EMBRYOPSIDA Pirani & Prado

Gametophyte dominant, independent, multicellular, initially ±globular, not motile, branched; showing gravitropism; glycolate oxidase +, glycolate metabolism in leaf peroxisomes [glyoxysomes], acquisition of phenylalanine lysase* [PAL], flavonoid synthesis*, microbial terpene synthase-like genes +, triterpenoids produced by CYP716 enzymes, CYP73 and phenylpropanoid metabolism [development of phenolic network], xyloglucans in primary cell wall, side chains charged; plant poikilohydrous [protoplasm dessication tolerant], ectohydrous [free water outside plant physiologically important]; thalloid, leafy, with single-celled apical meristem, tissues little differentiated, rhizoids +, unicellular; chloroplasts several per cell, pyrenoids 0; centrioles/centrosomes in vegetative cells 0, microtubules with γ-tubulin along their lengths [?here], interphase microtubules form hoop-like system; metaphase spindle anastral, predictive preprophase band + [with microtubules and F-actin; where new cell wall will form], phragmoplast + [cell wall deposition centrifugal, from around the anaphase spindle], plasmodesmata +; antheridia and archegonia +, jacketed*, surficial; blepharoplast +, centrioles develop de novo, bicentriole pair coaxial, separate at midpoint, centrioles rotate, associated with basal bodies of cilia, multilayered structure + [4 layers: L1, L4, tubules; L2, L3, short vertical lamellae] (0), spline + [tubules from L1 encircling spermatid], basal body 200-250 nm long, associated with amorphous electron-dense material, microtubules in basal end lacking symmetry, stellate array of filaments in transition zone extended, axonemal cap 0 [microtubules disorganized at apex of cilium]; male gametes [spermatozoids] with a left-handed coil, cilia 2, lateral, asymmetrical; oogamy; sporophyte +*, multicellular, growth 3-dimensional*, cuticle +*, plane of first cell division transverse [with respect to long axis of archegonium/embryo sac], sporangium and upper part of seta developing from epibasal cell [towards the archegonial neck, exoscopic], with at least transient apical cell [?level], initially surrounded by and dependent on gametophyte, placental transfer cells +, in both sporophyte and gametophyte, wall ingrowths develop early; suspensor/foot +, cells at foot tip somewhat haustorial; sporangium +, single, terminal, dehiscence longitudinal; meiosis sporic, monoplastidic, MTOC [= MicroTubule Organizing Centre] associated with plastid, sporocytes 4-lobed, cytokinesis simultaneous, preceding nuclear division, quadripolar microtubule system +; wall development both centripetal and centrifugal, 1000 spores/sporangium, sporopollenin in the spore wall* laid down in association with trilamellar layers [white-line centred lamellae; tripartite lamellae]; plastid transmission maternal; nuclear genome [1C] <1.4 pg, main telomere sequence motif TTTAGGG, KNOX1 and KNOX2 [duplication] and LEAFY genes present, ethylene involved in cell elongation; chloroplast genome with close association between trnLUAA and trnFGAA genes [precursors for starch synthesis], tufA, minD, minE genes moved to nucleus; mitochondrial trnS(gcu) and trnN(guu) genes +.

Many of the bolded characters in the characterization above are apomorphies of more or less inclusive clades of streptophytes along the lineage leading to the embryophytes, not apomorphies of crown-group embryophytes per se.

All groups below are crown groups, nearly all are extant. Characters mentioned are those of the immediate common ancestor of the group, [] contains explanatory material, () features common in clade, exact status unclear.

POLYSPORANGIOPHYTA†

Sporophyte well developed, branched, branching dichotomous, potentially indeterminate; hydroids +; stomata on stem; sporangia several, terminal; spore walls not multilamellate [?here].

II. TRACHEOPHYTA / VASCULAR PLANTS

Sporophyte long lived, cells polyplastidic, photosynthetic red light response, stomata open in response to blue light; plant homoiohydrous [water content of protoplasm relatively stable]; control of leaf hydration passive; plant endohydrous [physiologically important free water inside plant]; PIN[auxin efflux facilitators]-mediated polar auxin transport; (condensed or nonhydrolyzable tannins/proanthocyanidins +); borate cross-linked rhamnogalactan II, xyloglucans with side chains uncharged [?level], in secondary walls of vascular and mechanical tissue; lignins +; roots +, often ≤1 mm across, root hairs and root cap +; stem apex multicellular [several apical initials, no tunica], with cytohistochemical zonation, plasmodesmata formation based on cell lineage; vascular development acropetal, tracheids +, in both protoxylem and metaxylem, G- and S-types; sieve cells + [nucleus degenerating]; endodermis +; stomata numerous, involved in gas exchange; leaves +, vascularized, spirally arranged, blades with mean venation density ca 1.8 mm/mm2 [to 5 mm/mm2], all epidermal cells with chloroplasts; sporangia in strobili, sporangia adaxial, columella 0; tapetum glandular; sporophyte-gametophyte junction lacking dead gametophytic cells, mucilage, ?position of transfer cells; MTOCs not associated with plastids, basal body 350-550 nm long, stellate array in transition region initially joining microtubule triplets; archegonia embedded/sunken [only neck protruding]; embryo suspensor +, shoot apex developing away from micropyle/archegonial neck [from hypobasal cell, endoscopic], root lateral with respect to the longitudinal axis of the embryo [plant homorhizic].

[MONILOPHYTA + LIGNOPHYTA]

Sporophyte growth ± monopodial, branching spiral; roots endomycorrhizal [with Glomeromycota], lateral roots +, endogenous; G-type tracheids +, with scalariform-bordered pits; leaves with apical/marginal growth, venation development basipetal, growth determinate; sporangium dehiscence by a single longitudinal slit; cells polyplastidic, MTOCs diffuse, perinuclear, migratory; blepharoplasts +, paired, with electron-dense material, centrioles on periphery, male gametes multiciliate; nuclear genome [1C] 7.6-10 pg [mode]; chloroplast long single copy ca 30kb inversion [from psbM to ycf2]; mitochondrion with loss of 4 genes, absence of numerous group II introns; LITTLE ZIPPER proteins.

LIGNOPHYTA†

Sporophyte woody; stem branching axillary, buds exogenous; lateral root origin from the pericycle; cork cambium + [producing cork abaxially], vascular cambium bifacial [producing phloem abaxially and xylem adaxially].

SEED PLANTS† / SPERMATOPHYTA†

Growth of plant bipolar [plumule/stem and radicle/root independent, roots positively geotropic]; plants heterosporous; megasporangium surrounded by cupule [i.e. = unitegmic ovule, cupule = integument]; pollen lands on ovule; megaspore germination endosporic, female gametophyte initially retained on the plant, free-nuclear/syncytial to start with, walls then coming to surround the individual nuclei, process proceeding centripetally.

EXTANT SEED PLANTS

Plant evergreen; nicotinic acid metabolised to trigonelline, (cyanogenesis via tyrosine pathway); microbial terpene synthase-like genes 0; primary cell walls rich in xyloglucans and/or glucomannans, 25-30% pectin [Type I walls]; lignin chains started by monolignol dimerization [resinols common], particularly with guaiacyl and p-hydroxyphenyl [G + H] units [sinapyl units uncommon, no Maüle reaction]; roots often ≥1 mm across, stele diarch to pentarch, xylem and phloem originating on alternating radii, cork cambium deep seated, gravitropism response fast; stem apical meristem complex [with quiescent centre, etc.], plasmodesma density in SAM 1.6-6.2[mean]/μm2 [interface-specific plasmodesmatal network]; eustele +, protoxylem endarch, endodermis 0; wood homoxylous, tracheids and rays alone, tracheid/tracheid pits circular, bordered; mature sieve tube/cell lacking functioning nucleus, sieve tube plastids with starch grains; phloem fibres +; cork cambium superficial; leaf nodes 1:1, a single trace leaving the vascular sympodium; leaf vascular bundles amphicribral; guard cells the only epidermal cells with chloroplasts, stomatal pore with active opening in response to leaf hydration, control by abscisic acid, metabolic regulation of water use efficiency, etc.; branching by axillary buds, exogenous; prophylls two, lateral; leaves with petiole and lamina, development basipetal, lamina simple; sporangia borne on sporophylls; spores not dormant; microsporophylls aggregated in indeterminate cones/strobili; grains monosulcate, aperture in ana- position [distal], primexine + [involved in exine pattern formation with deposition of sporopollenin from tapetum there], exine and intine homogeneous, exine alveolar/honeycomb; ovules with parietal tissue [= crassinucellate], megaspore tetrad linear, functional megaspore single, chalazal, sporopollenin 0; gametophyte ± wholly dependent on sporophyte, development initially endosporic [apical cell 0, rhizoids 0, etc.]; male gametophyte with tube developing from distal end of grain, male gametes two, developing after pollination, with cell walls; embryo cellular ab initio, suspensor short-minute, embryonic axis straight [shoot and root at opposite ends], primary root/radicle produces taproot [= allorhizic], cotyledons 2; embryo ± dormant; chloroplast ycf2 gene in inverted repeat, trans splicing of five mitochondrial group II introns, rpl6 gene absent; ??whole nuclear genome duplication [ζ/zeta duplication event], 2C genome size (0.71-)1.99(-5.49) pg, two copies of LEAFY gene, PHY gene duplications [three - [BP [A/N + C/O]] - copies], 5.8S and 5S rDNA in separate clusters.

IID. ANGIOSPERMAE / MAGNOLIOPHYTA

Lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, apigenin and/or luteolin scattered, [cyanogenesis in ANA grade?], lignin also with syringyl units common [G + S lignin, positive Maüle reaction - syringyl:guaiacyl ratio more than 2-2.5:1], hemicelluloses as xyloglucans; root cap meristem closed (open); pith relatively inconspicuous, lateral roots initiated immediately to the side of [when diarch] or opposite xylem poles; epidermis probably originating from inner layer of root cap, trichoblasts [differentiated root hair-forming cells] 0, hypodermis suberised and with Casparian strip [= exodermis]; shoot apex with tunica-corpus construction, tunica 2-layered; starch grains simple; primary cell wall mostly with pectic polysaccharides, poor in mannans; tracheid:tracheid [end wall] plates with scalariform pitting, multiseriate rays +, wood parenchyma +; sieve tubes enucleate, sieve plates with pores (0.1-)0.5-10< µm across, cytoplasm with P-proteins, not occluding pores of plate, companion cell and sieve tube from same mother cell; ?phloem loading/sugar transport; nodes 1:?; dark reversal Pfr → Pr; protoplasm dessication tolerant [plant poikilohydric]; stomata randomly oriented, brachyparacytic [ends of subsidiary cells ± level with ends of guard cells], outer stomatal ledges producing vestibule, reduction in stomatal conductance with increasing CO2 concentration; lamina formed from the primordial leaf apex, margins toothed, development of venation acropetal, overall growth ± diffuse, secondary veins pinnate, fine venation hierarchical-reticulate, (1.7-)4.1(-5.7) mm/mm2, vein endings free; flowers perfect, pedicellate, ± haplomorphic, protogynous; parts free, numbers variable, development centripetal; P = T, petal-like, each with a single trace, outer members not sharply differentiated from the others, not enclosing the floral bud; A many, filament not sharply distinguished from anther, stout, broad, with a single trace, anther introrse, tetrasporangiate, sporangia in two groups of two [dithecal], each theca dehiscing longitudinally by a common slit, ± embedded in the filament, walls with at least outer secondary parietal cells dividing, endothecium +, cells elongated at right angles to long axis of anther; tapetal cells binucleate; microspore mother cells in a block, microsporogenesis successive, walls developing by centripetal furrowing; pollen subspherical, tectum continuous or microperforate, ektexine columellate, endexine restricted to the apertural regions, thin, compact, intine in apertural areas thick, orbicules +, pollenkitt +; nectary 0; carpels present, superior, free, several, spiral, ascidiate [postgenital occlusion by secretion], stylulus at most short [shorter than ovary], hollow, cavity not lined by distinct epidermal layer, stigma ± decurrent, carinal, dry; suprastylar extragynoecial compitum +; ovules few [?1]/carpel, marginal, anatropous, bitegmic, micropyle endostomal, outer integument 2-3 cells across, often largely subdermal in origin, inner integument 2-3 cells across, often dermal in origin, parietal tissue 1-3 cells across, nucellar cap?; megasporocyte single, hypodermal, functional megaspore lacking cuticle; female gametophyte lacking chlorophyll, four-celled [one module, egg and polar nuclei sisters]; ovule not increasing in size between pollination and fertilization; pollen grains bicellular at dispersal, germinating in less than 3 hours, siphonogamy, pollen tube unbranched, growing towards the ovule, between cells, growth rate (ca 10-)80-20,000 µm h-1, tube apex of pectins, wall with callose, lumen with callose plugs, penetration of ovules via micropyle [porogamous], whole process takes ca 18 hours, distance to first ovule 1.1-2.1 mm; male gametophytes tricellular, gametes 2, lacking cell walls, ciliae 0, double fertilization +, ovules aborting unless fertilized; fruit indehiscent, P deciduous; mature seed much larger than fertilized ovule, small [<5 mm long], dry [no sarcotesta], exotestal; endosperm +, ?diploid [one polar nucleus + male gamete], cellular, development heteropolar [first division oblique, micropylar end initially with a single large cell, divisions uniseriate, chalazal cell smaller, divisions in several planes], copious, oily and/or proteinaceous, embryo short [<¼ length of seed]; plastid and mitochondrial transmission maternal; Arabidopsis-type telomeres [(TTTAGGG)n]; nuclear genome [2C] (0.57-)1.45(-3.71) [1 pg = 109 base pairs], ??whole nuclear genome duplication [ε/epsilon event]; ndhB gene 21 codons enlarged at the 5' end, single copy of LEAFY and RPB2 gene, knox genes extensively duplicated [A1-A4], AP1/FUL gene, palaeo AP3 and PI genes [paralogous B-class genes] +, with "DEAER" motif, SEP3/LOFSEP and three copies of the PHY gene, [PHYB [PHYA + PHYC]]; chloroplast IR expansions, chlB, -L, -N, trnP-GGG genes 0.

[NYMPHAEALES [AUSTROBAILEYALES [MONOCOTS [[CHLORANTHALES + MAGNOLIIDS] [CERATOPHYLLALES + EUDICOTS]]]]]: wood fibres +; axial parenchyma diffuse or diffuse-in-aggregates; pollen monosulcate [anasulcate], tectum reticulate-perforate [here?]; ?genome duplication; "DEAER" motif in AP3 and PI genes lost, gaps in these genes.

[AUSTROBAILEYALES [MONOCOTS [[CHLORANTHALES + MAGNOLIIDS] [CERATOPHYLLALES + EUDICOTS]]]]: phloem loading passive, via symplast, plasmodesmata numerous; vessel elements with scalariform perforation plates in primary xylem; essential oils in specialized cells [lamina and P ± pellucid-punctate]; tension wood + [reaction wood: with gelatinous fibres, G-fibres, on adaxial side of branch/stem junction]; anther wall with outer secondary parietal cell layer dividing; tectum reticulate; nucellar cap + [character lost where in eudicots?]; 12BP [4 amino acids] deletion in P1 gene.

[MONOCOTS [[CHLORANTHALES + MAGNOLIIDS] [CERATOPHYLLALES + EUDICOTS]]] / MESANGIOSPERMAE: benzylisoquinoline alkaloids +; sesquiterpene synthase subfamily a [TPS-a] [?level], polyacetate derived anthraquinones + [?level]; outer epidermal walls of root elongation zone with cellulose fibrils oriented transverse to root axis; P more or less whorled, 3-merous [?here]; pollen tube growth intra-gynoecial; extragynoecial compitum 0; carpels plicate [?here]; embryo sac monosporic [spore chalazal], 8-celled, bipolar [Polygonum type], antipodal cells persisting; endosperm triploid.

[CERATOPHYLLALES + EUDICOTS]: ethereal oils 0 [or next node up]; fruit dry [very labile].

EUDICOTS: (Myricetin +), asarone 0 [unknown in some groups, + in some asterids]; root epidermis derived from root cap [?Buxaceae, etc.]; (vessel elements with simple perforation plates in primary xylem); nodes 3:3; stomata anomocytic; flowers (dimerous), cyclic; protandry common; K/outer P members with three traces, ("C" +, with a single trace); A ?, filaments fairly slender, anthers basifixed; microsporogenesis simultaneous, pollen tricolpate, apertures in pairs at six points of the young tetrad [Fischer's rule], cleavage centripetal, wall with endexine; G with complete postgenital fusion, stylulus/style solid [?here], short [<2 x length of ovary]; seed coat?; palaeotetraploidy event.

[PROTEALES [TROCHODENDRALES [BUXALES + CORE EUDICOTS]]]: (axial/receptacular nectary +).

[TROCHODENDRALES [BUXALES + CORE EUDICOTS]]: benzylisoquinoline alkaloids 0; euAP3 + TM6 genes [duplication of paleoAP3 gene: B class], mitochondrial rps2 gene lost.

[BUXALES + CORE EUDICOTS]: mitochondrial rps11 gene lost.

CORE EUDICOTS / GUNNERIDAE: (ellagic and gallic acids +); leaf margins serrate; compitum + [one position]; micropyle?; γ genome duplication [allopolyploidy, 4x x 2x], x = 3 x 7 = 21, 2C genome size (0.79-)1.05(-1.41) pg, PI-dB motif +; small deletion in the 18S ribosomal DNA common.

[ROSIDS ET AL. + ASTERIDS ET AL.] / PENTAPETALAE / [SANTALALES, CARYOPHYLLALES, SAXIFRAGALES, DILLENIALES, VITALES, ROSIDAE, [BERBERIDOPSIDALES + ASTERIDAE]: root apical meristem closed; (cyanogenesis also via [iso]leucine, valine and phenylalanine pathways); flowers rather stereotyped: 5-merous, parts whorled; P = K + C, K enclosing the flower in bud, with three or more traces, odd K adaxial, C with single trace; A = 2x K/C, in two whorls, alternating, (many, but then usually fasciculate and/or centrifugal); pollen tricolporate; G [(3, 4) 5], when 5 opposite K, whorled, placentation axile, style +, stigma not decurrent, compitum + [one position]; endosperm nuclear/coenocytic; fruit dry, dehiscent, loculicidal [when a capsule]; floral nectaries with CRABSCLAW expression, RNase-based gametophytic incompatibility system present.

Phylogeny. Prior to the seventh version of this site asterids were part of a major polytomy that included rosids, Berberidopsidales, Santalales, and Caryophyllales, but then the order of branching below the asterids seemed to be stabilizing, perhaps with a clade [Berberidopsidales [Santalales [Caryophyllales + Asterids]]] while rosid relationships seemed to be [Saxifragales [Vitales + Rosids]]]. However, recent work suggests a polytomy is indeed probably the best way to visualize relationships around here at present. So for further discussion of relationships at the base of asterids and rosids, see the Pentapetalae

[BERBERIDOPSIDALES + ASTERIDAE]: ?

ASTERIDAE // ASTERANAE Takhtajan: nicotinic acid metabolised to its arabinosides; (iridoids +); tension wood decidedly uncommon; C enclosing A and G in bud, (connate [sometimes evident only early in development, petals then appearing to be free]); anthers dorsifixed?; if nectary +, gynoecial; G [2], style single, long; ovules unitegmic, integument thick [5-8 cells across], endothelium +, nucellar epidermis does not persist; exotestal [!: even when a single integument] cells lignified, esp. on anticlinal and/or inner periclinal walls; endosperm cellular.

[ONCOTHECALES [LAMIIDAE/ASTERID I + CAMPANULIDAE/ASTERID II]] // CORE ASTERIDS // EUASTERIDS // GENTIANIDAE: plants woody, evergreen; ellagic acid 0, non-hydrolysable tannins not common; vessel elements long, with scalariform perforation plates; sugar transport in phloem active; inflorescence usu. basically cymose; flowers rather small [<8 mm across]; C free or basally connate, valvate, often with median adaxial ridge and inflexed apex ["hooded"]; A = and opposite K/P, free to basally adnate to C; G [#?]; ovules 2/carpel, apical, pendulous; fruit a drupe, [stone ± flattened, surface ornamented]; seed single; duplication of the PI gene.

ASTERID I / LAMIIDAE / [CARDIOPTERIDALES [GARRYALES, AQUIFOLIALES [ICACINALES [[GENTIANALES + BORAGINALES], VAHLIALES, SOLANALES, LAMIALES]]]]: ?

[GARRYALES, AQUIFOLIALES [ICACINALES [[GENTIANALES + BORAGINALES], VAHLIALES, SOLANALES, LAMIALES]]]: G [2], superposed; loss of introns 18-23 in RPB2 d copy. - check

AQUIFOLIALES Senft - Main Tree.

Shrubs or trees; iridoids?; petiole bundles arcuate; petiole bundle arcuate; leaves spiral, lamina margins toothed, stipules +, small, cauline; inflorescence axillary; C lacking median adaxial ridge and incurved apex; tapetal cells binucleate; nectary +; style 0; ovule 1/carpel, integument 9-15 cells across, parietal tissue 0, endothelium +; embryo sac breaking through the nucellar epidermis, antipodal cells ephemeral; fruit with separate pyrenes; exotesta and endotesta recognizable, rest crushed. - 3 families, 3 genera, 412 species.

Includes Aquifoliaceae, Helwingiaceae, Phyllonomaceae.

Note: In all node characterizations, boldface denotes a possible apomorphy, (....) denotes a feature the exact status of which in the clade is uncertain, [....] includes explanatory material; other text lists features found pretty much throughout the clade. Note that the precise node to which many characters, particularly the more cryptic ones, should be assigned is unclear. This is partly because homoplasy is very common, in addition, basic information for all too many characters is very incomplete, frequently coming from taxa well embedded in the clade of interest and so making the position of any putative apomorphy uncertain. Then there are the not-so-trivial issues of how character states are delimited and ancestral states are reconstructed (see above).

Age. K. Bremer et al. (2004) suggested an age of about 113 Ma for crown-group Aquifoliales, Wikström et al. (2015) an age of (112-)100(-84) Ma, Tank and Olmstead (pers. comm.) ages of (110.7-)94.2(-75.8) Ma, Magallón et al. (2015) an age of about 92 Ma, Bell et al. (2010) ages of (101-)88, 87(-85) Ma; ca 95.8 and 74.4 Ma are ages in Nylinder et al. (2012: suppl.), ca 52.3 Ma is the age in Nicolas and Plunkett (2014; ?sampling).

Evolution: Divergence & Distribution. In their study of the evolution of plant habit in the campanulids, Beaulieu et al. (2013b) noted that growth form was notably constrained in Aquifoliales, all members of which are woody. As mentioned elsewhere, the woody habit is a feature of the gentianids as a whole (see also Stull et al. 2018).

Chemistry, Morphology, etc.. Stipular morphology would repay study. Structures called stipules in Helwingia (e.g. F.o.C. vol. 14. 2005) appear to be aggregations of colleters; they are not vascularized. In Ilex, structures that can be called colleters terminate the triangular stipules (Gonzalez & Tarragó 2009); nodes are at least sometimes 3:3 in the genus, as is common in stipulate angiosperms.

For a summary of pollen variation, see Schori and Furness (2011, esp. 2014); Lobreau (1969) included a number of taxa from this order in her study of taxa possibly associated with Celastrales, so look there, too...

Phylogeny rbcL and other data suggested the relationships [Phyllonoma [Hellwingia + Ilex]] (Morgan & Soltis 1993; see also Soltis & Soltis 1997; Olmstead et al. 2000; Kårehed 2002b; Winkworth et al. 2008; Lens et al. 2008b; Manen et al. 2010; Bell et al. 2010). The absence of evidence that the two taxa with epiphyllous inflorescences formed a clade - they also have several other features in common (see below) - seemed a little odd, but a comprehensive analysis of the campanulids (Tank et al. 2007) recovered a sister group relationship between them (1.0 p.p.), as did Soltis et al. (2011: 99% ML bootstrap). C. Zhang et al. (2020) did not include Phyllonoma in their analyses.

Previous Relationships. Aquifoliaceae were included in a very heterogeneous Celastrales by Cronquist (1981). Thus it is not surprising that Lobreau (1969) included a number of taxa from this order in her study of taxa possibly associated with Celastrales.

Synonymy: Aquifoliineae Shipunov - Helwingiales Takhtajan, Ilicales Martius

AQUIFOLIACEAE Berchtold & J. Presl, nom. cons. - Ilex L.  -  Back to Aquifoliales —— Synonymy: Ilicaceae Dumortier

Aquifoliaceae

(Plant deciduous), (lianes); tanniniferous, iridoids 0; (vessel elements in multiples); (wood with crystals); resiniferous, laticiferous idioblasts +; nodes 1:1, 3:3, etc.; petiole bundles also annular, with wing (and medullary) bundles; stomata also (cyclocytic, bicyclic); branching from previous flush; leaves (opposite), (two-ranked), lamina vernation supervolute (conduplicate), teeth with single vein and opaque, glandular, deciduous apex, (margins entire), (stipules 0); plants often dioecious; flowers 4-23-merous; K valvate, C imbricate, often connate basally; A adnate to base of C (free), anthers basifixed; pollen surface conspicuously gemmate/with clavate processes; nectary gynoecial; G [(2-)4-6(-many)], opposite C, placentation axile basally, becoming free-central, stigma broad, wet; ovules (2/carpel), apotropous, endothelium 0, parietal tissue ca 1 cell across, hypostase +, funicular obturator papillate (0); pyrenes with endocarp only thickened, stigma prominent, K deciduous (semipersistent); exotestal cells cuboid, tangentially elongated, inner walls lignified, endotesta tanniniferous; endosperm hemicellulosic; n = (17-)20, x = 20, nuclear genome [1 C] (0.99-)1.275(-6.426) pg; loss of introns 18-23 in RPB2 d copy, mitochondrial coxII.i3 intron 0.

1 [list]/596. ± World-wide, esp. South America and South East Asia-Malesia, but only two species in Africa, three in Europe, one in Australia and one in Hawaii (map: see Meusel et al. 1978; Loizeau et al. 2005: fig. 4 - fossils). [Photo - Staminate Flower, Carpellate Flower.]

Age. Crown group Ilex, or at least its plastome, may be a mere 15 Ma old (Miocene), which suggests that there may previously have been much extinction in the clade (Manen et al. 2010). However, crown and stem ages of 52 and 65 Ma respectively were suggested by Quirk et al. (2012) and a crown age of (57.6-)50.8(-43.5) Ma by Yao et al. (2020). There is considerable variation in crown-group ages, but little can be said about stem-group ages given the movement of the order around the tree.

The distinctive pollen of Ilex is known from Cretaceous-Turonian deposits ca 80 Ma from the Otway Basin in S.E. Australia and from deposits 75-65.5 Ma, almost as old, in central Australia, and there are perhaps older records, although not documented by photographs of the distinctive pollen (see also Martin 1977; Dettmann & Jarzen 1990: Fig. 2; Loizeau et al. 2005; Friis & Pedersen 2012; Carpenter et al. 2015; Manchester et al. 2015). However, Manen et al. (2010) and Yao et al. (2019) used an age of ca 69 Ma for the oldest fossils, an age based on fossil fruits found by Knobloch and Mai (1986) in central Europe, Martínez-Millán (2010) an age of 61.7 Ma, and Beaulieu et al. (2013a) an age of ca 65 Ma based on a fossil "seed".

Evolution: Divergence & Distribution. Loizeau et al. (2005) and Yao et al. (2019) discuss literature on the common and widespread fossils, including the distinctive pollen, of Ilex that are from pre-crown group diversification times. Note that Hironoia fusiformis, fruits from Cretaceous-early Coniacian deposists in Japan ca 89 Ma, was used to calibrate times in the phylogeny of Yao et al. (2020), in other studies this fossil has been placed in Cornales somewhere around Nyssaceae (Takahashi et al. 2002; see also Manchester et al. 2015; Atkinson 2018). For divergence dates within Ilex, see Yao et al. (2020).

There may be an evolutionary fuse of anything from 65 to 13 Ma based on the age estimates given above. Interestingly, the fuse in Yao et al. (2020), some 34 Ma, was followed by a period of ca 18 Ma during which only two small clades (with 3 extant species, but sampling?) of Chinese species diverged, while at ca 32.7 Ma more extensive diversification began. Yao et al. (2020) suggested an origin of the genus in subtropical East Asia, although from fossil evidence it could be anywhere; subsequent migration - efficient seed dispersal? - was very extensive (Yao et al. 2020: Fig. 4).

Cuénoud et al. (2000) obtained several clades correlating with geography, and Manen et al. (2010) also found strong geographic structure in the phylogeny (see also Selbach-Schnadelbach et al. 2009; Yao et al. 2020). Ilex is one of the genera that has become extinct in New Zealand in the Caenozoic (Lee et al. 2001), while I. canariensis is sister to one of the South American clades, their divergence being estimated as having occurred ca 27.7 Ma (Yao et al. 2020).

There is evidence of extensive hybridization within Ilex (e.g. Setoguchi & Watanabe 2000; Manen et al. 2002, 2010).

Pollination Biology & Seed Dispersal. The great majority of visits by bees to the 12 species of Ilex observed on Hongkong were made by a single species, Apis cerana (Tsang & Corlett 2012).

The fruits are of low quality; they are eaten by birds (Tsang & Corlett 2012).

Genes & Genomes. Chromosome numbers in references like Cronquist (1981) and Mabberley (2008) are very different from those in Loizeau et al. (2016); the latter are correct.

Yao et al. (2019) noted a very high level of selection on the chloroplast rbcL gene, the highest known, but this is probably connected with the hybridization and introgression prevalent in the genus that has led to cytonuclear discordance.

Chemistry, Morphology, etc.. Palisade glandular tissues with protein-rich secretions are found on the leaf teeth and stipules, consequently, the latter have been called colleters (Gonzalez & Tarragó 2009). Spiral strands may join the two halves of a tranversely-torn leaf blade.

For the gynoecial nectary, see Erbar and Leins (2010); the nectar may seem to come from the petals (Loizeau et al. 2016). It collects between the stamens in a little pocket formed by the gynoecium and petals. The embryo is often minute and barely developed at the time when the fruit is dispersed, only maturing slowly afterwards (Herr 1961; Tsang & Corlett 2005 for references).

See Copeland (1964) and Loizeau et al. (2016) for general information, Baas (1973b, 1975, 1978) for vegetative anatomy, Lobreau-Callen (1977), Martin (1977) for pollen, Erbar (2014 and references) for nectaries, and van Tieghem (1898) for ovules; Galle (1997) provides an account of the cultivated members of the family.

Phylogeny. The erstwhile genus Nemopanthus is deeply embedded in Ilex (Powell et al. 2000), the two having the same distinctive pollen, etc.. Cuénoud et al. (2000) obtained several clades in their study of Ilex s. str., however, support for some was weak; Ilex canariensis was not associated with any of these clades. However, I. canariensis was sister to the rest of the genus in the morphological analysis by Loizeau et al. (2005), but support was generally very weak indeed. Selbach-Schnadelbach et al. (2009) found the relationships [South American group [the rest + I. canariensis]]. The position of I. canariensis was still unclear in Manen et al. (2010), and Hawaiian and New Caledonian species were embedded in an American clade (MCC value of 0.84). Yao et al. (2020) found the East Asian I. intricata and I. sinica to be successively sister to the rest of the genus, branches in this part of the stem being long, and I. canariensis was well embedded in the genus and sister to an American clade, but with a very short branch. However, understanding relationships in Ilex is complicated by evidence of ancient hybridization (e.g. Manen et al. 2010), but there was no discussion of this in Yao et al. (2020: nuclear and chloroplast markers used).

Previous Relationships. Phelline and Sphenostemon have sometimes been included in Aquifoliaceae (e.g. Mabberley 1997), but Phelline is here recognised as Phellinaceae (in Asterales) while Sphenostemon is in Paracryphiaceae (Paracryphiales).

[Phyllonomaceae + Helwingiaceae]: plant glabrous; nodes 1:1; lamina with second order veins looping and joining towards margin [brochidodromous], stipules fimbriate; inflorescence epiphyllous, on adaxial side of lamina; nectary annular; ovary inferior, stigma/styles separate, ± elongated, recurved; parietal tissue 0, suprachalazal zone of embryo much elongated [developing late].

Age. The age of this node is estimated at around 66 Ma (K. Bremer et al. 2004a), ca 61.3 Ma (Tank et al. 2015: Table S2), ca 56.5 Ma (Magallón et al. 2015) or (82-)59(-32) Ma (Wikström et al. 2015).

Chemistry, Morphology, etc.. Flowers of both Phyllonomaceae and Helwingiaceae are drawn with the odd sepal/perianth member abaxial, i.e. the unusual condition for eudicots (Ao & Tobe 2015: see also below).

PHYLLONOMACEAE Small - Phyllonoma Roemer & Schultes  -  Back to Aquifoliales —— Synonymy: Dulongiaceae J. G. Agardh, nom. illeg.

Phyllonomaceae

Plants Al accumulators; chemistry?; stem anatomy?; young stem with separate bundles; petiole bundle annular; plant glabrous, leaves ?two-ranked; inflorescence monochasial cyme, bracteoles 0; flowers perfect, odd sepal abaxial; K 4-5, with one trace, quincuncial, with stout marginal glandular hairs, C 3-5, valvate, adaxially weakly ridged; filaments shorter than anthers; G collateral(-suboblique), placentation intrusive parietal; ovules 6-7/carpel, campylotropous, endothelium 0; fruit a berry, few-seeded; testa multilayered, exotestal cells large, thick-walled, mucilaginous, forming irregular (multicellular) papillae, palisade or not, 2-3 layers of flattened cells; endosperm copious, with oil, haustoria 0 [?level]; n = x = ?

1 [list]/4. Mexico to Peru (map: see Mori & Kallunki 1977). [Photo - Leaves, Flowers.]

Chemistry, Morphology, etc.. Although the inflorescence of Phyllonoma has been described as being "truly phyllogenous", it appears to represent a displaced axillary shoot, as in Helwingia (Weber 2004c, and references; see also Dickinson and Sattler 1974); it is a monochasial cyme (Tobe 2014), although it has been described as racemose, etc., in the past (including early versions here). There is some confusion over integument number and thickness in the literature, and the embryo is described as being very small by Bittrich (2016; see also Tobe 2015), but is illustrated there as being close to the length of the seed.

See Thouvenin (1890), Mori and Kallunki (1977) and Bittrich (2016) for general information, Gornall et al. (1998: as Escalloniaceae) for anatomy, Tobe (2013) for floral morphology, Mauritzon (1933) and especially Tobe (2015a) for embryology, and Krach (1976) and Takhtajan (2000) for seed anatomy.

Previous Relationships. Krach (1977) suggested that the seeds of Phyllonoma and those of Grossulariaceae were similar. Indeed, Phyllonoma was included in Grossulariaceae by Cronquist (1981), and as Phyllonomaceae, in Hydrangeales, by Takhtajan (1997).

HELWINGIACEAE Decaisne - Helwingia Decaisne  - Back to Aquifoliales

Helwingiaceae

(Plant deciduous); flavones, chlorogenic acid, unidentified iridoids +; septate fibres with minutely bordered pits; silica grains +; pericyclic fibres 0; petiole also with two small inverted adaxial bundles; cuticle wax crystalloids 0; lamina vernation supervolute-curved; plant dioecious; inflorescence fasciculate; P +, uniseriate [?= corolla], 3-5, valvate-imbricate, apex ± incurved; nectary stomatiferous, on top of G; staminate flowers: stamens alternating with P, filaments short; pollen spinulate, with diffuse endoapertures; pistillode 0; carpelate flowers: staminodes 0; G [(2-)4], alternating with P, stigma dry; ovule apotropous, endothelium weakly developed; testa multiplicative, to 20 cells across, most collapsed; endosperm weakly ruminate; n = 18, 19, x = 20 (?10).

1 [list]/3. Himalayas to Japan. Map: from Hara (1972). [Photo - Fruit.]

Age. Ca 50 Ma fossil fruits that may be those of Helwingia are reported from the Okanogan Highlands in W. North America (Princeton, Republic: see Wehr & Hopkins 1994).

Evolution: Pollination Biology & Seed Dispersal. T. Wu et al. (2020) recorded a variety of generalist visitors to the flowers of Hellwingia japonica, solitary bees being the most effective pollinators.

Chemistry, Morphology, etc.. The fasciculate inflorescence is clearly cymose (Weber 2004c; pers. obs.). Helwingiaceae have a single perianth whorl, and probably lack a calyx (e.g. Takhtajan 1997); in this interpretation, stamens and corolla alternate, as is almost universal in the gentianids, and the flowers are normally orientated. Eichler (1878) noted that there was a little rim outside the perianth members in carpelate flowers, suggesting that they were indeed petals. If the corolla is absent (Tobe 2013, tentative suggestion; esp. Ao & Tobe 2015), the stamens would be antepetalous, very odd for a gentianid. Furthermore, Ao and Tobe (2015) drew both staminate and carpelate flowers with the odd sepal/perianth member abaxial, unusual for a broad-leaved angiosperm; nothing was said about either stamen position or floral orientation (see also above). The ovule is described as "anatropous and epitropous dorsal at maturity" (Ao & Tobe 2015: p. 169). The ventral carpel bundles are central.

See also Decaisne (1836), Wangerin (1906), Hara and Kurosawa (1975) and Q. Xiang (2016), all general, Iwashina et al. (1997: chemistry), Noshiro and Baas (1998: anatomy), Horne (1914: flower), Dickinson and Sattler (1975: inflorescence), and Korobova (1980: embryo and seed).

Previous Relationships. Helwingiales were included in Aralianae by Takhtajan (1997); Helwingia was included in Cornaceae by Cronquist (1981) and Mabberley (1997), in the latter only with hesitation.