than thinking of models per se (see also Barthélémy et al. 1989; Barthélémy & Caraglio 2007; etc.).
At the same time, there are general universal (to flowering plants, at least) scaling relationships in growth such as that between branch thickness and leaf size (Corner's Rule - see Corner 1949b, 1953), vessel diameter and stem length, rather than climate, etc. (Olsen et al. 2014), rate of biomass production, differences in wood density and growth rate (Enquist et al. 1999), etc., that suggest that a number of aspects of growth, etc., should not be considered separately (see also Enquist 2002; Enquist et al. 2007). Thus Olson et al. (2009: p. 217) emphasized some "causal links between stem size, branching frequency, leaf size, stem tissue density, stem growth rate, and carbon assimilation rates, and suggest that this interplay produces the well-known pattern Corner's Rules."
Poorter et al. (2006) analyse architectural s. l. traits in moist Bolivian forests, finding four functional groups there. León Enriquez et al. (2008) examined variation in plant models in the context of phylogeny in Phyllanthaceae, and found that whether growth was rythmic or continuous correlated well with the major clades recognized, and growth characters also vary in an interesting way within Fagraea (Wong & Sugumaran 2012).
How are the growth patterns that result in these architectural models produced? Costes et al. (2008) show how growth forms of trees can be generated given the careful specification of appropriate starting variables. Prusinkiewicz and Barbier de Reuille (2010: p. 2125) discuss tree form from the point of view of "a competitive, self-organizing process through which branching forms emerge", contrasting this with an approach that emphasizes a "precisely controlled genetic program which determines their development" of Hallé and Oldeman (1978, p. 74) (see also Palubicki et al. 2009; also leaf insertion, form, and venation, inflorescence morphology, etc., below). "Models" are the result of the interaction of internal variables (hormones, nutrient flow, etc.) with the external environment.
Habit is indicated only in a very general fashion in the characterizations. However, habit/life form classifications are ways of looking at whole-plant morphology in the context of ecology and function. For an interesting survey and categorization of plant life forms that emphasizes the position of resting buds, see Raunkiaer (1934); Dulin and Kirchoff (2010) discuss the occurrence of secondary thickening in plants variously and confusingly called herbs/annuals/therophytes while Ellenberg and Mueller-Dombois (1967) provide a key to a revised Raunkiaer system. Du Rietz (1931) is another approach to categorizing growth forms, Barkman (1988) provides a more recent discussion of growth forms and phenology, while von Willert et al. (1990) suggest that the term growth form refers more to architectural features of the plant (see Plant Architecture above). For rheophytes, plants growing in or near flowing water and often with distinctive narrow leaves, see van Steenis (1981, 1987) and Boyce and Wong (2020), for growth forms of aquatic plants, see Schuyler (1984) and Cook (1996), and for the evolution of the cushion growth form, particularly common in alpine-type environments, see Boucher et al. (2016b).
Some plants trap litter, and such plants have a rather distinctive habit. Litter may be trapped in basket-like structures formed by negatively geotropic roots or in appropriately oriented and arranged leaves (the plant may then have a Schopfbaum-type habit), as is discussed by Zona and Christenhusz (2015). Ortega-Solis et al. (2021) have recently surveyed what they call trash basket epiphytes, some 209 species of epiphytes that collect litter; most common in Araceae and Polypodiaceae, this group of plants includes practically no Bromeliaceae, in which there are of course numerous tank epiphytes which also may trap litter. The growth of monocots, predominantly a perennial herbaceous group but also with some woody clades, woodiness variously achieved, can be interpreted as variations on a basically sympodial and often hypogeal (subterranean) theme (Holttum 1955).
Groover (2005) discussed the multiple derivations of the herbaceous life form from the woody, and the reverse; the latter transition can often be detected by the presence of distinctive details of xylem anatomy (see e.g. Carlquist 2009; Lens et al. 2012) and is mentioned under individual families. (However, the distinction between herbaceous and woody plants can be difficult to make - e.g. Lens et al. 2012b; Kidner et al. 2015.). Annuals have evolved many times in angiosperms, alone among vascular plants, frequently as a response to hot/dry/disturbed conditions, and there have been reversals to the perennial condition (J.-C. Wang et al. 2016; Azani et al. 2019 and references). As discussed elsewhere, although secondary growth may not seem to occur in annuals (but see Krumbiegel & Kástner 1993) the ability to carry out secondary growth is rarely completely lost in annual clades - c.f. water plants. For secondary woodiness, especially on (sky) islands, see e.g. Dulin and Kirchoff (2010) and Nürk et al. (2019).
Vegetative dormancy in which above-ground shoots do not appear every year is quite widespread but probably much underrecorded in angiosperms, whether mycoheterotrophic, mixotrophic or autotrophic (Reintal et al. 2010; Shefferson et al. 2018; Hurskainen et al. 2018).
For a survey of vascular epiphytes, often herbaceous plants, see Madison (1977), Kress (1986a, 1969) and Gentry and Dodson (1987). Zotz (2013) and in particular Zotz et al. (2021b) provide a checklist of vascular epiphytes, some 31,300 species (including hemiepiphytes and facultative epiphytes) in 79 families, perhaps 10% of all vascular plants (Tay et al. 2023). Some two thirds of all vascular plants in the lowland Amazon basin are not self-suporting plants, and these include hemiepiphytes and nomadic vines, the latter being much more common than hemiepiphytes (CLemente-Arenas et al. 2022); nomadic vines germinate in the soil, they then climb the plant, but their roots and/or stems eventually lose contact with the ground. Here roots are "adventitious", and the plant may "abandon" its roots as it grows through the canopy; extractable nitrogen and phosphorus content of the soil (it differs in sandy and clay soils, and P in the soil may have a distinct effect on true epiphyte composition), etc., are important when thinking of where plants with such life styles grow, also the neighbouring trees, although bark texture was perhaps surprisingly less important (Boelter et al. 2014; Clemente-Arenas et al. 2022). See also Benzing (1990) for a general discussion and Zotz (2016), Hietz et al. (2021), K. Wagner et al. (2021) and Zotz et al. (2021a), etc., for the ecophysiological features of epiphytes - they are on the slow end of the Leaf Economic Spectrum (note that features of the roots, the plant as a whole, seeds, etc., of epiphytes are not often studied). Most embryophytic epiphytes - although some bryophytes s.l. growing on leaves are exceptions - grow on twigs and trunks of vascular plants. Here there is considerable variation in bark surface texture, but Tay et al. (2023) note that the importance of features of the bark for the epiphyte depends on how the plant - whether seed or adult - attaches to the plant and the relative sizes of the structures involved. Adhesion mechanisms - root secretions, for instance - tend to preponderate when the bark is more or less smooth, interlocking mechanisms, as when a root grows into a crevice, maybe swelling as it does so, are commoner on rough surfaces. There is also the question of how one measures roughnesss (Tay et al. 2023). Schuettpelz (2007) and Dubuisson et al. (2009) discuss epiphytism in ferns, and there the particularly long-lived gametophytes can be important; of course, many bryophytes, also gametophytes, are epiphytes. Many Orchidaceae are epiphytes, but particularly noteworthy here are the 300+ species of Epidendroideae-Vandeae which have a plant body that consists very largely of relatively large and sometimes flattened photosynthesizing roots (Carlsward et al. 2006a; Suetsugu et al. 2023). Features - some related - like dessication tolerance, CAM photosynthesis, low rates of stomatal conductance, low growth rates, lower photosynthetic rates, lower leaf nitrogen, etc., are also associated with the adoption of the epiphytic habit (North et al. 2018; Hietz et al. 2021, and references). CAM photosynthesis is not found in all epiphytic groups (Holtum et al. 2007) and it may be more common in epiphytes growing in dry habitats than those growing in rainforest, however, in Central Brazil the overall proportion of CAM epiphytes was higher in flooded gallery forests (78%) than in non-flooded forests (ca 10%) - one might have expected more CAM plants in drier habitats (de Paula Oliveira et al. 2020). For the scanty fossil evidence of epiphytes, see e.g. Rößler (2000) and Bippus et al. (2019). Woody epiphytes are poorly known.
For a summary of carnivorous plants, see e.g. Chase et al. (2009c), Schlauer (2010), esp. Givnish et al. (2018a), papers in Ellison and Adamec (2018), the Carnivorous Plants Database, and Fleck and Jobson (2023: esp. relationships). Carnivorous plants may have a flat leaf surface, either sticky or with glandular hairs, or snap traps or various kinds of bladders or pitchers. A number of other plants have sticky glandular hairs, and such plants are suspected of being at least protocarnivorous, being able to digest proteins (?source of enzymes) and take up at least some of the products of the insects stuck on the hairs (Spomer 1999). Indeed, carnivory has recently been demonstrated in such a situation in Triantha occidentalis (Tofieldiaceae) by Q. Lin et al. (2021); this is unlikely to be a unique situation. Carnivory in similar situations may be indirect, as when mirid bugs of subtribe Dicyphina are involved, the plant then absorbing nutrients from the excreta of the insects that are released by their microbial breakdown (e.g. Chase et al. 2009c; Gonçalves et al. 2011; Wheeler & Krimmel 2015; Selosse et al. 2017c, Hartmeyer & Hartmeyer 2022). Karban et al. (2019) found that in Nicotiana attenuata with its sticky hairs that the number of insects trapped ∝ (positively) the number of predators of those insects ∝ seed capsules produced. This is the "assisted carnivory" of Obregon (2017: p. 74) looking at the behaviour of the mirid Cyrtopeltis (?= Nesidiocoris) eating insects stuck to his cultivated Roridula. Even if plants with glandular hairs are not directly or indirectly involved in carnivory, the insects that they trap may attract yet other insects that protect the plant (Romero et al. 2008; LoPresti et al. 2015: also a list). All known carnivorous plants also carry out photosynthesis and so are mixotrophic, "necrotrophic mixotrophy" (Selosse et al. 2017c; for mixotrophy, see also Tešitel et al. 2018). Paungfoo-Lonhienne et al. (2010) found that nitrogen from Escherichia coli and Saccharomyces cerevisiae that had entered intact roots of tomato and Arabidopsis was used by the plants as the protists were broken down, so perhaps these plants are also technically carnivorous... (see also Selosse et al. 2017c). Indeed, the distinction between carnivorous and non-carnivorous plants is not clear (e.g. Hartmeyer & Hartmeyer 2022); it would seem that the production of digestive enzymes by the plant might be key in the distinction between the two. Carnivory is a much reviewed topic, e.g. Adamec (2011b), Rice (2011), Ellison and Adamec (2018), Fleischmann et al. (2018a: evolution), Hatcher et al. (2020), Adamec et al. (2021), Freund et al. (2022: glands and digestion), Fleck and Johnson (2023: relationships in the Angiosperms353 phylogeny), etc..
For lianes, see also branching. There are around 10,000 species of lianes/vines in some 98 families of seed plants in the Neotropics alone, the precise number of species depending on exactly what else is needed other than "climber" to be included in any particular list; the number of genera and families oscillates depending on current taxonomic practice (see e.g. Gentry 1991; Caballé 1993; Sperotto et al. 2023). There are estimates of there being at least 40,000 and possibly more than 53,000 species of trees (ca 10≤ cm d.b.h.) in the tropics (Slik et al. 2015) with climbers being 18% of continental tropical floras to ca 35% of woody plants - clearly, estimates (and any estimate of climber numbers) vary widely (Gentry 1991; Schnitzer 2018). Estimates of the number of climbers in more temperate regions are lower, for example, those in Krings (2000) are ca 4-7.5% of the flora. A guesstimate of the number of species of climbers would be around 30,000... Rowe and Speck (2005), Schnitzer and Bongers (2002) and Sperotto et al. (2023), for example, discuss the ecology of climbers, and there is also general information in Darwin (1867), Schenck (1892), Putz and Mooney (1991), Schnitzer et al. (2015) and so on. Climbing may be with the aid of tendrils (both twining stems and modified leaves, etc., are included here - Sousa-Baena et al. 2018) to establish contact with supports, grapnels being the another main modification, also roots (see Krings et al. 2003 for comparable modifications in Carboniferous climbers). Chery et al. (2021) discuss the importance of G(gelatinous)-fibres developing the movement in both twining stems and tendrils - they are also involved in gravitropic movements, etc.. Givnish and Vermeij (1976) describe the leaf shape, etc., of lianas - cordate leaf blades on ascending, rigid petioles are common. Lianas are interesting hydraulically in that under dry conditions they maintain a high hydraulic conductance yet are not compromised by the development of embolisms that would occur in trees growing under similar conditions (van der Sande et al. 2019), although exactly how they do this is unclear (Schnitzer 2018). Since vessel diameter scales with stem length, and lianas have long narrow stems, their vessels are proportionally wide... (Olson et al. 2014). Bouda et al. (2019) looked at how ca 15% of the water flow of wide vessels in grapes was diverted into narrow vessels. Lianas in general grow remarkably well in the dry season, proportionally much more than trees (Schnitzer et al. 2019, see also Schnitzer 2018 for the various habitats in which lianas are prominent).
Sperotto et al. (2023) look at New World climbers to see what correlations there might be between how the plant climbs and geography, ecology, diversification, etc.. Of the 9,071 New World vines for which they had data, they found that 4,291, 42% climbed by twining, the next three kinds of climbers, by tendrils, simply scrambling (this included members of the most families), and adhesive roots, added 53%, while all the other kinds of climbers added a mere 5%. Climbers were relatively abundant in the dry diagonal of South America, Overall, Sperotto et al. (2023) found little in the way of correlations. Indeed, Sperotto et al. (2023) remind us that much more is needed for a plant to be a climber than simply how it climbs, as will be evident from the discussion in the previous paragraph.
Lianas are woody and vines are more or less herbaceous, and they often have distinctive growth with anomalous patterns of secondary thickening/vascular variants, and the number of cambia, their position, the nature of the tissue in which they originate and the nature of that they produce, all vary considerably (e.g. Obaton 1960; Philipson et al. 1971; Carlquist 1991b; Caballé 1993; Rowe & Speck 2005; Angyalossy et al. 2012; Isnard & Feild 2015: esp. function; Angyalossy et al. 2015; Rowe & Speck 2015: esp. biomechanics; Luna-Márquez et al. 2021; Nejapa et al. 2021; Cunha Neto 2023). In some cases this odd secondary thickening seems to increase stem flexibility, always important for climbers (e.g. Isnard & Rowe 2008a; Leme et al. 2021; see also Putz & Mooney 1991; Schnitzer et al. 2015 and references), and water transport is also an issue (Bouda et al. 2019; Chery et al. 2019b, 2020 and references). There has been widespread convergence in the anatomy of angiosperm, gymnosperm and pteridophyte lianas, and within angiosperms, convergence of liana anatomy in groups like Fabaceae-Papilionoideae, such that there is a distinctive anatomical syndrome, the "lianescent vascular syndrome" (Angyalossy et al. 2015; Chery 2019b and references; Leme et al. 2021) for lianas that is readily recognizable, even in fossils. At the same time successive/ectopic cambia, commonly found in lianas, can develop in different ways, e.g. they may originate from the cortex or the phloem parenchyma (Nejapa et al. 2021). Leme et al. (2021) note that, comparing lianes with trees in Fabaceae-Faboideae, the former have wider (but varying considerably in size) and more numerous vessels that occupy much more of the wood (25% versus 6% in t.s.), more axial and radial parenchyma compared to fibres, taller rays, longer fibres, and so on - scoring of apomorphies in clades in which the liana habit is itself an apomorphy becomes a little tricky. Lima et al. (2023) note that when lianes attach to their support there are major changes in xylem anatomy, the xylem transcriptional profile, etc.. There is growth competition between lianes and their supporting trees, and the results may favour the former in the dry season, but in some species liane growth seems to be favoured in the wet season (Venegas-González et al. 2020).
Much has been written about succulent plants plants, often with a focus on those that are drought avoiders, although succulence is also associated with salt tolerance (see above: Ogburn & Edwards 2010) and with the epiphytic habit, as in many Orchidaceae - there are over 4,500 species of succulents there alone (Eggli & Nyffeler 2023). Succulent plants are usually either stem or leaf succulents, as in Cactaceae and Aizoaceae respectively. Eggli and Nyffeler (2009), Ogburn and Edwards (2010) and others have noted how hard it is to define succulence clearly - thus Tillandsia usneoides is ecophysiologically, even if not morphologically, a succulent. For general surveys of succulent plants see also von Willert et al. (1990), Eggli (2001, 2002: dicots, 2003: Crassulaceae), Eggli and Nyffeler (2009, 2020, 2023), Nyffeler and Eggli (2010b), Hearn et al. (2013) and Hartmann (2017: Aizoaceae). Most of these latter references are to the Illustrated Handbook of Succulent Plants, now in its second edition and with a rather complicated publication history (see Eggli & Nyffeler 2023: pp. ix-xiv); all succulent species are described.
Geophytes. Geophytes are plants with underground storage organs, or plants with buds at or below ground level (for the latter, see Tribble et al. 2021), and these include bulbs, corms, root tubers, stem tubers, and so on. Procheŝ et al. (2006) noted the richness of the geophytic flora in the Cape region of South Africa, while at the same time they observed how hard it was to define a geophyte - a perennial refrain. Plants with rhizomes may be particularly difficult to categorize - in some, like Solidago and Aster, the rhizomes are thin yet the plants still persist through the winter and their buds are underground, while in others, like some species of Iris, the thizomes are much stouter, yet in neither case are they often called geophytes (but see Tribble et al. 2021). Geophytes are perhaps particularly common in some monocot groups (Tribble et al. 2021). Tribble et al. (2022) examined possible connections between different kinds of geophytes in Liliales - geophytes are common here - and climate, but found that the climatic niches occupied by bulbs, corms, etc., were all largely similar, differing no more than expected by chance. The exception was plants with root tubers, as in Alstroemeriaceae-Alstroemerieae, which showed significantly different lower temperature seasonality. Tribble et al. (2020/2021) had earlier found that different kinds of geophytes had some gene groups in common (the focus of their work was Bomarea multiflora and its root tubers), although other groups that had been implicated in geophyte development seemed notably similar in root tubers and fibrous roots. They thought that "repeated morphological convergence may be matched by independent evolutions of similar molecular mechanisms" (ibid. p. ). Another topic really: For the bizarre leaf morphologies of plants, mostly geophytes and especially Eriospermum (Convallarioideae - it is often tuberous), from Namaqualand, an arid coastal region of Namibia and South Africa, see Vogel and Müller-Doblies (2011).
Geoxyles are large woody structures that are formed below ground by plants in grasslands and savannas and enable the plants that make them to survive disturbance, perhaps most notably fires, by producing shoots from these structures (e.g. Courtenay et al. 2023). They form the celebrated "underground forests of Africa" of Frank White (White 1976) that include plants from at least 40 families there (Maurin et al. 2014), and they are also well known in appropriate habitats in South America. They can indeed be thought of as underground forests, and are some combination of stem and root, but above ground they may be no more than flowering shrubs.
Dessication tolerance. This is basically a physiological character; see Vicré et al. (2002b), Lüttge et al. (2011) and Gaff and Oliver (2013) for reviews. A relatively few plants, only about 300 species of angiosperms (the majority are monocots), but rather more mosses, liverworts, lycophytes and leptosporangiate ferns, all herbaceous or rarely small shrubs, show various degrees of extreme dessication tolerance and are commonly known as resurrection plants. Dessication tolerance (when the plant dehydrates to less than 0.1 g H2O g-1) has evolved maybe 13 times in angiosperms, examples including Myrothamnaceae, Velloziaceae-Vellozioideae, some Cyperaceae, and perhaps surprisingly also some genera in Plantaginaceae, Gesneriaceae, etc., and also surprisingly few Cactaceae or Aizoaceae (Porembski 2011; Costa et al. 2017 and references). The preferred habitat of such plants is inselbergs (Burtt 1998; Porembski & Barthlott 2000; Alpert & Oliver 2002; Proctor & Pence 2002; Dickie & Pritchard 2002; Porembski 2011; Gaff & Oliver 2013). (A number of these plants have seeds that can tolerate dessication, also surviving very high temperatures, that is, they are anhydrobiotes - Mertens et al. 2008.) Genes involved in such dessication tolerance seem be derived from those expressed in seeds, commonly more or less dessication tolerant, and they include late embryogenesis abundant (LEA) genes (in other dessication-tolerant embryophytes genes originally expressed in spores are involved), not other stress-tolerance genes - and of course the seed often dries out during the maturation phase (Oliver et al. 2005; K. Liu et al. 2008; Fisher 2008; Rodriguez et al. 2010; Gaff & Oliver 2013; Costa et al. 2016). Some of the genes involved in seed development and maturation, the LEC1- type HAP3 genes, are inductively expressed under drought stress in non-seed plants like lycophytes and ferns (Xie et al. 2008). Plants showing extreme dessication tolerance may be poikilochlorophyllous, losing their chlorophyll, etc. (monocots), during drying, but reconstituting this on rehydration, or homoiochlorophyllous, retaining their photosynthetic apparatus and chlorophyll (Lamiales) (e.g. Porembski & Barthlott 2000; Proctor & Pence 2002).
A word on Ageing. The bristlecone pine, Pinus longaeva, is the longest-living non-clonal seed plant and it can live up to 4,844 years or so (Munné-Bosch 2014 and references; Piovesan & Bondi 2021); its needles, which can live for over 30 years (Hacke et al. 2015), are the longest-lived leaves of all land plants except Welwitschia - but unlike P. longaeva, the leaves of the latter are ever-growing. (Interestingly, the longest-living trees are all gymnosperms.) The longevity of P. uncinata, at 700 years a veritable spring chicken, was attributed i.a. to loss of apical dominance, the development of epicormic buds, and modular senescence (Pasques & Munné-Bosch 2022). L. Wang et al. (2020) noted how in Ginkgo biloba the stem vascular cambium maintained its activity over time (>500 years), the amount of vascular tissue produced, plant fertility, etc., all remaining constant. Xylem, etc., cells in the wood stop functioning in water conduction quite early (the width of the sapwood seems to be constant - K. C. Yang & Hazenberg 1991, c.f. at least some angiosperms), even if polyphenolic parenchyma cells in the phloem of Norway spruce (Picea abies) can remain alive for over 70 years (Krokene et al. 2008). Interestingly, some trees in Amazonian rainforest may live for quite some time - at least 1,400 years is an estimate for the age of Cariniana micrantha (Lecythidaceae) (Chambers et al. 1998).
Other trees, and many herbs, have vegetative reproduction, and there it is the clone as a whole, the genet, not the individual plant stems, the ramets, that get old. A single clone of Populus tremuloides is recorded as covering 43.6 ha and it was made up of around 47,000 stems (DeWoody et al. 2008), numerous vegetative buds developing from the roots (references in Bosela & Ewers 1997). Note, however, that Yang and Hazenberg (1991) found that the the oldest sapwood in P. tremuloides trees ca 90 years old was up to ca 40 years old, an age increasing linearly with time (see also Fahn & Arnon 1963). Ally et al. (2010) found that after 500 years or so the clones showed signs of ageing, at least in terms of the amount and viability of pollen they produced, and the fertility of the pollen of the oldest clone at which they looked, perhaps 10,000 years old, was less than one quarter that of young plants. Centenaro et al. (2023) looked at the age of clones of Salix herbacea, and from their literature review (ibid.: esp. Appendix S1) the oldest clonal plant was Gaylussacia spp. (= "clonal herb") at ca 13,000 years and Larrea tridentata, at ca 11,000 years. However, clones of Lomatia tasmanica (Proteaceae) are estimated to be some 43,000 years old (DeWoody et al. 2008) and those of Posidonia oceanica in the Mediterranean may be up to 15 km across and as much as 200,000 years old (Arnaud-Haon et al. 2012; see also Abrahamson et al. 2023 for references).
This leads on to thinking abount taxa that lack secondary thickening - for instance, most of the monocots (including Posidonia oceanica just mentioned), ferns, etc.. Such plants may be herbaceous or woody. If herbaceous, the plant may be rhizomatous, bulbous, etc., and here the older part of the plant rots - not only is there then no physical connection between the different parts of the one individual, but individual cells do not live more than a very few years. However, plants without secondary thickening that are woody face problems like whether and/or how cells that differentiated long ago can remain functional or perhaps how long cells can remain undifferentiated and still differentiate normally. Palms, for instance, lack a vascular cambium, and here in particular the question is how cells that are dead (vessels, etc.) or without a nucleus (sieve tube cells) can remain functional for hundreds of years (e.g. Tomlinson & Huggett 2012; see also the discussion under palms for more detail). The longevity of cells in seed plant vascular tissue in general would repay investigation - some xylem parenchyma cells even in broad-leaved angiosperms are reported to remain metabolically active for 200 years or so (Spicer & Holbrook 2007), functional xylem in lianas perhaps being particularly long-lived (references in Angyalossy et al. 2012). Earlier on in this section, I juxtaposed the bristlecone pine and poplars, now it is the turn of palms, perhaps something like Coryphya umbraculifera in particular, and bamboos. There is apparently just a single clone of Phyllostachys edulis in Japan (where the species was introduced in 1736) and much of China, and Isagi et al. (2016) estimated that its weight was 6.6 x 1011 kg - although I have seen nothing that suggests bamboo clones live as long as the conifers just mentioned.
There is another aspect of ageing, and that is the accumulation of mutations as vegetative cells divide, and the effect this might have on present and future generations. On the positive side, the longevity of trees may perhaps be facilitated by the accumulation of somatic mutations, leading to the expansion of R genes involved in immune defence, the diversification of defence genes, etc. (Plomion et al. 2018). In oaks, at least, there is no genetic mosaic of clonally distinct cell lineages (see also Tobias & Guest 2014), and mutations may accumulate in meristematic tissues that ultimately give rise to spore-producing reproductive structures, for example, in buds in trees that produce pollen and ovules hundreds of years after the production of the seed. Here the negative side of ageing may become evident, that is, the accumulation of deleterious mutations, or Muller's Ratchet (if reverse mutations are rare and no recombination, offspring have at least as much or more mutational load as their parents). However, there may be many fewer cell generations - and hence mutations - in such buds than the age of the plant or number of cell generations in the tissues in the stem that bear the bud might suggest (Burian et al. 2016); see also Y. Ren et al. (2021) for the rather complex story in Salix.
Ant-Plant relationships. Plants in which there is a close relationship between ant and plant, loosely linked under the term myrmecophytism, are widely scattered phylogenetically. Davidson and McKey (1993) and Davidson and Epstein (1989) are general accounts, while Webber et al. (2007) clarify the kinds of relationships involved. It has become clear that scale insects, fungi, bacteria and rhabditid nematodes are also frequently obligate associates in such relationships (Defossez et al. 2009; Maschwitz et al. 2016). Ant gardens, in which the seeds of epiphytic plants are placed in the carton of ant nests, are known from both the Old and New World tropics (Orivel & Leroy 2011); this movement of seeds is a variant of myrmecochory, for further details of which, see below.
Mycorrhizae. As will be seen, the mycorrhizal and mycoheterotrophic and even parasitic life styles are in some ways not so very different (see also Thorogood et al. 2021), all involving asymmetrical exchanges of nutrients between the partners, some of the signalling between the two partners is similar, and in both the first two cases the partners are fungi and embryophytes. For the evolution and ecological significance of mycorrhizae, see Malloch et al. (1980), Read et al. (2000), etc., and for an account with a summary of the distributions of the main mycorrhizal types within angiosperms, see Brundrett (2002, 2004), B. Wang and Qiu (2006), and especially Brundrett (2009, see also 2008 for updated online resource), F. A. Smith and Smith (1997), S. E. Smith and Read (1997), and Landis et al. (2002) - more details are to be found elsewhere. Akhmetzhanova et al. (2012) is a database containing information of mycorrhizal type, etc., in some 3,000 species in the old U.S.S.R., and Brundrett (2004; see also Peterson & Massicotte 2004) offers a classification of mycorrhizal types based on anatomical criteria regulated by the host plant. Mycorrhizal development is intimately connected with fine root thickness, branching, the development of root hairs, etc. (for more on roots and mycorrhizae, see elsewhere, although correlations are by no means absolute (Baylis 1975; St John, 1980; Schweiger et al. 1995) and plants can have at first sight bewildering complexes of root morphologies and fungal associations (e.g. Gao & Yang 2010). Although taxa at various levels may be assigned a particular mycorrhizal status in the pages below, this usually represents merely the condition most common there.
Ectomycorrhizae (ECM) form a Hartig net of hyphae investing the rootlets and penetrating between the cortical cells; the hyphae are septate and are not intracellular - with the exceptions of the distinctive ectomycorrhizae of Ericaceae and Orchidaceae. Bruns and Shefferson (2004) provide a convenient summary of taxa with ectomycorrhizae, but more detail will often be found here (see e.g. Ducousso et al. 2008 and references); sometimes the fungus-root association results in the formation of tuberculate structures (M. E. Smith & Pfister 2009). Although basidiomycetes are frequent ectomycorrhizal associates, Pezizales and other ascomycetes are also quite common (Tedersoo 2006, ascomycetes with an hypogeous life style are derived from them). ECM are common in Fagales, which dominate in temperate woodland, but they are also notable in caesalpinioids in African Miombo vegetation, Dipterocarpaceae in the forests of Malesia, etc.. ECM - along with endomycorrhizae - also occur in plants like Graffenrieda emarginata (Melastomataceae) that grow in tropical montane environments (Haug et al. 2004 and references). ECM are discussed further below, and the more ecological aspects of these mycorrhizae are discussed separately.
Endomycorrhizae, or vesicular-arbuscular mycorrhizae, or just arbuscular mycorrhizae (AM), are formed by an association of Glomeromycota (Schüßler et al. 2001) with land plants - indeed, Glomeromycota are found only in association with plants, whether sporophyte or gametophyte. There is evidence of AM mycorrhizae in the fossil record from the Silurian/early Devonian ca 400 million years ago, but this association has almost certainly arisen - and been lost - a number of times (e.g. Baylis 1975; Redecker et al. 2000b; Duckett et al. 2006). Thus although plants of the first pectinations of the liverwort clade are associated with Glomales (Kottke & Nebel 2005), this association may subsequently have been lost (Duckett et al. 2006b), indeed, in some cases the fungus involved may have moved to the liverwort from a tracheophyte (Ligrone et al. 2007). Within Jungermanniopsida, Porellales lack fungus associations, but within Jungermanniales associations with ascomycetes are very old, more than 250 million years (Pressel et al. 2008). Glomus itself is probably paraphyletic (or worse: Redecker et al. 2000a; Schwarzott et al. 2001) and Glomeromycota seem to be a very ancient asexual group (Pawlowska & Taylor 2004) whose basic genetic structure is not well understood (Rodriguez et al. 2004). Mucoromycota may also be involved in these associations.
In vesicular-arbuscular mycorrhizae s. str. the aseptate hyphae are intracellular, often forming vesicles or branching structures called arbuscules within the cells (when the latter alone are formed, an arbuscular mycorrhiza s. str. may result). In a few taxa, root nodules are formed, and these are modified lateral roots that occur in 2-3 longitudinal series opposite the protoxylem poles - similar to the root branchlets of Proteoid roots and actinorrhizal nodules (Duhoux et al. 2001; Schwendemann et al. 2011 for literature). Baylis (1975; see also St John 1980) emphasized the prevalence of mycorrhizal "magnolioid" roots in plants included in the magnoliid clade here, such roots were coarsely branched and rarely less than 0.5 mm across; they often lacked or had only a few root hairs, and these were small, less than 100 x 15-20 µm. Similar roots are also known from Griselinia (Apiales) and Liquidambar (Saxifragales: Baylis 1975), so their overall distribution is unclear, but Comas et al. (2012) reexamined factors like root density, biomass, and root diameter in the context of angiosperm evolution, suggesting that root diameter has greatly decreased within the angiosperm clade. Root diameter and mycorrhizal type interact in the exploitation of nutrients when their availability is patchy (W. Chen et al. 2016: 13 species in temperate forest), and when considering ferns, lycophytes and other tracheophytes, it appears that fine roots ≤1 mm across quite often lack mycorrhizal associations (Pressel et al. 2016) - although c.f. ericoid mycorrhizae...
For phylogenetic aspects of AM associations, see also Trappe (1987). The two main AM variants described there, the Paris and Arum types (see also Gallaud 1905; Dickson et al. 2007) show little association with higher-level groupings, except perhaps when Asparagales are compared with Liliales (F. A. Smith & Smith 1997); the Paris type may be under-recorded. Note also that both types are known from several families and there are intermediate morphologies (Dickson 2004; Dickson et al. 2007). Thus it has been suggested that these mycorrhizal types should be discarded, emphasis being better placed on the morphological and physiological details of particular associations (Brundrett 2004), but some think that the types are indeed useful enough (Dickson et al. 2007). Interestingly, in holomycoheterotrophic plants other than Orchidaceae and Ericaceae which are associated with ascomycetes and basidiomycetes, the pattern of fungal infestation seems always to be a variant of the Paris type of AM, with well-developed intracellular hyphal coils (Imhof 2007 and references; Imhof et al. 2013), and it has recently been found that this may have very important implications for movement of C between fungus and plant (Giesemann et al. 2019, 2021) - so there may well be links between AM "type" and aspects of ecophysiology. In addition to variation in details of intra-plant fungal infestation, there is also variation in the proportion/amount of fungal biomass inside the plant compared to that outside the plant, and this variation is linked with the taxonomy of the fungus (Maherali & Klironomos 2007). Some species produce both ECM and AM associations (e.g. Frioni et al. 1997; Akhmetzhanova et al. 2012). For more discussion about AM associations, see elsewhere, esp. para. 2 but also in other places in that section, also Imhof et al. (2013) and papers there.
Mycoheterotrophic plants. There are around 880 full mycoheterotrophs (M.-M. Li et al. 2022), and in the past such plants, usually rather small and echlorophyllous, were vaguely thought of as being saprophytes. However, as Leake (1994, 2005), Leake and Cameron (2010) and others have been at pains to point out, they are really parasites (of mycorrhizal fungi) or hyperparasites (of the plants with which the mycorrhizal fungi are associated); for plant-on-plant parasitism, see immediately below. Leake (1994; see also Imhof 2007; Merckx et al. 2009b; Merckx & Freudenstein 2010; Leake & Cameron 2010; papers in Merckx 2013a; Jacquemyn & Merckx 2019; Li et al. 2022) surveyed the biology of holomycoheterotrophs, observing that most were monocots, some 3/4 of the origins of this condition (there are at least 40, but quite possibly far more) being in Orchidaceae alone, although they are also found in e.g. Gentianaceae, Ericaceae, Polygalaceae, the gametophytes of a few bryophytes and lycophytes, etc. - and of course in the seedlings of just about all Orchidaceae (e.g. Merckx & Freudenstein 2010; Merckx 2013b). Within angiosperms, the association of holomycoheterotrophy with monocots may be connected with their lack of secondary thickening and of a primary root, presence of a thick cortex, development of tertiary thickenings on the endodermis, etc. (Imhof 2010; Imhof et al. 2013). The vegetative morphology of such plants is of course much reduced and modified and the flowers can also be much modified. Thus stomata are often lacking, the roots are more or less clustered, stout, little-branched, lacking root hairs and in monocots the cortex may disintegrate, leaving the thick-walled endodermis as the outer layer; the flowers often have parietal placentation, many ovules with sometimes long funicles, tiny seeds with little endosperm and an undifferentiated embryo, and so on. See Mower et al. (2021) for possible connections between parasitism, the photosynthetic process, and the loss of ndh genes. For images of some mycoheterotrophs, see the Parasitic Plants Website (Nickrent 1998 onwards), Imhof et al. (2013), etc.. Perez-Lamarque et al. (2019/2020) looked at the evolution of mycoheterotropic relationships from the point of view of the mycoheterotrophs being cheaters. They note that the plants involved are highly specialized and their fungal associates tend to be closely related. Mycoheterotrophs interact with far fewer fungi (ca 1/5th) than do autotrophs, and the fungi interact with ca 1/2 as many plants, the older mycoheterotrophic families in particular showing conservatism in their fungal partners (Perez-Lamarque et al. 2019/2020). Much work has been carried out to establish the direction of flow of nutrients between the fungus, the echlorophyllous mycoheterotroph, and other plants with which the fungus may have a mycorrhizal association (see Merckx et al. 2009b; Field & Pressel 2018). Full holomycoheterotrophy is particularly common in orchids, and germination and rinitial subsequent griowth is also a mycoheterotrophic process; adult orchids are predominantly mixotrophic. Glomeromycota are often involved in mycoheterotrophic relationships in tropical echlorophyllous plants other than Ericaceae and Orchidaceae, and details of the nutrient exchange between the two partners may be different from situations where ectomycorrhizal fungi, whether basidiomycetes or ascomycetes, are involved, as in Ericaceae and Orchidaceae (Franke et al. 2006; Courty et al. 2011). For a survey of mycoheterotrophs, see Merckx et al. (2013a); note that more or less mycoheterotrophic gametophytes are found pretty much throughout non-seeding embryophytes. Cai (2023: esp. Table 1) compared changes in holomycoheterotrophic plants with those in holoparasitic plants, for which see immediately below.
There is no sharp distinction between full autotrophy and full mycoheterotrophy (Jacquemyn & Merckx 2019), and autotrophs and mycoheterotrophs can be hybridized (Ogura-Tsujita et al. 2014; Shutoh et al. 2016). All Orchidaceae are more or less mycoheterotrophic, certainly when they have just germinated, but most carry out at least some photosynthesis when they are adults, i.e. they are (serial) mixotrophs, and groups like Ericaceae and Dioscoreales have comparable variation; in orchids, the fungus may supply the below-ground parts with carbon, with that for the flowers and fruits coming from the leaves. For mixotrophy, see also Selosse et al. (2017c) and Tešitel et al. (2018), it includes uptake of carbon and/or elements like N, P, etc., from fungal associates (e.g. mycorrhizae), prey (in carnivorous plants, "necrotrophic mixotrophy"), or soluble organic matter from the soil.
Timilsen et al. (2022b) compared gene loss in unrelated mycoheterotropic plants in Orchidaceae, Burmanniaceae and Triuridaceae. They found that 174/1372 of the BUSCO (Benchmarking Universal Single Copy Orthologous) genes they looked at were lost, the Missing In Mycoheterotrophs genes. Of these 174 genes most (ca 88%) were photosynthesis-thylakoid-membrane-associated. Genes involved in photosynthesis were progressively lost, but not genes responsible for the early steps of haeme synthesis since they were involved in pathways outside photosynthesis, furthermore, all species had the photosystem II gene pxb29, although its function in these mycoheterotrophic plants was unclear (Timilsen et al. 2022b). Indeed, plastomes in mycoheterotrophic plants are much reduced and may have have only a couple of dozen or even fewer functional genes remaining, the number depending in part on which genes have moved to the nucleus, although there does seem to be a core group of genes like accD and trnE involved in things like ribosomal synthesis that are less likely to move (Barbrook et al. 2006; Schelkunov et al. 2015; Lim et al. 2016; Wicke et al. 2016; Graham et al. 2017; Garrett et al. 2023). The progressive loss of chloroplast genes as the dependence of the plant on the fungus for nutrients increases can be usefully compared with comparable losses in plants conventionally described as (hemi)parasitic, the main difference between the two being the nature of the organism being parasitized (fungus versus plant). Even very reduced plastomes tend to have the normal tetrapartite arrangement of the genome with an IR (Lim et al. 2016, and references), however, it can be difficult to decide exactly when a gene is present, lost, or pseudogenized (e.g. Wicke & Naumann 2018). Plastome changes in plants becoming mycoheterotrophic start off with the loss/pseudogenization of ndh genes, then the loss of genes for photosynthesis and some housekeeping genes, then the loss of more housekeeping genes, and finally the loss of genes coding for the plastid (e.g. C. F. Barrett & Davis 2012; Wicke et al. 2016; C.-S. Lin et al. 2017; Graham et al. 2017; X. Li et al. 2019; Timilsen et al. 2022b, see also below), although there are many exceptions (Wicke & Naumann 2018). The rate of evolution of the plastome in both parasitic and mycoheterotrophic plants can be extremely high so leading to problems in phylogenetic analyses like long branch attraction and difficulties in phylogeny reconstruction, and here analyses of the more slowly evolving genes of the mitochondrial genome may have an advantage (see e.g. Q. Lin et al. 2022, also discussion below), interestingly, analyses of the nuclear genome, as in the Angiosperms353 data set, can also be tricky to interpret (see Seed Plant Tree of Life, version 2, Jan. 2022).
Echlorophyllous holoparasites, i.e. the parasite lacking chlorophyll, and with direct plant-plant interactions, are known only from broad-leaved angiosperms (see Barkman et al. 2007; Tesitel 2016), Parasitaxus (Podocarpaceae) being the only exception (Fay et al. 2010 for a good general account); they are not known in monocots. A variety of different kinds of parasites have been proposed by Tešsitel (2016) and Krasylenko et al. (2021). Hemiparasites, which have chlorophyll but depend on their hosts for water, minerals, (etc.), are more common than holoparasites. No reversals to the free-living state from either the hemi- or holoparasitic condition are known. Perhaps 1.5% of flowering plants are hemi/holoparasites, and the great majority of these are in Santalales (mostly woody, especially the hemiparasites) and Orobanchaceae (mostly herbaceous). All told, the parasitic habit has evolved some 12 times or so, and some 292 genera and 4,750 species are involved (Barkman et al. 2007; X. Li et al. 2013; esp. Nickrent 2020). There has been convergent evolution in the extensive genome changes is the holoparasites Balanophora and Sapria, and less convergence in hemiparasites (X. Chen et al. 2013); for changes in the plastomes and mitogenomes of holoparasites, especially those in Balanophoraceae, see Sanchez-Puerta et al. (2023). For the recognition of the host by the parasite - and various unorthodox kinds of parasitism - see the review by Jhu and Sinha (2022a); note that host recognition is a rather different process in stem and root parasites. Physiological relations between host and parasite can be complex (e.g. Press et al. 1990; Ehleringer & Marshall 1995). Three stages/phases are often mentioned in descriptions of the evolution of parasitism: 1, gain of a haustorium, which has happened, ca 12 times (Krasylenko et al. et al. 2021); for stem haustoria, see Jhu & Sinha 2022b); 2, loss of functions that are taken over by the host; and 3, specialization of the relationship (e.g. Searcey & MacInnis 1970); two and three in particular may overlap. However, Cai (2023) questioned the value of this approach and emphasized the overarching importance of the loss of photosynthesis in his funnel model; photosynthesis is central in plant metabolism and its loss is associated with many other changes in the plant body like the loss of carotenoids and the convergent acquisition of anthocyanins for floral pigmentation (for genome changes, see also Lyko & Wicke 2021, etc.). Seeds are often minute. This may be associated with a reduction in flower size, etc., as in Balanophora where the female flowers are a mere 50 cells or so (Su et al. 2019) and there is only 1 seed per flower, this is a holoparasitic member of Santalales (the order as a whole has but a single ovule per flower). Commonly, however, there are many tiny seeds per fruit (Cai 2023), and the flowers may be gigantic, as in Rafflesia. Cai (2023: Table 1) compared changes in holoparasitic with those in holomycoheterotrophic plants, the latter also lacking chlorophyll, but, as Cai emphasized, their associates are fungi, which leads to somewhat different relationships between the partners; the flowers of most holomycoheterotrophs are somewhat more conventional than those of most holoparasites (but similar ages?). Hyperparasites, parasites of parasites, including self-parasites, are reviewed by Krasylenko et al. (2021); a few taxa, mostly in Santalaceae, are always hyperparasites (= obligate epiparasites). For parasites in general, see also Press and Graves (1995).
Being a parasite often entails having a high rate of transpiration both day and night, and if parasites have stomata, these are often permanently open (Stewart & Press 1990), alternatively, parasites like Cuscuta campestris may force the opening of host stomata (Landi et al. 2022). Establishment of a vascular connection between host and parasite via some kind of haustorium is a critical phase in the establishment of the parasitic relationship, and this is discussed further under each case. Connection between host and parasite is usually via both xylem and phyloem in holoparasites, and via the xylem only in hemiparasites (Tesitel 2016). Details of the hormonal control of the establishment of the connection between the xylem of host and parasite (there can be perforations in xylem wall between the two, and these probably form as the host xylem is developing) and the phloem (connections are symplastic via plasmodesmata, and may develop after the host phloem has matured) are discussed by Aloni (2021). Press et al. (1988) discuss water and C movement in root hemiparasites, while a summary of the physiology of plant-parasite relationships is provided by Tesitel (2016; see also Teixeira-Costa et al. 2021). The vegetative morphology of holoparasites is of course much modified, some species being endophytic, living and growing entirely within the host except when flowering. Teixeira-Costa et al. (2021) noted that in Santalaceae that had pronounced endophytic development, differentiation of a vascular connection between host and parasite was early, probably because the parasite needed water, etc., early, connection between host and parasite was indirect, and the vascular development of the host was notably affected. However, in Rafflesiaceae and Apodanthaceae at least (there is no information for other holoparasites) connections between host and parasite developed late, i.e. only at the time of flowering, they were direct, and the vascular development of the host was little affected. The floral morphology of holoparasitic plants, whatever their nature, can be very difficult to relate to that of their putative photosynthetic relatives, and their seeds and embryos (these latter are often undifferentiated) are also much modified, unfortunately, little is known about the germination of such seeds (Baskin & Baskin 2021b). For general information on parasitic plants see Kuijt (1969: still useful), the Parasitic Plants Website (Nickrent 1998 onwards, a great deal of information, images, etc.), and also Heide-Jørgensen (2008) and for horizontal gene transfer (HGT), quite common here, see e.g. Z. Yang et al. (2019 and references). Thorogood et al. (2021) note convergent evolution in holoparasitic plants (note that Apodanthaceae and Rafflesiaceae are likely to be sister taxa), and also in biotrophic fungi.
There are similarities in the evolution of the plastome in carnivorous, echlorophyllous holomycoheterotropic, and parasitic plants, and this is probably because all three groups of plants have more or less switched from a fully autotrophic mode of nutrition (Nevill et al. 2019; see also Sloan et al. 2012b; Wicke & Naumann 20183). For the evolution of the plastome in parasitic plants, see e.g. Krause (2011, 2015), X. Li et al. (2013), Molina et al. (2014), Bellot and Renner (2015) and Wicke and Naumann (2018); the mitogenome is usually little affected (for both plastomes and mitogenomes, see also below).
There is more on hemi-/holoparasitic ("p" in the list below) and hemi-/holomycoheterotrophic ("f" below) associations involving plants and other plants and/or fungi in Cassthya-Lauraceae (p), Cuscuta-Convolvulaceae (p), Corsiaceae (f), Burmannia, etc. (f), and Thismia (f), etc., all Dioscoreales, Ericaceae (f), Voyria-Gentianaceae (f), Orchidaceae (f), Orobanchaceae (p), Krameriaceae (p), Balanophoraceae (p) and most other Santalales (p, e.g. mistletoes, Loranthaceae, Santalaceae, etc.)Triuridaceae (f), Rafflesiaceae (p) and elsewhere.
Aquatic plants, hardly surprisingly, lack mycorrhizae, as do parasitic plants (Trappe 1987; Radhika & Rodrigues 2007 and references for records, also de Marins et al. 2009; for a convenient summary, see Brundrett 2008), although there may be infraspecific variation in some taxa depending on whether growth is in marshy or drier conditions (Bristow 1975). The frequent absence of mycorrhizae in Caryophyllales, Proteales, etc., is biologically and systematically interesting. In, say, the tundra habitat there are a number of plants that take up substantial amounts of amino acids directly from the soil, but the ability to do this is not obviously correlated either with mycorrhizal status or taxonomy. In such habitats a number of Cyperaceae, which usually lack mycorrhizae (but c.f. Muthukumar et al. 2004), take up N predominantly in an organic form, but other species in the family take it up in an inorganic form (Raab et al. 1999).
Endophytic fungi are found in a number of flowering plants, perhaps particularly in Poaceae (q.v.) and Ericaceae (e.g. Petrini 1986 and other references in this volume; Saikkonen et al. 2004 and references), although they are pervasive in angiosperms (Herre et al. 2005: tropical plants). Indeed, Arnold et al. (2001) found 418 morphospecies of endophytes in only 83 leaves of two species of tropical trees (Ouratea [Olacaceae], Heisteria {Erythropalaceae]). The effect of endophytes on their hosts is still little understood, Poaceae being something of an exception (Schardl 2010 and references). Endophytes of Poaceae seem to have evolved from an insect pathogen (e.g. Spatafora et al. 2007; Vega et al. 2009) and they may protect the plant against pathogens, as well as affect the water balance of seedlings, the branching of the root, the palatability of leaves and fruits, the uptake of phosphorus by the plant, etc. (references in Arnold & Engelbrecht 2007; Sasan & Bidochka 2012; Almario et al. 2017). They may also be involved in the synthesis of metabolites previously attributed to the plant host (e.g. Schulz et al. 2002; Schulz & Boyle 2005 and references), and the angiosperm-endophyte partnership has even been likened to a chimaera (Herre et al. 2005; see also Markert et al. 2008; Wink 2008). Endophytes may be either vertically or horizontally transmitted - via the seed or other plant propagules or via spores. Arnold (2008) provides a convenient entry into the literature; for further details, see also below.
Sebacinales are basidiomycetes that have a remarkable diversity of associations with angiosperms; they may form ectomycorrhizae, or ericoid, arbutoid or orchid mycorrhizae, and they may be endophytic (Oberwinkler et al. 2013; Varma et al. 2013; Weiß et al. 2016).
Another set of associations between plant and insect - although other organisms may be involved, too, sometimes fungi - result in the distinctive outgrowths evident as galls (see Redfern 2011 for a good introduction; Aloni 2021). Cecidomyiidae (dipterans), the most speciose gall formers (Yukawa & Rohfritsch 2005), are worldwide in distribution but show no particular pattern of host associations. Cynipidae (hymenopterans) are north temperate in distribution and do show an association with particular plant groups (Stone et al. 2009; Redfern 2011), while psyllids (jumping plant lice, hemipterans) are particularly common in Australia (Fernandes & Price 1991; Crespi et al. 2004; Espiritó-Santo & Fernandes 2007; Raman et al. 2005). Aphids (e.g. Fordini: H. C. Zhang & Qiao 2007, 2008), caterpillars, etc. may also on occasion form galls (Guedes et al. 2023). In general, gall-inducing insects are commonest on sclerophyllous plants growing on poor soils in warm climates between 25 and 45o N and S, or perhaps more generally in species-rich communities, whether dry or wet, but not necessarily in tropical climates (Price et al. 1998; Yukawa & Rohfritsch 2005; Redfern 2011). Co-option of part of the host's machinery for making flowers, or in particular carpels, by the galling insect seems to be quite common (Schultz et al. 2018); in general, galling insects can synthesize both auxins and cytokinins and effectively induce novel plant organs (Shorthouse et al. 2005; Aloni 2021).
For rusts and their hosts, see OTHER at the end of this page.
Nitrogen fixation. Angiosperms that can fix nitrogen in association with bacteria are uncommon, yet are found almost exclusively in a group of four orders, the N-fixing clade (Fabales, Rosales, Cucurbitales, Fagales - q.v.), where the association is scattered. Jeong et al. (1999) and Clawson et al. (2004) discuss this association in the context of the evolution of Frankia, the bacterium most commonly involved outside Fabaceae, and within Fabaceae (q.v.) themselves several very different bacteria are involved; recent findings suggest a reinterpretation of the evolution of N fixation in this clade (van Velzen et al. 2018; Griesmann et al. 2018). A few land plants - hornworts, the water fern Azolla, cycads, and Gunnera (Gunnerales) have established a relationship with the N-fixing cyanobacterium Nostoc (Adams et al. 2006 for a summary), and nitrogen from diazotrophic bacteria supplies at least some the N needs of a few grasses (Van Deynze et al. 2018), while Burkholderia is also associated with some Primulaceae-Myrsinoideae and Rubiaceae.
For some formulae, etc., see the Glossary.
Hegnauer (1962 onwards) remains the source of information on the distribution of secondary metabolites, Siegler (1998) and Arimura and Maffei (2017) are also very useful, and Gershenzon and Mabry (1983) can still be read with profit. Kite et al. (2000) provided a useful survey of the distribution of some chemicals in the monocots, while Strauss and Zangerl (2002) summarise the diversity of the major classes of compounds involved in the chemical defence of angiosperms (see also Waterman 2005, also the insect-plant and fungus-plant relationships mentioned at the end of this page - secondary metabolites are commonly involved here, too). Natural Products Alert (NAPRALERT: Loub et al. 1985, see https://napralert.org/ can also be usefully consulted when looking at the distributions of secondary products. In general, chemical characters are like others in terms of their value in understanding phylogenetic relationships; some, like the presence of glucosinolates, are very valuable, many others, much less so. Still others - presence of ellagic acid is an example - show fairly restricted distributions, but are still very variable in terms of local presence/absence (e.g. D. Soltis et al. 2005b). Monocots in general have a less diverse secondary chemistry than do other angiosperms.
Note that sampling for chemical characters may be spotty (although still often better than that for many embryological characters?). Unfortunately, systematic surveys of plant groups for particular classes of compounds are now very much out of fashion unless the compounds are of obvious biological/pharmacological interest, like glucosinolates, however, S. D. Smith et al. (2019) summarize quite a lot of recent information that is of interest here. Note that sophisticated screening methods are leading to the detection of some classes of secondary metabolites in families from which they had not been recorded (Lapcík 2007), however, it can be very difficult to say that a compound is really absent: Is an alkaloid present at 0.000001% concentration present or not (Waterman 2007, q.v. for the problems facing chemical systematics)? Almost all authors rightly emphasize the importance of the pathways by which compounds are produced, and apparently distinctive substances like napthoquinones or tropane alkaloids can have quite different biosynthetic origins.
Pichersky and Lewinsohn (2011) estimated that there were probably far more than 200,000 secondary/specialized metabolites to be found in "plants", any one species having 3,000-8,000 such compounds; at least 500,000 secondary metabolites is the estimate in J. Wu and Baldwin (2010) and even this is likely to be on the low side. The diversity of phytochemicals is in part understandable because it appears, for example, to be very easy for the sugar donor specificity of the enzymes which conjugate flavonoids with sugars to change (Noguchi et al. 2009). Along similar lines, individual terpene synthases may have many products, there are several terpene synthase genes that are easy to modify, and the terpene skeletons are easily modified (Davis & Croteau 2000; Kessler 2018; Pichersky & Raguso 2018) - as an example, γ-humulene synthase of Abies grandis can generate 52 different sesquiterpenes (Steele et al. 1998; Degenhardt et al. 2009). Genes involved in the biosynthesis of specialized secondary metabolites, particularly defence compounds like diterpenes which are subject to opposing selection pressures both over time and in space, are not infrequently assembled in operon-like clusters on the one chromosome (Takos & Rook 2012; Nüutzmann & Osbourne 2014; Boycheva et al. 2014). As with other features, parallelism is common, although the distinction between it and convergence can be difficult to make. For instance, gene-clustering of the cyanogenic glucoside defences of Fabaceae, Poaceae and Euphorbiaceae has developed independently (Takos et al. 2011; Olsen & Small 2018), intermediates in the pathways by which cyanogenic glycosides are synthesized are similar in insects and angiosperms (Bak et al. 2006), caffeine biosynthesis in angiosperms has evolved several times independently, but sometimes using the same intermediate pathway (de Noeud et al. 2016), similar regulatory changes involved in changes of flower colour evolve independently (Larter et al. 2018), and so on. Similarly, furanocoumarins are found in Ficus (Moraceae), Apiaceae and Rutaceae, quite unrelated, pyrrolozidine alkaloids are also widely scattered, and here the same pathways are involved, tropane alkaloids are also scattered, but there rather different pathways are involved (Berenbaum 1983 and references; Pichersky & Lewinsohn 2011; Reimann et al. 2004; Anke et al. 2004; Maia et al. 2012; Langel et al. 2010; Irmer et al. 2015; Y.-J. Wang et al. 2023). Furthermore, some biosynthetic pathways may be more or less inactive, although whether active in the past and now lacking a function and/or becoming active when conditions change, is unknown (Lewinsohn & Gijzen 2009). For secondary metabolites and species interactions, see also Kessler and Kalske (2018).
Indeed, it is useful to think of many aspects of plant chemistry as being combinatorial, which goes along with discussion of the "lego-ization" of plant chemistry or "lego-chemistry" (Menzella et al. 2005 and Sherman 2005: polyketides; Forrister et al. 2022: variation in Inga). Rather than chemical evolution being represented by a series of stepwise gradual changes, it is more the regulation of gene expression (Forrister et al. 2022) - and the genes that an individual has and those that are actually expressed may be rather different.
There is another wrinkle in that some important secondary compounds of plants are in fact synthesised by endophytic fungal or bacterial associates of the plant (e.g. Tan & Zou 2001; Schulz et al. 2002; Gunatilaka 2006 [surveys]; Markert et al. 2008; Wink 2008; Quach et al. 2023); families like Convolvulaceae, Celastraceae and especially Fabaceae and Poaceae are distinctive in this regard. Sporadic associations between plant and fungus/microbe, and/or horizontal transfer of genes from bacteria, etc. (HGT), may also go some way towards understanding the pattern of distribution of secondary metabolites, the presence of the metabolite in a particular organism then depending on regulation of these genes (Wink 2008, 2013). Indeed, secondary metabolites like terpenoids and quinolizidine alkaloids are produced more or less exclusively in mitochondria and/or chloroplasts - i.e. in bacteria whose association with plants is of very long standing (Wink 2008; see also Davis & Croteau 2000 for terpenoid synthesis). Finally, alkaloids and other noxious compounds may move from host to associated (hemi)parasite (e.g. Adler & Wink 2001; Cabezas et al. 2009).
Many secondary metabolites are involved in aspects of plant defence and are mentioned under Plant-Animal Interactions and Bacterial/Fungal Associations below. Note that the part of the plant sampled may well affect the metabolites that are detected (e.g. Webber & Miller 2008 and references; Ferreres et al. 1996), whether the plant is a juvenile or an adult (and whether the whole plant or a cell suspension culture is being examined) (M. J. Kato & Furlan 2007). There can be infraspecific variation in, for instance, the type of pyrrolizidine alkaloid synthesized (Langel et al. 2010 and references). This leads to thinking about the interactive diversity hypothesis, that is, interactions between plant and herbivore (for instance) mediated by a particular metabolite is independent from other such interactions, and overall they maintain chemical diversity, and there may be different independent interactions in different parts of the plant, times of the year, etc. (Whitehead et al. 2021; G. F. Schneider et al. 2023; etc.). Hence the thousands of secondary metabolites just mentioned.
It is well known that some noxious compounds are tolerated by herbivores, for instance (e.g. Ehrlich & Raven 1964), or are even sequestered by them (e.g. Opitz & Müller 2009). Indeed, plants that sequester metabolites that are generally effective against herbivores are nevertheless targeted by specialist herbivores; many such cases will be found in the pages below. A good example is the purine alkaloid, caffeine. Toxic to invertebrates, including bees, and in high concentration in the fruits and seeds of Coffea (Rubiaceae), the weevil Hypothenemus hampei is nevertheless an important pest of coffee beans - because it has a species of Pseudomonas in its gut that detoxifies caffeine (Ceja-Navarro et al. 2015). Adding further complexity to caffeine-plant-animal interactions, Stevenson (2020: p. 606) observed, "bees fed caffeine at ecologically relevant concentrations during a learning experiment were three times more likely to recall a trait associated with a food reward than bees fed a control diet" - under the right conditions, caffeine may benefit insects (and humans).
Acetylenes. Acetylenes are relatively uncommon in flowering plants (see Bohlmann et al. 1973 for a survey, etc.), although they are notably common in some families in Asterales and Apiales, where they seem to substitute for iridoids.
Alkaloids. For a general introduction, see Hegnauer (1988), Pelltier (2001), and Aniszewski (2007) and references. Alkaloids are extremely diverse (some 12,000 different kinds are known), and, complicating the issue, similar alkaloids can be formed via different biosynthetic pathways and similar alkaloids in quite unrelated organisms can be formed via similar pathways, or the pathway may be the same, but different enzymes are involved (e.g. Y.-J. Wang et al. 2023). Alkaloids can be classified according to the nature of the skeleton nucleus that they have, some of which are mentioned below. For a survey of the structure and distribution of isoquinoline alkaloids, see Buck (1987) and Bentley (1998), while Liscombe et al. (2005) put the origin of these alkaloids in a phylogenetic context. Detection of the activity of (S)norcolaurine synthase, the gateway to benzylisoquinoline synthesis, may suggest that these alkaloids will be found in groups in which they are not currently known, e.g. Chloranthaceae. For the synthesis of benzylisoquinoline alkaloids in the opium poppy (they are synthesised in the sieve tubes), see Bird et al. (2003); these are normally, but not always, derived from tyrosine. For pyrrolizidine alkaloids, the occurrence of which is concentrated in a few plant groups and are only sporadic elsewhere, see Hartmann and Witte (1995), Stegelmeier et al. (1999), Hartmann and Ober (2000, 2008), Ober and Hartmann (2000), Anke et al. (2004), Reimann et al. (2004), Langel et al. (2010), Stegelmeir (2011) and Irmer et al. (2015). They are used by plants for defence and by the insects that can tolerate them both in defence and for pheromones, and they can be toxic both to humans and livestock. The distribution of some distinctive alkaloid types such as the erythrina (Erythrina, Cocculus) and homoerythrina (Phelline, Dysoxylum, Schelhammera, some conifers) alkaloids is very scattered. For the distribution of calystegines (tropane alkaloids) see Dräger (2004), for that of ergot alkaloids, see Gröger and Floss (1998), and for that of indolizidine and quinolizidine alkaloids, see Michael (2008). Y.-J. Wang et al. (2023) look at details of the synthesis of tropane alkaloids in the widely separated Erythroxylaceae (q.v. for more information) and Solanaceae and find numerous differences - and some similarities that are only apparent.
Anthraquinones may be synthesised from polyacetates or shikimic acid. Overall, little detail seems to be known about this, but the broad patterns of variation are interesting (Jensen 1992 for a survey).
For calcium oxalate crystals, see below under anatomy.
There are over 500 characterised cardiac glycosides involved in plant protection; they are scattered over a variety of plant groups, and belong to two main classes, cardenolides and bufadienolides (see Singh & Rastogi 1970; Krenn & Krop 1998; Steyn & van Heerden 1998; Agrawal et al. 2012; for literature). For resistance to cardenolides - they inhibit the animal enzyme Na+/K+-ATPase - in herbivorous insects in which there is convergence at the amino acid level, see Dobler et al. (2012) and Petschenka et al. (2017).
Some information on the distribution of chelidonic acid is taken from Ramstad (1953).
Coumarins are involved in plant defense, some 800 different kinds being known from about 80 families (see also Berenbaum 1983).
Cyanogenetic pathways - see the surveys by Saupe (1981), Lechtenberg and Nahrstedt (1999), Conn (2008) and Bak et al. (2006) and comments by Hegnauer (1977, 1986), also Seigler and Brinker (1993), Miller et al. (2006) and Nielsen et al. (2017). Some 60 different kinds of cyanogenic compounds are known from about 2,500-3,000 species of plants placed in over 100 families (Conn 1990; Zagrobelny et al. 2008; Gleadow & Møller 2014). The taxonomic distribution of some, e.g. the cyclopentenoid cyanhydrin glycosides, is of particular interest (see Malpighiales, families near Achariaceae), and these are derived from the non-protein amino acid 2-(2-cyclopentenyl)glycine (e.g. Spencer & Seigler 1985b; Webber & Miller 2008). Cyanogenic compounds are stored as ß-glycosides and are activated by a ß-glycosidase; ß-glucosidases activate both the "cyanide bomb" and the "glucosinolate bomb", and the topology of an (abbreviated) tree produced by a phylogenetic analysis of the enzyme sequence is similar to that of other trees of angiosperms (Morant et al. 2008). For an example of the interactions of cyanogenic host and herbivorous insect (which can also synthesize the cyanogenic compounds itself), see e.g. Zagrobelny et al. (2008) and Zagrobelny and Møller (2011). Aside from defence, cyanogenic compounds are also involved in nitrogen storage and transport in some plants and in the production of pheromones, nuptial gifts, etc., in insects (Zagrobelny et al. 2008; Møller 2010 and references).
Ethereal oils are more or less volatile and aromatic; they are often terpenes of some sort. They may be found in idioblasts, i.e. specialized cells, as in basal angiosperms, and leaf blades, tepals, etc., containing ethereal oil cells may be punctate when a light is shone through them.
Fats, whether saturated or unsaturated, and their corresponding fatty acids (see also polyacetylenes below) are widespread, and are often important components of seeds. Petroselenic (cis-6-octadecenoic) acid has a distribution of considerable systematic interest (see Garryales and Apiales in particular: Kleiman & Spencer 1982 for a survey) and there are other distinctive fatty acids that have distributions that appear to be of systematic interest (Badami & Patil 1981).
For unlignified cell walls with UV-fluorescent ferulic and coumaric acids, see Harris and Hartley (1980), Hartley and Harris (1981), and Rudall and Caddick (1994).
Flavonoids. For general information about flavonoids, see Giannasi (1988), Bohm (1988), and Harborne and Baxter (1999), for minor flavonoids, see Bohm (1988), for isoflavonoids in particular (often phytoalexins), see Reynaud et al. (2005), Mackova et al. (2006) and Lapcík (2007), for biflavonoids, Geiger and Quinn (1975), and for flavonoid distribution in monocots, Williams and Harborne (1988). As Stafford (1990: p. 9) notes, "the use of duplicate or triplicate names for the same group of flavonoids is an unfortunate aspect of flavonoid nomenclature". Hegnauer (1986) suggests that flavonoids are of little use when looking at higher-level relationships. Anthocyanins are common flavonoid pigments, and when found in leaves they are usually red, perhaps protecting the young leaf (Manetas 2006: insect herbivores cannot see red, and if they are green, they contrast with leaf color).
Mustard oils, glucosinolates, are uncommon in flowering plants and are largely restricted to Brassicales, q.v., but they are also found in Malpighiales-Putranjivaceae. For details of glucosinolates and their distribution, see Fahey et al. (2001); there are 88, perhaps up to 137, different glucosinolates (Blazevic et al. 2019). They are broken down by the enzyme thioglucoside glucohydrolase (myrosinase) into glucose and aglucones, which automatically rearrange into a isothiocyanates, mustard oils, which have a R-N=C=S arrangement (see Cyanogenetic pathways above for ß-glucosidases), but the aglucones can also be converted into nitriles, thiocyanates, etc. (Halkier & Gershenzon 2006; Burow et al. 2009; Winde & Wittstock 2011). Note that some of the more unexpected records of glucosinolates, e.g. in Phytolaccaceae and Pittosporaceae, are reported by Daxenbichler et al. (1981), however, there are no vouchers and the reports must be considered suspect (J. E. Rodman pers. comm.; Mithen et al. 2010 for Brassicales). For the ecological and agricultural implications of glucosinolates, etc., see e.g. Courtney (1986), Chew (1988), Brown and Morra (1997), Rask et al. (2000), and Kakizaki (2017). For herbivores that are attracted to mustard oils, see Host-plant preferences below.
Gums, non-crystalline mixtures of sugars and organic acids, are scattered in angiosperms, being notably common in Fabaceae, where they are often found in the seeds (Nair 1995).
Hemicelluloses, see polysaccharides below.
Iridoids. Data are taken mainly from Bate-Smith et al. (1975), Hegnauer and Kooiman (1978), Bate-Smith (1984), Fredericksen et al. (1999), and especially Jensen (1991, 1992, 1999) and Jensen et al. (1975b) and other papers from his laboratory. Iridoids are formed from two C5 isopentane (isoprene) units. They are cyclic C10 compounds, often (always?) with O in one ring; they are formed in two main ways; they may be route I (secoridoids) or route II (carboxylated and decarboxylated iridoids: see the Glossary for their structures). Although a very useful character, presence/absence of iridoids may vary in closely related taxa (e.g. Jensen et al. 1975b). (Note that Inouye and Uesato [1986] questioned a classification of iridoids that was based on their biosynthetic pathways.) Iridoids are produced by the mevalonate pathway, and although polyacetylenes have a very different origin, being derived from their corresponding fatty acids, in families or groups of families of asterids one of these two classes of compounds may dominate to the exclusion of the other. Families that contain iridoids are largely asterids, although there are a few records from Saxifragales, etc.; all told, some 600 different structures are known. For further details of possible evolutionary pathways of iridoids, see Albach et al. (2001a). As glycosides, many have distinctive, often adverse, physiological effects on mammals, micro-organisms, etc. (see also Dobler et al. 2011); Bowers (1988) summarises aspects of the relationships between iridoids, plants and insects and Nishida (2002) and Opiz and Müller (2009) give examples of insects that sequester the compounds. See also Host-plant preferences below.
Isoprene. Plants can produce substantial amounts of isoprene, a gas that plays an important rols in atmospheric chemistry. Sharkey et al. (2013) discuss the evolution of isoprene synthase genes; Kesselmeier and Staudt (1999) provide a convenient summary of the distribution, etc., of the gas (see also Loreto & Fineschi 2014). Isoprenes are not found in annuals or C4 plants, but are especially commonly produced by temperate deciduous plants (Loreto & Fineschi 2014).
Latex is mentioned only when it occurs (see also laticifers, below). Gutta has the trans- configuration of isoprene units, and is distinguished from latex in the strict sense, which has the cis- configuration, in the descriptions; other white exudates are also sometimes (incorrectly) called latex (Alencar et al. 2020 and references). See Konno (2011), Bauer et al. (2014: esp. coagulation) and papers in Adv. Bot. Research 93. 2020 for aspects of the chemistry of latex and Konno et al. (2004: antiherbivore role of cysteine proteases), Agrawal and Konno (2009) and Dussourd (2016) for latex and plant defence; latex is also involved in wound sealing.
For plant lectins, a group of haemagglutinating proteins that have at least one non-catalytic domain that binds reversibly to a specific carbohydrate, see Peumans and van Damme (1995); note that lectins are defined by their activity, what they do, rather than by general protein structure. Lectns are often most prominent in seeds and resting storage organs, and target the proteins of herbivores like insects in particular, but even mammals (see also Vandenborre et al. 2011). They may also be involved in nitrogen storage (Peumans & van Damme 1995).
Lignans and neolignans. Lignans are ß,ß'(8-8')-linked dimers of cinnamic acid residues or their biogenetic equivalents (diaryl propanoids/phenylpropanoid dimers) that are stored in the cytosol. They are widespread, although they apparently do not occur in monocots, snd they are also found in gymnosperms, liverworts, etc.. Neolignans, more directly linked, or at least with other than ß,ß' links, are found especially in magnoliids (monomeric allyl- and propenylphenols are also found in the groups where they occur), also scattered throughout the eudicots. For definitions (which are not consistent, and depend either on structure or on biosynthetic pathway), distribution, etc., see McRae and Towers (1984), Bedigian et al. (1985), Whiting (1985: structure) and Ayres and Loike (1990). Umezawa (2003) surveyed lignan biosynthesis.
Lignins are major components of secondary cell walls that are synthesized in the apoplast. Complex and still poorly understood, their composition is of considerable interest. For the monolignols/phenylpropanoid units/phenol units/glycosides of the three major types of lignin see the coniferyl (MIG)/guaiacyl (G-lignin)/vanillyl/coniferin; sinapyl (MIS)/syringyl (S-lignin)/syringyl/syringin; and p-coumaryl MIH)/p-hydroxyphenyl (H-lignin)/p-hydroxyl/? lignins. Under certain conditions lignins yield substantial amounts of aromatic aldehydes - various combinations of vanillin, syringaldehyde, and p-hydroxybenzaldehyde. The Mäule reaction, in which a reddish colour is obtained after the treatment of a plant sample with potassium permanganate, then dilute hydrochloric acid, and then ammonia, signifies the presence of syringaldehyde, derived from sinapyl alcohol (Gibbs 1957 for an early but fairly comprehensive survey). The occurrence (or otherwise) of this reaction is correlated with fairly major taxonomic groups; note that vascular tissue may not always be stained, and even when it is, the primary xylem is not always stained. Conventionally, distinctions are drawn between G lignin, found in conifers, also tree ferns, G + S lignin, found in many angiosperms, but also elsewhere, and G + S + H lignin, found in monocots, but the situation is not that simple. Syringyl (S) lignin is also found in some lycophytes, e.g. Selaginella, and in other vascular plants, but it is (?always) synthesised in a way different from that of similar lignin in flowering plants (Xu et al. 2009; Weng et al. 2011), while at least some red algae can produce lignin-like substances (Martone et al. 2009). There is more variation in the three major "types" than commonly thought. They are not restricted to the major plant groups they nominally characterize, and there can even be substantial variation ontogenetically and/or in different parts of the plant. For instance, in Eucalyptus globulosus, the order of monolignol deposition is H, G, and then S (Rencoret et al. 2010), while the lignins of the bark and wood of Betula pendula differ (Logan & Thomas 1985; see also Lewis & Yamamoto 1990; Boerjan et al. 2002). H-lignin is somewhat restricted, being absent from broad-leaved angiosperms - at least from magnoliids and eudicots (Towers & Gibbs 1953), where syringyl units are particularly common. For lignin composition and synthesis, see also Novo-Uzal et al. (2012).
2-hydroxycinnamyl alcohols - usually not considered to be be monolignols - can also be involved: 5-hydroxyconiferyl alcohols can be found in angiosperm lignins, while caffeoyl alcohol (catechyl - C - units) has been found in the seed coats of Orchidaceae (Vanilla) and a number of Cactaceae (F. Chen et al. 2012, 2013) and 5-hydroxyconiferyl alcohol (5-hydroxyguiaacyl - 5H - units). There are also a number of minor lignin components, as in conifers and grasses, with tricin, a flavone, and ferulate nucleating lignin chains in the latter (Lan et al. 2016).
The complexity of lignins comes from the diversity of units, both monomers and oligomers, that make them up and the variety of ways in which they are joined together, and Lan et al. (2016) describe lignin synthesis as a whole as a combinatorial process that is independent of proteinaceous control. For a general discussion on details of the synthesis of lignin and its precursors and the evolution of the whole process, see Li et al. (2001), Weng and Chapple (2010), and Weng et al. (2010), and especially elsewhere for discussion on the distribution of lignin types and synthesis of lignins, see Logan and Thomas (1985), Whetten et al. (1998), Harris (2005), Weng et al. (2010), Guo et al. (2010), Li and Chapple (2010), Espiñeira et al. (2010, 2011) and Lan et al. (2016).
Metal accumulation. A number of plants, especially plants growing on serpentine or other extreme soils, accumulate substantial quantities of odd elements including several metals (Reeves et al. 2017 for a summary). Useful surveys of aluminium accumulation are found in Chenery (1948, 1949a, b), Webb (1954), Kukachka and Miller (1980), Jansen et al. (2002b, 2004a, c) and Schmitt et al. (2017); blue fruits (and flowers) are quite common in taxa that accumulate aluminium. For selenium (Se), see Cappa et al. (2014b), White (2016), Schiavon and Pilon-Smits (2016) and Irish et al. (2002); some Brassicaceae and Fabaceae are particularly notable Se accumulators. Gupta and Gupta (2017) suggest that Se may have a number of beneficial effects in plants, although it is not an obligate nutrient, and the value of hyperaccumulation is unclear to me. Broadley et al. (2001) and Cappa and Pilon-Smits (2014) summarize patterns of hyperaccumulation of heavy metals, e.g. nickel (see also Baker & Brooks 1989; Krämer 2010; Mesjasz-Przbylowicz et al. 2016: Ni accumulation generally in epidermis; Isnard et al. 2020), also manganese, etc., and other unusual elements in angiosperms. Reeves et al. (2017) discussed the need for a global database for plants that hyperaccumulate metals (see SMICMLR Global Hyperaccumulator Database). Uptake of such elements can be affected by the mycorrhizal status of the plant (Orlowska et al. 2013). Freeman et al. (2009), Cappa and Pilon-Smits (2014) and others advance hypotheses for the advantages of hyperaccumulation for the plant. See also papers in Front. Plant Sci., 2020.
Fructose is a kind of monosaccharide that is sometimes stored by the plant; families in which storage fructose polysaccharides like inulin have been detected are listed by Pollard and Amuti (1981) - these are mentioned only when inulin accumulation occurs reasonably consistently within a family. Thus they are not mentioned in Cornaceae, where they occur only in a few species of Cornus, but not others, nor in Melianthaceae, where they are reported only in trace amounts. For the distribution of stem fructans in monocots, see Pollard (1982); for fructans in general, see Meier and Read (1982), Hendry and Wallace (1993), Van den Ende (2022) and Shen et al. (2023).
The metabolic pathway of nicotinic acid in tissue culture may be of systematic significance, although at some 50 species the sampling is poor (see Willeke et al. 1979). Gymnosperms and all flowering plants except asterids metabolise nicotinic acid into trigonelline.
Non-protein amino acids are mentioned only when they are abundant, as in families like Fabaceae and Cucurbitaceae; they are quite widely distributed, and some 600 different forms are known, over 300 in flowering plants (see Rosenthal 1982 for the compounds, etc., Hunt 1991 for some other literature; Huang et al. 2011).
Oligosaccharides, containing three to ten sugar units, include raffinose, a prominent component of the translocate; it is synthesized in the phloem and actively loaded via the symplast into the phloem (e.g. see Davidson et al. 2010, also sugar transport below); the disaccharide sucrose is the commonest component of the translocate (see also polyols below.
Phenols are widespread. Hydroxycinnamic acids such as caffeic acid, p-coumaric, ferulic and sinapic acids and their derivatives are widespread, and the distributions of disaccharide esters of caffeic acid and related compounds (Mølgaard & Ravn 1988) and of rosmarinic acid, an ester of caffeic acid with 3,4-dihydroxyphenyllactic acid (see M. Petersen et al. 2009) are of particular interest. The distribution of caffeic acid itself, perhaps involved in plant defence, seems to be of some systematic interest. It is especially common in herbaceous groups, and is produced from cinnamic acid; proanthocyanidins or non-hydrolyzable tannins (see below under tannin) are also produced from cinnamic acid and tend to show an inverse distribution.
Phorbol esters are diterpenes, often with a toxic effect (Evans & Taylor 1983 for distribution; Evans & Edwards 1987 for physiological effects [see also other papers in Bot. J. Linnean Soc. 94).
There are several photosynthetic pathways involved in carbon fixation. Carbon is incorporated into the organism or, perhaps more accurately, it is initially captured prior to being incorporated into metabolic cycles in three main ways: The C3 and C4 pathways and CAM (Crassulacean Acid Metabolism), the two latter being ways of concentrating CO2 (see Ehleringer & Munson 1993; Yamori et al. 2014 for general accounts; for photosynthesis in bryophytes and early land plants, see papers in Hanson and Rice 2014). Note, however, that aquatic plants in particular can move between different photosynthetic pathways and use multiple carbon concentrating mechanisms simultaneously (Gilman et al. 2023), and there are intermediates between variants of these types and also between the types themselves. For instance, the evolutionary sequence C3 → C3 + CAM → strong CAM has been established in a number of taxa (Gilman et al. 2023) and there is a CAM continuum in most CAM lineages (Messerschmid et al. 2021). E. J. Edwards (2019, especially 2023) discusses the evolution of CAM and C4 photosynthesis from the point of view of the evolution of continuous characters, or as that of distinct "types"; was evolution here a continuum, or did it happen in steps? Although inclining towards the former, she notes that "the creation of discrete phenotypes has great heuristic value, in that it is an essential communication tool and allows us to discuss roughly the evolutionary phases of trait origination, even if the discrete states are not entirely real" (Edwards 2023: p. 720). The slippery slope is evident!
C3 photosynthesis has as it were design flaws, being negatively affected by low CO2 concentration and water salinity stress, for example (e.g. J. J. Sage et al. 2011; Bauwe 2011: esp. photorespiration). Keeley and Rundel (2003) and Raven et al. (2008) discuss the evolution of C-concentrating mechanisms in general. CAM plants tend to grow in places that are inhospitable to C3 plants, while C4 plants more outcompete associated C3 plants (e.g. Keeley & Rundel 2003), as is frequently mentioned (e.g. E. J. Edwards 2019). In CAM changes in CO2 concentration are temporal within the plant, while in C4 photosynthesis they are positional. CAM and C4 photosynthetic pathways, especially their subtypes, are rarely constant in major taxa - sometimes not even within an individual plant - and have evolved in parallel many times. However, both C4 and CAM photosynthesis are particularly common in core Caryophyllales and in Poales, in the latter including Bromeliaceae (CAM; see also below) and Poaceae and Cyperaceae (both C4) in particular. There are intermediate "types", and variation during the ontogeny of the individual (Monson & Rawsthorne 2000; Kellogg 2013; Braütigam & Gowik 2016). It has recently been shown that in Portulaca oleracea, at least, C4 and CAM metabolism are fully integrated and elements of both pathways occur in both mesophyll and bundle sheath cells (Moreno-Villena et al. 2022). To emphasize the point: It can be difficult to establish the presence of a particular CAM mechanism in any one species because its expression there may depend on local environmental conditions (= facultative CAM), there is phenotypic lability, a variety of CAM types, and so on (e.g. Hancock et al. 2019; Winter et al. 2019). There are some aquatic CAM plants like Isoetes, and Gilman et al. (2023) note that aquatic plants in particular can move between different photosynthetic pathways and use multiple carbon concentrating mechanisms simultaneously.
CAM is particularly common in epiphytes and succulents, the former represented by Orchidaceae and the latter by Aizoaceae and of course Crassulaceae; CAM even occurs in the stomata-less but photosynthesizing roots of leafless epiphytic orchids (Winter et al. 1985, 2015; Kerbauy et al. 2012; Carlsward et al. 2021; Heyduk 2022).For a general survey of C4 photosynthesis, see the papers in Sage and Monson (1999) and J. Experim. Bot. 65(10). 2014, also R. Sage et al. (1999, 2012), Kellogg (1999, 2013a) and R. Sage (2016). Although particularly common in Poaceae, it occurs in other families, especially Cyperaceae, Amaranthaceae and other Caryophyllales, and in Euphorbia subgenus Chamaesyce (Osmond et al. 1980; R. Sage et al. 1999; Muhaidat et al. 2007; T. Sage et al. 2011; Horn et al. 2014); it has been much studied in Flaveria (Asteraceae) (Christin & Osborne 2014; Aldous et al. 2014: PEPC protein kinases). C4 photosynthesis is usually a feature of in plants from rather hot, also dry and saline habitats, but also sometimes in plants growing in decidedly cooler conditions (e.g. D. Wang et al. 2008; Christin & Osborne 2014). It acts as a counter to photorespiration, a "design flaw" of RuBisCO most evident at higher temperatures and low CO2 concentrations (R. Sage et al. 2012, but c.f. Busch et al. 2017: stimulation of CO2 uptake by NO3- under photorespiratory conditions); RuBisCO is perhaps the most abundant enzyme on earth (Bar-On & Milo 2019 for estimates of its mass). Keeley and Rundel (2003) note that changing climate, e.g. increasing seasonality leading to changing disturbance regimes, notably increasing fires, and associated changing patterns of rainfall, and also declining atmospheric CO2 concentrations may have been drivers of the later Miocene spread of grasslands; as Kadereit et al. (2012) emphasize, there is unlikely to be a single ecological explanation for the origin of this syndrome (Sage et al. 2012). Neither C4 nor CAM photosynthesis are generally found in trees, and although S. N. R. Young et al. (2020, 2022) looked at C4 photosynthesis as it is found in a few Hawaiian woody species of Euphorbia subgenus Chamaesyce, it was unclear what was driving its evolution there.
As already mentioned, C4 photosynthesis includes several morphological and enzymatic variants (see esp. Poaceae), although some kind of Kranz anatomy with enlarged bundle sheath cells and closely-spaced veins is typical (Sage et al. 2012; for such cells in C3 plants, see Leegood 2008), indeed, bundle sheath cells become major contributors to leaf photosynthesis (Nelson & Dengler 1992; Kumar & Kellogg 2018). Chloroplasts in mesophyll cells commonly move towards the bundle sheath in response to stress, a movement ("aggregative movement") more pronounced in the monocots examined and differing somewhat between the C4 subtypes, e.g. more in the phosphoenolpyruvate carboxykinase than in the NADP-ME subtypes (Y. Kato et al. 2022). E. J. Edwards (2019) emphasized the sequence of events involved in putting together the C4 syndrome, and suggested that an early rate-limiting step was structural, probably involving the bundle sheath. Lundgren et al. (2014), emphasizing the polyphyly of C4 photosynthesis, noted that concentration of chloroplasts in the area in which the Calvin cycle went on was about the only common feature shared by all C4 plants, and this concentration was evident in proto-Kranz plants (R. Sage et al. 2014). The distinctive segregation of the various elements of the C4 photosynthetic pathway may even be evident within a single cell in the spatial segregation of organelles (e.g. G. E. Edwards et al. 2003; Edwards & Voznesenskaya 2011). However, in some submerged monocots and a few terrestrial dicots there is C4 photosynthesis without this spatial segregation of organelles (Boykin et al. 2008 and references), rather, this segregation is at the scale of the cytosol (PEPC) and chloroplast (RuBisCO) within the one cell (see also Bowes et al. 2002; Voznesenskaya et al. 2003; Bowes 2010; von Caemmerer et al. 2014). More examples of separation at the subcellular scale continue to be reported. McKown and Dengler (2010) discuss the distinctive vein patterning in C4 plants, while Lundgren et al. (2018) emphasized that just a single change, specifically, an increase in venation density, was all that was needed for the origination of C4 anatomy in the photosynthetically variable grass Alloteropsis semialata (Paniceae).
The CAM photosynthetic pathway (for which, see e.g. Kluge & Ting 1978; Silvera et al. 2010b; Heyduk 2022) has evolved over 60 times in vascular plants, and in 29 or more families of angiosperms alone (Silvera et al. 2010b; Hultine et al. 2019 and references). It is especially common in epiphytes and plants of arid areas (J. A. C. Smith & Winter 1996; Holtum et al. 2007), and is known from some aquatic plants (for the latter, see Keeley 1998a: Isoëtes is a good example). Silvera et al. (2010b) estimated that there were some 16,800 CAM species (not distinguishing between strong and weak CAM), and of these some 7,800 were orchids, nearly all Epidendroideae. However, CAM photosynthesis is certainly not found in all epiphytic groups (Holtum et al. 2007; Silvera et al. 2010b for a list of families with CAM), and it may be commoner in epiphytes growing in dry habitats than in rainforest and in flooded rather than non-flooded gallery forests (Oliveira et al. 2021). Both epiphytes and plants in arid areas live in habitats where the water supply is erratic. There are four phases in CAM: In phase I there is nocturnal CO2 uptake, carboxylation occurs and malic acid forms; in phase II stomata open in the early morning, carboxylation via RuBisCO occurs; in phase III (most of the day) the stomata are closed, malate moves out of the vacuole and is decarboxylated, high concentrations of CO2 developing around the RuBisCO; and in phase IV the stomata open and RuBisCO carboxylation is driven by a draw down of malate. Overall, evapotranspiration is low and water use is very efficient (Heyduk 2022). In general in CAM plants the cells are rather closely packed and intercellular spaces are reduced (Nelson et al. 2005; Earles et al. 2018). CAM also has a number of variants (see also Heyduk 2022) and it has been suggested that there are intermediates between C3 photosynthesis and CAM, the distinction between CAM and non-CAM species is not sharp, and leaf anatomy and CAM function are not correlated in hybrids (see esp. Silvera et al. 2010b; Winter et al. 2015; Kuzniak et al. 2016; Tay et al. 2021; Heyduk et al. 2020: hybrid Yucca); however, how these purported "intermediates" are treated in analyses affects our understanding of CAM evolution (e.g. Mort et al. 2007). The evolution of phosphoenolpyruvate carboxylase (PeP C), central in CAM photosynthesis and involved in the dark fixation of CO2, is discussed by Silvera et al. (2010b: Fig. 5). Seedlings of at least some CAM plants have C3 photosynthesis, and if conditions are favourable some CAM plants can revert to C3 photosynthesis (Winter & Holtum 2014; Winter et al. 2015). The two photosynthetic mechanisms may be active sequentially as the plant grows, or at the same time in different places on the one plant, even in different places on the same leaf, and members of pairs of opposite leaves may photosynthesize differently, and so on (Lüttge 2008; Freschi et al. 2010; Martin et al. 2010). It has been suggested that the CAM pathway is not fundamentally different from the Hatch-Slack pathway, and this may help explain its flexibility (Bräutigam et al. 2017), in some respects the circadian and diurnal rhythms in CAM and C3 plants being similar (Schiller & Bräutigam 2021), although major changes in the diurnal activity of some of the components of the photosynthetic pathway have to change in CAM photosynthesis (Yin et al. 2018). However, E. J. Edwards (2019) emphasized the importance of structural changes late in the evolution of the CAM syndrome that constituted a rate-limiting step for the whole process, while Winter and Smith (2021) argue that night-time malic acid accumulation represents a discrete evolutionary innovation. For CAM in Kalanchoë compared with that in some other CAM plants, with both sequence convergence and changes in temporal expressions of genes, see X. Yang et al. (2017). For the stomatal biology of CAM plants, see Males and Griffiths (2017), and for other papers on CAM photosynthesis, see e.g. Osmond (1978: important early paper), Griffiths (1989), Winter and Smith (1996), Sayed (2001), Keeley and Rundell (2003), Lüttge (2004, 2005), Boxall et al. (2017), Winter (2019) and other papers in J. Experim. Bot. 70(22). 2019 and I. Y. Y. Tang et al. (2021). On the other hand, Herppich (2004) wondered for what exactly CAM might be an adaptation... See Crassulaceae for a terrestrial CAM family and Orchidaceae for a major epiphytic CAM family.
As already suggested, C4/CAM and C3 photosynthetic pathways are not that sharply differentiated. Thus there are intermediate species with C2 photosynthesis in which CO2 produced by photorespiration by the decarboxylation of glycine concentrates in enlarged bundle sheath cells (Vogan et al. 2007; R. Sage et al. 2011, 2012; Kellogg 2013). That C3 and C4 pathways, or different variants of the C4 pathway, can occur in the same organism (e.g. Surridge 2002; Sage 2004; Muhaidat et al. 2018 for references) may facilitate the reversals that may have happened (Kadereit et al. 2012); Bräutigam et al. (2017) noted that reversals from C4 to C3 photosynthesis were uncommon. Along similar lines, facultative CAM occurs in a number of species of Portulaca, for example, where there are also C3, C4 and C3-4 intermediates (Winter et al. 2019). For the evolution and evolutionary inter-relationships of these three types of photosynthetic mechanisms, see Keeley and Rundell (2003), West-Eberhard et al. (2011 and references), E. J. Edwards and Ogburn (2012), S. D. Smith et al. (2019) and Winter et al. (2019b); note that how photosynthetic types are conceptualised affects our understanding (e.g. Winter et al. 2015, 2019b). In any event, both types of photosynthesis are wildly polyphyletic. Thus CAM photosynthesis is known from 343 genera in 35 families (Silvera et al. 2010b) and
The recent finding that calcium oxalate crystals can be rapidly broken down into CO2 (and H2O2) by oxalate oxidase during the day, so serving as a CO2 source, particularly when the plant is water-stressed and the stomata close (Toolakou et al. 2016), further blurs the boundaries of the photosynthetic types (see also Bräutigam et al. 2017) while suggesting another function for the sometimes massive amounts of calcium oxalate stored in the plant. This behaviour has been noted in eudicots with the three main photosynthetic mechanisms; the calcium oxalate reforms during the night using up non-atmospheric C, i.e. CO2 produced by the plant (Toolakou et al. 2016) - a kind of CAM-cycling.
Phytoalexins, antifungal or antimicrobial substances produced by plants following infection, are very variable chemically. However, some families (Cucurbitaceae, Rosaceae) seem rarely to produce them, others (Brassicaceae) produce chemically very distinctive phytoalexins, while in yet others (Fabaceae) there is some infrafamilial systematic information in the type of phytoalexin produced (Harborne 1999).
It might seem that phytochrome behaviour is perhaps of interest phylogenetically; very limited evidence suggests that Pr is converted to Pfr, and then in core Caryophyllales, Pfr undergoes light-dependent decay, while in broad-leaved angiosperms it reverts to Pr in a thermal dark reaction (Kendrick & Hillman 1971). However, Sarah Mathews (pers. comm.) observes that light-dependent decay of Pfr is very widespread in angiosperms.
Polyacetylenes (more accurate;y acetyleneic compounds) are often derived from their corresponding fatty acids; they have a C C triple bund, but are by no means always polymers. In asterids either polyacetlyenes or iridoids dominate to the exclusion of the other even although they are biosynthetically unrelated; exceptionally, the two may co-occur, as in Torricellia angulata (Torricelliaceae: see Pan et al. 2006; Liang et al. 2009). For an entry into the literature, see Minto and Blacklock (2008).
Polyols are linear reduced forms of monosaccharides that are carbon transporters in the phloem of a few families. They are loaded into the phloem particularly under stress conditions caused by drought or high sodium chloride, although the families which are recorded as having them - Celastraceae, Apiaceae, Oleaceae, Plantaginaceae, etc. - are not particularly notable components of vegetation that is frequently water- or salt-stressed (see Pommerrenig et al. 2007 for the physiological literature). Mannitol is a polyol that is notably common in groups like Oleaceae, but the systematic significance of its distribution is unclear (see Stoop et al. 1996). In others plants sorbitol or dulcitol (galactitol) predominate (see Reidel et al. 2009; Turgeon 2010a; Fu et al. 2011 for details of phloem loading). Root-parasitic plants commonly have mannitol as the main sugar alcohol (Noiraud et al. 2001)
Primary cell wall polysaccharides show interesting variation within land plants (see Scheller & Ulvskov 2010: excellent review; Domozych et al. 2010: comparison of land plants and their immediate relatives; Silva et al. 2011: variation in ferns). These polysaccharides include cellulose, callose, pectins, and hemicelluloses, the latter all having an equatorial β-(1→4)linked backbone Scheller & Ulvskov 2010). Poaceae and perhaps a large part of the asterid I clade differ in xyloglucan hemicellulose composition from other angiosperms and gymnosperms, and Poaceae have a generally different hemicellulose/pectin composition from other seed plants (O'Neill & York 2003; Hsieh & Harris 2012). (1->3),(1->4)-ß-D-glucans are found in many, but not all, Poales (Smith & Harris 1999; Trethewey et al. 2005). There is also be variation in primary wall structure and composition at deeper levels in the land plants (Nothnagel & Nothnagel 2007; Scheller & Ulvskov 2010; Hsieh & Harris 2012). Interestingly, the orientation of cellulose microfibrils in the outer epidermal walls of the elongation zone in roots varies (Kerstens & Verbelen 2002: ANITA grade and gymnosperms not studied). However, sampling in such studies generally leaves something to be desired. For amyloid/hemicelluloses/other polysaccharides in vegetative parts of the plant, see also Meier and Reid (1982), while hemicelluloses in seeds, whether in cotyledons or endosperm, are mentioned below.
Quaternary Ammonium Compounds such as glycine betaine commonly occur in plants growing in saline habitats, and are probably involved in maintaining the osmotic balance of cells and organelles (Rhodes & Hanson 1993). Tertiary sulfonium compounds may also be involved. Halophytes, plants that can tolerate conditions in which the electrical conductivity of the soil solution is equivalent to ca 80 mM NaCL or more (Bromham & Bennett 2014), are clustered in groups like Caryophyllales, Alismatales, etc.. Bennett et al. (2013), Moray et al. (2015), Saslis-Lagoudakis et al. (2016) and others discuss salt tolerance and its evolution in angiosperms, highly polyphyletic, particularly in Poaceae, for example, but much less so in Amaranthaceae s.l., and there are also connections with C4 photosynthesis, alkali and heavy metal tolerance, and so on. Note that details of the distribution of glycine betaine and related compounds are still not well understood, for example, they are also common in many Lamiaceae (Blunden et al. 1996) and Convolvulaceae - families with vanishingly few halophytic members. For a database on halophytic plants, see Santos et al. (2016). The literature on plants growing in saline habitats is extensive, and also includes some literature on mangroves. Growing in mangrove vegetation are not only Rhizophoraceae-Rhizophoreae but taxa from several other genera and families. For more on mangroves and the mangrove habitat, see Rhizophoraceae, and on halophytes in general, see Gul et al. (2019 and references) - this is the sixth and last volume in the series that covers such plants.
Resins and substances either similar to or confused with them are quite widespread in plants; for their distribution, see see Nair (1995), and for a readable summary, Langenheim (2002). For fossilized resins, that is, amber, see Seyfullah et al. (2018).
Saponins. Previously defined as compounds that produced soap-like foams when shaken with water, they are now characterized as being derived from the 30-carbon oxidosqualene (this contains 6 isoprene units) to which glycosyl residues are attached (Vincken et al. 2007, who also provide a classification of saponins). By and large, the distributions of saponins with particular skeletons seems to be of little systematic interest (Vincken et al. 2007). See Sahu et al. (2008) for steroidal saponins.
Sesquiterpene lactones a subclass of C15 terpenoids (= sesquiterpenoids, sesquiterpenes), bitter-tasting and toxic, sometimes with allelopathic effects (Abdelgaleil & Hashinaga 2007), that are derived via the mevalonate pathway from three C5 isopentenyl pyrophosphate units.
Silica (SiO2) accumulation, which can be defined as accumulation of amounts of SiO2 greater than 2% dry weight, is scattered in land plants, but it is perhaps less abundant in seed plants than elsewhere (Trembath-Reichert 2015). See also silica bodies. What exactly silicon might do in/for the plant is poorly understood (de Tombeur et al. 2022).
Steroids, compounds characterized by a nucleus of 17 carbon atoms in the form of four fused rings, three containing six carbon atoms and one containing five; they are derived from triterpenoids - for the synthesis of which, usually mediated by CYP716 enzymes in embryophytes, see Miettinen et al. (2017). For phytoecdysteroids, perhaps protecting plants against herbivorous insects by affecting moulting, etc., of the latter, see Lafont et al. (1991). Steroids" includes quite a variety of structures, and things like bufadienolides (see above) may be included in surveys of steroids; for a still useful literature survey, see Borin & Gottlieb (1993), also Nohara (1989).
For suberin, see Bernards (2002).
The sugar that is the main non-structural or storage carbohydrate in the plant varies. Although usually glucans, polymers of glucose, predominate, in some plants fructans are found (for the latter, see also fructose oligosaccharides above. The distribution of plants with fructans is of systematic interest (for taxa involved, see e.g. Pollard & Amuti 1981: "dicots"; Pollard (1982: "Liliales"), Hendry (1987: taxa in England), and Hendry & Wallace 1993: general). Fructan accumulation may be associated with low temperatures (taxa accumulating fructans are rare in the tropics), and is involved in osmoregulation and cell growth by expansion - perhaps seasonality in general is an important trigger (Hendry 1993; Hendry & Wallace 1993; Livingston III et al. 2009). Note that the taxa storing fructans are a rather heterogeneous group ecologically (a number of Ericales, Poaceae-Poöideae [but not all], a number of Asterales, etc.). Zimmermann and Ziegler (1975) list sugars - Oligosaccharides - and sugar alcohols - see polyols above - found in exudates from sieve tubes (for the latter, see also Noiraud et al. 2001); in many plants the disaccharide sucrose is the main component.
Sulphated/sulfated compounds are particularly common in plants growing in saline habitats, e.g. Juncaginaceae and relatives (Alismatales) and Frankeniaceae/Polygonaceae and relatives (Caryophyllales).
Tannins are either condensed and non-hydrolyzable, proanthocyanidins of of flavonoid origin (see Dixon et al. 2005) or hydrolyzable, and here caffeic acid and in particular gallic acid are the building blocks. The two kinds of tannins are not chemically immediately related, and although the vague terms "tannins" and "tanniniferous" occur in some of the characterisations, the more specific non-hydrolyzable and hydrolyzable tannins are to be preferred. Proanthocyanidins/condensed tannins are synthesised in the chloroplasts, whence they move into vacuoles (Brillouet et al. 2013). They and caffeic acid tend to be alternatives and the latter is especially common in herbaceous taxa, e.g. the asterid I and II groups (Mølgaard 1985 and Mølgaard & Ravn 1986, which see for more details than have been incorporated here). The immediate precursor for both galloyl and ellagitannins is pentagalloylated glucose (1,2,3,4,6-pentagalloyl glucose), and although the derivation of gallotannins from this and their biogenetic relationships are fairly well understood, those of ellagitannins is still unclear (Niemetz & Gross 2005). Ellagic acid, basically two units of gallic acid, is easily detected and its distribution was much commented on in the 1900s. Early surveys by Bate-Smith (1962: phenolics in general) and Bate-Smith and Metcalfe (1957: non-hydrolyzable tannins) are still useful; Bate-Smith (1983) discussed the distribution of galloyl esters. Okuda et al. (2000) reviewed the distribution of various types of hydrolyzable tannins in the context of Cronquistian relationships; ellagic acid is uncommon in the asterid I + II clade. Barbehenn and Constabel (2011) summarized the role of tannins in general in herbivore defence; see also Salminen and Karonen (2011) for tannin type, synthesis and function.
Terpenoids are a diverse and ecologically important group of compounds (e.g. Harborne & Tomas-Barberan 1991) made up of 5-carbon isoprene building blocks (see Bohlmann et al. 1998; Davis & Croteau 2000 for early steps in synthesis, inc. cyclization). Two isoprene units make up monoterpenes, three make up sequiterpenes, etc. Terpenoids include sesquiterpene lactone, resins, and ethereal oils, and are related to steroids, etc. (see above). Well over 30,000 different structures are known, with over 15,000 found in land plants alone, hundreds (some are primary metabolites) being found in a single plant (Pichersky & Raguso 2018); Davis and Croteau (2000), Theis and Lerdau (2003), Degenhardt et al. (2009), Pichersky and Raguso (2018) and others discuss how terpene skeletal diversity in plants is generated and the evolution of their functions. Isoprene (2-methyl-1,3-butadiene) is a hemiterpenoid released in immense amounts by many woody plants (but isoprene production seems to vary infragenerically in a systematically interesting fashion, as in Quercus: Harley et al. 1999) that can have direct effects on biotic interactions between plants and insects, for instance, affecting herbivory (Loivamäki et al. 2008). Although terpenes may have originally functioned in plant defence, they become co-opted by insects that have evolved resistance to them and function as pheromones, floral attractants, etc., the roles than terpenoids play being evolutionarily context dependant. The outcomes of particular plant-insect interactions are sometimes exquisitely sensitive, depending not merely on the presence of an attractant, for when its concentration increases, it may then become a repellant... (Schiestl 2010; Pichersky & Raguso 2018 and references).
For definitions, etc., see the Glossary.
Metcalfe and Chalk (1950; 2nd edition, 1979 onwards) provide information on general plant anatomy, although characters like nodal structure are rarely mentioned in the first edition; the recent Atlas of Stem Anatomy by Schweingruber et al. (2011, 2013) is full of magnificent illustrations. Much classical literature remains useful (see e.g. Thouvenin 1890; Beauvisage 1920; Watari 1939 for taxa that used to be placed in Saxifragaceae). Gregory (1994) is a good bibliography with the more important contributions conveniently indicated, Dickison (2000) is a very accessible introduction to general plant anatomy and Carlquist (2001) updated his survey of comparative plant anatomy (see also Carlquist 1988b; Olson & Pace 2023; Olson 2023); Esau (1977), Mauseth (1988), Fahn (1990), Rudall (2020), etc., are also to be consulted.
For a general survey of the organization of the vascular system in flowering plants, see Scarpella and Meijer (2004) and for vascular anatomy and how it is affected by changes like heterochrony and heterotopy, see Onyenedum and Pace (2021). Of course, the various expressions of heterochrony are hardly restricted to the vascular system (see e.g. Buendía-Monreal & Gillmor 2018).
Note that a number of aspects of development are under the control of physical forces. Thus Sampathkumar et al. (2018) noted that growth affects mechanical stresses in the cells which in turn affects microtubule positioning and auxin transport, which affect the growth and shapes of the cells involved, which affects stress... Self-assembly also plays an important role in systems like pollen wall development in a system akin to crystallization (e.g. Gabarayeva & Hemsley 2006; Blackmore et al. 2007; Gabarayeva & Grigorjeva 2016; Gabarayeva et al. 2018, 2023), and there are truly remarkable similarities between the structures produced by the experiments in Gabarayeva et al. (2019) and the structure of the walls of actual pollen grains.
For programmed cell death (apoptosis, apoptosis-like cell death, autophagic cell death, and necrosis), its nature and role in plant development and organogenesis, see Kacprzyk et al. (2011), van Hautegem et al. (2015) and Dickman et al. (2017). It is much involved in the development of vascular tissue, both xylem (Iakimova & Woltering 2017) and phloem (the sieve tube nucleus becomes non-functional, autolysis occurring, the nuclear contents being released into the cytoplasm where they are degraded - Furuta et al. 2014), the anther, the embryo sac, seed, and so on. It also causes fenestration in leaves (Gunawardena & Dengler 2006); for fenestration in Aponogeton madagascariensis, see Rantong and Gunawardena (2018) and references. The reduction of ATP production in Viscum album, at least, seems to affect senescence: Normal senescence of the leaves does not occur, the leaves falling off the plant when green (Schröder et al. 2022).
Gross Root Morphology. The root systems of a number of central European plants in particular have been described and illustrated (e.g. Kutschera & Lichtenegger 1992). For a general survey of the anatomy of primary roots, see von Guttenberg (1968), for a classfication of root systems, see Cannon (1949), and for the root anatomy of a number of central European plants, see Kutschera and Sobotik (1992) and Betekhtina et al. (2023: monocots). The latter group noted that different monocot families had rather different root morphologies - the differences were probably accentuated by their sampling. For more on roots, see also elsewhere and of course including mycorrhizae above and also elsewhere.
There is a considerable amount of variation in details of root morphology and anatomy, and infraspecific variation that can be linked with climate and soil as is discussed by Clowes (1951), Laliberté et al. (2015, 2017), Boonman et al. (2019) and Ehmig and Linder (2020). Baylis (1975) described the stout (over 0.5 mm across) and often almost hairless endomycorrhizal roots that he noted were common in magnoliid families in particular, and at the other extreme are the hair roots common in Ericaceae that are barely wider than a root hair (their vascular tissue may consist of a vessel, a sieve tube and a companion cell). Roots in many carnivorous plants can be much reduced or even absent (Adlassnig et al. 2005), and Comas et al. (2012) note a reduction of fine root diameter in angiosperms (see also W. Chen et al. 2016). Variation in families like Euphorbiaceae is extreme (Kong et al. 2014) and roots in epiphytic Orchidaceae and some woody monocots like Pandanaceae are notably thick (see also Pagès 2016 for descriptions of branching patterns, root thickness, etc.). Roots may be aggregated and form cluster or proteoid roots, as in many Proteaceae and a few other groups (Dinkelaker et al. 1995; Skene 1998; Neumann & Martinoia 2002; Watt & Evans 1999; Shane & Lambers 2005; Zúñiga-Feest et al. 2014; Lambers et al. 2019); plants with such roots are generally not mycorrhizal (see above). These cluster roots consist of closely-spaced lateral roots, although in some Proteaceae they are more complex, with two or more orders of branching. Other distinctive root morphologies include bottlebrush-like cluster roots in Proteaceae, responses of the plant to nutrient-poor conditions (e.g. Schweiger et al. 1995; Shane et al. 2004b, 2006; Playsted et al. 2006; Gao & Yang 2010). In the nitrogen-fixing clade there are root nodules with a variety of morphologies (see e.g. Corby 1988; Gualtieri & Bisseling 2000; Vessey et al. 2004); N-fixing taxa may also form root clusters of varying morphologies (Lambers et al. 2006, 2012b). Vegetative buds develop on the roots of some species (Peterson 1975), and plants in which this happens may be pernicious weeds.
In gymnosperms like conifers and Ginkgo and in angiosperms other than monocots the radicle or primary root keeps growing throughout the life of the plant, of course producing lateral roots along its length; such plants have a taproot system and are called allorhizic. In monocots the seedling radicle is usually at best poorly developed, but roots develop along the stem, usually at or immediately below the nodes (the so-called adventitious roots), and are lateral in origin (true lateral roots are branches of the primary root); such plants have a homorhizic or fibrous root system (see Mangin 1882 for a survey; Barlow 1986; Groff & Kaplan 1988; Bellini et al. 2014; Pacheco-Villalobos & Hardtke 2018). Aerial roots developing along the stem are quite common in allorhizic angiosperms, helping in the attachment of climbers to their hosts or in support, but the roots may also be thorn-like and have a variety of other functions (see Gill & Tomlinson 1975 for a survey). Monocots are often said to have adventitious roots, which implies a rather haphazard and contingent origin, but their fibrous root systems are anything but that (see also Bellini et al. 2014). For root buds and root sprouts, i.e. stems developing directly from roots, whether in response to damage or not, see references in Bosela and Ewers (1997).
Root apical meristem. For early work, see Schüepp (1917, 1926). Details of the organization of the root apical meristem are known for relatively few extant vascular plants, still less for fossils (but see Hetherington et al. 2016b; Hetherington & Dolan 2018). Whether or not the tiers of initials are closed, i.e. are clonally distinct, open, with the fate of the derivatives of the apical cells not being immediately obvious, or intermediate-open, with some more or less intermediate condition, may be of systematic significance (e.g. Clowes 2000; Groot et al. 2004). The character has been placed on the tree, as much to draw attention to it as anything else; monocots are notably variable. Heimsch and Seago (2008) provide a recent summary of the information about root meristems; patterns of development are difficult to interpret (see also Charbonnier & Vallade 2011). Recent work on root apical meristems in lycophytes (Fujinami et al. 2017) suggest both (near) parallelisms between some modes of development there and those in other vascular plants; the different modes of development described there fit this open/closed distinction. In broad-leaved angiosperms, the root cap is made up of gravity-sensing columella and peripheral root cap cells. Cells of the outer layers of the root cap, the border cells, may remain attached because of mucilage secreted by columella cells. Normally they detach, either individually, the common condition, or in rows, as in Brassicaceae (Driouich et al. 2006), although sampling of this feature is very poor.
The apical meristems of the roots of some monocots, especially those like Pandanus with aerial roots (but see also Rhizophoraceae?) may be very large (Gill & Tomlinson 1975), but I know of no surveys of root meristem size. In some plants, especially Cactaceae and Proteaceae, the apical meristems of cluster or other ephemeral roots, or even the radicle, constitutively abort (Shishkova et al. 2008, 2013).
Root epidermis development. Whether or not the epidermis of the root develops from the proto-epidermal layer that makes up the inner layer of the root cap or from the outer layer of the cortex varies at about the same level as root hair development (Clowes 2000). The inner layer of the root cap is lost completely in monocots (and Nymphaeaceae), the epidermis then developing from the cortex, although the inner layer of the root cap remains attached in broad-leaved angiosperms (van Tieghem & Douliot 1888).
Root hair development quite often occurs in epidermal cells that are just like cells that do not have hairs, that is, there are no distinctive trichoblasts. However, in basal vascular plants, many monocots, etc., trichoblasts, large, densely staining cells that give rise to root hairs, alternate with their sister cells, the smaller atrichoblasts, and both of these cells are differentiated from other epidermal cells. Trichoblasts are usually the proximal cells of the trichoblast/atrichoblast pair (i.e. they are nearer the root apex), but sometimes (e.g. in Poales) they are the distal cells, and in both cases these pairs occur in vertical files. Within some alismatalean families some species have trichoblasts and some do not, and there is interesting variation within grasses. In a third major type of root hair development, scattered in core eudicots including Arabidopsis, root hairs develop above the radial wall of two adjacent underlying cortical cells join, the H position, but if there is no underlying radial cortical cell wall, the N position, then no hair develops (Schiefelbein et al. 1997: Arabidopsis; Clowes 2000; Pemberton et al. 2001; Dolan & Costa 2001; C. M. Kim & Dolan 2011 and references); sampling is very poor. The development of these hairs is similar to that of all cells that show apical growth, including bryophyte rhizoids (see also D. W. Kim et al. 2006; L. Huang et al. 2017; Hwang et al. 2017; Salazar-Henao et al. 2016 and references, also the discussion elsewhere). It has recently become apparent that in some species the thickening on the walls of the root hairs is laid down in spirals, and these hairs break down into spirals (= helical crack root hairs) that are probably effective energy-dissipating units (Kolátková & Vohník 2019 and references). Examples so far known are from epiphytic or aquatic plants, and are ?all monocots.
Most roots have root hairs, although they are less frequent in holomycoheterotrophic (von Guttenberg 1968), aquatic and ectomycorrhizal plants, and in epiphytic orchids, at least; they are also absent in Cupressaceae, etc. (Noelle 1910). Root hairs may be exceptionally long and dense, and resulting in dauciform roots, notably common in Cyperaceae (Shane et al. 2005) or variants such as vellozioid roots (Teodoro et al. 2019). Such features are of both systematic and physio-ecological interest, being involved in e.g. phosphorus uptake (see also Lambers et al. 2006; Shishkova et al. 2008; Brundrett 2008, 2009; see also cluster roots below). In experimental conditions, at least, long and dense (more cortical cells, smaller epidermal cells) root hairs develop when iron and phosphorous are in low supply (Ma et al. 2001; López-Bucio et al. 2003). Note that some fungi associated with plants can stimulate root hair development by the production of auxin-like compounds (Contreras-Cornejo et al. 2009). Furthermore, species of Kobresia (= Carex) may have dauciform roots, and they also form ectomycorrhizal and perhaps other fungal associations (Gao & Yang 2010 and references; see also above under mycorrhizae.
The development of a distinctive outer tissue in roots, the velamen, one to several cell layers across and with variously thickened walls, is widespread in Orchidaceae and is known some other monocots, often in epiphytes (including in Araceae), but also in some terrestrial species (von Guttenberg 1968; Pridgeon 1987; Porembski & Barthlott 1988; Benzing 1996; Kauff et al. 2000). Zotz and Winkler (2013) is one of the few studies to look in detail at velamen behaviour (they worked on epidendroid orchids). In dicots, at least, the cork cambium in aerial roots of various kinds may be superficial, rather than deep-seated as it normally is (von Guttenberg 1968; see also elsewhere); I do not know whether this superficial cork cambium and the velamen might be functionally similar.
In some monocots, especially those with a velamen, hypodermal cells may also be dimorphic (e.g. Kauff et al. 2000), root hairs developing from these cells and pushing up through the overlying cells. There seems to be a relationship between the development of the cutinized root hairs that develop from outer cortical cells and the absence of secondary growth in the root (Pinkerton 1936); there is usually no secondary growth in monocot roots (see Carlquist 2012a for the odd exception). A hypodermis of one or sometimes a few layers of cells is common in roots. In Selaginella and most (ca 90%) angiosperms, but not in other vascular plants, this hypodermis is more or less suberized and has Casparian band-type thickenings, and it is then called an exodermis. For surveys of the hypodermis s.l., see Kroemer (1903), von Guttenberg (1968), Pridgeon (1987), Perumalla (1990a), Peterson and Perumalla (1990) and Damus et al. (1997). These is systematic information in taxa that lack a hypodermis or (in angiosperms) have an unsuberized hypodermis.
In a number of monocots in particular, ?mostly grasses, there are prominent rhizosheaths. These are made up of mucilage from root cap cells, root cap cells, soil particles, bacteria, etc., all anchored to root hairs and surrounding the root; the rhizosheath may occupy a volume up to 16 times greater than that of the root proper (McCulley 1995).
Root stele. The stele or vascular tissue in the root is central, and the xylem forms a solid mass, although it is medullated in many monocots; the root stele of a number of broad-leaved angiosperms, e.g. Mimusops (Sapotaceae) and the primary roots of Clusiaceae and Dipterocarpaceae is also medullated, while that of some monocots, e.g. mycoheterotrophic taxa, some Alismatales, Eriocaulaceae and relatives, Acanthochlamys (Velloziaceae), Sisyrinchium (Iridaceae), etc., is not medullated (e.g. van Tieghem & Douliot 1888; von Guttenberg 1968). The proportion of the root occupied by the stele varies considerably, and in a small study it was found to occupy 20-48% of the cross-sectional area in carnivorous plants (and was sometimes medullated), usually rather less than 34% in other plants (Adamec et al. 2006). Tracheids, and sometimes also phloem, are to be found scattered in the pith in some monocots (e.g. von Guttenberg 1968), while taxa like Brasilochloa sampiana (Poaceae-Bambusoideae-Olyreae) may have a single central metaxylem element (Oliveira et al. 2019).
In the roots of broad-leaved angiosperms there are commonly two to five xylem poles (thus they are di- to pentarch) alternating with phloem poles. Diarch and tetrarch, etc., taxa commonly occur in the same family, but some larger groups (e.g. Rosales, possibly Brassicales) are overwhelmingly diarch. Lateral roots arise on the xylem radii except when the roots are diarch, and then they arise on either side of the xylem poles, but in Pittosporaceae and their relatives origination in this distinctive position is found in taxa that are other than diarch (van Tieghem & Douliot 1888; von Guttenberg 1968). Monocots are more often polyarch (even the primary roots are not diarch), and in a number - but not all - of Poales the lateral roots arise opposite the phloem poles (van Tieghem & Douliot 1888). However, there is substantial intra-individual variation in the number of xylem poles, especially in lateral roots, with increases and decreases occuring along the length of the one root (Torrey & Walllace 1975).
Shoot apical meristem. Romberger (1963), Hagemann (1967), Kaplan and Cooke (1997) and Bowman and Eshed (2000) discuss the basic organization of the apical meristem. In angiosperms the apex of the stem is covered by layers of cells, the tunica, in which cell division is predominantly in an anticlinal direction. The tunica surrounds the corpus, a central mass of cells in which the plane of cell division is not so restrained. Tunica-corpus construction may be a synapomorphy for angiosperms and a parallelism with Araucaria and Gnetales (Johnson 1951; Fagerlind 1954; Pohlheim 1971; also Gifford 1954 for angiosperms; Evert 2006 for gymnosperm meristems). Although details of the organization of the shoot apical meristem are known for relatively few plants, the numbers of corpus layers may be of some systematic interest (Bowman & Eshed 2000). Tissues in monocot leaves often come from three types of cells (Stewart & Dermen 1979), but a 1-layered tunica is somewhat more common there than in other angiosperms. The tunica may be up to four cell layers thick (Gifford 1950; Brown et al. 1957; Jouannic et al. 2011 for literature and information).
There is considerable variation in the size of apical meristems, and stem meristems of Cactaceae are substantially wider than those of most other angiosperms: 400-1500 µm across in cacti, versus often less than 325 µm across, although up to 528 µm in Phoenix canariensis (but lepidocaryoid palms have slender stems and small apices) and almost as big in Nymphaeaceae. Within both polysporangiates and gymnosperms there is also considerable variation in meristem size, and in the gymnosperms the shoot apices of Cycadales are notably larger than the rest - 500-3,300 µm across, versus 400> µm (Gifford 1954; Clowes 1961; also references in Gifford & Corson 1971; Jouannic et al. 2011). Pachycaul plants in general have wide meristems (see also Staff 1968). I do not know of any recent surveys of meristem size. The shape of the apical meristem also varies considerably, from strongly convex in taxa like Poales and Rubiaceae to convex in Plantaginaceae and Onagraceae, and the shape may correlate with various features of the adult plant (Schnablová et al. 2019).
There is little discussion about biomechanics in the pages here, although there are a number of groups like the climbing palms where understanding something about this increases one's appreciation of how they grow (for climbers, see Feild et al. 2012; Rowe & Speck 2015). For instance, hollow stems, as in many monocots, achieve very high bending stiffness despite the relatively low commitment of biomass (Speck et al. 2003). Sheathing leaves are important in preventing the stems from breaking if there are intercalary meristems, as in Poaceae and Arecaceae (Kempe et al. 2013). Details of anatomy can be linked to how the plant deals with biomechanical problems, and there can be substantial variation within the genus as plants deal with similar problems in different ways, or evolve different habits, as in Equisetum, Asclepiadaceae-Secamonoideae, etc. (Speck et al. 2003).
The tunica-corpus construction pattern is involved in the distinctive variegation patterns in the leaves of many cultivated taxa (e.g. Tilney-Basset 1986), i.e., the cells from the differemt layers may/may not have functional chloroplasts, and as the leaf develops these layers produce green/white tissues - the basic structure of the apical meristem is quite stable, although all-white and all-green shoots may be produced (Baur 1909 for an early study). Leaf variegation is quite common in plants of the forest floor, and this may be structural and not affect photosynthesis (Hara 1957; Sheue et al. 2012). J.-H. Zhang et al. (2020) assembled a list of over 1,700 species of angiosperms with variegated leaves. In around 56% of these species the variegated areas were white and were caused by the presence of intercellular air spaces below the epidermis and/or between the palisade mesophyll cells, and in ca 39% of the cases the variegated areas were reddish, purplish, etc., and were the result of the accumulation of non-photosynthetic pigments (Zhang et al. 2020). Y.-S. Chen et al. (2017) also discuss details of the mechanisms involved in variegation - these have evolved in parallel in quite unrelated taxa. M.-H. Zhao et al. (2020) outline various aspects of the genetic control of variegation, the focus there being on mutations affecting the chloroplast/chlorophyll synthesis and on carotenoid and anthocyanin synthesis.
For the vascular anatomy of broad-leaved angiosperms in particular, see the numerous publications by Sherwin Carlquist and his collaborators, and for an appreciation of his work, see Olson (2020) and papers in Olson and Pace (2023). The emphasis in Carlquist's work is more on function, and phylogenetic considerations were found to be less immediately relevant than had been thought in the first part of the twentieth century - not that wood anatomy never correlates with clades... (Onyenedum & Pace 2021). Note that the standardized definitions of details of xylem anatomy in InsideWood: An Internet Accessible Wood Anatomy Database, a great aid to those who are trying to identify woods, may conflict with less static definitions of those more interested in xylem functioning (see e.g. Olson 2023).
In the primary stem vascular system there can be separate bundles (an eustele), or a (pseudo)siphonostele, where the vascular tissue forms an apparently complete cylinder or a complete cylinder. However, Benzing (1967b) suggests that there is no sharp difference between siphonosteles and eusteles in angiosperms, moreover, the use of such terms may be inappropriate when describing the vascular system there (Benzing 1967a; Namboodiri & Beck 1968c; Howard 1979a). The angiosperm primary vascular system can be interpreted as a series of sympodially-branching bundle systems, and this reflects the initial development of the vascular system; the stimulus for its initiation is basipetal auxin movement from the apex of the primordium, so finally linking up with existing stele (). Beck et al. (1982) suggested that there is a correlation in broad-leaved angiosperms between closed primary stelar patterns (with anastomoses between sympodia) and distichous or opposite phyllotaxy and between open patterns (the sympodia are separate) and spiral phyllotaxis; within-family variation in details of stelar construction may be quite extensive (Jensen 1968). Note that interpretation of the primary vasculature in terms of axial or foliar theories yields very different results (Al-Turki et al. 2003), and of course the theories suggest very different pathways for the evolution of the plant body. See Schmid (1982), also Namboodiri and Beck (1968a, b, c), Slade (1971) and Beck et al. (1982) for a discussion of stelar variation and terminology in both angiosperms and gymnosperms; see also below for nodal anatomy. This line of thought originally developed in the context of gymnosperms, but it applies to seed plants as a whole, including seed ferns like Lyginopteris (Beck 1970); monilophytes, on the other hand, have a leaf trace—leaf gap system, a primary vascular system from which traces leave radially.
Cortical and medullary bundles, vascular bundles independent of leaf traces that run in the cortex and pith respectively of broad-leaved angiosperms, are mentioned only when they occur; Col (1904) provides an early discussion and summary of information. They can be confused with especially early diverging (i.e. diverging from the stele well below the leaf they innervate) vascular traces, as in Hasseltia (Salicaceae) and Casuarina (Casuarinaceae). In monocot stems the vascular bundles are usually scattered, and I mention their arrangement only when they are in rings.
In general, cauline vascular bundles are collateral, with xylem to the center of the stem and phloem to the outside. Variants of this are systematically interesting, and are mentioned when they occur; this variation is often reflected in the general arrangement of tissue types in the vascular bundles of the petiole and midrib. Thus in the leaf collateral vascular bundles have xylem adaxially and phoem abaxially, bicollateral vascular bundles have three layers of tissue, phloem-xylem-phloem, while vascular bundles in terete leaves in particular may be exoscopic, with xylem to the outside and phloem to the inside, while endoscopic vascular bundles have the reverse arrangement. In monocot rhizomes in particular, but not in the annual stems, the scattered bundles are frequently amphivasal, i.e., they consist of phloem entirely surrounded by xylem (Jeffrey 1917; Arber 1925), amphicribral vascular bundles have the reverse arrangement.
There are distinctive phi thickenings (lignifications) in root cortical cell walls that are found variously on cells immediately under the epidermis, immediately outside the endodermis, or on cells pretty much throughout the cortex; quite frequently branched, they occur mostly on the radial walls of these cells and they are known from both angiosperms and gymnosperms (van Tieghem 1888 and references; Fernández-García et al. 2014; Aleamotu'a et al. 2019; Collings et al. 2020 for a review). Called "phi" thickenings because of their shape in t.s. (from the Greek letter φ), they are found throughout the seed plants, although by no means in all taxa, and they may serve as mechanical reinforcement, and/or be a response to abiotic stress (Collings et al. 2020). Surprisingly little is known about them, although their presence and details of their morphology may have systematic significance (e.g. Gerrath et al. 2002); they have sometimes been conflated with the endodermis.
Details of the initiation of endodermis and pericycle, etc., differ across seed plants (Stewart & Tomescu 2009), but the systematic significance of this variation is unclear. The endodermis consists of one or a few layers of cells that surrounds the central stele and sometimes also vascular tissue elsewhere (see Kroemer 1903 for a still useful survey, also Trapp 1933). In the root the endodermis is often marked by a single layer of cells with Casparian bands (or Casparian strips), a band of lignification laid down on the anticlinal walls of the endodermal cells (see Rojas-Murcia et al. 2020 for the somewhat unexpected requirements for lignification in Arabidopsis, at least). As the cells age, suberin and more lignin may be laid down, and not always as a band. Such clearly-developed endodermes are uncommon in above-ground stems and even more so in the leaf. However, they may occur there, perhaps especially in herbaceous/aquatic taxa and in monocots (Seago 2020), or in the subepidermal layer in the stem of rhizomes (Perumalla et al. 1990b); Bonnetia (Bonnetiaceae), woody, also has a foliar endodermis (see Gutenberg 1943; Metcalfe & Chalk 1979 for references); Lersten (1997) found reports of an endodermis in conifer leaves to be conflicting. In the stem a ring of starch-containing cells (the starch sheath) may be found in the endodermal position, and Seago (2020) suggested that this was not an endodermis s. str., although Casparian bands may develop when the stem is placed underground (Van Fleet 1961). However, Onyenedum and Pace (2021: pp. 2333, 2335) note "The endodermis is the bundle sheath surrounding the veins in leaves, the starch sheath in stems, and the Casparian strip endodermis in roots ...the only consistent feature of the stem endodermis is topological; it positionally separates the vasculature from the cortex and can sometimes be morphologically recognized by the presence of starch or by a Casparian strip that is most visible in young shoots". Details of the distribution and nature of cauline and foliar endodermes that do have Casparian bands may be of systematic and/or ecological significance - see Alseuosmiaceae, etc.; the recent survey by Seago (2020) of angiosperm shoots with Casparian band-type endodermes should be consulted, and he records such cauline endodermes from many monocots (see also Van Fleet 1942) and also from other angiosperms, especially those that live in more or less aquatic conditions. In the characterizations below any mention of endodermis in the stem or leaf refers to an endodermis with Casparian bands unless specified otherwise.
The pericycle is the outermost part of the stele and is made up of a single layer of cells. In the roots of at least some angiosperms, this layer early differentiates into cells that can subsequently divide and initiate lateral roots and those that cannot (Parizot et al. 2008). There are often lignified fibres immediately external/peripheral to the phloem in the stem, the so-called pericyclic sheath. This sheath is sometimes absent, or it may be made up of sclereids. Since there is no endodermis (see above) in the stems of gymnosperms and woody angiosperms, recognizing a pericycle becomes even harder. Gibson (1993) discussed the need to distinguish between fibres that are derived from phloic tissue and those that are extra-phloic (see also Blyth 1958). Although simple presence/absence and nature (if present) of this sclerified sheath may be of systematic interest, as in Schlegliaceae, Dipsacales, etc., distinguishing between its different origins may also be of value. Morot (1885) discussed variation in the pericycle.
Unlignified cell wall fluorescence is caused by the presence of ferulic and/or coumaric acids. Unlignified walls of most angiosperms do not fluoresce, and only those taxa with fluorescence are mentioned (data largely from Hartley & Harris 1981). Other information on the composition of primary cell walls, especially in monocots, is given by Smith and Harris (1999) and Harris (2000).
Iqbal (1995) and Spicer and Groover (2010) provide an entry into the literature on plant cambia, or lateral meristems (secondary thickening meristems), and the cells that differentiate from them. There are two main kinds of lateral meristems or cambia, cork cambia, which produce bark, and vascular cambia, which produce vascular tissue.
Bark, loosely, that part of the older stem or root outside the vascular cambium, is a complex feature, how it appears being determined in part by the age of the tree, etc.. Although foresters may be able to accurately identify trees in forests they know well to species using bark characters, they tend to be of little value at higher levels. There are exceptions, of course, Myrtales being one, and Whitmore (1962, 1963) attempted to apply bark features systematically to Dipterocarpaceae, and see also Yunus et al. (1990). The products of the cork cambium or phellogen (for a review, see Serra et al. 2022) make up a major part of the bark. Cork cambium produces phellem to the outside and a little phelloderm to the inside; together the three make up the periderm. Cork oak, Quercus suber, is unusual in that its phellogen persists, producing the distinctive and massive cork of that species, but usually sequential phellogens develop, producing the rhytidome. This then consists of a series of phellogens, their products and the tissues they isolate; new phellogens are formed every few years of so successively deeper and deeper in the stem, and pockets of cortical or phloem tissue may be included between each phellogen. Different kinds of cells may be produced as the phellem differentiates from the phelloderm (Serra et al. 2022), when it is first produced (see e.g. Moeller 1882; Esau 1965; E. J. Edwards & Donoghue 2006), and, perhaps most importantly from a systematic point of view (Weiss 1890), where it is first initiated. Cork is commonly made up of suberized cells in radial files, but lignified tissues may also be produced; cork cells in lenticels are not tightly packed, often being rounded, lenticels being involved in gas exchange, but also in stem biomechanics, etc. (Rosner & Morris 2022). Phellogens are widespread in both broad-leaved angiosperms and gymnosperms. In the stem it tends to be either superficial, the common condition in angiosperms, initially being initiated at or immediately below the epidermis (I have not distinguished between these positions), or deep-seated, being initiated deep in the cortex, inside the pericycle, or even in the phloem (for still invaluable surveys, see Moeller 1882 [also much information on gymnosperms]; Douliot 1889, also Kuhla 1987; Waisel 1995; Serra et al. 2022: five positions). Initiation in the cortex is also quite common and there is of course no absolute distinction to be made between the superficial and deep-seated positions - and ultimately periderm initiation ends up being deep-seated when there is a rhytidome.
In broad-leaved angiosperms, at least, the position of the cork cambium in the stem and root of the same plant commonly differs, that in the roots usually being deep-seated (Serra et al. 2022), and in the stem, quite often superficial (see Peterson 1975; Waisel & Liphschitz 1975; Esau 1977; Fahn 1990); the former is the "pericambiale Abschlußgewebe" of Kutschera and Sobotik (1992). However, in plants with aerial roots of various kinds the cork cambium in these roots may be superficial (von Guttenberg 1968); thus Clusieae, alone of Clusiaceae, are often epiphytic and have superficial cork cambium in their roots, but the cork cambium is deep seated in Clusiella, a Clusia look-alike that recent work has placed in Calophyllaceae. However, information on the position of initiation of cork cambium in the roots is hard to come by.
The cork cambium in the stem of monocots is also usually superficial, although records are few (Thompson 1976; Jura-Morawiec et al. 2015); of course, the aerial stems of many monocots are more or less short-lived and lack any secondary thickening at all (see below) - indeed, Serra et al. (2022) suggest that monocots lack a periderm, although there are periderm-like tissues, as in some palms. The cork cambium in the root, when developed, is usually to be found just under the exodermis, i.e. in a rather superficial position (Philipp 1923; Arber 1925; Tomlinson et al. 2011); again, many monocot roots are quite short-lived, so the function of any cork cambium is not obvious. Etagenkork, suberised cells in the cortex that are not produced by a cork cambium, are also to be found in some monocots; there is a connection with storied cork such as that found in species of Philodendron which originates by the periclinal division of cortical cells (e.g. Tenorio et al. 2012).
Czaja (1934) discusses the cork of several taxa that have cork wings on the young stem, although such variation is not of much importance at higher taxonomic levels. Lenticels, a localized development of cork commonly found on stems, vary considerably in anatomy, and are probably involved in a variety of functions as well as gas exchange (Rosner & Morris 2022). The polyderm is a distinctive cambial derivative that is rather infrequently found, but whose distribution often seems to be of systematic significancet, being known from roots in Myrtaceae and Rosaceae (Mylius 1913 for a survey; Serra et al. 2023); here the cambial cells cut off alternating layers of suberized and unsuberized cells - the latter more than a single layer.
Finally, one of the components of bark may be stratified phloem, secondary phloem in which there are bands of fibres alternating with ordinary phloem tissue; this is sometimes well developed and characterises groups like Malvales, Annonaceae, etc.. It is easy to recognize using a hand lens, or even with the naked eye, in phloroglucinol-stained hand sections; stems of plants with such phloem typically have bark that can be pulled off in long strips, and this tissue is often used for making paper-type products. Overall, there is considerable variation in the amount, distribution, and nature (fibres, sclereids) of lignified tissue in the secondary phloem, as is evident in the illustrations in Schweingruber et al. (2019) - transverse sections of the bark of some North Temperate seed plants. At least some Pinus, Ericaceae, etc., may quite lack such lignified tissue. For a glossary of anatomical features found in bark, see Angyalossy et al. (2016). Compound vascular budles in monocot stems (French & Tomlinson 1986).The vascular cambium is the other main type of lateral meristem. In extant vascular plants other than lignophytes, a vascular cambium is found only in Isoëtes and perhaps some Ophioglossaceae, although unifacial cambia producing secondary tissue only from one surface are known from a few other taxa (Spicer & Groover 2010). In angiosperms, both whether or not a vascular cambium develops and the nature of its products are of considerable interest. Vascular bundles in which cambium does not develop are described as being closed; if a cambium develops, which normally happens at the interface between the phloem and xylem, they are open. Seed plants usually have a single bifacial vascular cambium that persists for the life of the plant and cuts off phloem externally/abaxially and xylem internally/adaxially, indeed, the cambium is the plant from one point of view. Note, however, that as with many other characters, vascular cambium is a complex feature, and Tomescu and Groover (2018) decompose a monolithic "vascular cambium" into its underlying variables. For general information on the vascular cambium, see Philipson et al. (1971), while Pfeiffer (1926) discusses "abnorme Dickenwachstum" in his still useful account of variants of secondary thickening - these are further discussed immediately below.
For climbers in particular and their anatomy, particularly their distinctive secondary thickening, see also above and for their branching, see below for more information.
Carlquist (2004, see also 2007b, 2013) studied the secondary tissue of Nyctaginaceae in detail, and suggested that in that family, at least, the use of the term "included phloem" was inappropriate; several taxa that had been described as having included phloem in fact have successive cambia (but see Cunha Neto et al. 2021). In plants with such cambia, a so-called master cambium produces conjunctive tissue adaxially. In this tissue new vascular cambia develop producing phloem externally and xylem internally. Each successive cambium and its products are surrounded by a narrow layer of conjunctive tissue, hence the phloem is not completely included or enclosed by xylem tissue (see also Carlquist 2010; also Philipson et al. 1971). Successive cambia are common in the climbing Caryophyllales in particular, but they are also found in the non-climbing Phytolaccaceae. Robert et al. (2011) note that in such cambia, often found in plants that are under some kind of water stress, both xylem and phloem are organized in a three-dimensional network. See Feild et al. (2012 and references) for more functional/biomechanical aspects of liana anatomy.
Cunha Neto (2023: Fig. 6) has proposed a tripartite division of what can be called vascular variants. 1. Procambial variants include things like medullary bundles, the monocot atactostele with scattered vascular bundles, and compound stems, where the procambium forms a number of independent structures. Procambial variants are usually associated with vascular cambia that are distinctive in some way (Cunha Neto 2023: Fig. 8). Plants with 2, cambial variants, have only a single cambium, the norm, but it may produce phloem wedges, interxylary phloem, or deeply-lobed vascular tissue. Finally 3, ectopic cambia (see also Cunha Neto & Oyenedum 2023: Fig. 1C) are additional cambia that develop ne novo in unusual places, often resulting in an oddly-shaped stem. These include what are called successive cambia here, one cambium forming immediately outside another.
In this site the term interxylary phloem is used to describe the situation when phloem islands cut off internally by a vascular cambium are completely surrounded by xylem cut off by that same cambium (see Carlquist 2013 for a list of taxa; Rajput et al. 2022), and internal phloem (= intraxylary phloem) the situation where phloem is found internally to the xylem in the primary stem (this latter condition is commonly associated with the presence of bicollateral vascular bundles in the leaves). The terms "interxylary phloem" and "intraxylary phloem" are confusing and should not normally be used, however, the terms used both here and to describe the anatomy of lianes (see immediately above) are under review (see especially Cunha Neto 2023).
A number of angiosperms are secondarily woody, their immediate ancestors being herbaceous. Secondary woodiness is sporadic in origin, sometimes being connected with the insular habitat (e.g. Lens et al. 2013 and references - see above; Kidner et al. 2015, etc.); paedomorphosis may be involved (for paedomorphosis, see Carlquist 1962, but c.f. definition; Dulin & Kirchoff 2010). It can usually be recognized by plotting length-on-age curves for the vessel elements; if these curves are flat or decrease, then secondary woodiness is likely, but if they gradually increase, then woodiness is probably primary (see Carlquist 2009 and references; Dulin & Kirchoff 2010; Nürk et al. 2019: secondary woodiness on (sky) islands). In addition, ray cells (see below) in secondarily woody plants are predominantly upright, not horizontal.
For primary thickening/primary thickening meristems/sustained primary growth of the stem in particular, see Boke (1954), Waterhouse and Quinn (1978), Stevenson (1980), etc.. In primarily herbaceous broad-leaved angiosperms, annuals and perennials, increase in width of the stem towards the base may be by expansion of cortical or medullary tissue, whether or not also in association with secondary growth (Troll & Rauh 1950); secondary growth can more or less mask this expansion. The annual/herbaceous habit is quite common in eudicots, and it seems to be the result of changes in gene expression and interactions; since the actual genes involved seem not to have been lost, reversal to woodiness is quite common (e.g. Carlquist 1973; Rowe & Paul-Victor 2012; Lens et al. 2012b, 2013; Davin et al. 2016), unlike the situation in herbaceous monocots where genes have been lost and acquisition of the woody habit involves the evolution of novel mechanisms of secondary thickening (Davin et al. 2016; Roodt et al. 2019). Monocots (?all) have a primary thickening meristem (Rudall 1991a for a summary), perhaps located in the pericycle-endodermis area (de Menezes et al. 2005). Details of its origin and the tissues to which it gives rise vary; the endodermis may produce radial files of cortical cells, while procambial strands are of pericyclic origin. However, de Menezes et al. (2011) have suggested that there was in fact no distinct primary thickening meristem in monocots; this may bear on the nature of monocot secondary thickening.
A normal vascular cambium is absent in monocots, although there may be traces of cambial activity in the vascular bundles (Stant 1970 and references). However, in some monocots a meristem develops that largely cuts off cells to the inside, and these differentiate into tissue made up of separate vascular bundles embedded in ground tissue, i.e., it is an unifacial vascular cambium. This is the so-called monocot secondary thickening that is scattered in Asparagales in particular (Rudall 1995b for records and literature; Jura-Morawiec et al. 2015, 2021), but it has also been reported from Melanthiaceae (Liliales: Cheadle 1937), Eriocaulaceae (Poales: Scatena et al. 2005) and even Arecaceae (Arecales) (Botánico & Angyalossy 2013). Monocot secondary thickening has been compared with the primary thickening meristem of cycads, although development in the first is primarily centripetal and in the second, centrifugal (Stevenson 1980). Jura-Morawiec et al. (2021: table 2) discuss the differences between monocot vascular cambia and cambia in other angiosperms - in the former, the cambial cells are of a single type, they are much shorter, there is no intrusive growth, etc.. Monocot roots rarely have a vascular cambium, although it is reported from Dracaena (Asparagaceae-Nolinoideae), but not in other monocots with secondary thickening in the stem (Arber 1925; Carlquist 2012). There is continuity between the primary thickening meristem of monocots and monocot secondary thickening and between the procambial tissues and the vascular cambium of broad-leaved angiosperms (Diggle & DeMason 1983; see also Zinkgraf et al. 2017: gene expression in monocot secondary thickening).
Reaction wood. The distinctive xylem frequently produced at the branch-stem junction is called reaction wood. It is often suggested that angiosperms and gymnosperms differ in the nature of their reaction wood, angiosperms producing cellulose-rich tension wood on the adaxial side of the branch, gymnosperms producing lignin-rich compression wood on the abaxial side. However, a summary of the information available for angiosperms (e.g. Höster & Liese 1966; Andersson et al. 1973; Erickson et al. 1973a, b; Fisher & Stevenson 1981; Schweingruber 2006; Aiso et al. 2013, 2014, 2016; Groover 2015; Nawawi et al. 2017; Ghislain et al. 2019) suggests that this is a considerable oversimplification, although compression wood may be somewhat less variable (see also Westing 1965, 1968; Timell 1986, 3 vols; Fisher & Marler 2006 for gymnosperms). Tension wood in the strict sense has modified fibres with a lignified primary cell wall, at least, but part of the secondary wall, the S3 and all or part of the S2 layers, is converted into the G[elatinous] layer that contains cellulose pectic mucilages, rhamnogalacturan and arabinogalactan proteins, etc. (G-fibres; called T[ension] fibres in Tomlinson et al. 2014), but no xyloglucans. These G-fibres generate active contraction forces to keep the plant upright - and they are in general involved in plant movement (Dadswell & Wardrop 1955: review; Bowling & Vaughn 2008; Clair et al. 2011; Chang et al. 2015: swelling of the matrix drives development of the tensile stress). However, in a number of taxa, especially tropical species, the G layer becomes lignified, and so tension fibres appear to be absent (Roussel & Clair 2015; Ghislain & Clair 2017: species without cellulosic G layer; Guedes et al. 2017). Furthermore, in many Salicaceae, at least, the G layer may be replaced by a multilayered structure (Ghislain et al. 2016). Compression wood in the strict sense is made up of distinctively modified and highly lignified tracheids, but there are no changes in adjacent xylem parenchyma cells (Donaldson et al. 2015). However, although it is clear that trunks/branches of seed plants that are maintaining their appropriate position vis-a-vis gravity have asymmetrical growth, not much more can be said. Thus Ruelle et al. (2006) noted that in angiosperms with increased xylem, etc., on the upper side of the stem, this wood was highly tensile-stressed and that on the lower side of the stem less so - but anatomical correlates were hard to come by. There can also be changes in the excentricity of the wood along a branch or within a species (e.g. Kucera & Philipson 1977). Note that G-fibres are also found in the tendrils and stems of twining climbers (e.g. Bowling & Vaughn 2009; Chery et al. 2021), in the stems of some Gnetales (Montes et al. 2012) - Gnetum is a liana, and in the roots of some Cycadales and other plants with contractile roots (Tomlinson et al. 2014). For more on reaction wood, see also articles in Gardiner et al. (2014).
Data on cambium storying are taken mostly from Carlquist (1988b); if not mentioned, the cambium is unstoried. Timonin (2021) discussed the evolution of storied fusiform initials; after non-storied initials divided there was subsequent extensive intrusive elongation, furthermore, many of the new initials died. One or both the kinds of cambial initials (ray, fusiform) may be storied, but only rarely are ray initials alone storied, as perhaps in Lauraceae (Paul van Rijckevorsel [pers. comm.] noted problems with this character).
There is a vast literature on tracheary (vessels and tracheids) morphology, especially the nature of scalariform perforation plates of vessels (e.g. the number of bars in the plates), the width of vessels and tracheids, the nature of their pitting, etc., although there is surprisingly little information about vessel length (Jacobsen et al. 2012). For useful lists of terms used to describe wood anatomy, see Wheeler et al./IAWA Committee (1989: hardwoods; see also Miller & Baas 1981 and Miller 1981 for characters, coding and computerization), Richter et al./IAWA Committee (2004: softwoods) and Crivellaro and Schweingruber (2015: flowering plants in general). InsideWood: An Internet Accessible Wood Anatomy Database http://www.lib.ncsu.edu/insidewoood/ is a huge and ever-developing resource for information about wood anatomy, also identification, and the like (see Wheeler et al. 2007 for a summary of the frequency of a number of characters there).
Throughout much of the twentieth century, the nature of the vessel perforations and other elements of tracheary anatomy were treated as being of very great phylogenetic importance, and variation in individual features involved were often described in the context of evolutionary "trends"; similarities in tracheary tissues were thought to be particularly important when determining relationships (e.g. Bailey & Tupper 1918; Bailey 1944; Cheadle 1944; Cheadle & Tucker 1961). As an example, one of these trends was supposed to proceed as follows - tracheids only -> scalariform perforation plates with many -> few bars -> simple perforation plates; the cells also became shorter and wider and the end wall less oblique, etc. (e.g. Tippo 1938; Bailey 1944, 1954). There is infraspecific variation in tracheary elements, both vessels and tracheids being found in wood, the variation occurring either during ontogeny or in the course of a season's growth (e.g. Carlquist 2018b). Carlquist has suggested that scalariform perforation plates help prevent embolisms, but they also reduce water flow and so are at an advantage in situations where high conductance is not at a premium, like cool, moist cloud forests (Carlquist 2018b). Once scalariform vessels have been lost, they are unlikely to be regained - Carlquist's Ratchet (Olson 2020). Vessels with simple perforation plates must be very highly homoplasious...
Carlquist (e.g. 1988, 1998b, 1998c, 2001b, 2012c; see Olson 2020) has repeatedly emphasized the connection between features of wood anatomy, evolution, function, and the environment. Baas and Wheeler (1996) think about xylem characters in the context of phylogeny and Baas and Wheeler (2011) more specifically discuss some of the literature bearing on the functional and phylogenetic implications of features of wood anatomy, an area where debate remains lively; M. dos S. Silva et al. (2020) look at the various features that make up the rings of wood in the context of both phylogeny and function. Futhermore, many characters have states whose limits need justification, especially in the context of angiosperm-wide surveys such as this, and for such reasons wood anatomical features must be interpreted with caution. For wood anatomy and cladistic characters, see e..g. Herendeen and Miller (2000) and Rosell et al. (2007). Indeed, Olson et al. (e.g. 2011, 2013, see also Olson & Rosell 2012) note that thinking of anatomical features as being linked directly to the environment may skew our perspective; there are scaling relationships between anatomical features and other features of the plant, thus vessel diameter may be more immediately connected to e.g. plant height, rather than being selected for independently (see also Plant architecture above. Kaack et al. (2021) examine the relationships between pore size in pits in xylem, pit membrane thickness, and embolism (cavitation) - membrane thickness determines embolism resistance.
The phylogenetic significance of variation in xylem anatomy in particular and wood anatomy in general may be rather less than was thought. Indeed, whether plants like Amborella, Nymphaeaceae and Cabombaceae, and Trochodendrales have vessels is unclear; it partly depends on the definition of vessels. Herendeen et al. (1999b) surveyed wood anatomical features in basal angiosperms and compared their findings to the classical evolutionary trends (see below); Carlquist (2012) provided an extensive critical survey of monocot vessel and tracheid morphology and their use in phylogeny. Olson et al. (2012, 2013) found that vessel diameter was strongly linked with stem diameter, although the Baileyan trends are thought to be more or less evident in the fossil record even though stem diameter may be less clear (Wheeler & Baas 1991). Herendeen et al. (1999b) noted that there was polymorphism in perforation type (scalariform/simple) in no fewer than 54 families of broad-leaved angiosperms, although it was uncommon in five of these. Scalariform perforation plates are most frequently found in taxa growing in cooler climates (Jansen et al. 2004b: context?), while holomycoheterotrophic monocots lack vessels, clearly a secondary absence (Cronquist 2012b), as may holoparasites.
The distribution of tracheids in protoxylem (common) and metaxylem (much less common) in broad-leaved angiosperms is detailed by Bierhorst and Zamora (1965). As already suggested, the distinction between vessels and tracheids is not always that sharp (e.g. Feild et al. 2000b; Hacke et al. 2007; Carlquist & Schneider 2009; Carlquist 2012a), fibrils across the plate being closer or more distant and breakdown more or less evident. Pit membrane remnants are turning out to be quite common in broad-leaved angiosperms (e.g. Aextoxicaceae, Bruniaceae, Hydrangeaceae, families near Ericaceae, Schisandraceae, Quintiniaceae, Rousseaceae), and in monocots, but the functional and systematic significance of this feature is unclear (e.g. see Schneider & Carlquist 2003, 2004a; Carlquist & Schneider 2004).
For information on the nature of the vessel element perforation plates in broad-leaved angiosperms, see Bierhorst and Zamora (1965), for those in monocots, see Wagner (1977, sampling needs to be extended/newer literature integrated) and Carlquist (2012). There has been discussion whether vessels in monocots and those in other angiosperms arose independently (e.g. Cheadle 1942; Cheadle 1953; c.f. Carlquist 2012a), and given the morphology of vessels in Nymphaeales (Carlquist & Schneider 2009), perhaps the same question may be asked of broad-leaved angiosperms - or perhaps the question as phrased, or the implications behind it, are really not that important. The distribution of vessels in the monocot plant body, whether in the stems, roots, etc., may be of systematic interest (Cheadle 1944 and references; Wagner 1977; but see Carlquist 2012a). Returning to function again, little is known about how the xylem in palms like rattans (Arecoideae) and large, long-lived palms in general remains functional since there is no secondary thickening, vessels are of course made up of dead cells, and the plants may be over 100 m long (rattans) or hundreds of years old (see elsewhere). A few vessels in dicotyledonous-type plants may be very long - the height of the tree (Zimmermann & Jeje 1981) - but they are soon replaced by cambial products.
Some information is included about the presence of vascular tracheids and wood fibres, and the presence and distribution of xylem parenchyma (see Hess 1950 and in particular Carlquist 2015a, 2018a), but these features are neither treated consistently nor mentioned for all families.
Pits. Vascular pits are quite variable in morphology and arrangement, although the distinction between some of the pit "types", such as bordered and non-bordered pits is arbitrary. It is thus hardly surprising that Herendeen et al. (1999b) noted that presence/absence of bordered pit varied in some 45 families of broad-leaved angiosperms. The nature of intervascular pitting may be of systematic interest, but I have not included many details of this character. Hacke et al. (2004) describe how the torus-margo pit membranes of gymnosperms function (see also Sperry & Hacke 2004; Pittermann et al. 2010; Hacke et al. 2015; Dute 2015 for a summary). A torus, sometimes lignified, also occurs in a few angiosperms (e.g. Coleman et al. 2004), and its distribution there may be of systematic interest. Note that the margo of such pits in angiosperms consists of closely woven cellulose microfibrils, compared with the distant microfibrils and openings in gymnosperms, and the pits in the two groups probably have different functions (Hacke et al. 2015; Dute 2015). Whether or not pits have tori is not always easy to recognize (Rabaey et al. 2006) and not all pits on the one plant have a margo-torus construction (Jansen et al. 1999). Vestured pits have close and minute sculpturing of the surface of the cell wall in the pit (this sculpturing may spread to the whole wall), and their distribution is of systematic interest (e.g. Jansen et al. 1998, 2001a, 2008; Carlquist 2017). Nearly all taxa with vestured pits - perhaps ca 30% of all woody flowering plants and ca 50% of woody species in tropical lowland forests - have vessels with simple perforation plates, and vestured pits may promote the functioning of these vessels (Jansen et al. 2003b, 2004b; Baas et al. 2003). Jansen et al. (2004b) noted that vestured pits were most likely to be found in plants growing in deserts or tropical seasonal woodlands. However, Jansen et al. (2008) noted that vestures were not to be found on the rims of large, simple perforations, being associated only with small perforations, which did not seem to make obvious functional sense; Carlquist (2010, 2017) also discussed how vestured pits might function.
Wood fluorescence. Data are taken largely from a survey of some 10,600 species summarized in Avella et al. (1988). I am unclear as to the significance of this character.
Details of vascular ray "types" are rarely mentioned, partly because it is difficult to reconcile the definitions of the terms as they have been used over the years (see Kribs 1935, 1959), partly because of the typology involved, and partly because it can be difficult even to define what a ray is (Carlquist 2003). Systematically interesting information in this feature is probably best recorded in descriptive terms, i.e., describing the morphology of the cells involved, the width of the rays, etc., and here the short discussion by Chalk (1983) is useful. Particularly distinctive rays are found in some Malvaceae (e.g. Chattaway 1933a, b). Ray width in both xylem and phloem may vary considerably. Broad phloem and xylem rays are a valuable field character for identifying families, and when the phloem rays are wide, tangential cuts of the phloem show a net-like arrangement of the paler-coloured, anastomosing rays (Keller 1996). More precise indication of ray width can provide systematically interesting information (see Herendeen et al. 1999b for some "basal" angiosperms and relatives). Frankiewicz and Oskolski (2023) discuss the absence/presence, time and place of development of rays in angiosperms with respect to whether or not the procambium consists of separate bundles or a continuous ring of vascular tissue and the subsequent development of tissues produced by the vascular cambium; for rayless angiosperms see also Carlquist (e.g. 1962, 2015b).
Phloem. For a good survey of phloem micromorphology, etc., see papers in Behnke and Sjolund (1990), also . In gymnosperms sieve cells are involved in carbohydrate transfer, and these cells are at least sometimes notably long (Jensen et al. 2012) and nucleated, although the nucleus degenerates and becomes pycnotic. The sieve pores are distinctive. They are narrow, and are traversed by endoplasmic reticulum (ER), and they join to form a cavity in the region of the middle lamella (e.g. Behnke 1990a; Iqbal 1995). These sieve cells are associated with Strasburger cells (albuminous cells) which, although closely linked functionally with the sieve cell, are not formed from the same mother cell. In angiosperms sieve tubes carry out the same function as sieve cells; they have rather wider pores that lack ER and the mature cells lack nuclei (the nucleus usually becomes chromalytic and disappears). Sieve tubes are usually closely associated with nucleated companion cells that are derived from the same immediate mother cell (Behnke 1986 for literature and definitions; Botha 2013). For microfilament-rich peripheral phloem cells, perhaps restricted to extant gymnosperms, see Pesacreta (2009).
There is a striking blue iridescence in the leaves of a number of ferns and a few monocots that is produced by so-called photonic structures, in these cases reflecting helicoid structures in the cell wall; perhaps basically involved in providing strength and support for the plant, blue iridescence would be a secondary "product" of such structures (Lundquist et al. 2024).
Chloroplasts are of course to be found in nearly all land plants, but they vary in what cells they are to be found, in number and position within those cells, as well as in morphology and function, and this variation is particularly evident in plants with C4 photosynthesis and in plants, quite often with variegated leaves, growing in low-light conditions (e.g. Solymosi & Keresztes 2012; Sheue et al. 2015; Pao et al. 2018; Beltrán et al. 2018). This leads on to the topic of how light moves through the plant (e.g. Vogelmann 1993). Thus in C4 photosynthesis the plastids in bundle sheath cells and those in the intervening mesophyll have different functions, they may or may not produce starch granules, and so on. There is also blue iridescence in a number of species of Begoniaceae which have a notably regular arrangement of thylakoids in chloroplasts (= iridoplasts, lamelloplasts) in the adaxial epidermis, while minichloroplasts, with normal grana-stroma structure, were found in other epidermal cells (Jacobs et al. 2016; Pao et al. 2018). Furthermore, some plastids in the epidermis and in vascular parenchyma, the so-called sensory plastids, are rather smaller than other chloroplasts; they are involved in various kinds of stress responses, not photosynthesis (Beltrán et al. 2018). Iridescence has also been recorded in some monoplastidic species of Selaginellaceae subfamily Selaginelloideae with distinctive bizonoplasts (J.-W. Liu et al. 2020).
An important set of characters is found in the structure and composition of sieve tube plastids, highly modified structures. Data on the ultrastructural morphology of these plastids, in particular, their starch and/or proteinaceous inclusions, are taken from the work of Behnke (e.g. 1969, 1981b, 1989, 1990a, 1994a, 2001; summaries in Benhke 1972, 1974, 1975, 1981a, 1981c, 1991a, 2000). Angiosperm sieve tube plastids usually include starch grains alone, and this is the primitive condition for the clade. However, in very nearly all monocots the plastid inclusions are cuneate protein crystals alone while in core Caryophyllales there are peripheral protein fibres; Pistia (Araceae) is the only monocot known to have starch-containing plastids (Behnke 1995). There are many other less striking variants with various combinations of starch and protein, and these may characterize smaller clades such as [Erythroxylaceae + Rhizophoraceae] (c.f. Behnke 1988b), whilst the absence of both starch and protein is common in parasitic groups, and also in Rosales, [Malpighiaceae + Elatinaceae], etc.. The sizes of the starch grains and fine details of the protein crystals in the plastids may provide still more evidence of relationships, although I have not always included this information. All told, this character complex is of considerable systematic significance, yet the function of sieve tube plastids, and hence the evolutionary significance of the variation they show, is unclear (Tratt et al. 2009). Chromoplasts are another kind of plastid, and they are involved in pigment synthesis and storage, while leucoplasts are non-pigmented plastids that include storage plastids like amyloplasts, involved in storing starch, and other plastids that are involved in the synthesis of fatty acids and a variety of other metabolites.
P-proteins are proteins in mature sieve elements of angiosperms that vary in origin (the come from the nucleus or elsewhere) and appearance (aggregated [non-dispersed] or not, shape of aggregations, fibrillar or tubular) and also behaviour, e.g. changing their morphology when the turgor of the sieve tube changes, as in Fabaceae-Faboideae (Knoblauch et al. 2001; Peters et al. 2008, 2010; Knoblauch & van Bel 1998). Information on this character, varying mostly in broad-leaved angiosperms, was obtained largely from Behnke (1981a, 1991b); P-proteins are absent from non-angiosperms and at least some monocots, e.g. Poaceae, but they are present in e.g. Iridaceae (Evert et al. 1973; Tóth & Sjölund 1994; Sabnis & Sabnis 1995). Callose is also deposited very quickly over the pores of sieve plates when phloem is damaged (Mullendore et al. 2010: Parre & Geitmann 2005: mechanical properties of callose), and both callose deposition and protein bodies that can reverse their shape (e.g. Peters et al. 2008, 2010) may be involved in the plugging of sieve plate pores. How the pores are plugged may depend on whether the phloem is exposed to bright light or there is mechanical damage (Knoblauch & van Bel 1999). Gymnosperms lack P-proteins, and there the pores may be plugged by the swelling of the ER that traverses them (e.g. Shulz 1992). However, the role of protein agglomerations in modulating phloem flow is unclear; they do not seem to affect it in Arabidopsis thaliana, at least (Froelich et al. 2012). All in all, sieve tube flow is poorly understood (Jensen et al. 2012).
There is little variation in other aspects of sieve tube morphology that is easily usable at higher levels. Sometimes sieve tubes or sieve cells have substantially thickened, lamellate and nacreous secondary walls; these seem to be sporadically distributed, although within gymnosperms they may be restricted to Pinaceae (see Behnke 1990b: cycads, etc.; Schulz 1990b: conifers; Evert 1990b: "dicots"; Eletheriou 1990b: monocots). Zahur (1956) described substantial variation in many characters, albeit it seems to be overlapping (Iqbal & Zahur 1995 list trends of specialization). Zahur (1956) found a weak correlation between presence of secondary septae and sympetalous families, but his data show variation within orders. Turgeon et al. (2001; see also Gamalei 1991) summarise variation in companion cell anatomy and delimit a number of "types" in the minor veins of leaves. Type I or open phloem probably has symplastic connections between bundle sheath and phloem, there being 10-100 plasmodesmata/mm2 between bundle sheath and companion cells, while Type II or closed phloem probably has apoplastic connections, there being only ≤10 plasmodesmata/mm2 (see also Batashev et al. 2013).
Recent work suggests that there is unexpected variation in phloem tissue that is connected to differentiation of function within the phloem. For example, within commelinid monocots, and especially Poales, some sieve tubes lack companion cells, are notably thick-walled, and seem to be involved in short distance transport of not very concentrated sugars (Botha 2013). The phloem system in Cucurbitaceae is very complex. Fischer (1884) early noted that those Cucurbitaceae that had bicollateral vascular bundles also have extrafascicular phloem (EFP) strands in the cortex outside the sclerenchymatous ring. The sieve tubes of the EFP system differ in morphology from those of the fascicular phloem, although they may be similar to cells in the peripheral part of the latter (Crafts 1932). The composition of EFP and fascicular phloem exudate is very different: Fascicular phloem exudate is rich in sugars and unidentified proteins, etc., EFP exudate contains P-proteins, amino acids, protein synthesizing machinery, and various secondary metabolites, but little sugar (Zhang et al. 2010). The EFP system is involved more in plant defence, and Gaupels et al. (2012) even thought that ecologically EFP exudate was like latex (see also Tallamy 1985; Konno 2011; Gaupels & Ghirado 2013). In both these systems aphids are able to distinguish between sieve tubes that have more concentrated sugars and those that do not.
There is interesting variation in how sugars are translocated within the plant that is linked both with details of phloem anatomy and with phsyiology. Intermediary cells in phloem tissue are characterized by having numerous plasmodesmata that branch in the outer part of the walls adjacent to the bundle sheath cells. There seems to be a correlation between the presence of intermediary cells and the presence of raffinose and stachyose in the translocate; sucrose is the most common form in which carbohydrates are translocated. However, whether or not such characters are more or less constant within families is not obvious (see Lamiales), and the link between type of carbohydrate translocated and details of phloem anatomy is not entirely clear (see also Goggin et al. 2001; Turgeon & Ayre 2005). However, there are interesting correlations between how sugars move into the phloem, plant habit, and climate (see e.g. Rennie & Turgeon 2009; Turgeon 2010b; Fu et al. 2011; Davidson et al. 2011, also the Garryales page). Unfortunately, how sugars move into the phloem in gymnosperms is unknown (Liesche et al. 2011), and I do not know how sugars are transported in monocots. Zimmermann and Ziegler (1975) list sugars and sugar alcohols found in exudates from sieve tubes in broad-leaved angiosperms; the transport of raffinose family oligosaccharides is involved in a particularly distinctive sugar tranport mechanism.
Transfer cells, metabolically very active cells with more or less labyrinthine intrusions of the walls, occur in various parts of the plant (e.g. Gunning & Pate 1969a, b; Gunning et al. 1970; Pate & Gunning 1972; Tölke et al. 2019), e.g. the heads of the glandular hairs in insectivorous plants, in nectariferous trichomes, at one or both sides of the gametophyte-sporophyte junction, associated with phloem in vascular bundles (they are one type of companion cell), especially in the xylem and at the nodes, and in seeds.
The stem, node and leaf are part of a continuum (see especially Howard 1974, 1979a), and to understand nodal anatomy serial sections of the stem, leaf base, and petiole should be examined together - this is not too difficult! For information about nodal anatomy see especially Sinnott (1914), Dormer (1946a), Marsden and Bailey (1955), Bailey (1956), Balfour and Philipson (1962), Cutler and Gregory (1998), Howard (1970, 1974), Beck et al. (1982), and Metcalfe (1987). Note that the behaviour of protoxylem strands in the young stem may not correlate with node type (e.g. Beck 1962; Kumari 1963; Benzing 1967a, b; Gibson 1994), and treating flowering plants as if they had a modified siphonostele (see above) may obscure information (Keating 2000). In particular, although I refer to "leaf gaps" in these pages, Beck et al. (1982) and Namboodiri and Beck (1968c) in particular argue that this is inappropriate when talking about the steles of seed plants given the basically sympodial construction of the primary vascular system (for sympodial construction, see also Balfour & Philipson 1962). However, when looking at nodal anatomy in stems with some secondary thickening, one cannot see that the ring of vascular tissue originally consisted of sympodia, the separate bundles going to the leaf originally being traces from these sympodia. In the descriptions I use formulae like 1:1, 5:5, etc.; the first number is the number of gaps, the second is the number of traces or separate vascular bundles leaving the gaps as seen in cross sections at or near the nodal region. These gaps are often recognizable as interruptions in the vascular cylinder formed by the early stages of secondary thickening. Split laterals occur in some taxa with opposite leaves and are single traces that send branches to both leaves (e.g. Howard 1970). They are designated by formulae like "1:1 + split laterals" in the characterizations; this means that each leaf has a three bundles entering the base, one from the central bundle (the "1:1" part), and one from each of the split laterals. Indeed, split laterals may be derived from 3:3 nodes by the approximation of the lateral bundles (Maity 2014). Related flank-bridges and variants are found in some Dipsacales and Rubiaceae (e.g. Neubauer 1982), etc.. 1:3 means that the single bundle immediately splits into three. There can be quite extensive variation in nodal anatomy even within an individual, especially in the context of heteroblastic leaf development, plants with anisophyllous leaves, leaves along an inflorescence, whether or not an axillary bud develops, and so on (see e.g. Post 1958; Ezalarab & Dormer 1963; Howard 1970; Dengler & Donnelly 1987; Dengler et al. 1989; Dengler 1999). This also applies to the primary vascular organization as a whole, not to mention what is going on at the cotyledonary nodes (see below). The nodal anatomy of the characterizations here is that of expanded leaves on a vegetative shoot.
In addition to variation in the innervation of the leaves, there is also variation in the vascular supply to the axillary buds (e.g. Dormer 1950; Ezalrab & Dormer 1963). This usually comes from the sides of the central gap (assuming that there is more than a single gap), but in some taxa the vascular tissue is derived from several leaf gaps.
The basic nodal condition for seed plants as a whole may be 1:1, although some have argued for 1:2 (Kumari 1963; Namboodiri & Beck 1968c). Gymnosperm nodal anatomy is also described in terms of gaps and traces (e.g. Namboodiri & Beck 1968a, b for information), although at the very least the behaviour of the traces can be unexpected from an angiosperm perspective, as with the girdling traces of the foliage leaves in Cycadales. Within Pinales (for example) 1:2 nodes occur only (but not always) in taxa with opposite leaves (Namboodiri & Beck 1968a, b; see also below).
Leaves with stipules usually have trilacunar nodes and often have blades with serrate margins (Sinnott & Bailey 1914; see also Ye & Ronse De Craene 2024). Celastraceae, with their unilacunar nodes, stipules, and more or less serrate blades, seem to be an important exception, however, their stipules can be the most evanescent of structures (see also some Myrtales), while both Perrottetia and Bhesa, recently removed from Celastraceae (and now in Huerteales and Malpighiales respectively), have more complex nodes - and much more obvious stipules, especially in Bhesa. Rosaceae tend to have 3:3 or more complex nodes, and are generally stipulate; the estipulate Spiraea has 1:1 nodes. There is a similar relationship between the normally trilacunar and stipulate Elaeocarpaceae that also include the unilacunar, estipulate Tremandra and its relatives, and also within the small family Surianaceae; some species of Euphorbia (subgenus Esula can be estipulate) have 1:1 nodes (Sehgal & Paliwal 1974). Lateral traces of trilacunar nodes often form wing bundles in the petioles, and branches from them may innervate stipules, when present. However, Rubiaceae, a family characterized by its conspicuous interpetiolar stipules, not infrequently have unilacunar nodes, but lateral bundles immediately split off (they can be a sort of 1:3 node) and form a vascular ring around the stem, and it is from this ring that the stipules are innervated (e.g. Majumdar & Pal 1958). Finally, broad-leaved angiosperms with sheathing leaf bases and also those with compound leaves usually have multilacunar nodes (Sinnott & Bailey 1914), whether or not they also have stipules.
Nodal anatomy is very complex in aquatic angiosperms like Nymphaeales, with a vascular plexus forming at the nodes and the internodal vascular tissue being very distinctive, even if ultimately the vasculature of the leaves can be interpreted in conventional angiospermous terms (c.f. Schneider 1980; Moseley et al. 1984). Although many asterids, especially Lamiales, etc., are commonly reported as having 1:1 nodes, Neubauer (e.g. 1977, 1978) emphasized that there the single trace often divided immediately into three or more (e.g. see Linderniaceae, Scrophulariaceae, also Cordia [Boraginaceae]). Nodal anatomy may repay attention in Gesneriaceae, and perhaps more generally in Lamiales, also in Melastomataceae, Primulaceae, etc..
For the nodal anatomy of cotyledons, see Bailey (1956). Nodal vascularisation of cotyledons and foliage leaves of the one plant may differ (e.g. Stone 1970). Cotyledons often have 1:2 nodal anatomy (E. N. Thomas 1907; Bailey 1956), whatever the nodal anatomy of the later leaves; this may be connected with the fact that cotyledons are opposite (c.f. gymnosperms!). Note that there can be quite a lot of variation at the cotyledonary node, too; it may be multilacunar in Juglandaceae, or 4:3 in some Magnoliaceae (with split laterals, e.g. Sugiyama 1976a).
Gross patterns of nodal anatomy are often easy to confirm in the field using a razor blade or sharp knife and a hand lens, and so can help in identification. Thus the 1:1 nodes of Celastraceae clearly differ from the 3:3 nodes common in Malpighiales and with which Celastraceae can otherwise be confused vegetatively.
Monocot leaves usually have broad bases into which several bundles proceed, and the course of the bundles in the stem may be very meandering (e.g. Falkenberg 1878), but Sinnott and Bailey (1914) noted that in the petiolate Potamogeton and Smilax there was a tendency for three main bundles to enter the leaf base (see also Colomb 1887), and this was noticed early by Nägeli (1858) in some Dioscoreaceae. Details of nodal vasculature are not generally recorded for monocots.
Aerenchyma is developed in aquatic plants both in the roots (Seago et al. 2005) and also elsewhere (Jung et al. 2008 for a convenient summary); the mode of formation of the aerenchyma varies.
Latex in the strict sense, an exudate in which terpenes predominates (in rubber polyisoprenes are common), is generally found in laticifers, rarely in isolated cells. It can be characterised as an emulsiuon of small particles dispersed in a liquid, the two having different refractive indices (Teixeira et al. 2020). Note, however, that there are all sorts of problems around here. 1. Any white exudate in plants is often uncritically called latex, which, as just mentioned, is an exudate with a particular composition; other exudates include resins, the exudate being mostly terpenoids or sometimes phenolics, gums rich in polysaccharides, etc.. 2. The distinction between isolated cells/multicellular glands and canals is arbitrary, groups of the former on occasion fusing to form the latter as in Kielmeyera (Calophyllaceae) and Casearia (Salicaceae), for example (Fernandes et al. 2018; Costa et al. 2021). 3. Much has been made of the distinction between articulated and non-articulated laticifers. Nonarticulated laticifers are branched or unbranched but not anastomosing syncytia that originate from single cells in the embryo and subsequently grow intrusively as the plant develops; Castelblanque et al. (2016) discuss their growth and development in Euphorbia lathyris, noting that these laticifers lack chloroplasts and also any plasmodesmatal connections with surrounding cells, the latter because of their intrusive growth. Articulated laticifers may be anastomosing or non-anatomosing. They are generally associated with the phloem and are tubes that develop from series of cells whose common end walls have broken down (c.f the distinction between glands and canals above). However, the difference between the two "types" may not be that great and they may occur in the one plant (see also Demarco et al. 2006, 2013; Dussourd 2016; Prado & Demarco 2018; Ramos et al. 2019; Ramos et al. 2020; Teixeira et al. 2020b; papers in Nawrot 2020).
Thus laticifers in the broad sense contain secretions other than latex in the strict sense - the use of laticifers in the broad sense is not very helpful. Various tissues in the plant contain distinctive secretions (see Langenheim 2003: resins; Lambert et al. 2015). For resin secretion, which occurs in various ways in schizogenous secretory ducts lined by epithelium, see Prado and Demarco (2018) and Alencar et al. (2020); gums, mucilages, etc., are also produced, and gums and resins may even be produced in different secretory canals in the one plant (Costa et al. 2021). Prado and Demarco (2018: Table 1) provide a comprehensive list of euphyllophytes with laticifers and resin ducts (see also Teixeira et al. 2020b). Latex s.l. defends plants partly by its stickiness, but associated chitinases and peptidases may also have negative effects on insects and fungi (Ramos et al. 2019). See also Mahlberg (1993: review), Hagel et al. (2008: laticiferous taxa displayed on a Dahlgrenogram), Pickard (2008: review), Agrawal and Konno (2009: latex), Konno (2011: latex and plant defence) and papers in Adv. Bot. Research 93. 2020 for further information.
Taxa like Rutaceae and Myrtaceae have glands, schizogenous cavities often containing distinctive secondary metabolites (see also below); it has been suggested that there are no truly lysigenous glands in plants, reports of such structures rather referring to artifacts of preparation (Turner et al. 1998; Turner 1999). Cells containing ethereal oils and those with mucilage are similar in their early development, as in basal angiosperms (Bakker 1992), and the main differences between the two is that oil cells often have a suberised layer between cellulose layers in the cell wall and plastids secrete the oil, while mucilage cells lack the suberised layer and mucilage is usually secreted in Golgi vesicles. Gregory and Baas (1989; see also Dickinson 2000) provide a useful survey of mucilage cells. Matthews and Endress (2006b) emphasize the distinctive nature of a type of mucilage cell with thickened inner periclinal wall and distinct cytoplasm, and they catalogue the distributions of this and of other kinds of mucilage cells. Some clusioids, for example, have both gland-type structures and canals in the one plant (see also Fernandes et al. 2018: Salicaceae).
Sclereids (sclerenchymatous idioblasts/stone cells) found free in the cortex, the mesophyll of the lamina, or elsewhere are variable in morphology; several sclereid types have been named. Sclereids are mentioned when they are common in a family (Rao 1991 for a survey), although those occuring only in the pith are rarely mentioned. Sclereids intergrade morphologically with fibres, very elongated and unbranched lignified cells. Cells of the tracheidal transfusion tissue in gymnosperm leaves may sometimes look very sclereidal, as in Sciadopitys (Hu & Yao 1981). Distinctive sclereids of various kinds, including tracheoidal cells, may be associated with vein endings; such sclereids are rarely mentioned below because they are of significance at lower levels. Leaf blades with sclereids may be punctate when a light is shone through the leaf, and even fibrous tissue is often evident, either in such transmitted light or in surface view. Sclereids make up the stone cell defences of Pinaceae, for example, wearing down insect mandibles and perhaps making the plants generally distasteful (Whitehill et al. 2018).
Calcium oxalate may crystallize in various forms - raphides are needle-like crystals that are aggregated in bundles, crystal sand, very small crystals that appear granular under the microscope, single rhomboid crystals that are little longer than broad, and styloid crystals that are narrowly oblong and quadrangular in transverse section, or the crystals are in the form of druses, irregular if more or less radially arranged aggregations of crystals (Horner & Wagner 1995; Raman et al. 2014). Crystals of some sort are rarely entirely absent, and two or more forms of crystal may occur in the one plant, e.g. druses and raphides occur together in some Araceae. Not only does the crystal form of calcium oxalate vary, but also the particular tissues in which the crystals accumulate (see Lawrie et al. 2023), and the combination of the two can be of systematic interest, as in the Apiaceae-Araliaceae area (Rompel 1895; Burtt 1991; Liu et al. 2006). Calcium oxalate crystals are quite commonly found in tissues that are to be discarded - perhaps this is a way of getting rid of excess calcium (Paiva 2019)? The occurrence of druses is rarely mentioned in the characterisations below; they are the common form of calcium oxalate. Many data are taken from Metcalfe and Chalk (1950); Prychid and Rudall (1999, 2000) provide surveys for monocots, Lersten and Horner (2005) discuss styloid morphology and distribution, and Lawrie et al. (2023) provide a recent survey of raphide distribution.
Raphides are a particularly distinctive crystal type. Raphide bundles occur in more or less enlarged cells or raphide sacs, and they can sometimes be seen in herbarium material when using a dissecting microscope if the tissue containing them is cut, the raphide sacs then being evident as small white patches, and they may also be visible on the cut surface of fresh material as it dries out. Individual raphide crystals vary in details of their morphology, e.g. shape in transverse section (Horner & Wagner 1995), and Raman et al. (2014) described a couple more raphide types in addition to the four described by Horner and Wagner (1995), however, the interrelationships between these types are unclear (Lawrie et al. 2023). Raphide morphology depends in part on whether whewellite (calcium oxalate monohydrate - CaC2O4-1H2O) or weddellite (calcium oxalate dihydrate - CaC2O4-2H2O) are involved; the latter is the less common form (Monje & Baran 2002), although I do not know what the general distributions of these forms are (but see Cactaceae). Hartl et al. (2007) suggest that more attention be paid to this variation when discussing crystal morphology. Individual raphides may be sheathed, e.g. the lamellated sheath found in the hexangular (in transverse section) raphides of Agave (Wattendorff 1976) or the membrane around individual raphides in Dioscorea (Raman et al. 2015). Raphides are practically unknown outside angiosperms, where they are especially common in monocots, they are not known from the ANA grade, while Piperaceae are the only magnoliid in which they are common; they are generally commonest in leaves (and just about restricted to leaves in Piperaceae), although they are also common in the stems of eudicots (Lawrie et al. 2023).
Some taxa show little or no accumulation of oxalate in any form (Hodgkinson 1977; Zindler-Frank 1976), conversely, in Cactaceae calcium oxalate can represent the bulk of the plant body. A few taxa produce soluble, rather than crystalline, oxalate, whether as potassium oxalate or oxalic acid itself, hence the pleasingly sharp taste of some Polygonaceae and Oxalidaceae. Vacuolar crystal formation associated with membranes and also paracrystalline bodies with widely spaced subunits occur in eudicots, while in monocots there are no membrane complexes and the paracrystalline bodies have closely spaced subunits (Horner & Wagner 1995; Evert 2006).
Little is known about why oxalate accumulates, or accumulates in one form rather than another (see Franceschi & Horner 1980; Lawrie et al. 2023 for reviews). Raphides have been implicated in the protection of the plant against herbivores (see Araceae, Onagraceae, etc.), and there may be connections between oxalate metabolism, the type of carbon fixation, the aquatic habit, etc.. Franceschi and Nakata (2005) suggested that oxalate formation is connected with calcium regulation, plant protection and metal detoxification, while Tooulakou et al. (2016) thought that the crystals were broken down during the day when the plant was stressed, reforming at night, so providing a sort of reserve of CO2 for the plant. Karabourniotis et al. (2020) also suggest that calcium oxalate (and calcium carbonate) is a source for water and CO2 when conditions are dry; the different forms of oxalate mentioned above will of course provide different amounts of water for the plant.
The walls of cells containing crystals may be distinctively thickened, e.g., the walls of styloid-containing cells are suberized (Wattendorff 1986 for references). Cristarque cells are distinctive cells with U-shaped lignification and with calcium oxalate crystals or druses in the centre part, and they are often found in the cortex, whether of the stem or the petiole. They are mentioned only in those taxa from which they have been reported.
Currie and Perry (2007) provide an introduction to the biochemistry of silica, SiO2 (see also Trembath-Reichert et al. 2015; de Tombeur et al. 2022). Crystalline silica is found either in the wood of families like Chrysobalanaceae, or in the leaf, as in many Poales. It may be present as sand, or as larger, more organized bodies of distinctive shapes. Silica bodies or other siliceous parts of plants - phytoliths - are commonly preserved in the fossil record (see Piperno 2006 for a good summary; Katz 2015 for the evolution of phytoliths - quite widespread; Strömberg et al. 2016 and S. N. Johnson et al. 2021: function); phytoliths are especially important in archaeology. Presence or absence of these phytoliths/silica bodies, where they are deposited in the plant, and their morphology provide especially valuable characters in the monocots (see Prychid et al. 2003b for a summary; International Committee for Phytolith Nomenclature 2019 for phytolith morphotypes). Silica can wear down the mouthparts of some animals that feed on plants containing it, and it can also have negative physiological effects (see Massey & Hartley 2006, 2009; Massey et al. 2007a, b; Katz et al. 2014; Strömberg et al. 2016). Silica may provide structural support in some plants (Strömberg et al. 2016 and references). Ma and Takahashi (2002) and Hodson et al. (2005) summarize the literature on silicon concentrations in plants and Cooke and Leishman (2011a) summarise its physiological importance; Westbrook et al. (2009) looked at the SiO2 concentration in the leaves of a number of Neotropical taxa. Although most broad-leaved angiosperms and non-commelinid monocots have low concentrations of silicon while commelinids have high concentrations, some commelinids, including members of Commelinales and Juncaceae sampled (but see conflicting information in Hodson et al. 2005), have low concentrations, but these groups also lack SiO2 bodies.
Pierantoni et al. (2017) noted that large calcium oxalate druses in the palisade mesophyll and epidermal silica deposits together may enhance photosynthesis in okra, Hibiscus esculentus, the former scattering incoming light into the spongy mesophyll and the latter reducing UV radiation damage - interestingly, in surface view, their distribution in the lamina is mutually exclusive.
Calcium carbonate, either crystalline or amorphous, may be deposited in cell walls or as concretions of one sort or another. Cystoliths are moderately common and their morphology and distribution is quite often of systematic interest. They may be concretions of amorphous calcium carbonate (as in the Ulmaceae-Moraceae group of families) sometimes developing on an intrusion of the cell wall, and their axis, and also stalk, if present, may be made up of silica (Pierantoni et al. 2018); the cells containing cystoliths are known as lithocysts. However, calcium oxalate is the common biomineral found in vascular plants (Karabourniotis et al. 2020, q.v. for suggested functions of such carbon-calcium inclusions - carbon dioxide and water produced on their breakdown, important under drought conditions). Cystoliths can sometimes be seen in the leaf blade when it is held up to the light, as in Acanthaceae and Urticaceae; they can also be visualized in spodograms, basically what remains after the leaf is calcined (e.g. Bigalke 1933). For possible functions of cystoliths, see Pierantoni et al. (2018 and references) and for a comprehensive survey of calcification in plants, see Arnott and Pautard (1970). Plants that can tolerate soils with much gypsum, hydrous calcium sulphate or CaSO4-2H2O, may have gypsum crystals in the leaf, especially those species that are regionally rather than narrowly distributed gypsophiles/gypsum endemics, and S may be sequestered in organic compounds, while some gypsophiles also accumulate much calcium oxalate (Palacio et al. 2014; Escudero et al. 2014; Moore et al. 2016; C. T. Muller et al. 2017). For a survey of cystoliths is dicots, see Fernández Honaine et al. (2023). Interestingly, many of the groups that include gypsophiles like Brassicales, Caryophyllales and Lamiaceae seem to lack mycorrhizal associations; Cistaceae are perhaps an exception (Escudero et al. 2014).
Petiole anatomy has been recorded rather sporadically. Radford et al. (1974) describe and name some of the main variants, although other sets of terms for describing petiole vasculature have also been proposed (e.g. Watari 1939; see also Howard 1979b). Col (1904) is a source for information in several groups. Families like Clusiaceae show great variation in this feature, and it is usually of systematic significance at levels lower than those emphasized here. However, Kim et al. (2003) have recently drawn attention to variation in how much adaxial surface is evident in petioles; when there is none the petiole bundles form a circle, or there is a single annular bundle, in both cases without any adaxial bundles, also the ± lateral "wing bundles" of the descriptions. The petiolar vasculature of taxa that have a clear adaxial petiolar surface is variable. Vascular bundles in the petioles of monocots are usually scattered, although sometimes they form a ring; only the latter feature is recorded.
Epidermis. There is much variation in features associated with the epidermis, even if there has been a tendency to be typological when describing their variation.
Epidermal cells may contain silica bodies (see above) or their walls may be lignified. In many monocots, but not, apparently, in Helobiae - members of Alismatales here (Löv 1926; Metcalfe 1960) - there are bulliform cells, large, thin-walled cells often of the adaxial epidermis, that help cause curling and uncurling of the leaf blade as its turgor changes; subepidermal cells may be involved as well or alone (Löv 1926; Linsbauer 1930). Of course, many Alismatales are more or less aquatic, and in submerged aquatics, whether freshwater or marine, stomata are absent and chloroplasts are more or less concentrated in the epidermal cells and the thickness of the leaf is correspondingly reduced, although less so in marine aquatics (Larkum et al. 2006b). Epidermal cell shape is usually of little interest at the genus level and above. Epidermal cells of plants growing in shady conditions may form a minutely bullate, almost velvety, surface, and along with distinctive colour patternings this contributes to the horticultural popularity of such plants. The blue iridescence of some of these plants is associated with the rearrangement of the chloroplast thylakoids to capture more light and enhance photosynthesis (Jacobs et al. 2016). Families like Begoniaceae and Marantaceae are noted for the numbers of their species with such leaves that grow in the shade.
Stomatal morphology. The stomatal types mentioned in the characterizations are largely those delimited by Van Cotthem (1970a) and slightly modified by Baranova (1983, see also Baranova 1987; Wilkinson 1979). However, there is much disagreement in the literature over stomatal morphology, even that of smaller families, and this is partly because there is considerable variation in this set of features, sometimes even in the one individual, and partly because of the terminology, which can be baroque. Thus stomatal "type" is variable, even within a leaf (Nisa et al. 2019: 10 stomatal types, 36 subtypes in Vincetoxicum arnottianum alone), and as Payne (1970) observed when introducing his helicocytic and allocytic stomatal types, what may seem to be a distinct type to one person can be considered a mere modification of an existing type to another. Further confusing the issue is the tendency for each author to use a different set of terms or to interpret a particular configuration of cells in a different way (Prabhakar 2004 is a recent effort to develop a synonymy). Carpenter (2005) introduced nine new types in an exhaustive study of stomatal variation in plants of the ANITA grade, although the forty four types recognized by Patel in 1979, but largely ignored since, is probably the record. Paliwal (1969) introduced Sanskrit terms like "chatushsahkoshik" (= tetraperigenous), but alack, without success. Baranova (1987) is a useful guide through the nomenclatural chaos, and she, too, noted "The distinctions among these types, although conceptually useful [although that is debatable], are often difficult to draw. We should not let the necessity to categorize the diversity among stomatotypes obscure the fact that variation is continuous." (ibid.: p. 64). Members of the ANITA grade, and also of a number of fossil groups, show considerable intra-individual variation in stomatal morphology (e.g. Upchurch 1984), and as more people look, more variation is being found (Mandal et al. 2014). Illustrations in Conover (1991) are useful for ascertaining stomatal morphology of some monocot groups. Inclusions in the guard cells may be of systematic interest (see Tiemann 1988). Pautov et al. (2020, 2022) discuss the variety of annular structures surrounding stomata and suggests functions they might have, while for Florin Rings in the stomata of some gymnosperms, see Oladele (1983). However, overall the literature is huge and discouraging, and I have looked at rather little of it.
Even aside from problems in the recognition of distinct stomatal types in adult leaves, there is the issue of relating the morphology of mature stomata to their development. Thus Stebbins and Khush (1961) provided an early stomatal survey for monocots, but Tomlinson (1974a; see also Rudall 2000) qualified their account, emphasizing the importance of understanding stomatal development (for the evolution of stomatal developm ent, see also Chater et al. 2017). In general, stomatal morphology may not be a very accurate guide to stomatal development (Paliwal & Bhandari 1962; Tomlinson 1970; Willmer & Fricker 1996; Rudall et al. 2013a; etc.); see also immediately below. Payne (1979) surveyed stomatal ontogeny across embryophytes from a developmental point of view (e.g. see also Fryns-Claessens & van Cotthem 1973; Rudall et al. 2013a). Interestingly, some of the patterns of cell division emphasized in work on stomatal development occur in the development of other epidermal structures (Rudall & Knowles 2013). A distinction has been made between mesogenous/syndetocheilic and perigenous/haplocheilic stomata, in the former the subsidiary cells are produced from the same cell (meristemoid, initial) that gives rise to the guard cell initials, in the latter, they are not, developing from different cell lineages. However, there can be variation within an individual in this (Taylor et al. 2009; Rudall et al. 2012), for instance, Paliwal and Bhandari (1962) found that stomata on the flowers of Magnolia were haplocheilic while those on the leaves were syndetocheilic. Indeed, the two sets of terms are not exact synonyms, and the syndetocheilic/haplocheilic pair may be best abandoned (e.g. Rudall et al. 2013a and references) and the mesogenous/perigenous pair need to be redefined (see Payne 1979 for some apposite comments; Rasmussen 1987 for extensive variation in Orchidaceae). Fryns-Claessens and van Cotthem (1973) provide a classification of ontogeny-based stomatal types, and Pole (2010) attempted to integrate the morphology of the adult stomata with their development, at least in part, in his study of the epidermis of Australian Sapindaceae. Rudall (2023a, see also Rudall et al. 2017a) noted that paracytic stomata in grasses, indeed, in monocots as a whole, developed differently from those in magnoliids, for example - the former are perigenous, the latter mesogenous (see also Gray et al. 2020 for stomatal development). Peterson et al. (2010) looked at stomatal development from a molecular point of view.
Aside from all this variation in morphology and development, how might this connect with stomatal function? The answer is that very little is known. The dumbbell-shaped paracytic stomata of grasses in particular seem to be able to open and close very quickly, and there have been suggestions as to how the anisocytic stomata of Crassulaceae might function, but little more (see Gray et al. 2020; Cheng & Raissig 2023 for references). About 150 years ago (Wilhelm 1883; Wulff 1898) it was found that stomata were quite often blocked by wax deposits; this was particularly notable in Pinaceae, quite common in Poaceae, but also scattered throughout seed plants - but not in succulents. In some cases, e.g. Papaver, stem stomata were blocked, foliar stomata not so (Wulff 1898). Jeffree et al. (1971), looking at Picea sitchensis, found that such deposits reduced transpiration by about two thirds, but photosynthesis by only one third. In Carex papillae on walls of cells around the stomatal stomium may perhaps have the same function.
Stomatal orientation also varies. In monocots with parallel leaf venation (see below), stomata are usually oriented with the long axes of their apertures parallel to that of the blade (it is perhaps more accurate to say that it is parallel to the venation), however, in those monocots with reticulate venation orientation is often random (Conover 1983). Elsewhere, random orientation is common, as is reticulate venation, although there are exceptions. Butterfass (1987) summarised information on taxa that have tranversely-oriented stomata, whether on the stem or leaf; transverse orientation is more frequent in succulent taxa and is notably common in Caryophyllales (see also Rudall & Bateman 2019: esp. Bennettitales; Rudall 2023b: Fig. 5). As to stomatal distribution, stomata are usually found on the abaxial side of the blade, but in plants growing in the full sun and with rapidly-fluctuating water conditions, and early successional or marshy conditions, hence often in plants with CAM or C4 photosynthesis, they occur on both surfaces (amphistomatic); there is quite often infraspecific variation in this feature (Metcalfe & Chalk 1950; Mott et al. 1982 for a survey). Croxdale (2000) discussed foliar stomatal patterning. Much has been said about isobifacial and unifacial leaves in monocots in particular (see below).
The patterning of cells around hair bases, epidermal oil cells, etc., can be described using the same set of terms as are used for stomata, even if the idea that all these structures are "homologous" seems unlikely (c.f. Carpenter 2006). Stomatal orientation immediately around hair bases can be very distinctive (e.g. Rudall 2023b).
Cuticle waxes. Here most data on the morphology of foliar (epi-)cuticular waxes are taken from Barthlott and his coworkers (e.g. Fehrenbach & Barthlott 1988; Ditsch & Barthlott 1994, 1997; Barthlott et al. 2003). For cuticle waxes in general, their morphology and composition, function, etc., see Wilhelmi and Barthlott (1977), Jenks and Ashworth (1999), Sharma et al. 2018; Watts and Karrigat (2022 and references, esp. function), papers in Riederer and Müller (2006), also the Cuticle Database Project (Barclay et al. 2012) for numerous images. Barthlott et al. (1998) standardized the terms used in describing wax crystals, and noted that unoriented platelets, often with more or less irregular margins, are common; indeed, their distribution at and above the familial level seems of little systematic significance, although there is some correlation with higher taxa in monocots, gymnosperms, etc. (e.g. Barthlott & Fröhlich 1983; Jeffree 2006), but even there the distinctive types are often disconcertingly sporadic in their occurrence. Thus although Fehrenbach and Barthlott (1988) included Dichroa (here Hydrangeaceae-Cornales), Francoa (Francoaceae-Geraniales), Vahlia (Vahliaceae-Vahliales), as well as Penthorum (Penthoraceae) and Saxifragaceae s. str. in their Saxifragaceae in a survey of cuticle waxes, no significant differences between these species which are in phylogenetically quite unrelated groups were noted. Leaf waxes on the one plant may differ considerably depending on the part of the plant (e.g. leaf blade, stem) and its age, and aside fom this there is infraspecific variation, etc. (e.g. Jenks & Ashworth 1999). Here I focus on waxes on the leaf blade and I usually mention only forms other than unoriented platelets with more or less irregular margins and sometimes also the chemical composition of these waxes (for which, see Meusel et al. 1994, 1999; Barthlott et al. 2003; Jetter et al. 2006). Amyrins, triterpene-type compounds, are found in the epicuticular waxes of a number of families, and in Asteraceae, Apocynaceae and Boraginaceae they are used by chrysomelid leaf beetles as defence compounds (Termonia et al. 2002), and alkanes and secondary alcohols like nonacosan-10-ol are other important components (e.g. Jetter et al. 2006; Diefendorf et al. 2011; Bush ∧ McInerney 2013). The stomata in a number of taxa are more or less blocked by epicuticular waxes, and this seems to reduce transpiration more than photosynthesis; such blocked/plugged stomata are not a feature of plants growing in dry conditions (Wulff 1898).
Wax crystals, cuticular folds (Barthlott & Ehler 1977) and trichomes (Barthlott et al. 2003) rarely occur together on the one plant, with wax crystals predominating in basal angiosperms (but they seem to provide little information of systematic interest in the ANITA grade) and monocots, while a well-developed indumentum - and conversely poorly-developed wax crystals - predominate for example in Lamiales, Solanales, and Asterales (Pierce et al. 2001 for Bromeliaceae; Agrawal et al. 2009c for the trade-off; Watts & Karigat 2022). There can be a change from wax-no hairs to no wax-hairs within the ontogeny of an individual plant (e.g. maize - Takacs et al. 2012).
In a few taxa, the epidermis is notably persistent (Damm 1901 for an early summary). The cuticle becomes progressively thicker, epidermal cells may die and get incorporated into this cuticular layer (it may be close to 600 μm across - Damm 1901), and in the Santalaceae-Visceae it at it were repaces the cork, which does not develop (Damm 1901; Wilson & Calvin 2003).
Hair type. Only particularly distinctive hair types are mentioned, and these rarely suggest relationships between families, although they are quite useful at rather lower levels. Hair types have the same problems as stomatal morphology, etc.: "Because of the intergradations between trichome types, and also in consequence of the use of imprecise and varied morphological and histological terms, it is often difficult, from the voluminous published descriptions that exist, to determine exactly what type of trichome is being discussed, unless there is an illustration." (Theobald et al. 1979: p. 41) - not to mention the ambiguity of terms like "pubescence". "Indumentum" covers everything here! For terminology, see Payne (1978), Hewson (1988), Stearn (1992), etc., for function, see Bar and Shtein (2019) and below.
Stinging hairs, which protect the plant against mammalian herbivores, occur in a few families, and they are quite similar in gross morphology, including having a slightly swollen tip that is easily broken off, but they differ quite substantially in the mineralization of their walls (Mustafa et al. 2018b). Pearl bodies, small multicellular hairs, function as food bodies and are eaten by ants (O'Dowd 1982) and are found in e.g. Indigofera (Fabaceae-Faboideae) and Vitaceae. Other kinds of glandular hairs trap insects, and other insects such as mirid bugs and spiders eat these insects, and also may protect the plant from herbivores (Romero et al. 2008; Glas et al. 2012; LoPresti et al. 2015; Wheeler & Krimmel 2015). In Roridula (Roridulaceae) nutrients from the excreta of mirid bugs, which suck haemolymph, etc., from insects stuck to the plant, are taken up by the plant, which thereby are indirectly carnivorous; overall, the line between carnivory and non-carnivory is not sharp (Spomer 1999), and similar systems continue to be found. Thus Triantha occidentalis (Tofieldiaceae) also acquires nutrients from insects stuck to the plant, but here plant-secreted enzymes may be involved (Q. Lin et al. 2021). In other cases dust may stick to glandular hairs, and such dusty hairs are not liked by herbivores - and if eaten by caterpillars, for instance, their growth is reduced (Lopresti et al. 2017: Nyctaginaceae). Hooked hairs may also capture leaf hoppers, etc., as in Phaseolus vulgaris (Rebora et al. 2020 and references). Tozin et al. (2016) suggested that the apparently ordinary small uniseriate/unicellular hairs of some Verbenaceae and Lamiaceae they examined in fact produced biologically active compounds, while the products of glandular hairs in tomatoes may be involved in plant communication and defence, and the diversity of bacteria in the phyllosphere is notably greater in plants with such hairs than those without (Kusstatscher et al. 2020).
Colleters are multicellular, more or less glandular but often unvascularised structures secreting resin, mucilage, or similar material, and sometimes lipids, proteins, etc. (Ribeiro et al. 2017). They are often found in the axils of petioles and stipules, sometimes covering the inner surfaces of the latter (e.g. Tresmondi et al. 2015), and quite often the calyx, too. Indeed, colleters may be found in other than the axillary position, as in several Apocynaceae, Rubiaceae, Rosaceae, and Caricaceae - on the leaf surface or margin, for instance, and some kinds of deciduous leaf teeth are simply colleters in an unusual position (Fernandes et al. 2016 and references; see below), and there is discussion about stipules and colleters in Ye and Ronse De Craene (2024) - the two may not be as distinct as one might think... The secretion that colleters produce may be involved in the lubrication of the tightly-pressed young parts of the plant as they slide over one another as the bud expands, or protecting those parts from dessication, it may be bacterio- or fungistatic, or it may gum up herbivores (Klein et al. 2004; Judkevich et al. 2017; Ribeiro et al. 2017; Rios et al. 2020); Judkevich et al. (2017) discussed the variety of colleters, some chlorophyllous, others notably long-lived, vascularized or not, etc., in Spermacoce (Rubiaceae) and relatives. There seems to be a correlation between habitat and nature of the secretion in colleters of similar morphology in Brazilian Rubiaceae (Tresmondi et al. 2015, 2017). The "intravaginal squamules" of monocots are included here, the only difference between them and colleters seems to be that the squamules are flattened and are found in monocots (Doyle & Endress 2000). A useful survey of colleters is provided by V. Thomas (1991), but they are very much under-recorded - especially if colleteriform leaf teeth are to be included. Lersten (1974) described the distinctive colleters found in some species of Psychotria that are perhaps involved in the bacterial leaf nodules there. However, the very definition of a colleter is becoming unclear. Thus Cardoso-Gustavson et al. (2014) described the mucilage-secreting bicellular hairs found on floral parts - often the outer floral parts - in some Epidendroideae as colleters, and also suggested connections with the extra-floral nectaries on the inflorescence of some genera of that subfamily. Palisade glandular tissues with protein-rich secretions are found on the stipules of Brazilian species of Ilex (Aquifoliaceae), and the latter have been called colleters ipso facto (A. M. González & Tarragó 2009), and the uniseriate glandular hairs on the fronds of some Thelypteridaceae have also been called colleters for functional reasons - again, they are doing what colleters do (Oliveira et al. 2017).
Understanding basic plant morphology is not simple, indeed, the vegetative body in particular of plants like Podostemaceae and Utricularia (Lentibulariaceae) is difficult to understand using the conventional distinctions between stem, root, and leaf (e.g. Rutishauser 2005 and references). Still extremely useful are general studies such as those of Arber (1925) for monocots and Arber (1920) and Sculthorpe (1967) for aquatic plants, while Goebel (1931, 1932) and especially Troll (1935-1971) remain without equal; Bell and Bryan (1991, 2008) provide an attractive short but comprehensive survey of plant morphology while Cronk (2009) reviews plant morphology in the context of gene expression and control. The importance of floral morphology for systematics has been much emphasized in the past, yet vegetative characters are mentioned below where possible, especially in the thumb-nail sketches of families - here Hallé, Oldeman and Tomlinson (1978), Keller (1994, 1996, 2004), van Balgooy (1997, 1998, 2001) and Schatz (2001) have been valuable sources of information. Vegetative characters are often most useful in a more local context, identifying members of the local flora; for identification using vegetative characters, see e.g. Keller (1996), van Balgooy (1997, 1998, 2001), Schatz (2001), Rejmánek and Brewer (2001), Spichiger et al. (2005), and others.
The Vegetative Body.
For definitions, etc., see the Glossary.
More or less distinct and organized (i.e. with leaf primordia evident) axillary buds are found in the axils of most or all leaves in nearly all angiosperms, but in gymnosperms their distribution is much more erratic (e.g. Namboodiri & Beck 1968a; Fink 1984). However, in some conifers in which most leaves appear to lack axillary buds there are persistently meristematic but not otherwise morphologically recognizable areas in the leaf axils that will produce organized axillary shoots on damage of the apex of the shoot, etc. (Namboodiri & Beck 1968a; Fink 1984; Burrows 1999). Organized axillary buds are absent in cycads, and they are in general rare outside seed plants (Stevenson 2010). In broad-leaved angiosperms axillary buds are associated with the adaxial base of the subtending leaf, although in Poaceae, at least, they are more associated with the cauline side of the base (McConnell & Barton 1998 and references). There may be more than one axillary bud (= supernumerary axillary buds), and the number of such axillary buds, and their arrangement (collateral, superposed) may be of interest. The development of the prophyll(s) of axillary buds may be precocious, as in some species of Aristolochia and Bignoniaceae-Bignonieae; they can then be confused with stipules (see also Ye & Ronse De Craene 2024). Axillary buds sometimes develop and form plantlets, and these may fall from the plant in a form of vegetative/asexual reproduction. Zona and Howard (2021) describe the variety of similar axillary structures, loosely called bulbils, in angiosperms; these seem to be relatively common in monocots. In some Myrtaceae, especially Eucalyptus, there are epicormic strands that enable regeneration after fire (Burrows 2002; Meier et al. (2012) review epicormic buds, while preventitious buds, buds that developed from the apical meristem, i.e. axillary buds (c.f. adventitious buds), but that are dormant, are to be found in some trees (Fink 1983).
Vegetative buds can be perulate (scaly) or "naked", that is, lacking morphologically modified leaves enclosing the apex; see Henry (1846) and Lubbock (1899) for classic accounts of variation in bud morphology, etc.; Schoonderwoerd and Friedman (2021) discuss the perhaps surprisingly common occurrence of naked buds in temperate plants. For the basic morphology of bud scales, see Foster (1928). Information on this character is only sometimes mentioned. Lamina vernation (see below) is best observed at the bud stage or when the leaves are beginning to unfold.
Branching. Branching is not always simply axillary (Fisher 1978), and in some cases, e.g. Solanaceae-Solanoideae, it can be difficult to understand how the plant is put together, the branches often appearing not to be associated with a leaf (see e.g. Zhang et al. 2022). A number of aquatic Alismatales show vegetative bifurcation of the vegetative axes, perhaps precocious axillary branching, but strictly dichotomous branching is very rare in seed plants, occuring only in Hyphaene (Arecaceae), Strelitzia (Strelitziaceae), and a few other taxa, mostly (?all) monocots (e.g. Wilder 1975; Fisher 1976; Tillich 1998), indeed, dichotomous branching comes in a variety of flavours, in which simple division of an apical cell directly producing two, equal branches is perhaps the least common mechanism in embryophytes (Gola 2014 for references). Particularly robust and quickly-developing axillary shoots may displace the the terminal bud/inflorescence/shoot, the result being that the erstwhile terminal structures appear to arise opposite the leaves and the axillary shoot appears to be terminal; the terminal bud/inflorescence/shoot is described as having been evicted.
Keller (1996, see also 1994) distinguished between immediate branching, with branches coming from the current flush, and delayed branching, with branches developed on the previous flush. This is close to the distinction between prolepsis and syllepsis, whether branches develop from the shoot with (prolepsis) or without (syllepsis) evident rest; Wheat (1980) discussed syllepsis in Myrsine. Shoots developing from naked buds in the axils of the last pair of leaves of the previous flush (e.g. Clusia, Garcinia) present problems for such distinctions, since they may grow out simultaneously with the elongation of the main axis, but after a period of rest, and lack basal scales. Branching in vines and annuals may also depart from any family norm, furthermore, branching behavior on sucker shoots or young plants may differ from that elsewhere on the plant, especially the canopy. Immediate/sylleptic branching is relatively rare in temperate taxa, but may occur in the local representatives of otherwise largely tropical families that commonly have such branching (e.g. Lauraceae). Although this character is mentioned quite frequently in the characterisations, comparative knowledge of it is poor. The relative development of the branches along a season's growth has been modelled (e.g. Lück et al. 1990), and for modelling branching, bud break and the like, see Evers et al. (2011).
Stems, including inflorescence axes, also roots and leaves, may have spiny structures of various kinds. These include spines s. str. (leaves, or parts of leaves: vascularized), thorns (stems or roots: vascularized) and prickles (often on the stem, sometimes elsewhere: unvascularized enations, made up of epidermis + cortex) for protection (Bell & Bryan 2008). Lefebvre et al. (2022) outline the various forms of protection afforded by such structures. (Note that although I have tried to use these terms correctly, when talking about pollen and seed surfaces, etc., the spiky structures are called "spines".) Prickles may sometimes seem insubstantial and inconsequential, however, Satterlee et al. (2024) recently described a remarkable case of convergent evolution here. The common ancestor of the taxa with prickles in angiosperms that they studied is about 150 Ma, and prickles are to be found in taxa as diverse as grasses, Rosaceae, sundry Solanum and relatives, etc.; prickles have evolved at least 26 times in angiosperms alone (and they have also frequently been lost). (Note that in some taxa, e.g. Tareneya hassleriana (Cleomaceae) and Zizyphus jujube (Rhamnaceae), the prickles may be paired and nodal, but they lack the vascularization of stipular spines.) Prickles vary from one to thousands of cells in size, but they share a common developmental element that evolved independently: They have members of the LONELY GUY (LOG)-family cytokinin biosynthetic pathway which catalyze the last step in the biosynthesis of cytokinin, a hormone involved in general plant cell proliferation and differentiation. Taxa, e.g. in the speciose "spiny" (= prickly) Solanum group that lack prickles, have a mutation, pl (= prickle loss), in this gene (Satterlee et al. 2024). Cytokinins of course greatly influence just about all aspects of plant development (Argueso & Kieber 2024).
Many plants are climbers, being vines (more herbaceous) or lianas (woodier). Here more grapnel-like structures - again, morphology is various, and see Sperotto et al. (2020) for terms to be used - may be involved in climbing in groups like Arecaceae-Calamoideae, Ancistrocladus (Ancistrocladaceae), Uncaria (Rubiaceae), and Artabotrys (Annonaceae). Tendrils, modified branches or leaves, are also common in climbers (see Sousa-Baena et al. 2018a, 2018b for a comprehensive survey - 17 types!), but of the 10 most speciose Neotropical clades of climbers, Dioscorea, Ipomoea, Calamus, Mikania, Rhynchosia, Combretum, Jasminum, Passiflora, Cissus and Smilax, only the last three have tendrils; Passiflora, at ca 420 species, is the most speciose Neotropical climbing genus (Sperotto et al. 2023). For how tendrils coil, which involves gelatinous fibres in twining stems and reaction wood, but not in the roots of root-climbers, see Bowling and Vaughn (2009). The spiral in tendrils functions by dissipating energy, sharing tension between adjacent tendrils (references in Yang & Deng 2016); the spirals at the two ends of the tendril are often opposing, and they reverse at what is called a perversion (e.g. Goriely & Tabor 1998; Gerbode et al. 2012) so there is minimal twisting between climber and support (c.f. also spiral thickenings on the walls of root hairs); for twining in tendrils, see also P. E. S. Silva et al. (2019). Stems themselves may also twine, and Burnham et al. (2019) provide a preliminary comparison of the chirality of climbers in three American forests; most climbers there were dextrorse. Recent work suggests climbers in Vitaceae may avoid the use of conspecifics as supports by sensing oxalate (Fukano 2017), while there may be mimicry of the leaves of the support in Lardizabalaceae-Boquila (Gianoli & Carrasco-Urra 2014). Plants with axillary branch tendrils (and thorns) often have supernumerary axillary buds, the original axillary bud having formed a tendril/thorn is then unavailable to function as a reserve meristem (see also Hernandes-Lopes et al. 2019: Passiflora). Climbing in other taxa like Hedera helix is by stem roots, and in shingle-leaf climbers modified short and usually relatively broad leaves are closely adpressed against the stem of the host, the climber being attached to the host by roots (Zona 2020). Although various functions have been proposed for such shingle leaves little definite is known, although in some cases they form domatia for associated ants (Zona 2020). climbing mechanisms do not significantly influence the distribution of neotropical climbers. Sperotto et al. (2023) found no strong support for correlations between climbing types and geography nor between higher diversification and particular climbing mechanisms in their survey of New World climbers.
Stems may also become flattened and leaf like, i.e. they are cladodes (e.g. Kaplan 1970b, 1980, 1997, vol. 1: chap. 11), while compound leaves in particular can become phyllodinous, i.e., they appear to have a simple blade. This blade may be equivalent to the petiole or petiole + rhachis. Thus there has been much discussion whether "leaves" of Asparagus really are foliar or not; Nakayama et al. (2010, 2012) discuss gene expression in such structures.
Variation of internode length is usually not of interest at higher levels, but taxa with short shoots (brachyblasts) in which internodes do not develop are conspicuous - Pinus and some other conifers, Cercidiphyllum, Ginkgo and Euptelea are well-known examples. Dörken (2012) suggested that in angiosperms deciduousness was correlated with shoot differentiation, intermediates being quite common, but few deciduous species had dimorphic shoots; most evergreen species did not have shoot differentiation. In gymnosperms, Pinaceae and Ginkgoaceae ahowed shoot differentiation, and intermediates were rare; Dörken (2012: p. 81) suggested that the shoot differentiation in genera like Pinus and Sciadopitys reflected "reminiscence of a deciduous ancestor".
Leaves. There are several classical accounts of leaf morphology and development that remain of interest; these include Goebel (1880), Troll (1937-1943) and Hagemann (1970); for a more recent summary, see Kaplan (2001a). For suggestions about the possible adaptive value of leaf shape, see Givnish (1979). There has been a recent flurry of interest in aspects of leaf morphology, especially in leaf teeth and aestivation, that are correlated with latitude (E. J. Edwards et al. 2016, 2017; Givnish & Kriebel 2017); see also Nakayama et al. (2022) for leaf development, diversity, etc..
There may be leaves - or more generally metamers or construction units - with quite sharply different morphologies and functions on the one plant. The phenomenon known as heteroblasty refers to leaf morphologies that differ depending on the developmental stage of the plant; such leaves may have quite different forms (bud scales/perulae, expanded leaves), internodes may be elongated or not, etc. (Zotz et al. 2011 for a review). Heterophylly, often environment-induced changes in leaf form of plants, phenotypic plasticity in leaf development, is particularly striking in many emergent aquatic plants (Zotz et al. 2011). However, the distinction between the two is not always clear. Anisophylly refers to the situation where one leaf of a pair (for example) differs from the other, in some cases being vestigial. See also Foster (1928), Pabón-Mora and González (2012), etc..
Leaf type. The main distinction in gross leaf morphology is between simple and compound leaves (see Doyle 2007 for this variation in the context of a phylogeny). In truly compound leaves the leaflets arise from separate primordia along the leaf, the activity of the blastozone having become restricted to those areas that produce the leaflets (see Gunawardena & Dengler 2006, Rosin & Kraemer 2009, and Blein et al. 2010 for useful reviews). Development of the leaflets in Ailanthus, etc., is acropetal, in Polemonium, etc., it is basipetal and although the leaflets appear to be transversely inserted, that simply reflects their development via this restricted blastozone (Hagemann & Gleissberg 1996).The adaxial area of the portion of the leaf with leaflets is continuous with the adaxial part of the petiole, and the whole leaf is bifacial (e.g. Kim et al. 2003). Most families of any size that have compound leaves also have some members with apparently simple leaves (derived); there, however, the blade is sometimes joined to the petiole by an articulation, as in Citrus, and such leaves are really unifoliolate, not simple. This variation is common and is rarely mentioned below. Bharathan et al. (2002), Geeta et al. (2011) and Nakayama et al. (2022) discuss the evolution of simple from compound leaves, and cases like Coffea, in Rubiaceae, a family which many would think always have simple leaves, nevertheless has a cryptic compound developmental program (KNOX1 is reactivated) early in their development clearly deserve further investigation.
However, the distinction simple/compound may not be so clear-cut when the phenomenon is observed at the level of gene expression, indeed, for over 150 years (Hofmeister 1868) it has been suggested that the distinction is not fundamentally important, and that the distinction between leaf and branch was not always simple (Kaplan 2001b and references). Thus Bharanthan et al. (2002) found that in many leaves dissection - both that resulting in simple lobing, and in fully compound leaves - was associated with expression of the KNOXI (Class 1 KNOTTED1-like) gene. Normally it was expressed in the stem apex, but not in leaves as they were initiated, however, KNOXI was normally expressed during the development of compound leaves, even in secondarily unifoliolate ones (Bharathan et al. 2002; Champagne et al. 2007; Uchida et al. 2010); exceptions to this may be of phylogenetic interest (see Fabaceae). Some simple leaves may show KNOXI expression early, but any lobing that develops is subsequently obliterated by inner blade growth. The result is that all simple leaves are not developmentally identical. Other aspects of leaflet development are similar across a broad array of angiosperms. An example is the genes that promote first the formation of boundaries between leaflets in the developing leaf, i.e., the leaflets separate, and later the formation of leaflets (Blein et al. 2008). The same genes are also implicated in the development of serrations on the leaf or leaflet margin and also the demarcation of the whole leaf at the stem apex (Blein et al. 2008) and similar patterns are seen with genes involved in ligule formation in grasses (Zhu et al. 2013; Johnston et al. 2014). Efroni et al. (2010) analyze leaf development in terms of several distinct ontogenetic programmes, while Runions and Tsiantis (2017) and Runions et al. (2017) look at the development of leaf form in the context of a common developmental programme in which the vascular system and antagonisms between promotors and repressors on the leaf margin played important roles - interestingly, Hofmeister's ideas of a century and a half before and those of Zimmermann over 60 years ago were compatible with their computational model.
A number of taxa with pinnate leaves also have palmate leaves, and commonly here the adaxial surface of the distal portion of the leaf has become much restricted so a rachis does not develop. In both these non-peltately palmate and in pinnate leaves the petiole bundle is more or less obviously dorsiventral, the adaxial surface being evident. Examples of non-peltately palmate leaves include Dioscorea pentaphylla, Lupinus albifrons, Vitex cannabifolia and Rhus lancea (Kim et al. (2003).
Monocots, with the exception of a very few Araceae and Dioscoreaceae, lack truly compound leaves (e.g. Gunawardena & Dengler 2006). Most apparently compound leaves in Araceae, as well as the fenestrate leaves found in some Araceae and Aponogetonaceae, are basically simple leaves. These subsequently become more or less modified by localized programmed cell death (e.g. Gunawardena et al. 2004), or, in the case of palms, the deep lobes in simple leaves, and the leaflets in apparently compound leaves, are the result of a process more like abscission (Nowak et al. 2007, 2008), although nothing, apart, sometimes, for the leaf margin, falls off.
Leaves are generally organs of determinate growth, but secondary growth has been noted in the leaves of a few angiosperms and conifers (Mathuse 1906; Ewers 1982). In Meliaceae like Chisocheton the apex of the compound leaf adds new leaflets over a period of several years, although the leaf always remains a leaf and does not produce vegetative or floral shoots (Fisher & Rutishauser 1990; Tsukaya 2005). In some Gesneriaceae-Didymocarpoideae and -Epithematoideae the plant body is a single ever-growing cotyledon, with flowers in some species developing along the midrib. The remarkable strap-like paired leaves of Welwitschia (Gnetales) may continue to grow for hundreds of years via a basal meristem.
Leaves are dorsiventral structures, and the blastozone, the developing lamina, and the leaf margins form at the boundary between the adaxial and abaxial surfaces (Fukushima & Hasebe 2014). Hagemann and Gleissberg (1996) discuss the difference between marginal blastozones in angiosperm leaves and meristems. Leaves in broad-leaved angiosperms are typically made up of petiole, lamina, and leaf base; stipules (see also below) are associated with the latter (see Cusset 1970 for a survey), while monocot leaves usually have entire, sometimes spiny, margins and broad bases, and stipules are at most uncommon (Ye & Ronse De Craene 2024, see also below). The terms petiole and lamina in monocots and other vascular plants are equivalent only by designation (Tillich 1998), and they may represent quite different parts of the leaf. For details of the classical approach to leaf morphology and development, e.g. whether the lamina develops from the leaf base (most monocots) or leaf apex (broad-leaved angiosperms), see Hagemann (1970), Kaplan (1973, 1997), Bharathan (1996), Tillich (1998), Rudall and Buzgo (2002), and Nardmann et al. (2004); Sinha (1999), Piazza et al. (2005) and especially Townsley and Sinha (2012) review leaf development in angiosperms. The terete, unifacial blades with stomata all over the surface that are found in some monocots may represent a development of the unifacial "tip" or "Vorläuferspitze" of the leaf (e.g. Goebel 1901; Arber 1925; Troll 1955; Troll & Meyer 1955; Kaplan 1975: comparison of Oxypolis and monocots), or from the middle portion of a bifacial leaf (see illustrations in Linder & Caddick 2001, q.v. for a summary of the literature), or from a leaf that has become abaxialized during development. The leaves of some broad-leaved angiosperms have stomata on both sides of the blade (amphistomatic), but the blade is still dorsi-ventrally flattened, i.e., they are isobifacial. In some monocots, apparently similar leaves are also isobifacial, but they are laterally flattened and they are often equitant at the base. They appear to be a bifacial dorsiventral blade that has folded and become connate adaxially, but they are more accurately described as being developed from the abaxial portion of the leaf primordium (e.g. Kaplan 1970a, 1975), or, developmentally, both they and terete unifacial leaves may represent the genetic abaxialization of the leaf, the genes normally expressed abaxially only becoming expressed over all the surface of the leaf (Yamaguchi & Tsukaya 2010; Yamaguchi et al. 2010). The development of an isobifacial monocot leaf such as is found in Acorus can be explained classically in quite different ways - is it a hyperphyll, and so equivalent to a broad-leaved angiosperm leaf, or does it originate from an intermediate zone between hyperphyll and hypophyll (Rudall & Buzgo 2002)? - but of course such descriptions are separate from those that result from developmental studies. Similarly, the "blade" of Hosta and Orontium may not be equivalent structures in other than a functional sense (Troll 1955). Ichihashi et al. (2011) recently noted the occurence of what was effectively an intercalary meristem at the base of the leaf blade in Arabidopsis. Cells were cut off both proximally and distally from this zone, rather like the pattern of development in many monocot leaves. A general survey of leaf development in angiosperms, with particular emphasis on monocots, will be very valuable; patterns of leaf development evidently vary at high levels. See below for connections between ligules, sheathing leaf bases, and stipules, and there is also further discussion of the whole problem under vegetative variation in the monocots.
There are various asymmetries in leaves and other parts of the plant (Bahadur et al. 2019a for an entry into the literature). The anodic (better, ascending) side of a leaf, i.e. that side of the leaf that is towards the ascending part of the genetic spiral, is often slightly less developed than the cathodic (= descending) side, or a bud on the ascending side of the leaf axil is less developed than that on the descending side, etc. (Korn 2006 for a summary; de Albuquerque et al. 2019: Marantaceae). Chitwood et al. (2012a) suggest that this is because the auxin concentration of the ascending side of the primordium is lower, some having diffused into the auxin sink represented by the next primordium developing on the apex. However, in decussate and distichous/two-ranked phyllotaxis the asymmetry of sequential leaf pairs or alternating leaves is mirrored (de Albuquerque et al. 2019), in taxa like Begonia very strongly so (Martinez et al. 2016). For anisophylly, which is evident in such situations and also when one of a pair of opposite leaves is reduced, see e.g. Dengler (1999) and Gerrath et al. (2001).
Nicotra et al. (2011) review leaf shape in anigosperms from a functional point of view, and while recognizing that shape and leaf temperature may be connected - shape affects leaf temperature - more of the variation in leaf morphology seems to be connected with water supply to the lamina and photosynthetic rates. Tsukaya (2006) and Kuchen et al. (2012) surveyed how leaf shape developed, while in a study of the relative importance of cell division frequency and cell size for the determination of leaf shape, Kuwabara et al. (2011) found that the latter could be more important than you might think.
More or less peltate leaves are known from a number of angiosperms (see Troll 1932 for a still useful review; Roth 1952; Ebel 1998: 144 herbaceous genera listed); such leaves are notably common in Menispermaceae and are scattered elsewhere. Peltate leaves may be simple or peltately palmate. In peltate leaves in general the petiole vasculature is strictly annular (or the vascular bundles form a circle), the leaf being largely abaxialized, although at the apex of the primordium there is a small adaxial zone from which the lamina or leaflets develop (Kim et al. 2003). It would be interesting to know if some taxa with simple leaves, strongly palmate venation, and apparently terete petioles, e.g. in Malvaceae, had a basically similar construction; the general distribution of peltate/peltately palmate leaves is not well understood. The very base of the leaf may be bifacial again - but not always (Gleissberg et al. 2005). Ascidiate leaves, found only in some carnivorous plants and in some terata on other plants like Codiaeum, are a variant of leaves with a restricted adaxial surface, and it is inside a tubular or pitcher-like structure in such leaves that prey are captured (Franck 1976 for a review).
For lamina vernation (ptyxis), how a leaf is folded in bud, terms and some data are taken from Cullen (1978) and Keller (1996: note that his convolute is Cullen's supervolute); Clos (1870) is an important early review. In descriptions of the vernation of compound leaves, the reference is to the folding of the leaflets. The sampling of this character is poor, the delimitation of the states needs attention, and variation may turn out to be rather too much for comfort when used at the level of this site. Indeed, Charlton (1993) shows how the plane of flattening of conduplicate leaves can change during development, and there is quite commonly variation in the plane of flattening within the individual, while in Begonia the vernation of the prophyll is different from that of the other leaves. When leaves remain rolled up as they elongate, the lower surface in particular of the fully expanded blades may have faint but distinct longitudinal lines; these often help in familial or generic identification of sterile material. The significance of the colours of the young leaves has occasioned some discussion (Queenborough et al. 2013 and references).
Four generalizations can be made about vernation types: first, in water plants with floating, peltate or cordate leaf blades, involute vernation is very common, second, the leaflets of compound leaves tend to be conduplicate, third, vernation in monocots is usually supervolute or supervolute-curved, and fourth, palmately-lobed leaves are often convolute-plicate in bud (Couturier et al. 2009, 2011). Couturier et al. (2011) emphasize that the growing leaves fill the bud (the filling law), and the veins of a leaf with palmate venation guide the folding of the leaf and its packing in the bud, the constraints of space being paramount; the folded shape of the developing lamina is much more conserved than its final shape. They compare the whole folding process of a leaf to Kirigami, where the final shape of a piece of paper is the result of folding it in a particular way and then cutting it down one side (Couturier et al. 2009).
Blade size. Ecologists in particular can find it useful to divide the size of the leaf or leaflet blade into a number of classes (Raunkiaer 1934; Webb 1959). Rather small, narrow leaves with very strongly revolute margins, ericoid leaves, are quite common in taxa that grow in warm and dry climates.
Lamina venation and blade margin can be considered together. Indeed, many aspects of foliar variation are covered by the umbrella concept of leaf architecture, and this is of particular importance for palaeobotanists; blade margins, venation arrangement and density, etc., provide valuable characters for leaf identification. Standardized terms allow that community to describe accurately details of fossil leaves; for the terms used, see Ellis et al. (2009) - the terms as used here should have the same definitions as those in the palaebotanical literature. In the course of his career, Leo Hickey made numerous slides of cleared leaves; these form the basis of the National Cleared Leaf Collecion and they are now freely available. For leaf architecture, see also Sack et al. (2012). Blonder et al. (2020) emphasized the importance of looking at leaf architectural traits at different scales, and they focused on features such as those likely to be involved in water, etc., transport, mechanical strength, and construction costs. They showed that there was considerable variation in such features - but little obvious correlation with phylogeny (Blonder et al. 2020).
Thinking about the blade margin in particular, in the category "toothed" are all margins that are serrate or dentate, even minutely so; the margin may even appear to be smooth, but close inspection may show small, more or less regularly spaced dots or glands. A number of tooth morphologies have been described for the leaves of broad-leaved angiosperms (Hickey & Wolf 1975). However, these are often difficult to recognize on simple inspection of a leaf (cleared leaves are best), and intermediates are also known, as in Fagales (Hickey & Taylor 1991), where two "types" and their intermediates may occur on the one leaf, and elsewhere (Doyle 2007). However, tooth morphology may yield information of systematic significance if analysed more carefully than it has been treated here, although the complexity of the venation associated with teeth to which can be added the variety of gland-type tissues/structures associated with them makes such analyses difficult (see also Doyle 2007; Rios et al. 2020). Note that nearly all families described as having leaves with teeth have some members with entire margins. Interestingly, the tips of some leaf teeth are colleter-like in structure and secretion, i.e., producing more or less mucilaginous exudate (Chin et al. 2013) that is perhaps involved in the lubrication of the leaf as it enlarges in bud; see also A. M. González and Tarragó (2009), Paiva (2012) and Fernandes et al. (2016: ?theoid leaf teeth in general) for a connection between leaf teeth and colleters (families: Aquifoliaceae, Lecythidaceae, Rosaceae, Salicaceae; salicoid leaf teeth?). Interestingly, the genes involved in the demarcation of leaflets are also implicated in the development of serrations on the leaf or leaflet margin (Blein et al. 2008). Although many woody plants with 1:1 nodes have leaves with entire margins; Celastraceae (1:1 nodes; serrate lamina) are an important exception (Sinnott & Bailey 1914) - and note also the correlation of nodal anatomy with stipule presence discussed above. In monocots, leaf teeth are rather uncommon, and there they are never glandular, rather, they are more or less spiny. Prusinkiewicz and Barbier de Reuille (2010) discuss the generation of various kinds of leaf margins in the context of space constraints, both major players in analyses of how leaves are folded in bud (Couturier et al. 2009, 2011).
Taxa with serrate leaves tend to be more common in temperate climates, but serration of leaves or leaflets also shows a correlation with phylogeny - e.g. the predominantly serrate lamina margins in the predominantly tropical Malvaceae (Burnham & Tonkovich 2011). Burnham and Tonkovich (2011 and references) discuss the complexity introduced into the use of features like lamina teeth as palaeoclimatic indicators because of such correlations (see also Bailey & Sinnott 1916; Little et al. 2010; Walls 2011; Schmerler et al. 2012; E. J. Edwards et al. 2016, 2017; Givnish & Kriebel 2017).
Rios et al. (2020: see esp. Fig. 3) looked at the anatomy of leaf teeth in a number of eudicots, and at the associations of the teeth with glands, whether hydathodes, colleters or extrafloral nectaries. In a number of taxa that have glandular leaf teeth there is guttation, the exudation of liquid droplets that is especially evident when conditions are humid, and it is often thought that this is water exuding because of the water pressure in the xylem vasularizing the teeth; it may be imbibed by insects, etc.. However, recent work questions this assumption. Urbaneja-Bernat et al. (2020) found that the concentrations of sugars and proteins in the guttation droplets coming from the leaf teeth of Vaccinium corymbosum were remrkably high, the droplets attracting everything from spiders and ants to gall midges, largely carnivorous animals (but not aphids or plant herbivores). The guttation droplets were notably prominent when the plant was metabolically particularly active, i.e. when leafing out and reproducing, presumably reflecting what would be going on in the xylem and phloem of the plant as a whole. Theae droplets were produced for months, the leaf teeth effectively functioniung as extrafloral nectaries (not a comparison made by Urbaneja-Bernat et al.). Hydathodal droplets with appreciable concentrations of nutrients have been recorded from a number of crop plants, both in Poaceae (produced from hydathodes at the end of the leaf) and core eudicots (references in Urbaneja-Bernat et al. 2020); the droplets are usually most evident when the plant is young. Clearly, the distinction between guttation and the products of extrafloral nectaries is not easy to make, and colleters and leaf teeth may be one and the same thing. See also S. Singh (2013) for a review of guttation.
Turning now to lamina venation in particular, Nelson and Dengler (1997) surveyed the development of leaf venation. Unfortunately, sampling within broad-leaved angiosperms was largely restricted to rosids, and within these, Arabidopsis (Brassicaceae) differed in having basipetal development of tertiary venation (it is normally acropetal in Rosids). Taxa such as Liriodendron (Magnoliaceae) have an intermediate pattern of initiation. Runions et al. (2005), Prusinkiewicz and Barbier de Reuille (2010), and others analyze leaf venation patterns from a more "process" point of view.
A distinction is drawn in the characterizations between leaves in which two or more major veins leave the midrib at or almost at the base of the lamina (palmate), those in which these veins leave the midrib along its length (pinnate), and those in which there is no distinction between a midrib and secondary veins, all veins being similar, parallel, and proceeding to the apex (parallel, especially common in monocots). Klucking (1986 onwards) provides a comprehensive survey of leaf venation and Christophel and Hyland (1993) is another useful source of information, however, the detail shown by the nature prints of von Ettingshausen (e.g. 1858, 1861, and throughout his career) has not often been bettered.
Other features of interest include whether the vein endings are free or form a dense reticulum, the density of the vein reticulum of the leaf, and whether or not the smaller veins are transcurrent, that is, joined to the leaf surfaces by echlorophyllous tissue. These features all have considerable physiological significance. Variation in the patterns made by the secondary and tertiary veins are important elements in the various venation "types", but these are referred to only sporadically in the characterisations. As mentioned, there are a number of different tooth "types" that are based on the nature of the tooth and of the veins that serve it, although given the variation in these types, the use of venation characters in phylogenetic studies may not be very comforting (e.g. Hickey & Taylor 1991; see also Doyle 2007 for leaf venation placed in a phylogenetic context). For definitions of the terms used, see e.g. Hickey and Wolfe (1975), Hickey (1979), the Leaf Architecture Working Group (1999) and Ellis et al. (2009); Roth-Nebelsick et al. (2001) looked at venation patterning and its development from a functional (support, transport) point of view.
Conover (1983) and Inamdar et al. (1983) discuss leaf morphology and architecture in broad-leaved monocots with reticulate venation; such leaves have evolved several times and are associated with particular ecological conditions (e.g. Givnish et al. 2004c). In many broad-leaved monocot taxa the parallel main veins are linked by well developed ladder-like cross veins. Venation density varies considerably, and this has been placed in an evolutionary/phylogenetic context, for example by Boyce et al. (2008, 2009), Feild et al. (2011), etc. Venation density tends to be notably higher in angiosperms, especially eudicots, than in other vascular plants, although it is lower in succulents, epiphytes, etc. Venation density affects the flow of water from the vascular bundles to the stomatal apertures and hence greatly affects photosynthetic rates. Minor vein morphology shows considerable variation that may be connected with the movement of assimilates in the leaf. These veins are of two major types. The "open" type is where there are plasmodesmatal fields in the common walls of the mesophyll cells and the cells immediately surrounding the phloem, the intermediate cells, and this is found in evergreen taxa, and phloem loading is symplastic, with oligosaccharides, amino acids and sugar alcohols in the phloem exudate. The "closed" type lack such plasmodesmatal fields, although some taxa have so-called transfer cells with wall ingrowths (c.f. the labyrinthine cells in the placental region that connect the sporophyte and gametophyte); the closed type is found in herbaceous taxa, phloem loading is apoplastic, and sucrose alone is in the phloem exudate. Another subtype is rather like the Open type, but it has no plasmodesmata in the walls between the bundle sheath and intermediate cells; this subtype is found in taxa with C4 photosynthesis (Gamalei 1989, 1991, q.v. for further details).
Another important feature of the lamina, more anatomical and rarely mentioned in the characterizations, is the presence of bundle sheath extensions. If present, they greatly facilitate flow of water from the vascular bundle to the epidermis, so affecting stomatal opening and closing - and hence photosynthetic rate again - Buckley et al. 2011.)
For a useful general discussion of variation in the surface of the leaf blade, see Wilkinson (1979). Hydathodes, domatia, and even lenticels may be found on the leaf surface, although they rarely mentioned in these pages because their variation is mostly at a level lower than is the focus here. Hydathodes are particularly well supplied with tracheids, not with phloem; extra-floral nectaries show the reverse relationship. A few taxa have nodules on the leaf blade that are inhabited by bacteria, although details of their functional significance are often unclear (Miller 1990 for a review; Pinto-Carbo et al. 2018), or there are bacteria liviung inside the leaf which can be fatal to (introduced) herbivores, and the clades involved may be more or less notably diverse (e.g. Verstraete et al. 2011b, 2017). For distinctive colour patterning and textures of the lamina surfaces, particularly evident in shade-dwelling species, see Jacobs et al. (2016) and references, also above.
Extra-floral nectaries (EFN: see e.g. Elias 1983; Schmid 1988; Blüthgen & Reifenrath 2001; Koptur 2005; Marazzi et al. 2013a; Weber & Keeler 2013: Zimmermann 1932 for an early summary; Wäckers 2005 and Lüttge 2013 for some information on nectar composition and secretion; Weber et al. 2015 for an annotated list) are often found on leaves, but also on other parts of the plant like the stem, the outside surface of the calyx, the developing fruit, etc. (e.g. Koptur 1992). Ants are common visitors to EFNs, and ant species largely the same as those visiting EFNs were notably common visitors to sap exuding from wounds on leaves of Fagaceae in subtropical S.E. China (Staab et al. 2017: planted forests), suggesting a possible route for the evolution of these nectaries. Interestingly, secretion at EFNs and nectar-producing wounds in Solanaceae is commonly stimulated by wounding/herbivory via a jasmonic acid response (Heil 2015; Lortzing et al. 2016), indeed, in a number of taxa a variety of stimuli result in the induction of extrafloral nectar (Heil 2015). Sucrose is uploaded from phloem in EFN, particularly in young plants where phloem flux tends to be highest (Heil 2015). The morphological and developmental relationships between EFNs found at various places on the plant, and between EFNs and leaf teeth, are complex. Thus for the expression of the CRABS CLAW gene in floral but not EFNs in core eudicots, see J.-Y. Lee et al. (2005a, b; but c.f. Krosnick et al. 2008a; Nakayama et al. 2010 - not in septal nectaries); extra-floral nectaries in Passiflora are rather different both from those in other broad-leaved angiosperms and from floral nectaries (see e.g. Krosnick et al. 2008a, b, 2011). Escalante-Pérez et al. (2012) recently found that foliar EFN on two species of Populus differed considerably in structure and mode of action; in one species they were persistent, with continuous nectar flow, while in another, large amounts of nectar were produced over a short time and cell death occured, but new nectaries could be produced; Thadeo et al. (2008) discuss the similarities between leaf teeth and foliar nectaries in Salicaceae (see also Leitão et al. 2005). One kind of nectary on the leaf margin in Prunus was functionally and anatomically similar to flat glands on the abaxial surface of the lamina (Chin et al. 2013). There is a close connection between nectary-like leaf teeth and colleters (see above). Various other kinds of surface "glands" and nectariferous structures are found on the lamina. Thus black-drying flat glands on the leaf surface are useful in identification as well as being common in and perhaps synapomorphies for sizable clades such as Ebenaceae, Chrysobalanaceae and relatives, etc. (these, too, are a kind of EFN), while other "glands" may in fact be cork tissue associated with stomata, as in a few species of Prunus (Chin et al. 2013).
A distinction can be made between extrafloral nectaries that are intimately involved in pollination, such as the nectaries on the cyathia of Euphorbia (= nuptial nectaries), and those that have nothing immediately to do with pollination, but may attract ants that help protect the plant against herbivores or destroy the young stems of vines that would otherwise use the plant as support and in the process smother it (extra-nuptial nectaries).
Punctations, often "glands" of various kinds, are evident when the leaf is viewed in transmitted light. Note that magnoliids with ethereal oils tend to have ± punctate laminas (e.g. van Balgooy 1997), as well as the text-book examples of Rutaceae and Myrtaceae where the glands are often much larger and more organized. Other taxa secreting oils, tanniniferous substances, etc., or with cystoliths or sclereids (see above) may also be punctate, and punctations may also be evident in the calyx, corolla, etc. Other oil bodies, especially in leaf mesophyll cells, may contain neutral oils, triglycerides (triacylglycols). This kind of oil body is widely distributed in angiosperms, although they have not been reported from the ANITA grade or the magnoliids (Lersten et al. 2006). Punctations are mentioned only when they are conspicuous, however, they can suggest the presence of these anatomical features and are, along with the presence of nectaries, etc., often very useful in identification.
The leaf base is commonly sheathing in monocots; the sheath may be open, with free edges, or closed and continuous around the stem. Cells that are recruited to become stipules (as in Arabidopsis) or sheathing leaf bases (as in grasses) come from the lateral part of the primordium, and mutations that abaxialize the leaf interfere with this process (Townsley & Sinha 2012). Monocot leaves may bear distinctive, adaxial flanges or ligules at the very base or some way up the sheath; auricles, lateral projections of the "petiole" or sheath/blade junction, also occur. The ligule in at least some cases in monocots demarcates the Vorläuferspitze or equivalent area from the rest of the leaf; in Zamioculcas the ligule is very near the base of the petiole, which would suggest that the leaf there is developmentally similar to that in broad-leaved angiosperms. In broad-leaved angiosperms the leaf base is commonly narrow, but it is distinctly wider in Dilleniaceae, Caryophyllaceae, Nepenthaceae, etc., while the leaf base in many Liliales is notably narrower than that of most other monocots.
Stipules in broad-leaved angiosperms are more or less foliaceous, vascularised, often paired outgrowths borne laterally or adaxially on the base of the petiole or on the stem lateral to the petioles; they are a part of the leaf. They can bear nectaries or colleters, be modified as spines, etc.. They may be petiolar, clearly inserted on the petiole, or cauline, largely inserted on the stem. Intrapetiolar stipules are inserted between the petiole and stem, interpetiolar stipules are single, often lobed stipules borne between opposing leaves, while sheathing stipules (= ochreae) completely surround the stem and form a tubular structure, whether or not they are more or less scarious, as in Polygonum, thick and robust, as in Coccoloba and some species of Fagraea, or bear foliar outgrowths, as in Platanus. Useful studies of stipules and stipuliform structures may be found in e.g. Roth (1949), Weberling (e.g. 1968, 1970, and especially 2006 [largely a summary]) and Weberling and Leenhouts (1965). Guédèes (1968) was inclined to call situations as in Potentilla and Caryophyllaceae-Paronychioideae (i.e. Paronychieae and tribes immediately following it) where there was an adaxial flange of tissue joining the stipules "ligular stipules", lateral stipules joined by a true ligule. Cruz et al. (2015) describe the development of stipules in Metrodorea, in Rutaceae, a family one does not normally associate with having stipules. See above for correlations between nodal anatomy and stipule presence/absence, Colomb (1887), Lubbock (1891, 1899) and Tyler (1897) for some of the older literature and Ye and Ronse De Craene (2024: esp. Appendix 1) for a survey of stipules in Angiosperms.
Little attempt has been made to distinguish between "true" stipules and other structures that are in the stipular position. However, some structures commonly called stipules appear to be more or less modified colleters (see below: e.g. some Myrtales, Apocynaceae-Asclepiadoideae) or leaflets (e.g. Burseraceae and Sapindaceae), and when this is obvious the characterisations are qualified. From a gross morpho-anatomical point of view, what a stipule "is" and how it can be distinguished from a monocot ligule, etc., is problematic. Recently de Aguiar-Dias et al. (2011) suggested that the paired nectary glands at the base of the leaf in Polygala are stipules because they are also vascularized from the nodal trace; nodes here are unilacunar, while pallisade glandular tissues with protein rich secretions on the leaf teeth and stipules of some species of Ilex have lead to the latter being called colleters (A. M. González & Tarragó 2009). But there is more. Some suggest that stipules ex definitio do not occur in monocots. However, as has been pointed out by authors like Roth (1949) and Rudall and Buzgo (2002), the developmental origins of monocot ligules and at least some stipules of broad-leaved angiosperms are basically similar; both arise from adaxial cross meristems in the transition zone between hyperphyll and hypophyll; Kaplan (1997: 1 ch. 5) called such structures - which would include seedling coleoptiles - stipules. Although I have not used the term "stipule" in the monocot characterisations, it is probable that there are structures there that have at least as good a title to the name as some of the things called stipules in broad-leaved angiosperms; there are certainly developmental connections between stipules, sheathing leaf bases, and ligules; see also elsewhere.
Leaf insertion or phyllotaxis. Mention of this feature in the characterizations refers to the insertion of leaves on flowering branches, not on non-flowering axes (when these are distinct) unless specified otherwise. I usually make no distinction between opposite and whorled leaf insertions in the family characterizations since these both commonly occur within a family or even genus; most families of any size in which opposite leaf insertion is common also have taxa with whorled leaves. I include bijugate leaves with opposite leaves, although there are distinct functional consequences in having bijugate leaves - shading of the lower leaves is reduced, compared to strictly decussating leaves. For systematically informative variation in leaf insertion on the main stem/trunk when leaves on branches are invariant in their insertion, see Johnson (1993). The main variations in phyllotaxis (rather simplistically conceived) mentioned are spiral, 2-ranked (distichous), 3-ranked (tristichous) and opposite (usually decussate). Mabberley (2007), too, makes the important distinction between spiral and distichous (see also Corner 1946a), which are too often lumped together and ambiguously referred to as 'alternate'. Two-ranked leaves vary in whether their plane of insertion on the branch is vertical or horizontal - horizontal is usual, but it is sometimes vertical (e.g. von Veh 1931). There are other phyllotactic variants, such as the 180o, 90 o, -180o, -90o positioning of successive leaves relative to the previous leaf, as in the recently-described orixate phyllotaxis (after Orixa japonica-Rutaceae): see Yonekura et al. 2019). Of course, leaves may also reorientate after their initiation, as in Coffea and some other Rubiaceae in which the leaves on the plagiotropic branches, although decussate when initiated, end up as being superposed as the internodes twist 90o, the leaf blades then all being at right angles to the incident light - the plants involved tend to grow in shady conditions. Adler et al. (1997) provide a history of ideas about phyllotaxis, and for general discussions on phyllotaxis, which include Fibonacci patterns or series (1, 1, 2, 3, 5, 8, 13...), as in the capitula of Asteraceae, see Jean (1994), Jean and Barabé (1998), Mauseth (2020), Yin and Kitazawa (2021) and other papers in J. Plant Res. 134(3). 2021, and for the measurement of phyllotaxy, see Rutishauser and Peisl (2001). Note, however, that in Lycophyta in particular the phyllotactic series is often n:(n + 1), perhaps associated with dichotomous branching (Turner et al. 2023). Describing phyllotaxis can be difficult, e.g., is the direction of a spiral given as viewed from above or below? For additional details of the ontogenetic transitions, control and modelling - becoming ever more realistic - of phyllotaxis, see Douady and Couder (1996 and references), Reinhardt et al. (2003), Hotton et al. (2006), Kuhlemeier (2007), Smith et al. (2006), Sampathkumar et al. (2015), Molteno (2021: Asphodelaceae-Asphodeloideae) and Walch and Blaise (2023). Early work (see e.g. that of Hofmeister 1868; Snow & Snow 1932, 1952) had suggested that the development of a leaf primordium somehow inhibited the development of new primordia immediately adjacent to it (see also Kirchoff 2003 for Hofmeister's Rule), but the diversity of phyllotactic types, and their respective frequencies, may be best modeled if the inhibitory power of primordia changes (increases) with age (Yonekura et al. 2019). Walch and Blaise (2022a) also discussed the inhibitory effect of bracts, other flowers, etc., on the position of initiation of perianh members.
Prophyll number, position, and orientation. Prophylls, the first leaves on axillary shoots, are usually either paired and lateral (probably the basic condition for seed plants) or single and adaxial, as in many monocots. In eudicots, Piperaceae (q.v.) and Annonaceae (e.g. Fries 1919) in particular seem to show variation in prophyll position, and monocots are also quite variable in this, especially in the inflorescence (see below: e.g. Eichler 1875; Engler 1888; Remizowa et al. 2006b; Stuetzel & Marx 2005; Walch & Blaise 2022a). Especially in monocots, there is extensive discussion as to what prophylls "are" - one leaf, two connate leaves?; Blaser (1944) summarized the often exasperating early literature on the topic. The bracteoles of flowers are simply the prophylls of the short shoot that makes up the flower.
Whether or not prophylls are basal on the branch is often, but not always, associated with whether branches are proleptic or sylleptic; in proleptic branches the prophylls are usually basal, while in sylleptic branches they have a well-developed internode, the hypopodium, below them. Exceptions have both biological and systematic significance. A major group in Rosales, including Ulmaceae, Cannabaceae, etc., have basal prophylls whatever the dynamics of shoot growth, and buds in the axils of these prophylls may be very conspicuous. Inflorescences here are often axillary in pairs, or paired and borne at the bottom of branches; in either case they come from buds is the axils of the prophylls. Taxa with axillary thorns or branch tendrils - these are usually sylleptic - may also show distinctive patterns of variation. In plants in which prophylls are not basal on the thorn (e.g. Gleditsia-Fabaceae) or tendril (e.g. Passiflora-Passifloraceae: Hernandes-Lopes et al. 2019) conspicuous serial buds in the axils of leaves that subtend the thorns/tendrils are developed, and these buds provide replacement meristems for the main axillary shoot that has been converted into structures that cannot function as replacement meristems. However, taxa with thorns/tendrils that have basal prophylls (e.g. Crataegus, Rosaceae) have functional buds in the axils of these prophylls and often lack obvious serial buds in the axils of the leaves.
Breeding systems, Inflorescences, and Pollination.
The breeding system predominating in the family is often mentioned. There is much variation in breeding systems, and this may be in floral type, i.e., whether the flowers have stamens and/or carpels, or in the relative timing of the maturity of the stamens and carpels - specifically, the receptivity of the stigma - of a single flower or plant. As regards the former, it is rare that any sizeable family recorded as being monoecious or dioecious is consistently so, conversely, families predominantly with "perfect" flowers (the common condition, and not mentioned when it occurs) nearly always have some taxa with other flower types/breeding systems. Thus Käfer et al. (2014) noted that although dioecy was an apomorphy for some quite large clades, in most of these there have been reversals to monoecy where the monoecious clade may be more or less extensive. The literature on this general topic is huge, see e.g. Ehlers and Bataillon (2007), Schaefer and Renner (2010), Barrett (2013), Pérez-Escobar et al. (2015), Sabath et al. (2015) and Goldberg et al. (2017). Henry et al. (2018) discuss the various ways in which dioecy has evolved in plants (see also Renner 2001b). Recent work has found a number of cases of the two-favtor model of dioecy, a dominant suppressor of female organs that is closely linked with a dominant activator of maleness. For mechanisms of sex determination, see e.g. Charlesworth (2008), Chuck (2010), Pérez-Escobar et al. (2015) and Schlessman et al. (2014), for the evolution of dioecy, see Käfer et al. (2014), and for sex chromosomes and their evolution, see Westergaard (1958: classic review, sex determination), Ming et al. (2011), Filatov (2015) and Akagi and Charlesworth (2019).
There are various correlations between apects of the breeding system and other features of the plant. Wind-pollinated plants are predominantly monoecious, sometimes dioecious (the latter especially in gymnosperms), and some kind of protogyny is quite common here (Bertin & Newman 1993); dioecy is commonest in woody, tropical plants, whereas gynodioecy is more associated with herbaceousness and temperate conditions (Renner & Ricklefs 1995; Renner 2014; Dufay et al. 2014; Caruso et al. 2015; Ramsey & Mandel 2019: esp. gynodioecy and heteroplasmy). In angiosperms the fruits of wind-pollinated plants are often dry and single-seeded, while in gymnosperms there is a correlation between dioecy and fleshy, animal-dispersed disseminules and monoecy and wind-dispersed disseminules (e.g. Bateman et al. 2011). In monoecious plants where staminate and carpellate flowers occur on the same inflorescence, the carpellate flowers are usually topologically basal; this is true of both monocots (e.g. Tomlinson 1982; Rudall 2003; Ambrose et al. 2005) and broad-leaved angiosperms (e.g. Krosnick et al. 2006), e.g. see many Euphorbiaceae, Kirkiaceae. This may be connected with the frequent occurrence on interfloral protogyny in such plants (Bertin & Newman 1993). Exceptions include Begonia (Begoniaceae) in which the carpellate flowers are produced in the cymose inflorescence after the staminate flowers, Ricinus (Euphorbiaceae) in which the carpellate flowers are in the top part of the inflorescence, Pteleopsis (Combretaceae), and even the fossil Archaefructus, at least under some interpretations of its morphology (Friis et al. 2003b). Diversification rates may increase in dioecious clades of angiosperms (Käfer et al. 2014).
Very often the stigma of an individual flower is not receptive at the same time that pollen is picked up by the pollinator. Dichogamy is the condition in which stamens and carpels of the one flower mature (anthers dehisce, stigmas are receptive) at different times, and it at least reduces the possibility of a flower selfing itself. This idea can be extended to floral behaviour on different plants, as in heterodichogamy, in which the reproductive phase of a flower varies between separate plants within a population; this condition is scattered, but is likely to be under-recorded (Renner 2001; Zhao et al. 2012); Rohwer (2009) suggested interesting possible variation based on a heterodichogamous theme in the [Lauraceae + Hernandiaceae] clade. Endress (2020) discussed heterodichogamy, pseudoheterodichogamy and duodichogamy. Although protandry might be supposed to be the default option since stamens would seem likely to mature before the carpels in flowers in which floral development was centripetal (Kalisz et al. 2006), protogyny, the common condition, is probably the plesiomorphic condition in angiosperms (e.g. Bertin & Newman 1993 for a survey; see also Routley et al. 2004).
Inflorescence position and morphology affects the access of pollinators to the flowers. Inflorescences may be axillary and/or terminal, or they may be borne along the branches, at the base of the trunk, or sometimes on long, slender branches that extend metres from the trunk. A few taxa are geocarpous, the inflorescences being underground (Kaul et al. 2000); the terms used to describe this and other similar behaviours are complex (Barker 2005). Epiphyllous inflorescences that arise from along the petiole or lamina are sporadic in occurrence (see Stork 1956; Dickinson 1978), but in Dichapetalaceae, Arecaceae-Calamoideae, etc., such inflorescences are common in quite substantial clades.
Inflorescence morphology. For a generally accessible introduction to classical inflorescence morphology, which can be very typological and complex and with a correspondingly complex and daunting terminology, see Weberling (1989); Rickett (1944) had earlier pointed out problems with how we went about describing inflorescence morphology (see also e.g. Parkin 1914; Troll & Weberling 1989; Troll 1964, 1969; Weberling 1998; the papers in Ann. Bot. 112(8). 2013). Leins (2000) distinguished between indeterminate (open) and determinate (closed) inflorescences. The former included racemes, etc., as well as thyrses, rather confusingly defined as inflorescences in which the main and sometimes the lateral axes might not be terminated by flowers, while the latter included "Vorblatt-Inflorescenzen" (cymes), panicles, etc. Briggs and Johnson (1979) suggest a "more logical (but not theory-limited)" approach to inflorescence description and comparison, but it is difficult to apply to a study at this level, Claßen-Bockhoff (2000) discusses previous attempts to describe and classify inflorescences (and suggests a general evolutionary schema for inflorescences in flowering plants herself). Claßn-Bockhoff and Bull-Hereñu (2013) describe details of inflorescence development of a number of taxa, making the point that in some cases it is better to think of floral unit meristems rather than inflorescence meristems, and the former, indeterminate like flower meristems, produce dense flower-analogues like the capitulum of Asteraceae (see also Zhang & Elomaa 2020). Prenner et al. (2009) and Endress (2010a) also discuss the need to revise inflorescence terminology; see also Stebbins (1973), Tucker (1999a), Tucker and Grimes (1999) and other articles in Bot. Review 65(4). 1999.
As Castel et al. (2010: p. 2236) noted when discussing the complex set of terms used to describe inflorescences, "no science can afford to have its descriptive terms, which are supposed to clarify, be such major sources of confusion" (see also Kiel et al. 2017). A major problem, as Park et al. (2013: p. 74-75) observed, was that "...what is most relevant in characterizing inflorescence forms ... is appreciating the continuum of meristem maturation processes both between meristems within a plant and between homologous meristems on different plants." However, if one decomposes the basic growth processes that are likely to be going on in inflorescences, the variables are encompassed quite readily by thinking of an axis that is terminated by a flower, or not; that keeps on growing, or dies; that produces branches or flowers; and has inflorescence bracts/prophylls subtending branches, or just flowers (branching is more important than any apparent absence of prophylls - for the latter, see below). An additional variable is, do internodes elongate, or not? - and that is basically that (Kellogg 2000b; see also Singer 2006). Castel et al. (2010) and others develop the approach adopted by Prusinkiewicz et al. (2007) in their discussion of the inflorescences of Solanaceae as they attempt to think of inflorescence morphology from a more dynamic and less typological point of view (see also Périlleux et al. 2014; Ma et al. 2017b; Zhang et al. 2022). Important questions are what determines whether a terminal flower is produced or not? and what causes internode elongation? Here Prusinkiewicz et al. (2007) have suggestions; see also Singer (2006), Prusinkiewicz and Barbier de Reuille (2010) and Harder and Prusinkiewicz (2013) for more ideas, Bull-Hereñu and Claßn-Bockhoff (2013: inflorescence apex size and subsequent morphology, and Teo et al. (2013) for archicture regulation at the molecular level. Benlloch et al. (2007), Thompson and Hake (2009) and Preston (2010) examine inflorescence architecture from the point of view of floral gene expression, Benlloch et al. (2007) emphasizing that the diversity of inflorescence architecture seems to be the result of the interactions of only a few genes in a rather simple regulatory network. Bull-Hereñu and Claßen-Bockhoff (2011a, see also b) note that gain and loss of a terminal flower in an inflorescence can happen by more than one ontogenetic pathway - and quite easily; Penin et al. (2005) thought that there had to be a leaf/bract at the node immediately below for a terminal flower to develop, but c.f. Périlleux et al. (2014). For much literature, see Ma et al. (2017b).
Given all this, how should one describe inflorescences? Since most inflorescence types represent morphologies produced by several largely independent variables (see above), I hope (as of viii.2011!) to be more simply descriptive when mentioning inflorescences. In the characterizations I will refer mainly to racemes or racemose (polytelic/indeterminate) inflorescences where the main axis does not terminate in a flower, the flowers being borne singly in axils along the axis (and the same for any branches of the inflorescence that are present), and cymes of various kinds, when there is no extended main axis and all lateral axes are immediately terminated by flowers; for a discussion of the various kinds of monochasial cymes, see Buys and Hilger (2003). More complex inflorescences include a thyrse, in which the main axis may or may not be terminated by a flower, but the branches are cymes, and panicle ("Rispe"), in which the inflorescence is branched, there are no simple, bracteate cymes, but all axes are terminated by flowers (extreme polytely); both terms are often used in the literature, but with more than one definition. Capitulae, corymbs, umbels and fascicles are also mentioned in the characterisations below. These are useful terms that describe what an inflorescence looks like, but, with the exception of corymb, carry no implications as to whether the inflorescence is indeterminate or not.
Bracts and bracteoles are usually mentioned only when they are absent. However, as Castel et al. (2010 and references) note, bracts that appear to be absent when looking at the adult plant, as in Brassicaceae and Solanaceae, may indeed be present if one looks carefully at the young plant; bracts and bracteoles that are entirely absent may be quite uncommon (see Fries 2011 for old arguments about this issue). The position of bracteoles is normally the same as that of prophylls on vegetative shoots (see above), since they are simply the prophylls of shoots that bear flowers. Nevertheless, in many monocots that have single adaxial prophylls on vegetative shoots the bracteoles are depicted as being lateral or even abaxial, and they can also be paired - in general, adaxial prophylls are found in plants that have 2-ranked leaves, and more or less lateral prophylls in those with spiral leaves, and these differences are associated with differences as to where the tepals are initiated, although as can be seen from sources like Eichler (1875: Vol. 1: 20-33) and Walch and Blaise (2012a, 2013) and references there is a considerable amount of variation in detail of the position of the prophylls and tepals. These "abnormal" positions are often associated with monosymmetric flowers that have inverted or oblique symmetry (see below: Eichler 1875, 1880; see also Bruhl 1995; Choob & Mavrodiev 2001; Buys & Hilger 2003); prophyll number and position in monocots will clearly repay further study. Indeed, Nuraliev et al. (2020b) report complex variation in bracteole number (0-3) and floral orientation in Thismia, and also mention less extreme variation in some other monocots. On the other hand, eudicots like Annonaceae have flowers and usually also vegetative shoots with adaxial prophylls, although some taxa like Annona itself have vegetative shoots with lateral prophylls (e.g. Fries 1911, 1919). For genes controlling floral prophyll development, see Masiero et al. (2004). Of course, in angiosperms in general, bracts and bracteoles cannot be recognized when the flower is single and terminal.
Pedicel articulation may be a useful character, especially in monocots (for information there, see Schlittler 1953a; Kubitzki 1998a); there is a line across the pedicel where non-fertilized flowers abscise. The part of the pedicel above the point of articulation has been considered to be different from the part below, being more strictly part of the flower proper; the term "pericladium" has been used.
For definitions, etc., see the Glossary.
Particularly valuable sources of information for the arrangement of the parts of the flower include Eichler (1875-1878), and for floral morphology in general Engler's Die natürliche Pflanzenfamilien, the various volumes of Das Pflanzenreich, the great Flora brasiliensis (Martius & others 1840-1906), etc.. Batygina (2002, 2006, 2009) has edited three volumes on terms used to describe flowers, embryology, and seed, etc., while Ronse de Craene and Endress and their collaborators and Leins and Erbar have revitalized the field of floral morphology over the last thirty years or so. There are a number of useful summaries of aspects of floral morphology and development, including those of Leins (2000), Endress (1994b; 2005a [especially development], 2005c, 2011, 2019 [relation between carpels and ovules]), and Leins and Erbar (2010). Features of the flower, especially its vascularization (by analogy to a vertebrate skeleton?), ovules, details of embryo development, etc., have been heavily mined in the past in particular for ideas about primitive floral morphology. These features have often been considered in isolation and without thinking of the flower as a functioning unit with adaptations to its particular pollinators, seed dispersers, etc., and as a result some of the earlier literature is not very edifying; Carlquist (1970b) provides a comprehensive critique that is still worth reading.
Pollination and floral/pollination syndromes are mentioned relatively infrequently below (for summaries, see Faegri & van der Pijl 1979; Endress 1994b; Leins & Erbar 2010) given the vast amount of work that has been carried out on them. This is because the floral variation associated with such syndromes is often at a finer scale than is the focus of these pages. Importantly, similar floral morphologies have often evolved independently in groups that may not be at all closely related in connection with pollination by the same pollinator or class of pollinators (see Assis 2023 for bat pollination, although a complex example), and past over-reliance on similarity in pollination syndromes as an indicator of relationships has caused serious taxonomic/evolutionary problems from the ordinal level down (e.g. see the demise of the old Amentiferae). However, the problems are now particularly pollination syndrome-driven phylogenetic confusion at lower levels, e.g. within Bignoniaceae, Ericaceae, Gesneriaceae, Orchidaceae, and Melastomataceae. Thus the buzz-pollination syndrome (see below) was often used to characterize genera since buzz-pollinated flowers can look distinctively different from their close relatives that are pollinated in other ways, however, such genera have quite often turned out out to be derived from within another zoophilous clade. Examples are Dodecatheon/Primula and Oxycoccus/Vaccinium), where recognition of the first genus in each pair makes the second paraphyletic.
Nevertheless, variation in pollination mechanisms is extensive and biologically, taxonomically and evolutionarily interesting. Even if the morphological characterization of these syndromes, e.g. as ornithophilous (see Cronk & Ojeda 2008), can be overly simplistic (Waser et al. 1996, 2018; S. D. Johnson & Steiner 2000; Waser & Ollerton 2006; Morales & Aizen 2006; Olesen et al. 2007; Raguso 2008; Smith et al. 2009; Ollerton et al. 2009a; S. D. Smith & Kriebel 2018; but c.f. in part Bernhardt 2000; Fenster et al. 2004; Willmer 2011; Quintero et al. 2016; Wilson et al. 2017; Lagomarsino et al. 2017; Serrano-Serrano et al. 2017; Guzmán et al. 2017; S. D. Johnson & Westra 2017; Mochizuki & Kawakita 2018; esp. Rosas-Guerrero et al. 2014; Dellinger 2020; Assis 2023; see also the papers in Ann. Bot. 113(2). 2014), there is often a connection between the kind of pollinator and the morphology, etc., of the flowers it pollinates, and this extends to features like nectar composition (Vandelook et al. 2019 and references). For predictions of pairwise plant–pollinator interactions based on species attributes, see Peralta et al. (2024). Syndromes include those involving bees (especially buzz pollination), birds, bats, flies, wasps, moths, butterflies, long-tongued flies, fungus gnats, beetles, carrion flies and non-flying mammals (Dellinger 2020: p. 1194). Of course, some species are pollinated by a variety of pollinators and can be called generalists, as in Melastomataceae, where vertebrate pollination may involve pollination by birds, bats and/or rodents, the morphologies associated with pollination by these different animals being very different (e.g. Kriebel & Zumbado 2014; Brito et al. 2016, 2017; Dellinger et al. 2021). Similarly, the large monosymmetric flowers of Catalpa speciosa are pollinated by several species of both day- and night-flying insects (Stephenson & Thomas 1977), although these are at least all insects, while Bernhardt (2020) discusses pollination events in which beetles and other insects are involved. However, Dellinger et al. (2019a: Melastomataceae again) suggest that some taxa have two or more quite different pollinators, a bimodal pollination system, and such systems are not situations in which a flower is becoming adapted to a new kind of pollinator. Syndromes continue to be described, a recent example being the fungus-gnat syndrome (Mochizuki & Kawakita 2017, see also Kawakita et al. 2022), and there must be around 13 syndromes (Assis 2023). Of course, the very definition of syndrome suggests that matches between the features of pollinator and plant involved in pollination may well be less than perfect in different species. Certainly, interpreting floral morphology from the point of view of the pollinator is very important, thus photographing the flower under u.v. light (see above) and making false colour floral reconstructions by combining u.v. and colour photographs so as to see what a bee sees can help clarify things; what the pollinator sees (and smells) is critical (e.g. Schaefer & Ruxton 2009, 2010; Schiestl et al. 2010; Lunau et al. 2021). The finding that in at least some birds there is categorical perception of colour (Caves et al. 2018) extends the problem. Scent is important in a variety of aspects of pollination, from aiding in the detection of the flower, whether in pollination by male euglossine bees or bees involved in sexual deception by the flower, or conveying information to potential pollinators that there is nectar or pollen (Dötterl & Vereecken 2010). In general, it can be argued that flowers effectively exploit the sensory biases of insects and other pollinators, and strict coevolution in the sense of co-speciation of plant and pollinator seems to be rather uncommon (Schiestl 2010; see also Amborellales page); although Baguette et al. (2020) mention "asymmetrical coevolutionary dynamics" in the context of sexual deception of its pollinators by Ophrys, the pollinators seem little affected and coevolution is not obvious. Barth (1985) provides a very readable if now somewhat out-dated summary of the interrelationships between insects and flowers; surveys such as that by Vogel (1954) still remain interesting (see Johnson & Westra 2017 for an appraisal of Vogel's work on the South African flora). And it should not be forgotten that there is deceptive pollination in some 10,000 or so angiosperms, their pollinators being attracted by flowers suggesting rewards that they do not provide (Johnson & Schiestl 2016). Finally, it should not be forgotten that pollination, say between bees and flowers, may involve more that the obvious protagonists. Here Steffan et al. (2023) emphasize the importance of microbes for both flower and insect in ensuring that the mutualism was fully effective - pollination relationships may be more complex than they appear to be.
Comments on particularly distinctive pollination mechanisms, or pollination by a particular agent that is common in a group, are frequently made after the family characterizations, for example, when there are oil flowers (Renner & Schaefer 2010), bat pollination (Fleming et al. 2009; Fleming & Kress 2013), or wind pollination (for which, see Niklas 1985; Friedman & Barrett 2008; Renner 2014; Henry et al. 2018). Wind pollination in angiosperms is often associated with monoecy or dioecy, catkinate male inflorescences, single-seeded fruits, etc. (Linder 1998), features not that dissimilar from those that characterize taxa with (hypo)hydrophilous pollination (Du & Wang 2014). For reversals from wind- to insect pollination, see Wragg and Johnson (2011). Seymour (2001) lists taxa in which thermogenic flowers (i.e., with respiratory heat production) have been found (see Onda et al. 2008 for the different systems involved, which may co-exist in a single plant); more thermogenic flowers are turning up. Gottsberger (1977) summarizes what was known about beetle pollination, which he thought was common in basal angiosperms (see also Bernhardt 2000). Parasitic and holomycoheterotrophic plants may have similar pollinators, often being visited variously by flies and fungus gnats (e.g. Vogel 1978a, 1978b). Flowers of many submerged aquatic (Cox & Humphries 1993; Philbrick & Les 1996; Les et al. 1997), parasitic, and holomycoheterotrophic angiosperms may have very distinctive pollination mechanisms and consequently their morphology can be difficult to understand, and this, too, has lead to the plants involved being taxonomically segregated.
Deceit pollination - no particular morphological syndrome, of course - is perhaps surprisingly common, especially in Orchidaceae (e.g. Renner 2006a; Lunau 2006; Ledford 2007; Cozzolino & Widmer 2005; Schiestl 2005; Peakall 2009; Schaefer & Ruxton 2010). The related floral mimicry (Roy & Widmer 1999 for a review; Benitez-Vieyra et al. 2007; esp. S. D. Johnson & Schiestl 2016), in which flowers of one species mimic the flowers of another species, attracting the same pollinators, is not well understood nor easy to categorize in terms of the classic Batesian/Müllerian dichotomy; this feature is probably under-recorded, but there are well-studied examples of Neotropical Orchidaceae-Epidendroideae and Fabaceae-Caesalpinioideae that mimic the distinctive oil-producing flowers of Malpighiaceae (e.g. Papadopulos et al. 2013; de Queiroz et al. 2023).
Although floral syndromes in the sense of distinctive morphologies that are associated with a particular pollinator class have been rather over-advertised, particular plant-pollinator associations can indeed be quite often recognised. Thus flowers in which buzz pollination (sonication) occurs are generally easily recognizable - the corolla, at least, is usually radially symmetrical, often with spreading or recurved petals, there are porose anthers often forming a cone, dry pollen, small pollen grains often with a high protein content, and a punctate/hollow stigma; nectar is often absent, there is often no anther endothecium (see below, Anther Wall), and heteranthy and enantiostyly are common (Teppner 2018: early history; Buchmann 1983; Roubik 1988; Endress 1994; Roulston et al. 2000; Arceo-Gómez et al. 2011; Vallejo-Marín et al. 2010; de Luca & Vallejo-Marín 2013, 2022; Cardinal et al. 2018: evolution of floral sonication in bees; Vallejo-Marín & Russell 2023; Russell et al. 2024). In such flowers pollen is the only/main reward, and this is the only "pollen" syndrome; note that the focus of most pollination literature until 2015, at least, was on flowers that had nectar as a reward (Russell et al. 2015; see Faegri 1986; De Luca & Vallejo-Marín 2013). That being said, buzz pollination occurs in flowers showing considerable variation in the androecium and sometimes also gynoecium, as in Commelinaceae, Melastomataceae, and the Cassia group (Fabaceae), although perhaps rather less so in Solanum. Goldenberg et al. (2008) note the diversity of anther morphologies associated with buzz pollination within Miconia and its immediate relatives; anther characters are not always a good guide to taxon relationships, and buzz pollination itself occurs in flowers that have anthers with a variety of morphologies. Dellinger et al. (2018) found three quite distinct buzz-pollinated morphologies in Melastomataceae-Merianeae, and although they all had porose anthers, other features in which they (and two other syndromes recognized in this group) varied "contradicted traditional syndrome expectations" (ibid. p. 1145), and Diering and Cabrera R. (2022) described buzz pollination in Agalinis (Orobanchaceae) where details of floral morphology also do not match expectations based on pollination type. Indeed, bees have been known to buzz all sorts of flowers, including roses (!: Nevard et al. 2021). Nevard et al. (2021) and Vallejo-Marín et al. (2021/2022) describe various experiments on buzz-pollinated flowers, especially Solanum spp., for instance the former group noting interactions with heteranthy, anthers on longer stamens moving more that do those on shorter stamens, so affecting pollen release, and the latter examining how gluing anthers together affected the process, i.a. it affected the amount of pollen released per visit. Delgado et al. (2023) looked at buzz pollination in the context of flower size; larger flowers had more and larger visitors, but fewer that actually buzzed the flowers, while smaller flowers had fewer and smaller visitors but more that were buzzers. Given the variation in floral morphology of buzz-pollinated flowers, working out the functional reasons for buzz pollination in any one case is not easy (Vallejo-Marín et al. 2021/2022). Nunes et al. (2020/2021) explored the relationship between the fundamental frequencies of the buzzes of different species of bees and the natural frequencies of the vibrations of the anthers of different species of Solanum - the two did not always match. Buchmann and Hurley (1978) suggest a biophysical model for pollen release in sonication; orbicules in the pollen, if present, may be microechinate, simulations suggesting that electrostatic charges at the tips of the spinules help to keep the pollen grains separate (Galati et al. 2019). For more on the mechanics and evolution of buzz pollination, see e.g. Corbet and Huang (2014) and Vallejo-Marín (2019). Perhaps half of all bees can buzz-pollinate, and around 22,000 or more species of plants from some 72 families are pollinated in this way (see e.g. Buchmann 1983; de Luca & Vallejo-Marín 2013; Cardinal et al. 2018; Russell et al. 2024; also Nevard et al. 2021, and especially Commelinaceae, Ericaceae, Fabaceae, Melastomataceae, Orobanchaceae, Primulaceae and Solanaceae.
There is often colour patterning of the corolla/perianth, and this is also discussed monosymmetry below. Simple petal spots are common and are also involved in pollinator attraction; how they develop in Clarkia gracilis has been worked out in some detail (Martins et al. 2012). For floral colour and its evolution, see Rauscher (2008) and Ma et al. (2017b), and for the interaction between pigments and petal structure to produce colour, see van der Kooi et al. (2016).
In addition to obvious colour patterning, details of the micromorphology of the surface of the petals/perianth vary. Individual cells may have distinctive surfaces (e.g. Christensen & Hansen 1998; Wilmsen 2017), and these sometimes depend on the particular petal involved - adaxial, abaxial, etc. (Ojeda et al. 2009), or the whole petal may be thrown into folds (Stirton 1981). Surface micromorphology may affect the colour a pollinator sees, while folds on the petal surface may affect the pollinator's grip on the petal, etc.. Fabaceae show extensive variation in both kinds of surface features.
In a number of taxa the pollinator does not pick up pollen from individual anthers, but from some other part of the flower, a phenomenon known as secondary pollen presentation. Thus pollen may be deposited on petals or styles and that is where it is picked up by the pollinator, or it is forced out of a tube formed by connate anthers or the corolla either by the elongation of the style or mechanically by the activity of the pollinator, or it lands on the pollinator only after bouncing from petal to petal inside the flower (Yeo 1993; Howell et al. 1993; Ladd 1994; Leins 2000; Amorim et al. 2019; El Ottra et al. 2023: esp. Table 1, Fig. 4). Particular secondary pollen presentation devices tend to characterize groups of related genera; overall, such pollination mechanisms have evolved many times and in a number of ways even in fairly closely related taxa (perhaps most notably in Asterales: see Leins & Erbar 2003b). The common mechanisms are brush (pollen presented in hairs on the style, brushed off there from anthers as style elongates), pump (or "noodle squeezer", the anthers forming a tube in which the pollen collects, the elongating stigma-style pushes up through) or the pollen is attached to sticky secretions on the style or other parts of the flower (El Ottra et al. 2023).
A final aspect of pollinator attraction is floral scent, which is produced by various parts of the flower, as in Oleaceae (see Nilsson 2000). Raguso (2008) and Schiestl (2010: note that linalool is not plesiomorphic in flowering plants given the phylogeny shown) surveyed the ecology and evolution of floral scent, which is clearly an integral part of a pollinator's reaction to the flower, just as much as is flower colour, shape, etc. (see also Knudsen et al. 2006 for a general survey), while Pichersky and Raguso (2018) discuss the big picture of terpenoid - that is what most of these attractants are - evolution. Scent composition is not known to be associated with major taxonomic groups of flowering plants, although there may be phylogenetic correlations at lower levels (Steiner et al. 2011) - extensive parallel evolution appears to be the norm (e.g. Johnson & Jürgens 2010; Maia et al. 2012; Jürgens et al. 2013; Kite et al. 2017). Scent is often produced by specialized structures called osmophores, and these are surveyed by Plachno et al. (2010) and Tölke et al. (2019).
Of course, pollinators are not noted for caring deeply about the morphological nature of the parts of the flower that attract them or provide them with nectar, pollen, or other reward. In many cases the inflorescence functions as a single flower (Asteraceae are a good example), or a single flower may appear to be three (e.g. Iridaceae). A few structures that look to all intents and purposes like single flowers, even on close inspection, in fact represent the aggregation of several highly reduced flowers - a good example is Cercidiphyllum. Such extremely reduced floral structures are called pseudanthia (e.g. Claßen-Bockhoff 1990, 1991a: Endress 1994b). The definition in Baczynski and Claßen-Bockhoff (2023: p. 181) is "clearly multiflowered blossoms divided into a central part that serves reproductive functions and peripheral, usually radiating advertising/protective structures consisting of (1) distinctly enlarged, often sterile peripheral flowers and/or (2) showy, coloured extrafloral organs (e.g. bracts, prophylls, stem leaves)". There are all intermediates between this condition and more ordinary inflorescences in species of Viburnum, which have enlarged flowers on the margin of a flat-topped inflorescence all flowers which open more or less together, and a capitulum type common in Asteraceae that is made up of numerous small flowers which open over a period of time but which similarly may be functionally a single unit. However, in both these latter cases individual flowers are perfectly easily recognizable, and in Asteraceae Taraxacum officinale may be a pseudanthium sensu lato, Cichorium intybus a pseudanthium sensu stricto (see especially Claßen-Bockhoff 1990 for images; Baczynski & Claßen-Bockhoff 2023: Table 1). Indeed, there has been a resurgence of interest in pseudanthia, focusing particularly on taxa like Lacandonia (Triuridaceae), Hydatellaceae (Rudall et al. 2009a) and on members of Alismatales (e.g., Rudall 2003b; Buzgo et al. 2006 for literature), although to the extent that what was a flower totally loses evidence of its origin as such, it perhaps would not fit the definition of pseudanthium above... In pseudanthia a group of several to many highly reduced flowers looks like a single flower. "Pseudanthia" sometimes include structures that are part flower, part inflorescence (Rudall & Bateman 2004; Sokoloff et al. 2006). These latter, which may be terminal (Sokoloff et al. 2006), can perhaps be confused with peloric flowers (Buzgo et al. 2006: see below); radially symmetrical terminal flowers in at least some Lamiales seem to represent complex primordia that have not separated (Mayr & Weber 2006). As mentioned, the capitulae of Asteraceae have also sometimes been called pseudanthia (Davis et al. 2008), as have the cyathia of Euphorbiaceae where the distinction between individual flowers is much less obvious. Ultimately, the definition and recognition of pseudanthia can get very tricky and it is not a term to get too excited about. In capitulae of Asteraceae and cyathia of Euphorbia genes that are normally active in flowers are active in the inflorescence, suggesting that these structures are at one level developmental hybrids or intermediates between flowers and inflorescences, whatever that might mean (Ma et al. 2008; Prenner et al. 2011). At another level heterotopy of the genes has occurred.
Self pollination is hindered by sporophytic and gametophytic incompatibility (see below; Ingrouille & Chase 2004), and less effectively by herkogamy, separation in space of stamens and stigma within a flower, and dichogamy, i.e. protandry or protogyny (the latter is the basal condition for flowering plants); see also heterostyly below. However, selfing is quite common in angiosperms, representing a kind of insurance mechanism if cross pollination fails.
Apomixis, in a way an extreme form of selfing, has been much discussed over the years (the term as used may also include vegetative reproduction). Sporophytic apomixis/adventive embryony/nucellar embryony occurs when an embryo forms from nucellar or integumentary tissue, and this is often associated with polyembryony (as in Citrus: for apomixis here, see N. Wang et al. 2022a). Gametophytic apomixis, either diplospory/generative apospory, the embryo developing from an archesporial cell, or apospory/somatic apospory, the embryo arising from some nucellar cell (so this would then seem to be sporophytic apomixis...?), is scattered; pseudogamy, the fusion of a gamete with the polar nuclei to produce endosperm, may also be needed if the whole process is to be successful. Gametophytic apomixis is often associated with polyploidy, and this kind of apomixis in particular has been divided into several "types". Apomixis and the associated lack of recombination can lead to the accumulation of deleterious mutations, Muller's ratchet, although a mere 5% of sexual reproduction counteracts these deleterious genetic effects - and indeed apomixis is often not obligate. Furthermore, if apomixis were obligate, the number of generations of this obligate apomixis (and population size) affects whether or not there is recovery of population fitness when sexual reproduction resumes (in Citrus, Ranunculus: e.g. Hodac et al. 2019; N. Wang et al. 2022a). See also Asker and Jerling (1992), Carman (1997), Hörandl et al. (2007), Hojsgaard et al. (2014), Majeský et al. (2017: gametophytic apomixis), Coughlan et al. (2017), Hörandl (2018: classification of apomicts), papers in Taxon 76(6). 2019, and the database at http://www.apomixis.uni-goettingen.de), for literature; Gustafsson (1947 and references) remains a classic. A number of examples of androgenesis, asexual reproduction via the male nuclear genome, have been recorded (Hedtke & Hillis 2010).
Floral development. The characterizations - and the discussion below - proceed from the outside of the flower in, from the calyx/sepals, to corolla/petals, to androecium/stamens, and finally to gynoecium/carpels, and end up with mention of the stigmatic surface. I do not pretend to even attempt a summary of the genetic/epigenetic control of floral development; see e.g. Causier and Davies (2014) and Thomson et al. (2016) for an entry into the vast literature on this subject. However, there is an increasing amount of work in this area that is of broadly comparative interest, and at least some of these findings are mentioned on the appropriate pages. Aspects of floral development, from the genetic to the gross morphological levels, are integrated into individual characterisations and throughout the hierarchy and are also discussed separately below. Indeed, although much of the subsequent discussion of the flower focuses on the flower at anthesis, it is often important to know how it gets there.
Floral variation is extensive and complex. Here the remarkable studies of floral development made by Payer (1857) and his co-illustrator, a M. Faguet, about whom very little seems to be known (A. Faguet was the illustrator for Baillon in a book on medical botany in 1889), can still be consulted with profit. Interestingly, Payer, a student of Brisseau de Mirbel, claimed to have carried out this work without any preconceived ideas (ibid., p. vii), yet (a historical "yet") as far as I know, it was largely ignored by the anglophone world, which, although often suspicious about any relationship between theory and observation, was perhaps even more suspicious of what the microscope might disclose. The floral diagrams of Eichler (1875-1878) still provide the most comprehensive survey of basic floral organization, and they are also appealing because of their simplicity and clarity. Ronse Decraene (2010) has recently re-emphasized the value of floral diagrams as a way of depicting the arrangement of the parts of the flower and the spatial relationships between them. Such diagrams are usually best made as one dissects a mature flower bud. Obvious variation such as the relative development of the K/C, diplostemony versus obdiplostemony and centrifugal versus centripetal development of the androecium has been incorporated into the characterizations, but other variation, such as the sequence of initiation of the parts of a flower (but see Fabaceae) or of the different members of a single floral whorl, usually has not. I have not grappled with the complexities of floral, particularly carpel, vascularization, although the vascular supply to individual organs is sometimes mentioned in the characterizations and some details of perianth/sepal/petal/tepal vascularization are mentioned - see van Tieghem (1871) for an important early account. Cortical vascular bundles in the flower are mentioned only when they occur (for information, see Ronse Decraene 1992).
In general, the timing of initiation of floral parts follows the outside-in sequence in which they are found in the mature flower: calyx - corolla - androecium - gynoecium, with the primordia, at least those of different whorls, all being separate. However, this acropetal arrangement is not necessarily the order of their initiation, and variation here is summarized by Remizowa (2019, see also Erbar 2010) in a comprehensive survey. Thus the androecium may be initiated before the corolla (Bello et al. 2004 for references) or the two are initiated as common primordia, or the gynoecium is initiated before the corolla, as in many Fabaceae (Prenner & Klitgaard 2008b); see also Sattler (1972), Rudall (2010, 2011) and Wanntorp et al. (2011b and references) for other exceptions. Furthermore, even if the timing of initiation of the whorls is normal, there can be striking variation in the timing of initiation of different members of the one whorl, or of the rates of development of different whorls (Remizowa 2019). Heterochrony, reviewed by P. Li and Johnson (2000) and Buendía-Monreal and Gillmor (2018), can greatly affect this (and other) aspects of floral morphology (generally the focus is on the perianth), and Chinga et al. (2021) even found that heterochronic processes differed in separate parts of the one corolla primordium in Schizanthus. Remizowa (2019) noted that exceptions to the centripetal sequence of initiation of floral parts occurred only if the flower parts were whorled, but not if they were spirally arranged. For variation in phyllotaxis especially in flowers with numerous and small primordia, see Rutishauser (2016b and references). Lacandonia (Triuridaceae) is practically the only angiosperm in which the carpels completely surround and develop before the stamens (see Rudall 2003; Ambrose et al. 2005; esp. Álvarez-Buylla et al. 2010; Endress 2014). However, if the flower of Lacandonia is a pseudanthium this exception may go away, but something like heterotopy is a more likely explanation. Similarities between structures that are apparent only early in development may be found in a wider variety of plants than those that are apparent only later, i.e. "ontogeny recapitulates phylogeny", but of course there are exceptions (e.g. Vasconcelos et al. 2016). For more of floral phyllotaxis, see Walch and Blaise (2022b: basal angiosperms, 2023).
Numbers of stamens, tepals, sepals or petals are mentioned only when they are other than what might be expected from the basic meristicity of the flower - expectations that change depending on where you are in the tree. The number of stamens refers to the number of fertile stamens irrespective of how they developed; staminodes are mentioned separately. For all floral parts, "many" is over fifteen. Numbers of parts for each organ type for a number of families are often summarized as floral formulae that are included in many textbooks. Such formulae can become very complex (Prenner et al. 2010; Simpson 2010; Ronse de Craene et al. 2014; Nuraliev et al. 2019). Floral formulae in these pages summarize only conditions common in a family, and they do not pretend to encompass all the variation found in a family (they are most used at this level). Endress (1990) noted that variation in the number of parts of the androecium in particular was likely when the perianth is absent or the primordia are small.
The relative rate of development of parts in the different floral whorls can be important. In many rosids the petals develop relatively slowly when compared with sepals and stamens, the sepals completely surrounding the rest of the flower in bud, although in Celastraceae, Santalales, and some Malpighiales, for example, it is the corolla that completely encloses the developing flower, the sepals being relatively smaller (Matthews & Endress 2002; Endress 2011), while in other rosids the petals develop noticeably slowly, even for a rosid (see Remizowa 2019 for examples). In asterids, on the other hand, the petals/corolla usually develop notably more quickly than the calyx and surround and protect the androecium and gynoecium of the developing flower (e.g. Ronse Decraene & Smets 1995c; Roels et al. 1997).
As Endress (2005c) emphasized when discussing petals, there are a number of criteria - position, function, development, shape, anatomy, histology, and gene activity, and also relationships to other taxa that clearly have petals - that "make" a petal a petal, so if a structure does not have one of these criteria, is it thereby excluded from petalhood? Or if it does have just one of these features, is it to be included (see also Warner et al. 2009 and literature)? Related to this problem, Maturen et al. (2005) found that floral organ diversity genes (B and C) were expressed in the large, white dogwood (Cornaceae, Cornales) bracts, and Geuten et al. (2006) suggest that heterotopic SEP3-like gene expression - in bracteoles and calyx in extant members - was present in the common ancestor of Balsaminaceae et al. (Ericales) clade. It is very probable that sharply differentiated petals have evolved several times, even if they show similar patterns of gene activity (as in Aristolochia and Arabidopsis - Jaramillo & Kramer 2004; see also Kramer & Irish 1999; Zanis et al. 2003; etc.). Complications also arise in cases where the petals are believed to be modified stamens (e.g. Lauraceae, Caryophyllaceae, for the latter, c.f. Wei & Ronse De Craene 2019)), whether or not these modified stamens are also functional nectaries, as in Ranunculaceae. Such apparent complications are discussed where they occur.
In some classical theories of floral evolution the petals of eudicots at least, if not broad-leaved angiosperms as a whole, are thought to represent sterilized and modified stamens (see also Yoo et al. 2009 for Nymphaeaceae), but Ronse de Craene (e.g. 2006) suggests that in core eudicots they may more often be modified perianth/bract members. Ideas that some flowers may really be pseudanthia (see above), or that evolution of floral parts has been mediated by homeotic changes (e.g. Ronse De Craene 2003; Rudall 2003), further confound our attempts to peg specific terms to the parts of the flower. Furthermore, the general plasticity of perianth parts, especially in members of the ANITA grade, compounds the difficulty of mapping of perianth evolution (for example) on the tree (e.g. Endress 2004; D. Soltis et al. 2005b; Sauquet et al. 2017). Thus Buzgo et al. (2004) in their study of Amborella noted that distinctions between different kinds of floral parts can be hard to make, even the distinction between perianth and prophylls; the numbers of parts and their arrangement also vary here and in other members of the ANITA grade and magnoliids in particular (see also Taylor et al. 2008; Endress 2008a, etc.), and also in unrelated groups like Fabaceae-Detarioideae (Ojeda et al. 2019). Molecular work (Chanderbali et al. 2009, esp. 2010) suggests that genes whose expression is quite tightly linked to particular whorls in eudicots show much less specificity in the Lauraceae and Nymphaeaceae studied (see also the summary in Ronse de Craene & Brockington 2013) and in Nymphaea, at least, whether a perianth member develops as a sepal depends in large part on whether or not it was exposed in bud (Warner et al. 2009). We commonly talk about the evolution of petals because most core eudicots, which are so diverse and on which so much work is being carried out, have them, but what has evolved may be more a sharp distinction between organs that function as sepals alone and those that function as petals alone from organs in which these functions and associated morphologies were not so sharply distinct (see also Chanderbali et al. 2009 and Warner et al. 2009 for somewhat differing developmental perspectives; Ronse de Craene & Brockington 2013). For the vascularization of the perianth in Lauraceae in particular, and its bearing on the evolutionary origin of the perianth, see Sajo et al. (2016), and for older literature on perianth vascularization, often used as evidence for what the perianth members "are", see Puri (1951).
Flower part insertion. Flower parts are most commonly whorled, but they may be spiral or even chaotically arranged (Ronse Decraene & Smets 1998a). The distinction between a whorled and a spirally initiated androecium is not always sharp (Buzgo et al. 2004; Sauquet et al. 2017; Ronse de Craene 2018). Ronse De Craene et al. (2003) surveyed the variation in this character in "basal" angiosperms, where it has often been suggested that spiral insertion is the plesiomorphic condition (see e.g. Sauquet et al. 2017; Sokoloff et al. 2017b; Rümpler & Theißen 2019). Buzgo et al. 2004: Ronse de Craene 2018). Endress (2008b) noted that in ANA-type angiosperms transitions between spiral and whorled arrangements are common, but intermediate types are not, and he emphasized that there can be a spiral sequence in initiation even when floral phyllotaxis is in fact whorled (Endress e.g. 1987a, 2011a; Friis & Endress 1990); Kitazawa and Fujimoto (2018) discuss inter- and infraspecific variation in spiral and whorled initiation of perianth parts in Anemone. Reyes et al. (2018) suggest that spiral phyllotaxis has originated at least 23 times, of which 15 are in the ANA group, the magnoliids, and the basal eudicots. Even in a multistaminate, spiral androecium, the outermost stamens may be initiated in pairs, at least when it comes to timing of initiation (e.g. Ronse Decraene & Smets 1993b). Ronse de Craene (2018) suggested that this might be due to the distance separating the petals, and he also noted that disruption of phyllotactic spirals tended to occur when primordia were small. Multistaminate androecia quite often do not show spiral initiation (Endress 2011a; see also below), while Remizowa (2019) noted that there was no variation in the sequence of initiation when the parts of the flower were initiated spirally, and there was no fusion of parts, either.
Meristicity. Especially when the parts of the flower are whorled, members of the different whorls, particularly the calyx and corolla, commonly also the androecium, and rather less frequently the gynoecium, have the same basic number. However, 2- or 3-carpellate gynoecia in otherwise 4- or 5-merous flowers are common in core eudicots. Meristicity of basal angiosperm clades and the eudicots (but less in core eudicots) is notably labile, and a trimerous perianth - and less frequently androecium - is quite common there (e.g. Kubitzki 1987; Endress 1987; Drinnan et al. 1994; Albert et al. 1998; Soltis et al. 2003; Zanis et al. 2003; P. Soltis et al. 2004; D. Soltis et al. 2005; Doyle & Endress 2011). Monocots are overwhelmingly trimerous in all five floral whorls, unlike the situation in other angiosperms (some Aristolochiaceae and Haloragaceae are close to fully trimerous), so the simplistic distinction (which I still teach) of monocots - overwhelmingly 3-merous flowers; dicots - often 5-merous flowers, needs qualification. Overall, there have been some 25 origins of a pentamerous perianth, along with some 201 reversals ( (Reyes et al. 2018). In many core eudicots there is inter- and even infraspecific variation in meristicity although a particular family may be predominantly either 4- or 5-merous.
Symmetry. Particularly valuable sources of information for the whole suite of characters associated with floral symmetry, whether monosymmetry, polysymmetry or haplomorphy, are Eichler (1875-1878) and the Flora brasiliensis (Martius & others 1840-1906). For general discussion, see also Mair (1977: dicotyledons), Friis and Endress (1990), Tucker (1997, 1999b), Endress (e.g. 1999, 2008a, 2012), Ronse de Craene (2010), Preston and Hileman (2009), Spencer and Kim (2017: esp. genetic control), Pullaiah and Bahadur (2019) and other papers in Bahadur et al. (2019), etc.. Nuraliev et al. (2019) observe that simply calling flowers actinomorphic or zygomorphic seems to be a great oversimplification of the variations of symmetry evident in flowers. However, they also note that some flowers are monosymmetric largely because of morphological constraints that seem to have no functional significance, and in some flowers that are monosymmetric by reduction, "the pollinator apparently does not recognize them as being bilateral" (ibid., p. 21). What the pollinator sees aside, their plea that in ancestral state reconstructions the monolithic zygo-/actinomorphy distinction should be broken down into the individual characters that are varying should be heeded.
Flowers may be monosymmetric (= bilateral, zygomorphic), disymmetric (two main planes of symmetry at right angles), asymmetric (clearly no plane of symmetry, see esp. Endress 2012), haplomorphic, or polysymmetric (= radially symmetrical, actinomorphic - see Neal et al. 1998; Endress 1999). The last two conditions are often lumped together; however, in haplomorphy the flowers only appear to be polysymmetric - they cannot be divided into mirror-image halves because the parts of the flowers are numerous and spirally inserted (e.g. some Magnolia), while polysymmetry refers to situations where there are three or more mirror-image planes of symmetry. The term disymmetric is sometimes use to refer to flowers like those in Brassicaceae. Highly reduced flowers with only one or two stamens (e.g. Peperomia) are necessarily monosymmetric, as is Acorus with its enlarged median abaxial tepal, indeed, many highly-reduced flowers are technically monosymmetric. Monosymmetry is sometimes evident solely in the curvature of the style and anthers/stamens in a more or less horizontally-held flower, as in Agapanthus (Citerne et al. 2010). Similarly, monosymmetry in flowers of Dilleniaceae, Melastomataceae, Commelinaceae and Lecythidaceae may barely involve the corolla at all, just the androecium, although this may be very strongly monosymmetric, and this is the initial condition in Solanaceae, too (J. Zhang et al. 2017). There may also be movement of some of the parts of the flower after it opens making it more or less monosymmetric, an extreme example is Passiflora mucronata (Sazima & Sazima 1978). Furthermore, the stigma/style quite commonly moves relative to the stamens (flexistyly: Raju et al. 2019 and references) as the flowers mature, and such slight monosymmetry these movements may cause is widespread. Naghiloo (2020) discusses the lability in expression of monosymmetry. This ranges from changes in the basic orientation of the flower, i.e. which petal is largest, although the flower is clearly monosymmetric, to more subtle changes where monosymmetry, evident at some stage during development, is not at maturity when the open flower is polysymmetric. These more subtle changes in particular may be of little systematic significance and may be caused by constraints exerted by the developing inflorescence as a whole, or by bracts, neighbouring flowers or organs within a flower (Naghiloo 2020).
The plane of symmetry in monosymmetric flowers is usually vertical, passing through the middle of the adaxial sepal and of the abaxial petal (or vice versa, as in some monocots, Rhododendron, etc.), oblique, passing between the adaxial and adaxial-lateral sepals and the abaxial and abaxial-lateral petals, strongly oblique, passing through the middle of an adaxial-lateral sepal and of an abaxial-lateral petal, or, rarely, transverse, with the plane being at right angles to the median plane of the flower. This last is found in e.g. some Papaveraceae-Fumarioideae, although there at least the flower can become vertically monosymmetric by resupination (Damerval et al. 2013), Vochysiaceae, and Haemodoraceae; similarly, flowers with an oblique plane of symmetry may well appear to the pollinator to have inverted/resupinate monosymmetric flowers, as in Solanaceae (J. Zhang et al. 2017; Bukhari et al. 2017). Indeed, CYC-like genes in Zingiberales and Commelinales are expressed abaxially in the flower, while in eudicots CYC genes are expressed adaxially (Reyes et al. 2016); this difference may be connected with the inverse orientations of the flowers in the two groups. In angiosperms in general the perianth part that is differentiated is the odd member (and sometimes also adjacent members) of the inner whorl (see e.g. Reyes et al. 2016: Fig. 4), Pelargonium being a notable exception. The direction of the plane of monosymmetry in obliquely monosymmetric flowers may vary, even in quite closely related taxa, for instance, whether monosymmetry runs from the odd petal to the odd sepal or vice versa (Ronse Decraene et al. 2002). Flowers with oblique or transverse symmetry are rather sporadic, the former being much more common (c.f. Neal et al. 1998). For a possible connection between monosymmetric flowers and racemose inflorescences, see above.
Rudall and Bateman (2004) surveyed the evolution of monosymmetry in monocots, Citerne et al. (2010) the evolution of symmetry and Reyes et al. (2015, 2016, 2018) the evolution of monosymmetry in angiosperms in general, Bukhari et al. (2017) focus on pentapetalous angiosperms, while O'Meara et al. (2016) examined the evolution of a particular flavour of monosymmetry across all angiosperms. Reyes et al. (e.g. 2018) found that monosymmetry has evolved some 148 times in angiosperms, with perhaps 69 reversals. Naghiloo (2020) emphasized how variable the timing of the origin of monosymmetry in a flower and the extent of its expression could be, the two not necessarily being correlated, and the expression of monosymmetry might also be transient.
For a discussion on the evolution of lobing of monosymmetric flowers, see e.g. Endress (2001). The lobing of the corolla in the monosymmetric and more or less sympetalous flowers of the core asterids is interesting. 2:3 lobing (two corolla lobes make up the adaxial part of the corolla, three make up the abaxial lip) is common in Lamiales in particular (e.g. Weberling 1989; Donoghue et al. 1998; Ree & Donoghue 1999; Donoghue & Ree 2000). 0:5 corolla lobing occurs in Cichorium, for example, which has a particularly distinctive monosymmetric flower since the corolla appears to be split down one side - it can be called split-monosymmetric. Such flowers occurs in a number of Asterales, but also sporadically elsewhere, as in some Lamiaceae, Loranthaceae, Anigozanthus (Haemodoraceae: 0:6), etc. The split-monosymmetric flower of Anigozanthus and other plants like Proteaceae where the whole perianth is involved must necessarily be slightly oblique, this is not so when the corolla alone is involved, as in Asteraceae, Loranthaceae and Lamiaceae.
Substantial infraspecific variation in the lobing pattern of the flowers in Eriastrum eremicum (Polemoniaceae) has been noted (de Groot 2011), and there is infraspecific variation in the occurrence of monosymmetric flowers in Erysimum (Brassicaceae) that is correlated with the identity of the insect that is the predominant pollinator (Gómez & Perfectti 2010). Finally, the marginal flowers of many more or less capitate, umbellate or corymbose inflorescences in Asteraceae, Apiaceae, Caprifoliaceae, and Brassicaceae that are polysymmetric as inflorescences may be more or less monosymmetric, the central flowers polysymmetric (Citerne et al. 2010; see also below).
Patterning of the colour of the flower emphasizes the structural aspects of monosymmetry. Colour patterning is often centred on the median petal, as in the median abaxial petal of many asterid I taxa (e.g. Lamiaceae, Plantaginaceae), and it is scattered in monocots. This position is perhaps connected with ensuring the correct orientation of the incoming pollinator, since the lower part of the visual field is important in shape recognition when the colours have long wavelengths (see Neal et al. 1998). There is variation here. Patterning is centered on the two adaxial petals of the normally-oriented flower of Collinsia (Plantaginaceae, lamiid), which has a very distinctive pollination mechanism for asterids - it has a papilionoid flower. Similar adaxial patterning is found in Rhododendron (Ericaceae: flowers inverted, see below) and Schizanthus (Solanaceae: also inverted and more or less papilionoid) and of course it is widespread in Fabaceae other than Mimosoideae. Patterning also occurs on the adaxial petals alone of some Pelargonium (Geraniaceae), the adaxial petal in several Pontederiaceae (flowers more or less obliquely symmetrical), and the two adaxial inner tepals in Alstroemeria (Alstroemeriaceae: flowers presented inverted). This adaxial patterning may be connected to the fact that in ultraviolet light the upper part of the insect's visual field is most important in the recognition of shape (Neal et al. 1998); do such flowers show u.v. patterning on these upper petals (Faboideae do!)? Monosymmetric flowers are typically held horizontally, and it may be easier for the pollinator to recognize the flower if it is held in this position, and/or it improves pollen transfer, the latter even in polysymmetric flowers (Ushimaru & Hyodo 2005; Fenster et al. 2009). Monosymmetric flowers are often borne in racemose-type inflorescences (Stebbins 1951; see also Prusinkiewicz et al. 2007) - interestingly, in the raceme of a foxglove, for example, which has monosymmetric flowers, polysymmetric peloric flowers are terminal. For links between floral symmetry, position and merosity, see Nakagawa et al. (2020); diversity in floral symmetry is largely regulated by a dorso-ventral inhibitory field (inflorescence axis, bract) and by meristem size. However, Lamiaceae have flowers in cymes; all flowers are terminal and monosymmetric, and there is a similar situation in monocots like Zingiberales, Commelinaceae, etc.. But perhaps these are not functional exceptions, since the main axis bearing the cymose inflorescences is indeterminate and upright while the cymose part-inflorescences are axillary and are held more or less horizontally (see also Robertson 1888a-c; Citerne et al. 2010).
Recent work in monocots has emphasized that taxa like Acorus (Acoraceae), Triglochin (Juncaginaceae), Kupea (Triuridaceae), etc., all with small and apparently undistinguished flowers, are technically monosymmetric (Buzgo 2001; Buzgo et al. 2006; Rudall et al. 2007b). Furthermore, detailed studies of development often suggest symmetries other than those evident in the adult flower, in particular, slight mono- or disymmetry may be evident early in development, even if not in the flower at anthesis (e.g. Sattler 1962: Primulaceae-Theophrastoideae; Olson 2002b: Moringaceae; Ronse de Craene 2005: Batis; Damerval et al. 2013: Papaveraceae-Papaveroideae). It has also been suggested that the flowers of plants like Passiflora and Nigella are functionally monosymmetric, largely because how the pollinator approaches the nectar is restricted (Westerkamp & Claßen-Bockhoff 2007). These authors noted that they had circumscribed the term widely and would consider most nototribe flowers to be monosymmetric, but in Nigella in particular it is hard to see that the behaviour of the pollinator is particularly constrained by the construction of the flower. However, the pollinator approaching the polysymmetric flowers of Iris will see a monosymmetric structure, and here three part-flowers or meranthia make up the flower. Finally, groups of flowers or pseudanthia can form monosymmetric pollination units, examples including the cyathia in the Pedilanthus group of Euphorbia, some Proteaceae, etc. (Westerkamp & Claßen-Bockhoff 2007). Conversely, in Iberis amara (Brassicaceae) monosymmetric flowers contribute to giving a pollinator the impression that the whole inflorescence is functionally a single, polysymmetric flower (Busch & Zachgo 2007) and in poinsettia-type Euphorbia species groups of cyathia and associated inflorescence bracts form a single polysymmetric/haplomorphic floral unit.
The significance of all these observations from the point of view of the involvement of monosymmetry in specific pollination mechanisms and in its very conceptualization and evolution is considerable (Westerkamp & Claßen-Bockhoff 2007). Endress (2008a) emphasized the diversity of monosymmetric flowers and categorized monosymmetry in various ways: Active versus passive, developmentally transient, and monosymmetry by reduction; he had already distinguished between constitutional, reduced and positional monosymmetry (Endress 1999). Monosymmetry is thus another character that has to be discussed with extreme care. For some comparative purposes it may be best to refer separately to each of the floral whorls that is monosymmetric, or to the various separate elements that nake up a particular kind of monosymmetric flower (O'Meara et al. 2016), while for other purposes a gross categorization such as "flowers obviously monosymmetric" may suffice, with highly reduced but ex ipso facto monosymmetric flowers being excluded from this category. From some ecological points of view it may be appropriate to focus on how the inflorescence appears, indeed, it is how the pollinator sees the flower that matters (Rodríguez et al. 2004). Certainly, monosymmetry is not a simple term to define and use, and furthermore it is highly homoplasious by any definition.
There is a large literature on the development of monosymmetric flowers. Reeves and Olmstead (2003) suggested that monosymmetric flowers in different lamiid clades arose in different ways. However, in clearly monosymmetric flowers of independent origin, the same genes may be co-opted in the development of asymmetry. Thus the CYC (Cycloidea) gene seems to have been independently co-opted into the development of monosymmetric flowers within Asteraceae (Chapman et al. 2010), in core eudicots (Preston & Hileman 2009; Citerne et al. 2010; Zhang et al. 2010), and also in Commelinaceae/Zingiberaceae (Preston & Hileman 2012) in monocots (see Hileman 2014a and Reyes et al. 2016 and references). The pattern of expression of CYC-like genes in Ranunculales is notably variable (Jabbour et al. 2014). Genome duplications are sometimes associated with the diversification of CYC genes (Jabbour et al. 2014 and references). For floral symmetry and its genetic control, see also Ma et al. (2017b).
For the systematic distribution and morphological correlates of enantiostyly, that is, the deflection of the style to one side of the floral axis, see Jesson and Barrett (2003); heteranthy and the loss of nectaries are also common in enantiostylous flowers. Pollen is the main reward, buzz pollination (see above) occuring in many enantiostylous taxa (Buchmann 1983; Marazzi & Endress 2008). Since the style, at least, is deflected to one side, enantiostylous flowers such as those of Chamaecrista are more or less asymmetric. Such asymmetric flowers characterize all Cannaceae and Marantaceae; in the latter family the asymmetric flowers are borne in mirror image pairs immediately next to one another. For enantiostyly, see also de Almeida and de Castro (2019).
Floral Orientation. The main variation in the orientation of the flower is whether the median ("odd") sepal, or the median member of the perianth or of the outer tepal whorl, is adaxial or abaxial. The plesiomorphic condition for the angiosperms seems to be to have the median member adaxial, although ascertaining this is complicated by the haplomorphy of the flowers of some of the basal pectinations, while in the monocots the median member is abaxial; this difference is associated with variation in prophyll/bracteole position, i.e. if this/these are absent, the median tepal may switch positions 180 degrees (see also Hofmeister's Rule; Kirchoff 2003 for discussion in the context of Zingiberales).
Spichiger et al. (2005; see also Eichler 1875-1978) suggest that Agave, Tillandsia (but this is a mistake), Allium, Galanthus, Dioscorea, and Lilium all have the median member adaxial, that is, in the reversed position for monocots. Indeed, exceptions to the rule in monocots are very common and are often systematically and biologically interesting, often - but by no means always - being associated with various forms of monosymmetry (see below). Stuetzel and Marx (2005) note the variability of the position of monocot bracteoles/prophylls, perhaps because axillary flowers may in fact represent reduced racemes. For additional discussion of tepal orientation in monocots, see also Eichler (1875), Engler (1888) and Remizowa et al. (2006b); the orientation of the flower may depend on the presence of a prophyll, also on the existence of other foliar structures on the pedicel. De Groot (2011) has found infraspecific variation in floral orientation in Eriastrum eremicum (Polemoniaceae); its developmental basis is unclear.
Inverted monosymmetric flowers may arise in three ways. 1. The distinctive orientation of the flower may be evident from the beginning of development; Bremer et al. (2001) describe such variation in the corolla orientation in monosymmetric flowers of euasterids. 2. Inversion may be secondary, by resupination (see also Dworaczek & Claßen Bockhoff 2016: App. A for list of resupinate taxa). Here the pedicel and/or ovary (when inferior) may twist and the flower becomes resupinate, as in many Orchidaceae, although in some species of Angraecum the pedicel twists 3600 so the flower ends up "normally" oriented and in others the flowers are not resupinate, while in yet others, the degree of resupination depends on where in the inflorescence the flower is borne, all the flowers along the curving inflorescence axis ending up presenting themselves in exactly the same way with resoect to gravity. The corolla itself may twist (Daniel & McDade 2005), as in some Acanthaceae. Finally, the flower may basically just flop over, as appears to happen in Balsaminaceae, for example. There the flowers have rather slender pedicels and most of the mass of the strongly monosymmetric flowers is in the form of a large, spurred, median sepal that is initially on the adaxial side, but in the open flower the sepal + spur is in the abaxial position. The group of monosymmetric flowers is very heterogeneous. 3. The individual flowers may be normally oriented with respect to the axis that bears them, but because of how the inflorescence itself is held, they are presented inverted (or vice versa). Monosymmetric flowers that have become inverted by one of these mechanisms seem to be notably common in monocots. Fischer et al. (2007) discuss the variety of ways - of which twisting of the pedicel is but one mechanism involved - that flowers in the speciose Bulbophyllum present themselves in the Malagasy region.
An epicalyx is of sporadic occurrence, and is mentioned only when it occurs. It origin is various; it may represent modified stipules of the calyx lobes (as perhaps in Rosaceae-Rosoideae), inflorescence bracts (Malvaceae), spines surrounding the flower (Neuradaceae), etc..
The hypanthium is defined here as a disc- or cup-like structure more or less surrounding or borne on top of the gynoecium, but separate from it, and bearing perianth and stamens on its margin. One can think of it as representing receptacular/axial tissue. If the hypanthium has become adnate to the gynoecium over evolutionary time, the latter is simply described as being inferior. Thus I never describe the hypanthium as being adnate to the ovary (see also below, also Gustafsson & Albert 1999). There is indeed often little evidence in groups like core asterids that an ovary has become inferior by the adnation of a hypanthial tube, although some authors do use the term to refer to the outer part of an inferior ovary (e.g. Vrijdaghs et al. 2015). Many monocots have stamens adnate to a tube formed by adnation of the two whorls of the biseriate perianth, the perianth tube (see below); I have not used the term "hypanthium" for this condition because the tube is apparently appendicular in origin (but c.f. e.g. Novikoff & Kazemirska 2012). However, the flowers of Velloziaceae and Hydrocharitaceae may have structures that are more like a "true" hypanthium. The tubes formed by the calyx and corolla in Passifloraceae, some Cucurbitaceae, Cuphea (Lythraceae), etc., do not bear stamens and are referred to as K-C tubes.
A perianth. The term perianth may be used to refer to all the more or less foliaceous structures enveloping the flower. However, a perianth in the strict sense (P in the characterisations here) refers to situations when there is only a single whorl of foliaceous/petal-like structures surrounding the flower and there is no evidence from comparative morphology what they "are". Thus the single whorl in Loranthaceae, Santalaceae, etc., is called a corolla because members of that whorl are interpreted as being equivalent to members of the inner whorl that is made up of petals in other members of Santalales, the calyx being much reduced - see the discussion on the Santalales page. In a bi- or multi-whorled perianth, all parts may be similar and then they are called tepals (T). Very frequently differentiation of the perianth occurs, and a calyx (K), made up of sepals, and corolla (C), made up of petals, are distinguishable. The four petal-like members of the flowers of Proteaceae, each opposite a stamen, are here called perianth, or the flowers could be described as having two whorls of tepals, each of two members. A rather different situation occurs when the parts are all similar, in spirals, and often quite numerous; often the outer members are more or less calyx-like/protective and the inner members are more or less corolla-like/attractive. I describe flowers with this condition as having a perianth, but I mention the fact that a spiral is involved and that some members are sepal-like and some petal-like - Nymphaeaceae are an example. However, in such situations, questions as to what the parts "are" become close to unanswerable.
Differentiation of the sepal/petal function in the perianth has occurred many times (see below under petals), and so the sepals and petals found in e.g. some commelinid monocot flowers and those of a core eudicot flower are equivalent only by designation, as are those in e.g. Saruma (Aristolochiaceae), Papaveraceae and core eudicots. Reyes et al. (2018) found some 44 origins of perianth differentiation in angiosperms, along with around 117 reversals. Many monocots have biseriate petal-like tepals, and in Lilium B-class floral homeotic genes are expressed in the outer whorl alone (Kanno et al. 1999); in eudicots such genes are expressed only in the inner (petal) whorl. Indeed, in general in monocots B-class genes are expressed in the inner tepal whorl, whether or not it is petal-like in morphology. A-class genes tend to be expressed more generally in the flower (Kanno et al. 2003). However, in Commelinaceae only A class genes are expressed in the outer whorl - which is a sepal (Kanno et al. 2004). Even when there are tepals in monocots, members of the two whorls are often somewhat different in morphology.
Ambrose et al. (2000) suggest that flowers in Poaceae can be directly compared with those of core eudicots, with the palea, at least, representing the calyx whorl and the lodicules the corolla whorl. This argument tends to emphasize gene expression, so favouring Remane's criterion of special properties (Remane 1952) over other criteria such as position. However, recent work confirms this general hypothesis, which is made more likely by comparative morphological studies as well (e.g. Whipple et al. 2006) and is largely consistent with the position of Poaceae in commelinids. Nevertheless, the evolutionary and developmental relationships between the arrangement and differentiation of the perianth of monocot and eudicot flowers remains unclear.
The developing flower inside the calyx/enveloping bracteoles is sometimes surrounded by liquid, forming a water calyx (Carlson & Harms 2007) - Spathodea and some other Bignoniaceae also have water calyces (seee also Burck 1910 for other examples and references). Indeed, a variety of other structures in the flower may also secrete water, if in smaller amounts (Burck 1910).
Calyx and corolla aestivation is mentioned only when it is other than imbricate in the strict sense. Thus if there is no mention of valvate or contorted aestivation, or of flowers with open development, it can be assumed that aestivation in the group is predominantly some version of imbricate. However, note that imbricate can also be used when referring to all aestivation types in which the edges of adjacent perianth members overlap one another, and also, for example, buds in which the bud scales are overlapping. In many families with predominantly imbricate (s. str.) aestivation other types also occur. For a survey of aestivation that focuses on the diversity of subtypes within the the aestivation classes mentioned here, see Schoute (1935). Endress (1999) observed that the direction of petal overlap in contorted corollas, i.e., whether left- or right-contorted, in those asterid families with contorted aestivation was usually constant (exceptions are Apocynaceae and Torricelliaceae), whereas in rosids and some Caryophyllales it was usually variable, even in different flowers from the one plant (see also Endress 2001b, 2010c; Diller & Fenster 2014; Sokoloff et al. 2018). In Lamiales and Fabaceae variation in whether the adaxial or abaxial petal(s) of a corolla overlap the others, some form of cochleate (whether descending or ascending) aestivation affords phylogenetically useful distinctions. In general, growth of petals is likely to be a rather precise process (e.g. Rolland-Lagan et al. 2003) given the interaction of flowers and pollinators, perhaps rather more so than leaf growth (Couturier et al. 2011).
Connation. It can be assumed that the calyx and corolla are free unless otherwise mentioned. Reyes et al. (2018) estimated that there have been some 71 origins of corolla fusion and 141 reversals. Erbar and Leins in particular (Erbar 1991; Erbar & Leins 1996b; Leins & Erbar 1997, 2003b; Leins 2000) have emphasized the different ways in which a corolla may become sympetalous - early and late corolla tube formation are the two extreme conditions, but intermediates ("early/late") occur in groups like Acanthaceae, Rubiaceae and Oleaceae (e.g. Vrijdaghs et al. 2015). In late corolla tube formation the corolla tube is formed by the confluence of originally free petal primordia, while in early corolla tube formation the part of the corolla is evident as a ring primordium from early on. In the former petals may lag behind stamen development, while in the latter they grow rapidly and soon cover the stamen primordia (Ronse Decraene et al. 2000). The correlation of early sympetaly with a convex floral axis (itself associated with an inferior ovary) and anthers that are relatively retarded developmentally, as in Rubiaceae, and of late sympetaly with a convex floral axis and relatively retarded petals, was emphasized by Ronse Decraene and Smets (2000). This correlation is not absolute, as Degtjareva and Sokoloff (2012) noted for Utricular (Lentibulariaceae), but it does raise the issue as to what extent the "late" tube initiation is at least partly a consequence of how inferior ovaries in the euasterids develop. Nuraliev et al. (2020) found that in Sciaphila (Triuridaceae), which has a superior ovary, members of the outer tepal whorl showed late sympetaly and members of the inner whorl showed early sympetaly.
Both filaments and petals together may form a tube, each being an integral part of the tube, which is built up of alternating corolla and stamen sectors; such a tube occurs in some Commelinaceae, Convolvulaceae, Diapensiaceae, and perhaps Rubiaceae. Alternating sectors of calyx and corolla together may form a tube, but this is rare in eudicots (e.g. Passifloraceae); however, a rather similar condition where the tube is formed from the tepals of both whorls is quite common in monocots (see above). Indeed, in monocots as a whole there is considerable variation, even between closely related taxa, both in the degree of connation of the tepals and of the adnation of the stamens to the tepals (see also Weberling 1989).
Perianth/sepal/petal/tepal venation (see also above). Sepals in core eudicots are often innervated via a three trace:three gap vascular supply, or the lateral sepal traces come from the petal traces, etc., - "bracteotepals". However, if the sepals are much reduced, there may be either a single trace, or no trace at all, as in some Ericaceae-Ericoideae and Oleaceae. In the reduced flowers of Morus (Moraceae), the perianth members of staminate flowers may have a single trace, those of carpellate flowers, three traces (Bechtel 1921). The sepals of other eudicots and of members of the ANITA grade sometimes have only a single trace (e.g. Glück 1919; von Gumppenberg 1929; Kaussmann 1941; Hiepko 1964a, b; von Balthazar & Endress 2002a). Petals often have a single trace, perhaps reflecting their derivation from stamens, "androtepals", which also have a single trace (e.g. Ronse de Craene 2007, 2008; Sajo et al. 2016 for literature). Interestingly, the single traces of petals in e.g. Campanulaceae represent fused branches from adjacent sepal bundles, while the single traces in many Asteraceae are commissural bundles. The single petal trace often has a complex branching pattern within the blade of the petal. Members of both tepal whorls in monocots commonly have three traces, but sometimes each member has only a single trace - perhaps particularly frequently in Asparagales (Gatin 1920; Kaussmann 1941; Utech e.g. 1984, 1987, and references) and Alismatales.
Another feature that may be of some systematic value is the presence or absence of stomata on the ad- and abaxial surfaces of the perianth members (Stevens 1971; Lipayeva 1989, and references).
Petals. Only distinctive features such as whether or not the petals are clawed, i.e. with a sharply narrowed and more or less elongated basal portion, or ligulate, with more or less petaloid productions on the adaxial surface, are mentioned. Monocots are described as having petals only when the perianth is clearly differentiated into two morphologically distinct whorls, the outer being more or less green and smaller than the inner whorl. The terms corolla or petals are not used to refer to the undifferentiated perianth members of the large flowers of taxa like Agave, Hemerocallis, or Blandfordia, brightly coloured although they may be; these and many other monocots are described as having petal-like tepals.
In a number of taxa there are petaloid outgrowths from the adaxial side of the petals or tepals - these are variously called ligules or coronas. These may be more or less closely associated with stamens, as in some Amaryllidaceae, Gentianaceae and Apocynaceae, or be independent of them, as in some Caryophyllaceae and Erythroxylaceae, and there has been much discussion as to what these structures "are" (see especially Appleton & Kramer 2024a).
Nectaries. Nectar is one important reward for pollinators. Bernadello (2007) provides a useful general survey of floral nectaries with an extensive bibliography (see also Kartashova 1965; Vogel 1977; Smets 1986, esp. 1988; Schmid 1988; Smets & Crescens 1988; Weberling 1989; esp. Erbar 2014: note fig. 183, t. 1); Tölke et al. 2019); Stadler (1886) is a good early study of some very different nectary types, Bonnier (1879) a still earlier survey that includes colleters, etc., while Brown (1938) provides a fairly comprehensive survey. Nectar may secreted by multicellular hairs/trichomatic, or it may be epithelial/in swollen cells that break down, or it may be mesophyllar/exuded via nectarostomata; Vogel (1977), Evert (2006) and Erbar (2014) summarised details of nectary morphology and secretion (see also Lüttge 2013 and green nectaries).
In core eudicots nectar may be secreted from a more or less annular, disc-like structure with nectarostomata through which the nectar emerges; these stomata are unable to regulate their apertures (Tölke et al. 2019). The nectary commonly immediately surrounds the ovary, or it is on top of it if the ovary is inferior. Although "discs" and nectaries are frequently noted in the eudicot characterisations it is by no means certain that all have a similar anatomy, etc. (e.g. see Smets 1986; Vogel 1997). Smets et al. (2003) distinguish between receptacular nectaries, characteristic of rosids, and gynoecial nectaries, typical of asterids; the names refer to the different places where the nectaries are found. There may also be a difference in their vascular supply, the former being supplied from receptacular or androecial traces, the latter by branches from the gynoecial vasculature (see Smets 1988 for a distribution of the main nectary types on a Dahlgrenogram). Nepi (2007) discusses nectary structure and ultrastructure, although without giving details of their vascularization; Frei (1955) described the nature of the vascular tissue supplying nectaries - none, phloem only, or phloem + xylem - but there seems to be no particular systematic signal there. Indeed, whether or not features like nectary vascularisation (as in e.g. Capparaceae, Passifloraceae, Salicaceae, and Cucurbitaceae) and/or the presence of stomata in the epidermis covering the nectary have systematic significance is unclear, and a detailed survey of the anatomy and development of nectaries would be useful (but see Smets 2003; Tölke et al. 2019); nectary vasularization varies at quite low levels (Saxena 1973; de Paula et al. 2011), as do other details of nectary morphology, its position, and nectar composition (Tölke et al. 2018). As mentioned, nectar may also be secreted by hairs on the calyx or corolla or more generally from folds or other tissue on the tepals or petals, from what are clearly modified stamens or parts of stamens, and even from the surface of the gynoecium. Smets et al. (2000) survey monocot nectaries, and Rudall (2002) and Remizowa et al. (2006a) discuss the diversity of septal nectaries, epithelial nectaries in the septal position that occur in many monocots (see also van Tieghem 1875; Daumann 1970; Schmid 1985; van Heel 1988; Vogel 1998b). Septal nectaries seem not to occur when placentation is parietal (Rudall et al. 2005) and of course when the gynoecium is initially apocarpous (it is difficult to have septal nectaries when there are no septae); there is a correlation between the presence of septal nectaries and the occurrence of postgenital fusion of the gynoecium (e.g. van Heel 1988; Remizowa et al. 2006a). Although some broad-leaved angiosperms have cavities in the ovary septae, these are not known to secrete nectar (Ronse Decraene et al. 2000b). For extrafloral and extranuptial nectaries, see above under leaf surface.
I. W. Lin et al. (2014) found that details of sucrose synthesis and secretion was similar in the nectaries of the Brassicaceae and Solanaceae examined (extrastaminal/receptacular and gynoecial respectively), while Solhaug et al. (2019) noted that sucrose might be supplied at least in part directly by the phloem (Nicotiana, Cucurbita) or indirectly via the break down of starch (e.g. Arabidopsis) in the nectary tissues. When it comes to bird pollinators, nectar-eating passerines prefer glucose and fructose over sucrose, but the latter can be readily handled by hummingbirds (Martínez del Rio et al. 1992). The presence of a nectary is noted in the appropriate place in the descriptive sequence of the flower, i.e. proceeding from the outside in; the complete absence of any nectary is noted immediately before the description of the gynoecium. Nectaries are quite frequently lost, and not only in connection with the development of the wind pollination syndrome, but also when there is buzz pollination, enantiostyly (see above), etc..
Note that the CRABS CLAW gene is expressed in both floral and extrafloral nectaries in the few core eudicots studied, and although details of the mode of expression in the two may vary, it would appear not to pay particular attention to differences in floral nectary type (J.-Y. Lee et al. 2005b; see also Fourquin et al. 2007 for the general function of CRABS CLAW orthologs). This gene is not expressed in the extrafloral nectaries of Passiflora (Krosnick et al. 2008a), the nectary spurs in Aquilegia flowers (Lee et al. 2005b), or in the septal nectaries of Asparagus (Nakayama et al. 2010).
Nectar is an ideal growth substrate for yeasts and other microbes and is more than just sugar, varying in the type of sugar, and often containing amino acids, some other compounds perhaps being antimicrobial (Nepi 2014). Vannette et al. (2012, see also Vannette & Fukami 2018) found that yeasts in the nectar of Mimulus aurantiacus had little effect of nectar composition, while the bacteria there reduced nectar pH, total sugar and glucose concentrations, but increased fructose concentrations - hummingbirds dislike fructose, and flowers with increased fructose set fewer seeds. The diversity of bacteria in the nectar of Marcgravia varies depending on the height of the flower in the canopy, being affected by pollinator, but not nectar, flower or inflorescence features, and being highest in mid-canopy flowers (Thiel et al. 2024). This is a little-studied phenomenon.
Little et al. (2014) and von Aderkas et al. (2014) discuss the composition of the nectar-like pollination droplet of gymnosperms. Nectar composition in angiosperms tends to be linked with particular classes of floral visitors, see Baker et al. (1973, 1998), Abrahamczyk et al. (2016b), Tölke et al. (2019), etc.; Parachnowitsch et al. (2018), Vandlook et al. (2019) and others discuss the evolution of nectar amount and composition. Quite often nectar contains defensive secondary compounds, e.g. in Asclepias, and P. L. Jones and Agrawal (2016) summarize the various suggestions that have been made as to how this might benefit the plant. Stevenson (2020, see also Fattorini et al. 2023) also tackle this issue, which is not straightforward. Thus caffeine, a purine alkaloid, is toxic to invertebrates, but as Stevenson (2020: p. 606) observed, "bees fed caffeine at ecologically relevant concentrations during a learning experiment were three times more likely to recall a trait associated with a food reward than bees fed a control diet".
Pollen is the other major reward, although there is clearly a tradeoff here, pollen used by the pollinator is so much pollen unavailable for pollination; Roulston and Cane (2000) discuss the kinds of rewards abtained from pollen, and how the pollinators access these rewards. Of course some floral visitors are pollen thieves, being incapable of pollination, and these include thrips, one of the few organisms able to pierce the walls of pollen grains (Roulston & Cane 2000). Pollen is sometimes collected by bees as they "buzz" the flower, leading to the distinctive buzz-pollination floral syndrome; the pollen grains are often small and protein-rich (for buzz pollination see also enantiostyly above: Buchmann 1983; Roulston 2000; Harter et al. 2002; Teppner 2005). For odours produced by pollen, mostly coming from the pollenkitt, perhaps involved in local-scale defence against pollen predators and also attracting pollinators, see Dobson and Bergström (2000).
There are other rewards, too. Pseudopollen is sometimes produced, as in Theaceae, although its function is poorly understood. Male euglossine bees, among others, may visit flowers for their fragrances (for euglossine bees, see e.g. Ramírez et al. 2002). Flowers that produce oils as a reward are relatively uncommon and tend to be rather restricted in their taxonomic distribution (e.g. Vogel 1974, 1986, 1990; Buchmann 1987; Renner & Schaefer 2010; Possobom & Machado 2017a and references); see Neff & Simpson 1981 for oil-collecting bees). Interestingly, oil in a flower is not infrequently contained in two separate spurs (e.g. Vogel 1984), the oil then being collected by both forelegs of the pollinator (see also Pauw 2006 for similar morphologies within Orchidaceae - Coryciinae). Plants produce oil in epithelial or in unicellular (monocots) or multicellular trichomatous elaiophores (Vogel 1974; Possobom & Machado 2017a; Tölke et al. 2019). Not uncommonly, especially in Orchidaceae, flowers may lack rewards (Renner 2006a for a review), although it is uncommon for the pollinator to leave the flower without some gratification, even in deceit pollination.
Stamen development and position. The stamens may all be free, more or less connate, or in obvious groups or fascicles, members of which may be connate (and then phalangiate) or not. The usual condition in many core eudicot groups is for there to be twice as many stamens as petals, and these stamens are borne in two whorls. The outer (antesepalous) whorl is normally initiated before the inner (antepetalous) whorl, the condition of diplostemony. However, in obdiplostemony (see Eckert 1966) the stamens of the antepetalline whorl appear to be outside the stamens of the antesepalline whorl. Diplostemony is the by far the most common condition, and only obdiplostemony is noted specifically in the descriptions. (I also note an associated feature, the arrangement of the carpels.) If the stamens are equal in number only to the sepals or outer perianth whorl, they may be opposite (haplostemony) or alternate with them, in the latter case being opposite to the inner whorl of the perianth or petals (obhaplostemonous). Ronse Decraene and Smets (1995a) suggest that other terms should be used to describe such features in monocots, while Bachelier and Endress (2009; see also Endress 2010d for a good discussion) have perhaps unfortunately redefined obdiplostemony, suggesting that in obdiplostemonous flowers the important feature is that the carpels are opposite the petals (see also below under carpel arrangement); the term cannot then be used when there are ten stamens but only three carpels. Be that as it may, obdiplostemonous androecia develop in a variety of ways (Hardy & Stevenson 2000b), and are quite common in rosids in particular perhaps because of the relatively delayed development of the petals there relative to that of sepals and stamens (Ronse Decraene & Smets 1995c; Roels et al. 1997). Ronse De Craene and Bull-Hereñu (2016: see Table 1) provide a recent review of the various flavours of obdiplostemony, noting that the term can be used even when there are no petals, as in Cephalotus.
When there are many stamens, i.e. the androecium is polyandrous or polymerous, and the primordia are separate, the sequence of initiation is commonly centripetal, especially in the ANITA grade and magnoliids, and this (= simple polyandry) seems to be the plesiomorphic condition for angiosperms. However, in a number of eudicots initiation may be in the opposite direction, being centrifugal (e.g. Corner 1946b, see Rudall 2010 for an assessment of Corner's work), a derived condition and common in taxa with fasciculate androecia. Details of how centrifugal/fasciculate androecia (= complex polyandry, see Remizowa 2019) develop vary considerably (see esp. Corner 1946b; also e.g. Hirmer 1917; Pauzé & Sattler 1978; Stebbins 1974; Weberling 1989; Leins 1979, 2000 and references; Prenner et al. 2008a; Rudall 2011; Erbar 2010, esp. Fig. 11), and in some taxa with secondarily numerous stamens the distinction between centrifugal and centripetal initiation may be unclear (e.g. Hufford 1990). Androecia with numerous stamens are relatively uncommon in monocots (see Kocyan 2007 for a summary; Nadot et al. 2011: palms, many stamens have evolved here several times). A number of taxa with secondarily numerous stamens initially have only five or ten primordia, in the former case, the primordia are often antepetalous and numerous individual stamen primordia then develop on these initial primordia. A number of taxa with secondarily numerous stamens initially have only five or ten primordia, in the former case, the primordia are often antipetalline and the stamens themselves may be more or less connate or in fascicles (see esp. Corner 1946b; also Hirmer 1917; Pauzé & Sattler 1978; Stebbins 1974; Weberling 1989 and references). Stamens may also develop from a single ring primordium on which individual stamens are initiated (e.g. Ronse Decraene 1988; Ronse De Craene & Smets 1987). The androecium of Ricinus (Euphorbiaceae), with its distinctive branched stamens, has sometimes been interpreted as being cauline, but it is probably a modification of a fasciculate androecium (Prenner et al. 2008a). There may be variation in both mode of initiation and direction of development between quite closely related taxa, as within Loasaceae and Hydrangeaceae (e.g. Hufford 1990; Ge et al. 2007), while in Aquilegia initiation of the stamens is centripetal and their maturation centrifugal (see Remizowa 2019).
Other patterns of stamen development have been much commented on. Thus the stamens in some Piperales and Alismatales (for example) may be initiated in pairs and in Hydrangeaceae-Hydrangeae as triplets associated with individual perianth members. Ronse Decraene and Smets (1996) distinguished between two kinds of stamen pairs, one associated with the process of reduction in number of stamens, the other with an increase in number, dédoublement, a term unfortunately freighted with much historical baggage and of little value (see Ronse Decraene & Smets 1993b for early literature on dédoublement; Wanntorp et al. 2011 for stamen doubling). By the criteria used by Ronse Decraene and Smets (1996), Caryophyllales vary in this feature, as do rosids as a whole.
Stamens within a single flower may be of different lengths, and this is commonly seen when comparing members of the two stamen whorls, although the differences are often only slight. The androecium in Brassicaceae is tetradynamous, with four long and two short stamens, Lamiales with only four stamens are commonly didynamous, with two long and two short stamens, and here the anthers of the stamen pairs are often connivent (see also Caprifoliaceae-Morinoideae, although the anthers there are not connivent). In some Polemoniaceae each of the five stamens of the single whorl may be of different lengths and inserted at different heights on the corolla tube (see also Loranthaceae). The term heteranthy refers to more substantial within-flower variation in stamen morphology, the stamen types often also differing in anther morphology and the morphology and fertility of the pollen that they produce, where they place the pollen on the body of the pollinator, whether or not they have stomata (absence of stomata tends to retard anther dehiscence), etc. (Paulino et al. 2016; Papaj et al. 2017; Saab et al. 2021 for a nice example). Heteranthy is notably common in families such as Commelinaceae, Melastomataceae and Fabaceae (Vallejo-Marín et al. 2010), however, its recognition is not straightforward (e.g. Peach & Mazer 2019; Dieringer & Cabrera R. 2022).
Recent work emphasizes movement of stamens during the lifetime of the flower. "Triggering" of the flower by the pollinator, as in some Loranthaceae, Stylidiaceae, Marantaceae, etc., has been known for some time, and helps explain the complex morphologies of the flowers involved, but it is also clear that movement of some sort, sometimes more subtle, of the style and/or stamens is quite widespread, e.g. M.-X. Ren (2010), Ren and Bu (2014) and Mittelbach et al. (2019) and references.
Stamen fusion. Ren (2008) noted that some sort of connation of the stamens is widespread. Anther connation is more common in asterids and filament connation in rosids, etc., although Campanulaceae-Lobelioideae, Calyceraceae (both Asterales), etc., have more or less connate filaments. The degree of connation of filaments and/or anthers also varies considerably, as in Campanulaceae, where variation is of systematic and floral biological interest; all Asteraceae (apart from wind-pollinated members) have connate anthers and free filaments, while the reverse situation occurs in their sister taxa, Calyceraceae. Connation may be incomplete, as in some Fabaceae-Faboideae where nine filaments are connate and one free (this allows access to the nectar). Some Hydrangeaceae and Styracaceae have flattened but more or less free filaments that form a tube, and in Humiriaceae interdigitating hairs from adjacent filaments help to form the tube. Buzz-pollinated taxa may have the anthers more or less tightly appressed to each other or connate, and forming a cone around the style-stigma. Finally, in Acanthaceae-Ruellieae more or less connate filaments that are also adnate to the corolla form a tube within which the nectar is found (Mantkilow 2000). Stamens are usually adnate to the corolla only when the latter is sympetalous, but not all sympetalous taxa have stamens adnate to the corolla (e.g. Ericaceae and a number of other Ericales), some monocots with free tepals have stamens adnate to those tepals, and a few asterids (e.g. some Convolvulaceae, Diapensiaceae) have stamens adnate to otherwise free petals, the resulting tube being a composite structure, filament alternating with petal. Obviously, fusion in both connation and adnation varies from congenital to postgenital. For the position of insertion of the stamens relative to the gynoecium, see Ovary Position below.
In a number of monocots, features like adnation of stamens to the tepals, common stamen-tepal primordia, and arrangement of the tepals and stamens become connected. Here, although much less frequently in the commelinids than elsewhere, each of the six stamens is borne opposite a tepal, and the bases of the two tepal whorls do not each separately completely surround the flower. Here, unlike the situation in broad-leaved angiosperms, a stamen may be strongly adnate to each petal-like tepal of both whorls, both when each tepal is more or less free (Androcymbium [Colchicaceae] is a particularly striking example - see also Endress 1995b) and even when the tepals form a tube. The result is often a flower that is functionally (from the point of view of the pollinator) six-merous, although of course monocots are generally thought of as having three-merous flowers. Posluszny et al. (2000) discuss such a perianth-androecium module in the context of the floral evolution of Alismatales (see also Endress 1995b in particular; Buzgo 2001; c.f. Rudall 2003), and I have (perhaps rather uncritically) applied a similar idea to non-commelinid monocots in their entirety and to some magnoliids. In some of these Alismatales the stamens have a small, abaxial, basal scale; this is interpreted here as a reduced tepal.
Endress (1995b, Fig. 6) described petals and stamens arising from a common primordium in Zingiberaceae (as also occurs in some groups of core eudicots, e.g. Primulaceae-Myrsinoideae and their relatives: see Ronse Decraene et al. 1993 for a summary; de Laet et al. 1995 for discussion; Ronse de Craene 2018), but this is a different situation. Here the perianth is completely biseriate, the outer (calycine) and inner (corolline) whorls successively completely surrounding the apex, unlike the condition that is suggested to be the plesiomorphic condition in monocots. Further complications occur in Acorales, some Alismatales and perhaps Piperales. There the slightly enlarged median (abaxial) tepal of the outer whorl encloses the young flower; it looks as if there is a composite structure made up of bract + tepal (Buzgo 2001), so being an organ of "hybrid" nature (Bateman et al. 2006b); Ronse deCraene (2010) interprets it as a bract, one tepal being missing. Such flowers can be described as monosymmetric (see above).
Stamen morphology is very variable, and only some of this variation is mentioned below. Hufford and Endress (1989) and Endress and Stumpf (1990, 1991) provide invaluable recent surveys of stamen morphology, Endress and Stumpf (1990) focusing on stamens that are other than tetrasporangiate; Wilson (1942), Dahlgren et al. (1985), Endress (1994b), and others also summarize variation.
Walker-Larsen and Harder (2000) review staminodes and their phylogeny (see also Ronse Decraene & Smets 2001b - lots of s.e.ms). Staminodes vary morphologically from structures that appear to be functional stamens but produce non-functional pollen to minute and strictly rudimentary structures; they may also be very unlike stamens, being complex and petal-like (especially in some Zingiberales) or nectar-secreting (Ranunculaceae) structures. The degree of development of staminodes, whether as members of androecial whorls that include perfect atamens in perfect flowers, as in Lamiales (e.g. Bignoniaceae, Plantaginaceae, Calceolariaceae, etc.: Endress 1998; C. F. Song et al. 2009: molecular control), or as complete whorls of staminodes in perfect flowers, or in carpellate flowers of monoecious or dioecious taxa, can vary considerably within a family (e.g. Appleton & Kramer 2024), although some families consistently never have staminodes. Furthermore, staminodes in different whorls in the same flower may have demonstrably different origins. Thus the oppositipetalous staminodes of female flowers of Paronychia (Caryophyllaceae) are modified filaments while the oppositsepalous staminodes are much-reduced, non-functional antherodes (Schenk & Appleton 2023).
Filaments are usually free and slender, however, rather stout, flattened filaments is the plesiomorphic condition for angiosperms, or filaments can be petaloid or with various appendages, etc.; Almeida et al. (2014) discuss control of flattening in filaments. There is usually a single vascular bundle in the filament, but there are three in many Magnoliales, three traces in stamens of Lauraceae that have basal glands (Sajo et al. 2016), or the single bundle may be branched, as in the complex stamens of many Melastomataceae.
The relationship between the sporogenous tissues of the anther and the supporting tissue of the filament, the connective, provides a further useful suite of characters. The stamens may be laminar, with the anthers more or less embedded in one surface (as in many magnoliids), or they may be stout, with little distinction between the anther with its well-developed connective and the filament (in most Ranunculales, see also Rousseaceae, etc.), or the filament may be quite narrow and be attached to the base of the anther, i.e., it is basifixed. The actual point of connection may be further more or less narrowed (Nothofagaceae), or hardly narrowed, although the base of the anther thecae may still be quite distinct from the filament (e.g. Pittosporaceae, Escalloniaceae, etc.), or the filament may join the anther in what appears to be a basal pit (esp. in Saxifragales). In general in core eudicots, the anther/filament junction is often more or less dorsal (dorsifixed). Finally, Rudall (2001b) summarizes the distribution of centrifixed anthers in which the slender filament tip is inserted into a hollow in the anther in monocots (c.f. Saxifragales above). It can be very difficult to distinguish clearly between these various "types" of stamens, and my treatment of this set of features leaves something to be desired. The connective may also be distinctly prolonged, often a systematically valuable feature.
Stamens have a basically diplopyllous structure, that is, they have more or less separate ad- and abaxial parts (Baum & Leinfellner 1953). Anthers are usually tetrasporangiate, with sporangia parallel and in pairs forming thecae. The paired sporangia of a theca dehisce via a single slit they have in common, i.e. they are synangia (c.f. Green 1980, for terminology). They are sometimes bisporangiate, in which case it is the two sporangia of a single theca that are usually lost, the stamens then being unithecate (see Weberling 1989; Endress & Stumpf 1990). Anthers vary in length (c.f. Achariaceae and Salicaceae), and the thecae can be laterally or apically confluent, alternatively, the sporangia can be quite separate (Lauraceae), superposed or not, in part sterilized, etc. (see Trapp 1956a, b, for Lamiales in particular). "Polysporangiate" or septate anthers - basically, anthers in which the four sporangia have become divided, rather than there being numerous independent sporangia - are scattered in the broad-leaved angiosperms in particular; the walls of the sporangial units may develop from the tapetum or from parenchymatous cells, even being vascularized (e.g. Lersten 1971; Endress & Stumpf 1990; ).
Details of anther dehiscence yield an important set of characters. Anthers are usually introrse, opening internally, but in a number of taxa they are extrorse, perhaps plesiomorphic for angiosperms; there is variation in this in the different anther whorls of a single flower in Lauraceae. As mentioned, each theca normally opens separatelyby longitudinal slits, less frequently by slits common to the two thecae, the thecae then being apically confluent, or by slits down each sporangium. The arrangement of the paired thecae varies; they may be in parallel, head to head, or even V-shaped. Dehiscence may be by flaps (valvate) or pores (porose), or each sporangium may open separately. Porose anthers, or pollen coming out the top of a cone formed by all the anthers, are common in buzz-pollinated plants. Only the uncommon conditions are mentioned.
Anther wall. The anatomy of the anther wall shows much variation, some connected with how the anther dehisces. There is variation in endothecial development, the endothecium normally being a single hypodermal layer of cells with distinctive thickening that is involved in anther dehiscence. Both secondary parietal cell layers (products of periclinal divisions of the primary parietal cells, themselves the product of the first division of the archesporial cells) of the anther wall normally divide further ("basic type" of wall development), or the inner cell may remain undivided (the "dicot type"), the outer divides, or the reverse occurs, in which case the endothecium develops directly from undivided outer secondary parietal cells (the "monocot type"), and there is also a "reduced type" (Davis 1966; Marchant & Walbot 2022). Sampling of this character is poor, there can be considerable infrafamilial variation, and the typology is questionable, the dicot type seemingly being particularly poorly understood (Hermann & Palser 2000; Tsou & Johnson 2003; Marchant & Walbot 2022: useful summary: see also Rudall & Furness 1997; Carrizo García 2003 for observations). I have not described or analysed variation concerning the extent of the mature endothecium and endothecium-like tissue in any detail; Chatin (1870), Hufford and Endress (1989) and Endress and Stumpf (1991) in particular provide much information on these features. Endress and Stumpf (1991) note a correlation in eudicots, especially in the rosid area, between the development of endothecial-like cells around the connective when the latter is well developed, and around the individual thecae when the connective is less well developed. Individual taxa like Haptanthus and Styloceras (Buxaceae) show massive development of the endothecium (Doust & Stevens 2005; Shipunov & Oskolski 2011). There is also much of interest in details of the elongation of the endothecial cells relative to the long axis of the anther and in the thickenings of endothecial cells (e.g. Noel 1983; Manning 1996), but these, too, are not often mentioned below; depending on the group, there may (e.g. Manning & Goldblatt 1990) or may not (e.g. French 1986) be information of systematic interest, and the patterns of thickening are difficult to describe and categorize. In porose anthers that have lost their endothecium, a condition that is quite common in eudicots but is decidedly uncommon in monocots (Tebbitt & MacIver 1999: porose anthers with endothecium; Gerenday & French 1988: monocots; Hardy & Stevenson 2000b: wall development and buzz pollination in Commelinaceae), epidermal cells are often notably thick walled and form an exothecium. Some monocots that do not have porose anthers may still lack an endothecium (Johri et al. 1992). An exothecium is also present in the anthers of many gymnosperms.
A number of asterid I families, especially in Lamiales and Solanales, have placentoids, a parenchymatous outgrowth of the connective into the anther loculi (Hartl 1964; Endress & Stumpf 1990: also some Caesalpinioideae, Cannaceae, Zingiberaceae, etc.). The detailed distribution of this character is unclear.
The tapetum is usually glandular (also called secretory or parietal), with separate cells, and less commonly syncytial (also called plasmodial or invasive), forming a syncytium, this latter condition being most frequent in monocots (Furness & Rudall 1998, 2001b). For general surveys, see Pacini et al. (1985, 2009), Pacini and Franchi (1991) and Gotelli et al. (2023: emphasis on ultrastructure), and for fifteen keys analysing different aspects of tapetal development, see Pacini (1997). Furness (2008a) suggests that there may be a distinction between amoeboid and invasive tapeta (see also Pacinoi & Franchi 1991), but it is not easy to distinguish between these in much of the literature, although Galati et al. (2007) described an invasive, non-syncytial tapetum in Modiolastrum (Malvaceae) and similarly Gotelli et al. (2023) note that in taxa like Cichorium intybus (Asteraceae) the tapetum is invasive, but the walls do not break down. The three terms used here are in bold above. The number of nuclei in tapetal cells varies from 1 to 6 or more and there may also be nuclear fusion; I have not handled this character well. The common situation seems for the tapetal cells to be binucleate, although some cells may be uninucleate. Wunderlich (1954) summarises information on this character; there is both much variation within families and also differences between observers. Wunderlich (1954) also noted extensive variation in the ploidy level of the tapetal cells.
Microspore mother cells usually form a more or less massive block of cells in the center of the sporangia. There are other arrangements, for instance, the sporogenous cells are sometimes in separate packets and the mature anther is then locellate (Judkevich et al. 2020b and references - sometimes called polysporangiate). Variation in how individual pollen grains in a loculus contact the tapetum, e.g. all are in contact, not all are in contact (Pacini 2009), may be of systematic significance (e.g. Kirpes et al. 1996; Kimoto & Tobe 2008), but the details of such variation across angiosperms are hard to acquire.
Data for variation in microsporogenesis are taken in part from G. Dahlgren (1991), Johri et al. (1992) and Nadot et al. (2008). In simultaneous microsporogenesis the microspores initially form tetrahedral tetrads and wall formation is centripetal, although there is a considerable amount of variation here (Nadot et al. 2008; Furness 2011). There is less variation shown in successive microsporogenesis (common, but not universal in the monocots - see esp. Stenar 1925; Furness & Rudall 2000a, 2001b; Furness 2008b). There the microspores are initially in linear tetrads, but these become tetragonal, and wall formation is centrifugal. There are other correlations, too - monolete spores, successive sporogenesis, trilete spores, simultaneous sporogeneisis (Blackmore et al. 2012 ans references). However, Sannier et al. (2007) find such correlations not to be that strong in angiosperms. Indeed, Konta and Tsuji (1982) had earlier found all possible arrangements of cells in pollen tetrads in Japanese orchids, there being variation within a single pollinium, although linear and T-shaped tetrads were least common. The occurrence of simultaneous microsporogenesis in monocots is correlated with that of trichotomosulcate pollen (Rudall et al. 1997; see also Blackmore et al. 2012), however, Furness et al. (2002b) caution against being overly typological when describing microsporogenesis. Schols et al. (2005) note that aperture morphology and microsporogenesis are not necessarily linked, as was confirmed by Sannier et al. (2006), who also observed infraspecific variation in microsporogenesis. See also immediately below for aperture development.
Attention has long been paid to variation in pollen and spore morphology details of which have been much used as important indicators of relationships. However, as Walker and Doyle (1975: p. 677) noted, "probably no other palynological character has been responsible for so much terminological confusion as pollen wall morphology". Thus although the term ektexine as originally defined (Erdtman 1943) was more or less synonymous with sexine, it is now invariably used in the redefined sense of Faegri (1956; see also Faegri & Iversen 1964). Unlike ektexine, sexine does not include the foot layer. Sexine and nexine are distinguished on purely morphological criteria, whereas ektexine and endexine differ in their staining properties, so the two sets of terms are therefore suited for slightly different applications. For a convenient glossary of pollen and spore terminology, which at times seems to be in a separate world, see Reitsma (1970a), Punt et al. (2006) and especially Halbritter et al. (2018). Many palynologists have described variation in pollen morphology in terms of types, but this effectively obscures variation. Thus Doyle (2009) summarises much of the literature on morphological variation of the infratectum, but the distinction between granular and columellar, the two main infratectum "types", can be less than clear. Several pollen characters refer to states that are subdivisions of continua, and although these states may have been in the literature a long time, this is hardly justification for their continued use in phylogenetic studies. In short, this area is almost a showcase for the problems that can be encountered when thinking of variation in the context of phylogeny when the terms used to describe the variation may have been coined for quite other purposes (see the Introduction for more discussion). For an online database of images of the pollen of over 2,700 species, see Weber and Ulrich (2017) - PalDat 3.0.
Here I refer consistently to the number and nature of the germination pores, or to their absence, and the number of endoapertures per ectoaperture (e.g. Verbeek-Reuvers 1976). For the development of tricolpate pollen, which follows Garside's rule in those "basal" angiosperms with such grains and usually Fischer's rule in eudicots, see Banks et al. (2010); microsporogenesis in the former is successive and in the latter, simultaneous. Pantocolporate or pantoporate grains have apertures all over the surface (see Prieu et al. 2017, 2019 for pantoporate pollen), zona-aperturate grains have a single, encircling aperture (Hesse & Zetter 2005), while in spiraperturate grains, known from both monocots and Pentapetalae, the aperture(s) are variously convoluted (e.g. Furness 1985). There seems to be some confusion as to whether pollen is porate or pororate, the latter having ecto- and endoapertures of different sizes, while in the former they are similar (Basak et al. 2023). Although most monocot families have mono(ana)sulcate grains, as do some magnoliids, etc., details of the developmental pathways of such grains may vary (Penet et al. 2005), and monocot families often have pollen with other morphologies as well, although I rarely mention these in the characterisations unless they are common within a clade. If there is a single point of germination in the pollen grain, this is usually at the distal pole, but there may be a few exceptions (Hesse et al. 2009a; Albert et al. 2010; Halbritter et al. 2012). However, the situation in Annona, one of the genera suspected of germinating at the proximal pole, is complicated, since the individual grains of the pollen tetrad rotate during development, so making the distal pole difficult to recognize (Lora et al. 2009b for references). Harley (2004) reviewed monocot pollen grains that have three apertures, while Ressayre et al. (2002) discussed aperture diversity in the context of pollen development - this diversity, at least when aperture numbers are low, is due largely to variation of what goes on during meiosis (see also Matomoro-Vidal et al. 2012). Operculate pollen is scattered (Furness & Rudall 2003).
Inaperturate pollen grains - in many cases, e.g. Araceae, perhaps more properly referred to as omniaperturate grains - are scattered in monocots in particular, where they characterize some families and Zingiberales as a whole (e.g. Furness & Rudall 1999, 2000b, 2001b); for a survey of inaperturate pollen in eudicots, see Furness (2007). Such pollen grains often lack exine, so are not resistant to acetolysis. Interestingly, omniapertuate pollen germination is quite common in Brassicaceae, even in species with tricolporate, and therefore apparently triaperturate, grains, although such germination is not often consistent within a species (Edlund et al. 2016). For pollen germination in general, see Heslop-Harrison (1987).
Details of pollen microstructure, whether visible under S.E.M. or T.E.M., are mentioned only inconsistently. Heslop-Harrison (1968) provides a still useful account of pollen wall development, while Harley and Zavada (2000) attempt to think of pollen variation in monocots as a whole in the context of phylogenetic analyses, Blackmore et al. (2009) decompose the pollen "types" of Asteraceae into a series of independent characters, and Mander et al. (2013) outline a quantitative morphometric analysis of some grass pollen grains in an approach which clearly has a lot of potential. Wortley and collaborators (e.g. Wortley et al. 2015) are involved in a major attempt to link phylogeny and pollen variation, although they clearly face major problems at several levels. As mentioned a couple of paragraphs above, the states of a number of characters are divisions of continua of variation, but that aside, Wortley et al. (2015) and some others have been fairly exploratory in their analysis. Thus they treated infrataxon variation in character states in different ways and also optimised characters using different methods, with the result that the one character state changes at different places on the tree depending on how the analysis was carried out (see also e.g. Lu et al. 2015; Luo et al. 2015; Jiang et al. 2019; L. E. Yang et al. 2020)... Endexine variation needs attention. In gymnosperms and at least some angiosperms it is lamellate (e.g. some Annonaceae, Acoraceae) or compact; it is usually absent in monocots, but it is present and spongy in Araceae (M. Weber et al. 1999; Weber & Ulrich 2010).
Despite the importance of pollen grains both for the plant and the taxonomist, rather little is known about how sporopollenin forms the incredibly diverse morphologies that characterize pollen grains (see Dobritsa 2011 for information; F.-S. Li et al. 2018 for sporopollenin). However, there is growing evidence that there are both sporophytic and gametophytic controls of the development of pollen and spore walls, and that self-assembly/self organization also plays an important role (e.g. Gabarayeva & Hemsley 2006; Blackmore et al. 2007; Gabarayeva & Grigorjeva 2010, 2016; Polevova et al. 2023; Gabarayeva et al. 2018 2023). There are truly remarkable similarities between the structures produced by the experiments in Gabarayeva et al. (2019) and the structure of the walls of actual pollen grains. Blackmore et al. (2010) discuss pollen development in Asteraceae, and show how self-assembly of many pollen features is common, but that changes in the glycocalyx, the primexine matrix and made up of glycoproteins, and in pH, etc., affect details of this self assembly, and some of this more proximate variation is probably under genetic control. The tetrad stage of pollen development seems to be particularly important, with many of the main features of the exine of the mature grains first appearing then - although little sporopollenin in produced by the tetrad, tapetum-derived sporopollenin being incorporated later (Grigorjeva & Gabarayeva 2018). Gabarayeva et al. (2021) returned to the problem, noting that over 100 genes might be involved in terms of the production of source materials, their nature and concentration, phase separation led to heterogeneity of the periplasmic space developing, at every stage phase separaation and micellar self-assembly being involved; the specific exine patterns were "based on physico-chemical principles of space-filling operations" (ibid. p. 221) in processes akin to crystallization (Gabarayeva et al. 2023; see also Polevova et al. 2023). As Gabarayeva et al. (2023) summarized pollen development in Campanula rapunculoides: "The sequence of events leading to exine emergence from early tetrad stage to maturity is as follows: the appearance of spherical micelles in the periplasmic space and de-mixing of the mixture in periplasm (condensed and depleted layers); appearance of plasma membrane invaginations and columns of spherical micelles inside condensed layer; appearance of rod-like units, pro-tectum and thin foot layer; the appearance of spiral substructure of procolumellae and of dendritic outgrowths on the tops of procolumellae, of vast depleted zone in aperture sites; formation of the endexine lamellae on the base of laminate micelles; gradual twisting of dendritic outgrowths (macromolecule chains) into clubs on the tops of columellae and into spines; final sporopollenin accumulation." Phase separation and self-assembly after the initial gene-controlled synthesis of the pollen materials, contributions from both the sporophyte and gametophyte genomes, etc., yield the intricate morphology of the mature pollen grain wall - indeed, Purgina et al. (2024a and references) suggest that sporopollenin can be synthesised by the tapetum alone. However, it is difficult to think of all this in the context of a phylogeny...
Furthermore, rather little is known about possible functional connections between all these pollen morphologies and details of pollination, although Muller (1979) and others have attempted to link some aspects of pollen grain morphology to function. Katifori et al. (2010) examined how the pollen grain folds during harmomegathic changes in shape (see also Hesse & Zetter 2005; Matomoro-Vidal et al. 2016), and Hoekstra (2002) discussed the dessication tolerance of the pollen and spores of "lower" plants. Porate pollen in "dicots" may be associated with wind pollination (Endress & Stumpf 1991). Although the pollen of bat-pollinated Fabaceae often has verrucate ornamentation (Stroo 2000 for references), that author did not find such a correlation across angiosperms as a whole, however, pollen of bat-pollinated flowers did tend to be larger (and the styles longer). Bat-pollinated monocots tend to have a very reduced exine and a much-elaborated intine (Stroo 2000). It has been suggested that spines (and pollenkitt, see below) on pollen may render it unattractive to corbiculate bees (Lunau et al. 2015). The micromorphology of pollen-associated orbicules has been implicated in wind and buzz pollination (Galati et al. 2019). Dajoz et al. (1991) and Furness and Rudall (2004) discuss possible functional aspects of the evolution of tricolpate grains, and Prieu et al. (2017) ditto of pantoporate grains. Pollen size may be related to the length of the style, but pollinators in general, perhaps especially bees, prefer smaller pollen grains (Hao et al. 2020). However, Chartier et al. (2021: p. 827) sum things up when they observed that it was unknown "which of the measured morphological pollen traits are adaptive and thus whether variation in these traits is driven by chance, taxonomy, or reflects evolutionary processes" (see also Mander 2016, 2018). The nature of the pollen surface in Orchidaceae seemed to be unconnected with pollinator type (Purgina et al. 2024b). Wallace et al. (2011) looked at pollen and spore development in the context of evolution.
Data on the number of cells in the pollen grains at the time of their dispersal are taken mostly from Brewbaker (1967); see also Williams et al. (2014) for the evolution of pollen cell number. The basic condition is to have only two cells, those of the vegetative and generative cells, and this is associated with a sporophytic incompatibility system, although at the level of gene expression the difference between the two may not be that great (Dickinson et al. 2000). Subsequent division of the nucleus of the generative cell occurs as the tube grows down the style and results in the production of the two gametes. However, in some angiosperms pollen at the time of anther dehiscence has all three cells; this is associated with gametophytic incompatibility systems (see Wheeler et al. 2001, also below). Interestingly, the number of nuclei can vary between grains in the same individual and even within the one pollen tetrad (Lora et al. 2009a).
Pollen grains vary in their water content, and if this is >30% they are called partly hydrated; such grains are recalcitrant (this term is also used for seeds with similar properties), and die easily when dessicated (Franchi et al. 2002). Developmental arrest is common during poellen development, and details of this and pollen dehydration are connected, the whole story being complex (Ferranti et al. 1996; Panini & Dolferus 2019, see also 2016). Zona (2001) surveyed the distribution of pollen grains containing starch in monocots, and Baker and Baker (1979) and Franchi et al. (1996) give further details for angiosperms as a whole. There are suggestive distribution patterns of taxa that commonly have starch, although sampling needs to be improved; it is fairly common for the odd taxon in an otherwise starch-free family to contain starch, and vice versa.
Pollenkitt, made up of oily substances on the surface of the pollen grain that help it to adhere to the stigma, is common in angiosperms, although less well developed in wind-pollinated plants (Teppner 2009). Trypine is more complex, and both pollenkitt and trypine are linked to the tapetum, although how they are deposited on the grain is unclear (Dickinson et al. 2000). Pollenkitt also causes the pollen to be clumped, but clumping also occurs in pollenkitt-free gymnosperm pollen - exactly how is not known. In general, a role in the progamic/pre-fertilization phase of pollination is likely (Chichiriccò et al. 2019). Interestingly, pollenkitt has similar distinctive fatty acids in Arabidopsis, Crocus, and Narcissus (Chichiriccò et al. 2019). Orbicules [= Übisch bodies] are also derived from the tapetum (Huysmans et al. 1998a; Vinckier et al. 2000; Verstraete et al. 2011; Moon et al. 2018; Galati et al. 2019; Ruggiero & Bedini 2020; Gotelli et al. 2023), and are often - but by no means always - associated with glandular tapetum (see above); although this correlation has been questioned (Galati et al. 2007; see also Verstraete et al. 2014), orbicules have been found in over 80% of the species examined that have a glandular tapetum, while ca 80% of species with an amoeboid tapetum lack orbicules (Moon 2018). They show some connection with phylogeny (as does tapetum type), but any function they might have was until recently unclear. However, it has been suggested that taxa with microechinate orbicules were likely to be wind or buzz pollinated, electrostatic charges at the tips of the spinules helping to keep the pollen grains separate (Galati et al. 2019; see also Amorim et al. 2019 and references). In a number of taxa raphides or other forms of calcium oxalate are mixed in with the pollen (Pohl 1941 for a review).Pollen grains are not always dispersed singly, they may be in tetrads (e.g. many Ericaceae) because of the failure of the individual products of meiosis to separate, and these tetrads may become functionally a single grain by abortion of three of the cells (Cyperaceae, Ericaceae-Epacridoideae), while in many Fabaceae-Mimosoideae there are 8, 18, or even more grains associated in a single polyad. In Orchidaceae and Apocynaceae in particular the contents of single anthers or two adjacent half anthers, along with adjacent tissues and/or secretions form units, pollinaria, dispersed by the pollinator; each pollinaria bears two or more pollinia, commonly including all the grains of a single anther loculus. For a survey of plants with pollen in tetrads, see Copenhaver (2005), for orchid pollen, see Purgina et al. (2024a, b), for the function and evolution of pollen that is dispersed as other than single grains, so including tetrads, see Harder and Johnson (2008). Individual pollen grains or tetrads may be connected with viscin threads, very fine threads made of sporopollenin and derived from the tapetum, and there are a number of other kinds of threads varying both in composition and function that entangle the pollen (Hesse 1986; Halbritter et al. 1997; Hesse et al. 2000 for reviews).
For general discussions about the gynoecium, see the series of papers by Shamrov (1998, 2000 [integument], 2002 [nucellus], 2003 [integument], 2004 [chalaza, funiculus, obturator], 2006, 2008, 2012, 2013, 2018, 2020, 2022b: terms proposed). Carpel number. This is usually quite easy to ascertain in a transverse section of the ovary. "Many" in the characterisations means that there is a variable and large (more than 15) number of carpels. The number of lobes of the stigma or style is often useful confirmatory evidence of carpel number, although such lobes may sometimes be double the number of carpels, as in Euphorbiaceae, Phyllanthaceae, Boraginaceae, and Aextoxicaceae, or individual styluli may be bilobed, as in the ANITA grade, or there may be no obvious connection between style and carpel number (Endress 2014). However, in Primulaceae with free central placentation the stigma may give little obvious indication of the carpel number. Carpel number in Papaveraceae and Brassicaceae and their relatives and in Berberidaceae has long been a bone of contention, and Brückner (2000, p. 273) expressed "her serious hope that she may be the last to have invested time and effort in refuting the 2n and 3n theories [basically, that the gynoecium is made up of two or three times the number of carpels it appears to be], at least for Berberidaceae, Papaveraceae, and Capparales." For the development of multicarpellate gynoecia and its morphological and functional implications, see the review by Endress (2014) and a distinction between floral axis and floral apex.
In a number of taxa apparently with but a single carpel, it can be unclear whether there is really only a single carpel or the gynoecium is reduced from a syncarpous condition, i.e. it is pseudomonomerous, an overused term rarely mentioned here (for pseudomonomerous gynoecia, see e.g. Eckardt 1937; also F. González & Rudall 2010; Endress 2011a for additional references). Apparently monomerous gynoecia have evolved in a variety of ways, and González and Rudall (2010) show how the character can be broken down into a number of states. Indeed, many pseudomonomerous gynoecia consist of two or more carpels in which only one is completely developed (a form of heterocarpy). 75 genera in Arecaceae alone may have only a single carpel, although in Geonoma interrupta there are three well-developed style-stigmas, but development of the ovarial portions of two carpels is rudimentary (Stauffer et al. 2002). Similarly, although early-developing gynoecia of Atripliceae (Amaranthaceae-Chenopodioideae) may consist of a featureless annular rim surrounding a single ovule, the style is strongly two-lobed (Flores-Olvera 2011); similar early gynoecium development occurs in some Poales. Sokoloff et al. (2017a) introduce the term "mixomery", a mixomerous gynoecium being one where carpel individuality is impossible to ascertain.
Carpel development, relationship to ovules, and closure. Carpel primordia are initially U-shaped, and if the area between the arms of the U becomes meristematic, the meristematic cross-zone, the carpel develops as if it were a tube, the ascidiate condition. If no meristematic cross-zone develops, the carpels are plicate (e.g. van Heel 1981, 1983, for a survey). Particularly in angiosperms of the basal pectinations, rarely elsewhere, the carpel margins are initially open (and ascidiate). Post genital occlusion occurs directly by tissue fusion or indirectly by secretion of the cells of adjacent margins (Endress & Igersheim 1997, 2000 [the latter a particularly useful summary]; Igersheim & Endress 1997; Doyle & Endress 2000); for this character optimized on trees, see e.g. P. Soltis et al. (2004) and D. Soltis et al. (2005b). There are intermediate conditions (e.g. Paulino et al. 2014 and references), while even fully ascidiate carpels may have elongated stigmas, which one might otherwise think were the signature of the plicate carpel condition. Furthermore, ovule position is not tightly correlated with carpel type (Endress 2005b). Taylor (1991) discusses this and many other aspects of carpel morphology. Although angiosperms are characterized by their closed carpels, in a number of taxa the young carpels are open and have exposed developing ovules (Tucker & Kantz 2001 for a summary) and in a few taxa the carpels open as the seed develops, so the plant is then effectively gymnospermous. This latter condition is sporadic, carpels that "open" during development being found in Dioncophyllaceae, some Berberidaceae, Malvaceae-Sterculioideae, etc.. The old stachyspory-phyllospory argument is not yet dead. Thus there are recent suggestions that carpels are better interpreted as consisting of an axial/cauline placental region supplied by amphicribral bundles (phloem completely surrounding the xylem) that is subtended by a bract, now represented by the carpel wall (e.g. X. Wang 2010a; Guo et al. 2103; Liu & Ni 2013), however, in a review of the relationships between carpels and ovules, Endress (2019) dismissed the possibility that the ovules of extant angiosperms could be cauline.
Carpel vasculature. Carpels normally are supplied by three vascular bundles, but in a few families there are five (Sterling 1969; Dickison 1971 for references). I have paid little attention to carpel vasculature although much has been written about it (e.g. van Tieghem 1871).
Carpel connation, syncarpy, is indicated by square brackets placed around carpel number. Details of the degree of syncarpy are often systematically useful, although syncarpy is highly homoplasious (Armbruster et al. 2002). In taxa like Boraginaceae, Ochnaceae and Lamiaceae with a lobed gynoecium and gynobasic style, it can seem that the carpels are free, however, there is a single central style. Endress et al. (1983) and others discuss secondarily apocarpous gynoecia. For the compitum, see below.
Ovary position. When the ovary, i.e., that part of the gynoecium bearing ovules, is inserted on the receptacle above the points of insertion of the sepals, petals, and stamens or the hypanthium (see above), it is superior, this being indicated in the characterizations and apomorphy lists by a lineunder the carpel number, and it is inferior when these structures are inserted on top of the ovary. Of course, there are intermediate conditions (semi-inferior, e.g. Gustafsson & Albert 1999), and in Peliosanthes teta, perhaps the only species in Peliosanthes (Asparagaceae-Nolinoideae), the ovary varies from superior to inferior (Jessop 1976).
The ovary may become inferior by early vertical growth beneath the perianth members making the whole apical meristem concave; initiation of the youngest floral primordia occurs on this concave meristem (appendicular epigyny), or, to put it in a somewhat different way, the inferior ovary forms through congenital adnation of the carpels to the bases of the perianth members and stamens. The vascular traces to the stamens and perianth members diverge in an acropetal sequence (e.g. Costello & Motley 2004). Alternatively, vertical growth of the periphery of the receptacle may occur after initiation of the primordia of at least sepals, petals and stamens on a normal convex apex, the vascular supply to these structures is displaced and there are descending traces to the carpels/ovules; this is the rather rarer case of receptacular epigyny (e.g. Kaplan 1967; Soltis et al. 2003b). Unless mentioned otherwise, ovaries become inferior by the action of the former developmental pathway. However, the ovary development of relatively few plants has been studied in detail and whether or not the distinction between the two is really that sharp is questionable (e.g. Dengler 1972; Smyth 2005); Pimentel et al. (2014) describe both appendicular and receptacular epigyny in Myrtaceae-Myrteae. Ovaries that are more or less immersed in nectariferous tissue alone, as in some Celastraceae, are described here as being superior (but see Berkeley 1953). The vascular supply to the gynoecium is recurrent in a few taxa, and that has been considered as evidence for receptacular epigyny (e.g. Berkeley 1953 for discussion). I do not use the terms hypogyny, epigyny and perigyny; these properly refer to floral architecture as a whole. There is a huge literature on the nature of the inferior ovary, and this merges with that on the nature of the carpels (e.g. Douglas 1944 and references).
Although the change from superior to inferior ovary used to be thought of as one of the major evolutionary "trends", we are realizing that there is a growing number of cases where the ovary may be secondarily superior: Rhoipteleaceae (Fagales), Opiliaceae (Santalales, but see the discussion there), within Haemodoraceae (Simpson 1998a, b), also some members of Apiales, Asparagales (reversion in ovary position here is much discussed), Asterales, Commelinales, Cucurbitales, Saxifragales and Poales are possible examples, although few have been studied in any detail. There may be an association of such secondarily superior ovaries with parietal placentation, as in Menyanthaceae (Asterales) and Pittosporaceae (Apiales) (see also Endress 2005a and references). Saxifragaceae and relatives in particular show great variation in ovary position (e.g. Soltis & Hufford 2004; Soltis et al. 2005b).
Carpel orientation. The basic source of data is Eichler (1875-1878: see also Baillon 1866-1892; Le Maout & Decaisne 1868; Goebel 1887; Eckert 1966). When the flower has two carpels, they are usually median, i.e., they are one above the other in the median plane of the flower, but they are sometimes side by side in the horizontal plane and so are collateral or transverse. Only the latter condition is mentioned in the descriptions of 2-carpellate flowers, which can otherwise be assumed to have median carpels. Infrageneric variation in this character, with the carpels being eithertransverse or median, is known, as in Ribes (Eichler 1878). The arrangement of carpels in 4-carpellate flowers is usually median + transverse, and only the diagonal arrangement is mentioned. When there are the same numbers of carpels as members of the outer perianth whorl, the position (alternate, opposite) of the carpels relative to that whorl is mentioned. Carpels borne opposite the corolla are common in obdiplostemonous taxa, indeed, obdiplostemony was redefined by Bachelier and Endress (2009) to refer specifically to the position of the carpels relative to the the corolla, but such carpels are also found in taxa that have five stamens opposite the petals, i.e. obhaplostemonous taxa. The normal condition is for carpels to be opposite the sepals or members of the outer tepal whorl. When there are three carpels and five sepals, the position (adaxial, abaxial) of the median carpel is mentioned.
Placentation in syncarpous gynoecia is described as being axile, lamellar, parietal, or free central (when the carpels are separate, their placentation is often described as being marginal). Basal ovules are nearly always ascending, apical ovules are pendulous. When multiovulate carpels are free, the ovules are often described as being marginal in their insertion (see also Endress 1994b). As with many other features, the character states are not sharply distinct, for instance, the difference between intrusive parietal and axile placentation may be slight (see also Ickert-Bond et al. 2014c; Harthman et al. 2018; etc.), while Simpson and Burton (2006) atomize placentation in a different way in their study of Pontederiaceae. In a few bicarpellate ovaries there is an apical septum; this is supplied by by the dorsal median bundle of the carpel, not the ventral bundle, and is a modification of a gynobasic stylar morphology (see below). See also Puri (1952), Stebbins (1974), Ickert-Bond et al. (2014c) and especially Shivaprakash and Bawa (2022) for reviews of placentation types and suggestions about their evolution, Klopfer (1969b) for parietal placentation, and Rakotonasolo and Davis (2006) for some odd placentation in Rubiaceae. There is a literature on whether placentae are cauline or carpellary, but I have not tried to digest this; Pimentel et al. (2014) found both placental types in Myrtaceae-Myrteae. Asociated with placentation type, there is variation in the number of ovules per flower, and Shivaprakash and Bawa (2022 and references) note that across angiosperms ovule numbers/gynoecium are bimodal, and that there may be a connection between placentatuion and ovule number and kin selection; there is of course also a connection between ovule number and plant habit, parasites and holomycoheterotrophs in particular usually having very large numbers of ovules/seeds and placentation there is often parietal.
Transseptal bundles are vascular bundles that run up the carpels in the septal radii, with branches vascularizing the placentae (Eyde 1988 and references). The normal condition, never mentioned in the characterisations, is for the vascular bundles to be in the placentae themselves. In the placentae of many taxa with parietal placentation there is an inverted bundle immediately underneath a normally orientated (i.e. phloem to the outside) placental bundle (Puri 1946).
Intralocular hairs and secretions may be evident in the young ovary. Such hairs are usually secretory in monocots (Rudall et al. 1998c), and they are commoner there than in broad-leaved angiosperms. In core eudicots the hairs, when they occur, appear to be non-secretory and may be very conspicuous when the fruit is mature, as in Malvaceae, Fagaceae and Chrysobalanaceae. Ovary loculi are sometimes filled with fluid secreted by tissue other than the hairs.
Style connation. I initially tried to make a distinction between styluli, terminal to basal on separate carpels, or the terminal free parts of otherwise connate carpels, and the style, single and borne on connate carpels (e.g. Baumann-Bodenheim 1954); stylodia were branches of a style, be it ever so short. Indeed, stylulus is a useful term to describe the elongated, terminal structures of free carpels, or of carpel apices that are manifestly separate, so I use it here. Hanf (1935) made a somewhat similar distinction between a style, an elongated, apical portion of a syncarpous gynoecium, i.e. a fundamentally compound structure, and a stylodium, a simple structure that includes any separated apical portion of that style, or the elongated apical portion of an individual carpel, or the free apical portion of otherwise connate carpels. However, the term stylodium is rarely used in general botanical literature and has a rather vague definition. The morphological distinction between style and stylulus is that the first is a fundamentally compound structure, the second is simple. I refer to on occasion to style branches in these pages. Normally the presence of a style is associated with that of a compitum (see below); the style may be branched, sometimes even to the base, but a compitum is still evident in the ovary. For variation is style connation (and stigma morphology) within Cuscuta, see Wright et al. (2011).
Style/stylulus position. The style is usually terminal on the ovary and more or less continuous with it. Variants are noted. Thus the stylulus may be distinctly lateral on individual carpels (some Rosaceae-Rosoideae), or the single style of a syncarpous gynoecium may be lateral (Chrysobalanaceae: only one carpel is fully developed, the gynoecium apparently having a single carpel - pseudomonomery). In some taxa the styluli of a syncarpous gynoecium are borne towards the periphery of the gynoecium, as in Hillebrandia (Begoniaceae), not in the center, as is the normal condition in such circumstances; the ovary is then described as having a well-developed roof. The style may also appear be more or less impressed in the apex of the ovary because of the "bulging" of the apical part of the carpel, the extreme condition being a gynobasic style, the individual carpels (or divisions of the carpels, as in Lamiaceae) appearing to be separate from the style, which arises between them (Endress 2011a for bulging and gynobasy). In such cases the ovary may secondarily come to surround the style which then appears terminal (Hartl 1962; Jäger-Zürn 2003 and references), however, this condition can be distinguished from a truly terminal style i.a. by the pollen tube transmitting tissue going down what appears to be the central axis of the ovary to the very base and by the distinctive vascularization of the apical septum of the ovary (e.g. Hanf 1935, Fig. 7).
In the characterizations I make a point of mentioning when the apices of the carpels of an otherwise syncarpous gynoecium are free and the gynoecium itself is without an intragynoecial compitum (see below), and also when the styluli/stigmas of such carpels are close together, or whether they are marginal (see above). (I am very grateful to K. Kubitzki for discussion about and references to the suite of characters associated with styles, stylodia, etc.)
Heterostyly is scattered in flowering plants, although particularly common in Rubiaceae (commonest here, see also Betancourt et al. 2023), Oxalidaceae plus Connaraceae, Primulaceae, Passifloraceae-Turneroideae, etc. (Simón-Porcar et al. 2024 for a review). There is variation in stamen length between and sometimes within an individual when the flowers are heterostylous, the latter, for example, in tristylous Oxalis. Here the stamens of the separate whorls are of different lengths, and different individuals have different stamens whorls; there is also complementary variation in style length and in pollen morphology (see Schill et al. 1985; Weller 2009 for literature). Heterostyly rarely occurs in taxa with monosymmetric flowers (Barrett et al. 2000). For a summary of other work on heterostyly, see Barrett (1992), Barrett and Shore (2008), Cohen (2019: origin of heterostyly from herkogamy), New Phytol. 171(3). 2006, Kappel et al. (2017), Gutiérrez-Valencia et al. (2021: heterostyly and supergenes) and Simón-Porcar et al. (2024). For more on stylar polymorphisms in general, see Raju (2019), and for enantiostyly, see de Almeida and de Castro (2019).
Stylar canals. Styles or style branches may be solid, filled with pollen tube transmitting tissue, or hollow, the central cavity usually being lined by epidermal-type cells of a variety of morphologies (Hanf 1935: see also Williams 2009; Sage et al. 2009), but this feature is recorded rather erratically. The common condition in eudicots at least is for the style to be solid, while that of the monocots is generally hollow (Hanf 1935; Weberling 1989; Rudall et al. 1998c, 2002). There are intermediates, Hanf's (1935) "halbgeschlossene Pollenschlauchleiter", and Guéguen (1901a, 1901b-1902) quite often talks about some kind of canals in eudicots. Indeed, hollow styles can be difficult to see, because the stylar canal can be very narrow, moreover, the presence/absence of a stylar canal may vary between closely-related taxa (Bensel & Palser 1975a). Capus (1878), Guéguen (1901a, 1901b, 1902) and Hanf (1935, and references) are useful early sources of information; data for asterids are in part taken from Anderberg (1992) and Bhatnagar and Uma (1969), and for the style in a few monocots, see also Hartl and Severin (1981) and Johri (1966a, b: "Liliaceae"). In general information on this character is very scattered. Crawford and Yanofsky (2008) discuss details of the movement of the pollen tubes through stylar and septal tissues on their way to the ovules.
The stigma) is that portion of the style, style branch or stylulus that has the function of picking up pollen grains. Stigma shape is variable and sometimes distinctive. It may be punctate, variously expanded, canaliculate or decurrent, sometimes being the length of the style. Some taxa have notably papillate stigmas, or the receptive surface may be localized on multicellular papillae or hairs (Heslop-Harrison 1981 for a summary) or on one side of the style (Baum-Leinfellner 1953). There is no convenient access to the scattered literature on stigma morphology,although some taxa like Malvaceae-Malvoideae show considerable variation in stigma morphology. Although not strictly a shape characteristic, whether or not the stigmatic lobes are commissural is of some interest; commissural stigmas are perhaps particularly common when placentation is parietal.
The presence of secretions produced by the stigmatic surface may be of interest. Wet stigmas are quite frequently found in taxa with binucleate pollen grains and gametophytic incompatibility systems, and dry stigmas in taxa with tricellular pollen gains and a sporophytic incompatibility system (see Heslop-Harrison 1981; Heslop-Harrison & Shivanna 1977; Schill et al. 1985). However, variation often seems to occur between families that are closely related and taxa with porose stigmas can be hard to place (Dulberger et al. 1994); in general the nature of the stigma surface needs further study (e.g. Dulberger et al. 1994; Igersheim et al. 2001: conflicting reports in Alismatales; Costa et al. 2014). The plesiomorphic condition for angiosperms may be to have a wet stigma (e.g. Endress 2001a, c.f. Sage et al. 2009).
The correlation of stigma surface with incompatibility type is not perfect (Heslop-Harrison 1981; Wheeler et al. 2001). Details of incompatibility systems are described by Charlesworth et al. (2005), Allen and Hiscock (2008), Barrett (2013), L. Wang et al. (2019) and others; cell death may be involved. Gametophytic incompatibility systems: wet stigmas, pollen grains that are bicellular at dispersal, incompatibility phenotype of pollen grain determined by haploid pollen genome, reaction evident in the style: sporophytic incompatibility systems: dry stigmas, tricellular pollen grains, incompatibility expression determined by diploid genome of parental plant, reaction evident on the stigma surface (Allen & Hiscock 2008). For the evolution of cell number in pollen grains, see Williams et al. (2014). Both gametophytic and sporophytic systems seem to have evolved in parallel, but it has been suggested that the gametophytic system in both rosids and asterids may be identical (e.g. Steinbachs & Holsinger 2002: the stylar response is mediated by a glycoprotein with ribonuclease activity). At exactly what level incompatibility "types" might be synapomorphies is unclear, largely because so little is known about details of the whole system and their distributions. However, a RNase-based gametophytic incompatibility system might be a synapomorphy at the level of (most) core eudicots. Ingrouille and Chase (2004) analyze incompatibility in the context of phylogeny, and they show that both main incompatibility types are scattered throughout the angiosperms. Many of the incompatibility systems in monocots, where they are quite common, are as yet uncharacterized (Sage et al. 2000). Self compatability and protogyny and self incompatibility and protandry seems to be linked (e.g. Bertin 1993; Routley et al. 2004). Late acting incompatinbility systems in which the incompatibility is manifest as late as fertlization, are discussed by Gibbs (2014). For more on incompatibility systems and their evolution, a much discussed topic, see also Dickinson et al. (1998), Hiscock and Tabah (2003), Igic and Kohn (2001, 2006), Igic et al. (2006), Franklin-Tong and Franklin (2003), papers in Franklin-Tong (2008a), e.g. Allen and Hiscock (2008), articles in Ann. Bot. 108(4). 2011, Robertson et al. (2010), Raduski et al. (2012) and Wyatt and Lipow (2021).
Compitum presence. In many syncarpous gynoecia with at least partly plicate carpels the loculi/placentae are in connection with each other via an intragynoecial compitum, tissue that allows pollen tubes to fertilize any ovule no matter where the pollen grains landed on the stigma, or, if the style is branched, no matter on which stigma they landed (Carr & Carr 1961; Friis & Endress 1990; Endress 1994, 2011; van der Schoot et al. 1995). If the carpels are completely synascidiate there can be no intragynoecial compitum, on the other hand, a compitum can develop by post-genital connation of the styles in taxa like Apocynaceae and Malvaceae-Sterculioideae in which the carpels are otherwise free. Some Nymphaeales, Laurales, etc., with free carpels have an extragynoecial compitum, of which the hyperstigma is a variant, and here carpels are placed in contact not by pollen tube transmitting tissue but by secretions of the stigmas through which the pollen grains grow (e.g. Endress 1982, 2001a; Endress & Igersheim 2000).
Ovules. Useful surveys of various aspects of ovule morphology and development - a number in Russian - are those of Yakovlev (1983), Takhtajan (editor: 1985, 1988, 1991, 1992), Kamelina et al. (editors: 1981, 1983), Batygina et al. (editors: 1985, 1987, 1990), Johri et al. (1992), Danilova (editor: 1996) and Kamelina (2009); see also Shamrov (e.g. 2000, 2002, 2003, 2004, 2008, 2012, 2013, 2018, 2022b) and especially Bouman (1984), Endress (2011b) and Rudall (2021: seed plants in general). A number of early studies can still be consulted with profit, e.g. Chatin (1874), Vesque (1876), Warming (1876), Guignard (1882), Brandza (1891), van Tieghem (1898a), Billings (1901), Dahlgren (1916, 1927, 1928a, 1940b), Schnarf (1929: summary of variation in Liliaceae s.l.), Mauritzon (1933, 1936a, 1939a, 1939b) to Maheshwari and Kapil (1967), and indeed they need to be as Endress (e.g. 2011b) has redefined some terms so that the original literature now more than ever cannot simply be mapped on to the present. Rudall (1997) surveyed ovule morphology in monocots; Endress and Igersheim (1997, 1999) and Igersheim and Endress (1997, 1998) describe ovule morphology and anatomy in magnoliids and the ANITA grade and Taylor (1991) also emphasized these taxa in his survey. However, for a number of taxa, the only information available remains that in early works such as those just mentioned.
Ovules are complex structures, and a considerable number of phylogenetically informative characters can be derived from a study of ovule morphology. Much time has been spent in working out a classification of ovule "types" (e.g. Shamrov 1998, 2022b, and references), nucellus "types", etc., and in providing sets of names for all the variants, although these can be difficult to recognise and the terms are inconsistently applied. There is an increasing number of suggestions that ovule terminology needs to be reformed (e.g. Shamrov 1998; Endress 2005c). Although some of the new terms that are being proposed are in part confusing and, like the old terms, are arbitrarily delimited, terminological reform is badly needed.
Some parasitic or hemiparasitic taxa lack organized ovules, an embryo sac alone being readily recognizable (see Santalales in particular, Gentianaceae, and the ovules of Cardiopteris-Cardiopteridaceae are really rather odd), and that makes understanding many aspects of their embryology and seed and fruit development difficult since ovule orientation, seed/fruit anatomy, etc., become problematic; about the only feature that can be estimated easily is the number of ovules per ovary.
Ovule number is always mentioned, although it is often very variable. "Many" means that there is a large (more than 15) number of ovules.
Ovule orientation. The direction of curvature of ovules relative to the axis of the flower and the carpel margins is usually consistent within taxa where there are few ovules, and ovule orientation is usually mentioned only for such taxa. Epitropous ovules are curved adaxially (= dorsal raphe), apotropous ovules are curved abaxially (= ventral raphe: Björnstad 1970); this variation is independent of whether the ovules are apical or basal. Since I initially recorded only the apotropous condition, epitropous ovules may be under-reported. Pleurotropous ovules are held sideways so the micropyle faces laterally. When there are many ovules per carpel their orientation is either variable or pleurotropous; ovules are epi- and apotropous within a single ovary of Pittosporum floribundum (Narayana & Sundari 1983). Even in families like Rutaceae, Anacardiaceae, Sapindaceae and Menispermaceae where there are only two ovules per carpel, ovule orientation can vary within the carpel, or there can be changes during development. Thus in Burseraceae the ovules start off more or less apotropous and become epitropous (e.g. Svensson 1925; Mauritzon 1936; Bachelier & Endress 2009). Endress (1994b) suggested that it might be more useful to refer to the curvature of the ovule with respect to that of the curvature of the carpel margins. These terms, syntropous, curvature in the same direction as that of the carpel margins, versus antitropous, curvature in the opposite direction, focus on curvature that is at right angles to the axis that determines epi- versus apotropy in plicate carpels. In gymnosperms, the ovule may be erect or recurved, i.e. with the micropyle pointing away from the axis or towards it; again, ovule orientation can change during ontogeny (Taylor et al. 2009).
The orientation of the ovule in relation to its stalk, the funicle, has attracted much attention. Ovules can be described as being atropous (= orthotropous, but straight is surely better), anatropous, amphitropous, campylotropous, circinotropous or hemitropous, depending on the curvature of the body of the ovule and its relation to the funicle. These terms simply refer to points along a continuum, and ovule "type", as with micropyle "type" (see below), can change during development (e.g. Mauritzon 1934g), and Gifford and Foster (1989) and Bouman and Boesewinkel (1991) emphasize the variety of ways in which an ovule can become campylotropous. Endress (2011b) has linked the curvature of the ovule to the development of a second integument; straight ovules are often unitegmic; for the evolution of the second (= outer) integument, see Shi et al. (2021). This is not the case in asterids, but here the two integuments may have congenitally fused to form the single integument (see below). Bitegmic Piper has straight ovules.
Integument number is a character of some systematic interest. Shamrov (2003) provides a useful survey; see also Endress (2011b). Ovules usually have one (unitegmic - ovules often straight) or two (bitegmic - ovules often variously curved/bent) integuments. The outer integument may be dermal or subdermal in origin and arising from L2 (and L3), the inner integument dermal and developing from L1 (van Tieghem 1898a; Roth 1957; Boeswinkel & Bouman 1967; Bouman 1984); the inner integument usually appears first. Grootjen and Bouman (1981) and Bouman (1984) suggest that variation in the details of the position of initiation may be of systematic significance, but I have not followed up on their suggestions (see Pankow 1962 for some details); in any case, observations are relatively few, and there is infrafamilial variation (Bor & Bouman 1975). In much of the older literature variation in details of integument morphology and development tend to have an inordinate effect on authors' ideas of relationships, and some of these were pretty far-fetched. The two integuments are likely to have quite different evolutionary origins (Doyle 2006; Endress 2011b; Lora et al. 2015; Gasser & Skinner 2018; Shi et al. 2021). Gymnosperms always have an unitegmic ovule, while in angiosperms such an ovule is derived, and may arise either by adnation of the two integuments or by suppression of one of them (Bouman 1984). Congenital fusion or adnation of the two integuments seems to be common, and then the ovule is often anatropous; the outer layer of such an integument is equivalent to the outer layer of the outer integument. The molecular basis for this is beginning to be understood, for example, the ABERRANT TESTA SHAPE gene may be involved (e.g. Kelley et al. 2009; McAbee et al. 2005, 2006; Lora et al. 2015; Gasser & Skinner 2018). Interestingly, when the integuments fuse, the thickness of the combined integument may be greater than that of the two separate integuments might have been (McAbee et al. 2006). The latter condition does does occur (Skinner et al. 2016), the outer integument not developing because of a mutation in the INO (INNER NO OUTER) gene, and here the ovule is often straight - and the outer layer of the integument is equivalent to the outer layer of the inner integument.
Endress (e.g. 2011; Endress & Matthews 2006a) and others have emphasized the importance of the relative integument thickness as a systematic feature. For general information on integument thickness, see the surveys mentioned above, also e.g. Netolitzky (1926), Huber (1969), Corner (1976), Grootjen and Bouman (1989), and Johri et al. (1992), as well as very many studies on individual species. Integuments are commonly two or three cells thick over the body of the ovule, and only when they differ in thickness is this included in the characterisations. Integument thickness is recorded as the number of cell layers on the side of the ovule away from the raphe (when the ovule is curved) visible when the ovule is mature; although the integuments are commonly rather thicker at the micropyle than elsewhere, this is generally not mentioned. Multiplicative integuments are strictly speaking those in which integument thickness increases after fertilization, but c.f. e.g. Tokuoka & Tobe 2002 who use "multiplicative" as equivalent to a "thick" integument - several cells across - and this at the ovule stage. "Multiplicative integument" as used here refers to post-fertilization increase in thickness and is mentioned when the seed is described. In straight ovules the outer integument is often thinner than the inner, and it has been suggested that a thick (outer) integument helps to ensure curvature of the ovules (Endress 2005c, 2011b). The outer integument at the time it is initiated may be cup- or hood-shaped (Yamada et al. 2001), reflecting its likely origin (Shi et al. 2021; see also Endress & Igersheim 2000; Endress 2005c). Lobing of the integument is uncommon (but see e.g. van Heel 1970); Endress (2011b) discussed the association of integument lobing with other features of the ovule.
The micropyle in the mature ovule, i.e., at the time of fertilization, may be formed from the outer integument only (exostomal), the inner integument only (endostomal), or both integuments (bistomal), or it may be zig-zag, the integuments overlapping in such a way that the passage from the nucellus to the outside is not straight, or in taxa with a single integument, the micropyle is clearly offset with respect to the apex of the nucellus... Most ovules with zig-zag micropyles are variants of the bistomal "type". In a few taxa, e.g. some Laurales, the nucellus is not completely covered by the integument(s) when the flower is at anthesis, the micropyle then being absent; this condition is described as nucellus apex exposed. Extensive infraspecific variation in micropyle morphology has been observed in Putranjivaceae (Tokuoka & Tobe 1999), and given the sampling of this character, more variation is to be expected. Indeed, there appears to be extensive inframilial variation, although some of this may be the result of observations being made on ovules of different ages. For example, Agrawal (1952) noted that the micropyle of Lilaea subulata (Juncaginaceae) was naked even the 8-nucleate stage of the embryo sac, endostomal when the embryo sac was mature, the polar nuclei having fused, while it was bistomal just after fertilization (see also Nair & Joseph 1960).
Nucellus condition. Shamrov (2002) discusses nucellus morphology in some detail; Endress (2003c) provided extensive information on the distribution of the various kinds of nucellus in Malpighiales and many asterids, while Endress and Matthews (2006a) focused on variation in rosids. In crassinucellate ovules the archesporial cell (see below) divides periclinally and there are two or more hypodermal layers in the ovules above the embryo sac - effectively a eusporangium. In tenuinucellateovules there is no periclinal division of the archesporial cell, which gives rise directly to the embryo sac, and so there are no parietal cells between the embryo sac and the epidermis of the ovule - the leptosporangiate condition. In a "pseudotenuinucellate" ovule the parietal cell does not divide again (it may even disappear), and so the ovule may look as if it were tenuinucellate; weakly crassinucellar (Endress 2003c, 2011b; Endress & Matthews 2006a) is a better name for this condition. Endress (2003c) added the term incompletely tenuinucellar; here there are no hypodermal cells above the embryo sac but there are such nucellar cells laterally and/or below it. Interestingly, a limited survey suggested that tenuinucellate ovules tend to be larger than crassinucellate ovules (Greenway & Harder 2007). A nucellar cap quite often develops when epidermal cells at the apex of the ovule divide periclinally (giving "pseudocrassinucellate" ovules - Davis 1966; also Bouman 1984; Rudall 1997; Endress 2003c, 2011b). Note that otherwise tenuinucellate ovules that have this nucellar cap have also been called "pseudocrassinucellate", but this term has little to recommend it; here nucellar caps are specifically mentioned whenever they occur, whatever the thickness of the nucellus. Nucellar caps seem to be underrecorded in gymnosperms (Singh 1978).
Funicle length. Some taxa, most notably in Caryophyllales, have long funicles; these are defined as being about the length of the body of the ovule at anthesis or longer. In taxa with circinotropous ovules the funicles are very long and curled. In some groups, e.g. Sapotaceae and Sapindaceae, the ovule is sessile. When funicle length is not mentioned it can be assumed that it is unremarkable.
Ovule variants. The nucellus may protrude as a beak through the micropyle (Bouman 1984, for data). Obturators, whether funicular, placental, or integumentary in origin (Shamrov 2004), are closely associated with the micropyle; the ponticulus is a kind of obturator found in some Anacardiaceae. Unfortunately, I have not been systematic in recording obturator morphology, furthermore, obturators may become arils in mature seeds (see Romero et al. 2021). Vascular bundles from the funicle usually terminate in the base of the ovule, but bundles may also occur in the outer or somewhat less frequently in the inner integument, and they may be branched or not. Quite a number of taxa lack ovular bundles entirely. Such features are mentioned in the description of the ovule, and sometimes also in that of the seed coat. The endothelium (integumental tapetum is a synonym) is a distinctive layer or layers of cells (sometimes up to 32-ploid) of the inner (or only) integument immediately abutting the nucellus; it is commonest in unitegmic taxa (Kapil & Tiwari 1978) and may directly abut the embryo sac due to the breakdown of the intervening cells. In some Lamiales the endothium has much-branched processes from the cell wall and seems to function as transfer tissue (Joel et al. 2012). Swamy and Krishnamurthy (1971) suggest that monocots lack an endothelium, but other authors describe one there; most monocots lack any parietal tissue or it is one, perhaps two, layers thick. The chalaza, tissue at the base of the embryo sac/apex of the funicle, is variously developed, and there is frequently distinctive vasculature, or thickening or staining of groups of cells in the chalazal region, the hypostase (see e.g. Vesque 1903, also Lötscher 1905 for early literature), c.f. the epistase. It has been suggested that in Onagraceae, at least, hypostase presence is correlated with dry conditions and its presence is environmentally determined (Johansen 1928) and correlations betweem absence of a hypostase and the presence of chalazal endosperm haustoria (Vesque 1903), etc., have been suggested. Sometimes a group of nucellar cells protrude into the base of the embryo sac, forming the postament (Dahlgren 1940b for a survey), or nucellar cells are simply persistent at the base of the embryo sac, forming a podium, or the chalazal cells die early and form a persistent cap-like structure, the petasus, at the base of the embryo sac. This whole set of terms is not very satisfactory. For instance, the hypostase may appear at different stages of the development of the ovule, although note that morphologically quite different structures may be called a hypostase (e.g. Bor & Bouman 1975) in the same family (van Tieghem 1903a: Euphorbiaceae) or even in the same article (Johri & Kapil 1953); the same is true of epistase.
Embryo sac/female gametophyte. For reviews, see e.g. Maheshwari (1941), Kapil and Bhatnagar (1981) and Willemse and van Went (1984). The archesporial cell (megaspore mother cell) is usually single. Exceptions are quite widespread, and where they are common they are usually noted, the odd occurrence of two or more megaspore mother cells is frequent and is often ignored. In Fagales there are often numerous megaspore mother cells, and several embryo sacs may develop in the one ovule (see also Bachelier & Friedman 2011); multicellular archesporia develop in some Euphorbia (Vinogradova 2022: review of female arechesporium). For megaspore mother cell development and megaspore differentiation, see Demesa-Arévalo and Vielle-Caldaza (2013). Normally a single megaspore mother cell produces a single embryo sac or female gametophyte from the germination of a single megaspore, i.e., it is monosporic in origin. The megaspore itself is a meiotic product of a single megasporocyte or archesporial cell (see Bouman 1984 for some information). The Polygonum-type embryo sac, monosporic and with eight nuclei, the egg cell being adjacent to the micropyle, is commonest in angiosperms and in part for that reason had long been thought to be plesiomorphic/primitive. However, this view has been shown to be incorrect, both Nymphaeales and Austrobaileyales have 4-nucleate embryo sacs and subsequently a diploid endosperm while Amborella has a 9-nucleate embryo sac and triploid endosperm (see e.g. Friedman et al. 2003a, esp. b; Friedman & Williams 2004; Friedman 2006). There is a considerable amount of older literature on embryo sac development, e.g. Vesque (1878), Fagerlind (1938c, 1939b, 1944, esp. tetrasporic embryo sacs); see also S. Maheshwari (1955) for an evaluation of reports of bisporic embryo sacs and P. Maheshwari (1947) for a now somewhat dated review of tetranucleate embryo sacs. There is sometimes substantial infraspecific variation in the development of the embryo sac (e.g. Fagerlind 1939b: Limnanthes). Haig (2020) provides a useful review of embryo sac development.
The two synergid cells that lie next to the egg cell are intimately involved in the fertilization process, as is also the central cell (Puwani et al. 2007; Chen et al. 2007); Dahlgren (1928a) summarized the distribution of hooked or protruding synergids (see also). For a discussion on the persistence of antipodal cells and their multiplication, see Holloway and Friedman (2008). On occasion, the whole embryo sac enlarges greatly and become haustorial (Mikesell 1990 for a review). Highly reduced ovules present problems for the interpretation of embryo sac morphology because of the absence of landmarks to orient the observer (see also above). It has been suggested that the egg apparatus arises at the lower pole of the embryo sac in some mycoheterotrophic Gentianaceae (Bouman et al. 2002), but we may be dealing with a highly reduced anatropous ovule. Ross and Sumner (2004) describe ovule development in Arceuthobium americanum in detail; embryo sac orientation there and in Viscum seem to be diametrically opposite (cf. Zaki & Kuijt 1994, 1995). Tobe (2016) described the whole bizarre process of embryo sac development, fertilization and embryogenesis in Cardiopteris quinqueloba, without parallel in other angiosperms.
For an outline of the major variants in embryo sac morphology, see e.g. Haig (1990: cautions on the typology of the embryo sac "types") and Johri et al. (1992). As Madrid and Friedman (2008) note, detailed studies that go beyond simple pattern and that are placed in a phylogenetic context are the best way to understand the evolution of embryo sac development, rather than considering transformations of these "types" in the abstract. Friedman (2001b) outlines the main theories of the evolution of the embryo sac, which is characterized (usually) by its bipolar development, that is, the micropylar and chalazal haves of the embryo sac are in some respects very similar. Any adaptive significance of the variation in embryo sac development, some of which affects the balance of maternal and paternal genes in the parent sporophyte-endosperm-seedling system, is still not well understood (but see Friedman et al. 2008). Sokoloff and Remizowa (2021) compare angiosperm embryo sacs with those of other embryophytes, suggesting i.a. that the angiosperm egg is equivalent to the ventral canal cell of other embryophytes...
Fertilization. In most gymnosperms a substantial time elapses between pollination and fertilization, whereas in most angiosperms fertilization occurs within two days of pollination. However, in some angiosperms pollination is delayed, in some species of Quercus as much as a year or even more, and in Corylus avellana the ovule may not have even started developing at the time of pollination; in such cases pollen tube growth is also notably intermittent. This may lead to competition between the developing ovules (Sogo & Tobe 2006d for literature). The pollen tube usually grows down the micropyle before penetrating the embryo sac (porogamy), but in a few taxa, most notably in a number of Fagales, the tube penetrates the ovule in the chalazal region (chalazogamy) or sometimes through the side.
There is interesting variation in pollen tube wall composition in seed plants (Yatomi et al. 2002). As to pollen tubes of angiosperms, Prósperi and Cocucci (1979) and Cocucci (1983) suggest that the occurrence of callose in pollen tubes as they grow down the style may be of systematic interest; these plugs were absent in Lamiales and present in Solanales, for example. Normally, as angiosperm pollen tubes move towards the ovules, callose is deposited at intervals along the tube, a feature that may be of considerable interest in the evolution of angiosperms (e.g. Williams 2008); Parre and Geitmann (2005) discuss the mechanical properties of callose. Mogami et al. (2006) suggested that both details of plug morphology and periodicity of plug deposition differs between monocots and broad-leaved angiosperms (complete and regularly deposited vs. incomplete and irregularly deposited), but there are many exceptions.
Fruit, Seed and Seedling.
For definitions, etc., see the Glossary. As will be mentioned again below, the terms "fruit" and "seed" - and others around here - are often used in a variety of ways, in particular one more morphological and the other more functional/ecological. Thus "fruit" can mean the structure formed from the ovary after flowering, containing seeds, although technically that would exclude things like apples and cucumbers, which are the products of inferior ovaries. Likewise, "seeds" are the derivatives of ovules, containing an embryo, etc., although the term is also used for any (small) dispersal unit whatever its morphology, so including the disseminules of grasses, Asteraceae, etc.. It is clear that here, as elsewhere, there are tensions between separate sets of terms, in this case those used to describe a "fruit" based on its morphological nature (not to mention whether that is based on observation using a hand lans, anatomy, or gene expression) and how fruit-eating/-dispersing organisms, for example, see the world.
General information about fruits is widely scattered. For ideas about the evolution of fruits and seeds and of the plant as a whole that are stimulating, if some are now rather suspect, see Corner (e.g. 1953-1954); for some stunning photographs of fruits, see Stuppy and Kesseler (2008). There is the issue of relating structure to function in dispersal (van der Pijl 1966: early ideas about dispersal syndromes, 1982) and whether or not there are dispersal syndromes such as bird-, ant-, wind- and mammal-dispersed fruits/seeds (see also pollination syndromes above) - Beattie (1985), Lengyel et al. (2009, 2010), Rojas et al. (2022), Valenta and Nevo (2020, 2022) and many others help clarify the issues. Rojas et al. (2022) noted that seed dispersers selected for fruit morphologies in predictable ways, probably more comprehensively that these authors were able to detect; in addition to links between the size and colour (e.g. Nevo et al. 2018b; Sinnott-Armstrong et al. 2020, 2021), scent (Nevo et al. 2018), and perhaps even sugar concentrations (Lotz & Schondube 2006) and so on of the fruits and the kind of animal dispersing the fruits (Valenta & Nevo 2022). Indeed, when thinking about the ecology of fruit and seed (= diaspore) dispersal, some of the more purely morphological distinctions that are made in the family characterizations can usefully be ignored (see also the discussion on seeds). As with floral morphology and pollination, the morphology and senses of the disperser have to be taken into account, and recent history cannot be ignored. Thus seeds with elaiosomes may be functionally equivalent to achenial-type fruits with a distinct fleshy zone; plumed seeds and fruits may be functionally equivalent, likewise a fig syconium and an Actinidia berry (kiwi fruit); Dahl et al. (2019) even provide a classification of fruit syndromes in tropical forests from an insect's point of view. And of course some dispersers may recently have gone extinct, e.g. members of the megafauna in the New World in particular (Janzen & Martin 1982; van Zonnefeld et al. 2018 and references). Thinking about fleshy fruits in Argentina in particular, Rojas et al. (2022) noted that seed dispersers, bats, terrestrial mammals and birds, selected for three particular morphologies of fleshy fruits; there are dispersal syndromes of sorts (see also Valenta & Nevo 2020, 2022; Nevo et al. 2018: scent and primate frugivores; Messeder et al. 2024: Solanum). Indeed, Rojas et al. (2022) noted that there was also variation in chemical and display traits in the context of the major morphological variation of the three fruit types that they found, while Sinnott-Armstrong et al. (2021) suggested that dispersers (bird versus mammal), along with aspects of the environment, were the drivers of global variation in fruit colour syndromes. Furthermore, fruits of the one plant may be dispersed in different ways (see also pollination), and this almost self-evident observation leads in various directions. Thus Sádlo et al. (2018), focussing on the Czech flora, describe what they call dispersal strategies, and these are found in groups of plants whose propagules are dispersed in a similar combination of ways. In quite a number of taxa seeds from the one plant are dispersed in very different ways, the variation enabling this being at the level of the seed, fruit or fruit + associated structures; the terminology here is off-putting, but the term heterodiaspory can be used, while amphicarpy, really another variant of this theme, refers to plants in which some fruits are subterranean while others mature above ground (Teppner 2003). Leins and Erbar (2010 - e.g. "nautochores"; also Vittoz & Engler 2007) provide a well-illustrated summary of terms, morphologies and mechanisms involved in diaspore dispersal. For surveys of seed dispersal, see Snow (1981), Howe and Smallwood (1982) and of course especially Van der Pijl (1982).
Fruit type. I define fruit loosely as a post-fertilization structure developed from either a single carpel; or connate carpels (ovary superior); or connate (or free) carpels (ovary superior) + associated calyx and/or corolla; or connate (or free) carpels + inferior ovary or hypanthium; or ditto + carpels of adjacent flowers; or carpels of separate flowers plus inflorescence axis... (and for "fructoids" in gymnosperms, see Contreras et al. 2016). Similarly, although terms such as "berry" and "drupe" have precise definitions, they are also used more loosely, as in "gooseberry", "blueberry", and the like. Here the use of terms like "baccate" and "drupaceous" in the characterizations is a warning that these terms are not being used in the morphologically correct sense. If more detail is required about how fruits are categorized, there are complex and detailed sets of terms and fruit types available, for which, see Stopp (1950), Baumann-Bodenheim (1954), Hertel (1959), Barroso et al. (1999), Spjut (1994, see also 2003 onwards), Roth (1997), Bobrov et al. (2009), de Almeida et al. (2018), etc., etc.; Judd (1985; see also Judd et al. 2015) and Leins and Erbar (2010) provide a simplified set of terms, although terms like "berry" in the former would seem to have little morphological utility. Since the number of fruit "types" runs to three figures and these types, like practically all "types", serve to obscure rather than to clarify details of variation and the evolution of morphology, I find little to recommend in any fruit classification. And of course if one is thinking of fruits and seeds s.l. from a more ecological point of view, an aggregate of drupelets and a berry both go down - and come out - in much the same way, thank you very much.
I had initially wanted to use terms for fruit "types" that reflected whether the fruit was derived from a superior or from an inferior ovary, and if from the former, whether the carpels were free or fused. However, some of the terms were cumbersome and others contradicted common usage; using separate terms for fruits developing from apocarpous and from monocarpellary gynoecia runs in to similar problems (e.g. Leins 2000; c.f. Leins & Erbar 2010). Nevertheless, fruit types as commonly used are something of a disaster area from the point of view of basic morphology. Most fruit types are composites of several characters, so thinking about the evolution of one type from another can be tricky. A number of fruit types used in the literature refer - more or less by convention - to fruit morphologies found only in single families or parts of families ("pepo", "hesperidium", "legume", "anthocarp", "cactidium", "pome"), yet if interpreted properly, they would seem to have a wider application - do not blueberries and cucumbers have "pomes", just like apples? Other fruit types imply distinctions when either none really exist and/or variation is at a lower level than is the focus here - but the confusing set of terms "silique", "siliqua" and "silicula" creep in to the tribal characterisations of Brassicaceae. Nevertheless, despite all these problems (see e.g. Clifford & Dettmann 2001; Costea et al. 2003; Steel & Wilson 2012), fruits are complex structures and there is much of systematic interest to be gained from their careful study (see, e.g. Bobrov et al. 2017). For fossil fruits, see also Takhtajan (1974, 1982) and Budantsev (1994, 2005).
Details of fruit anatomy are rarely mentioned in the characterizations. However, general information can be found in e.g. Vaughan (1970) and especially Takhtajan (1985 and subsequent volumes - summary and new data); some more recent studies touch on the fruit anatomy of more limited groups, e.g. Wannan and Quinn (1990), Romanov et al. (2007), Pabon Mora and Litt (2007), Bobrov et al. (2012 and references), Arecaceae, while Moon et al. (2009b) and Salmaki et al. (2009) both describe the anatomy of nutlets in Lamiaceae, and Seibert (1978), Ovczinnikova (2007) and Simpson and Hasenstab (2009), that of nutlets in Boraginaceae-Boraginoideae. Indeed, the anatomy of the fruit wall allows one to decide whether fruits that are ostensibly of the same basic kind really are similar enough to be considered immediately comparable - i.e., by applying Remane's criteria of special properties (anatomy), development, etc. - simple gross anatomy may be insufficient (Clifford & Dettmann 2001). Thus Bobrov et al. (2005) and others discuss the need to study the developmental origins of the woody layer surrounding the seed - not all drupes are created equal. Manchester and O'Leary (2010) report on the diversity of morphologies that is encompassed by "fin-winged" fruit, and use their knowledge to assign most fossils of such fruits to several different extant families.
Here I restrict myself largely to the simplified terms suggested below and defined in the glossary, although additional information may be provided in the characterisations. Any fruit descriptions/"types" must be interpreted carefully, particularly taking into account the developmental origins of tissue such as the stony layer, the position of the ovary, and also the presence of other organs associated with the fruit proper and involved in fruit or seed dispersal - thus a wingwd propagule may be a seed, a fruit, or a fruit plus associated structures like sepals, bracts, etc.. This will sound rather like a cracked record, but function, how a seed is dispersed, has little to do with the morphology of the plant parts involved. The terms used are for descriptive purposes only, and too much importance should not be attached to the fact that two groups have the same or different kinds of fruits. Thus there may be only very slight differences between a circumscissile capsule/pyxidium and an achene/utriculus, as Costea et al. (2003) emphasize in a study of the fruits of Amaranthus. Fruit morphology is evolutionarily rather labile, berries having evolved many times, for example, within monocots (e.g. Dahlgren & Clifford 1982; Givnish et al. 2005, 2006b), and capsules may even be derived from berries (Rasmussen et al. 2006). Fruit colour is important in animal-dispersed fruits, and Lu et al. (2019a) discuss its importance in diversification. Finally, it should be noted that there may be extensive commonality at the genetic level in the control of the development of different kinds of fruits. Thus the homologous MADS box genes SHP1/2 (Arabidopsis - the "shatterproof" gene) and TAGL1 (Solanum esculentum - tomato agamous-like) are involved in fruit dehiscence and fruit expansion and ripening respectively, and similar genes are also involved in other aspects of fruit development in other eudicots (Vrebalov et al. 2009). And when it comes to function, things are not always straightforward (c.f. Larson-Johnson 2023 and Augspurger & Hogan 1983: wind dispersal, Carpinus and Lonchocarpus),
Of the terms commonly used here, products of superior, syncarpous ovaries include a capsule, a dry, dehiscent, syncarpous fruit; berry, which has a ± entirely fleshy pericarp; and a drupe, which is indehiscent and fleshy, but with a more or less woody layer enclosing the seeds individually or together ("stones" or "pits"), certainly not always endocarpial in origin (e.g. Bobrov et al. 2005, 2009). An achene is a dry, indehiscent, single-seeded fruit with a moderately developed pericarp, and is generally used for the product of a single carpel, but it also used for the fruits of Asteraceae, which have a syncarpous inferior ovary; "cypsela" is a term used to distinguish these fruits from achenes, etc.). A nut is usually larger and with a very strong pericarp or fruit wall; it is generally used when the gynoecium is syncarpous, but the distinction between nut and achene is often not clear in the general literature. A follicle is a single carpel dehiscing down the adaxial side. The suffix "-let" is useful on occasion when describing fruit derived from a single carpel, so other terms sometimes used here for fruits derived from separate carpels include berrylet and drupelet. Fruits that are the products of an inferior ovary are described using the same terms as for fruits developed from syncarpous superior gynoecia. Of course, the actual tissues involved e.g. in being fleshy may well differ in the two cases (but see below). A schizocarp is any syncarpous fruit that splits into separate units, each usually based on a single carpel, and consisting of pericarp plus seed or seeds; these units are dispersed independently, and/or the seeds in them may later be released. Many schizocarps are variants of septicidal/septifragal fruit dehiscence (see below). A samara is any dry, winged, indehiscent fruit, and a lomentum is a fruit with transverse constrictions across which the fruit later breaks. A few taxa have more than one fruit type on the plant, a phenomenon known as heterocarpy/heterodiaspory (Venable 1985; Kaul et al. 2000). Heterocarpic plants with different fruit/seed morphologies, i.e. with dimorphic diaspores on the one plant that have different dispersal properties/germination requirements, are most frequent in plants growing in dry/saline conditions, and are commonest in Amaranthaceae (especially ex-Chenopodiaceae), also Asteraceae (Imbert 2002; Kadereit et al. 2017; Zerdoner Calasan & Kadereit 2023).
Capsules usually dehisce either down the septal or placental radii or down the interseptal or interplacental radii - such fruits are described as being septicidal (or septifragal, a variant) and loculicidal respectively. In this context, no distinction is made between fruits derived from ovaries with axile placentation and those with parietal placentation. Thus Ericoideae, Cleomaceae and Brassicaceae are all described as having septicidal capsules, even though the first has an ovary with septae and largely axile placentation, the second, a unilocular ovary and parietal placentation, and the third, a false septum and parietal placentation; dehiscence in all occurs in a topographically similar position (see also Stopp 1950). Dehiscence may also be circumscissile, the fruit opening around the circumference of the ovary or carpel (a fruit with this type of dehiscence is often called a pyxidium). In dry, dehiscent fruits with an inferior ovary, the actual dehiscence is often via openings in the pericarp at the top of the fruit, as in many Myrtales, and so dehiscence can reasonably be described using the terms just mentioned. Dehiscence may also occur through the sides of an inferior ovary, as in Campanuloideae, Orchidaceae, etc.; this situation is described clearly when it occurs, but dehiscence is here not simply septicidal or loculicidal. Dehiscence usually occurs ar the fruit dries out (xerochastic), but it sometimes occurs on wetting (hydrochastic), while increasing turgor pressure in fruits like Impatiens and Dorstenia causes the explosive dehiscence of the fruit.
The above terms are usually used to describe the products of the gynoecium of a single flower. Another way of describing fruits is to distinguish between a simple fruit, the product of a syncarpous gynoecium, or of a single, free carpel, an aggregate fruit, all the products of separate carpels of a single flower, and a multiple fruit, a unitary structure that is produced from several separate flowers, although the notion of a simple fruit so defined is rather vague. An anthocarp is a fruiting structure produced from a single flower but which is more or less closely invested by an accrescent calyx or perianth; although it is quite often used to describe the fruits of Nyctaginaceae, there is no reason why is should not apply to those of Dipterocarpaceae, Elaeagnaceae, etc., and it is a term of little utility.
Whether or not the calyx is deciduous, marcescent, persistent or accrescent (as in the fruit type anthocarp!) in fruit can be a surprisingly consistent character at higher levels and is generally mentioned in the characterizations.
For surveys of mucilages and gums in fruits, see Grubert (1974a, 1981) and Western (2011).
For a bibliography of seeds defined broadly, see Jensen (1998). Seed size (mass) is obviously a continuous variable. Thus dust seeds (see also the micro seeds of Martin 1946) have no precise definition except that they are very small, usually less than 5µg dry weight and 1 mm long, while the embryo is 0.2-0.3(-4) mm long, undifferentiated and with 4-100 cells (Eriksson & Kainulainen 2011; Baskin &anp; Baskin 2021b). Variation in seed size is placed in a phylogenetic context by Linkies et al. (2010) and especially Moles et al. (2005a, b). Reference to "large" or "small" seeds in the characterisations is always with respect to the seed size of their immediate relatives, and so is imprecise, but dust seeds are described above - details of endosperm and embryo are given in the characterizationms where known (see Baskin & Baskin 2021b).
Seeds may have a variety of appendages. These include arils, which "typically" are fleshy, post-fertilization outgrowths of the funicle, although there has in the past been a great deal of argument about what an aril really is and how it can be distinguished from an arillode (Corner 1953, 1976; van der Pijl 1955, 1966, 1982; Endress 1973; Kapil et al. 1980 and references). In the characterizations I do not restrict the term "aril" to funicular outgrowths alone, rather using the term for any more or less fleshy post-fertlization outgrowth of the seed, but I try to note the position of origin of the structure - in some cases, the obturator of an ovule may become an aril later. Caruncles are also widespread, and are generally somewhat harder outgrowths of the seed in the micropylar region; a coma is a tuft of hairs on the seed and has various origins (Hildebrand 1872).
I often use the term elaiosome, especially in discussions about diaspore dispersal, and this is another ecological, rather than a morphological, term, and it is applied to any appendage of a small seed, whether arillate or carunculate, or of a fruit(!) that attracts ants (dispersal or propagules by ants = myrmecochory), although it may also have other functions (Lisci et al. 1996, see also Beattie 1983; Giladi 2006); the distinction between an aril and a caruncle may be of little interest to an ant carrying a seed. Elaiosomes are notably common in a number of clades; Lengyel et al. (2009 [see especially the electronic Supplement], 2010) provide valuable information about the taxonomic distribution of elaiosomes while Fokuhl (2008) focused on European ant-dispersed plants. Peduncle elongation/arching may increase the effectiveness of ant dispersaL (Tanaka 2023). Some Lamiales have conspicuous seed pedestals of placental origin that may be attractive to ants (Rebernig & Weber 2007). All told, around 11,000 species of plants in 77 families are myrmecochorous, and myrmecochory has originated about 100 times (Lengyel et al. 2009, 2010). Interestingly, perhaps half the species of stick insects (Phasmatodea) lay eggs that mimic the seeds of myrmecochorous plants, and here what are called seed capitula function like elaiosomes (Hughes & Westoby 1992; Sellick 1997). Finally, appendages on cynipid oak galls may also function the same way as seed elaiosomes - they produce similar ant-attracting lipids, and the ants carry the galls underground (Warren II et al. 2022). For fossilized elaiosomes in Euphorbiaceae some 30-28.5 Ma, see Hamersma et al. (2022).
Details of seed coat anatomy are taken especially from Brandza (1891), Netolitsky (1926), Schnarf (1937: gymnosperms only), Huber (1969: old lilies, seed coat groupings make only slight sense systematically), Vaughan (1970: testa and tegmen not always distinguished), Corner (1976), Krach (1976), Takhtajan (editor: 1985, 1988, 1991, 1992, 2000, 2004), Danilova (editor: 1996), Werker (1997), and Bouman and his collaborators (e.g. Bouman & Boesewinkel 1997); see also Batygina (2006), and for fossil seeds, see Takhtajan (1974, 1982) and Budantsev (1994, 2005). As Wunderlich (1967a), Corner (1976), G. Dahlgren (1991) and many others have emphasized, variation in seed coat anatomy is of considerable systematic interest. Fortunately, details of seed coat anatomy can often be observed in hand sections that are stained for lignin, however, which cells are testal and which tegmic in origin - an important distinction - can be difficult to see if the coat is mature, and also in euasterids. Fot stomata in the seed coat, see Jernstedt and Clark (1979) and Wang and Hanstein (2016) and references; although they may be involved in photosynthesis, in other cases they are involved in water uptake by the seed.
The testa develops from the outer integument and the tegmen from the inner integument. The prefixes exo- meso- and endo- refer to tissues developing from the outer epidermis, the middle part, and inner epidermis respectively of either the testa or tegmen (Corner 1976; see also Schmid 1986). The shape, lignification and inclusions of the cells in these layers is of systematic interest, in particular, much attention has been paid to which part of the seed coat forms the protective or mechanical layer. A malpighian layer of vertically elongated and much thickened cells is quite common, although varying in origin (Werker 1997); it is often a systematically important character. A vascularised (see ovule variants above) and multiplicative testa and/or tegmen, in the latter the number of cell layers increasing after fertilization, are mentioned only when they occur. Some seeds have more or less annular operculum in the micropylar region - this has a variety of aliases and morphologies - which is pushed off during germination. Other seeds that have hard coats and physical dormancy have a water gap, a place in the coat where water enters the seed and starts the germination process (Turner et al. 2009); this water gap may be quite a cryptic feature anatomically. Distinctively thickened transfer cells may be found in various places in the seed coat (see e.g. Boraginaceae, Lamiales [endothelium] - Joel et al. 2012) or embryo.
Many asterids have only a single integument, and this also sometimes occurs elsewhere; the seed coat of such taxa is called a testa in the characterisations here. It might seems that whether or not the asterid exotesta is the same as the exotesta in angiosperms with two integuments is an open question since a single integument may be the result of the abortion of one integument or the congenital fusion of two integuments; this is discussed above Integument number. On balance the outer layer of an anatropous euasterid seed coat may indeed be an exotesta s. str., while one could argue that the outer layer of an orthotropous/staight unitegmic ovule might well be equivalent to an exotegmen (Gasser & Skinner 2018). The amount and patterning of the thickening of the walls of the exotestal cells of this single integument often varies greatly within a family, as in Gentianaceae (e.g. Guérin 1904) and Ericaceae; the thickening on the outer periclinal wall is often less than that on the other walls. However, much of the variation in thickening, cell shape, etc., of this single-layered exotestal-type seed coat is of interest at levels lower than those on which I focus here. For testal stomata, see Jernstedt and Clark (1979) and Wang and Hasenstein (2016) for literature.
The seed coat anatomy of holomycoheterotrophs (Bouman et al. 2002) and parasites may also be of little use when thinking about relationships since the seeds of such plants are often very reduced, light, and dispersed by wind; the coat is one or two cells across, and the cell walls are thin.
In drupe-, achene- or nut-type fruits in particular the seed coat is quite often undistinguished at maturity and systematically uninformative (e.g. Rodrigue 1893; c.f. in part Verkeke 1984). In these fruits, protection for the embryo is afforded by the fruit wall, and development of the seed coat becomes functionally superfluous. However, there may be a surprising amount of detail in the testa in the indehiscent cypsela of Asteraceae (e.g. Grau 1980) and in the drupaceous fruits in the Acronychia-Melicope clade of Rutaceae (Appelhans et al. 2014b).
For a survey of mucilages and gums in seeds, see Grubert (1974, 1981; Western 2011), and for the possible functions of these mucilages, see Western (2011), X. Yang et al. (2012) and Engelbrecht et al. (2014). Mucilage production in seeds when wetted, myxospermy (see also below), may be involved in seed dispersal and/or germination under rather dry conditions (Teixeira et al. 2019), and germination may occur even after the passage of the seed through the gut of a pigeon, although the extent of germination may depend on the composition of the mucilage - Kreitschitz et al. (2020) found that germination was quite high if the mucilage was hemicellulosic, lower/none if the mucilage was pectic or cellulosic. Some monocots have distinctive substances associated with the testa, in particular, black phytomelan and brownish phlobaphene. The former is also found in some Asteroideae; it is an inert and very resistant compound lacking nitrogen rather like green tea polyphenolics and is probably derived from catechol (see especially Graven et al. 1998 for what is known about its chemistry [not very much], etc.; Rasmussen et al. 2006).
The focus in the early literature on endosperm development tends to be on the evolution of endosperm "types". The initial divisions of the endosperm may be accompanied by cell wall formation (cellular endosperm), as in basal angiosperms, or they may involve the nucleus alone, cell walls forming only later (nuclear or free nuclear). In helobial endosperm, the endosperm forms two compartments in one or both of which the protoplasm is not immediately divided by wall formation despite division of the nucleus (see Samuelsson 1913; Dahlgren 1923; Stenar 1925; Wunderlich 1959). Krishnamurthy and Indra (1985) summarise discussion about the occurrence of helobial endosperm; authors like Swamy and Parameswaran (1962a) restrict its occurrence to monocots (but c.f. e.g. Mauritzon 1933). This classification hardly describes the subtleties of endosperm development (e.g. Floyd et al. 1999; Floyd & Friedman 2000 [comprehensive dissection of endosperm development], 2001; Friedman 2001a, b; Linkies et al. 2010). Thus the cells formed by the first division of the endosperm nucleus are frequently variously asymmetric (c.f. embryo sac development), the wall is transverse or oblique, cell divisions in one or both of the chambers that result from the first division may be nuclear or cellular, etc.. Nevertheless, Olson (2004) noted that many distinctive details of cellularization in the nuclear endosperm of Arabidopsis and cereals were similar, although cellular endosperm must have evolved indepedently in the two groups. In families like Asteraceae the distinction between cellular and nuclear endosperm is not sharp, that is, no, one, two, etc., divisions of the endosperm nucleus occur before cell walls begin to be laid down (Kapil & Sethi 1963). Endosperm is usually triploid, but other ploidy levels are known; thus Nymphaeales and Austrobaileyales, with 4-nucleate embryo sacs, have diploid endosperm, in Peperomia the endosperm may be 15n, while endosperm is not developed at all in a few angiosperms, e.g. Podostemaceae. See Olsen (2007) and Raghavan (2006) for the development and molecular biology of endosperm. Costa et al. (2014 and references) note that products of maternally-expressed genes may accumulate in the diploid central cell and hence via the endosperm affect early embryonic development, e.g. of the suspensor or the epidermis, while in crosses involving parents of different ploidy levels, maternal genome excess is associated with early cellularization and paternal excess with delayed cellularization (Gehring & Satyaki 2017). Haig (2020) in a useful summary looks not only at the ploidy level of the endosperm, but also at where endosperm nuclei come from and details of the variation that genomes from different nuclei might show. For more on endosperm developmental typologies see e.g. Di Fulvio and Cocucci (1986 and references), etc., and especially Shamrov (2021, 2022a). The latter recognises two main types, cellular and helobial, eight subtypes based on haustorial variation, and in cellular endosperm he recognizes a number of variations that reflect differences in the orientation of the cell walls during the second division of the endosperm. I do not pretend to have digested this...
Endosperm presence/absence refers to the situation in the ripe seed, and it can be a difficult character to deal with. As already mentioned, endosperm is very nearly always found in the very young embryo, but whether or not and in what quantity it persists is of interest here. There is a continuum between scanty and copious endosperm, and even the absence of endosperm is by no means as distinct a state as it might appear - it may be reduced to a single layer, or found in only a part of the seed, or vary in the stage at which it gets broken down (e.g. Guignard 1893 for an early discussion). Indeed, the function of a thin endosperm may not be as a food reserve, but when intact it may prevent germination (Linkies et al. 2010). Endosperm has been much studied in grasses, and different cell types such as aleurone, transfer, starchy endosperm and embryo surrounding cells, each with their own histories, can be recognised (Sabelli & Larkins 2009; see also Olsen 2007). Some distinctive endosperm variants, such as ploidy levels other than triploid in the endosperm cells, are mentioned as they occur. Only Viscum and its relatives (Santalaceae), Amaryllidaceae-Amaryllidoideae-Amaryllideae, and perhaps one or two other taxa have endosperm that is green and chlorophyllous.
Ruminate endosperm is sporadically distributed, from the relatively huge seeds of Myristicaceae to the small seeds of some Scrophulariaceae (it is rare in monocots). Rumination develops in various ways, and characterizes a number of taxa mostly at the lower levels of this survey (Periasamy 1962b; Bayer & Appel 1996 for a summary); Hartl (1959, q.v. also for terms) described the small, alveolate/ruminate seeds of some Lamiales.
Especially in asterids, endosperm haustoria, generally multicellular semi-invasive projections from the micropylar and/or chalazal ends of the seed, are common (e.g. Crété 1951; Mikesell 1990). They are mentioned only where they occur, as are other endosperm variants such as the highly asymmetric early endosperm development of Acanthaceae.
Endosperm food reserves are usually oily and/or proteinaceous, and when this is the case it is rarely mentioned. However, polysaccharides such as starch, hemicelluloses, and amyloid (Kooiman 1960; Czaja 1978; Meier & Reid 1982; Reid 1985; Buckeridge et al. 2000a; Buckeridge 2011) are also to be found (but amyloid is unknown from monocots), and the occurrence of such reserves is recorded (amyloid may occur in the embryo, too). Starchy seeds are often associated with parasitic and aquatic habits, but starchy and/or thick-walled and hemicellulosic endosperm is especially common in the commelinid monocots, but not Arecaceae (Huber 1969). ADP-glucose pyrophosphorylase, which is involved in starch synthesis, is largely located in the cytosol of the endosperm in the PACMAD/BEP clade in grasses, and in plastids in other flowering plants, but the sampling is poor (Beckles et al. 2001; Comparot-Moss & Denyer 2009). In monocots with starchy endosperm, as in several Poales and Commelinales, the outer part of the endosperm, the aleurone layer, commonly has other than starchy reserves (e.g. Xu & Messing 2008); this is widespread and is rarely mentioned. Lott (1981) described the inclusions found in protein bodies/aleurone grains in the embryos of a few plant families; although the sampling was poor, there were suggestions that Cucurbitaceae and some Apiaceae were distinctive in this respect. Starch grains in the young endosperm and in the vegetative plant are commonly of the "Hülle" type, that is, circular when seen from above, and homogeneous (Czaja 1978, see also Reichert 1913 for information); only variants of this type found in the seed are mentioned in the descriptions, but this is a difficult character to deal with.
In a few taxa the reserve tissue is in fact perisperm, derived from nucellar or similar tissue of the parental sporophyte. Rudall (2000) emphasized a distinction between perisperm and chalazosperm, the latter being derived from the chalaza, not from subdermal nucellar tissue. Even perisperm s. str. originates in various ways, and can develop from the nucellar epidermis alone, as in Acorales (e.g. Floyd & Friedman 2000), or from other parts of the nucellus - and there is a tendency to develop a sets of terms to describe this variation. Perisperm s. l. usually contains starch as a reserve (Floyd & Friedman 2000 for "basal" angiosperms), only rarely oil or protein, as in Acoraceae; the nature of the reserves here, where known, is mentioned in all cases.
Embryo development. Study of the patterns of cell division in young embryos and of the roles of the cells in the production of the different tissues of the mature embryo has resulted in embryos being placed in a number of "Types" and "Variations" (Johansen 1950; see e.g. Johri et al. 1992, pp. 62-80 for a good summary). This is perhaps because, as Souèges emphasized, it was thought that only internal factors affected development and hence there was the possibility of getting at "laws" of embryogeny - of which he recognized four (Souèges 1937); these laws allowed him to recognize groups of embryo types and to understand why they were linked ("enchaînement"!) in a classification (Souèges 1938). In this context, it seemed that developmental variants were of potentially great phylogenetic importance (see Wardlaw 1955 for a criticism, furthermore, to be told that an embryo belonged to the "Second period, Megarchetype IV, and Series A'" is not really very helpful). However, there is more than one way to look at these patterns and roles. Thus Yamazaki (1982, see also 1974) emphasized the position of origin of the root cortex initials when detailing his variants (see also Charbonnier & Vallade 2011). Johansen (1950, p. 94) observed of the six "types" he recognized, "merely to state a prophecy, it is believed that they will survive the test of time". To quote Lersten (2004: p. 179) "Many 19th century investigators of embryogeny concluded that cell walls in the early proembryo form by precise patterns of cell division that can be classified into types characteristic of certain groups of plants. Other investigators who bothered to sample several proembryos of the same species usually found that these patterns were variable, as Wardlaw (1955) pointed out." Indeed, little attention has often been paid to the sometimes quite extensive infraspecific variation in such features (but see e.g. Sachar 1956a). See also Shamrov (2021) for early embryo development - compared with endosperm development.
Variation in the plane of the first cell division of the zygote (Philipson 1990; Kaplan 1999: 1 ch. for summaries) seems to be at a rather high level. However, I have not utilized other variation in early embryo development very much, and I have largely ignored the embryo "types" that still remain the focus of some embryological studies. Taxa like Phaseolus and Poaceae have apparently disorganized cell divisions that contrast sharply with the more precise patterns found in Arabidopsis and Capsella, yet without any apparent effect on embryo development (Johri et al. 1992; Chandler et al. 2007; Lau et al. 2012).
The embryonic suspensor is not part of the embryo proper, i.e. it forms no part of the seedling, although in some cases an embryo may develop from it (P. Zhao et al. 2016 for references). There is considerable variation in suspensor size and morphology, particularly in groups like Fabaceae, and there are haustoria in the remarkable suspensors of Tropaeolum (Yeung & Meinke 1993), Orchidaceae, etc.. Di Fulvio (1979) suggested that suspensor morphology (along with endosperm type) characterized groups of families (e.g. in the asterid I group), however, in some taxa, the suspensor does not develop at all, and it is not easy to distinguish in monocots (Zhao et al. 2016). Yeung and Meinke (1993) discussed the the physiological significance of the suspensor; it may have highly endopolyploid cells with a genome size that can reach 8000 C. The radicle develops where the suspensor attaches to the embryo, although apparently not always in monocots (Yamashita 1976), perhaps because the suspensor is not clearly differentiated there. See also Raghavan (2006), Kawashima and Goldberg (2009), Hehenberger et al. (2012) and Lafon-Placette and Köhler (2014) for the relationship between the suspensor, the rest of the embryo, and the endosperm; the suspensor is in the initial provisioning route for the embryo, but failure of endosperm cellularization results in embryo arrest/death.
Embryo length varies considerably, and I have not treated this feature critically enough; Martin (1946) is still a very useful - and more consistent - source of much basic information (see also Baskin & Baskin 2007a, 2018; Ren & Zhu 2007; Linkies et al. 2010). The relative length of the embryo is emphasized here. It is the length of embryo relative to the length of the endosperm or perisperm ("seed" below), the latter length being the distance from the micropylar to the chalazal ends of those structures (the embryos of curved seeds may thus be absolutely longer than those of straight seeds of the same length). Long embryos are at least half the length of the mature seed. Medium embryos are about half the length of the seed, short embryos are between one half and about one tenth the length of the seed, while minute embryos are still smaller. The states of this character are arbitrarily delimited. Some embryos are notably broad (Martin 1948; Baskin & Baskin 2007b, 2018). Of course, that embryos are long does not mean that endosperm is necessarily absent, also, if seeds are minute (the "Micro" type of Martin 1946, the dust seeds of Eriksson & Kainulainen 2011, see also Baskin & Baskin 2014, 2021b) their embryos necessarily will be minute in absolute size, although using the criterion of relative length they may well be long. I have not mentioned relative embryo size for such seeds, however, their embryos are often undifferentiated, and the state of differentiation of the embryo at the time of dispersal of the seed is mentioned (see below, Embryo morphology, Germination).
Embryo position. The embryo is more or less central in the seed, the radicle being adjacent to the micropyle, if present, and any endosperm present surrounds the embryo. However, in a few families such as Poaceae, Polygonaceae, and also Caryophyllaceae and their relatives (this latter group makes up the old Curvembryonae) the embryo is lateral, lying against the testa on one side and adjacent to endosperm (or perisperm) on the other. Sometimes the position of the embryo relative to the fruit as a whole is of interest, thus in Lamiaceae the radicle points towards the base of the fruit and in Boraginaceae towards the apex - base and apex being relative to the pedicel.
Overall embryo morphology, that is, the gross morphology of the embryo at the time of fruit dispersal, varies considerably. In the characterizations I mention mainly cotyledon number, whether (and how) the cotyledons are folded, and whether the embryo is straight, curved, and/or flattened. In embryos derived from curved ovules the cotyledons are accumbent when the plane separating them is the same as that formed by the long axis of the seed plus chalaza or simply by the curvature of the embryo, incumbent when they are at right angles to this plane; they can (of course!) also be intermediate. In monocots the shape of the embryo varies at about the family level. The relative proportions of cotyledon:hypocotyl + radicle and the thickness of the cotyledon can be of systematic interest; in some Clusiaceae, Myrtaceae and Lecythidaceae in particular the embryo - sometimes quite massive - is largely hypocotylar. In mycoheterotrophic and/or parasitic plants with minute seeds the embryo is more or less undifferentiated, even the cotyledons not being visible (Eriksson & Kainulainen 2011). Larger seeds can also have undifferentiated embryos, thus at most weakly differentiated embryos characterize much of the entire Cyperaceae - Eriocaulaceae - Poaceae clade, although the embryos of Poaceae themselves represent another extreme in embryo differentiation having the first leaves of the seedling already developed before germination, and this is also seen in embryos of of Fabaceae-Faboideae, etc.. Some taxa in Lecythidaceae and Myrtaceae, for example, have macropodial embryos in which any cotyledon evident is at most small, even if the embryo is large (see Prance & Mori 1979; Mori & Prance 1990a: Lecythidaceae; Kausel 1955; McVaugh 1956; Amshoff 1958: Myrtaceae). Anatomical studies of some of these embryos would be of interest.
Data on embryo colours are taken largely from Yakolev and Zhukova (1980), but see also Janzen (1982) and Wright et al. (2000). The sampling is poor, but some taxa commonly have green embryos, others have white embryos; the latter is the common condition (the distinction is of course between embryos with chlorophyll and those without). Embryo colour may be under the control of a single gene (see Armstead et al. 2006). Seubert (1993) suggests that in monocots green embryos are found only in Alismatales.
Cotyledon number is usually an unambiguous character, although in taxa with two cotyledons like Cyclamen, some Ranunculaceae, etc., that early produce subterranean storage organs the cotyledons may be more or less connate. Burger (1998) and others have suggested that the single cotyledon of the monocots might be equivalent to the third leaf of the nymphaealean seedling, and that the young embryo of both Nelumbo and Nymphaeales is initially monocot-like. Unfortunately for this idea, Nelumbonaceae, Nymphaeaceae and monocots are not now thought to be immediately related. For the literature on monocotyly in broad-leaved angiosperms, and suggestions that Syneilesis (Asteraceae) seems to lack cotyledons entirely, see Teppner (2001). A few dicotyledous clades include taxa with single cotyledons, perhaps most notably in Apiaceae-Apioideae (Kljuykov et al. 2020), while polycotyledony is particularly noteworthy in Pinus (as in pine "nuts") and some other conifers, in Persoonia (Proteaceae), and it also occurs sporadically elsewhere, as in Idiospermum (Calycanthaceae); it is not always constant within a species (see Y.-B. Fu 2024).
Cotyledon position. The cotyledon(s) are usually lateral structures, but in monocots, with the exception of Poaceae, the single cotyledon appears to terminate the embryonic axis.
Germination. Baskin and Baskin (2004, 2014 and references; see also Finch-Savage & Leubner-Metzger 2006) provide much information on various kinds of dormancy of the seed, linking it with embryo size, etc. (see also Forbis et al. 2002). "Minute" embryos as defined above, e.g. in Ilex (see also Baskin & Baskin 2007), are often undifferentiated and require a period after dispersal for maturation to be completed (morphological dormancy - see Tuckett et al. 2010); even if they have cotyledons, etc., they will have to grow to fill up the inside of the seed before germination begins (see also Forbis et al. 2002). An extreme example of morphological dormancy occurs in Hydatellaceae in which differentiation of the embryo occurs only after germination has begun and the embryo has broken through the seed coat (Tuckett et al. 2010). A number of tropical trees have recalcitrant seeds that need to remain hydrated if germination is to occur, while others have very hard seed coats that have physical dormancy, orthodox seeds; in the latter, germination begins only when water starts entering the seed through a water gap or the like (Baskin et al. 2000; Turner et al. 2009; Gama-Arachchige et al. 2013; see also recalcitrant pollen above). Viviparous seeds are recalcitrant. Franchi et al. (2011) suggested the use of "dessication sensitivity" for recalcitrance and "dessication tolerance" for orthodoxy, which seems eminently sensible, but they did not follow their own advice. See also K. Liu et al. (2008) for dessication tolerance in seeds, Fogliani et al. (2017) for the dormancy type of the basal angiosperm, Willis et al. (2014b) for dormancy types and angiosperm diversification, and Subbiah et al. (2019) for the evolution of dormancy types.
Speculations on the evolution of embryo size, type and dormancy, should be treated with caution; Forbis et al. (2002) have recently evaluated embryo size (measured as the embryo:seed ratio) in the context of phylogeny (see Vandelook et al. 2012a for the ecological implications of this ratio). Coccucci (2005) provided a classification of the seeds of all spermatophytes that was based on the nature of the reserve tissue and how far the embryo had developed at maturity of the seed.
For seed/fruit heteromorphism, see Song and Wang (2015), L. Wang et al. (2010) and Gul et al. (2013). Seeds from the same capsule or different capsules on the same plant (e.g. Amaranthaceae-Chenopodioideae) or fruits from the same capitulum (e.g. Asteraceae) may vary substantially in morphologiy and also the conditions under which they will germinate.
Vivipary, the germination of the seed while still in the fruit and so on the maternal plant, is sporadic; it tends to be more of ecological than of systematic interest (Cota-Sánchez et al. 2007). The embryos of mangrove and aquatic, particularly marine, taxa like Nymphaeaceae, Ceratophyllaceae, Nelumbonaceae and Alismatales tend to be large and well developed, and seed germination there is frequently more or less precocious (Juncosa 1982), perhaps to ensure rapid establishment of the seedling after it germinates. Rapid establishment/very fast germination also occurs in groups like Amaranthaceae-esp. Chenopodioideae, some Acanthaceae, etc., that grow is more or less arid conditions where rapid establishment is at a premium (Parsons et al. 2014; Kadereit et al. 2017; Vandelook et al. 2021). At another extreme, in many dust seeds an association between seedling and host, whether fungus or other seed plant, has to be established if the seedling is to survive (Eriksson & Kainulainen 2011; Jacquemyn & Merckx 2019).
Seedling morphology provides a wealth of systematically interesting characters, and there are general surveys in e.g. de Vogel (1980), who both developed a complex typology of germination patterns and provided references to other such endeavours, Lubbock (1892: general), Burtt (1991b: survey of taxa with cryptocotylar germination), Duke (1969: tropical taxa), Ji and Ye (2003: seedling "types" of dicots), papers in Leck et al. (2008), esp. Leck and Outred (2008), and Garwood (2009: Neotropical taxa) - see also below for monocots in particular. However, much variation in seedling morphology is somewhat below the level that is of interest here (see Tillich 2007 for variation within Poales, for example).
In hypogeal seedlings the epicotyl is elongated, while in epigeal seedlings it is the hypocotyl that is elongated; cryptocotylar seedlings have non-photosynthetic cotyledons that remain enclosed by the seed coat and/or pericarp during germination, while in phanerocotylar seedlings the cotyledons are exposed and photosynthetic. There is frequent infrageneric variation in broad-leaved angiosperms in particular as to whether or not the hypocotyl is developed, and also whether or not the cotyledons are photosynthetic (e.g. Burtt 1972a). The shape of the exposed cotyledons can be of systematic interest, as in e.g. Bignoniaceae and Burseraceae, and also, as in monocots, whether the cotyledon is unifacial or bifacial. Cotyedonary vasculature can vary considerably within a family, and/or differ when compared with that of adult leaves (Stone 1970). In many monocots, and some aquatic broad-leaved angiosperms, the radicle is poorly developed or aborts; abortion of the radicle also occurs in some Cactaceae (Rodríguez-Rodríguez et al. 2003; Shishkova et al. 2013).
When it comes to monocot seedlings, much detail can be found in Arber (1925), Boyd (1932), and Huber (1969); Kaplan (1997: 1 ch. 5) and Tillich (1992, 2007) attempt to clarify monocot seedling morphology. Tillich (e.g. 2000, 2003) suggests that, with a few exceptions, there is little variation in seedling morphology within monocot families. Rather unfortunately, the terms hypogeal and epigeal as used in descriptions of monocot seedlings (e.g. in Kubitzki ed. 1998a, c; Linder & Caddick 2001) largely correspond to the terms crypto- and phanerocotylar used to describe the seedlings of broad-leaved angiosperms, a hypocotyl rarely being much developed in monocots (although this depends in part on the morphological interpretation of the monocot seedling... see Kaplan 1997: 1 ch. 5); I have used neither of these pairs of descriptors in the monocot characterisations. In a monocot seedling the cotyledon is commonly exposed and photosynthetic at least in its lower part, although morphologically different areas may be photosynthetic in different groups, while at least the apex remains enclosed by the testa/fruit wall and is absorbtive; a seedling can thus be phanerocotylar and cryptocotylar at the same time (see also Hydatella - Sokoloff et al. 2013b). As mentioned, any hypocotyl present is at most short by comparison to that of a broad-leaved angiosperm with epigeal germination (c.f. Tillich 2007 in part). In monocots in particular the plumule is frequently carried below the soil surface during the process of germination, a variety of mechanisms being involved - 1, direct downward growth of what is effectively a rhizome, 2, contractile roots, or 3, by the base of a leaf and associated bud growing down the primary root which has become a hollowed cylinder (Galil 1969; Haines & Lye 1979; Clarkson & Gifford 1987: literature, including examples of broad-leaved angiosperms), and this is associated with the hypogeal growth habit (= geophytes, plants with buds at or below ground level - Tribble et al. 2021) of many monocots - rhizomatous, cormose, bulbous (see below).
Phyllotactic patterns of very young plants are interesting. In monocots the first leaf is generally opposite the single cotyledon, whereas in broad-leaved angiosperms it is at right angles to the plane of the two cotyledons. Henslow (1893 and references) discussed some of the abrupt shifts in phyllotaxis in monocot seedlings, while in broad-leaved angiosperms the first two foliage leaves may be opposite, even when other leaves of the plant are two-ranked or spiral (e.g. some species of Phaseolus); when bijugate phyllotaxis becomes established varies within Rhizophoraceae (). Furthermore, the leaves of seedlings and young plants can have look very different from those of the adult.
THE GENOME.
Nucleus, Chromosome Number, Morphology and Organization.
Chromosome numbers are taken largely from secondary sources, including the various indices of chromosome numbers; all counts have been silently converted to haploid numbers (n). Raven (1975) is a convenient entry into the older literature in which base numbers (x) for families or orders are suggested, while Mayrose et al. (2010) discuss problems associated with establishing such numbers. A recent comprehensive attempt to establish base numbers that includes the great majority of angiosperm families is that by Carta et al. (2020), and their sugestionms are largely followed here. Carta et al. (2020) give Bayesian posterior probabilities for three possible chromosome numbers for each group, but here only the numbers that have values about one fifth or more of the most probable number are mentioned; it is extremely uncommon for the first number to have a value of 1.000 (Alseuosmiaceae are an exception!). Karyotype: For a survey of the various features that make up the karyotype, and their variation, see Kackson (1971). Detailed features of the karyotype have been used to characterize a number of monocot (in particular) groupings at around the family level in Asparagales and Liliales (e.g. Tamura 1995 summarises much information), and although I may have made less of such characters than I might, details are slowly being added. The karyotype is not notably conservative as was once thought, thus a bimodal karyotype characterizes Asparagaceae-Agavoideae, including genera that used to be in Hostaceae and Hyacinthaceae-Chlorogaloideae, etc., but it is also found elsewhere in Asparagales; indeed, the very decision that a karyotype is bimodal or not is not easy (e.g. Chase et al. 2000a). Muffato et al. (2023) discuss how the organisation of ancestral genomes can be reconstructed from genome sequences; such genomes allow one to think about things like inter- and intrachromosomal rearrangements over time and the contiguous ancestral regions reconstructed ultimately link on to chromosomes. Elliott et al. (2022b: see Supplement) graph a number of aspects of the karyotype for seed plant families, although since observations from at least 5 genera and 20 species were necessary for a family to be included (not unreasonable), families like Gnetaceae and Lentibulariaceaeare not in the graphs. Most chromosomes have telomeres, and it was thought that telomere construction was rather invariant, the sequence that was repeated being very conservative. However, there is quite a bit of variation that is systematically interesting at various level from individual genera on up, e.g. within Asparagales and within Solanaceae (e.g. Adams et al. 2001; Sýkorová et al. 2003a, b, 2006); there is also variation in telomere size, which is long in Caricaceae and Solanaceae and short in Brassicaceae and Caryophyllaceae (Shakirov et al. 2009). Centromeres, a part of a chromosome to which the spindle attached, are almost ubiquitous, but a few taxa have holocentric chromosomes (= diffuse centromeres, holokinetic chromosomes); for discussions, see Melters et al. (2012), Bureš et al. (2013), Bureš and Zedek (2014: holokinetic drive; Cuacos et al. (2015), Escudero et al. (2016b), Zedek and Bureš (2018) and Elliott et al. (2022b: pros and cons of holocentric chromosomes). In a survey or both animal and plant groups with holocentric chromosomes Márquez-Corro et al. (2018) could not not detect any obvious evolutionary advantage accruing to clades with such chromosomes. For information on the numbers and positions of 5S and 35S rDNA sites in the nuclei of seed plants, see Roa and Guerra (2012) and Garcia et al. (2016); Rosato et al. (2016) discuss the distribution of 45S RNA sites in bryophytes s.l.. Sex chromosomes are not very common, although they are probably underrecorded since they can be homomorphic (Filatov 2015) - see also above.
The occurrence of polyploidy within families, etc., is rarely mentioned except when it is particularly common. There has been much discussion on the effect polyploidy may have on diversification, and there are several surveys on the distribution of polyploidy with respect to geography, life form of the plant, etc. (Doyle & Coate 2018; Rice et al. 2019 and references). But if polyploidy is common, there has also been widespread subsequent reduction in chromosome numbers (e.g. Wolfe 2001), and in clades like Brassicaceae and Asteraceae chromosome number is especially plastic. For these and other reasons, working out the evolution of chromosome numbers can be difficult; Cusimano et al. (2012) show how using different methods of inferring ancestral numbers result in different estimates. Finally, note that genome size (see below) is at least in part independent of chromosome number in angiosperms, at least (e.g. Schnable et al. 2009; Garcia et al. 2010). All in all, the genome is turning out to be remarkably plastic.
There is considerable variation in ploidy levels of cells in the one plant (see also discussion on the embryonic suspensor above) that is connected to the developmental stage of the cell/tissue and the response of the plant to stress (see Bhosale et al. 2018). Indeed, endoreduplication of the genome is common in flowering plants, especially in the endosperm and cotyledons (Joubès & Chevalier 2000; Larkins et al. 2011), with a figure of 24,576n estimated for the cells of the endosperm haustorium in Arum maculatum (Bennett 2004). There may be no endoreduplication in some families, but there is no obvious correlation with phylogeny (Barow & Jovtchev 2007). Interestingly, endoreduplication is not recorded from liverworts, but it is quite common in mosses (Bainard & Newmaster 2010a, b).
There is increasing evidence that genome duplications (the focus in this literature is more on the results, not the cause, which is presumably some kind of auto-/allopolyploidy) have been quite common throughout the history of land plants and they are increasingly being implicated in their evolution and diversification (see also elsewhere for more details).
Some of the gene duplications that are often mentioned in the literature are linked to these genome duplications. For instance, much work has been done on the duplication of the PHY genes (genes for phytochrome variants); Mathews et al. (2003) follow the early evolution of the PHYA and PHYC genes (see also Mathews et al. 1995; Mathews & Sharrock 1996, etc.; for general background see Karniol et al. 2005 and especially Mathews 2006b [the big picture of phytochrome evolution in an ecological context]), while Schmidt and Schneider-Poetsch (2002) discuss the complex pattern of duplication of the PHY genes in the gymnosperms. The duplication of the RPB2 gene (the gene coding for the second largest subunit of RNA polymerase II) provides important phylogenetic information (Oxelman et al. 2004). For the duplication and distribution of the LEAFY gene, see Frohlich and Parker (2000) and Frohlich (2002). Rates of gene duplication independent of polyploidy are appreciable (Lynch & Conery 2000). Both gene and genome duplication are valuable sources of phylogenetic information and play an important role in evolution.
Nuclear genome size, whether measured as the 1C or C-value (C = unreplicated gametic genome) or Cx value (unreplicated basic genome) or recorded as weight (picograms) or base pair number, shows considerable variation. Within angiosperms, the genome varies around 2400-fold in size, Genislea margaretae (Lentibulariceae), has a 1 C value of only 0.065 pg/63 mbp while that of some species of Paris is as high as 152.2 pg/148.8 Gb (Greilhuber et al. 2006; Garcia et al. 2014; Hidalgo et al. 2017c), while that of Tmesipteris oblanceolata, at 160.45 Gbp, is the largest of all eukaryotes (Fernández et al. 2024). Leitch et al. (2005) summarise what is known about genome size for all seed plants (see Leitch et al. 2001 for gymnosperms; also Soltis et al. 2003; Leitch 2007) and Bennett and Leitch (2005) extend this to all land plants (see also Bai et al. 2012; Garcia et al. 2014, also Plant DNA C-values Database). Carta et al. (2020) give inferred ancestral 1 C values for the majority of angiosperm families, and these have been incorporated into the family characterizations. The variation they detail is largely consistent with broad-scale phylogeny; many flowering plants have very small genomes (1C = less than 1.4 pg) compared to those of most gymnosperms (see also Franks et al. 2012). Size variation of 1C flowering plant genomes has been broken up as follows: [very small] <1.4 pg - [small]- 3.5 pg - [intermediate] - 14.0 pg - [large] 35< pg [very large], see Soltis et al. (2003c). There are other lists of genome sizes in angiosperms (e.g. Hanson et al. 2005; Zonneveld et al. 2005; Garcia et al. 2010a; Zonnefeld 2012; Lyu et al. 2017). Suda et al. (2005) suggested that members of the Macaronesian flora tended to have particularly small genomes, while Lyu et al. (2017) suggested that true mangroves had notably smaller genomes than their non-mangrove relatives (or relatives that are mangrove associates), apparently largely because of a reduction in transposable elements in their genomes (much change in genome size is driven by the increase or decrease in numbers of these elements - Bennetzen et al. 2005). It has been suggested that both nitrogen availability and genome size tend to be low in carnivorous plants but high in parasitic plants (Vesely et al. 2013), but any connection between low genome size and carnivory is unclear - indeed, there is probably no connection (Veleba et al. 2020). There are a number of articles on genome size in the online Journal of Botany 2010 and Pellicer and Leitch (2020) have developed an online repository of plant genome size; see also Flowering Plant Evolution.
For variation in the length of the mitotic cycle, see Evans and Rees (1971); the length seems to be associated with the degree of coiling of the chromosomes.
Nuclear inclusions such as protein bodies in nuclei of various shapes and sizes are occasional (e.g. Thaler 1966; Speta 1977, 1979 for information); they are mentioned only when they occur. Other nuclear inclusions in asterids are described by Bigazzi (e.g. 1995), and literature describing such inclusions dates back to the late nineteenth century (see Speta 1979).
Plastid and Mitochondrial Genomes; Their Organization, etc..
For general information on mitochondrion and chloroplast evolution, see Hagemann (2004) and Volkmar and Knoop (2010) and for plastid evolution, see Sibbald and Archibald (2020); there may be connections/similarities between the evolution of mitochondrial (= mitogenome) and chloroplast (= plastome) genomes (Sloan et al. 2012b). Evolution of the plastome in particular, but also to a certain extent the mitogenome, has been notably extensive in holoparasitic plants; see Sanchez-Puerta et al. (2023) for a review that focuses on Balanophoraceae. The plastome is commonly circular and the whole genome can be considered to be but a single gene (Doyle 1992, p. 144: "molecular systematics as one-character taxonomy"), while the mitogenome is physically quite variable, being linear, branched, or consisting of (numerous) circular chromosomes. Inclusion of RNA editing sites may affect the results of analyses of mitogenomes or plastomes, and this is discussed further by Dong et al. (2023), who recommended excluding them - gymnosperms and lycophytes in partricular may have many such sites. A question is whether or not recombination occurs in these organelles (e.g. McCauley 2013; Shrestha 2019; Gonçalves et al. 2019, 2020b). There is trans-splicing in the mitogenome in vascular plants (W. Guo et al. 2020). Overall, the mitogenome in both flowering plants and ferns has lower substitution rates than the plastome (Cárdenas & Lehtonen 2023). Ramsey and Mandel (2019) emphasized the implications of heteroplasmy, with different plastid and/or mitogenomes within a cell or individual (a quite common phenomenon), for evolution, phylogeny reconstruction, etc..
Plastids and mitochondria are most often transmitted by a single parent, but biparental inheritance, transmission occuring via either parent, is not uncommon (Q. Zhang et al. 2003; Zhang & Sodmergen 2010; Rogalski et al. 2015; Ramsey & Mandel 2019). For surveys of chloroplast inheritance, whether via the pollen grain and/or the egg cell, see Corriveau and Coleman (1986), Owens et al. (1995), Mogensen (1996), Zhang et al. (2003), Snijder et al. (2007), Hu et al. (2008), etc.; although the latter is most frequent, overall there is a great deal of variation, with paternal transmission potentially occurring in some 20% of angiosperms, and perhaps becoming increasingly frequent there (Zhang & Sodmergen 2010). However, it is difficult to understand why there have been switches between the different modes of inheritance (also true of mitochondria), although the operation of Muller's ratchet may be an element in any explanation (Birky 1995; Greiner et al. 2014). In systems that end up with maternal transmission of the plastids, elimination of the plastids from the male gametes may occur in various ways (e.g. Sears 1980; Birky 1995; Zhang & Sodmergen 2010). For heteroplasmidy, generally uncommon except in conifers, see C. Lee et al. (2020 and references). There is some connection between extensive rearrangements of the plastid genome, incompatibility between the plastid and nuclear genomes, and biparental inheritance of the plastid genome, as in groups like Campanulaceae, Geraniaceae and Passifloraceae (Shrestha et al. 2019; Sobanski et al. 2019: chloroplast competition; Cauz-Santos et al. 2020). There may be plastome—nuclear genome incompatibility (PGI) in hybrids, with death of the plastids and resultant variegation or complete albinism (Ruhlman & Jansen 2018). Genome variation in plastomes and chondromes is for the most part lower than that in the nuclei.
Jansen and Ruhlman (2012) summarize much literature on the evolution of the chloroplast genome/plastome in seed plants, Mower et al. (2018) focus more on lycophytes, and Mower and Vickrey (2018) and Gitzendanner et al. (2018b) on land plants as a whole; see also Ruhlman and Jansen (2018), C. Lee et al. (2020) and Sibbald and Archibald (2020). Some major genome rearrangements are mentioned in the characterizations. The chloroplast inverted repeat (IR) characterizes most land plants and a few of their immediate relatives (e.g. Turmel et al. 1999), but it can be lost, as in a major clade of Fabaceae-Faboideae (Wojciechowski 2003 and references), in some extreme parasites/mycoheterotrophs, etc. (see Garrett et al. 2023: Table 2 for a list of the taxa involved) while there is also no inversion in some species of Selaginella where the IR has been converted into a direct repeat (Mower et al. 2018). Cupressales and Pinales are other groups that have lost a copy of the IR, probably independently (Chaw et al. 2018), and Guo et al. (2014) discuss changes between predominant and substoichimetric isomers of plastid genomes by substoichimetric shifting in the latter group in particular. In such a situation, new IRs may develop (J. Li et al. 2016). Early literature on the use of chloroplast DNA rearrangements in reconstructing phylogeny is summarized by Downie and Palmer (1992b), and there is much information on later work in Raubeson and Jansen (2005); see also Cosner et al. (2004). For the Plastid-Encoded RNA Polymerase (PEP) subunits, α (encoded by the rpoA gene), β (rpoB), β' (rpoC1), and β'' (rpoC2), see Blazier et al. (2016). Data on the loss of the intron in the chloroplast rpl2 gene is taken from Downie et al. (1991), that in the rpoC1 intron from Downie et al. (1996; see also Labiak & Karol 2017), and in the rpl16 gene from Campagna and Downie (1998). For the evolution of plastid ndh genes, see Martín and Sabater (2010), Lallemand et al. (2019a) and especially Mower et al. (2021) for possible connections between various distinctive life styles, including parasitism, carnivory and growth in dry conditions, all of which may affect the photosynthetic process and result in the loss of such genes (and so of the ability to produce much chloroplast ATP) - for mixotrophy and holomycoheterotrophy, see Orchidaceae in particular. Lallemand et al. (2019) Sabater (2021) notes that some gymnosperms (including Gnetales) also lack ndh genes, and they may be very long-lived plants, the function of these genes there perhaps being different than in other plants. These genes may also be lost in the mitochondria. There are also connections with the absence of necrosis in plants that lack ndh genes, so perhaps linking to the very long-lived needles in some pines and perhaps also the fact that in plants like Viscum album the leaves fall from the plant when green (Schröder et al. 2022). Millen et al. (2001) and Su et al. (2014) summarize information about the loss of the infA gene from the chloroplast which has happened many times in the rosids alone (or it moves around in a way that is not understood). For the loss of the ndh genes in the chloroplast of Pinus thunbergii, see Wakasugi et al. (1994) and Martín and Sabater (2010), and for its sporadic loss more generally in land plants, see Labiak and Karol (2017) and Qu et al. (2022) and references. There may be substantial phylogenetic signal in such characters, but some genes are lost/move so frequently that any signal is difficult to discern, at least with current sampling (e.g. Su et al. 2014), although since chloroplasts can now be sequenced for around two a penny, things are changing (e.g. H.-T. Li et al. 2019: 2,881 plastid genomes). S. W. Graham et al. (2000) discussed microstructural changes in noncoding DNA; the distributions of these changes support clades such as all angiosperms, the eudicots, monocots minus Acorus, and Austrobaileyales. For substitution rates in the plastome comparing the single copy with the inverted repeat regions (those in the latter are lower), see Zhu et al. (2015). The maternal inheritance of the plastome in Nicotiana tabacum tends to break down when male gametogenesis is at low temperatures (Chung et al. 2023). Overall there is relatively little variation in the size of the plastome in autotrophic plants, variation in the size of the IR perhaps being most common. There are serious issues concerning the assembly and annotation of plastome genomes (e.g. Qu et al. 2023; Joste & Wanke 2024). For plastomes in mycoheterotrophic plants, see under the latter above.
There is a general issue that I touch on: Phenomena like organelle capture, hybridizatioin and introgression, etc., may mean that trees based on chloroplast and nuclear data have different topologies. The extensive use of data from the plastome in producing phylogenetic trees is in part a historical accident - plastome data were early used and were easy to obtain - and indeed the topologies they yielded have often stood the test of time. However, as Doyle (2022: p. 486) noted, "There simply appears to be no good reason to chose the plastome as the primary source of data for reconstructing species trees"; not that these plastome≡single gene trees are without interest - far from it - but it is species trees that are ultimately of importance here, and comparisons between numerous (nuclear) gene trees may well clarify the history of the species.
For the evolution of the mitochondrial genome, the mitogenome, see Knoop et al. (2010), Knoop (2012), Gualberto et al. (2014), Mower (2020: land plants), G. Petersen et al. (2020), etc.; less is known about the mitogenome than the plastome. Overall, plant mitogenomes are large and variable in size, structure, gene and intron content, so synteny breaks down, there is extensive RNA editing, extreme differences in substitution rates and frequent incorporation of retrotranscribed sequences, and they show low substitution rates - these may even be clock-like (Cole et al. 2018) - when compared with those of nuclear or chloroplast genomes. Horizontal gene transfer (HGT) of mitochondrial DNA is also common as is movement of DNA between genomic compartments (see below). Note also that like the plastome, the mitogenome as a whole basically represents but a single gene (e.g. Palmer & Herbon 1988; G. Petersen et al. 2017; Christensen 2021). The mitogenome can be huge and is sometimes organised as a large number of circular chromosomes, not all necessarily with functional genes, as in Silene noctiflora (at least 100 chromosomes), and since loss of mitogenome chromosomes with non-functional genes is quite easy there is infraspecific variation in chromosome number (Wu et al. 2015 and references; Sanchez-Puerta et al. 2016). Plasmids are common in mitochondria, and they may be circular or linear. Although plasmid sequences are usually quite different from those of the mitogenome, they may have some similarities with the nuclear genome (Gualberto et al. 2014 and references). Y. L. Qiu has suggested that how mitochondrial introns are spliced (cis or trans) may be of systematic significance (see Cameron et al. 2003). There can be considerable mitochondrial polymorphism within an individual, which can cause complications when analyzing relationships using nrDNA (Alvarez & Wendel 2003; J. Song et al. 2012; Weitmier et al. 2015); Small et al. (1987) provide an early description of how uncommon and substoichiometric variants might be generated and how they might become common. Despite such problems, Q. Lin et al. (2022) noted that the low substitution rate in the mitochondrial genome might be an advantage in mycoheterotrophic plants where plastome substitution rates could be excessively high and a focus on gene sequence and ignoring order would allow the combination of data from the whole mitogenome - the mitogenome was largely unaffected by mycoheterotrophy, and they provided examples from Ericaceae and Dioscoreales, q.v.. As with genome size, the rate of mitogenome rearrangement, mediated by repeats, is very variable, but can be high (Cole et al. 2018); Jiang et al. (2023) found such recombinations in Taraxacum mongolicum. For recombination in the mitogenome of embryophytes, see Sullivan et al. (2019). DeBenedetto et al. (1992) and Joly et al. (2001) discuss the loss of the coxII.i.3 intron from the mitochondrion; there is substantial variation in this within Dipsacales and Gentianales, for example.
Intergenomic movement (intracellular gene transfer - IGT). Adams et al. (2001, 2002a, b) follow the loss of a number of genes from the flowering plant mitochondrial genome, probably because of their transfer to the nucleus; the rps13 gene seems to have been replaced in many Rosids by a chloroplast gene that is now in the nucleus (see also Park et al. 2015 for mitochondrion to nucleus moves). Jansen et al. (2010 and references) discuss the movement of the rpl22 gene from the chloroplast to the nucleus and Rousseau-Gueutin et al. (2013) the accD gene; overall, such movements are rather uncommon (Park et al. 2015b). In a number of cases, fairly high-level groupings appear to be marked by gene migration, the loss of the rps2 and rps11 genes perhaps in Pentapetalae being particularly significant systematically (see also Bergthorsson et al. 2003; Ong & Palmer 2006), although in other cases individual genera (or perhaps groups of genera) such as Phlox, Allium, etc., show quite extensive migration of genes. Genes involved in these transfers are mostly ribosomal protein and succinate dehydrogenase genes, not respiratory genes (Palmer et al. 2000; Adamas et al. 2002). Indeed, there has been a certain amount of transfer of genes between genome compartments in seed plants (Keeling & Palmer 2008; Bock 2009; Talianova & Janousek 2011 for summaries). Mitochondrial genes in particular are transferred relatively easily (Sanchez-Puerta 2014; T. Sun et al. 2016; Gandini & Sanchez-Puerta 2017), and this may wreak havoc in phylogenetic analyses (Hao et al. 2010). Y. Chen et al. (2023) looked at nuclear organellar genes with a focus on Poaceae (15 spp. examined), overall, mitochondrial genes moved more than plastid genes, but in both cases gene evolution became more dynamic after the move. There is extensive parallel transfer of the mitochondrial cox1 intron in flowering plants (Sanchez-Puerta et al. 2008: mechanism?, 2011: c.f. Cusimano et al. 2008), also transfer of plastid genes from mitochondrion to mitochondrion (Gandini & Sanchez-Puerta 2017 and references). Such transfers are essentially a continuation of the adjustment between host and endosymbiont that resulted in organelles such as chloroplasts and mitochondria in the first place (e.g. Soucy et al. 2015).
Nuclear Genome. Obviously, sequencing of the nuclear genome or parts of it are now commonplace - witness the 7,500+ genera that were recently included in an Angiosperms353 phylogenetic study of angiosperms (Zuntini et al. 2024). However, there are a couple of other issues to be discussed first.
1. Tettelin et al. (2005) introduced the concept of the pan-genome, which includes core genes, present in all individuals of a species, and accessory genes, present in only some individuals – and they noted that the gene reservoir that could be included in bacterial pan-genomes in particular could be huge. Although this concept was initially applied to bacteria, it has been used in other cases where there is horizontal gene transfer by one means or another, and it has even been extended to movement of genes between genomes within grasses (e.g. Tao et al. 2021; Grass Phylogeny Working Group 2024).
2. Horizontal gene transfer, HGT, "the movement of genetic material across branches of the tree of life" (Van Etten & Bhattacharya 2020: p. 915), is rather uncommon, if evolutionarily disproportionately important, in streptophytes. HGT is reported to be sporadic in Bryophyta s.l., etc., and some genes from fungi, algae, etc., have moved to these plants. Van Etten and Bhattacharya (2020) found that only a small portion of the genome was involved, perhaps 0.04-2.97(-6.49)%, although these figures may be underestimates. The genes transferred may be involved in extremophily, colonization of the land, etc., however, HGT in also known in mesophytic plants, parasites, etc., and the genes transferred have a variety of metabolic functions. HGT was involved in major evolutionary transitions like the origin of primary plastids (Van Etten & Bhattacharya 2020), while for HGT in Zygnematophyceae and the origin of land plants, see Cheng et al. (2019), Van Etten and Bhattacharya (2020), etc.. Lateral gene transfer is quite common in Poaceae, q.v., and here reproductive contamination through illegitimate pollination seems a possible cause.
In some parasitic plants there has been extensive replacement of parasite mitochondrial genes by those of the host (C. C. Davis & Xi 2015; Sanchez-Puerta et al. 2016 and Gatica-Soria 2021, both Lophophytum mirabile) or movement of other genes from the parasite to the host with complicated patterns of replacement of one of the copies (Mower et al. 2010), and of course the host and parasite are not at all related. Mitochondria are usually the vectors of such genes, and they can incorporate substantial amounts of the chloroplast genome; the movement between species is probably preceded by intragenomic movement from chloroplast to mitochondrion (Richardson & Palmer 2007 for a summary; Sanchez-Puerta et al. 2008; Chaw et al. 2008; Alverson et al. 2010; W. Wang et al. 2012; D. R. Smith 2013; Gandini & Sanchez-Puerta 2017). C. C. Davis and Xi (2015), Cusimano and Renner (2019) and Z. Yang et al. (2019) discuss HGT in parasitic plants in general, and not surprisingly there can also be HGT in mycoheterotrophs (Cusimano & Renner 2019). HGT may also happen when there is grafting (Sanchez-Puerta 2014 for references), although in the latter case the individuals involved are often the same species, in epiphytes, when there is wounding, in illegitimate pollination (c.f. Poaceae above) (G. Petersen et al. 2020). In some host—parasite associations genes, including transposable elements, from various compartments move from the host to the parasite (Davis & Wurdack 2004: mitochondrion; Mower et al. 2004; Yoshida et al. 2010: nucleus; Filipowicz & Renner 2010; Davis & Xi 2015; Sanchez-Puerta et al. 2016; Gandini & Sanchez-Puerta 2017); movement may be extensive, and the genes moved may be expressed and functional (Xi et al. 2013; T. Sun et al. 2016: transposable elements; Sanchez-Puerta et al. 2016; Kado and Innan 2018; Z. Yang et al. 2019). Genes can also move between between angiosperms and gymnosperms and even angiosperms and bryophytes, and this may result in large and complex chimaeric mitochondrial genomes that are little understood, as in Amnborella (Won & Renner 2003; Bergthorsson et al. 2004; Renner & Bellot 2012; Rice et al. 2013; Park et al. 2015); G. Petersen et al. (2006) sound a note of caution in the interpretation of such phenomena. Some parasites with a chimaeric mitochondrial genome have a reduced photosynthetic capacity (Gatica-Soria et al. 2021 and references). How such transfers, whatever the genomic compartments in question (e.g. foreign plastid sequences in mitochondria - Gandini & Sanchez-Puerta 2017), occur unless parasitism is involved is unclear. However, note that in Poaceae, at least, just about any random pollen grain can at least germinate on the stigma of the one plant (Kellogg 2015 and references), and this may set up the possibility for wide HGT in that family. HGT between fungi and plants may occur via mycorrhizal/endophytic associations, and HGT between cnidaria, sea anemones and plants (for the latter, see Hoang et al. 2009) has also been recorded. Wickell and Li (2019) discuss the evolutionary significance of HGT in plants in general; for HGT, see also Pereira et al. (2022) and elsewhere.
Sequence Data. Support for many of the relationships suggested here comes from analyses of variation in molecular sequence data that continue to pour out; many of the papers involved are cited separately in the appropriate places on the order pages. Not all sequences are of equal value when it comes to understanding relationships, with mitochondrial ITS sequences (Álvarez & Wendel 2003) and mitochondrial information in general (G. Petersen et al. 2006b) perhaps being particularly difficult to use (but see Q. Lin et al. 2022b for a study with a focus on Thismiaceae). Initially most of the data came from analyses of one or a few genes from the plastome (Gitzendanner et al. 2018b for an entry into the vast literature), and it is going to be interesting to see how hypotheses of relationship developed using this genome hold up as massive amounts of data from all three genomic compartments become available for analysis in the next few years (e.g. Davis et al. 2014). Indeed, it should be remembered that classificatory changes in land plants up around about 2019 were often dependent on phylogenies based on variation in a few chloroplast genes, perhaps with the odd nuclear gene thrown in, a problematic practice (e.g. see Gonçalves et al. 2020b); as mentioned above, both the plastome and mitogenome can be thought of as single genes (e.g. Doyle 1992, 2022).
The rate of change in molecular sequences is very unequal across the tree, and some clades show notably accelerated rates, rates also differ across genomic compartments, mitochondrial genes, for example, but not the mitochondrial ganome as a whole, tending to evolve only slowly (e.g. Q. Lin et al. 2022b). Clades with accelerated rates often have distinctive life styles, whether herbaceous, parasitic, mycoheterotrophic, or carnivorous, although abrupt rate changes may also occur elsewhere (e.g. Duff & Nickrent 1997; Caddick et al. 2002a; Müller et al. 2004; G. Petersen et al. 2006b). Thus the rate of change of the nrITS region was found to be faster in herbs than in woody plants (Kay et al. 2006), and the rate of molecular evolution in general is faster in herbs than in trees (e.g. Smith & Donoghue 2008; Couvreur et al. 2009; c.f. Nürk et al. 2019: insular radiations). For rate changes in molecular evolution of 18S rDNA of mycoheterotrophic and parasitic taxa, see Lemaire et al. (2011a); it has had little effect on function. A number of these rate changes are indicated on the order pages, but take them all with a grain of salt. Although the rate of change of mitochondrial gene sequences tends to be low, there have been some cases of spectacular acceleration (up to 10,000X the normal rate, e.g. Mower et al. 2007) and the mitochondrial genome varies greatly in size, etc. (Alverson et al. 2010; G. Petersen et al. 2020; etc.).
Host-plant preferences, particularly of butterfly larvae (e.g. Forbes 1958; Ehrlich & Raven 1964; Ackery 1988, 1991; Farrell et al. 1992; Powell et al. 1999; Ward et al. 2003; Pichersky & Raguso 2018), but also of other insects that are herbivores or otherwise closely associatwd with plants, can provide information that bears on land-plant evolution or even indirectly on relationships, although interpretation may be difficult and there is no recent synthesis of the huge and scattered literature. Any synthesis is made more difficult because studies have tended to focus either on temperate or on tropical areas (see Janz & Nylin 1998; Novotny & Basset 2005; Lewinsohn et al. 2005); Fiedler (1998) compared host plant utilization by temperate and tropical butterflies. Larvae of individual species may also show interesting host-plant preference patterns. There is a valuable database of caterpillar host plants that I have consulted at times - see Hosts - and associated with this are conventional books that detail food preferences of the caterpillars of parts of the area covered in the database (Robinson et al. 2001, 2002); note also papers in Scriber et al. (1995) and especially Berenbaum (1995) for swallowtails (Papilionidae) and their foodplants. Similarly, the patterns of fungal parasite/host associations (see mycorrhizae and endophytes above, also elsewhere) are also often of some systematic interest, and Savile (1979b, also Hijwegen 1979 and other papers in Symb. Bot. Upsalienses 22(4). 1979) provide a comprehensive and appropriately cautious summary of these associations, although much work has been carried out since. A number of plant/herbivore and plant/parasite associations are mentioned in the pages below
Since both fungi and insects that eat, parasitize or are otherwise closely associated with plants are often affected by the chemistry of their hosts, parallelisms and convergences in chemistry may be reflected by finding related fungi or butterfly or moth groups (for example) on plants with similar chemistries, but that are otherwise unrelated. Thus members of the pairs magnoliids and Rutaceae (both have similar alkaloids), Rutaceae and Apiaceae (furanocoumarins), Putranjivaceae and Brassicales (glucosinolates), and Daphniphyllaceae and asterids (iridoids) have caterpillars of related butterflies eating them. Along the same lines, that similar caterpillars are found e.g. on Onagraceae and Vitaceae (Forbes 1956) may reflect the fact that both groups have raphides that deter some herbivores.
Some organisms co-opt noxious metabolites used as defence by plants for their own defence. Nishida (2002) summarized sequestration of defensive compounds from plants by lepidoptera, Opiz and Müller (2009) that by insects in general; see also Bowers (2022: iridoids, cardenolides, etc.).
The ability of grafts between different species, genera, and even families to take reflects something of the underlying physiology of the plants concerned; grafts have been made in gymnosperms, monocots and of course also in other angiosperms. Grafting is important in crop production in annual Cucurbitaceae and Solanaceae in particular, helping to protect against soil-borne diseases, increase yield, etc. (A. R. Davis et al. 2008; Warschefsky et al. 2016; Kyriacou et al. 2017). Grafts between distantly related plants have sometimes been carried out (e.g. see Horne 1914; Hartmann 1951; Reeves et al. 2022). Thus Horne (1914) noted that Ilex and Buxus could be intergrafted, although the graft did not really take - see also Garryaceae, Pinaceae and Portulacaceae; successful grafts have been established between C3 and C4 grasses of the PACMAD and BOP clades, the graft junction being made in the mesocotylar area (Reeves et al. 2022). Notaguchi et al. (2020: Fig. 1) were able to intergraft members of a variety of different families, including some monocots, using Nicotiana stem as an interscion (i.e. stock-Nicotiana stem-scion); extracellular β-1,4-glucanases in the Nicotiana played a central role. Chloroplasts and other organelles can move across graft junctions via plasmodesmata (Stegemann et al. 2012; Sanchez-Puerta 2014 and references) in a way similar to parasitism, the parasite here being the eqivalents of the interscion - e.g. see Cuscuta (Liu et al. 2019).