EMBRYOPSIDA Pirani & Prado

Gametophyte dominant, independent, multicellular, not motile, initially ±globular; showing gravitropism; acquisition of phenylalanine lysase [PAL], microbial terpene synthase-like genes +, phenylpropanoid metabolism [lignans +, flavonoids + (absorbtion of UV radiation)], 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, 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, sporopollenin + laid down in association with trilamellar layers [white-line centred lamellae; tripartite lamellae], >1000 spores/sporangium; nuclear genome size <1.4 pg, main telomere sequence motif TTTAGGG, LEAFY and KNOX1 and KNOX2 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.

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; sporophyte with polar transport of auxins, 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].


Sporophyte 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]; (condensed or nonhydrolyzable tannins/proanthocyanidins +); xyloglucans with side chains uncharged [?level], in secondary walls of vascular and mechanical tissue; lignins +; stem apex multicellular, with cytohistochemical zonation, plasmodesmata formation based on cell lineage; tracheids +, in both protoxylem and metaxylem, G- and S-types; sieve cells + [nucleus degenerating]; endodermis +; 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; suspensor +, shoot apex developing away from micropyle/archegonial neck [from hypobasal cell, endoscopic], root lateral with respect to the longitudinal axis of the embryo [plant homorhizic].


Sporophyte endomycorrhizal [with Glomeromycota]; growth ± monopodial, branching spiral; roots +, endogenous, positively geotropic, root hairs and root cap +, protoxylem exarch, 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; 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].


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].


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.


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 apical meristem intermediate-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 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; P +, ?insertion, members each with a single trace, outer members not sharply differentiated from the others, not enclosing the floral bud; A many, filament not sharply distinguished from anther, stout, broad, with a single trace, anther introrse, tetrasporangiate, sporangia in two groups of two [dithecal], 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, 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, not photosynthesising, 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 land on stigma, bicellular at dispersal, mature male gametophyte tricellular, germinating in less than 3 hours, pollen tube elongated, unbranched, growing 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 gametes lacking cell walls, ciliae 0, siphonogamy; double fertilization +, ovules aborting unless fertilized; P deciduous in fruit; mature seed much larger than fertilized ovule, small [], dry [no sarcotesta], exotestal; endosperm +, 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 very small [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]; tectum reticulate; anther wall with outer secondary parietal cell layer dividing; 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).

[CERATOPHYLLALES + EUDICOTS]: ethereal oils 0.

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

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

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

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

CORE EUDICOTS / GUNNERIDAE: (ellagic and gallic acids +); leaf margins serrate; compitum + [one position]; micropyle?; γ whole nuclear genome duplication [palaeohexaploidy, gamma triplication], PI-dB motif +, small deletion in the 18S ribosomal DNA common.

[ROSIDS ET AL. + ASTERIDS ET AL.] / PENTAPETALAE: root apical meristem closed; (cyanogenesis also via [iso]leucine, valine and phenylalanine pathways); flowers rather stereotyped: 5-merous, parts whorled; P = calyx + corolla, the calyx enclosing the flower in bud, sepals with three or more traces, petals with a single trace; stamens = 2x K/C, in two whorls, internal/adaxial to the corolla whorl, alternating, (numerous, but then usually fasciculate and/or centrifugal); pollen tricolporate; G [5], G [3] also common, when [G 2], carpels superposed, placentation axile, style +, stigma not decurrent; compitum +; endosperm nuclear; fruit dry, dehiscent, loculicidal [when a capsule]; RNase-based gametophytic incompatibility system present; floral nectaries with CRABSCLAW expression; (monosymmetric flowers with adaxial/dorsal CYC expression).

[DILLENIALES [SAXIFRAGALES [VITALES + ROSIDS s. str.]]]: stipules + [usually apparently inserted on the stem].


[VITALES + ROSIDS] / ROSIDAE: anthers ± dorsifixed, transition to filament narrow, connective thin.


ROSIDS: (mucilage cells with thickened inner periclinal walls and distinct cytoplasm); if nectary +, usu. receptacular; embryo long; chloroplast infA gene defunct, mitochondrial coxII.i3 intron 0.

ROSID I / FABIDAE / [ZYGOPHYLLALES [the COM clade + the nitrogen-fixing clade]]: endosperm scanty.

[the COM clade + the nitrogen-fixing clade]: ?

[FABALES [ROSALES [CUCURBITALES + FAGALES]]] / the nitrogen-fixing clade / fabids: (N-fixing by associated root-dwelling bacteria); tension wood +; seed exotestal.

[ROSALES [CUCURBITALES + FAGALES]]: ovules 1-2/carpel, apical.

[CUCURBITALES + FAGALES]: P parts similar; ovary inferior; fruit 1-seeded, indehiscent.

Age. The age for this node has been estimated at (107-)103(-99) or (92-)88(-84) m.y., with some estimates slightly older, to 109 m.y. (H. Wang et al. 2009; see also Foster et al. 2016a); Wikström et al. (2001) calibrated their tree on an age of ca 84 m.y. for this node, while Magallón and Castillo (2009) estimated an age of ca 102.4 m.y. (see also Lohmann et al. 2015), Bell et al. (2010) an age of (110-)96 m.y.; (125.4-)124.5(-121.1) m.y. is the age in Xiang et al. (2014), 125-98 m.y.a. in Xing et al. (2014), around 117 m.y. in Z. Wu et al. (2014) and ca 104.4 or 73.4 m.y. in Tank et al. (2015: Table S1, S2). An age of 389-181 m.y. was suggested by Jeong et al. (1999) while almost the opposite extreme is the age of ca 89.7 m.y. in Naumann et al. (2013).

Evolution: Divergence & Distribution. Imperfect flowers pervade the two orders. However, flower type varies considerably in Anisophylleaceae, with perfect flowers occurring in Combretocarpus, as well as in fossils placed in href="../orders/fagalesweb.htm#Fagales">Fagales) and a few extant members of that order, so there may have been reversals of this character, or imperfect flowers have evolved more than once. "Embryo with large cotyledons" may be another synapomorphy (Zhang et al. 2006), also a three-carpellate gynoecium. However, ovary position and fruit characters in particular reverse spectacularly in this clade (see also Matthews & Endress 2004; Zhang et al. 2006), although Endress (2011a) thought that an inferior ovary might be a key innovation somewhere around here. See also Taylor et al. (2012) for additional possible apomorphies.

Phylogeny. For relationships, see above.

CUCURBITALES Berchtold & J. Presl  Main Tree.

(Frankia infection +, mechanism unclear); ellagic acid ?; storied fusiform cambial initials; perforation plates not or minimally bordered; tension wood?; rays wide, multiseriate; cuticle wax crystalloids 0; leaves spiral; K or P valvate, stomata on K/P raised, the two whorls rather similar in texture; styluli +, (ovary with a roof, styluli often marginal); ovule with bistomal micropyle; codon changes [see Filipowicz & Renner 2010]. - 7 families, 129 genera, 2,320 species.

Age. The age suggested by H. Wang et al. (2009) for this node was (85-)80, 78(-73) m.y. (two penalized likelihood dates), while Bayesian relaxed clock estimates were slightly older, to 90 m.y.a.; (103.3-)86.9, 86.2(-71.3) m.y. are the ages suggested by H.-L. Li et al. (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. It is unclear where some of the features suggested by Filipowicz and Renner (2010) as being apomorphies of the order should be placed on the tree. Some, such as inferior ovary, are likely to characterize the [Cucurbitales + Fagales] clade, others, such as breeding system, are very labile and are perhaps more likely to characterize a clade within Cucurbitales. Zhang et al. (2006) also discuss aspects of morphological evolution and evaluate the extensive variation in breeding system in the clade.

Ecology & Physiology. For nitrogen fixation by Frankia, see elsewhere.

Pollination Biology & Seed Dispersal. Zhang and Renner (2003) suggested that the flowers are usually imperfect, but perfect flowers are known from Anisophylleaceae. Indeed, breeding systems vary considerably in Cucurbitales. Schaefer and Renner (2010) suggested that even within Momordica (Cucurbitaceae) there have been perhaps seven reversals from dioecy to monoecy - in a clade that is very approximately 35 m.y. old, while Bertin and Newman (1993) and Routley et al. (2004) note various kinds of dichogamy in the order.

Plant-Animal Interactions. Butterfly caterpillars appear to be relatively uncommon on members of the order.

Chemistry, Morphology, etc. Cuticle waxes are usually not well developed. Possession of libriform fibres and slightly oblique end walls of vessel elements may be synapomorphies (Wagstaff & Dawson 2000, see also data in Nandi et al. 1998), as may banded wood parenchyma (Baas et al. 2000), homogeneous rays, and the possession of bitter compounds. Stipules are not placed as a synapomorphy of the order, although the data presented by Matthews and Endress (2004) might suggest that this was an option. However, not only does the morphology of the stipules in Anisophylleaceae and Corynocarpaceae need clarification, but the presence of stipules may be a synapomorphy at a much higher level (see rosids et al. above). Polarity of the character of leaf venation is unclear, since Combretocarpus is sister to other Anisophylleaceae and Corynocarpaceae are sister to Coriariaceae; the first member of both pairs has pinnate venation, and the two clades are successively basal to the rest of the order.

More or less lacinate petals (and staminodes) are common in the order (Endress & Matthews 2006b). The thickness of the outer integument varies considerably. Matthews and Endress (2004, summarized in 2006b) provide an excellent survey of floral morphology of the group.

Phylogeny. For the circumscription of the clade see e.g. Setoguchi et al. (1999) and Schwarzbach and Ricklefs (2000); there is now general agreement as to what it contains. Coriariaceae and Corynocarpaceae are consistently recognized as sister taxa, and their very similar wood anatomy is consistent with such a position (Carlquist & Miller 2001). However, other relationships remained poorly understood (Brouillet 2001 for some comments), and although Zhang and Renner (2003a), using a variety of both chloroplast and nuclear genes, suggested that Anisophylleaceae were sister to the rest of Cucurbitales, H.-L. Li et al. (2015) found the clade [Anisophylleaceae + Cucurbitaceae], but its position had little support (c.f. H.-L. Li et al. 2016). Zhang et al. (2006) in a nine-gene study (all three compartments) confirmed these relationships and also placed Cucurbitaceae as sister to a [Tetramelaceae + Datiscaceae + Begoniaceae] clade, although relationships within this latter group were still not entirely clear. The clade [Datiscaceae + Begoniaceae] had at best only moderate support (Zhang et al. 2006; see also Schaefer et al. 2009; Schaefer & Renner 2011b), but this topology is followed here - c.f. Soltis et al. (2007a) and Bell et al. (2010). For possible relationships between Tetramelaceae and Datiscaceae, see Swensen et al. (1994, 1998) and H.-L. Li et al. (2015: support low); this family pair was also recovered by M. Sun et al. (2016), but most of the relationships there had little support.

The relationships of the holoparasitic Apodanthaceae were for some time unclear (e.g. they are unplaced in A.P.G. 2009). Nickrent et al. (2004) suggested a place either within Malvales (especially the three-gene analyses and that of nuclear SSU rDNA), or in or near Cucurbitales (analysis of matR), but inclined to the former position. Barkman et al. (2007: support weak, but rather comprehensive analysis) also suggested the latter position; the mitochondral genes cox1 and matR showed massive divergence, but not the atp1 gene (Barkman et al. 2007). Additional molecular analyses (D. Nickrent, pers. comm.; esp. Filipowicz & Renner 2010) support the position of Apodanthaceae in Cucurbitales. This is consistent with their dioecy, extrose anthers, inferior ovary and parietal placentation, all features common in Cucurbitales (see also Filipowicz & Renner 2010), but all these features are generally common in parasitic plants (Renner & Ricklefs 1995). There are also a number of codon subsitutions in common between Apodanthaceae and Cucurbitales (Barkman et al. 2007; Filipowicz & Renner 2010). The exact position of the family in Cucurbitales remains unclear, the relationships suggested with the morphologically rather different (but apomorphically so) Corynocarpaceae and Coriariaceae being only weakly supported, and Apodanthaceae are on a very long branch (Filipowicz & Renner 2010; see also M. Sun et al. 2016). The situation remained the same in Bellot and Renner (2014b), and in trees used when estimating substitiution rates Apodanthaceae linked either with a clade [Anisophylleaceae + Corynocarpaceae] or a clade including the whole of the rest of the family, but with a rather different topology to that used here; other topologies were also obtained, although none with strong support.

Previous Relationships. Cucurbitales are another rather unexpected assemblage of families. Coriariaceae have often been placed with families that have separate carpels and so were thought to be "primitive". Rhizophoraceae and Anisophylleaceae were often associated in the twentieth century, e.g. being placed in separate but adjacent orders, as in Takhtajan (1997), or even in the same family. However, although both were placed in Rosidae by Cronquist (1981), they were not adjacent. Indeed, morphological differences between the two are marked (e.g. Juncosa and Tomlinson 1988; Tomlinson 1988), and Rhizophoraceae are now securely placed in Malpighiales where they are sister to Erythroxylaceae; the two have much in common. Apodanthaceae have often been included in Rafflesiaceae s.l.

Similarities in floral morphology between Anisophyllea and Ceratopetalum (Oxalidales-Cunoniaceae: see Matthews et al. 2001; Endress & Matthews 2006b), although striking, are unlikely to be evidence of immediate close relationships of the two, even although the fossil Platydiscus peltatus seems to suggest similar relationships (Schönenberger et al. 2001a; see also Schönenberger & von Balthazar 2006); it was included in a study of Oxalidales by Heibl and Renner (2012).

Includes Anisophylleaceae, Apodanthaceae, Begoniaceae, Coriariaceae, Corynocarpaceae, Cucurbitaceae, Datiscaceae, Tetramelaceae.

Synonymy: Anisophylleales Reveal & Doweld, Begoniales Link, Coriariales Lindley, Corynocarpales Takhtajan, Datiscales Dumortier - Begonianae Doweld, Corynocarpanae Takhtajan, Cucurbitanae Reveal - Coriariopsida Parlatore, Cucurbitopsida Brongniart

ANISOPHYLLEACEAE Ridley   Back to Cucurbitales


Trees and shrubs; plants Al-accumulators; cork?; cambium storying?; nodes 1:1; cuticle waxes as platelets; stomata usu. paracytic; serial [superposed] axillary buds; branching from current growth, rythmic; lamina margins entire, secondary veins pinnate, (stipules 2-4, minute, at the very base of the petiole [= colleters?]); inflorescence branched, racemose or spicate; flowers small; K epidermis with mucilaginous inner walls, postgenitally coherent, C open (0), lobed or laciniate (entire), bundle number?, ± enclosing groups of A; A 2x K, obdiplostemonous, incurved in bud; nectary of separate lobes; G (stylulus hollow), compitum 0, stigma expanded or punctate; ovules often unitegmic, epitropous, outer integument 7-9 cells across, parietal tissue 1(?+) cells across, nucellar cap +; fruit 1-seeded, K persistent; embryo fusiform, largely hypocotylar; n = 7, 8; germination hypogeal.

4[list]/71: Anisophyllea (67). Pantropical (map: see Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003, 6. 2011; Clement et al. 2004). [Photo - Anisophyllea Fruit]

Age. Crown-group diversification in Anisophylleaceae may have begun (107-)85(-67) m.y.a. (Zhang et al. 2007).

1. Combretocarpus Bentham & J. D. Hooker

Indumentum lepidote [on flowers]; lamina with secondary veins pinnate; flowers perfect, 3(-4) merous; embryo sac sac bisporic [chalazal dyad], eight-celled [Allium-type]; fruit 3(-4) longitudinally winged; cotyledons small.

1/1: Combretocarpus rotundus. Malesia: Malay Peninsula to Borneo.

2. Anisophylleae Bentham & Hooker

(Cuticle waxes beaker-like - Polygonanthus); anisophyllous, leaves appearing 2-ranked, alternate leaves very much reduced, lamina base asymmetric, (secondary veins palmate); plant monoecious (flowers perfect); flowers 4(-5) merous; nectary lobes also interstaminal; (roof over ovary, styluli marginal - Anisophyllea); (filaments very short); ovule 1/carpel; fruit a drupe, (4-seeded), (K large, wing-like - Polygonanthus); testa multiplicative, 10-30 cells across, (vascularized), (mesotesta also lignified); cotyledons indistinct.

3/70: Anisophyllea (67). Pantropical, not E. Malesia to the Pacific.

Synonymy: Polygonanthaceae Croizat

Chemistry, Morphology, etc. Vincent and Tomlinson (1983) discussed the distinctive vegetative architecture of Anisophyllea, while Dengler et al. (1989) looked at the primary vascular organization of the orthotropic and plagiotropic shoots - quite different.

The staminate flowers of Anisophyllea disticha appear to have a semi-superior ovary with central styluli while the carpellate flowers have an inferior ovary, there is a roof on the ovary and the styluli are submarginal (Ruth Crevel, in Ding Hou 1858).

For further information, see Dahlgren (1988), Schwarzbach and Tomlinson (2011) and Chen et al. (2015), all general, Schönenberger et al. (2001a: fossils), Tobe and Raven (1987e, 1988a, c: floral morphology, embryology, fruit), and Matthews et al. (2004: floral development).

Phylogeny. Combretocarpus is sister to the rest of the family (Zhang et al. 2007), somewhat in conflict with morphology-based relationships (e.g. Tobe & Raven 1987c, 1988c); this may have an important effect on the polarity of characters in the family or even the order as a whole. However, M. Sun et al. (2016) recovered the groupings [Combretocarpus + Polygonanthus] [Poga + Anisophyllea.

Previous Relationships. Anisophylleaceae were often linked with or included in Rhizophoraceae (Malpighiales: see above). However, the inner integument is ca 2 cell layers thick, there are no laticifers, the petals are not aristate, and a sclerified exotegmen is absent; in these and many other characters Anisophylleaceae differ from Rhizophoraceae (see Juncosa & Tomlinson 1988a, b).

[[Corynocarpaceae + Coriariaceae] [Cucurbitaceae [Tetramelaceae [Datiscaceae + Begoniaceae]]]]: uniseriate rays 0; lamina with secondary veins palmate; filaments shorter than anthers in bud, anthers basifixed; nectaries 0 .

Age. Magallón and Castillo (2009) gave an age of ca 86.7 m.y. for this node, Tank et al. (2015: Table S2) an age of around 71.8 m.y., and Bell et al. (2010) an age of (78-)67, 61(-48) m. years. Wikström et al. (2001: c.f. topology) estimated an age of (68-)66, 65(-63) m.y..

[Corynocarpaceae + Coriariaceae]: ellagic acid +; wood with broad rays; sieve tube plastids lacking both starch and protein inclusions; stomata paracytic; lamina margin entire; flowers small, K quincuncial; C thick, base broad; G superior, ascidiate; compitum 0; ovule 1/carpel, outer integument vascularized; cotyledons very large.

Age. Wikström et al. (2001) suggested that this node was (55-)52, 48(-45) m.y.o. and Bell et al. (2010) that it was (64-)49, 43(-29) m.y.o.; (79.5-)65.7, 41.4(-10.2) m.y. is the rather broad spread in H.-L. Li et al. (2015), but they preferred the older ages.

Chemistry, Morphology, etc. For sieve tube plastids, see Behnke (1981c), for compitum presemce/absence, see Armbruster et al. (2002).

CORYNOCARPACEAE Engler, nom. cons.   Back to Cucurbitales


Trees; young stem with separate bundles; petiole bundles in a line; lamina vernation conduplicate, secondary veins pinnate, stipule single, intrapetiolar; inflorescence paniculate; calyx and corolla distinct; stamens = opposite and basally adnate to C, incurved in bud, staminodes 5, fringed, petal-like, opposite sepals, nectary basal, adaxial; pollen heteropolar, dicolpate, psilate, exine infratectum granular; G [2], transverse?, only 1 fertile, stylulus short, usu. single, conduplicate, stigma capitate, dry; ovule with outer integument ca 11[?-30] layers across; fruit a drupe, seed one, stylulus excentric; seeds large; seed coat ?pachychalazal, initially thick, vascularized, becoming crushed; endosperm starchy; n = 22, 23.

1[list]/6. New Guinea to New Zealand, introduced on Hawaii (map: from van Steenis & van Balgooy 1966; Fl. Austral. 8. 1984). [Photo - Flower] [Photo - Fruit]

Chemistry, Morphology, etc. The cork develops from the cell layer beneath the epidermis. It is perhaps unclear whether the gynoecium is pseudomonomerous or unicarpellate. However, since some flowers have two styluli (e.g. Matthews & Endress 2004), the single, excentrically-placed structure at the apex of the gynoecium is called a stylulus and the gynoecium is pseudomonomerous {sic]. The seeds are very poisonous, having bitter glucosides.

Some information is taken from Hemsley (1903: general), Nowicke and Skvarla (1983: pollen), Philipson (1987a: general), and Kubitzki (2011: general).

Previous Relationships. Corynocarpaceae were Celastralean in affinity according to Cronquist (1981), isolated, according to Takhtajan (1997), so here they are!

CORIARIACEAE Candolle, nom. cons.   Back to Cucurbitales


Usu. shrubs; roots with N-fixing Frankia; coriolic fatty acid [CH3(CH2)4CH(OH)CH=CHCH=CH(CH2)7COOH] in seed, sesquiterpenes, myricetin +; vessels in multiples, perforation plates bordered, true tracheids +, wood parenchyma (confluent) vasicentric; nodes 1:1; petiole bundle arcuate; buds usu. perulate; leaves opposite, lamina vernation ± flat, stipules small; plant polygamous or flowers perfect, inflorescences racemes; flowers often protogynous, (6-merous), bracteoles 0; K quincuncial, C open, fleshy, often keeled adaxially; A 10, connective thin, septum between sporangia of theca not developed; tapetal cells 2-4-nucleate; pollen (2 colpate), starchy, (3-nucleate); G [5], opposite K, [(10)], stylulus slender, stigmatic all around, stigma dry; ovule apotropous, micropyle endostomal, outer integument 3-4 cells across, inner integument 2-3 cells across, parietal tissue ca 8 cells across, nucellar cap ca 4 cells across; fruitlets achenes [nutlets], several, surrounded by fleshy accrescent C; exotesta of cuboid, "tanniniferous", thick-walled, lignified(?) cells, rest undistinguished; n = 10, 15.

1[list]/5. Very disjunct: circum S. Pacific to China and Himalayas, Mediterranean (map: from van Steenis & van Balgooy 1966; Good 1974). [Photo - Inflorescence] [Photo - Fruit.]

Age. Molecular estimates of the age of crown-group Coriariaceae are around 69-63 m.y. (Yokoyama et al. 2000).

Fossils of Coriaria are known from about 33 m.y.a. (Saporta 1965).

Evolution: Divergence & Distribution. Biogeographic relationships within the family can be summarized as [Eurasia [[S. and W. Pacific + Central and N. South America]] (Yokoyama et al. 2000).

Chemistry, Morphology, etc. Although the carpels seem to be separate, a compitum appears to be developed (Matthews & Endress 2004). There is but a single seed per carpel, but several seeds are produced by each flower.

Information on nodal anatomy is taken from Sinnott (1914), on embryology from Sharma (1968a), and on wood anatomy from Yoda and Suzuki (1992). For gynoecial development, see Guédès (1971), and for general information, see Kubitzki et al. (2011).

Phylogeny. For phylogenetic relationships within the family, see Yokoyama et al. (2000).

Previous relationships. Coriariaceae were placed in Ranunculales by Cronquist (1981) and as a monotypic Coriariales in Rosidae (Takhtajan 1997), largely because of their apparently separate carpels.

[Cucurbitaceae [Tetramelaceae [Datiscaceae + Begoniaceae]]]: perennial herbs; cucurbitacins [triterpenes] +, myricetin, ellagic acid 0; young stem with separate bundles; leaves with teeth, medial vein ending in a pad of packed translucent cells, lateral also entering [in Begonia lateral is dominant], stipules 0; flowers imperfect; G opposite sepals or median member adaxial, placentation parietal, a roof over the ovary, so styluli marginal, stigmas large, elongated, bilobed; ovules many/carpel; seeds many/fruit.

Age. The age of this node has been estimated as (74-)62, 56(-43) m.y. (Bell et al. 2010), ca 71.1 or 69 m.y. (Tank et al. 2015: Table S1, S2), (83-)81(-79) m.y. (Schaefer et al. 2009), or ca 57 m.y.a. (Naumann et al. 2013).

Chemistry, Morphology, etc. For information on leaf teeth, see Hickey and Wolfe (1975). The development of a roof over the ovary formed from tissue adaxial to the stylulus (Matthews & Endress 2004) is obvious when well developed; the styluli are then widely separate and borne towards the margin of the ovary. Matthews and Endress (2006) note details of ovule morphology that this group has in common.

CUCURBITACEAE Jussieu, nom. cons.   Back to Cucurbitales


Climbers, tendrils axillary, ± lateral, bifid (unbranched), both branches and stem of tendril coiling [= zanonioid tendril]; (Si02 accumulation); alkaloids, bitter tetra- and pentacyclic triterpenoids, punicic acid [C18H30O2], non-protein amino acid citrullin [α-amino-delta-ureidopentanoic acid], saponins +, little oxalate accumulation, tannins 0; phloem loading via intermediary cells [specialized companion cells with numerous plasmodesmata, raffinose etc. involved]; root cork superficial; stem cork variable in position; cambium storying?; extra-fascicular phloem +; vascular bundles initially in two rings [outer opposite the angles of the stem]; rays multiseriate; outer collenchyma and sclerenchymatous sheath in cortex; petiole bundle arcuate, or ring of arcuate bundles; no pericyclic sheath; (cuticle waxes as platelets); indumentum rough hairy/prickly, walls calcified, cystoliths + (0), hairs often glandular; leaves often with extrafloral nectaries, (lamina margins entire); plants (dioecious) monoecious, inflorescences axillary; interfloral protogyny, flowers ebracteolate or not, (3-)5(-7)-merous; hypanthium + (0; tube formed by K and C alone), short, K often connate, open, (0), C (induplicate-)valvate, connate; staminate flowers: nectary type?; A extrorse, anthers monothecal; pollen grains prolate, to 40 µm long, (micro)striate, starchy; pistillode 0; carpellate flowers: staminodes +; G 1 [(2) 3(-5)], inferior, (median member abaxial), placentae intrusive, stigmas dry or wet, (channelled; not bilobed); ovules pendulous or horizontal, outer integument 6-15+ cells across, parietal tissue 5-11 cells across; seeds flattened (not), pitted or not, testa multiplicative, complex, tegmen ± persistent, outer cells ± tracheidal; endosperm 0, chalazal haustorium + (0), cotyledons large, flat; germination epigeal (hypogeal - Momordica, etc.), seedlings with a peg [cortical outgrowth at the root-shoot transition].

98[list]/1,000 - five groups below. Largely tropical and subtropical, especially drier parts of Africa (map: from Heywood 1978 [N. part of range]; Saade 1998; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003, 6. 2011; Florabase 2006). [Photos - Collection, Staminate flower, Carpellate flower, Fruit.]

Age. The crown-group age of Cucurbitaceae may be (66-)63(-60) m.y. (Schaefer et al. 2009).

"Fevilleoideae" Burnett is to be disposed of and the characters below to be integrated with the first few tribes as recognised by Schaefer and Renner (2011b).

Axillary bud also present; hypodermal tissue ± thick-walled and lignified, inner sclerenchymatous layer several cells across, brachysclereidal, thickened, arenchyma with banded thickenings, inner layer +.

[Gomphogyneae [Triceratieae + Zanonieae]]: ?

Age. The age of this node - if it exists - is some (62-)59(-56) m.y. (Schaefer et al. 2009).

1. Gomphogyneae Bentham & J. D. Hooker

(Tendrils with adhesive pads); nectary of multicellular hairs on C; A 5, 1-thecal, 3, 2- or both 2- and 1-thecal, inserted at base of C and connate to middle of C, thecae straight; (pollen perforate-rugulate - Alsomitra); (ovules ca 6/carpel); fruit a capsule [?type] (berry); seeds with broad, membranous wing (not); n = 11, 13.

6/56: Hemsleya (30). China and South East Asia to Australia and Fiji.

Age. Crown-group Gomphogyneae are (59-)65(-53) m.y.o. (Schaefer et al. 2009).

[Triceratieae + Zanonieae]: ?

Age. The age of this node - if it exists - is (61-)58(-55) m.y. (Schaefer et al. 2009).

2. Triceratieae A. Richard

Nectary of multicellular hairs on C; A 1-3, 5, variously 1 or 2-thecal, inserted at base of C, thecae straight or arcuate; (pollen larger, reticulate - Gerrardanthus); carpellate flowers: staminodia 5, (styluli central); fruit circumscissile, with "longitudinal splits", or indehiscent - 1(-3)seeded samara, baccate; seeds narrowly winged or not; n = ?

5/24. Mostly tropical, New World (E. and S. Africa and Madagascar - Cyclanthopseris).

Age. Crown-group Triceratieae are (51-)46(-41) m.y.o. (Schaefer et al. 2009).

Synonymy: Nhandirobaceae Lestibudois

3. Zanonieae Bentham & J. D. Hooker

(Flowers weakly monosymmetric); nectary of multicellular hairs on C[?]; A 5 (4), 1-thecal, inserted at base of C to middle of tube, thecae striaght or arcuate; (pollen reticulate); (flower single, central); fruit capsular; seeds with membranous (narrow) wing; n = ?

4/13. Pantropical.

Age. Crown-group Zanonieae are (60-)56(-52) m.y.o. (Schaefer et al. 2009).

Synonymy: Zanoniaceae Dumortier

4. Actinostemmateae H. Schaefer & S. S. Renner

Nectary of multicellular hairs on C; A inserted on base of tube, 5, or 2 pairs + 1, 1-thecal, thecae straight; style single, central; ovules 2-4, pendulous; fruit circumscissile; seeds winged or not; n = 8.

1/3. Central and East Asia.

5. Cucurbitoideae Eaton

Additional non-protein amino acids +; vascular bundles bicollateral; extrafascicular phloem system linked with adaxial phloem of bundles; nectary parenchymatous, with stomata; staminate flowers: hypanthium well developed (short); pollen grains ± spherical, reticulate; carpellate flowers: style shortly branched or not, stylar canal +, filled with secretion; ovules horizontal (to erect), micropyle endostomal or nucellus apex exposed, outer integument vascularized [?level], inner integument (1-)2-5(-ca 6 - Bryonia, Sechium) cells across, nucellar cap +/0, nucellar beak well developed [?level], suprachalazal region massive; antipodals degenerate; fruit indehiscent; seed not winged; exotesta enlarged, ± palisade or cubic, mucilaginous, hypodermal tissue various, sclereidal [how common?], sclereid layer sharply distinguished, single cell across, cells much enlarged, elongated or not, walls much thickened, walls of aerenchyma usu. unthickened, innermost layers green, chlorenchymatous.

82 [11 tribes]/900: Trichosanthes (100), Sicyos (75), Momordica (60), Zehneria (60), Cucumis (55), Cayaponia (55), Cyclanthera (40), Gurania (37). Tropical to warm temperate.

Age. The age of this node is around (56-)53(-50) m.y. (Schaefer et al. 2009).

Synonymy: Bryoniaceae G. Meyer, Cyclantheraceae Lilja

5A. Indofevilleeae H. Schaefer & S. S. Renner

Woody liane; lamina entire; plant dioecious; A inserted on base of tube, 2 pairs + 1, 1-thecal, thecae curved, hairy, filaments short; pollen grains ca 49 x 53 µm long; fruit dry, pericarp thick and woody; n = ?

1/1: Indofevillea khasiana. Assam, India.

The Rest:Perennial or annual vines (lianes), (cauduciform [hypocotylar] succulents); when monoecious, staminate inflorescence + carpellate flower + bud + tendril making up axillary complex; tendrils (-8 fid), (0), (stem incapable of coiling); monoecy quite common; nectary (of multicellular hairs - Sicyoeae); A 5 [Luffa] or fewer, ?inserted, anthers often much bent and coiled, (locellate); pollen grains 40-70(-200: Cucurbiteae) µm long, (colpate and [panto]porate, operculate), (smooth, echinate); n = 9, 11, 12, 14 (etc.).

Age. This node is (54-)51(-48) m.y.o. (Schaefer et al. 2009).

Evolution: Divergence & Distribution. For numerous dates within the family, see Schaefer et al. (2009).

The current world-wide range of Cucurbitaceae is in large part the result of extensive dispersal, Madagascar being colonized an estimated thirteen times and Australia twelve times - and the latter currently has only twelve genera and thirty species of Cucurbitaceae (Schaefer et al. 2009). The secondarily woody Socotran endemic Dendrosicyos is dated to (30-)22(-14) m.y., although Socotra itself is only about ten m.y. old, which suggests that the clade now represented by just the single species was once on the mainland and has since become extinct there (Schaefer et al. 2009, but c.f. Renner & Schaefer 2016). Sebastian et al. (2012) suggested that there had been four westwards trans-Pacific dispersal events in the New World Sicyos alone, while de Boer et al. (2014) also dated extensive dispersal in Trichosanthes. For more on dispersal in the family, see Duchen and Renner (2010).

Ecology & Physiology. Cucurbitaceae are very largely a group of climbing plants, whether lianes or vines, and are a prominent component of this vegetation element in the New World (Gentry 1991).

The phloem system in Cucurbitaceae is very complex. Fischer (1884) early noted that not all Cucurbitaceae had bicollateral vascular bundles (they are an apomorphy of only part of the family - see above). Taxa that do have bicollateral vascular bundles also have extrafascicular phloem (EFP) strands in the cortex outside the sclerenchymatous ring, although their development there is weak in taxa like Thladiantha and Momordica (Fischer 1884). EFP strands link with the adaxial phloem cells of the vascular bundles (Schmitz et al. 1987), but only at the nodes (Fischer 1883); in taxa like Cucurbita EFP strands permeate the cortex, even occuring in the collenchyma, and commissural strands are common (Fischer 1884). The sieve tubes of the EFP system differ in morphology from those of the fascicular phloem, although they may be similar to cells in the peripheral part of the latter (Crafts 1932).

When the plant is damaged, the copious phloem exudate comes largely from EFP, flow from the bundle phloem being blocked by callose almost immediately. The composition of EFP and fascicular phloem exudate is very different: Fascicular phloem exudate is rich in sugars and unidentified proteins, etc., EFP exudate contains P-proteins, amino acids, protein synthesizing machinery, and various secondary metabolites, but little sugar (Zhang et al. 2010). Zhang et al. (2012) found that phloem exudate came from different parts of the system in different species, although the completely extrafascicular sieve tubes were not involved. Not much of the exudate was from the fascicular phloem itself, and they thought that one of the functions of the P-protein in EFP exudate might even be to block the flow of water from the cut xylem as it congealed, although initially the water helped make large droplets of noxious (the exudate contains cucurbitacins - see below) and sticky exudate (Gaupels & Ghirado 2013). There is substantial evidence (Gaupels et al. 2012; see also Turgeon & Oparka 2010) that the EFP system is involved more in plant defence, and Gaupels et al. (2012) even thought that ecologically EFP exudate was like latex (see also Tallamy 1985; Konno 2011; Gaupels & Ghirado 2013). Interestingly, aphids feed on the abaxial phloem, and autoradiograms of minor veins suggest that abaxial phloem cells here are the sole conduits for carbon export and import, indeed, in the very finest veins there is no adaxial phloem system at all, i.e. the bundles there are collateral (Botha & Evert 1978; Schmitz et al. 1987; Hebeler 2000 and references).

More needs to be done to understand the complex vascular anatomy of the family, especially in the basal clades, to work out further details of how EFP is involved in plant defence, and how it links with the adaxial intrafascicular system. Much of the earlier work on phloem and phloem transport in Cucurbitaceae - because of the copious exudate, this had seemed to be an ideal system and has been much studied - actually has been carried out on EFP (Zhang et al. 2010)!

Pollination Biology & Seed Dispersal. There are a number of interesting pollinator-plant interactions in the family. In general, carpellate flowers produce no nectar and the style with its branching stigmas allows them to mimic nectar-producing staminate flowers (Renner & Schaefer 2016). Heliconius butterflies, whose caterpillars eat Passiflora vines (see Passifloraceae), are also closely associated with Psiguria (Cucurbitaceae), which they pollinate while at the same time obtaining nutrients from the pollen, probably by enzymatic activity of the saliva; the butterflies also visit some species of the closely related Gurania (e.g. Gilbert 1972, 1975; Boggs et al. 1981; Spencer 1988; Eberhard et al. 2009: see Steele 2010 for a summary and Steele et al. 2010 for a phylogeny of Psiguria). Interestingly, both Psiguria and Gurania have pollen grains in tetrads, alone in the family (Steele 2010). Psiguria in particular has very long-lived staminate inflorescences, and flowers are produced continuously for months or more. Other Cucurbitaceae, notably Momordica and Thladiantha, are oil flowers, the ca 19 extant species of Ctenoplectrini bees being associated with Cucurbitaceae and collecting material from the oil-secreting hairs, as well as pollen and nectar (Buchmann 1987; Vogel 1981b, 1990, 1998c: variation in nectary morphology and secretion). Ctenoplectrini are an Old World group and are probably sister to the Eucerini; they may have diverged in the early Eocene ca 50 m.y.a. and now probably pollinate over 100 species of the family (Schaefer & Renner 2008b). Although Ctenoplectra bees visit Momordica, carpellate flowers in some species lack rewards (Schaefer & Renner 2010), deceit pollination?

Squash and gourd bees, some 20 species of the genera Peponapis and Xenoglossa, pollinate only species of Cucurbita. They feed early in the day, even flying in the dark pre-dawn hours (Hurd et al. 1971). They are attracted by particular floral volatiles, repelled by others which attract the cucumber beetles, while yet others seem to attract both herbivore and pollinator (Andrews et al. 2007). The bees, restricted to the Americas north of northern Peru, show some species-specific variation in pollen collecting devices (Hurd & Linsley 1964); Cucurbita can clearly be pollinated by a variety of bees since it is cultivated pretty much world wide. Within Cayaponia there have been shifts from bat to bee pollination, uncommon elsewhere in flowering plants (Duchen & Renner 2010). A number of taxa have elaborately fringed margins of their corolla lobes, while Momordica anigosantha has quite strongly monosymmetric staminate flowers, both in form and especially colour patterning, yet the carpellate flowers are less remarkable (Zimmermann 1922).

Breeding systems in Cucurbitaceae can be very labile, with multiple reversals from dioecy to monoecy likely in Momordica alone (Schaefer & Renner 2010; see also Kocyan et al. 2007; Volz & Renner 2008); determination of the sex of the flower by environmental cues is also known in the family (Renner et al. 2007b). Boualem et al. (2015) discuss the molecular control in the transition from monoecy to dioecy. Bertin and Newman (1993) consider the family to be interflorally protandrous, while Bentley et al. (2004) record it is being protogynous; the latter are correct.

Myxospermy is reported from a number of Cucurbitoideae (Grubert 1974). Large mammals, relatively unaffected by the bitter cucurbitacins commonly found in the fruits (see below), have been implicated in the dispersal of cucurbitaceous seeds; the megafauna involved is in places (the New World) now extinct (Kistler et al. 2015).

Plant-Animal Interactions. Low concentrations of the very bitter cucurbitacins, tetracyclic sterol-like triterpenes that are among the most bitter substances known to humans, elicit a compulsive feeding response from luperine beetles, including rootworm leaf beetles (Chrysomelidae-Galerucinae-Luperini: see Metcalf et al. 1980; Jolivet & Hawkeswood 1995). Gillespie et al. (2008) outline their phylogeny; there are some 4,000 species. 80% of the host plant records of the group are from Cucurbitaceae, and many species are pharmacophagous. That is, adults visit the flowers, feeding on pollen and sometimes other parts of the plant, and they sequester these bitter cucurbitacins (Eben 1999; Tallamy et al. 2005). The beetles are attracted by volatiles coming both from flowers and other parts of the plant (Andrews et al. 2007). Furtheromore, large mammals are relatively unaffected by cucurbitacins in fruits, while smaller mammals may find these fruits to be toxic, and smaller mammals also have more genes encoding bitter taste receptors to help avoid such fruits than do larger mammals (Kistler et al. 2015).

The larvae of some galerucines also feed on Cucurbitaceae, and this ability may have evolved independently in Old and New World members, Aulacophorina and Diabroticina respectively (Gillespie et al. 2003). The larvae sometimes cut leaf veins (they "trench" the leaves), so locally interrupting the translocation of cucurbitacins to the leaf tissue and so apparently allowing the insect to eat it (Dussourd & Eisner 1987). However, since at least some of these beetles will eat cucurbitacin crystals neat, physical avoidance of the copious sap produced by Cucurbitaceae is a more likely explanation of this feeding behaviour. Indeed, the concentration of cucurbitacins inside and outside the trench is about the same, but the sap is very rich in P-protein and eventually gels and so would probably thoroughly gum up the mouth parts, etc., of the beetle larvae if they ate untrenched leaves (McCloud et al. 1995; see also below).

The glandular hairs of Cucurbitaceae are another element of the defence of the plant against herbivores, quickly-solidifying secretions being produced when the trichomes are touched by insects (Kellogg et al. 2002). Discharge of sap by these hairs may be explosive, Zimmermann (1922) mentioning what he called "Explosionshaare" in the family.

Larvae of a remarkable number of species of Blepharoneura (Diptera-Tephritidae [fruit flies]) are being discovered in flowers and fruits of neotropical Cucurbitoideae like Gurania. Some species are specific to staminate flowers, others to carpellate; all told some 52 species of flies were found on 24 species of cucurbits (Condon et al. 2008; Steele 2010 for Psiguria). It is estimated that there are around 200 species of Blepharoneura, all likely to be restricted to Cucurbitaceae (Norrbom & Condon) - perhaps the whole subfamily is. 14 species of these flies, on which there were 18 species of parasitoid wasps, were found in one site in Peru; they depended on two species of Gurania (Condon et al. 2014).

Butterfly caterpillars are not often found on members of this family (Ehrlich & Raven 1964).

Vegetative Variation. The tendrils of Cucurbitaceae are branched, and represent a branch complex. The length of the unbranched part of the tendril varies considerably, and the tendril may be ad- or abaxially curved in bud (Zimmermann 1922). Often there is a sublateral tendril + bud + slightly lateral flower associated with each leaf, or a tendril + vegetative bud + carpellate flower + staminate inflorescence, all more or less collaterally arranged, or other variants. Eichler (1875) and Goebel (1932) suggested that the tendril branches were prophylls, and in Bryonia dioica paired tendrils occur on the pedicel of an axillary flower (see also Zitnak et al. 2010). Non-flowering Zanonioideae have tendrils more or less lateral to vegetative axillary buds. When flowering finally begins, tendrils are replaced by more or less axillary flowers. The axillary bud produces an inflorescence branch that has an internode below the prophyllar leaf that subtends the first flower. Most Cucurbitoideae lack an initial prolonged vegetative period, and in one interpretation the inflorescence branch lacks a basal internode, so the first flower, often carpellate, arises in the leaf axil of the main branch and is subtended by a prophyll; the staminate inflorescence represents the development of this prophyllar bud (Lassnig 1997; axillary structures may be collateral in the vegetative part of the plant, sometimes superposed in the reproductive part). However, Gerrath et al. (2008) found that in Echinocystis lobata tendril, axillary bud, carpellate flower, and staminate inflorescence were all more or less independent in origin, although the latter two did arise from a common primordium (see also Zitnak et al. 2010). Joliffieae may be critical in understanding the evolution of the branch-tendril complex.

Genes & Genomes. In Cucumis, at least, mitochondria (but not chloroplasts) are transmitted paternally (Havey et al. 1998). The mitochondrial genome is very variable in size, being from ca 379,000-2,900,000 bp long, the shorter sequences, at least, having expanded by the acquisition of chloroplast sequences and the accumulation of numerous short repeats (Alverson et al. 2010; see also Bellot & Renner 2015: Apodanthaceae), and the genome is organised as a number of circular chromosomes (Alverson et al. 2011).

Economic Importance. Cucurbitaceae were particularly important in early agriculture in the Americas, being one of the triumvirate of squash, corn and beans. For discussion of various aspects of the history of cultivation of Lagenaria and Cucurbita in particular, see Teppner (2004). For the domestication of squash (Cucurbita spp., inc. C. moschata and C. agyrosperma) which began ca 10,000 years ago, see Dillehay et al. (2007), Piperno et al. (2009) and Ranere et al. (2009); for phytoliths of the family, see Piperno (2006). Sebastian et al. (2010) suggest that the relatives of cucumber and melon (Cucumis) are Asian-Australian. Kistler et al. (2014) proposed that the pre-Columbian global distribution of the bottle gourd, Lagenaria siceraria, was in part caused by gourds drifting across the Atlantic from Africa to South America; seeds can remain viable for about a year in sea water, and simulations suggested that gourds could drift across the Atlantic between the equator and 20oS in less than this time. For the origin of watermelons (Citrullus), bedevilled by misidentifications in the past, see Chomicki and Renner (2014). See also papers in Grumet et al. (2016).

Chemistry, Morphology, etc. Cucurbitaceae produce phytoalexins only with difficulty (Harborne 1999). Raffinose is the main transport carbohydrate (Turgeon & Ayre 2005). Distinctive long-chain fatty acids occur in the seed oils; eleostearic acid, an isomer of punicic acid, is restricted to Joliffieae (Hopkins 1990). There are crystalloid inclusions in the protein bodies found in embryos of this family, perhaps unusual for flowering plants (Lott 1981). Phytoliths are commonly produced by members of this family (Piperno 2006).

A number of African Cucurbitaceae have swollen stem bases. The ring of fibres in the stems of Cucurbita, at least, has nothing to do with the vascular bundles (Blyth 1958). Acanthosicyos has paired thorns at the nodes, but I do not know anything about their development; Xerosicyos is a woody, succulent-leaved vine. Vascularisation of the leaf is complex, e.g. the leaf being supplied by one of the outer ring of bundles in its entirety and by branches from two other bundles of the outer ring, the bud being supplied by the inner ring (Sensarma 1955). Indeed, as the literature summarized by Sensarma (1955) suggests, there has been much speculation about the nature of the cauline vascular system and, related to this and based on how leaves are supplied from the cauline system, whether from the inner or inner + outer rings of bundles, about the presumed cauline versus foliar nature of the tendrils.

For the determination of the "sex" of the flower, see Chuck (2010). Flowers in taxa in which the androecium has two pairs of stamens and a single stamen, four stamens and a staminode (Gerrardanthus), etc., are strictly speaking monosymmetric. The petals of Xerosicyos are free; those of Echinocystis and Lagenaria at least have several traces. When the stamens are connate 2 + 2 + 1, the vascular supply shows evidence of this, although there are differences over the interpretation of the apparently bithecal stamens (e.g. de Wilde & Duyfjes 1999); Schaefer and Renner (2011; see also Renner & Schaefer 2016) suggest that the plesiomorphic condition of the family is to have five bithecal stamens. Several tubes may arise from the one pollen grain (the pollen is polysiphonous), and some Cucurbiteae have very large almost spherical grains up to 200 µm or so long and across. The carpellate flower may have two rings of what can be interpreted as rudimentary anthers, while in the staminate flowers a ring of processes may alternate with the stamens. The nucellar beak is very large, in some species directly abutting placental tissue; depending on the species, the pollen-tube may swell up considerably there (Lizarazu & Pozner 2014). The chalazal haustorium of the embryo sac of Sechium [= Sicyos] edule, at up to 19,000 µm long, is apparently the longest in the family, although others are also quite long; only some Santalales have longer embryo sacs (Mikesell 1990; Johri et al. 1992). Seedlings commonly have a peg, a cortical outgrowth towards the bottom of the hypocotyl at the root-shoot transition (e.g. Klebs 1884 for a list of taxa); this is not found in species in which germination is hypogeal (Zimmermann 1922).

For additional general information, see Zimmermann (1922), Jeffrey (1980), Bates et al. (1990), Jeffrey and de Wilde (2006), Renner and Scaefer (2016) and especially Schaefer and Renner (2011a), for non-protein amino acids, see Fowden (1990), for cork cambium, see Dittmer and Roser (1963), for wood anatomy and secondary thickening, the latter odd, see Carlquist (1992c) and Patil et al. (2011), for seed coat anatomy, which is complex, Kratzer (1918), B. Singh (1972), Dathan (1974), D. Singh and Dathan (1973, 1974, 1998, 2001) and Teppner (2004), for embryology, etc., Kirkwood (1905: some details about Fevillea), Warming (1913), Chopra and Agarwal (1958: endosperm haustoris), Johri and Roy Chowdhury (1957) and Singh (1970), for floral morphology, etc., see Leins and Galle (1971) and Leins and Erbar (2010), for pollen, see Van der Ham et al. (2010: reticulate pollen derived?).

Phylogeny. Renner et al. (2002) suggested that Cucurbitoideae were probably monophyletic, with Thladiantha sister to the rest; tribes of Fevilleoideae (Zanonioideae) formed an unresolved basal polytomy. This was largely confirmed by Kocyan et al. (2007), although Indofevillea was sister to other Cucurbitoideae; monophyly of Fevilleoideae was not well suppported, Alsomitra sometimes appearing as sister to Cucurbitoideae. Schaefer and Renner (2008a) also found that Fevilleoideae were paraphyletic and so did not recognise the subfamily. There may be a grade of four clades basal to a well-supported Cucurbitoideae, in which Indofevilleeae were well supported as being sister to the rest. This basal grade includes Gomphogyneae - only moderate support, Alsomitra sister to the rest of the tribe, a strongly supported Fevilleeae, Zanonieae, with 76% ML bootstrap, and a strongly supported Actinostemmateae, although relationships between these clades had no support (Schaefer et al. 2009; Schaefer & Renner 2011b). Schaefer et al. (2009) used a topology in which [Gomphogyneae [Triceratieae + Zanonieae]] were sister to the rest of the family, Actinostemma being placed within Zanonieae, in their reconstructions. H.-L. Li et al. (2015), M. Sun et al. (2016) and Z.-D. Chen et al. (2016) also provide extensive details of relationships within the family, the basal topology in the latter in particular being similar to that just discussed. Establishment of the topology within the basal polytomy is important since it may well affect optimisation of characters on the tree.

Within Cucurbitoideae, phylogenetic studies suggest that Jeffrey's tribes (Jeffrey 2005) are largely monophyletic, although his subtribes are not (Kocyan et al. 2007). Jobst et al. (1998: ITS) found Benincaseae (Cucurbitoideae) to be polyphyletic; Chung et al. (2003) and Schaefer et al. (2008, esp. 2009: Alsomitra in Zanonieae) also looked at relationships within Cucurbitoideae. Schaefer et al. (2009) found Indofevillea to be sister to Cucurbitoideae. For smaller-scale studies within Cucurbitoideae, see Ghebretinsae et al. (2007), Wilde and Duyfjes (2006), Renner et al. (2007a), Schaefer and Renner (2010), Duchen and Renner (2010), Sebastian et al. (2010: Cucumis), Sebastian et al. (2012: Sicyos) and de Boer et al. (2015: Benincaseae).

Classification. For the suprageneric classification I follow Schaefer and Renner (2011b); the latter provide a comprehensive tribal classification which should be consulted for details (see also Renner & Schaefer 2016; c.f. Jeffrey 2005).

There are many small genera in Cucurbitaceae, and generic limits need attention, thus Ghebretinsae et al. (2007) had to adjust the limits of Cucumis; see also Wilde and Duyfjes (2006), Renner et al. (2007a) and Schaefer et al. (2009). Sebastian et al. (2012) included 13 of these small genera in Sicyos.

Previous Relationships. Cucurbitaceae have usually been associated with other families that have parietal placentation, whether placed all together in Violales (Cronquist 1981) or in a group of small orders placed next to each other in Dilleniidae (Takhtajan 1997).

[Tetramelaceae [Datiscaceae + Begoniaceae]]: pollen spherical, stigmas elongated; fruit a septicidal capsule [dehiscing apically]; seeds with lid [operculate]; exotestal cells honeycomb, inner walls strongly thickened and lignified; cotyledons moderate in size.

Age. This node can be dated to (60-)57, 50(-47) m.y. (Wilström et al. 2001) or (76-)73(-70) m.y. (Schaefer et al. 2009); in both, c.f. topology, also around 62.7 or 59.7 m.y. (Tank et al. 2015: Table S1, S2).

Age. {Begoniaceae + Tetramelaceae]: The age of this node - if it exists - is around (67-)63(-59) m.y. (Schaefer et al. 2009).

Chemistry, Morphology, etc. Tebbitt (2005) suggests that the seeds of this group have a operculum or lid, but whether this is a synapomorphy or not is unclear. Seeds of Tetramelaceae are apparently unknown, and Boesewinkel (1984) found that the opercula of Datiscaceae and Begoniaceae were rather different.

See Mauritzon (1936b) for some details of the ovules, Clement et al. (2004) for testal morphology.

TETRAMELACEAE Airy Shaw   Back to Cucurbitales


Trees; tannin 0; (wood fluorescing); (nodes with 2 traces from the lateral gaps); hairs glandular or lepidote; (lamina margins entire); plant dioecious; inflorescence spicate; K 4-8, postgenitally coherent; staminate flowers: C 0, or 6-8 [Octomeles], stamens = and opposite petals, incurved; carpellate flowers: C 0; G [3-8], (nectariferous disc on top), placentation axile, placentae bilobed [Octameles], stigmas undivided, decurrent to clavate; fruit also opening down the sides; seed coat?; n = ca 23.

2[list]/2. Indo-Malesia (map: from van Steenis 1953). [Photo - Tree.]

Age. The two genera diverged (33-)26(-19) m.y.a. (Schaefer et al. 2009).

Tetrameles wood is known fossil (as Tetramelioxylon prenudiflorum) from the Deccan Traps in India ca 70.6-65.5 m.y.a. (Zhang et al. 2007).

Chemistry, Morphology, etc. Octomeles has sclereids; its capsular fruits split into two layers, the outer of which falls off. For general information, see Swensen and Kubitzki (2011, in Datiscaceae).

[Datiscaceae + Begoniaceae]: herbs; outer integument ca 2 cells across, inner integument ca 2 cells across.

DATISCACEAE Dumortier, nom. cons.   Back to Cucurbitales


Roots with N-fixing Frankia; cucurbitacins?; cambium not storied; medullary bundles +; tannin sacs +; nodes 1:3; leaves deeply divided to odd-pinnate, lamina vernation conduplicate, secondary veins ± pinnate; plant (andro)dioecious; inflorescence fascicles on racemose axis; flowers protogynous; P 4-10; staminate flowers: P valvate; A 6-25, outer members opposite P, filaments very short [anthers almost sessile]; pistillode 0; carpellate flowers: staminode 0; G [3-8], opposite P, styles elongated; ovules with parietal tissue 3-5 cells across, cap 2-3 cells across; embryo sac bisporic, 8-nucleate; fruit septicidal?; exotegmic cells large, cuboid; endosperm slight; n = 11.

1[list]/2. W. North America, Crete to India (map: from Liston et al. 1989; Clement et al. 2004). [Photo - Flower, Flowers.]

Age. Ecology & Physiology. Nitrogen-fixation in this clade is perhaps as much as (85.8-)66.4, 42.7(-22.4) m.y.a., the date of divergenece of Datiscaceae and Tetraamelaceae (H.-L. Li et al. 2015: older ages prefered); (76-)73(-70) m.y. is when Datiscaceae diverged from [Begoniaceae + Tetramelaceae] (Schaefer et al. 2009).

Bacterial/Fungal Associations. VAM associations have been reported from Datiscaceae (e.g. Rose 1980).

Chemistry, Morphology, etc. The lid on the seeds of Datisca is not surrounded by a ring of collar cells (Boesewinkel 1984: c.f. Begoniaceae). The stamens show no particular positional relationships to the calyx (Takhtajan 1997).

Much general information is taken from Davidson (1973, 1976) and Swensen and Kubitzki (2011); see Leins and Bonnery-Brachtendorf (1977) for floral development.

BEGONIACEAE C. Agardh, nom. cons.   Back to Cucurbitales


Fleshy herbs; tanniniferous, soluble oxalate accumulation; cork subepidermal; cortical (and medullary) bundles +; vessel elements also with scalariform perforation plates; nodes swollen; petiole bundles annular (central bundles +); no pericyclic sheath; sclereids and uncalcified cystoliths +; stomata anisocytic or with accessory cells in two rings [helicocytic]; hairs diverse, often prominent, flattened, pearl glands + [hairs spherical, multicellular, sessile]; leaves two-ranked, vernation laterally or vertically conduplicate (supervolute-curved [prophylls]), asymmetric, stipules +, large, cauline-extrapetiolar; inflorescence cymose, staminate flowers first produced [= interfloral protandry]; K petal-like; staminate flowers: A many, centrifugal, connective enlarged; pollen colpate; carpellate flowers: placentae large, bilobed, stigmas twisted; ovules with parietal tissue 1-2 cells across, micropyle zig-zag, endothelium +; seeds minute, with lid and surrounding collar cells.

2[list]/1621: Begonia (1620). Largely tropical (map: from Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003, 6. 2011; Tebbitt 2005).

Age. The age of Hillebrandia, and hence crown-group Begoniaceae, has been estimated at 58.5-45 m.y. (Clement et al. 2004, see Errata 2005) or (35-)29(-23) m.y. (Schaefer et al. 2009).

1. Hillebrandia Oliver

Plant ± tuberous; T 10, 2-whorled, inner [= "C"] very small; A often with branched vasculature; G [5], only partly inferior, placentation axile at base and parietal at top; n = ?

1/1: Hillebrandia sandwicensis. Hawaii (green in the map above). [Photos - Collection, also Begonia.]

2. Begonia L.

Plant rhizomatous (tuberous), (scandent; shrubby); (stomata in groups); leaves (spiral; opposite), (compound), (margins entire); (plant dioecious); (inflorescence racemose), (carpellate flowers first produced - Symbegonia group); staminate flowers: (flowers disymmetric), T in 2s, 2(3)4(-8); A 3-many, (connate), (porose); carpellate flowers: P (2-)5(-9); G [(1)2-3(-6)], placentation axile to parietal, (placentae not bilobed), styles central; (endothelium +); fruit a capsule dehiscing laterally loculicidally (and septicidally), often asymmetrically winged, (a berry); n = 8-21+.

1/1600. Largely tropical, but neither Hawaii nor the Antipodes (red in the map above). [Photo - Flower, Fruit.]

Age. Crown-group Begonia is estimated to be (29.4-)22.3(-14.9) m.y. (Moonlight et al. 2015) - or 37.3-23.2 m.y. (Clement et al. 2004, see Errata 2005), although other estimates put diversification of the genus as occurring some time from the Eocene to early Oligocene 45-25 m.y.a. during a period of global cooling (Goodall-Copestake et al. 2009: sampling extensive) or (31-)24(-18.2) m.y.a. (95% HPD: Thomas et al. 2011b, focus on Malesia).

Evolution: Divergence & Distribution. The age of Hillebrandia, 45< m.y. (Clement et al. 2004, errata 2005), causes some biogeographical problems. Either Hillebrandia arrived in the Hawaiian area from some presumably continental region where it is now extinct, or it has been island hopping in the Pacific for 50 m.y. or more (for the ages of the Hawaiian island chain, see Sharp & Clague 2006 and references), or there was some combination of these scenarios (or Hillebrandia may be far younger than previously thought - Renner 2005). Things are not made any easier if Begonia itself initially diversified in Africa (Moonlight et al. 2015).

Begonia may have originated in Africa (see also Moonlight et al. 2015), and sister to the South American and Southeast Asian clades that represent the rest of the genus (whatever the reconstruction) are seasonally adapted species with perennating organs (Goodall-Copestake et al. 2010). Thomas et al. (2011b) found several invasions of Malesia by Begonia and subsequently generally west-to-east movement. The main clade of Malesian species includes members of four sections, including the speciose section Petermannia, with at least 270 species; the age of that whole clade was (16.5-)11.5(-6.6) m.y. (95% HPD) (Thomas et al. 2011b). Sections in Begonia are generally limited to single continents, but the very recently described B. afromigrata, from Thailand and Laos but in a section otherwise known only from Africa, is an exception (de Wilde et al. 2011). Chinese species of limestone-inhabiting Begonia form a single clade, despite a variety of sectional assignments, and they diversified (11.7-)8.4(-5.3) m.y.a., perhaps 2 m.y. after the origin of the stem group of this clade (Chung et al. 2012). Moonlight et al. (2015) discuss the evolution of the neotropical species, derived from two separate origins from Africa and much subsequent intracontinental movement.

Hughes and Hollingsworth (2008) suggested that the dearth of widespread species in Begonia is due in part to the low levels of gene flow (found in the few studies that have been carried out) and hence for the propensity of divergence in allopatry (and Twyford et al. 2015: also strong reproductive barriers). De Wilde et al. (2011) drew attention to the broader distributions of those species of Begonia that had fleshy fruits compared to the narrower distributions of species with dry fruits - despite the fact that these latter species had minute seeds and perhaps might be supposed to be dispersed easily by wind.

Hillebrandia has a number of perhaps plesiomorphic features, and some of the features we think of as being characteristic of Begoniaceae as a whole (style position, fruit dehiscence) may in fact be apomorphies for Begonia alone.

Ecology & Physiology. Begonia is noted for the diversity of the colours and colour patterns on its leaves, making it popular in horticulture, and these features are quite common in groups that, like Begonia itself, often grow in shady conditions (Gould & Lee 1996; Jacobs et al. 2016 and references). Blue iridescence in Begonia leaves is caused by the rearrangement of the thylakoids in epidermal chloroplasts (= iridoplasts) that allow them to capture light at green wavelengths, of which there is much in such conditions, and also increases the quantum yield, overall substantially boosting photosynthetic efficiency (Jacobs et al. 2016).

Pollination Biology & Seed Dispersal. Staminate flowers of Begoniaceae produce pollen, carpellate flowers usually have no reward, but have bright yellow and anther-like stigmas; deceit polination is probably involved (Schemske et al. 1996; de Wilde 2001). There are a few ornithophilous species with nectaries at the base of the styles in carpellate flowers only, others have no reward at all; various levels of deceit/mimicry are again involved, male flowers perhaps mimicking females in some cases... (Vogel 1998c; Renner 2006). Artificial hybridisation within Begonia has been extensive.

Tebbit et al. (2006) looked at the evolution of dispersal mechanisms in the speciose Southeast Asian Begonia; within a clade, taxa with animal or rain-ballist dispersal predominate. De Wilde (2011) discussed possible dispersal mechanisms in detail, and de Wilde et al. (2011) focussed on seed dispersal of fleshy-fruited members of the genus, which seem to have wider distributions than their dry-fruited congeners.

Animal-Plant Interactions. Butterfly caterpillars are not often found on Begoniaceae (Ehrlich & Raven 1964).

Genes & Genomes. There may have been a genome duplication somewhere near the base of the Begonia clade some 22 m.y.a. or more (Brennan et al. 2012). For hybridization between species with very different leaf morphologies, etc., see Dewitte et al. (2011)

Chemistry, Morphology, etc. The vegetative morphology of Begonia is interesting. It is easy to propagate many species of Begonia from parts of leaves, and stems developing from leaves and other odd developments are common in the appropriately-named B. phyllomaniaca. Barabé et al. (1992) discuss the development of the distinctively asymmetrical laminaa of the family; Martinez et al. (2016) noted that the leaf bases were mirror-asymmetrical, with auxin concentrations and leaf development as predicted by theory, rather than directionally asymmetrical, i.e. with all leaves asymmetrical in the same way, as in spiral phyllotaxis. For clustered stomata, see Hoover (1986 and references) and Peterson et al. (2010). There are various intermediates between trichomes, leaf teeth, and leaf-like appendages on the leaf, and some taxa have epiphyllous inflorescences (Dickinson 1978 for references). The leaf teeth are supplied by several veins.

Begoniaceae are somewhat unusual among monoecious taxa with cymose inflorescences in that the first flowers produced in the inflorescence are staminate, carpellate flowers being produced only later; the derived Symbegonia group has racemose inflorescences and shows the reverse arrangement (de Wilde 2011).

There are five small orange inner perianth parts (= "petals") in Hillebrandia that are very different from the large white outer perianth members (= "sepals"); the stamens are also orange... (Gauthier & Arros 1963). It has been suggested that the perianth of Begonia is to be compared with the sepals of Hillebrandia (see Gauthier 1959), and also that the petals of Hillebrandia are staminodial (Ronse Decraene & Smets 1990a, comparison with Papaveraceae), which they are in colour but not in position. The plesiomorphic tepal number of Begonia may be four in staminate flowers (a single whorl, c.f. Garcinia, or two bimerous whorls?) and five in carpellate flowers (Forrest et al. 2005). Not surprisingly, symmetry types of flowers is various (e.g. Reyes et al. 2016). De Wilde (2011 and references) noted the variation in vascular supply to members of the perianth, while the vascular bundle to the stamen may be branched (Gauthier 1963). There is a variety of enothecial thickenings in the family, and some taxa with porose anthers have these thickenings (Tebbitt & Maciver 1999). The stigmas are described as being antisepalous (Davidson 1973); any style is at most short.

For floral development, see Charpentier et al. (1989), for ovules, Boesewinkel and de Lange (1983) and Chandrasekhara Naidu (1985), for placentation, de Wilde and Arends (1989), for seed morphology, de Lange and Bouman (1999 and references), and for general information, see Sandt (1921) and especially de Wilde (2011).

Phylogeny. Hillebrandia, from Hawaii, is sister to Begonia as a whole (Clement et al. 2001; Swensen et al. 2001), however, H.-L. Li et al. (2015) found that Symbegonia was sister to the rest of the family. For phylogenetic relationships within Begonia, see Plana et al. (2004), Forrest and Hollingsworth (2003) and Forrest et al. (2005). Thomas et al. (2011a), focusing on Asian Begonia, emphasized that several sections were para- or poplyphyletic, while Thomas et al. (2011b) showed that there had been several invasions of Malesia, including one now represented by members of four sections.

Classification. For a sectional classification, etc., of Begonia, see Doorenbos et al. (1998), and for the species of the genus, see Smith et al. (1986), Golding and Wasshausen (2002) and Tebbitt (2005: more horticultural).

Previous Relationships. Like Cucurbitaceae, Begoniaceae have usually been associated with the other families that have parietal placentation, whether placed in Violales (Cronquist 1981) or in a group of small orders placed next to each other in Dilleniidae (Takhtajan 1997).

Botanical Trivia. The 39 genera described by Klotzsch and all now synonymized under Begonia must be a record.

[? + Apodanthaceae]: ?

Age. The age of a clade [Apodanthaceae [[Begoniaceae + Cucurbitaceae]] has been estimated as (91.9-)75.1(-58.6) m.y.o. by Naumann et al. (2013), while estimates for a stem age for the family ranged from (98-)81-65(-45) m.y.a. in Bellot and Renner (2014b).

APODANTHACEAE Takhtajan   Back to Cucurbitales


Stem parasite, plant endophytic; stomata anomocytic; plant monoecious or dioecious; flowers fairly small; P +, 2-3(-4)-seriate, bi- or trimerous [e.g. 2 + 4 + 4 or 3 + 6 + 6], members of inner whorl with adaxial tufts of hairs; nectary +, at base of style/gynostemium; staminate flowers: gynostemium +; A synandrial, to 72 "pollen sacs", in 1-4 rings, no vascular bundles evident, extrorse, filaments 0, endothecium 0; pollen tricolpate, (apertures 0 - "Berlinianche"), psilate; pistillode +/0, vesicular hairs on margin (all over); carpellate flowers: staminodes 0; G [4 (5)], ± inferior, carpels opposite inner P, placentation parietal, style short, very stout, hollow, stigma ± hemispherical; ovules many/carpel, lacking vascular supply, micropyle bi/endostomal, or nucellus apex exposed, outer integument 1 cell across, inner integument 1-2 cells across, parietal tissue 0; antipodals persist?; fruit baccate; seeds minute; testa thin-walled, mucilaginous, exotegmen massively lignified; endosperm +, embryo undifferentiated; n = ± 12, 16, 30, chromosomes ca 1.4 µm long.

2[list]/10: Pilostyles (9). New World from the S. W. U.S.A. southwards, S. W. Asia, S. W. Australia and E. (mostly) Africa (map: from Fl. Austral. 8. 1984; Novoa 2005; Trop. Afr. Fl. Pl. Ecol. Distr. 5. 2010; Bellot & Renner 2014a). [Photo - Flower.]

Age. The age of crown-group Apodanthaceae was estimated to be (77-)57-33(-25) m.y.a. (Bellot & Renner 2014b: high-end ages, some older than stem-group estimates, ignored).

Evolution. Ecology & Physiology. Recorded hosts include Fabaceae (Pilostyles) and Salicaceae (Apodanthes) (Bellot & Renner 2014a). Its distribution is probably an underestimate, since in Africa it is a parasite of e.g. the widespread Brachystegia and Julbernardia in the Miombo woodland (White 1983); it has also been mistaken for a rust...

For the effect of Pilostyles on the wood structure of its host, Mimosa, see do Amaral and Ceccantini (2011).

Pollination & Seed Dispersal. Apodanthaceae are pollinated by short-tongued flies and possibly by wasps, too, and the fruits are animal dispersed (Bellot & Renner 2013).

Genes & Genomes. Bellot and Renner (2015) examined the plastomes of two species of Pilostyles (from different continents) and found only five to six functional genes remaining and minute but probably circular plastomes lacking an inverted repeat. There were numerous plastid regions in the nucleus and particularly mitochondrion, although it is possible some of these may have come from the host (Bellot & Renner 2015); the mitochondrial genome of those Cucurbitaceae examined also show a propensity to take up sequences from the other genomes (Alverson et al. 2011).

For the much increased rate of variation in synonymous substitution in some mitochondrial genes, see Mower et al. (2007 and references). Barkman et al. (2007) found that mitochondrial genes (atp1) from host Fabaceae had moved to Pilosyles thurberi.

Chemistry, Morphology, etc. There are cushions of hairs at the bases of the inner perianth parts. Interpreting the meristicity of the flower is not easy, and the androecium in particular is difficult to understand (Blarer et al. 2004).

For information, see Harms (1935a: general), Kuijt (1969: general), Rutherford (1970: esp. anatomy, cytology), Takhtajan et al. (1985: pollen), Visser (1981), Blarer et al. (2004: floral morphology). For vesicular cells, see Blarer et al. (2002, 2004) and for a detailed study of Pilostyles ingae, see Endriss (1902). The Parasitic Plants website (Nickrent 1998 onwards) and Heide-Jørgensen (2008) - both general - can be consulted with profit.

Phylogeny. For relationships within the family, see Filipowicz and Renner (2010).

Previous Relationships. Apodanthaceae, like other holoparasitic angiosperms, were often previously included in Rafflesiaceae s.l., Rafflesiaceae s.s. here is included in Malpighiales. Relationships of Apodanthaceae with Malvales have been suggested, some Malvaceae in particular lacking normal anther thecal structure, the androecium may be fused, etc. (e.g. Blarer et al. 2004; Endress & Matthews 2006a; Schönenberger & von Balthazar 2006).

Thanks. I am gratefull to S. Renner for comments.