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.


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


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].


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.


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].


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.


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.


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 [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [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 [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [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.

[[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [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.

[MONOCOTS [CERATOPHYLLALES + EUDICOTS]]: (veins in lamina often 7-17 mm/mm2 or more [mean for eudicots 8.0]); (stamens opposite [two whorls of] P); (pollen tube growth fast).

[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: 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, C with single trace; A = 2x K/C, in two whorls, internal/adaxial to C, alternating, (numerous, but then usually fasciculate and/or centrifugal); pollen tricolporate; G [(3, 4) 5], whorled, placentation axile, style +, stigma not decurrent, compitum + [another position]; endosperm nuclear/coenocytic; fruit dry, dehiscent, loculicidal [when a capsule]; floral nectaries with CRABSCLAW expression.



[CARYOPHYLLALES + ASTERIDAE]: seed exotestal; embryo long.

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.

[ERICALES [LAMIIDAE/ASTERID I + CAMPANULIDAE/ASTERID II]]: ovules lacking parietal tissue [tenuinucellate].

[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]; ="apo">seed single; duplication of the PI gene.


Myricetin 0; style shorter than the ovary; endosperm copious, embryo short/very short. - 7 orders, 29 families, 2,340 genera, 37,230 species.

Age. Wikström et al. (2001) suggested a crown-group age of (112-)107, 99(-94) Ma for this clade, Bremer et al. (2004) an age of about 121 Ma, Janssens et al. (2009) an age of 113±9.8 Ma, Wikström et al. (2015) an age of (119-)112(-104) Ma, Tank and Olmstead (pers. comm.) an age of (124.9-)110.7(-97.2) Ma, and Magallón and Castillo (2009) an age of ca 99.5 Ma. Moore et al. (2010: 95% HPD) suggested ages of (81-)75(-71) Ma, Bell et al. (2010) ages of (109-)102, 100(-85) Ma (about the same in Magallón et al. 2015), while Beaulieu et al. (2013a: 95% HPD) estimated ages of (115-)104(-95) Ma and Beaulieu and O'Meara (2018) an age of ca 127 My; around 120-101.8 Ma are estimates in Nylinder et al. (2012: suppl.), 92.7 Ma is an estimate in Naumann et al. (2013), ca 91.8 Ma in Tank et al. (2015: Table S1) and around 127.6 Ma in Nicolas and Plunkett (2014). Rather as in this last estimate, the age is around 124 Ma in Z. Wu et al. (2014), but it is 101-91 Ma in Foster and Ho (2017).

The oldest fossils that have been associated with this clade are ca 83.5 Ma, from the Late Santonian-Early Campanian, and have been assigned to Paracryphiales (q.v.), although their identity is suspect (see also Cornales - Beaulieu et al. 2013a). However, other fossils assigned to Aquifoliaceae are about the same age (Loizeau et al. 2005; Martínez-Millán 2010; Friis & Pedersen 2012, c.f. Beaulieu et al. 2013a).

Evolution: Divergence & Distribution. Diversification at this node may have occurred in the southern hemisphere (Beaulieu et al. 2013a). Crown group ages of all the orders except Paracryphiales are thought to be Cenomanian in age, ca 100-94 Ma, while the crown-group ages of all families except Aquifoliaceae are Caenozoic (Beaulieu et al. 2013a; Beaulieu & O'Meara 2018).

Beaulieu et al. (2013b) and Stull et al. (2018) discussed the evolution of plant habit in the campanulids; woodiness is plesiomorphic. Stull et al. (2018) suggest that an inferior ovary may be an apomorphy at this node - or the next one up. Note that Aquifoliales, Bruniales, Escalloniales and Paracryphiales are all (largely) woody and species poor, as are basal Apiales, woody clades in Asterales and the two basal lamiid clades (the [Oleaceae + Carlemanniaceae] clade has 620-800 species, so it may not count...). For further details of evolution in the basal gentianids, see discussion at the euasterid node in particular.

Pollination Biology & Seed Dispersal. In the campanulids the fruits often have few (commonly only 1-2) seeds, although families like Campanulaceae and Goodeniaceae are exceptions. Even when each flower has only one or two seeds, these are generally small, indeed, gentianids as a whole have rather small seeds (Linkies et al. 2010). Beaulieu and Donoghue (2013; see Beaulieu & O'Meara 2016) examined fruit evolution in campanulids from an ecological point of view and concluded that the plesiomorphic fruit type for the whole group was likely to be dry, dehiscent, and with two or more seeds. Clades with achenes, dry, indehiscent, single-seeded fruits (they include Apiaceae, although there the disseminules are individual mericarps that result from the septicidal separation of the two-seeded fruits) were often associated with increased diversification rates. However, Beaulieu and Donoghue (2013) were unclear as to any causal connections between fruit types and diversification rates. These results may have to be modified somewhat when outgroups are included (e.g., what are the likely states for the gentianids as a whole?), if fruit types are redefined, and as different methods of analysis are used (Beaulieu & O'Meara 2016); it is perhaps more likely that the plesiomorphic fruit morphology of the campanulids (and lamiids) was quite large, fleshy, indehiscent and single-seeded (see above).

Plant-Animal Interactions. Clades of the dipteran agromyzid leaf miner Phytomyza diversified considerably in the campanulids; they moved there from Ranunculaceae (Winkler et al. 2009: >700 species in the genus).

Phylogeny. There is now moderate to strong support for Aquifoliales as sister to all other campanulids (e.g. Olmstead et al. 2000; Soltis et al. 2000; B. Bremer et al. 2002; Janssens et al. 2009; Barba-Montoya et al. 2018; Beaulieu et al. 2013b; Beaulieu & O'Meara 2018; Stull et al. 2018), although there has been some discussion about the position of Aquifoliaceae and the circumscription of Aquifoliales and of the woody lineages at the base of the lamiid clade, related issues - see the euasterid page. However, there are still question marks about the relationships of some of the major clades within the campanulids. The position of Dipsacales within this large clade in early phylogenetic analyses was unclear. Downie and Palmer (1992) associated Adoxaceae with Asterales, while they were sister to Apiales in some studies (Backlund & Bremer 1997). The clade [Asterales [Apiales + Dipsacales]] (e.g. Nandi et al. 1998; Olmstead et al. 2000; Lundberg 2001c; Lens et al. 2008a; see also B. Bremer et al. 2002; Winkworth et al. 2008a; Beaulieu et al. 2013b) is generally supported. On the other hand, Janssens et al. (2009: two genes) found weak support for the clade [Dipsacales [Asterales + Apiales]], Qiu et al. (2010) for [Apiales [Dipsacales + Asterales]], and Soltis et al. (2011) in their 17-gene study found little support for any relationships other than strong support for Aquifoliales as sister to the rest of the clade. Relationships towards the base of asterids are also different from those shown here - there is a clade [Escalloniales ["Bruniales" + Asterales]] - in Wikström et al. (2015: Bruniales are not monophyletic), while Beaulieu and O'Meara (2018) found Bruniales to be sister to [Dipsacales + Paracryphiales] in some analyses.

Various small families have been placed around Escalloniaceae in the campanulids, but initially with uncertain support; recent work is clarifying their relationships (Winkworth et al. 2008a; especially Tank & Donoghue 2010; Beaulieu et al. 2013b; Wikström et al. 2015). For Polyosmaceae and Escalloniaceae, see Escalloniaceae. However, where Escalloniales go is somewhat unclear (see Beaulieu & O'Meara 2018 for literature). Thus Barba-Montoya et al. (2018) recovered a topology [Asterales [Escalloniales [Bruniales...]]], and in some analyses in Beaulieu and O'Meara (2018) a topology [Escalloniales [Asterales [Bruniales [Apiales...]]]] was recovered. Tank and Olmstead (pers. comm.) even recovered Escallonia as sister to Desfontainia (Bruniales), while Polyosma was well separated. Focussing on relationships along the spine of the Pentapetalae, Zeng et al. (2017) found the relationships [Apiales [Dipsacales + Asterales]], but no Escalloniales, Bruniales or Paracryphiales were included, only Asteraceae of Asterales, etc., so no sleep need be lost here. Magallón et al. (2015) recovered the relationships [[Escalloniales + Asterales] [Bruniales...]] and Stull et al. (2018) also recoved an [Asterales + Escalloniales] [Bruniales...]] grouping, and these relationships were strongly supported (95% bootstrap) by H.-T. Li et al. (2019) in their chloroplast genome analysis, and they are followed here.

Paracryphiaceae form a clade sister to Dipsacales (e.g. Stull et al. 2018). However, in an early study Paracryphia was linked quite strongly with Rutaceae + Meliaceae + Simaroubaceae (Källersjö et al. 1998; c.f. Savolainen et al. 2000a). In a 17-gene analysis by Soltis et al. (2011), Quintinia linked with Polyosma (Escalloniales here), but support for this position came from the mitochondrial component of the analysis; Soltis et al. (2011) were inclined to think that horizontal gene transfer of the mitochondrial genes might be involved. Paracryphiaceae form a clade in Lundberg's three-gene Bayesian analysis (Lundberg 2001e); Cameron (2001, 2003) also suggested an association between Paracryphia and Sphenostemon. The clade [Paracryphia + Quintinia] was sister to Dipsacales, although not in analyses that included coding chloroplast genes (Winkworth et al. 2008a); see also especially Tank and Donoghue (2010), but support for the position adopted here was only slight in the full analysis of Soltis et al. (2011). The position of Quintinia remains unsatisfactory for some (Friis et al. 2013b). Interestingly, Polyosma (Escalloniales) linked with Quintinia (Paracryphiales) in an analysis of mitochondrial genes, but not of other genes; this was probably because of horizontal transfer of the mitochondrial genome from Quintinia to Polyosma (Soltis et al. 2011) - the two may grow together.

In the pre-April 2008 versions of this site [Columelliaceae + Desfontainiaceae] (= Columelliaceae s.l.) were placed sister to Dipsacales; the position of Columelliaceae s.l. in that area had been suggested by Bremer et al. (2001) and especially by Lundberg (2001e; see also Backlund 1996), although support was at best moderate. Indeed, both Columelliaceae s.l. and Dipsacales have opposite leaves, and Columellia has amoeboid tapetum (c.f. Bremer et al. 2001) like Dipsacales although Desfontainia does not (Maldonado de Magnano 1986a). The similarities that the pair has with Dipsacales may indicate either substantial homoplasy or (less likely) a suite of rather basal synapomorphies in the campanulids of which there is currently no indication. Other relationships have been suggested (Gustafsson et al. 1996; Backlund & Bremer 1997; Pyck & Smets 2000; Bell et al. 2001); for the possible association of Bruniaceae with Asterales, see Lundberg (2001e) and Soltis et al. (2011). Here Columelliaceae s.l. together with Bruniaceae make up Bruniales, an unexpected grouping.

To summarize: The overall topology [Bruniales [Apiales [Paracryphiales + Dipsacales]]] seems to be fairly well established (Winkworth et al. 2008a; Tank & Donoghue 2010; Beaulieu et al. 2013a; Barba-Montoya et al. 2018; Stull et al. 2018), and, as mentioned above, the clade [Escalloniales + Asterales] is sister to them.

AQUIFOLIALES Senft - Main Tree.

Shrubs or trees; iridoids?; petiole bundles arcuate; inflorescence axillary; tapetal cells binucleate; nectary +; embryo sac breaking through the nucellar epidermis, antipodal cells ephemeral. - 5 families, 21 genera, 536 species.

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, possession of the woody habit is a feature of the gentianids as a whole (see also Stull et al. 2018).

Chemistry, Morphology, etc.. 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....

Phylogeny Discussion on the placement of the genera included in the Cardiopteridaceae and Stemonuraceae below can also be found elsewhere; nearly all genera in these two families used to be in Icacinaceae. Of the other families in Aquifoliales, 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).

Includes Aquifoliaceae, Cardiopteridaceae, Helwingiaceae, Phyllonomaceae, Stemonuraceae.

Synonymy: Aquifoliineae Shipunov - Cardiopteridales Takhtajan, Helwingiales Takhtajan, Ilicales Martius

[Cardiopteridaceae + Stemonuraceae]: iridoids +; vessel elements also with simple perforation plates, pits usually not bordered; apotracheal parenchyma and variants common; (styloids +); stomata cyclocytic to anisocytic; hairs unicellular (adpressed); leaves two-ranked or spiral, lamina margin entire, tertiary venation ± obscure, stipules 0; (pedicels articulated); A basifixed; (pollen grains ± asymmetric); G asymmetric, unilocular, adaxial carpel alone fertile; ovules 2, epitropous, with parietal tissue, integument vascularized, funicular obturator +; fruit (asymmetric); seed (ruminate); endosperm nuclear/coenocytic.

Age. Estimated ages for this clade are broadly similar - ca 86.8 Ma is suggested by Tank et al. (2015: Table S2), (90-)83, 65(-58) Ma by Wikström et al. (2001), (90-)73, 66(-43)Ma by (Bell et al. 2010), and about 74.1Ma by Magallón et al. (2015).

Evolution: Divergence & Distribution. Kårehed (2001, 2002b) discussed the taxa in their current familial circumscriptions, while Lens et al. (2008a) provided a detailed anatomical survey in a phylogenetic context.

Chemistry, Morphology, etc.. For a summary of gynoecial variation in the clade, see Kong et al. (2018); in Cardiopteridaceae in particular there is variation in which carpels have a style and which produce ovule(s), but our basic knowledge of gynoecial and ovular development is very poor. The two sides of the gynoecium/fruit are sometimes dramatically different in appearance, as in Medusanthera; this too needs to be related to gynoecial development (see also the euasterid node).

For additional information, see Sleumer (1942a, b, 1971a), Howard (1942b), and Utteridge et al. (2005), all general, also Kaplan et al. (1991: chemistry), Lens et al. (2008a: measurements = range of means and upper end of variation, Cardiopteris [immature] excluded) and Bailey and Howard (1941a-d), all vascular anatomy, Heintzelmann and Howard (1948: crystals and indumentum), van Staveren and Baas (1973) and Baas (1973a, 1974), all epidermis and stomata, Teo and Haron (1999: anatomy), Lobreau-Callen (1972, 1973, 1977, 1980: pollen), and Mauritzon (1936c), Fagerlind (1945a) and Padmanabhan (1961: Gomphandra), all embryology.

Classification. These two families have quite a lot in common morphologically, however, Kårehed (2001) recognised them as separate.

Previous Relationships. For the other genera that were until recently included in Icacinaceae s.l., see Icacinaceae themselves and relatives, i.e. Metteniusaceae, in Metteniusales, Icacinaceae, in Icacinales, and Pennantiaceae, in Apiales.

CARDIOPTERIDACEAE Blume, nom. cons.  - Back to Aquifoliales


(Lianes); plants Al accumulators [?all], secoiridoids +; (vessel elements with scalariform perforation plates only - Citronella), 500-1,390(-1,950) µm long, fibres 2,190-2,970(-3,450) µm long; (articulated laticifers + - Cardiopteris); petiole bundles annular (+ medullary); stomata also anomocytic and paracytic; (lamina margins toothed/spiny), (secondary veins palmate); (plant dioecious, andromonoecious); (inflorescence branched, ultimate units clearly cymose or not), (bracts 0); K (free)/basally connate/cupular, quincuncial, (protective in bud - Cardiopteris), C (imbricate - Cardiopteris); A basally adnate to C/(not - Citronella), also dorsifixed; (pollen porate), (endoapertures enlarged - not Citronella); (nectary 0); G [3], odd carpel adaxial, (pseudoloculus - Pseudobotrys, Citronella), style usu. slender, about as long as ovary, (± laterally positioned), stigma truncate or capitate, (styles branched to the base, branches heteromorphic, two stout, subconnate, lobed and grooved, one slender, with capitate stigma Cardiopteris); ovule (1), (integument not vascularized), (ategmic - Cardiopteris [for more details, see below]), parietal tissue 0/?ca 2 cells across; fruit (asymmetric - Gonocaryum), endocarp C-shaped in transverse section, (2-winged samara, wings horizontally striate, stout styles accrescent Cardiopteris); testa thin, ?structure; endosperm (ruminate), (embryo long, with foliaceous cotyledons - Gonocaryum); n = 14 [Leptaulus].

5 [list]/43: Citronella (21). Tropics, inc. the Pacific, to Taiwan (map: from Sleumer 1971a, c; Utteridge & Brummitt 2007; Trop. Afr. Fl. Pl. Ecol. Distr. 5. 2010).

Chemistry, Morphology, etc.. Leptaulus has a violet-colored flavonoid; in L. daphnoides the shoot apex aborts.

Tobe (2011b) clarified the gynoecial morphology of Cardiopteris and noted that there was a nectary on the bottom part of the gynoecium. Variation of carpel number in this clade is not well understood; in Cardiopteris the carpel with a functional stigma has no associated ovules, while the two abaxial carpels with non-functional stigmas each has a single ovule (Kong et al. 2014). The ovary apex, i.e., the apices of the abaxial carpels, develops into a fleshy appendage on the fruit; this and other distinctive features of Cardiopteris (Kong & Schori 2014) are likely to be autapomorphies for the genus, although the embryology of other members of the family is poorly known.

Indeed, the embryology and seed development of Cardiopteris are without parallel in other angiosperms. Kong et al. (2002) described the ovules of Cardiopteris as being ategmic, straight, tenuinucellate and with the egg at the chalazal end of the embryo sac, similarly, Kong et al. (2014; see also Kong & Schori 2014) described the megaspore mother cells as being at the end of the long, straight ovule near the chalaza while the zygote was at the other end (their Fig. 7J). Painstaking work by Tobe (2016) on C. quinqueloba has clarified what happens here. The ovule is pendant in the loculus, with neither micropyle nor integument and with procambial tissue lying alongside the developing embryo sac. Megasporogenesis occurs in a hypodermal cell at the tip of the ovule, perhaps the "micropylar" end, and the innermost megaspore develops into the embryo sac. This elongates rapidly, and the egg cell, which is at the "chalazal" end of the ovule, is fertilized sfter the pollen tube has grown down the funicle. The embryo develops very slowly, and the first division of the endosperm nucleus results in two cells, one of which pushes out of the "micropyle", ballooning out and completely filling the ovary loculus before dying. As the seed develops, aymmetric growth results in the "micropyle" coming to be at the base of the seed near the funicle, and the late-developing chalazal vascular bundle almost surrounds the seed. Periclinal divisions of the nucellar epidermis in the area opposite the chalazal bundle ("antiraphe"), give rise to a two-layered tissue that forms a sort of testa. Insofar as one can work out the orientation of the embryo sac, the egg cell + synergids are the three cells that would be the antipodal cells in a normal Polygonum embryo sac (see Tobe 2016 for details of the whole process).

For additional literature, see above, also Schori (2016a: general), Damtoft et al. (1993: iridoids), Lobreau-Callen (1982: pollen, Peripterygium), Baillon (1874: fruit), and Vera-Caletti and Wendt (2001: new genus described).

Phylogeny. Citronella was sister to the three other genera examined (Kårehed 2001); Pseudobotrys is sister to Citronella (Schori, in Schori & Furness 2014); the latter genus (and Cardiopteris) has an imbricate corolla.

Previous Relationships. The relationships of Cardiopteris, a vine with distinctive morphology, were previously paricularly obscure. It was included in Celastrales by Cronquist (1981) and near there by Takhtajan (1997).

Synonymy: Leptaulaceae van Tieghem, Peripterygiaceae G. King

STEMONURACEAE Kårehed  - Back to Aquifoliales


Vessel elements in radial multiples, 600-1,510(-2,000) µm long, fibres 2,000-3,650(-4,500) µm long; (crystal sand in wood rays); petiole bundles arcuate + wing/annular + medullary; sclereids +/0; (plant glabrous); (plant dioecious); inflorescence often cymose, flowers 4-5(-7) merous; K connate, ± valvate, (C 0, minute); A radiating, (adnate to C), filaments often stout and with club-shaped hairs, and/or connective with appendages, or filaments thin; tapetal cells multinucleate, pollen (1-)3(-9)-porate, usu. ± prolate, surface microechinate (not - Lasianthera), (columellae enlarged, only around pores); nectary (unilateral), (0); (staminate flowers: pistillode +); (carpelate flowers: staminodes +/0); G ?; style 0, stigma broad; ovule with integument ca 10 cells across, parietal tissue 1-2 cells across, (nucellar cap ca 2 cells across); drupe asymmetric [the two sides very different, one with a fleshy "appendage" developing over the sulcus], (symmetric - Stemonurus), (pseudoloculus + Cantleya), mesocarp with fibre bundles, inner mesoocarp with ridges and grooves on the side of the appendage, when present, endocarp cells at right angles to inner mesocarp cells; testa thick, outer cells thick-walled, elongate, inner cells not thickened, post-chalazal bundle +; n = 22; seedling with hypocotyl, phanerocotylar. ILLUSTRATION.

12 [list]/95: Gomphandra (55), Stemonurus (15). Tropics, esp. Indo-Malesia to Australia (Queensland) and the West Pacific (map: from Sleumer 1971a; Utteridge & Brummitt 2007; Trop. Afr. Fl. Pl. Ecol. Distr. 5. 2010; Schori et al. 2013).

Chemistry, Morphology, etc.. The family appears to lack stipules (c.f. Mabberley 2017).

The carpelate flowers of Gomphandra are monosymmetric, having a single reflexed staminode (M. Schori, pers. comm.). Schori et al. (2009) discuss fruit variation in the family,

For additional literature, see above; also Potgieter et al. (2016: general), Schori et al. (2009: pollen) and Schori (2016b: fibre bundles in the mesocarp).

Phylogeny. Lasianthera is sister to the other Stemonuraceae, but only five genera were sampled (Kårehed 2001).

Thanks. I am grateful to Melanie Schori for comments.

[Aquifoliaceae [Phyllonomaceae + Helwingiaceae]]: petiole bundle arcuate; leaves spiral, lamina margins toothed, stipules +, small, cauline; C lacking median adaxial ridge and incurved apex; style 0; ovule 1/carpel, integument 9-15 cells across, parietal tissue 0, endothelium +; fruit with separate pyrenes; exotesta and endotesta recognizable, rest crushed.

Age. Janssens et al. (2009) dated this node to 62±11.9 Ma, Magallón et al. (2015) to 64.2 Ma, while ca 69 Ma is the age in Tank et al. (2015: Table S1, S2). Bell et al. (2010: note topology) suggested that this node was (72-)56, 51(-35) Ma, in Wikström et al. (2015) an age of (90-)72(-62) Ma, and Yao et al. (20120) an age of (89.8-)84.7(-76.6) Ma.

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.

AQUIFOLIACEAE Berchtold & J. Presl, nom. cons.  - Back to Aquifoliales


(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; loss of introns 18-23 in RPB2 d copy, mitochondrial coxII.i3 intron 0.

1 [list]/405 (500): Ilex. ± 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).

The distinctive pollen of Ilex is known from Cretaceous-Turonian deposits ca 80 Ma 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 (Martin 1977; Loizeau et al. 2005; Carpenter et al. 2015; see also 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. See Loizeau et al. (2005) and Yao et al. (2019) for literature on the common and widespread pre-diversification fossils, including distinctive pollen, of Ilex. 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 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 by a single species, Apis cerana (Tsang & Corlett 2012).

The fruits are 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). Aquifoliaceae were included in a very heterogeneous Celastrales by Cronquist (1981).

Synonymy: Ilicaceae Dumortier

[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  - Back to Aquifoliales


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 = ?

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).

Synonymy: Dulongiaceae J. G. Agardh, nom. illeg.

HELWINGIACEAE Decaisne  - Back to Aquifoliales


(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 = , 1819.

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

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.