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].
II. TRACHEOPHYTA / VASCULAR PLANTS
Sporophyte long lived, cells polyplastidic, photosynthetic red light response, stomata open in response to blue light; plant homoiohydrous [water content of protoplasm relatively stable]; control of leaf hydration passive; plant endohydrous [physiologically important free water inside plant]; PIN[auxin efflux facilitators]-mediated polar auxin transport; (condensed or nonhydrolyzable tannins/proanthocyanidins +); borate cross-linked rhamnogalactan II, xyloglucans with side chains uncharged [?level], in secondary walls of vascular and mechanical tissue; lignins +; roots +, often ≤1 mm across, root hairs and root cap +; stem apex multicellular [several apical initials, no tunica], with cytohistochemical zonation, plasmodesmata formation based on cell lineage; vascular development acropetal, tracheids +, in both protoxylem and metaxylem, G- and S-types; sieve cells + [nucleus degenerating]; endodermis +; stomata numerous, involved in gas exchange; leaves +, vascularized, spirally arranged, blades with mean venation density ca 1.8 mm/mm2 [to 5 mm/mm2], all epidermal cells with chloroplasts; sporangia in strobili, sporangia adaxial, columella 0; tapetum glandular; sporophyte-gametophyte junction lacking dead gametophytic cells, mucilage, ?position of transfer cells; MTOCs not associated with plastids, basal body 350-550 nm long, stellate array in transition region initially joining microtubule triplets; archegonia embedded/sunken [only neck protruding]; embryo suspensor +, shoot apex developing away from micropyle/archegonial neck [from hypobasal cell, endoscopic], root lateral with respect to the longitudinal axis of the embryo [plant homorhizic].[MONILOPHYTA + LIGNOPHYTA]
Sporophyte growth ± monopodial, branching spiral; roots endomycorrhizal [with Glomeromycota], lateral roots +, endogenous; G-type tracheids +, with scalariform-bordered pits; leaves with apical/marginal growth, venation development basipetal, growth determinate; sporangium dehiscence by a single longitudinal slit; cells polyplastidic, MTOCs diffuse, perinuclear, migratory; blepharoplasts +, paired, with electron-dense material, centrioles on periphery, male gametes multiciliate; nuclear genome [1C] 7.6-10 pg [mode]; chloroplast long single copy ca 30kb inversion [from psbM to ycf2]; mitochondrion with loss of 4 genes, absence of numerous group II introns; LITTLE ZIPPER proteins.
Sporophyte woody; stem branching axillary, buds exogenous; lateral root origin from the pericycle; cork cambium + [producing cork abaxially], vascular cambium bifacial [producing phloem abaxially and xylem adaxially].
SEED PLANTS† / SPERMATOPHYTA†
Growth of plant bipolar [plumule/stem and radicle/root independent, roots positively geotropic]; plants heterosporous; megasporangium surrounded by cupule [i.e. = unitegmic ovule, cupule = integument]; pollen lands on ovule; megaspore germination endosporic, female gametophyte initially retained on the plant, free-nuclear/syncytial to start with, walls then coming to surround the individual nuclei, process proceeding centripetally.
EXTANT SEED PLANTS
Plant evergreen; nicotinic acid metabolised to trigonelline, (cyanogenesis via tyrosine pathway); microbial terpene synthase-like genes 0; primary cell walls rich in xyloglucans and/or glucomannans, 25-30% pectin [Type I walls]; lignin chains started by monolignol dimerization [resinols common], particularly with guaiacyl and p-hydroxyphenyl [G + H] units [sinapyl units uncommon, no Maüle reaction]; roots often ≥1 mm across, stele diarch to pentarch, xylem and phloem originating on alternating radii, cork cambium deep seated, gravitropism response fast; stem apical meristem complex [with quiescent centre, etc.], plasmodesma density in SAM 1.6-6.2[mean]/μm2 [interface-specific plasmodesmatal network]; eustele +, protoxylem endarch, endodermis 0; wood homoxylous, tracheids and rays alone, tracheid/tracheid pits circular, bordered; mature sieve tube/cell lacking functioning nucleus, sieve tube plastids with starch grains; phloem fibres +; cork cambium superficial; leaf nodes 1:1, a single trace leaving the vascular sympodium; leaf vascular bundles amphicribral; guard cells the only epidermal cells with chloroplasts, stomatal pore with active opening in response to leaf hydration, control by abscisic acid, metabolic regulation of water use efficiency, etc.; branching by axillary buds, exogenous; prophylls two, lateral; leaves with petiole and lamina, development basipetal, lamina simple; sporangia borne on sporophylls; spores not dormant; microsporophylls aggregated in indeterminate cones/strobili; grains monosulcate, aperture in ana- position [distal], primexine + [involved in exine pattern formation with deposition of sporopollenin from tapetum there], exine and intine homogeneous, exine alveolar/honeycomb; ovules with parietal tissue [= crassinucellate], megaspore tetrad linear, functional megaspore single, chalazal, sporopollenin 0; gametophyte ± wholly dependent on sporophyte, development initially endosporic [apical cell 0, rhizoids 0, etc.]; male gametophyte with tube developing from distal end of grain, male gametes two, developing after pollination, with cell walls; embryo cellular ab initio, suspensor short-minute, embryonic axis straight [shoot and root at opposite ends], primary root/radicle produces taproot [= allorhizic], cotyledons 2; embryo ± dormant; chloroplast ycf2 gene in inverted repeat, trans splicing of five mitochondrial group II introns, rpl6 gene absent; ??whole nuclear genome duplication [ζ/zeta duplication event], 2C genome size (0.71-)1.99(-5.49) pg, two copies of LEAFY gene, PHY gene duplications [three - [BP [A/N + C/O]] - copies], 5.8S and 5S rDNA in separate clusters.
IID. ANGIOSPERMAE / MAGNOLIOPHYTA
Lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, apigenin and/or luteolin scattered, [cyanogenesis in ANA grade?], lignin also with syringyl units common [G + S lignin, positive Maüle reaction - syringyl:guaiacyl ratio more than 2-2.5:1], hemicelluloses as xyloglucans; root cap meristem closed (open); pith relatively inconspicuous, lateral roots initiated immediately to the side of [when diarch] or opposite xylem poles; epidermis probably originating from inner layer of root cap, trichoblasts [differentiated root hair-forming cells] 0, hypodermis suberised and with Casparian strip [= exodermis]; shoot apex with tunica-corpus construction, tunica 2-layered; starch grains simple; primary cell wall mostly with pectic polysaccharides, poor in mannans; tracheid:tracheid [end wall] plates with scalariform pitting, multiseriate rays +, wood parenchyma +; sieve tubes enucleate, sieve plates with pores (0.1-)0.5-10< µm across, cytoplasm with P-proteins, not occluding pores of plate, companion cell and sieve tube from same mother cell; ?phloem loading/sugar transport; nodes 1:?; dark reversal Pfr → Pr; protoplasm dessication tolerant [plant poikilohydric]; stomata randomly oriented, brachyparacytic [ends of subsidiary cells ± level with ends of guard cells], outer stomatal ledges producing vestibule, reduction in stomatal conductance with increasing CO2 concentration; lamina formed from the primordial leaf apex, margins toothed, development of venation acropetal, overall growth ± diffuse, secondary veins pinnate, fine venation hierarchical-reticulate, (1.7-)4.1(-5.7) mm/mm2, vein endings free; flowers perfect, pedicellate, ± haplomorphic, protogynous; parts free, numbers variable, development centripetal; P = T, petal-like, each with a single trace, outer members not sharply differentiated from the others, not enclosing the floral bud; A many, filament not sharply distinguished from anther, stout, broad, with a single trace, anther introrse, tetrasporangiate, sporangia in two groups of two [dithecal], each theca dehiscing longitudinally by a common slit, ± embedded in the filament, walls with at least outer secondary parietal cells dividing, endothecium +, cells elongated at right angles to long axis of anther; tapetal cells binucleate; microspore mother cells in a block, microsporogenesis successive, walls developing by centripetal furrowing; pollen subspherical, tectum continuous or microperforate, ektexine columellate, endexine restricted to the apertural regions, thin, compact, intine in apertural areas thick, orbicules +, pollenkitt +; nectary 0; carpels present, superior, free, several, spiral, ascidiate [postgenital occlusion by secretion], stylulus at most short [shorter than ovary], hollow, cavity not lined by distinct epidermal layer, stigma ± decurrent, carinal, dry; suprastylar extragynoecial compitum +; ovules few [?1]/carpel, marginal, anatropous, bitegmic, micropyle endostomal, outer integument 2-3 cells across, often largely subdermal in origin, inner integument 2-3 cells across, often dermal in origin, parietal tissue 1-3 cells across, nucellar cap?; megasporocyte single, hypodermal, functional megaspore lacking cuticle; female gametophyte lacking chlorophyll, four-celled [one module, egg and polar nuclei sisters]; ovule not increasing in size between pollination and fertilization; pollen grains bicellular at dispersal, germinating in less than 3 hours, siphonogamy, pollen tube unbranched, growing towards the ovule, between cells, growth rate (ca 10-)80-20,000 µm h-1, tube apex of pectins, wall with callose, lumen with callose plugs, penetration of ovules via micropyle [porogamous], whole process takes ca 18 hours, distance to first ovule 1.1-2.1 mm; male gametophytes tricellular, gametes 2, lacking cell walls, ciliae 0, double fertilization +, ovules aborting unless fertilized; fruit indehiscent, P deciduous; mature seed much larger than fertilized ovule, small [<5 mm long], dry [no sarcotesta], exotestal; endosperm +, ?diploid [one polar nucleus + male gamete], cellular, development heteropolar [first division oblique, micropylar end initially with a single large cell, divisions uniseriate, chalazal cell smaller, divisions in several planes], copious, oily and/or proteinaceous, embryo short [<¼ length of seed]; plastid and mitochondrial transmission maternal; Arabidopsis-type telomeres [(TTTAGGG)n]; nuclear genome [2C] (0.57-)1.45(-3.71) [1 pg = 109 base pairs], ??whole nuclear genome duplication [ε/epsilon event]; ndhB gene 21 codons enlarged at the 5' end, single copy of LEAFY and RPB2 gene, knox genes extensively duplicated [A1-A4], AP1/FUL gene, palaeo AP3 and PI genes [paralogous B-class genes] +, with "DEAER" motif, SEP3/LOFSEP and three copies of the PHY gene, [PHYB [PHYA + PHYC]]; chloroplast IR expansions, chlB, -L, -N, trnP-GGG genes 0.
[NYMPHAEALES [AUSTROBAILEYALES [[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).
MONOCOTYLEDONS / MONOCOTYLEDONEAE / LILIANAE Takhtajan
Plant herbaceous, perennial, rhizomatous, growth sympodial; non-hydrolyzable tannins [(ent-)epicatechin-4] +, neolignans 0, CYP716 triterpenoid enzymes 0, benzylisoquinoline alkaloids 0, hemicelluloses as xylan, cell wall also with (1->3),(1->4)-ß-D-MLGs [Mixed-Linkage Glucans]; root epidermis developed from outer layer of cortex; endodermal cells with U-shaped thickenings; cork cambium [uncommon] superficial; stele oligo- to polyarch, medullated [with prominent pith], lateral roots arise opposite phloem poles; stem primary thickening meristem +; vascular development bidirectional, bundles scattered, (amphivasal), vascular cambium 0 [bundles closed]; tension wood 0; vessel elements in roots with scalariform and/or simple perforations; tracheids only in stems and leaves; sieve tube plastids with cuneate protein crystals alone; ?nodal anatomy; stomata oriented parallel to the long axis of the leaf, in lines; prophyll single, adaxial; leaf blade linear, main venation parallel, of two or more size classes, the veins joining successively from the outside at the apex and forming a fimbrial vein, transverse veinlets +, unbranched [leaf blade characters: ?level], vein/veinlet endings not free, margins entire, Vorläuferspitze +, base broad, ensheathing the stem, sheath open, petiole 0; inflorescence terminal, racemose; flowers 3-merous [6-radiate to the pollinator], polysymmetric, pentacyclic; P = T = 3 + 3, all with three traces, median T of outer whorl abaxial, aestivation open, members of whorls alternating, [pseudomonocyclic, each T member forming a sector of any tube]; stamens = and opposite each T member [A/T primordia often associated, and/or A vascularized from T trace], anther and filament more or less sharply distinguished, anthers subbasifixed, wall with two secondary parietal cell layers, inner producing the middle layer [monocot type]; pollen reticulations coarse in the middle, finer at ends of grain, infratectal layer granular; G , with congenital intercarpellary fusion, opposite outer tepals [thus median member abaxial], placentation axile; compitum +; ovule with outer integument often largely dermal in origin, parietal tissue 1 cell across; antipodal cells persistent, proliferating; seed small to medium sized [mean = 1.5 mg], testal; embryo long, cylindrical, cotyledon 1, apparently terminal [i.e. bend in embryo axis], with a closed sheath, unifacial [hyperphyllar], both assimilating and haustorial, plumule apparently lateral; primary root unbranched, not very well developed, stem-borne roots numerous [= homorhizic], hypocotyl short, (collar rhizoids +); no dark reversion Pfr → Pr; nuclear genome [2C] (0.7-)1.29(-2.35) pg, duplication producing monocot LOFSEP and FUL3 genes [latter duplication of AP1/FUL gene], PHYE gene lost. (Some synapomorphies - almost whatever the immediate sister taxa to monocots might be - are in bold.)
[ALISMATALES [PETROSAVIALES [[DIOSCOREALES + PANDANALES] [LILIALES [ASPARAGALES + COMMELINIDS]]]]]: ethereal oils 0; (trichoblasts in vertical files, proximal cell smaller); raphides + (druses 0); leaf blade vernation supervolute-curved or variants, (margins with teeth, teeth spiny); endothecium develops directly from undivided outer secondary parietal cells; tectum reticulate with finer sculpture at the ends of the grain, endexine 0; septal nectaries + [intercarpellary fusion postgenital].
[PETROSAVIALES [[DIOSCOREALES + PANDANALES] [LILIALES [ASPARAGALES + COMMELINIDS]]]]: cyanogenic glycosides uncommon; starch grains simple, amylophobic; leaf blade developing basipetally from hyperphyll/hypophyll junction; epidermis with bulliform cells [?level]; stomata anomocytic, (cuticular waxes as parallel platelets); colleters 0.
[[DIOSCOREALES + PANDANALES] [LILIALES [ASPARAGALES + COMMELINIDS]]]]: nucellar cap 0; ovary inferior; endosperm nuclear [but variation in most orders].
Age. The age of this node was estimated at (127-)118, 105(-94) Ma (Bell et al. 2010), around 120 or 114.5 Ma by S. Chen et al. (2013), ca 119.8 Ma by Magallón et al. (2015; see also Givnish et al. 2016b), and ca 128 Ma by Foster et al. (2016a: q.v. for details), but only about 83.6 or 83.1 Ma by Xue et al. (2012).
Evolution: Divergence & Distribution. This is the core monocot clade of Coiffard et al. (2019), and they described Cratolirion bognerianum from rocks ca 113 Ma from the Crato formation in northeast Brazil which they thought could be placed around here - it was often associated with this clade in morphological analyses, perhaps particularly in the Dioscoreales/Pandanales area. The fossil implied that Liliales could already have diverged (Coiffard et al. 2019) - Acaciaephyllum, an early monocot fossil, had been associated with Liliales by Doyle et al. (2008b).
I largely follow Tobe et al. (2018) in the evolution of gynoecial position in monocots, in part to help think about different paths the evolution of this feature may have taken. Thus Endress (2011a) suggested that an inferior ovary was a separate key innovation for Zingiberales, Asparagales and Dioscoreales. There is evidence that inferior ovaries can become secondarily superior (e.g. Simpson 1998a; Remizova et al. 2008a; Tobe et al. 2018).
Thadeo et al. (2015) found that the anatomy of fleshy fruits in taxa scattered in this clade was quite similar, and they entertained notions of a long-conserved developmental pathway for these fruits, or perhaps the differences between capsular and baccate fruits were so slight that transitions between the two might be relatively simple.
The optimisation of nuclear endosperm to this node of the tree (Tobe & Kadokawa 2010) may well not hold up; variation in the patterns of endosperm development is great in many orders.
Plant-Animal Interactions. Larvae, and sometimes also adults, of the Chrysomelidae-Criocerinae are scattered as herbivores on plants throughout this clade, being perhaps especially common on commelinids (e.g. Schmitt 1988; Gómez-Zurita et al. 2007).
Genes & Genomes. The ORSAγ duplication event (Landis et al. 2018), ca 137.5 Ma, is to be placed here; c.f. another(?) duplication event two nodes up.
[DIOSCOREALES + PANDANALES]: root hairs from unmodified rhizodermal cells, exodermal cells not dimorphic; outer integument 2(-3) cells across; genome size <10 pg ([C].
Age. The divergence of these two orders is dated to about 131.4 Ma by Tank et al. (2015: Table S2: stem age of Dioscoreaceae) and similar in Alcantara et al. (2018: see spread), ca 134.4 and 119.6 Ma by Magallón and Castillo (2009); estimates were ca 124 Ma in Givnish et al. (2018a), (130-)121(-119) Ma in Merckx et al. (2008a), ca 110.5 Ma in Magallón et al. (2015), (129-)119, 116(-110) Ma in Hertweck et al. (2015), (131.4-)117(-102.4) Ma in Eguchi and Tamura (2016), and (124.5-)104(-78) Ma in Givnish et al. (2016b). 123-96 Ma is the spread in Mennes et al. (2013, 2015), and (117-)106, 84(-70) Ma by Soto Gomes et al. (2020). Although Janssen and Bremer (2004) showed Dioscoreales and Pandanales as successive branches in the tree, they gave stem ages for both of ca 124 Ma.
Evolution: Genes & Genomes. This clade is characterized by the DIVIβ duplication event, some 131 Ma (Landis et al. 2018).
Leitch and Leitch (2013) record small genomes in this clade, but sampling is poor.
Phylogeny. For discussion on the relationships of Dioscoreales and Pandanales, see the Petrosaviales page.
DIOSCOREALES Martius - Main Tree.
Steroidal saponins +; vascular bundles in rings; vessels also in stem and leaf; flowers or inflorescence with glandular hairs; styles free early in ontogeny, branches well developed, adaxially grooved; T persistent in fruit; ovules many/carpel; endotegmen tanniniferous; embryo at most short; genome size usu. 0.4-6.8 pg [1C]. - ?5 families, 21 genera, 900 species.
Includes Burmanniaceae, Dioscoreaceae, Nartheciaceae, Taccaceae, Thismiaceae.
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. Crown group Dioscoreales are dated to ca 123 Ma (Janssen & Bremer 2004); estimates were ca 119 Ma in Givnish et al. (2018a), (126-)116(-113) Ma in Merckx et al. (2008a), (120-)116(-111) Ma in Merckx et al. (2010a; see also Viruel et al. 2015), 116-85 Ma in Mennes et al. (2013, 2015), (123-)115, 110(-104) Ma in Hertweck et al. (2015) and (120.2-)95.2(-61.4) Ma in Eguchi and Tamura (2016), about 95.2 Ma in Magallón et al. (2015) and (115-)76(-35) Ma in Givnish et al. 2016b)
WARNING. Since the basic phylogenetic structure of Dioscoreales is unclear, ages for clades in the literature need to be read in the context of the phylogenies on which they were based.
Chemistry, Morphology, etc.. For morphology and anatomy, see Ayensu (1972), for seed coat, see Bouman (1995) and Oganezova (2000b), for pollen morphology and development see Caddick et al. (1998) and Schols et al. (2005a: Nartheciaceae and Dioscoreaceae). For much information on morphology in the order, see Caddick et al. (2000a: floral morphology and development, 2000b: general); prolongations of the anther connective are homoplasious.
Phylogeny. Nartheciaceae are rather consistently placed with the other Dioscoreales, albeit sometimes with only moderate support (e.g. Chase et al. 2000a; Caddick et al. 2002a; Tamura et al. 2004a: 97% bootstrap, Nartheciaceae well sampled, but otherwise only Dioscorea, Tacca and three Pandanales; Janssen & Bremer 2004: one gene, very good sampling; Chase et al. 2006; Givnish et al. 2006: see also Goldblatt 1995). However, Davis et al. (2004) found them to associate with Pandanales, although support was weak (<70%) and they lack the 6bp atpA deletion of many members of that clade, while in mitochondrial genome analyses Burmannia was sister to [Pandanales + Narthecium] yet Thismia was in Dioscoreales (G. Petersen et al. 2006b).
Evidence suggests that the mycoheterotrophic members of Dioscoreales do not come close to forming a clade. Merckx et al. (2006: good sampling, no outgroup to Dioscoreales), using both mitochondrial and nuclear genes, found substantially different relationships within Dioscoreales from those depicted in the tree given by Caddick et al. (2002a: see also /APweb/ version 6 [November] and earlier, classification as in Caddick et al. 2002b). However, as Merckx et al. (2006) note, the relationships found by Caddick et al. (2002a) were dominated by chloroplast data, and since Burmanniaceae s.l. are largely mycoheterotrophic they have much diverged plastid sequences. Indeed, Geomitra, apparently Thismiaceae without any doubt, nevertheless came out with Burmanniaceae in some analyses (Caddick et al. 2002a). Yokoyama et al. (2007: support slight) found the relationships [Burmanniaceae [Dioscoreaceae [Taccaceae + Thismiaceae]]]. The situation is yet more complex, since Merckx and Bidartondo (2008) and Merckx et al. (2009a) suggest that Thismiaceae s. str. may be paraphyletic, Afrothismia being sister to [Taccaceae + rest of Thismiaceae] (but c.f. Yokoyama et al. 2007). Merckx et al. (2010a; see also Merckx & Smets 2014) confirmed the paraphyly of Thismiaceae, and also suggested that Trichopus could be sister to [Taccaceae + Thismiaceae]; Stenomeris was well embedded in Dioscorea. However, Hertweck et al. (2015) found Burmannia and Thismia to be sister taxa with very long branches, but sampling was poor since this was not the main point of their paper. In other studies where broader relationships were also not the point, Viruel et al. (2015) and Z.-D. Chen et al. (2016) found the relationships [Burmanniaceae [Taccaceae + Dioscoreaceae s.l.]]. In a three-plastid gene analysis, Lam et al. (2016) found that in gene and codon position unpartitioned analyses Thismiaceae tended to wander (sister to Petrosaviaceae), but in other analyses they were included in Dioscoreales, while when photosynthetic Dioscoreales alone were included, relationships were [Burmanniaceae [Nartheciaceae [Dioscoreaceae [Taccaceae + Trichopodaceae]]]]. Relationships found by Lam et al. (2018) are [Nartheciaceae [Burmanniaceae [Dioscoreaceae [Taccaceae + Thismiaceae]]]], although sampling was slight, and similar relationships were also recovered by Givnish et al. (2018b) although support for the position of Thismia (one species sampled) was rather weak and Afrothismia was not included. Finally, Shepeleva et al. (2020) found the relationships Dioscorea, [Burmannia + Afrothismia], [Tacca + Thismiaceae].
Classification. The classification below follows that suggested by Merckx et al. (2006), although for relationships within Dioscoreaceae, see Caddick et al. (2002a, b). However, if the tree suggested by Mercx et al. (2010a) holds up, Afrothismia and Trichopodaceae will have to be split off, or... Trias-Blasi et al. (2015) recognised a Burmanniaceae that includes Thismiaceae and a Dioscoreaceae that includes Taccaceae, but, as they noted, phylogenetic relationships needed attention.
Synonymy: Burmanniales Martius, Nartheciales Reveal & Zomlefer, Taccales Dumortier, Tamales Dumortier
NARTHECIACEAE Bjurzon - Back to Dioscoreales
(Plants Al accumulators - Aletris); chelidonic acid +, flavonols 0; air spaces in root cortex; fibers intermixed in phloem; (sieve tube plastids with large polygonal crystal - Narthecium); endodermal cells evenly thickened [distribution around here?]; raphides 0, usu. druses +, but prismatic crystals in bundle sheath; cuticular wax with parallel platelets; leaves spiral (two-ranked, ventralized isobifacial [oriented edge on to the stem]); bracteole 0 (+); (odd T of outer whorl adaxial); T free to connate; A adnate basally; pollen orbicules with a circular perforation; septal nectaries +/0; G to half inferior, partly ascidiate, fusion congenital to postgenital, compitum +/0, (stylulus long), (with 3 canals); ovules ana-campylotropous, integuments lack cuticle [check], integumentary obturator + [Aletris]; antipodal cells not multinucleate; seeds obliquely stacked, (with appendages), shape various; tegmen flattened, persistent, or testa cells flattened, (esp. outer anticlinal walls of exotegmen thickened - Lophiola); endosperm helobial, [how much?, walls?]; embryo size?; n = (12) 13 (21, 22), x =14 (?13, ?7), chromosomes 0.7-1.4 µm long, nuclear genome [1 C] (0.0.31-)1.164(-43.279) pg; cotyledon bifacial or not, ?collar rhizoids.
4-5[list]/41: Aletris (30). Interrupted N. temperate, Venezuela and Guiana and scattered in W. Malesia (map: from Hultén & Fries 1986; Jessop 1979; Fl. China 24. 2000; Fl. N. Am. 26: 2002). Photo: Inflorescence.
Age. Crown-group Nartheciaceae are dated to ca 76 Ma (Janssen & Bremer 2004) and (92-)41(-10)Ma by Merckx et al. (2010a).
Evolution: Divergence & Distribution. For such a small family, variation in floral morphology and development is very considerable, and Tobe et al. (2018; see also Remizova et al. 2008a) have put it in a phylogenetic context. Although genera like Lophiola and Narthecium have two-ranked and isobifacial leaves, such leaves are unlikely to be an apomorphy for the family.
Chemistry, Morphology, etc.. Metanarthecium may have an abaxial prophylls, in Lophiola they can be lateral, while in Narthecium it is adaxial.
The ovary may be secondarily superior in Metanarthecium and Narthecium (Remizowa et al. 2008a; Fuse et al. 2012; Tobe et al. 2018). There are reports that the ovules of Narthecium may be unitegmic (Remizowa et al. 2006a).
Additional information: For endodermal thickening, see Zomlefer (1997a), for leaf anatomy, see Luque Arias et al. (2006), for pedicel anatomy, see Gatin (1920), for inflorescence and flower development, see Remizowa et al. (2006a, b), for pollen morphology, see Merckx et al. (2008b), for embryology, see Ono (1929) and Cave (1968), for seed coat, see Takhtajan (1985: as Hypoxidaceae).
Phylogeny. Aletris, with its spiral and bifacial leaves, was sister to the three other genera examined (Tamura et al. 2004a), with Metanarthecium having weak support as sister to the rest of the family in Fuse et al. (2012). Isidrogalvia (Alismatales-Tofieldiaceae!) sometimes ends up around here, but this is because of contamination or misidentification (Tamura et al. (2004b; c.f. Azuma & Tobe 2011; Luo et al. 2016).
Previous Relationships. The relationships of Nartheciaceae, with their rather ordinary-looking monocot flowers, have long been problematic. Cronquist (1981) did not even mention them, but they would probably have been included in his highly heterogeneous Liliaceae, Dahlgren et al. (1985; see also Takhtajan 1997) placed them - along with representatives of Tofieldiaceae (here Alismatales) and Petrosaviaceae (Petrosaviales) - in Melianthaceae (Liliales), while Tamura (1998) placed them in Petrosaviaceae, along with genera here included in Tofieldiaceae. Lophiola is included in Haemodoraceae in the Flora of North America, although with some hesitation.
Synonymy: Lophiolaceae Nakai
[[Taccaceae + Thismiaceae] [Burmanniaceae + Dioscoreaceae]]: plants geophytes; stem with endodermis; T tube well developed, broad, [?vasculature]; A incurved [± pendulous, anthers ending up extrorse], inserted towards the mid/upper part of the tepal tube, usu. close to stigma; ovary inferior, style short; exo- and endotesta tanniniferous.
Age. Divergence times at this node are (118-)109(-98) Ma (Merckx et al. 2010a: Burmanniaceae sister to rest); other estimates are (112-)96, 93(-87) Ma (Wikström et al. 2001), ca 115 and 127 Ma (Magallón & Castillo 2009) and (111-)92, 83(-68) Ma (Bell et al. 2010). The node is dated to ca 116 Ma by Janssen and Bremer (2004), (122.5-)104(-86.4)Ma by Couto et al. (2018) and ca 79.9 Ma by Magallón et al. (2015). The age of a clade including Afrothismia, Thismiaceae, and Trichopodaceae is some (109-)95(-79) Ma (Merckx et al. 2010a). Ages should be carefully checked here, because sampling in several studies is poor and relationships unclear.
Evolution: Divergence & Distribution. Mycoheterotrophy has evolved at least three, perhaps six or ten times in this clade (Merckx et al. 2006, 2008a, 2009, 2010a), but the exact number depends very much on relationships within the group. Glomeromycota are the fungi involved (Franke et al. 2006). The mycoheterotrophic habit may have evolved some time before the beginning of the Palaeocene (83-)63(-45) Ma when Afrothismia gesnerioides diverged from the rest of the Taccaceae-Thismiaceae clade (Merckx et al. 2010a).
The early evolution of mycoheterotrophism here and elsewhere in this clade (in Burmanniaceae) raises the issue of when more or less closed tropical rainforest developed (Merckx et al. 2008a, 2010a) - see also the parasitic Rafflesiaceae
Endress (2011a) thought that the inferior ovary in Dioscoreales might be a key innovation.
Pollination Biology. Flowers with incurved stamens, more or less expanded stigma and sometimes also features of the corolla can combine to form complex flowers with the anthers very much in the interior in small chambers and opening towards the corolla tube - such flowers are found in Tacca, Thismia nand some Dioscoreaceae. Recent findings on pollination in Tacca (see below) suggest how the system might function.
Chemistry, Morphology, etc.. Cell walls in the endosperm are often thick, but are usually not pitted. The embryos of Taccaceae and Diocoreaceae are similar in their more or less lateral cotyledon (Solms Laubach 1878).
Phylogeny. Remember, relationships in this clade remain unclear!
[Taccaceae + Thismiaceae]: septal nectaries 0; placentation parietal, stigmas broad.
Age. The age of this node is some (92-)79(-68) Ma (Merckx et al. 2010a) or ca 11.5 Ma (Givnish et al. 2018b), neither including Afrothismia.
TACCACEAE Dumortier, nom. cons. - Back to Dioscoreales
Plant with stem tubers or rhizomes; (velamen +); secondary thickening +[?]; vessels 0; hairs with multicellular stalk row, a head, and then another cell row; petiole bundles in ring; leaves basal, blade ± deeply pinnately or palmately divided to entire, fine venation reticulate, petiole +, base somewhat sheathing; inflorescence scapose, umbellate, of groups of cincinni, inflorescence bracts petal-like, floral bracts long, filiform, among the flowers; flowers medium in size; T with median member of outer whorl adaxial, whorls weakly differentiated, tube short; A adnate to P at base, connective broad, not prolonged, forming a hood enclosing anther; middle layer of anther wall from outer secondary parietal cells [dicot type]; G opposite C/inner T, stylar canal with secretion, stigma ± petal- or mushroom-like, (lobes bilobed); nucellar cells laterally anticlinally expanded, nucellar cap 0; megaspore mother cells several; fruit a berry (capsule); seed ribbed; (endotesta crystalliferous), exotegmen ± thick-walled and elongated, esp. radially; embryo short to minute, cotyledon ± lateral; n = 15, x = ?; cotyledon ?bifacial, sheath lobed.
1[list]/12. Pantropical, esp. Malesian-Pacific (map: from Drenth 1976; Australia's Virtual Herbarium, i.2015). [Photos - Collection.]
Age. Crown-group Taccaceae are (60-)35(-15) Ma (Merckx et al. 2010a).
Evolution: Divergence & Distribution. For the fossil record of Tacca, see Ran (2017); the oldest fossils, seeds, are from Europe at the Eocene-Oligocene boundary ca 33.9 Ma.
Pollination Biology. The dark purple flowers of most species of Tacca and the long, dangling bracts suggest some sort of fly pollination. The inflorescence as a whole can be strongly monosymmetric, as in Tacca integrifolia, where two large and conspicuous white inflorescence bracts are held above the dark purple flowers and less conspicuous lower inflorescence bract and the whitish dangling filiform bracts. The broad stamens of T. cristata are incurved and held horizontally in the mouth of the flower and abut the stigma, and they are then incurved another 1800, the anthers ultimately facing upwards in a little pollination chamber formed largely by the stamens alone. Although a variety of insects may visit the flower, pollination is likely to be carried out by female biting midges (Ceratopogonidae: Forcipomyia, Culicoides: Lim & Raguso 2017; Chua et al. 2020). The midges visit the flowers on the first day of anthesis when the flowers are held vertically; on the second day they become pendulous.
Chemistry, Morphology, etc.. Tacca lacks the distinctive vasculature of Dioscoreaceae, in which it used to be included. It is unclear if the midrib is distinct or multistranded (Inamadar et al. 1983).
The flowers are drawn with the odd member of the outer whorl in the adaxial position by Ronse de Craene (2010). The cells around the raphal bundle can be thin-walled; perhaps they are attractive to animals?
For general information, see Limpricht (1928) and Kubitzki (1998b), for vegetative anatomy, including that of the young plant, see Queva (1894), for xylem, see Carlquist (2012a), and for pollen, see Tarasevich (2019: Convolvulaceae = Convallariaceae?).
THISMIACEAE J. Agardh nom. cons. and sensu stricto - Back to Dioscoreales
Plants echlorophyllous, mycoheterotrophic, associated with glomeromycotes, not rhizomatous; saponins?; roots coralloid, vermiform or tuberous, stele not medullated [?all]; root hairs 0; stomata 0; leaves reduced to scales, (borne immediately below the flower); flowers single, or inflorescences (branched), cymose [Haplothismia]; flowers with 3 or so bracts at the base, (monosymmetric); T with single trace, (spreading), whorls (not differentiated - Oxygyne, Haplothismia), or inner T whorl (apex) long, linear/connate and the whole like a mitre, (apex prolonged - "pillar"), outer T lobes then small or even 0/peltate and fungiform, annulus or ring of short projections at mouth of tube + (0 - Haplothismia), T tube well developed and expanded below attachment of A at apex; A (3, opposite outer T, Oxygyne), (± connate = "stamen connectives fused into a stamen tube"), incurved, (interstaminal lobes +), connective broad, with (paired apical ["wing-like appendages"] and basal projections) and (interstaminal glands), filaments variously ornamented (not); tapetal cells uninucleate; endothecial cells with U thickenings (not); pollen grains (tricellular), porate; placentae as separate columns, often ± free from walls, ± apical, or parietal, style short, connate at least early in ontogeny, branches slightly dorsi-ventrally flattened, (undivided), stigmas capitate to elongated (with round appendages - Oxygyne); ovules lacking parietal tissue, funicles long [?all]; (embryo sac bisporic); stem/pedicel elongating considerably in fruit, T basally circumscissile (not - Haplothismia), fruit irregularly dehiscent, ± cup-like; seeds dust-like, testal cells ± spiral, tegmic cells compressed; endosperm helobial, basal chamber bicellular, thick-walled, with starch when young, not persisting; embryo undifferentiated; ?seedling; n = 6-9, 11-14, x = ?, chromosomes 1-4 µm long.
5 [list]/95: Thismia (>80). Widely scattered, mostly (sub)tropical. Map: from Jonker (1938), van Steenis and van Balgooy (1966), Maas et al. (1986), Larsen and Averyanov (2007), Dauby et al. (2008), Ho et al. (2010: n.b. Thismiaceae s. str. in Africa only from Cameroon and Central African Republic - Oxygyne) and Cheek et al. (2018b). [Photo - Thismia.]
Age. The age of crown Thismiaceae is some (85-)68(-49) Ma (Merckx et al. 2010a: excl. Afrothismia).
Evolution: Divergence & Distribution. Shepeleva et al. (2020) looked at the distribution of a number of floral features on their tree of Old World Thismia and found extensive homoplasy, thus zygomorphy originated three times there alone. Haplothismia is different in a number of respects from the other genera.
Thismiaceae are notably diverse in submontane forests around Rio de Janeiro (Sainge et al. 2017), although a continuous stream of new species is being described from the South-East Asia-West Malesian area.
The immediate relatives of Thismia americana, collected near Chicago just before W.W. 1, not seen after 1916, and now apparently extinct, were thought to be Antipodean, a remarkable disjunction (Thorne 1972, 1992). However, the recently-described Thismia huangi, from Taiwan, is also morphologically similar to these Antipodean species, although in molecular analyses they are not so close (Merckx & Smets 2014); either way, biogeographic scenarios need to be rethought. Oxygyne is known from Japan and Cameroon (e.g. Cheek et al. 2018b).
Pollination Biology & Seed Dispersal. Self-pollination or apomixis may be common (e.g. Maas et al. 1986), although (sapro)myophily is a likely means of cross pollination (Woodward et al. 2007; Mar & Saunders 2015). There are no nectaries (Caddick et al. 2000).
Splash-cup seed dispersal is likely in at least some taxa (e.g. Mar & Saunders 2015).
Bacterial/Fungal Associations. Glomeromycote fungi form quite specific associations with species of Thismiaceae (Merckx et al. 2012), however, the fungi (Rhizophagus spp.) are quite widely distributed (Merckx et al. 2017) and the often rather localized distributions of the plant do not reflect any restrictions caused by fungal distributions. Mycorrhizae are of the Paris type (Imhof et al. 2013). In a study of Antipodean Thismia, Gomes et al. (2016) found that the specificity of their associations with local glomeromycotes was greater than that of AM plants from the same localities, but even the latter were associated with only a subset of the fungi.
Genes & Genomes. See Tsukaya et al. (2007) for chromosome number and size.
The plastome of Thismia tentaculata is very much reduced (Barrett & Kennedy 2018), as might be expected for a mycoheterotrophic species, but its IR is not syntenic with that of the two other Dioscoreales examined, suggesting that the original IR may have been lost and then reassembled de novo (Lim et al. 2016: see also Erodium-Geraniaceae).
Chemistry, Morphology, etc.. The stems may be endogenous in origin (Pfeiffer 1914). The underground parts of Tiputinia are quite massive, and the roots in general are thick.
The inflorescence morphology of species of Thismia described by Larsen and Averyanov (2007) is not easy to understand. Although the androecium is incurved in all species, details of how this incurvature is achieved vary considerably (Cheek et al. 2018b) and the morphology of the stamens, with variously expanded and ornamented connectives, varies considerably (Sochor et al. 2018). Cheek et al. (2018b) specifically note that the three stamens of Oxygyne are opposite the outer tepals, that is, they differ in position from the three stamens in Burmanniaceae, but from Maas-van de Kamer (1998) one would assume thay they were opposite the inner tepals; Jonker (1938), etc., do not, or do not clearly, state their position. Shepeleva et al. (2020: character 9) noted that in those species of Thismia they examined that had only three stamens, those stamens were opposite the inner tepals.
Additional information is taken from Dahlgren et al. (1985), Rübsamen (1986), Maas et al. (1986), Maas-van der Kamer (1999), Merckx et al. (2013a) and Cheek et al. (2018b: Oxygyne), all general, Imhof et al. (2013: roots, mycorrhizae), and Waterman et al. (2013: pollination).
Phylogeny. For the delimitation of Thismiaceae, see above. Relationships within Thismiaceae s. str. are unclear, although Thismia itself may be paraphyletic. Indeed, Shepeleva et al. (2020: 41 Thismia species, 2 nuclear and 1 mitochondrial genes) found Old World Thismia to be monophyletic, the one New World species they sampled was in the clade [Haplothismia [T. panamensis + Tiputina]] sister to the Old World species. Within these latter there were five well supported (1.00 p.p.) clades and six unplaced species; the sections recognized by Kumar et al. (2017) were largely para- or polyphyletic. Oxygyne (as the Japanese species, O. shinzatoi) may be sister to the rest of the family (Yokoyama et al. 2007: 18S rDNA, parsimony; Merckx et al. 2009a; Merckx & Smets 2014; Shepeleva et al. 2020) or embedded in the family, as was Afrothismia (Yokoyama et al. 2007: maximum likelihood).
Classification. Kumar et al. (2017) provide an infrageneric classification for Thismia, but this has not held up well. Shepeleva et al. (2020) suggest how species groupings - with associated characters - may develop in Thismia, and note that generic limits in New World taxa need attention.
Botanical Trivia. Thismia must currently have the fastest relative growth rate in terms of numbers of new species being described of any genus with more than 30 species or so.
Plants echlorophyllous, mycoheterotrophic, associated with glomeromycotes, usu. epiterrestrial, rhizomatous, with aggregations of small tuberous roots along its length [= basally swollen roots each with a terminal rootlet, "tubers"]; inflorescence cymose, a cincinnus; flowers with basal bract, monosymmetric, plane of symmetry oblique; T whorls not differentiated, (with lateral spreading or basal retrorse projections), tube bent/(straight, with mushroom-like corona), usually divided into two chambers by an annulus or constriction; A inserted in the middle of the tube, incurved, connective expanded, apical part ± adnate to the stigma; pollen porate; stigma capitate-funneliform, (6-lobed); placentation basal, with swollen sterile basal axile column; fruit circumscissile, T tube also basally circumscissile; seeds presented on central column, dust-like; n = ?; ?seedling.
1 [list]/20. West and East Africa (Map above: Africa; see Sainge et al. 2017).
Age. The age of crown-group Afrothismia is some (83-)63(-45) Ma (Merckx et al. 2010a).
Evolution: Divergence & Distribution. Merckx and Bidartondo (2008) described what they called delayed co-speciation (the delay is 65-170 My!) of a group of Afrothismia on/with their Glomus fungal symbiont, which seems a little odd (see also Winkler & Mitter 2008).
Sainge et al. (2017) discuss the habitat preferences of Afrothisma and suggest that it could be quite widespread in wet, calcium poor, closed submontane rainforests in Africa.
Bacterial/Fungal Associations. For details of the complex fungal colonization pattern in the genus, see Imhof (1999b) and Imhof et al. (2013); details of the morphology of the fungus depends on the tissues in which it is growing.
Chemistry, Morphology, etc.. Two adjacent tepals may be much longer than the other four; see also the floral diagram in Maas-van de Kamer (2003). The seedling is also not easily describable (Imhof & Sainge 2008).
Some information is taken from Cheek (2003b), Maas-van de Kamer (2003), Sainge et al. (2013) and Merckx et al. (2013a), all general, Imhof et al. (2013: esp. roots, mycorrhizae), and Waterman et al. (2013: pollination).
Classification. Most Thismiaceae s.l. are small to minute plants with small and inconspicuous flowers and are not often found in flower - and judging by the continuous stream of new species and even genera that are being described, extremely poorly known on even an alpha taxonomic level (see Franke 2007: comments on distributions).
[Burmanniaceae + Dioscoreaceae]: fruit winged, dehiscing laterally.
Age. Note that Janssen and Bremer (2004) included Geomitra (Thismiaceae) in their Burmanniaceae, so ages are compromised; ca 72.8 Ma is the age of this node in Magallón et al. (2015).
BURMANNIACEAE Blume, nom. cons. - Back to Dioscoreales
Plants often echlorophyllous, mycoheterotrophic, associated with glomeromycotes; roots ± fleshy, radiating, or root tubers +, (cortex disintegrating); saponins?; (root hairs 0); root stele di- to pentarch, (not medullated); (stem with vascular bundles in a single ring); raphides 0; (stomata 0), (cuticular waxes as platelets transversely arranged in parallel series); leaves (two-ranked), usu. reduced to scales, (scales peltate); inflorescence (1-flowered), cymose; bracteoles + (lateral - Burmannia); (flowers monosymmetric); T (moderately large), valvate, outer larger (hardly), (3-lobed), (with marginal wings), enclosing the inner, (inner 0), T tube well developed and expanded below attachment of A; A 3, opposite inner T, connective broad, oten with up to 4 short apical and basal appendages, thecae widely separate, lateral, transversely dehiscent; endothecial cels thickened/not; pollen often tricellular, monoporate, sulcate or inaperturate, smooth [psilate]; anthers ± associated with style; (nectary on top of ovary), placentation ± parietal, (axile - Burmannia), (paired nectar glands [modified septal nectaries] at apex of each placenta), style long, stigmas ± capitate, (with paired short to long and filiform apical processes); ovules many/carpel, (outer integument growing far beyond micropyle after fertilization, funicle long), parietal tissue none, chalazal tissue quite conspicuous, persistent; (antipodal cells persist - Gymnosiphon); fruit transversely (Burmannia) or septicidally and/or loculicidally dehiscent (indehiscent/fruit horizontal, dehiscent down upper side only), T persistent, (circumscissile at the middle of the tube); seeds dust-like; testal cells ± spiral, ± elongated, tegmic cells compressed, (tanniniferous); endosperm usu. helobial, basal chamber uni--multinucleate (multicellular - Hexapteralla), thick-walled, with starch when young, ± 0 when mature, chalazal endosperm semi-haustorial?; embryo undifferentiated; ?seedling; n = 6 (7) 8, 12, 16, ... 88, much and high polyploidy, x = 16, chromosomes 0.7-5.9 µm long, nuclear genome [1 C] (0.025-)1.098(-48.078) pg.
9 [list]/97: Burmannia (63), Gymnosiphon (32). Largely tropical, esp. America and the Guianan area (map: from Jonker 1938; Maas et al. 1986). [Photo - Flower, Campylosiphon, Hexapterella.]
Age. Crown-group Burmanniaceae are dated to ca 93 Ma (Janssen & Bremer 2004: three genera sampled); dates in Merckx et al. (2008a), at 96.4 Ma, are similar, while Merckx et al. (2010a) suggests somewhat younger ages of (99-)75(-52) Ma.
Evolution: Divergence & Distribution. The rather wide geographical range of the family is thought to have been achieved largely by migration. Diversification rates were notably high in the Cretaceous and again in the Eocene (Merckx et al. 2008a).
Ecology & Physiology. There have been perhaps eight losses of chlorophyll in Burmanniaceae, assuming that loss is irreversible - if Burmannia, the only genus with some autotrophic species, is indeed well embedded in the family (Merckx et al. 2006, 2008a, but c.f. Merckx et al. 2010a; see also Lam et al. 2016). At least some of the chlorophyllous species of Burmannia can grow well under high light conditions without any association with arbuscular mycorrhizal glomeromycotes (Merckx et al. 2010b) while others like B. coelestis are partly mycoheterotrophic (Bolin et al. 2016). For mycoheterotrophism in general, see Hynson et al. (2013).
Bacterial/Fungal Associations. Glomeromycote fungi are involved in mycoheterotrophy (Hynson & Bruns 2010; Imhof et al. 2013).
Genes & Genomes. The chloroplast genome of the mycoheterotrophic Burmannia itoana has undergone extensive gene loss, being a little more than a quarter of the size of the genome of B. disticha, and there have also been four inversions and two translocations; the sequence of loss of some of the genes is a little unusual (X. Li et al. 2019). See also Aoyama et al. (2014 and references) for chromosome numbers.
Chemistry, Morphology, etc.. Although roots of Burmanniaceae are often described as lacking root hairs (e.g. Maas-van der Kamer 1998), as might befit their close association with fungi, root hairs have been shown in Burmannia (von Guttenberg 1968). In echlorophyllous taxa vessels may be restricted to the roots, in others there are vessels in the leaves.
Rübsamen (in Maas et al. 1986) emphasizes the great variety of nectaries in the family. In a floral diagram (Eichler 1874) the stigmas are shown as being commissural.
Information is taken from Jonker (1938), Dahlgren et al. (1985), Rübsamen (1986), Maas et al. (1986), Maas-van der Kamer (1998) and Merckx et al. (2013a), all general, Imhof et al. (2013: roots, mycorrhizae), Waterman et al. (2013: pollination), and Johow (1889 and references: anatomy, embryology).
Phylogeny. Merckx et al. (2008a) provide a detailed phylogeny of the family that has quite good support. Relationships are [[Campylosiphon + Burmannia reducta (mycoheterotrophic)] [Dictyostega [[Hexapterella + Gymnosiphon] [Aptera + Burmannia]]]]. However, in a subsequent analysis Burmannia and [Campylosiphon + Burmannia reducta] were successively sister to the rest of the clade,
DIOSCOREACEAE R. Brown, nom. cons. - Back to Dioscoreales
Plant rhizomatous; lianes or vines, climbing by twining; (saponins 0), norditerpenes, flavonols +; in the stem small common [proceeding to the leaf] and larger cauline bundles alternating, vascular bundles in two rings, outer ring ± V-shaped, inner ± elliptic, with 1-5 separate phloem units, phloem internal to metaxylem, xylem and phloem glomeruli at nodes joining vascular bundles and interrupting general course of vascular tissue; vessel elements with scalariform perforation plates in petiole but not blade; sieve tubes large, plates with very oblique end walls and several sieve fields; epicuticular wax crystalloids +. not oriented, stomatal ontogeny irregular; hairs glandular; (prophylls lateral); leaves ?spiral, with pseudopetiole and blade, blade cordate, venation palmate, fine venation reticulate, (vein endings free), vernation conduplicate, petiole pulvinate at both ends, leaf base not sheathing; inflorescences axillary; microsporogenesis simultaneous [tetrads tetrahedral]; carpels plicate, compitum +, stigma wet; ovules with bi(endo-)stomal micropyle, (outer integument ³3 cells across); seeds winged; endotestal cells elongated, thick-walled, with crystals, exotegmen thickened; embryo broad, cotyledon ± lateral; x = 8 (?7, ?14), nuclear genome [1 C] = (0.022-)0.093(-38.176) pg.
4[list]/870. Largely tropical. Three groups below.
Age. Crown-group Dioscoreaceae are dated to ca 80 Ma (Janssen & Bremer 2004), some (54-)26(-9) Ma (Merckx et al. 2010a: c.f. topology), or (91.4-)77.2(-63.7) Ma (Viruel et al. 2015: Tri Ste Dio).
1. Stenomeris Planchon
Stem annual, left twining, underground stem thickened; ?chemistry; tanniniferous cells 0; petiole bundles in arc; hairs with two-celled gland heads; ?petiole pulvini?; T tube well developed [= torus] and expanded below attachment of A; anther connective broad, prolonged apically, adnate to stigmatic head, filaments flattened; microsporocytes markedly elongated; tectum (undulate) perforate; G half inferior, style bowling-pin shaped, stigmas 3, bifid; ovules many/carpel; fruit elongated, dehiscence loculicidal; seeds distally asymmetrically winged; seed coat with phlobaphene, tegmen collapsed; endosperm walls thin; n = ?; seedling?
1/2. Northern West Malesia, not Java and islands east (Map: from Caddick & Wilkin 1998).
Age. The age of the [Stenomeris + Dioscorea] clade is (85.9-)71.4(-57.7) Ma (Viruel et al. (2015).
Synonymy: Stenomeridaceae J. Agardh
[[Trichopus + + Avetra] Dioscorea]: anthers ± erect, adnate to base of the tepal tube; pollen with orbicules; ovules (1) 2/carpel, superposed, hypostase +; endosperm walls thickened.
2. Trichopus + Avetra
Stems long-lived; endodermoid layer fibrous; pseudopetiole with bundles in arc; inflorescence fasciculate/short racemose; stamens concave, surrounding style, anther connective (very) broad, apical prolongations connivent over stigma; microsporocytes large, somewhat elongated; pollen sexine spinulate; nectary 0; fruit ± indehiscent; seeds not winged; endotesta not thickened, crystals ?0, exotegmic cells elongated, with reticulate thickenings; endosperm ruminate, walls not pitted, embryo minute; n = 14, chromosomes 1.5-2.7 µm long; germination?
2/2. Madagascar, Peninsula India, Sri Lanka, Peninsula Malaysia (Map: from ).
2A. Trichopus Gaertner
Stem erect, not twining, with 1 leaf; flavones +; cauline vascular bundles in one ring, xylem and phloem glomeruli 0; large sieve tubes 0, plastids lacking starch grains; pseudopetiole pulvini 0; glandular hairs with transversely elongated cells in series; bracts 2-ranked; anther connective very broad, ridged adaxially between thecae; pollen sulcate; stigma lobes 6, spreading-recurved; parietal tissue none, nucellar cap 0, lateral nucellar cells +, obturator +; fruit keeled, slightly fleshy; seed 1, minutely hairy.
1/1: Trichopus zeylanicus. Southern Peninsula India, Sri Lanka, Peninsula Malaysia
Synonymy: Trichopodaceae Hutchinson, nom. cons.
2B. Avetra H. Perrier
Stem right twining; glandular hairs 0; pseudopetiole with basal pulvinus; microsporogenesis successive; pollen 4-5-pantoporate; stigmas lobes 3, erect, longitudinally bilobed; ?embryology; fruit winged; seeds -6.
1/1: Avetra sempervirens. Madagascar.
Synonymy: Avetraceae Takhtajan
3. Dioscorea L.
Stem annual, left (right) twining, (not climbing); spirostanol steroidal saponins +, chelidonic acid, (mannans) +; (root thorns +); (velamen +); (monocot secondary thickening +); sieve tube plastids with protein crystals and starch grains; nodes 3:3, mucilage cells +, tanniniferous cells +; petiole bundles in ring (not D. hemicrypta); (stem tubers +); stomata oriented randomly, (morphology odd/actinocytic); gland heads many-celled; leaves two-ranked (opposite), (palmately lobed/compound), fine venation reticulate, (midrib +), vernation flat to curved or conduplicate, petiole pulvinate at both ends, bifacial [?all], (base with paired evascular processes); serial axillary buds common; plant dioecious, (monoecious), inflorescences two or more together, (bracteoles lateral); flowers small; T free or connate, with a single trace; staminate flowers: A (1)/(3 [opposite outer T] (+ 3 staminodes)), (3, 6 connate); pollen sexine perforate (to perforate-reticulate), (striate), (rugulate); pistillode +; carpelate flowers: staminodes +; loculi filled with secretion [?level], stylar canal with secretion, stigma bilobed or not; ovules 2/carpel, with outer integument 4-5 cells across, nucellar cap ca 3 cells across, supra-chalazalal tissue ± massive, hypostase +; seeds 1-6, variously winged/not; testa (multi-layered), (with much phlobaphene), exotegmen sclerotic [with branched protrusions of the cell walls], endotesta crystaliferous, exotegmen (not thick-walled if seeds proximally winged), endotegmen tanniniferous; endosperm usu. (very) thick-walled, embryo small to medium; n = (7, 8), 9, 10, 12, (up to 14-ploid), chromosomes 0.3-2.9 µm long; cotyledon flattened and photosynthetic or not, second leaf a scale leaf.
1/350-630-?800: 2 subgenera below. Largely tropical, also warm temperate, esp. seasonal. Map: see Meusel et al. (1965) Fl. N. Am. vol. 26 (2002) and FloraBase (2004). [Photo - Inflorescence, Flower, Fruits.]
Age. Crown-group Dioscorea is dated to (49.1-)48.3(-47.6) Ma, in the Eocene (Viruel et al. 2015) or rather earlier, (77-)63.7(-52.6) Ma (Couto et al. 2018).
The fossil Dioscorea eocenicus was recently described from Early Eocene deposits 57-54 m.y.o. from northwest India but then at the Equator (Mehrotra & Shukla 2018).
3A. Subg. Dioscorea
Plant rhizomatous; pollen monosulcate.
35 spp.. Temperate east Asia to Malesia, The Caucasus, North America.
3B. Subg. Helmia (Kunth) Bentham & J. D. Hooker
Plant with ± hypocotylar tubers; pollen disulcate (monosulcate - sect. Borderea); (fruit baccate - Tamus s. str./samaroid - Rajania s. str.).
Ca 595 spp.. Tropical, also warm temperate, esp. seasonal.
Synonymy: Tamaceae Berchtold & J. Presl, Tamnaceae J. Kickx f..
Evolution: Divergence & Distribution. For an evaluation of the fossil record, see Iles (2015), Viruel et al. (2015) and Raz (2017); the latter thought that the oldest fossil attributable to the genus was from derposits in the Paris basin ca 47.8 Ma, early Eocene in age.
Viruel et al. (2015: many dates) discuss the biogeographic history of Dioscorea; most diversification is Oligocene or later, and Madagascar was colonized from Asia. It has been suggested that there have been four movements into the Neotropics (Couto et al. 2018).
Schols et al. (2005b) outline pollen evolution.
Ecology & Physiology. Dioscoreaceae are a major clade of mostly rather herbaceous twining climbers that have some sort of rhizome/"tuber"/underground rootstock; some taxa are left-handed twiners (Burnham et al. 2019).
Plant-Animal Interactions. Extrafloral nectaries are common in Dioscorea (Weber & Keeler 2013).
Bacterial/Fungal Associations. Orrella dioscoreae (Burkholderiales) is the inhabitant of leaf tip glands of Dioscorea sansibarensis, the glands running the length of the acumen (I. M. Miller & Reporter 1987; De Meyer et al. 2019). Indeed, the leaf/its lobes have notably long-acuminate apices, hence the plant's name, "stiff-tipped air potato". For more information, see I. M. Miller (1990) and C.-J. Yang and Hu (2018).
Vegetative Variation. The cork in the tubers of Dioscorea is subepidermal and there may be secondary thickening. The exact morphological nature of the tuber is in some dispute, but in D. cayenensis/D. rotundata, at least, it develops in the hypocotyl/cotyledondary node area; the second leaf of the seedling is a scale leaf which has a number of axillary buds (Trouslot et al. 1994).
The vascular bundles in the stem may be arranged in 0ne or two rings (e.g. Ayensu 1972; Tenorio et al. 2017: much other detail), and are either cauline or common bundles, the former running up the stem and the latter proceeding to the leaves. If there are two rings, the cauline bundles are in the inner ring, and if there is but a single ring, the two kinds of bundles tend to alternate. Nägeli (1858), Ayensu (1969) and others discuss nodal anatomy in Dioscorea; as Ayensu (1972) emphasized, the phloem and xylem glomeruli at the nodes are unique in angiosperms. Trichopus zeylanicus lacks the distinctive vascular bundles of Avetra and the xylem and phloem glomeruli in the stem (the two are often put in a single genus, but here they are kept separate) found in other Dioscoreaceae (Ayensu 1966, 1972), but Trichopus is not a climber and its stems have but a single leaf. For midrib anatomy, see Edeoga and Ikem (2001); three vascular bundles may enter the leaf (Periasamy & Muruganathan 1985) although there are often more bundles in the petiole (e.g. Ayensu 1972). There are very distinctive raphides in Dioscorea polystachya: The individual raphides are longitudinally lamellate, each is surrounded by a membrane, and they are individually and as a group embedded in mucilage (Raman et al. 2014). Leaflets of compound leaves are initiated in basipetal pairs and may be represent localised activity in the marginal blastozone (Periasamy & Muruganathan 1985: apparently not; Gunawardena & Dengler 2006), and the very apex of the leaflets differentiates early; there is a late-developing adaxial petiolar meristem, as in palms, Acorus and Araceae. Prophylls are at least sometimes lateral.
Genes & Genomes. Martí and Ortiz (1963) discuss aspects of chromosome evolution; for chromosome numbers, etc., see also Viruel et al. (2008). Noda et al. (2020) suggest that the base chromosome number for Dioscorea is x = 10. The chromosomes of Dioscorea/Epipetrum are relatively large, being 1.9-2.9 µm long.
The plastomes show nothing much out of the ordinary (Zhao et al. 2018).
Economic Importance. In addition to being important sources of starch, tubers of Dioscorea spp. can contain very large amounts of steroidal saponins that provide the precursors of drugs like testosterone, progesterone, estrone, cortisone, and the like that are now synthesized artificially.
Chemistry, Morphology, etc.. Dioscorea batatas has storage mannans in its vegetative tissues (Meier & Reid 1982).
The position of the inflorescence in Trichopus is unclear. The flowers of Dioscorea are shown with the median member of the outer whorl in the adaxial position (Spichiger et al. 2004). The thickness of the parietal layer of the ovule is taken from Torshilova et al. (2003); Nagaraja Rao (1953) described it as being massive, and it could be interpreted as being 6-8 cells across. Seed coat anatomy would repay attention (Huber 1998). Huber (1998) noted that the mechanical layer of the seed coat was the exotegmen, but Nagaraja Rao (1953) drew the endotesta of D. oppositifolia as being made up of small, heavily U-thickened and crystal-bearing cells.
The pollen of Avetra s. str. is pantoporate; for microsporogenesis there, see Caddick et al. (1998, 2000b). There is infraspecific variation in pollen apertures; pollen grains may have one or two sulci, and this variation may even occur between grains from the one anther (Schols et al. 2003).
For additional information, see Burkill (1960), Conran and Clifford (1985), Al-Shehbaz and Schubert (1989), Huber (1998), Viruel et al. (2010), all general, and Rowley and Eggli (2020: succulents), for steroidal saponins, see Sautour et al. (2007) and references, for vegetative anatomy, Queva (1894) and Ayensu (1972), Behnke (1990b: nodal anastomoses), for pollen, van der Ham (1994: not Dioscorea), for ovules, Igersheim et al. (2001), and for ovules and seeds, Nagaraja Rao (1955: Trichopus) and Torshilova and Titova (2010).
Phylogeny. Much detailed information is provided by Caddick et al. (2002b), although the positions of Stenomeris and Trichopus remain unclear (Viruel et al. 2015 and references); most recently Noda et al. (2020) placed Stenomeris as sister to Dioscorea. For the circumscription of Dioscorea and relationships within the genus, see Bharathan et al. (2001), Caddick et al. (2002a), Wilkin et al. (2005) and especially Viruel et al. (2015) and Couto et al. (2018: 2 plastid genes). Analysis of variation in the nuclear Xdh gene yielded a topology largely similar to that using variation in four plastid genes (Viruel et al. 2018); see also Noda et al. (2020) and Soto Gomez et al. (2020: target enrichment) for relationships. The largely North Temperate section Stenophora (= subgenus Dioscorea) is sister to the rest of the genus, which has implications for generic apomorphies since subgenus Dioscorea is the only clade in the genus with tricolpate pollen, the plant is rhizomatous, etc. (Viruel et al. 2015, 2018; Noda 2020).
Classification. The three genera have usually been placed in separate (albeit more or less closely related) families, although Ayensu (1972) was inclined to think that Trichopus s. str. (see above for its anatomy) was rather separate from the other three genera, all of which he included in Dioscoreaceae.
Dioscorea s. str. was divided into 22 sections by Huber (1998), and all were fully described, but, assuming their monophyly holds up, having 22 genera would not seem a desirable option. For the beginning of an infrageneric classification, see Noda et al. (2020) with subgenera Dioscorea (= section Stenophora) and Helmia, the latter with 19 sections.