EMBRYOPSIDA Pirani & Prado (crown group)

Gametophyte dominant, independent, multicellular, thalloid, with single-celled apical meristem, showing gravitropism; flavonoids + [absorbtion of UV radiation]; protoplasm dessication tolerant [plant poikilohydric]; cuticle +; cell walls with (1->4)-ß-D-glucans [xyloglucans], lignin +; rhizoids unicellular; several chloroplasts per cell; glycolate metabolism in leaf peroxisomes [glyoxysomes]; centrioles in vegetative cells 0, metaphase spindle anastral, predictive preprophase band of microtubules, phragmoplast + [cell wall deposition spreading from around the spindle fibres], plasmodesmata +; antheridia and archegonia jacketed, stalked; spermatogenous cells monoplastidic, centrioles develop de novo, associated with basal bodies of flagellae, multilayered structure +, proximal end of basal bodies lacking symmetry, stellate pattern associated with doublet tubules of transition zone; spermatozoids with a left-handed coil; male gametes with 2 lateral flagellae; oogamy; diploid embryo initially surrounded by haploid gametophytic tissue, plane of first division horizontal [with respect to long axis of archegonium/embryo sac], suspensor/foot +, cell walls with nacreous thickenings; sporophyte multicellular, sporangium +, single, with polar transport of auxin, dehiscence longitudinal; meiosis sporic, monoplastidic, microtubule organizing centre associated with plastid, cytokinesis simultaneous, preceding nuclear division, sporocytes 4-lobed, with a quadripolar microtubule system; spores in tetrads, sporopollenin in the spore wall, wall with several trilamellar layers [white-line centred layers, i.e. walls multilamellate]; spores trilete [?level]; close association between the trnLUAA and trnFGAA genes on the chloroplast genome.

Note that many of the bolded characters in the characterization above are apomorphies in the streptophyte clade along the lineage leading to the embryophytes rather than being apomorphies of the embryophytes.

STOMATOPHYTES

Abscisic acid, ?D-methionine +; sporangium with seta, seta developing from basal meristem [between epibasal and hypobasal cells], sporangial columella + [developing from endothecial cells]; stomata +, anomocytic, cell lineage that produces them with symmetric divisions [perigenous]; underlying similarities in the development of conducting tissue and in rhizoids/root hairs; polar transport of auxins and class 1 KNOX genes expressed in the sporangium alone; MIKC, MI*K*C* and class 1 and 2 KNOX genes, post-transcriptional editing of chloroplast genes; gain of three group II mitochondrial introns.

[Hornworts + Polysporangiophyta]: archegonia embedded/sunken in the gametophyte; sporophyte long-lived, chlorophyllous, nutritionally largely independent of the gametophyte; sporophyte-gametophyte junction interdigitate, sporophyte cells showing rhizoid-like behaviour; spores trilete.

POLYSPORANGIOPHYTA

Sporophyte well developed, branched, free living, sporangia several; spore walls not multilamellate [?here]; apical meristem +.

EXTANT TRACHEOPHYTA / VASCULAR PLANTS

Photosynthetic red light response; water content of protoplasm relatively stable [plant homoiohydric]; control of leaf hydration passive; (condensed or nonhydrolyzable tannins/proanthocyanidins +); vascular tissue +, sieve cells + [nucleus degenerating], tracheids +, in both protoxylem and metaxylem; endodermis +; root xylem exarch [development centripetal]; stem with an apical cell; branching dichotomous; leaves spirally arranged, blades with mean venation density 1.8 mm/mm2 [to 5 mm/mm2]; sporangia adaxial on the sporophyll, sporangia derived from periclinal divisions of several epidermal cells, wall multilayered [eusporangium]; columella 0; stellate pattern split between doublet and triplet regions of transition zone; placenta with single layer of transfer cells in both sporophytic and gametophytic generations, embryo with roots arising lateral to the main axis [plant homorhizic].

[MONILOPHYTA + LIGNOPHYTA]

Branching ± monopodial; lateral roots +, endogenous, root apex multicellular, root cap +; tracheids with scalariform-bordered pits; leaves with apical/marginal growth, venation development basipetal, growth determinate; sporangia borne in pairs and grouped in terminal trusses, dehiscence longitudinal, a single slit; cells polyplastidic, microtubule organizing centres not associated with plastids, diffuse, perinuclear; male gametes multiflagellate, basal bodies staggered, blepharoplasts paired; chloroplast long single copy ca 30kb inversion [from psbM to ycf2].

LIGNOPHYTA

Plant woody; lateral root origin from the pericycle; shoot apical meristem multicellular; branching lateral, meristems axillary; cork cambium + [producing cork abaxially], vascular cambium bifacial [producing phloem abaxially and xylem adaxially].

EXTANT SEED PLANTS/SPERMATOPHYTA

Plant evergreen; nicotinic acid metabolised to trigonelline, (cyanogenesis via tyrosine pathway); primary cell walls rich in xyloglucans and/or glucomannans, 25-30% pectin [Type I walls]; lignins derived from (some) sinapyl and particularly coniferyl alcohols [hence with p-hydroxyphenyl and guaiacyl lignin units, so no Maüle reaction]; root with xylem and phloem originating on alternate radii, vascular tissue not medullated, cork cambium deep seated; arbuscular mycorrhizae +; shoot apical meristem interface specific plasmodesmatal network; stem with vascular cylinder around central pith [eustele], phloem abaxial [ectophloic], endodermis 0, xylem endarch [development centrifugal]; 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 +; stem cork cambium superficial; branches exogenous; leaves with single trace from vascular sympodium [nodes 1:1]; stomatal pore with active opening in response to leaf hydration, control by abscisic acid, metabolic regulation of water use efficiency, etc.; leaves with petiole and lamina, development basipetal, blade simple; axillary buds +, not associated with all leaves; prophylls two, lateral; plant heterosporous, sporangia borne on sporophylls; microsporophylls aggregated in indeterminate cones/strobili; true pollen +, grains mono[ana]sulcate, exine and intine homogeneous; ovules unitegmic, parietal tissue 2+ cells across, megaspore tetrad linear, functional megaspore single, chalazal, lacking sporopollenin, megasporangium indehiscent; pollen grains landing on ovule; male gametophyte development first endo- then exosporic, tube developing from distal end of grain, gametes two, developing after pollination, with cell walls; female gametophyte endosporic, initially syncytial, walls then surrounding individual nuclei; seeds "large" [ca 8 mm3], but not much bigger than ovule, with morphological dormancy; embryo cellular ab initio, endoscopic, plane of first cleavage of zygote transverse, suspensor +, short-minute, embryo axis straight, so shoot and root at opposite ends [plant allorhizic], white, cotyledons 2; plastid transmission maternal; ycf2 gene in inverted repeat, whole nuclear genome duplication [zeta duplication], two copies of LEAFY gene, PHY gene duplications [three - [BP [A/N + C/O]] - copies], nrDNA with 5.8S and 5S rDNA in separate clusters; mitochondrial nad1 intron 2 and coxIIi3 intron and trans-spliced introns present.

MAGNOLIOPHYTA

Lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, apigenin and/or luteolin scattered, [cyanogenesis in ANITA grade?], S [syringyl] lignin units common [positive Maüle reaction - syringyl:guaiacyl ratio more than 2-2.5:1], and hemicelluloses as xyloglucans; root apical meristem intermediate-open; root vascular tissue oligarch [di- to pentarch], lateral roots arise opposite or immediately to the side of [when diarch] xylem poles; origin of epidermis with no clear pattern [probably from inner layer of root cap], trichoblasts [differentiated root hair-forming cells] 0, exodermis +; shoot apex with tunica-corpus construction, tunica 2-layered; reaction wood ?, associated gelatinous fibres [g-fibres] with innermost layer of secondary cell wall rich in cellulose and poor in lignin; starch grains simple; primary cell wall mostly with pectic polysaccharides, poor in mannans; tracheid:tracheid [end wall] plates with scalariform pitting, wood parenchyma +; sieve tubes enucleate, sieve plate with pores (0.1-)0.5-10< µm across, cytoplasm with P-proteins, cytoplasm not occluding pores of sieve plate, companion cell and sieve tube from same mother cell; sugar transport in phloem passive; nodes 1:?; stomata brachyparacytic [ends of subsidiary cells level with ends of pore], outer stomatal ledges producing vestibule, reduction in stomatal conductance to increasing CO2 concentration; lamina formed from the primordial leaf apex, margins toothed, development of venation acropetal, overall growth ± diffuse, venation hierarchical-reticulate, secondary veins pinnate, veins (1.7-)4.1(-5.7) mm/mm2, endings free; most/all leaves with axillary buds; flowers perfect, pedicellate, ± haplomorphic, parts spiral [esp. the A], free, numbers unstable, development in general centripetal; P +, members 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], ± embedded in the filament, with at least outer secondary parietal cells dividing, each theca dehiscing longitudinally, endothecium +, endothecial cells elongated at right angles to long axis of anther; tapetum glandular, cells binucleate; microspore mother cells in a block, microsporogenesis successive, walls developing by centripetal furrowing; pollen subspherical, tectum continuous or microperforate, ektexine columellate, endexine thin, compact, lamellate only in the apertural regions; nectary 0; carpels present, superior, free, several, ascidiate, with postgenital occlusion by secretion, stylulus short, hollow, cavity not lined by distinct epidermal layer, stigma ± decurrent, carinal, dry [not secretory]; 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 [crassinucellate], nucellar cap?; megasporocyte single, hypodermal, functional megaspore lacking cuticle; female gametophyte four-celled [one module, nucleus of egg cell sister to one of the polar nuclei]; supra-stylar extra-gynoecial compitum +; ovule not increasing in size between pollination and fertilization; pollen grains landing on stigma, bicellular at dispersal, mature male gametophyte tricellular, germinating in less than 3 hours, pollination siphonogamous, tube elongated, growing between cells, growth rate 20-20,000 µm/hour, outer wall pectic, inner wall callose, 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 gametes lacking cell walls, flagellae 0, double fertilization +, ovules aborting unless fertilized; P deciduous in fruit; seed exotestal, becoming much larger than ovule at time of fertilization; endosperm diploid, cellular [micropylar and chalazal domains develop differently, 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; embryogenesis cellular; dark reversal Pfr -> Pr; Arabidopsis-type telomeres [(TTTAGGG)n]; 2C genome size 1-8.2 pg [1 pg = 109 base pairs], whole nuclear genome duplication [epsilon duplication]; protoplasm dessication tolerant [plant poikilohydric]; 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, paleo AP3 and PI genes [paralogous B-class genes] +, with "DEAER" motif, SEP3/LOFSEP and three copies of the PHY gene, [PHYB [PHYA + PHYC]].

[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]]]]: vessel elements with scalariform perforation plates in primary xylem; essential oils in specialized cells [lamina and P ± pellucid-punctate]; tension wood +; tectum reticulate; anther wall with outer secondary parietal cell layer dividing; carpels plicate; 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 [possible position]; pollen tube growth intra-gynoecial; embryo sac bipolar, 8 nucleate, antipodal cells persisting; endosperm triploid.

[MONOCOTS [CERATOPHYLLALES + EUDICOTS]]: (extra-floral nectaries +); (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.

EUDICOTS: (Myricetin, delphinidin +), asarone 0 [unknown in some groups, + in some asterids]; root epidermis derived from root cap [?Buxaceae, etc.]; (vessels with simple perforation plates in primary xylem); nodes 3:3; stomata anomocytic; flowers (dimerous), cyclic; K/outer P members with three traces, ("C" +, with a single trace); A few, (polyandry widespread, initial primordia 5, 10, or ring, ± centrifugal), 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]; seed coat?

[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]: ?

CORE EUDICOTS / GUNNERIDAE: (ellagic and gallic acids +); leaf margins serrate; compitum + [one place]; micropyle?; whole nuclear genome duplication [palaeohexaploidy, gamma triplication], 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 = calyx + corolla, the calyx enclosing the flower in bud, sepals with three or more traces, petals with a single trace; stamens = 2x K/C, in two whorls developing internally/adaxially to the corolla whorl and successively alternating, (numerous, but then usually fasciculate and/or centrifugal); pollen tricolporate; G [5], G [3] also common, when [G 2], carpels superposed, compitum +, placentation axile, style +, stigma not decurrent; endosperm nuclear; fruit dry, dehiscent, loculicidal [when a capsule]; RNase-based gametophytic incompatibility system present; floral nectaries with CRABSCLAW expression.

[SANTALALES [BERBERIDOPSIDALES [CARYOPHYLLALES + ASTERIDS]]] / ASTERIDS ET AL. / SUPERASTERIDS : ?

[BERBERIDOPSIDALES [CARYOPHYLLALES + ASTERIDS]]: ?

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

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

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

[ASTERID I + ASTERID II] / CORE ASTERIDS: ellagic acid 0, non-hydrolysable tannins not common; sugar transport in phloem active; inflorescence basically cymose; A = and opposite sepals or P, (numerous, usu. associated with increased numbers of C or G); (pollen with orbicules); style short[?]; duplication of the PI gene.

ASTERID II / CAMPANULIDAE Back to Main Tree

Myricetin 0; vessel elements with scalariform perforation plates; flowers rather small; style shorter than the ovary; endosperm copious, embryo short/very short.

Age. Wikström et al. (2001) suggested an age of (112-)107, 99(-94) m.y., Bremer et al. (2004) an age of about 121 m.y. and Magallón and Castillo (2009) an age of ca 99.5 m.y. for the crown group, Janssens et al. (2009) an age of 113±9.8 m.y., Moore et al. (2010: 95% HPD) suggested ages of (81-)75(-71) m.y., Bell et al. (2010) ages of (109-)102, 100(-85) m.y., while Beaulieu et al. (2013a: 95% HPD) estimated ages of (115-)104(-95) m.y.. around 92.7 m.y. is an estimate in Naumann et al. (2013).

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

Evolution. Divergence & Distribution. Diversification at this node probably occurred in the southern hemisphere (Beaulieu et al. 2013a). For the evolution of plant habit in the asterid II clade, see Beaulieu et al. (2013b).

As mentioned on the asterid I/Garryales page, taxa with relatively small flowers that are aggregated into flower-like inflorescences (see Leins & Erbar 2010: fig 157) are common in all three large orders in this clade. However, the feature "small flowers" may be assignable to the asterid I + II node, since the first nodes of both the asterid I and II clades may have this feature; I have only tentatively placed it here. The asterid II clade as a whole certainly has many taxa with small flowers (but c.f. Campanulaceae, etc.) that are often aggregated into more conspicuous inflorescences, the apices of the petals tend to be pointed (not in Aquifoliaceae), valvate corollas are common.

In the asterid II clade the fruits often have few (often 1-2) seeds. Beaulieu and Donoghue (2013) examine fruit evolution in the clade from an ecological point of view and conclude that the plesiomorphic fruit type for the whole group was likely to be dry, dehiscent, and with two or more seeds. Achenes, dry, indehiscent, and single seeded fruits (they include Apiaceae here, although in this case achenes are the individual mericarps that result from the separation/dehiscence of the two-seeded fruits) and were often associated with increased diversification rates - although they note that it is unclear if there was a causal connection. These results may have to be modified somewhat when outgroups are included and if fruit types are redefined.

Plant-Animal Interactions. There has been much diversification of asterid II clades by dipteran agromyzid leaf miner Phytomyza clades moving from Ranunculaceae (Winkler et al. 2009: >700 species in the genus).

Phylogeny. For discussion about the position of Aquifoliaceae and the circumscription of the asterid I and II clades, see the [asterid 1 + asterid II] clade).

There is now moderate (Olmstead et al. 2000; Soltis et al. 2000) to strong (B. Bremer et al. 2002; Janssens et al. 2009) support for Aquifoliales as sister to the rest of the asterid II clade. The position of Dipsacales within the asterid II 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]] and Qiu et al. (2010) for [Apiales [Dipsacales + Asterales]], while 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.

For the positions of the smaller clades along the asterid II spine, which are now mostly settling down, see Escalloniales.

AQUIFOLIALES Senft  Main Tree.

Iridoids?; vessel elements with scalariform perforation plates; petiole bundles arcuate; inflorescence axillary; C valvate, free, ?development; A free; nectary +; ovules 1-2/carpel, apical, pendulous, apotropous; fruit drupaceous, stones one-seeded. - 5 families, 21 genera, 536 species.

Age. K. Bremer et al. (2004) suggested an age of about 113 m.y. for this node, Bell et al. (2010) ages of (101-)88, 87(-85) m.y..

Note: Possible apomorphies are in bold. However, the actual level at which many of these features, particularly the more cryptic ones, should be assigned is unclear. This is partly because many characters show considerable homoplasy, in addition, basic information for all too many 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 is the not-so-trivial issue of how ancestral states are reconstructed...

Evolution. Divergence & Distribution. In their study of the evolution of plant habit in the asterid II clade, Beaulieu et al. (2013b) noted that growth form was notably constrained in Aquifoliales; all members are woody.

Chemistry, Morphology, etc. With the partial exception of Aquifoliaceae, gynoecial morphology, embryology, testa anatomy, and chemistry of this order are little known. For a summary of pollen variation, see Schori and Furness (2011).

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 monophyletic clade - they also have several other features in common (see below) - seemed a little odd, but recent comprehensive analyses of the asterid II clade (Tank et al. 2007) recovered a sister group relationship between them (1.0 p.p.), as did Soltis et al. (2011: 99% ML bootstrap).

Irvingbaileya and Gomphandra, ex-Icacinaceae, were placed with strong support in Aquifoliales (D. Soltis et al. 2000), and the group was expanded by Kårehed (2001). There is very strong support for the basic structure [[Cardiopteridaceae + Stemonuraceae] [Ilex, Phyllonoma, Helwingia]] (Kårehed 2001; only 1 sp. of Ilex included; Lens et al. 2008b). The grouping [Cardiopteridaceae + Pentaphylacaceae] had weak support in an earlier single gene analysis (Savolainen et al. 2000b); for the latter family, see Ericales.



Includes Aquifoliaceae, Cardiopteridaceae, Helwingiaceae, Phyllonomaceae, Stemonuraceae.

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

[Cardiopteridaceae + Stemonuraceae]: pits usually not bordered; apotracheal parenchyma and variants common; (crystal sand in wood rays); nodes 3:3; stomata cyclocytic to anisocytic; hairs unicellular (adpressed); leaves two-ranked or spiral, lamina margins entire; (plant dioecious); petals inflexed at apex, (ridged adaxially); A basifixed; pollen (1-)3(-6)-porate; G [2], unilocular, adaxial carpel alone fertile; ovules 2/carpel, apical, thinly crassinucellate, integument vascularized, funicular obturator +; fruit 1-seeded; testa vascularized; embryo very short.

Age. An age for this clade of (90-)83, 65(-58) m.y. is suggested by Wikström et al. (2001) and of (90-)73, 66(-43) m.y. by (Bell et al. 2010).

Chemistry, Morphology, etc. The two sides of the gynoecium/fruit are sometimes dramatically different in appearance; this needs to be related to gynoecial development.

For information, see Bailey and Howard (1941, their group II: anatomy), Mauritzon (1936c), Fagerlind (1945a), and Padmanabhan (1961: Gomphandra), all embryology, Heintzelmann and Howard (1948: indumentum and crystals), Sleumer (1942, 1971a: general), van Staveren and Baas (1973) and Baas (1973, 1974) all epidermis and stomata, Lobreau-Callen (1977, 1980: pollen), Kaplan et al. (1991: chemistry), Teo and Haron (1999: anatomy). Kårehed (2001, 2002b) discusses the taxa in their current familial circumscriptions, while Lens et al. (2008a; see also Noshiro & Baas 1998) provide a detailed anatomical survey in a phylogenetic context.

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, near (Garryales) and Pennantiaceae, in Apiales.

CARDIOPTERIDACEAE Blume, nom. cons.   Back to Aquifoliales

Cardiopteridaceae

(Twining vine); plants Al accumulators [?all], iridoids?; (vessel elements with scalariform perforation plates only); petiole bundles annular (+ medullary); (articulated laticifers + - Cardiopteris); stomata also anomocytic and paracytic; (lamina margins toothed), (secondary veins palmate); (plant dioecious, andromonoecious); (inflorescence branched, ultimate units clearly cymose or not), (bracts 0); K basally connate, quincuncial, C usu. connate, (imbricate); A often adnate to C, also dorsifixed; (pollen tricolporate - Citronella), (nectary 0); carpels superposed, (pseudoloculus - Pseudobotrys, Citronella), style usu. slender, relatively long,, stigma truncate or capitate, (branched to the base, branches heteromorphic, one stout, lobed and grooved, the other slender, with capitate stigma Cardiopteris); (ovule 1); (fruit 2-winged samara, wings horizontally striate, stout style accrescent Cardiopteris); ?testa; endosperm ?development, (ruminate), (embryo long, with foliaceous cotyledons); 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).

        Cardiopteridaceae are a rather heterogeneous group of genera, although there are one or sometimes two rather slender and quite short styles. The fruits are more or less flattened and/or ridged drupes.

Chemistry, Morphology, etc. Cardiopteris itself looks rather like Dioscorea, but the latter has three-merous flowers and an inferior ovary. 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. 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. This is rather remarkable and needs confirmation; the ovules are more likely to be anatropous.

For additional literature, see above, also Lobreau-Callen (1982: pollen, Peripterygium), and Vera-Caletti and Wendt (2001: new genus described).

Phylogeny. Lasianthera was sister to the four other genera examined (Kårehed 2001). Dendrobangia does not (see Apodytes group - Garryales) and Pseudobotrys may not belong here (M. Schori, pers. comm. vi.2010).

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

Stemonuraceae

Iridoids +; vessel elements with simple perforation plates, in multiples; petiole bundles arcuate + wing or annular + medullary; sclereids +/0; plant dioecious or flowers perfect; pedicels articulated, flowers 4-5(-7) merous; K connate, (C connate), (adaxially keeled); filaments often stout and with club-shaped hairs, connective well developed, tapetum multinucleate, (staminodes +/0 - carpellate flowers); (pollen colpate), (surface echinate, striate); (nectary unilateral), (0); (pistillode + - staminate flowers); carpel arrangement?; style 0, stigma broad; ovule with integument ³10 cells across; drupe compressed dorsi-ventrally (rounded), often broadly sulcate, (the two sides very different, one with a fleshy "appendage" developing over the sulcus), (pseudoloculus + Cantleya), endocarp with ridges and grooves on the side of the appendage, when present; testa thick, outer cells thick-walled, elongate, inner cells not thickened, post-chalazal bundle +; endosperm free-nuclear; n = 22. ILLUSTRATION.

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

Chemistry, Morphology, etc. The carpellate 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.

Phylogeny. Note that Lasianthera, with colporate pollen, 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]]: nodes 1:1; petiole bundle arcuate; leaves spiral, lamina margins toothed, "stipules" +, small, cauline; style 0; fruit with separate pyrenes.

Age. Janssens et al. (2009) dated this node to 62±11.9 m.y.; however, any of the fossil records attributed to Ilex itself, some apparently much older - must be minimum estimates of the age of this crown group. Bell et al. (2010: note topology) suggested that this node was (72-)56, 51(-35) m.y.o..

The distinctive pollen of Ilex is known from Cretaceous Turonian deposits ca 80 m.y.o. in S.E. Australia, and there are perhaps older records, although lacking photographs of the distinctive pollen (Martin 1977; Loizeau et al. 2005); Manen et al. (2010) used a date of ca 69 m.y. for the oldest fossils, Beaulieu et al. (2013a) an age of ca 65 m.y. (a fossil "seed").

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

Aquifoliaceae

Evergreen (deciduous) trees or shrubs (climbers); tanniniferous, iridoids 0; (vessel elements in multiples); resiniferous, laticiferous idioblasts +; nodes also 3:3, etc.; petiole bundles arcuate to annular and complex; 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 4-9-merous; C imbricate, often connate basally; A adnate to base of C (free); pollen surface conspicuously gemmate/clavate; G [(2-)4-6(-many)], opposite petals, gynoecial nectary +, placentation axile basally, becoming free-central, stigma broad, wet; ovules (2/carpel), integument 12-15 cells across, parietal tissue ca 1 cell across, hypostase +, funicular obturator papillate (0); fruit with several stones, stigma prominent in fruit, K deciduous (semipersistent); exotestal cells cuboid, tangentially elongated, inner walls lignified, rest crushed, endotesta tanniniferous; endosperm hemicellulosic; n = 9, 10; loss of introns 18-23 in RPB2 d copy, mitochondrial coxII.i3 intron 0.

1[list]/405: Ilex. ± World-wide, esp. America and South East Asia-Malesia, one species in Africa (map: see Meusel et al. 1978; Loiseau et al. 2005). [Photo - Staminate Flower, Carpellate Flower.]

Age. Crown group Ilex, or at least its plastome, may be a mere 15 m.y. old (Miocene), which suggests that there may previously have been much extinction in the clade (Manen et al. 2010).

Evolution. Divergence & Distribution. There is evidence of extensive hybridization within crown-group Ilex (Manen et al. 2010).

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 and below). Ilex is one of the genera that has become extinct in New Zealand in the Tertiary (Lee et al. 2001).

Pollination Biology & Seed Dispersal.The great majority of visits to the 12 species of Ilex observed on Hongkong were from the one species of bee, Apis cerana; the fruits are low quality and are eaten by birds (Tsang & Corlett 2012).

Chemistry, Morphology, etc. Palisade glandular tissues with protein rich secretions are found on the leaf teeth and stipules; the latter have been called colleters as a result (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, but in any event it collects between the stamens in a little pocket formed by the gynoecium and petals. The integument is about 15 cells across (e.g. van Tieghem 1898). The embryo is often minute and barely developed at the time when the fruit is dispersed, only slowly maturing afterwards (Herr 1961; Tsang & Corlett 2005 for references).

See Copeland (1964) for general information, Baas (1975) for vegetative anatomy, Lobreau-Callen (1977), and Martin (1977) for pollen; 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. 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); it is noteworthy that Hawaiian and New Caledonian species were embedded in an American clade (MCC value of 0.84).

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; lamina with brochidodromous venation, stipules fimbriate; inflorescence epiphyllous, on adaxial side of lamina; nectary annular; ovary inferior, stigmas & separate, ± elongated, recurved.

Age. The age of this node is around 66 m.y. (K. Bremer et al. 2004).

PHYLLONOMACEAE Small   Back to Aquifoliales

Phyllonomaceae

Evergreen trees or shrubs; plants Al accumulators; cork cambium?; young stem with separate bundles; petiole bundle annular; plant glabrous, leaves ?two-ranked; inflorescences racemose, usu. branched, bracteoles 0; flowers perfect, odd sepal abaxial; K 4-5, with one trace, quincuncial, with stout marginal glandular hairs, C 3-5, adaxially weakly keeled; filaments shorter than anthers; G 2, collateral(-suboblique), placentation intrusive parietal; ovules 6-7/carpel, parietal tissue ca 1 cell across, nucellus base broad; fruit a berry, few-seeded; testa multilayered, exotestal cells large, thick-walled, mucilaginous, 2-3 layers of flattened cells; endosperm hemicellulosic; n = ?

1/4. 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).

See Thouvenin (1890) for general information, Tobe (2013) for floral morphology, Mauritzon (1933) for some embryology, Krach (1976) and Takhtajan (2000) for seed anatomy, Mori and Kallunki (1977) for a revision.

Previous Relationships. Krach (1977) suggested that the seeds of Phyllonoma and those of Grossulariaceae were similar. 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

Helwingiaceae

Deciduous or evergreen trees or shrubs; flavones, chlorogenic acid, unidentified iridoids +; septate fibres with minutely bordered pits; silica grains +; pericyclic fibres 0; petiole bundle arcuate, also two small adaxial inverted bundles; cuticle wax crystalloids 0; lamina vernation supervolute-curved; plant dioecious; inflorescence fasciculate; P +, 3-5, valvate; staminate flowers: stamens alternating with P; pollen with diffuse endoapertures; ?pistillode minute [not seen]; carpellate flowers: staminodes 0; G [2-4], alternating with P, stigma dry; ovule 1/carpel, ?apotropous, pachychalazal, integument thick, incompletely tenuinucellate; testa thin; endosperm weakly ruminate, ?development; n = 19.

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

Chemistry, Morphology, etc. The fasciculate inflorescence is clearly cymose (Weber 2004c; pers. obs.). Helwingiaceae may be interpreted as lacking a calyx, and so stamens and corolla would alternate (e.g. Takhtajan 1997), as is almost universal in the asterid I + II clades. There is no evidence of a calyx from external morphology, but if the corolla is indeed absent (as tentatively suggested by Tobe 2013), the stamen position would then be very odd for a member of this clade. In staminate flowers, small globules (?nectar) form on the flat central area between the stamens. The ventral carpel bundles are central.

For chemistry, see Iwashina et al. (1997), for embryo and seed, see Korobova (1980); see also Decaisne (1836) and Wangerin (1906), both general, Horne (1914: flower), Dickinson and Sattler (1975: inflorescence), and Hara and Kurosawa (1975: revision).

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.