EMBRYOPSIDA Pirani & Prado
Gametophyte dominant, independent, multicellular, initially ±globular, not motile, branched; showing gravitropism; acquisition of phenylalanine lysase* [PAL], flavonoid synthesis*, microbial terpene synthase-like genes +, triterpenoids produced by CYP716 enzymes, 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; glycolate metabolism in leaf peroxisomes [glyoxysomes]; 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; 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 [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]; 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 gene moved to nucleus; mitochondrial trnS(gcu) and trnN(guu) genes +.
Many of the bolded characters in the characterization above are apomorphies of subsets 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.
Abscisic acid, L- and D-methionine distinguished metabolically; pro- and metaphase spindles acentric; class 1 KNOX genes expressed in sporangium alone; sporangium wall 4≤ cells across [≡ eusporangium], tapetum +, secreting sporopollenin, which obscures outer white-line centred lamellae, columella +, developing from endothecial cells; stomata +, on sporangium, anomocytic, cell lineage that produces them with symmetric divisions [perigenous]; underlying similarities in the development of conducting tissue and of rhizoids/root hairs; spores trilete; shoot meristem patterning gene families expressed; MIKC, MI*K*C* genes, post-transcriptional editing of chloroplast genes; gain of three group II mitochondrial introns, mitochondrial trnS(gcu) and trnN(guu) genes 0.
[Anthocerophyta + Polysporangiophyta]: gametophyte leafless; archegonia embedded/sunken [only neck protruding]; sporophyte long-lived, chlorophyllous; cell walls with xylans.
Sporophyte well developed, branched, branching apical, dichotomous, potentially indeterminate; hydroids +; stomata on stem; sporangia several, terminal; spore walls not multilamellate [?here].
Vascular tissue + [tracheids, walls with bars of secondary thickening]; stomata numerous, involved in gas exchange.
EXTANT TRACHEOPHYTA / VASCULAR PLANTS
Sporophyte long lived, chlorophyllous, with 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]; polar auxin transport, PIN [auxin efflux facilitator] involved; (condensed or nonhydrolyzable tannins/proanthocyanidins +); xyloglucans with side chains uncharged [?level], in secondary walls of vascular and mechanical tissue; lignins +; roots +, 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 +; leaves +, vascularized, leaves/sporophylls spirally arranged, blades with mean venation density ca 1.8 mm/mm2 [to 5 mm/mm2], all epidermal cells with chloroplasts; sporangia adaxial, columella 0; tapetum glandular; ?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]; 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 size [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 lateral, meristems axillary; lateral root origin from the pericycle; cork cambium + [producing cork abaxially], vascular cambium bifacial [producing phloem abaxially and xylem adaxially].
Growth of plant bipolar [roots with positive geotropic response]; 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].
EXTANT SEED PLANTS / SPERMATOPHYTA
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]; root stele diarch to pentarch, xylem and phloem originating on alternating radii, cork cambium deep seated; 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.; 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; female gametophyte initially syncytial, walls then surrounding individual nuclei; embryo cellular ab initio, suspensor short-minute, embryonic axis straight [shoot and root at opposite ends; plant 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], two copies of LEAFY gene, PHY gene duplications [three - [BP [A/N + C/O]] - copies], 5.8S and 5S rDNA in separate clusters.
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; origin of epidermis with no clear pattern [probably 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, wood parenchyma +; sieve tubes enucleate, sieve plate 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 pore], 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; 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 lamellate only in the apertural regions, thin, compact, intine in apertural areas thick, 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, nucleus of egg cell sister to one of the polar nuclei]; 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 (20-)80-20,000 µm/hour, 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; P deciduous in fruit; mature seed much larger than fertilized ovule, small [<5 mm long], dry [no sarcotesta], exotestal; endosperm +, ?diploid, 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 [1C] <1.4 pg [mean 1C = 18.1 pg, 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 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 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).
MONOCOTYLEDONS / MONOCOTYLEDONEAE / LILIANAE Takhtajan
Plant herbaceous, perennial, rhizomatous, growth sympodial; non-hydrolyzable tannins [(ent-)epicatechin-4] +, neolignans 0, CYP716 trterpenoid enzymes 0, benzylisoquinoline alkaloids 0, hemicelluloses as xylan; 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; stomata oriented parallel to the long axis of the leaf, in lines; prophyll single, adaxial; leaf blade linear, main venation parallel, 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 = 3 + 3 T, each 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; fruit a loculicidal capsule; 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, hypocotyl short, (collar rhizoids +); no dark reversion Pfr → Pr; duplication producing monocot LOFSEP and FUL3 genes [latter duplication of AP1/FUL gene], PHYE gene lost.
[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; endosperm nuclear [but variation in most orders].
[DIOSCOREALES + PANDANALES]: root hairs from unmodified rhizodermal cells, exodermal cells not dimorphic; outer integument 2(-3) cells across; genome size <10 pg [1C].
PANDANALES Berchtold & J. Presl Main Tree.
Anthers basifixed; nucellar cap +; endosperm type?, (reserves starch), embryo minute; genome size 0.4-1.5 pg [1C]. - 5 families, 36 genera, 1345 species.
Age. Crown group Pandanales are estimated to be (130-)117(-116) m.y.o. (Merckx et al. 2008a), ca 114 m.y.o. (Janssen & Bremer 2004), (111-)103(-95) or (98-)91(-89) m.y. (Hertweck et al. 2015), (96-)90, 84(-78) m.y.o. (Wikström et al. 2001), (117-)82, 72(-65) m.y.o. (Bell et al. 2010), (101-)74(-53) m.y. (Givnish et al. 2016b), ca 72.3 m.y.a. (Magallón et al. 2015) or only ca 50 m.y. (Bremer 2000b). Ages are 110-69 m.y. in Mennes et al. (2013, 2015).
Note: Boldface denotes possible apomorphies, (....) denotes a feature common in the clade, exact status uncertain, [....] includes explanatory material. Note that the particular 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).
Evolution: Divergence & Distribution. Stevenson et al. (2000) suggest other possible characters for the order and the groups of families within it. These include a 6 bp deletion in atpA - absent in Talbotia (Velloziaceae), whether or nor it occurs in Barbaceniopsis is unclear (c.f. Davis et al. 2004) - and a distinctively connate androecium; tenuinucellate ovules may be another synapomorphy, and starchy endosperm is common here.
Chemistry, Morphology, etc. Rudall et al. (2005b) note that floral meristicity, usually not very variable in the monocots, varies considerably in Pandanales; general floral construction is rather labile here.
Some information on pollen morphology is taken from Grayum (1992); for pollen and tapetum, etc., see Furness and Rudall (2006a).
Phylogeny. For discussion on the relationships of Pandanales, see the Petrosaviales page.
The circumscription of Pandanales is somewhat unexpected, including as it does some of the most delicate (Triuridaceae) and most woody and robust (Pandanaceae) and drought-tolerant (Velloziaceae) monocots. The phylogeny above is taken from Behnke et al. (2000, 2013), and especially Caddick et al. (2002a), Davis et al. (2004: Fig. 1) and Mennes et al. (2013), although even in the last study, quite comprehensive, the position of Stemonaceae was not very strongly supported. Janssen and Bremer (2003: Triuridaceae not included) suggested a somewhat different set of relationships. The [Pandanaceae + Cyclanthaceae] clade appears consistently and also has strong morphological support.
Triuridaceae often group with Pandanales in molecular analyses (e.g. Chase et al. 2000a: 18S rDNA; Graham et al. 2005), but they vary in their relationships within the order. Relationships in Hertweck et al. (2015) are [Velloziaceae [Triuridaceae [Stemonaceae...]]]. Morphological analyses even suggested that Triuridaceae were nested within Stemonaceae (Rudall & Bateman 2006), but without strong bootstrap support (50³%, hardly the robust placement claimed), and characters that supported this position included thick filaments, free carpels, and pollen morphology. However, recent analyses using plastomes, including the very small plastome of Sciaphila, yielded the rather well supported relationships in the tree below; only in parsimony analyses was a clade [Sciaphila + Xerophyta] obtained, and it had low support (Lam et al. 2015); sampling may be a worry, only 10 Pandanales were included in the study (see also Lam et al. 2016: weak support, some sequences on occasion placed with Dioscoreales-Nartheciaceae).
Although Triuridaceae were found to be sister to Zingiberaceae in some analyses by Davis et al. (2004), this is an unlikely position, if morphology means anything! Nartheciaceae have sometimes tended to associate with Pandanales, rather than Dioscoreales (q.v. for further details), the clade in which they are included here.
Includes Cyclanthaceae, Pandanaceae, Stemonaceae, Triuridaceae, Velloziaceae.
Synonymy: Cyclanthales Martius, Roxburghiales Martius, Stemonales Doweld, Triuridales J. D. Hooker, Velloziales Reveal
VELLOZIACEAE J. Agardh, nom. cons. Back to Pandanales
Xeromorphic; roots with vessel elements with simple perforation plates, band of fibres in cortex; vessels in stem and leaf; phloem in at least smaller bundles in two abaxial-lateral strands; sieve tube plastids in the stem 1³ µm across; stem cortex in three zones, divided by bundles of fibres or fibrous sheath; stomata brachyparacytic; leaves persistent; inflorescences axillary; flowers large; A borne in mouth of "hypanthium"; pollen grains bi- or tricellular; ovary inferior, placentae bifid, stalked-capitate, style long; ovules many/carpel, parietal tissue none; fruit dehiscing laterally, loculicidal; exotesta thick walled, endotegmen thin-walled, with phenolics/tanniniferous; aleurone cells with thick walls, endosperm with starch.
9 [list]/240 (306). South America and Africa-Madagascar to Arabia, China.
Age. The crown age of this family must be 115 m.y. or so (Mello-Silva et al. 2011).
1. Acanthochlamydoideae P. C. Kao
Caespitose rhizomatous herb; steroidal saponins +?; (velamen +), root stele tri- or tetrarch, not medullated; lateral roots arise opposite xylem poles; sive tube plastids lacking crystals, "small"; cauline vascular tissue aggregated in the centre of the stem, phloem dispersed among the xylem; scape with ca 6 central vascular bundles, leaf adnate to scape; raphides and tannin cells 0; palisade tissue 0; endodermis surrounding two back-to-back vascular strands in leaf; leaves spiral, ligule basal, sheathing [?what], large, mostly open on side away from blade; inflorescence scapose, compound-capitate; T ca 1/2 connate; anthers short, bisporangiate, ?thecae, filaments short; septal nectaries 0; nucellar cap 0; exotestal cells evenly thickened, ± elongated; endosperm nuclear, embryo large/medium; n = 19, chromosomes <1 μm long; seedling?
1/1: Acanthochlamys bracteata. S.E. Tibet and S.W. China (Map: from Ying et al. 1993 - green). [Photo - Flower, Fruit.]
Synonymy: Acanthochlamydaceae P. C. Kao
2. Vellozioideae Rendle
Woody or herbaceous, plants showing extreme dessication tolerance, roots often growing down through persistent leaf bases; biflavonoids + [Xerophyta]; (velamen +); tracheids in stem main conducting tissues; sieve tube plastids with angular crystals and other loosely-packed crystals; (vessels in leaves absent - Talbotia); transfusion tracheids in leaf bundles; (raphides/styloids +); stomata in grooves, (on both surfaces), (cuticular waxes as aggregated rodlets), leaves with marginal bundles and transfusion tissue; indumentum various; leaves (spirally)3-ranked, (blade abscising), vernation conduplicate-flat, midrib +, margins usu. spiny; inflorescences often single-flowered, bracteoles lateral; flowers with multicellular glands on the outside: hypanthium +/0; T often violet, median T in outer whorl adaxial [e.g. Barbacenia], largely free; (corona +, usu. adnate to adaxial A); A 6-many, not adnate to T, (3 or 6 fasciculate [A in fascicle connate], development within fascicles ± centripetal), filaments cylindrical, anthers long, (dorsifixed); tapetal cells uninucleate; (pollen in tetrads); septal nectaries +; stigmas large, erect or spreading, capitate; micropyle bi/endostomal, outer integument 2 cells across, inner integument 2 cells across, nucellar cap ?+/0, endothelium +, funicular obturator +, suprachalazal tissue massive; archesporial cells several; fruit also poricidal or with intercostal apertures; exotesta with spiral/reticulate (0) thickenings, endotegmen with outer periclinal and anticlinal walls thickened (not); endosperm helobial, cells elongated, wall formation in small chalazal chamber precedes that in large micropylar chamber, (aleurone cell walls unthickened), embryo medium to short; n = 7, 8, 17, 24 [x = 12?]; collar rhizoids +.
8/240: Vellozia (105), Barbacenia (90). South America and Africa-Madagascar (to Arabia) (Map: see Ayensu 1973b - red). [Photo - Habit, Flower.]
Age. Crown-group Vellozioideae have been dated to a mere ca 14 m.y.a. (Janssen & Bremer 2004: note sampling), or some 100 m.y.a. or so (Mello-Silva et al. 2011).
Synonymy: Barbaceniaceae Arnott
Evolution: Divergence & Distribution. Mello-Silva et al. (2011) interpreted the split of Acanthochlamys from the rest of the family and other generic disjunctions in terms of drift-induced vicariant events.
Ecology & Physiology. Velloziaceae include many dessication-tolerant taxa common on inselbergs, and a number of arborescent taxa (Porembski & Barthlott 2000; Farrant 2000: Xerophyta; Naidoo et al. 2009: Xerophyta viscosa, analysis of substances secreted on adaxial surface of the leaf). Indeed, Vellozioideae as a whole (?Acanthochlamys) show extreme dessication tolerance, being poikilochlorophyllous (their chloroplasts ± break down) resurrection plants (Gaff & Oliver 2013). The physiology of this has been studied in detail in the octoploid African Xerophyta viscosa (Farrant et al. 2015), and this species i.a. has several clusters of dessication-associated genes, including late embryogenesis abundant genes, genes that are also involved in the expression of dessication tolerance in seeds (Costa et al. 2017; see also Oliver et al. 2005; Gaff & Oliver 2013). Xerophyta is poikilochlorophyllous, losing all of its chlorophyll during drying, and its leaves may remain viable for more than two years (Costa et al. 2017).
Martins and Paiva (2016) looked at resin secretion and composition in Vellozia variabilis (see also Saldala-Castilho et al. 2016), noting that the resin had both flavonoid and terpenoid components and, perhaps paradoxically, protected the plant from serious fires damage by burning easily and quickly. The true stem is narrow and soon rots away, the "trunk" consisting of roots, each initially with a velamen, and persistent leaf bases (Porembski 2006).
Plant-Animal Interactions. Meliponine bees (Trigonia, Tetragonisca) remove resin from the glands on the outside of the flowers of Barbacenia and Vellozia, although this seems to be of little importance for the plant (Sadala-Castilho et al. 2016).
Bacterial/Fungal Associations. There are endophytic bacteria in the glands on the outside of the flowers of Barbacenia and Vellozia (Sadala-Castilho et al. 2016).
Chemistry, Morphology, etc. The vegetative morphology and anatomy of Acanthochlamys are remarkable and difficult to understand. Its roots are tetrarch or triarch and lack pith, and so are unlike the roots of most other monocots (Cattai 2007), some Alismatales excepting, Triuridaceae, some Burmanniaceae, etc., also having non-medullated roots. The anatomy of the stem/rhizome of Acanthochlamys is unclear; it seems to consist of perhaps four vascular bundles in the centre, almost touching, and apparently with a small amount of non-vascular tissue in the middle (c.f. de Menezes et al. 2013). The anatomy of the scape has been described as "similar to that of a leaf ensheathing a rhizome" (Kao & Kubitzki 1998: 56; see also Gao 2017), although the central part of the stem is more like a root, not a rhizome and how the "foliar" bundles relates to the stele and to an inflorescence bract is unknown. Large amounts of sclereidal/fibrous tissue ("secondary phloem", "sieve cell": Gao 2017) underlie the epidermis and surround the central stele. There are apparently two pairs of leaves (Z.-D. Chen et al. 2016), and leaves have a rather large basal adaxial ligule ensheathing the ?stem and lack axillary buds (de Menezes et al. 2013); the other genera have more simply sheathing bases. However, leaves are not shown as sheathing the rhizome by Gao (2017: fig. 1"J" = L,) so what the ligule is ensheathing is unclear. Phloem in the "midrib" bundles of the leaves is sometimes arcuate in Vellozioideae, but in smaller bundles in particular it is broken up into two abaxial-lateral strands (Smith & Ayensu 1976), while in Acanthochlamys there appear to be two U-shaped collateral vascular bundles surrounded by an endodermis in the centre of the leaf (de Menezes et al. 2013; Gao 2017). Amaral and Mello-Silva (2005, esp. 2008) suggest that the tetracytic stomata of Vellozioideae are better thought of as paracytic.
The single flowers/inflorescences are apparently always terminal (Kubitzki 1998b), although this can be hard to make out; work on branching patterns would be useful. What is described here as the hypanthium in Velloziaceae may bear the same indumentum as that on the pedicel; assuming the traditional definition of a hypanthium, the perianth members here would usually be more or less free. The stamens may be adnate to the tepals for most of their length, as in Barbaceniopsis. The corona develops late, and although partly associated with the bases of the filaments, its vasculature is in part tepal-like (Sajo et al. 2010: q.v. also for androecial development). In Acanthochlamys the anthers opposite the inner tepal members are inserted higher up on the tube than the anthers opposite the outer members. For the possibility of a chalazal haustorium in the embryo that develops from the antipodal cells or from chalazal nucellar tissue, see Sajo et al. (2013).
Additional information is taken from Ayensu (1973a), Kubitzki (1998b), and Behnke et al. (2000), all general, Williams et al. (1991: chemistry), Smith and Ayensu (1976: monograph - with anatomy - of New World taxa), Behnke et al. (20013: anatomy), de Menezes (1980: androecial evolution), Stenar (1925: embryology of Vellozia elegans, both layers of cells of inner integument palisade), Strassburg and de Menezes (2001: fruit and seed) and Sousa-Baena and de Menezes (2014: seed coat anatomy); for Acanthochlamys in particular, see also Kao and Kubitzki (1998: much detail), Kao (1989), de Menezes et al. (2013) and Gao (2017 and references) - Kao and Gao are one and the same.
Phylogeny. Talbotia (African) is mesophytic and its filaments are not adnate to the tepals. It is perhaps sister to the other Vellozioideae (but c.f. Behnke et al. 2000), however, basal relationships are unresolved. Barbacenia is paraphyletic, but Barbacenioideae are monophyletic (corona +; n = 7). Vellozioideae sensu Menezes are paraphyletic (Salatino et al. 2001), however, there is considerable disagreement between the topologies implicit in different morphology-based classifications of the family (Mello-Silva 2005), and that in Mello-Silva is only partly congruent with that of the molecular tree of Behnke et al. (2000, 2013). Nevertheless, Acanthochlamys is clearly sister to the rest of the family (Behnke et al. 2000, 2013; Mello-Silva 2005). In a joint molecular and morphological study, Mello-Silva et al. (2011: see data matrix) found the relationships [Acanthochlamys [Xerophyta (inc. Talbotia) + the rest (support not strong)]] (see also Behnke et al. 2013: support much higher in Bayesian than ML analyses), and suggest a number of apomorphies for the main clades, although optimisation of some of them is difficult. For relationships within Xerophyta, see Behnke et al. (2013).
Classification. Although Acanthochalmys, sister to the rest of the family, is morphologically and anatomically distinct, subfamilial status is appropriate (Behnke et al. 2000; Mello-Silva 2005; c.f. Gao 2012, 2017). If a family, it would be monotypic, yet Velloziaceae s.l. are well characterized.
For suggestions as to generic limits in the family, see Mello-Silva et al. (2011). The list above will ultimately have to be emended.
[Stemonaceae [Triuridaceae [Pandanaceae + Cyclanthaceae]]]: vessels also in stem, with scalariform perforation plates; (styloids +); flowers other than P3 + 3 A6 G3; septal nectaries 0; placentation parietal, style 0, stigmas/stigmatic branches ± separate.
Age. The age of this node is estimated at ca 101.7 m.y. (Magallón & Castillo (2009), (109.6-)99.3(-91.9) m.y. (Eguchi & Tamura 2016), about 80.8 m.y. (Tank et al. 2015: Table S2), (84-)76, 66(-50) m.y. (Bell et al. 2010), or only ca 53.7. m.y.a. (Magallón et al. 2015).
Evolution: Divergence & Distribution. Floral variation in this really quite small clade is remarkable and is conveniently summarized by Rudall (2017), indeed, even in Velloziaceae stamen number is often other than six. However, confirmation of the position of Triuridaceae in particular is needed to understand morphological evolution here (see Garay-Arroyo et al. 2012), and the flowers may be so highly modified that it is unclear exactlyat what one is looking (e.g. Rudall 2017) - and under such circumstances one can hardly talk about evolution. There is also some pretty odd vegetative variation - especially in Acanthochlamys above and Sararanga below.
STEMONACEAE Caruel, nom. cons. Back to Pandanales
Plant monopodial, (tuberous), with cataphylls, stem erect (twining); (unspecified saponins - Stemona), alkaloids with pyrrolo- or pyrido(1,2,-α)- azepine nucleus, +; stem vascular bundles in 1 or 2 rings, those of inner or only ring amphivasal; petiole bundles in arc; (styloids +); plant glabrous; stomata oriented transverse to long axis of leaf [Stemona; leaves two-ranked or opposite, with petiole, blade and midrib, base not sheathing, midrib simple (not distinct), petiole bifacial [Croomia], cataphylls +, sheathing; inflorescences axillary, cymose, or flowers single; (flower monosymmetric - Croomia heterosepala), pedicel articulated; T 4(-5), perianth tube short; A adnate to base of T, ± connate, (apex of anther sterile), connective expanded, (apiculate); pollen (inaperturate), reticulate to perforate, intectate, (hyper)scabrate); G 1 to , (inferior), placentae apical or basal, style branches long; ovules 2 to many/carpel, outer integument to 5 cells across, inner integument to 3 cells across, parietal tissue (0?-2) cells across; fruit a capsule [?type]; seeds longitudinally ridged, aril of uniseriate or vesicular hairs from hilum, raphe or micropyle; testa multiplicative, several-layered, ridges many cells high, tanniniferous, inner 4 layers thick-walled, (test ca 2 layers across, radial wall of exotesta thickened, forming the ridge - Pentastemona), (tegmen persists, cell walls thickened); endosperm copious, starchy, walls not pitted; n = 7, 9, 12; seedling with non-photosynthetic cotyledon, primary root well developed.
4 [list]/27 (37). China and Japan to Australia, S.E. U. S. A. (Croomia ) (map: from Duyfjes 1993; Fl. N. Am. 26: 2002). [Photo - Croomia - Habit].
Age. Crown group Stemonaceae are dated to ca 84 m.y. (Janssen & Bremer 2004).
Evolution: Pollination Biology & Seed Dispersal. At least some Stemonaceae are pollen flowers (Vogel 1981).
Myrmecochory is common in the family (Lengyel et al. 2010).
Chemistry, Morphology, etc. The distinctive alkaloids found in Stemonaceae with their pyrrolo- or pyrido(1,2,-α)-azepine nucleus (see also Pilli & Ferreira de Oliveira 2000) are probably an apomorphy of the family. Duyfjes (1992) inadvertently suggested that Stemonaceae s. str. - i.e. not including Pentastemona - lacked cataphylls, however, these are well documented on the underground parts (e.g. Tomlinson & Ayensu 1968), while van Steenis (1982) noted that they were sheathing and compared this feature to the sheathing photosynthetic leaves of Pentastemona, suggesting an equivalence. Stemona, etc., do not have sheathing leaves.
The morphology of the inflorescence and the nature of the breeding system of Pentastemona need more study - also its anatomy, chemistry, etc. Stemona phyllantha has epiphyllous inflorescences. The anatomy of the seed ridges varies considerably.
Additional information is taken from Duyfjes (1991) and Kubitzki (1998b), both general, Swamy (1964b) and Bouman and Devente (1992), both ovules and seeds, Endress (1995b: flowers of Pentastemona), van der Ham ((1994) and Furness and Rudall (2000b), both pollen, and Rudall et al. (2005b: floral morphology).
Phylogeny. Pentastemona appears to be well embedded within the family (e.g. Jiang et al. 2006: molecular data, c.f. Rudall & Bateman 2006: morphological analysis); on balance, its distinctive features are likely to be derived. However, Lam et al. (2015: plastome analyses) found the relationships [Pentastemona [Stemona + The Rest]].
Pentastemona can be briefly characterised as follows: Succulent monopodial herb; cataphylls 0; hairs uniseriate; stomata para- or tetracytic; leaves spiral, with compound midrib, sheath ?closed; inflorescences (branched) racemose; flowers 5-merous, perianth tube long to short; A 5, connate into a fleshy ring, basally adnate to T and connectives apically adnate to stigmas; pollen inaperturate, atectate; [G 3], inferior, placentation parietal, many ovules/carpel, stigmatic lobes well developed; fruit a berry; seed arillate; sarcoexotesta +, endotesta with massive U-shaped thickenings, producing ridges; seedling?
Synonymy: Croomiaceae Nakai, Pentastemonaceae Duyfjes, Roxburghiaceae Wallich
[Triuridaceae [Pandanaceae + Cyclanthaceae]]: leaves spiral; inflorescence racemose; flowers imperfect.
Age. The stem node of Triuridaceae has been dated to to 86.3 m.y.a. based on the New Jersey fossil Mabelia connatifila (Isles et al. 2015).
TRIURIDACEAE Gardner, nom. cons. Back to Pandanales
Plant mycoheterotrophic, echlorophyllous; chemistry?; roots in pairs from the axils of scale leaves; vessels 0; root pith not medullated; stem with vascular bundles in a single ring, (endodermis +); crystals 0; plant glabrous; cuticular waxes as parallel series of platelets, within a series transversely arranged; stomata 0; leaves reduced, (base sheathing), (closed); bracteole 0; T valvate, ?trace number, (nectary +); A connate or not, filaments stout; tapetal cells uninucleate; pollen grains tricellular, 15-25 µm across, inaperturate, surface gemmate, gemmae with protruberances or spines; G 10-many, separate, plicate, styles solid, no transmitting tissue, stigma penicillate to smooth, ?dry; basal, parietal tissue none, nucellar cap 0, endothelium, hypostase +; fruit indehiscent; seeds endotestal, inner cuticle very thick, exotesta persisting; endosperm hemicellulosic, copious, almost a chalazal haustorium; n = 9, 11, 12(-16); seedling?
11 [list - in tribes]/50. Pantropical (map: from van de Meerendonk 1984; Maas & Rübsamen 1986; Rübsamen-Weustenfeld 1991; Trop. Afr. Fl. Pl. Ecol. Distr. 7. 2012).
Age. The age of crown-group Triuridaceae is estimated at 90-50 m.y. (Mennes et al. 2013).
Despite the delicate nature of plants in this family, fossil flowers of Triuridaceae (two genera) have been reported from ca 90 m.y.o. rocks in New Jersey (Gandolfo et al. 1998a, 2002). They were then the earliest monocot fossils known, but that honour has now been taken by Araceae (see Friis et al. 2004), and anyhow their identification has been questioned (Rudall 2003b; Friis et al. 2011).
1. Kupeaeae Cheek
Roots stout, radiating, root hairs 0; inflorescence a spike; plant dioecious; flower monosymmetric; T 4, (basally connate), with a single trace [Kupea], apex acute, (bifid); staminate flowers: (bract adnate to flower - Kupea); A 4, anther dehiscence transverse; pollen ca 25 µm across; carpellate flower: staminodes 0; style (sub)terminal, stigmatic zone indistinct; ovules 2/carpel, hemitropous to campyltotropous; fruit an achene, 2-seeded; ?endosperm.
2/3. Africa: Cameroon and Tanzania.
[Sciaphileae + Triurideae]: plant rhizomatous; roots slender; staminate flowers: pistillodes usu. 0; carpellate flowers: staminodes 0; style ± lateral to basal; ovule 1/carpel.
2. Sciaphileae Miers
(Roots stout, radiating, diarch, no pith, root hairs 0); (stem a dictyostele; leaf trace single); plant monoecious, (flowers perfect); T 4, 6, 8, (basally connate), apex acute, with a tuft of hairs or not; staminate flowers: A 2, 3, 4, 6, anther dehiscence diagonal-transverse (vertical), (connective with appendage); tapetum amoeboid; pollen (monosulcate - Sciaphila), 24-40 µm across; carpellate flowers: (staminodes +); carpel development centripetal, spiral/whorled, style gynobasic; fruit a follicle (achene); seed with testal cells on chalazal side collapsed, or small, thickish walled, over rest of seed endotestal cells large and radially elongated, wall thickenings radial.
5/40: Sciaphila (30). Mostly Old World, esp. Indo Malesia and the Pacific, few New World. [Photo - Sciaphila].
3. Triurideae Miers
(Roots thin, radiating), (moderately thick), root hairs few to none; plant usually dioecious; T 3, 6, (connnate basally), apex with caudate appendage (short); staminate flowers: A 3 (6, unithecal), (androphore +, anthers sessile), anther dehiscence longitudinal (horizontal); pollen 15-21 µm across; central appendage +; carpellate flowers: carpel development centrifugal, ± fasciculate, (style (sub)terminal); embryo sac tetrasporic, the three chalazal megaspores fuse, divide twice, 7-celled and 8-nucleate, the antipodals triploid [Fritillaria-type]; fruit an achene; endotestal cells with wall thickenings parallel to long axis of seed; endosperm pentaploid, initially with starch.
4/9. American Tropics, esp. the Guianan area, scattered. [Photo - Triuris.]
Synonymy: Lacandoniaceae E. Martínes & Ramos
Evolution: Divergence & Distribution. Mennes et al. (2013) found long branch lengths within Triuridaceae, and noted that these, along with the age of the family and its mycoheterotrophic life style, made its morphological distinctiveness comprehensible.
Rübsamen-Weustenfeld (1991) lists other characters, especially of endosperm, embryo size and seed anatomy, that separate Sciaphileae and Triurideae; some may turn out to be apomorphies, but Kupeaeae are poorly known.
Lacandonia schismatica (s very similar species has recently been found in Brazil) has stamens borne inside the carpels, almost unique in angiosperms. Although it has been suggested that these "flowers" may be pseudanthia (Rudall 2003b), heterotopy/homeosis is a more likely explanation (Ambrose et al. 2006; esp. Álvarez-Buylla et al. 2010; Rudall et al. 2016). Interestingly, the carpels still develop after the stamens, despite their reversed positions (Garay-Arroyo et al. 2012), and Endress (2014) offered an ingenious suggestion that the relative position of the two is normal, only appearing to have been thrown off because of the distortion at the floral apex caused by the development of numerous carpels. Indeed, the carpels of Peltophyllum luteum develop on ridges snaking up and down around the apex of the flower (Rudall et al. 2016; see also Sokoloff et al. 2007b). It has been suggessted that the recognition of Lacandonia may make Triuris paraphyletic (Vergara-Silva et al. 2003); if this relationship is confirmed (it was not by Mennes et al. 2013), the morphological context for an explanation of the distinctive floral construction of Lacandonia becomes very specific indeed.
Pollination Biology. Lacandonia can self pollinate: Pollen grains germinate while still in the anther and the tubes grow through the tissue of the flower to the ovule (Márquez-Guzmán et al. 1989; X.-F. Wang et al. 2011; Rudall et al. 2016). In general, polllination by small flies is likely (Rudall & Bateman 2006).
Bacterial/Fungal Associations. Mycorrhizae are of the Paris type (Imhoff 1998). Glomeromycote fungi are involved in mycoheterotrophy, and there can be very complex patterns of fungal colonization in the one plant (Hynson & Bruns 2010; Imhof et al. 2013). Imhof (2004) discussed the extensive variation in underground parts in the family.
Genes & Genomes. For the very small chloroplast genome of Sciaphila densiflora with its 28 functional genes, see Lam et al. (2015); it is largely colinear with that of Carludovica, over seven times its size.
Chemistry, Morphology, etc.The roots lack pith (von Guttenberg 1968) and the root stele is monarch or diarch - the entire stele from the endodermis inwards may be lignified (Johow 1889 and references).
The tiny staminate flowers of Kupea and Kihansia are quite strongly monosymmetric (Cheek 2003a; Rudall et al. 2007b). Endress (1995b) illustrated more or less paired tepal nectaries in Triuris. Inter- and intraspecific variation in the number of parts of the flower is considerable (see Rübsamen-Weustenfeld 1991; Maas-van der Kamer 1995; Rudall et al. 2007b). In the perfect flowers of Lacandonia and carpellate flowers of Triuris individual carpel primordia develop from compound primordia, and in the former stamen and carpel primordia develop from a common precursor. Rudall (2008) suggested that the basic construction of the gynoecium in some Triuridaceae is fasciculate, the fascicles being radially elongated and developing centrifugally - there is considerable variation in gynoecial development (see also Rübsamen-Weustenfeld 1991). Hooker (1859) noted that the ovules were anatropous and unitegmic. Although some Triuridae have tetrasporic embryio sacs of the Fritillaria-type, ordinary monosporic Polygonum-type embryo sacs have also been reported here (Espinosa-Matiás et al. 2012). The strong asymmetry of the seeds, apparently restricted to some Sciaphileae (e.g. Wirz 1910, c.f. Batygina et al. 1990: interpretation difficult, plane of sections?), is reflected in their being more or less winged on one side.
For general information, see Rübsamen-Weustenfeld (1991), Maas-van der Kamer and Weustenfeld (1998), Franke et al. (2000: Triurideae) and Merckx et al. (2013a), for pollen, etc., Furness et al. (2002a), for ovule and seed, see Johow (1889), and for carpels, etc., see Igersheim et al. (2001).
Phylogeny. In morphological analyses Kupea was sister to the rest of the family and Sciaphileae were paraphyletic (Rudall & Bateman 2006: Kihansia not included). The three tribes above were recovered as monophyletic in the four-gene study by Mennes et al. (2013), but inclusion of additional taxa with fewer than three genes suggested that Sciaphileae, and in particular Sciaphila, were paraphyletic, Sciaphileae and Triurideae together being sister to Kupeaeae (see also Mennes et al. 2015).
Classification. For tribes, I follow Rübsamen-Weustenfeld (1991) and Cheek (2003a).
Previous Relationships. Triuridaceae have often been associated with Alismataceae and relatives, all having separate carpels and so assumed to be primitive.
[Pandanaceae + Cyclanthaceae]: stem vascular bundles compound; styloids +; stomata tetracytic, subsidiary cells with oblique cell divisions; inflorescence bracts conspicuous, inflorescence a dense spike or head [a spadix], inflorescence bracts coloured or not; flowers dense, sessile, in spirals, small; staminate flowers: stamens usu. several-many; pollen porate; pistillode +; carpellate flowers: staminodes +; ovules apotropous, with radiating subepidermal nucellar/chalazal cells; fruit an indehiscent syncarp [baccate or drupaceous]; endotesta well developed, internally to that are two persistent cuticular layers; cotyledon not photosynthetic, seedling with all internodes ± elongated.
Age. The divergence between the two families has been dated to (74-)68, 66(-60) m.y. (Wikström et al. 2001), ca 98 m.y. (Janssen & Bremer 2004), (71-)52, 47(-31) m.y. (Bell et al. 2010), and (139.3-)86, 81(-49) m.y. (Gallaher et al. (2014).
Chemistry, Morphology, etc. The compound vascular bundles can sometimes be seen under a hand lens; the vascular bundles have groups of vessels at opposite ends with smaller cells in between. See Carlquist (2012a) for xylem anatomy.
Previous relationships. A group recognised in the past was the Spadiciflorae; this included those taxa with a spadix and often also a spathe, i.e. Pandanaceae, Cyclanthaceae, Araceae and Arecaceae. These families are now placed in three orders, Pandanales, Alismatales and Arecales. Engler (1892) linked Pandanaceae, Arecaceae and Cyclanthaceae.
PANDANACEAE R. Brown, nom. cons. Back to Pandanales
Plant woody, habit various, trees, shrubs, or climbers with roots from leaf axils, rhizomes 0; vessel elements also in leaf; sieve tube plastids also with peripheral fibres; (cuticular waxes as aggregated rodlets); leaves (amphistomatic), spirally three-ranked, (?decussate), vernation conduplicate-flat, ± V or M-shaped when mature, margins spiny, (sheaths closed; base auriculate - Freycinetia); plant dioecious (monoecious); (inflorescence branched, paniculate, flowers ?single - Sararanga); (pedicel + - Sararanga sinuosa]; T 0 (connate as cupule - Sararanga/6 primordia - Freycinetia); staminate flowers: A 1-many, variously free to connate or aggregated [on underside of peltate structure], filaments papillate or not; pistillode 0; pollen exine three-layered [level?]; pistillode + (0); carpellate flowers: staminodes + (0); G 1-several, free to connate, intra-ovarian trichomes +, (placentation parietal); ovule 1/carpel (many - Freycinetia), apotropous, (micropyle bistomal), parietal tissue 1-5 cells across, (nucellar cap ca 2 cells across), obturator and hypostase +; (embryo sac incorporating nucellar cells at chalazal end - Pandanus), (bisporic - Pandanus); fruit baccate or drupaceous; seed coat thin, (exotesta sclereidal, some cells spiny, groups of sclereidal cells at both ends - Sararanga); (endosperm starchy); n = 25, 28, 30; hypocotyl long [Freycinetia], primary root branched [Pandanus].
5 [list]/885 (982): Pandanus (650), Freycinetia (180), Benstonea (50). W. Africa to the Pacific (map: see Heywood (1978: Africa); Callmander et al. 2003). [Photos - Staminate Flower, Carpellate Flower.]
Age. Crown group Pandanaceae began to diverge ca 49 m.y.a. (Buerki et al. 2017), ca 51 m.y.a. (Janssen & Bremer 2004), (101-)65, 58(-38.3) m.y.a. (Gallaher et al. 2014), or 95 m.y.a. or more (Callmander et al. 2003).
The pollen genus Pandaniidites is known from North America where it spans the Cretaceous-Caenozoic boundary and has been found in rocks up to 70 m.y. old (Hotton et al. 1994). However, since Pandaniidites is associated with flowers of Limnobiophyllum it is to be assigned to Araceae-Lemnoideae (Stockey et al. 1997; Stockey 2006), not Pandanaceae. Fossils of Pandanus around 80 m.y.a. are reported from Austria (Kvacek & Herman 2004), but Gallaher et al. (2014) are sceptical of the identity of most other fossils attributed to the family.
Evolution: Divergence & Distribution. Callmander et al. (2003) discussed the biogeography of the family in the context of the Gondwanan break-up, which sets up rather discordant estimates for the age of the family (see above). However, Gallaher et al. (2014) present revised age estimates and suggest that dispersal is more likely to explain the Gondwanan elements of current distributions in the family, indeed, given the Laurasian fossils of the family, they thought that Pandanaceae might even originate there. Diversification within the speciose Pandanus itself started a mere (20.2-)12.9, 11.5(-5.4) m.y.a., and water dispersal in particular is discussd as facilitating the current wide distribution of the genus, with the Pandanus tectorius complex achieving the range of almost the entire family within the last 6 m.y. (Gallaher et al. 2014). Buerki et al. (2017) discuss the evolution of Benstonea which may have begun on Borneo.
Ecology & Physiology. Freycinetia is a sizeable clade of woody root climbers in the Old World. A number of species of Pandanus are trees, sometimes moderate in size, and they have massive unbranched "adventitious" prop roots.
Pollination Biology & Seed Dispersal. Bat pollination may be quite common (Fleming et al. 2009), and polliantion by birds and other animals also occurs (Cox 1990), while at least some species of Pandanus are wind pollinated (and apomictic) (Cox 1990). The development of staminate and carpellate flowers seems to be quite labile in Freycinetia, and sex changes of plants have been recorded (Huynh 1992 and literature; Cox 1990 for breeding systems).
For diaspore dispersal in Pandanaceae, predominantly by water or animals, see Gallaher et al. (2014).
Chemistry, Morphology, etc. Although the leaves of Sararanga in branches developing after the first inflorescence has been produced are described as being two ranked, both North and Willis (1971) and Cox (1990) illustrate them as being decussate, Cox (1990: p. 821) noting "each successive node produc[es] a pair of opposite leaves".
Since there is ususally no perianth, the position of the ovary is difficult to ascertain, but it is clearly superior in some species of Freycinetia (e.g. Huynh 1991, 1992) at least. Cox (1990) shows staminate flowers of F. arborea as having bracts and six perianth primordia, while North and Willis (1971) described both staminate and carpellate flowers of Sararanga as having an entire perianth or cupule (Cox 1990 is less sanguine about its morphological nature). The carpels vary from free to variously connate and fasciate, and they may face ad- or abaxially (c.f. Cercidiphyllum), sometimes within a single floral unit (Stone 1968). The stigmas of Sararanga are sessile and in two sinuous lines, and North and Willis (1971) described the fruits as being polypyrenoid drupes, although they talked about flattened seeds with a one-layered sclereidal testa. Fagerlind (1940a) suggested that Pandanus did not always have a bisporic embryo sac. The embryo sac of Pandanus appears to have extra antipodal cells, however, these come from the nucellus (see Maheshwari 1955 for discussion).
Some information is taken from Dahlgren et al. (1985) and Stone et al. (1998), both general, see also Zimmermann et al. (1974: vascular organization in the stem), Strömberg (1956) and Cheah and Stone (1975), both embryology, Hotton et al. (1994: pollen), and Huynh (2001: Sararanga).
Phylogeny. For early studies on the phylogeny of the family, see Stevenson and Loconte (1995) and Cox et al. (1995). Callmander et al. (2003) did not show the full tree they obtained, albeit it was apparently poorly resolved. In a tree with more limited taxonomic but greater gene sampling, relationships were [Pandanus [Martellidendron, Freycinetia, Sararanga]] (Callmander et al. 2003). Buerki et al. (2012b: sampling extensive) found the well-supported set of relationships [Sararanga [Freycinetia [Acrostigma clade (later = Benstonea), core Pandanus, Martellidendron]], and these were similar in Gallaher et al. (2014), although there was little support for Benstonea as sister to Pandanus in the chloroplast data alone. Buerki et al. (2017) recoverd the relationships [Saraanga [Freycinetia [Martellidendron [Benstonea + Pandanus]]]], with moderate to good support. However, Nadaf and Zanan (2012: Indian species the focus) recovered the relationships [[Benstonea + Pandanus] [Sararanga [Freycinetia + Martellidendron]]].
Classification. Callmander et al. (2003, 2012) have divided the large genus Pandanus; the segregates can be identified only with fertile material, sometimes pistillate alone...
Botanical Trivia. Gill and Tomlinson (1975) note that the apices of aerial roots of Pandanus may be up to 11 cm in diameter.
Synonymy: Freycinetiaceae Le Maout & Decaisne
CYCLANTHACEAE A. Richard, nom. cons. Back to Pandanales
Large herbs; vascular tracheids or vessels [?type] in root and leaf; petiole bundles scattered; mucilage cells +; leaves spirally two-ranked, petiolate, blade vernation plicate or variants, bi-or tricostate, veins extend to the end of the leaf, Vorläuferspitze 0 [in elaborated leaves], petiole ± terete; plant monoecious; inflorescence (branched), spadiciform; flowers with mucilage canals; staminate flowers: A connate basally; pollen lacking endexine lamellae; carpellate flowers: ovules many/carpel, (epitropous), micropyle bistomal, outer integument 3-5 cells across, parietal tissue none, nucellar epidermal cells radially elongated, hypostase + (0), (postament +); endosperm helobial, embryo short; collar rhizoids +.
12 [list]/225: Two subfamilies below. Central and tropical South America (map: from Harling 1958; fossil Cyclanthus [blue] from Smith et al. 2009).
Age. Crown group Cyclanthaceae are dated to (55-)49, 45(-39) m.y.a. (Wikström et al. 2001), ca 77 m.y.a. (Janssen & Bremer 2004), (50-)33, 30(-14) m.y. (Bell et al. 2010), and (72.7-)45, 42.3(-22.9) m.y. (Gallaher et al. 2014).
Cyclanthus has quite recently been identified from the European Eocene sediments ca 47 m.y.o.; the seeds had previously been misidentified as Scirpus (Smith et al. 2008; see also Collinson et al. 2012; Smith 2013; Isles et al. 2015). If correct, this questions some of the ages that have been suggested for the family.
1. Cyclanthoideae Burnett
(Growth monopodial); root with multiseriate circum-cortical sclerenchymatous tissue; subepidermal sclereids +; druses +, mucilage cells in inflorescence only, tanniniferous cells 0, non-articulated laticifers +; lysigenous air spaces with transverse septae +; leaf blade deeply bifid [by tearing of tissues], otherwise entire, bicostate, vernation modified plicate [plicate across principal veins]; inflorescence with whorls of staminate and carpellate "flowers", flowers coalescent; staminate flowers: P 0; A in 4 rows per whorl; carpellate flowers: P +, small; staminodes +; G, ovary cavity with closely-set placentae; outer integument ca 2 cells across, inner integument ca 3 cells across, nucellar cap 0, funicles long [longer than embryo sac]; embryo sac with chalazal prolongation, fruit dry, syncarpous, carpellary annulus sliding off the inflorescence axis and splitting down the middle; seeds ridged, embedded in mucilage; endotestal cells palisade, inner periclinal walls granular; n = 9.
1/1: Cyclanthus bipartitus. Central and N. South America, the Lesser Antilles. [Photo - Flower.]
2. Carludovicoideae Harling
Also epiphytes, and/or lianes and vines; root (with multiseriate circum-cortical sclerenchymatous tissue - Schultesiophytum), (not medullated, centre portion occupied by intermixed xylem and phloem); (stem cork subepidermal or outer cortical); (styloids +); mucilage and tanniniferous cells +; leaves (spiral), blade ± bilolobed or 3-partite, 2-3-costate [lateral costae short], apex usu. deeply dissected, (blade entire, 1-costate, margins entire), (hastula +); inflorescences (axillary); staminate flowers: (monosymmetric); P (0-)10-many, small [?= staminodia], glandular abaxially; A ca 10-many, filaments swollen basally; carpellate flowers: connate basally, 4(-8)-merous; staminodes long-filiform, opposite P; G 4, ± inferior, alternating with P, (placentae apical); outer integument ca 3 cells across, inner integument ca 2 cells across, nucellar cap 2-3 cells across; fruit baccate, syncarpous or not, apically circumscissile or with other unusual methods of opening; (seeds exotegmic); (endosperm starchy); n = 9, 15, 16.
11/225: Asplundia (100), Dicranopygium (50), Sphaeradenia (50). Central and tropical South America, the Greater Antilles. [Photo - Flower, Fruit.]
Evolution: Divergence & Distribution. The discovery of Cyclanthus in the European Eocene (Smith et al. 2008; see also Collinson et al. 2012; Smith 2013) changes how one thinks of the evolution and distribution of the family. Cyclanthus is common there and may even be a diagnostic element of the vegetation - along with Nypa.
Pollination Biology & Seed Dispersal. Carludovicia is associated with derelomine flower weevils the adults of which pollinate the flowers while the larvae eat the developing seeds (Franz 2004). Indeed, weevils are commonly associated with inflorescences of Carludovicioideae, and their larvae may also eat the staminate flowers; Cyclanthus is pollinated by cyclocephaline scarabeid beetles (Eriksson 1994a; Moore & Jameson 2013). Thermogenesis is reported from flowers of Carludovicioideae, and the long staminodes produce scent (Eriksson 1994a).
The fruits of Carludovicioideae are baccate, syncarpous or not, and are apically circumscissile or have other unusual methods of opening. For example, the subfleshy infructescences of genera like Carludovica open irregularly from the apex as the outer part of the infructescence (the apical parts of the connate gynoecia) recurves and pulls away, exposing the brightly-coloured interior. Dispersal is by animals.
Chemistry, Morphology, etc. Leaf development is rather like that of broad-leaved angiosperms, a Vorläuferspitze was evident only in leaves of Carludovica palmata developing early in the ontogenetic sequence (Wilder 1976, 1981a). Leaf insertion can change from spiral to two-ranked or two-ranked to spiral during the growth of the plant (Wilder 1981a). Further information on the morphology and vernation of leaves is given by Wilder (1981b) and on growth habit by Wilder (1992b).
In staminate flowers, both perianth and stamen number may increase. There are varying interpretations of the staminate flowers of P in one (two) whorls, 6+ (-30), with abaxial glands, or P 0, staminodia abaxial, glandular (Sajo et al. 2014). The gynoecium/carpellate flowers of Cyclanthus are shown as having the gynoecium immediately surrounded by staminodes and then by perianth lobes; stamens/staminate flowers alternate with the gynoecium (Sajo et al. 2014). There is considerable variation in pollen morphology and seed morphology and anatomy; Furness and Rudall (2006) suggest that the pollen grains of Cyclanthaceae, alone in the order, lack endexine lamellae.
For much information on just about everything, see Harling (1958) and Harling et al. (1998), for anatomy, see Tomlinson and Wilder (1984) and Wilder (1986, 1992a and references), for embryology, see Harling (1946), and for seeds of Cyclanthus, see Smith et al. (2008).
Phylogeny. For a detailed morphological phylogeny of the family, see Eriksson (1994b).