EMBRYOPSIDA Pirani & Prado (crown group)

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

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

STOMATOPHYTES

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

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

POLYSPORANGIOPHYTA

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

EXTANT TRACHEOPHYTA / VASCULAR PLANTS

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

[MONILOPHYTA + LIGNOPHYTA]

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

LIGNOPHYTA

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

EXTANT SEED PLANTS/SPERMATOPHYTA

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

MAGNOLIOPHYTA

Lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, apigenin and/or luteolin scattered, [cyanogenesis in ANITA grade?], S [syringyl] lignin units common [positive Maüle reaction - syringyl:guaiacyl ratio more than 2-2.5:1], and hemicelluloses as xyloglucans; root apical meristem intermediate-open; root vascular tissue oligarch [di- to pentarch], lateral roots arise opposite or immediately to the side of [when diarch] xylem poles; origin of epidermis with no clear pattern [probably from inner layer of root cap], trichoblasts [differentiated root hair-forming cells] 0, exodermis +; shoot apex with tunica-corpus construction, tunica 2-layered; reaction wood ?, associated gelatinous fibres [g-fibres] with innermost layer of secondary cell wall rich in cellulose and poor in lignin; starch grains simple; primary cell wall mostly with pectic polysaccharides, poor in mannans; tracheid:tracheid [end wall] plates with scalariform pitting, wood parenchyma +; sieve tubes enucleate, sieve plate with pores (0.1-)0.5-10< µm across, cytoplasm with P-proteins, cytoplasm not occluding pores of sieve plate, companion cell and sieve tube from same mother cell; sugar transport in phloem passive; nodes 1:?; stomata brachyparacytic [ends of subsidiary cells level with ends of pore], outer stomatal ledges producing vestibule, reduction in stomatal conductance to increasing CO2 concentration; lamina formed from the primordial leaf apex, margins toothed, development of venation acropetal, overall growth ± diffuse, venation hierarchical-reticulate, secondary veins pinnate, veins (1.7-)4.1(-5.7) mm/mm2, endings free; most/all leaves with axillary buds; flowers perfect, pedicellate, ± haplomorphic, parts spiral [esp. the A], free, numbers unstable, development in general centripetal; P +, members each with a single trace, outer members not sharply differentiated from the others, not enclosing the floral bud; A many, filament not sharply distinguished from anther, stout, broad, with a single trace, anther introrse, tetrasporangiate, sporangia in two groups of two [dithecal], ± embedded in the filament, with at least outer secondary parietal cells dividing, each theca dehiscing longitudinally, endothecium +, endothecial cells elongated at right angles to long axis of anther; tapetum glandular, cells binucleate; microspore mother cells in a block, microsporogenesis successive, walls developing by centripetal furrowing; pollen subspherical, tectum continuous or microperforate, ektexine columellate, endexine thin, compact, lamellate only in the apertural regions; nectary 0; carpels present, superior, free, several, ascidiate, with postgenital occlusion by secretion, stylulus short, hollow, cavity not lined by distinct epidermal layer, stigma ± decurrent, carinal, dry [not secretory]; ovules few [?1]/carpel, marginal, anatropous, bitegmic, micropyle endostomal, outer integument 2-3 cells across, often largely subdermal in origin, inner integument 2-3 cells across, often dermal in origin, parietal tissue 1-3 cells across [crassinucellate], nucellar cap?; megasporocyte single, hypodermal, functional megaspore lacking cuticle; female gametophyte four-celled [one module, nucleus of egg cell sister to one of the polar nuclei]; supra-stylar extra-gynoecial compitum +; ovule not increasing in size between pollination and fertilization; pollen grains landing on stigma, bicellular at dispersal, mature male gametophyte tricellular, germinating in less than 3 hours, pollination siphonogamous, tube elongated, growing between cells, growth rate 20-20,000 µm/hour, outer wall pectic, inner wall callose, with callose plugs, penetration of ovules via micropyle [porogamous], whole process takes ca 18 hours, distance to first ovule 1.1-2.1 mm; male gametes lacking cell walls, flagellae 0, double fertilization +, ovules aborting unless fertilized; P deciduous in fruit; seed exotestal, becoming much larger than ovule at time of fertilization; endosperm diploid, cellular [micropylar and chalazal domains develop differently, first division oblique, micropylar end initially with a single large cell, divisions uniseriate, chalazal cell smaller, divisions in several planes], copious, oily and/or proteinaceous; embryogenesis cellular; dark reversal Pfr -> Pr; Arabidopsis-type telomeres [(TTTAGGG)n]; 2C genome size 1-8.2 pg [1 pg = 109 base pairs], whole nuclear genome duplication [epsilon duplication]; protoplasm dessication tolerant [plant poikilohydric]; ndhB gene 21 codons enlarged at the 5' end, single copy of LEAFY and RPB2 gene, knox genes extensively duplicated [A1-A4], AP1/FUL gene, paleo AP3 and PI genes [paralogous B-class genes] +, with "DEAER" motif, SEP3/LOFSEP and three copies of the PHY gene, [PHYB [PHYA + PHYC]].

[NYMPHAEALES [AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]]: wood fibres +; axial parenchyma diffuse or diffuse-in-aggregates; pollen monosulcate [anasulcate], tectum reticulate-perforate [here?]; ?genome duplication; "DEAER" motif in AP3 and PI genes lost, gaps in these genes.

[AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]: vessel elements with scalariform perforation plates in primary xylem; essential oils in specialized cells [lamina and P ± pellucid-punctate]; tension wood +; tectum reticulate; anther wall with outer secondary parietal cell layer dividing; carpels plicate; nucellar cap + [character lost where in eudicots?]; 12BP [4 amino acids] deletion in P1 gene.

[[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]] / MESANGIOSPERMAE: benzylisoquinoline alkaloids +; sesquiterpene synthase subfamily a [TPS-a] [?level], polyacetate derived anthraquinones + [?level]; outer epidermal walls of root elongation zone with cellulose fibrils oriented transverse to root axis; P more or less whorled, 3-merous [possible position]; pollen tube growth intra-gynoecial; embryo sac bipolar, 8 nucleate, antipodal cells persisting; endosperm triploid.

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

[CERATOPHYLLALES + EUDICOTS]: ethereal oils 0.

EUDICOTS: (Myricetin, delphinidin +), asarone 0 [unknown in some groups, + in some asterids]; root epidermis derived from root cap [?Buxaceae, etc.]; (vessels with simple perforation plates in primary xylem); nodes 3:3; stomata anomocytic; flowers (dimerous), cyclic; K/outer P members with three traces, ("C" +, with a single trace); A few, (polyandry widespread, initial primordia 5, 10, or ring, ± centrifugal), filaments fairly slender, anthers basifixed; microsporogenesis simultaneous, pollen tricolpate, apertures in pairs at six points of the young tetrad [Fischer's rule], cleavage centripetal, wall with endexine; G with complete postgenital fusion, stylulus/style solid [?here]; seed coat?

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

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

[BUXALES + CORE EUDICOTS]: ?

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

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

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

[SAXIFRAGALES [VITALES + ROSIDS]] / ROSANAE Takhtajan / SUPERROSIDAE: ??

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

ROSIDS: (mucilage cells with thickened inner periclinal walls and distinct cytoplasm); embryo long; genome duplication; 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]: ?

[CELASTRALES [OXALIDALES + MALPIGHIALES]] / the COM clade: seed exotegmic, cells fibrous.

[OXALIDALES + MALPIGHIALES]: ?

Age. This node was dated to around (109-)102, 91(-84) m.y., with Bayesian estimates to 112 m.y. (Hengcheng Wang et al. 2009: stem ages for the two orders differ slightly...); estimates by Wikström et al. (2001) were only (94-)91, 88(-85) m.y., rather like the ca 88.3 m.y. suggested by Naumann et al. (2013).

Ages in Magallón and Castillo (2009) were ca 102 m.y. and in Bell et al. (2010) were (109-)102, 98(-94) m.y., although in both these last two, note the topology, OCM, not COM.

OXALIDALES Heintze  Main Tree.

Characters? - 7 families, 60 genera, 1815 species.

Note: Possible apomorphies are in bold. However, the actual level at which many of these features, particularly the more cryptic ones, should be assigned is unclear. This is partly because many characters show considerable homoplasy, in addition, basic information for all too many is very incomplete, frequently coming from taxa well embedded in the clade of interest and so making the position of any putative apomorphy uncertain. Then there is the not-so-trivial issue of how ancestral states are reconstructed...

Age. The age of crown group Oxalidales was estimated as (105-)93, 89(-78) m.y. by Bell et al. (2010; note topology).

Chemistry, Morphology, etc. Leaves of Cunoniaceae and Elaeocarpaceae can be almost indistinguishable. Diplostemony does not occur in the order; the androecium of Cunoniaceae is obdiplostemonous, according to Huber (1963), and so agrees with that of Oxalidaceae (and Brunelliaceae [Orozco 2002] and Connaraceae). Connaraceae and Brunelliaceae have ovaries with adaxial furrows (c.f. the ventral slit: Matthews & Endress 2002b). Is the distribution of taxa that have carpels with five vascular traces of any interest?

Some information is taken from Nandi et al. (1998). There is much information on floral morphology and development for the whole order in Matthews and Endress (2002b, summarized in 2006b).

Phylogeny. This is a somewhat unexpected association of families. Molecular data recover a clade [Oxalidaceae + Connaraceae] in particular (Price & Palmer 1993; Williams et al. 1994; Fernando et al. 1995, etc.), and this also has strong morphological support. The other families are in a clade sister to this pair (e.g. Zhang & Simmons 2006: Cephalotaceae not included; Soltis et al. 2011). For the relationships of Brunelliaceae, see Bradford and Barnes (2001), although morphological analyses (Miranda-Esquivel 2001; Orozco 2001a; Orozco Pardo 2002) variously mixed Brunelliaceae and Cunoniaceae. The family pair [Brunelliaceae + Cephalotaceae] was retrieved by Davis et al. (2004) and Crayn et al. (2006). However, Heibl and Renner (2012) suggest relationships in this part of the tree of [Cunoniaceae [Brunelliaceae [Cephalotaceae + Elaeocarpaceae]]], which implies a rather different scenario of character evolution.

Zhang and Simmons (2006: see also Soltis et al. 2007a) found that Huaceae were sister to the other Oxalidales they examined, with quite strong support (jacknife values over 80%); they suggest that Huaceae should be included in Oxalidales. Zhu et al. (2007) also found quite strong bootstrap support for this position when the mitochondrial matR gene was examined, but support was lost when two chloroplast genes were added. Support was only weak in the recent analysis of Wang et al. (2009) and Qiu et al. (2010), but moderate to strong in the multiple gene analysis of Soltis et al. (2011). All in all, however, Huaceae seem to be finding a more fixed place on the tree (see also Wurdack & Davis 2009), and movement is in order. However, they lack even the rather unimpressive morphological features that characterize other Oxalidales.

Although the flowers of Anisophyllea (Anisophylleaceae-Cucurbitales) are remarkably similar to those of Ceratopetalum (Matthews et al. 2001; see also Matthews & Endress 2004, 2006b), and Matthews and Endress (2002b) note the filaments are longer than the anthers in bud in Oxalidales (but not in Elaeocarpaceae) and in Anisophylleaceae. There are perhaps comparable similarities in the fossil Platydiscus peltatus (Schönenberger et al. 2001a; Schönenberger & von Balthazar 2006; see above). However, none of these similarities is likely to reflect a close relationships between the two; Ceratopetalum is somewhat embedded in Cunoniaceae (see below) and the two families are not even in immediately related clades.


Includes Brunelliaceae, Connaraceae, Cephalotaceae, Cunoniaceae, Elaeocarpaceae, Huaceae, Oxalidaceae.

Synonymy: Bauerales Martius, Cephalotales Martius, Connarales Link, Cunoniales Martius, Elaeocarpales Berchtold & J. Presl, Huales Doweld, Tremandrales Martius

HUACEAE A. Chevalier

Huaceae

Evergreen, woody (lianes); ellagic acid?; hairs stellate or peltate (unequally 2-armed); cork?; cambium storying?; vessel elements with simple (scalariform) perforations; phloem with broad rays; cristarque cells +; petiole vasculature complex; stomata paracytic, cuticle waxes 0; leaves two-ranked, lamina margins entire, glands +, basal on margin or on abaxial surface, (strong vein pair from the very base); inflorescence axillary, fasciculate; (flowers 4-merous); K valvate or completely connate, C clawed or strongly obovate; pollen porate; nectary?; G [5], unilocular, placentation basal, style +, stigma punctate; ovules 1, (4-)6, micropyle?; fruit a ?septicidal capsule or drupe, pericarp with stony layer in middle; seed 1; testa with vascular bundles, (hairy - Hua), exotegmen of lignified palisade cells; endosperm copious, ?development, cotyledons flattened; n = ?

2[list]/3. Tropical Africa (map: from Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003).

Chemistry, Morphology, etc. The family is poorly known, especially its chemistry and floral development/embryology. Hua has long-clawed petals with a peltate blade, unremarkable anthers, a single ovule, and the fruit is a capsule; Afrostyrax has strongly obovate petals, aristate anthers dehiscing from the apex, and the fruit is a drupe.

For additional information, see Heywood et al. (2007: general), Baas (1972: anatomy) and Hegnauer (1989: a little chemistry).

Previous Relationships. The family has been of uncertain position in the past, being included in Malvales (e.g. Baas 1972; Takhtajan 1997), in the more heterogeneous Violales (Cronquist 1981), and hardly unsurprisingly less out of place there, or left unplaced in the rosids by A.P.G. I and II (1999, 2003).

[[Connaraceae + Oxalidaceae] [Cunoniaceae [Elaeocarpaceae [Brunelliaceae + Cephalotaceae]]]]: vessel element type?; mucilage cells +; stomata ?; leaves compound, odd-pinnate, tri-, or unifolioliate; nectary extrastaminal; styles separate, stigma secretory; micropyle bistomal; testa multiplicative, endotesta crystalliferous and palisade, exotegmen also tracheidal.

Age. The age of this node was estimated as (74-)69, 62-(57) m.y. (two penalized likelihood dates: Hengchang Wang et al. 2009). Wikström et al. (2001) suggested an age of some (80-)77, 72(-69) m.y., Magallón and Castillo (2009) an age of ca 90.5 m.y., and Bell et al. (2010) ages of (78-)64, 59(-44) m.y..

[Connaraceae + Oxalidaceae]: plant construction sympodial; benzoquinone rapanone +, ellagic acid 0; roots diarch [lateral roots 4-ranked]; vessel elements with simple perforations; wood rays uniseriate; sieve tube plastids with protein crystalloids; calcium oxalate druses 0; cuticle wax platelets as rosettes; leaves pinnate, leaflets articulated, pulvinate, margins entire, secondary veins pinnate to palmate, stipules 0; flowers di- and tristylous, pedicels articulated; C postgenitally subbasally united, with uniseriate glandular hairs; A of two whorls of different lengths, connate basally, (5, with antepetalous A staminodial), with uniseriate glandular hairs; (pollen colpate); (stigma with rounded multicellular ornamentations); ovules with endothelium; K persistent in fruit; exotesta ± fleshy.

Chemistry, Morphology, etc. Sieve tube plastids may have protein crystalloids + starch [Connaraceae], crystalloids + fibres + starch [both], or crystalloids alone [Oxalis].

CONNARACEAE R. Brown, nom. cons.   Back to Oxalidales

Connaraceae

Shrubs or lianes, scrambling or twining, (trees); hairs uniseriate, submesifixed or not; wood commonly siliceous or with SiO2 grains; (nodes 5:5, 7:7); petiole bundles?; stomata variable; leaves two-ranked or spiral, (unifoliolate); (plants dioecious); (flowers 4-merous); (K connate); (nectary 0); (androgynophore +); A connate or not; tapetal cells binucleate; G separate, 1 (3) 5 (7, 8), (stipitate), placentation near-basal, stigmas capitate, ?type; ovules 2/carpel, collateral, apotropous, funicle 0, (micropyle exostomal), outer integument 5-15 cells across, inner integument 3-5 cells across, parietal tissue 1-3 cells across, chalazal columnar; postament ± +; fruit a follicle (also dehiscing abaxially; drupe), often only one developing, sepals persistent, ± indurated; seed 1 (2); testa vascularized, black, sarcoexotesta ± developed, exotesta various, inc. palisade (lignified), tegmen multiplicative; endosperm 0 to abundant, oily; n = 14, 16.

12[list]/180: Connarus (80), Rourea (40-70). Pantropical, especially Africa and Old World (map: from Leenhouts 1958; Forero 1983; Trop. Afr. Fl. Pl. Ecol. Distr. 6. 2011). [Photo - Flower, Fruit.]

Chemistry, Morphology, etc. The plants are often poisonous. Growth is rarely sylleptic (Keller 1994). There are often five traces to each carpel. The ovules may be straight or anatropous. Number of nuclei in pollen?

There is much useful information in Jongkind and Lemmens (1989) and Lemmens et al. (2004); Mauritzon (1939a) described ovule morphology, Dickison (1971) carpel anatomy.

Previous Relationships. The cuticle waxes of Connaraceae are similar to those of Fabaceae-Fabales (Ditsch & Barthlott 1994) with which Connaraceae have frequently been confused. However, the two are not particularly close, and can usually be distinguished because the Connaraceae lack stipules and have rather small, polysymmetric flowers with ten stamens of two different lengths, a combination of features unknown in Fabaceae.

Synonymy: Cnestidaceae Rafinesque

OXALIDACEAE R. Brown, nom. cons.   Back to Oxalidales

Oxalidaceae

Trees to herbs (vines); tannins +; petiole bundle(s) annular (with medullary bundles); mucilage cells?; juice acrid because of soluble calcium oxalate accumulation; stomata paracytic; leaves spiral (two-ranked), (simple; palmate), (stipules +, small), colleters + [Oxalis]; inflorescence cymose; C contorted, often clawed; nectaries often glands opposite petals; anthers extrorse; G [(3-)5], styluli +, stigmas spathulate/capitate; ovules (1-)2-many/carpel, (micropyle zig-zag; exostomal), outer integument 3-5 cells across, inner integument 3-5(-6) cells across, parietal tissue often 0; (megaspore mother cells several), (embryo sac bisporic, 8-celled), antipodals degenerate; fruit a ± ribbed/angled capsule or berry; seed (arillate), (subruminate), (explosive); testa (not multiplicative), often mucilaginous, (endotesta walls thickened; not palisade), (exotegmen 2-layered), testa and tegmen less differentiated when fruit a berry, or tegmen 0 (Biophytum); endosperm +, starchy (0), embryo large, green or white [Oxalis]; n = (5-)7(-12).

6[list]/770: Oxalis (700), Biophytum (50). Usu. tropical or subtropical: species like Oxalis corniculata are very weedy and widespread (map: from Hultén 1958, 1971; Hultén & Fries 1986; Lourteig 2000 and references; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; GBIF Biophytum vii.2008; FloraBase vii.2008). [Photo - Flower.]

Age. Crown Oxalidaceae were dated to (56-)52, 43(-39) m.y. (Wikström et al. 2001). A rather older age for stem Oxalis (i.e. crown Oxalidaceae) of (62.3-)56(-49.2) m.y. was suggested by by Heibl and Renner (2012), and the age estimate in Bell et al. (2010) was (52-)37, 34(-22) m.y..

Evolution. Divergence & Distribution. It is estimated that divergence within Oxalis began (55.2-)48.6(42.3) m.y.a. (Heibl & Renner 2012, q.v. for other dates within the genus). Oxalis in the Cape region is a major element of the geophytic flora (Procheŝ et al. 2006); of the some 200 species in southern Africa, about 180 grow in the Greater Cape floristic region. Diversification of Oxalis in the Fynbos began about (31-)15.75 m.y.a., that in the succulent karoo some (20-)10 m.y.a. (Verboom et al. 2009). All have tunicate bulbs, some species having very distinctive methods of vegetative reproduction and perennation, and they show more vegetative than floral variation (Oberlander et al. 2009). African Oxalis has its origin in South America (Oberlander et al. 2011), indeed, Oxalis is most diverse there.

Oxalis is diverse in South America, particularly in drier parts of southern South America, with some 54 species known from Chile alone. Here the genus seems to have moved into drier habitats over a period of years. There have been 6-8 invasions of the alpine habitate alone, but with no obvious radiations there or correlation of the origins of those clade with the uplift of the Andes; one clade is predominantly to be found in the hyperarid Atacacama desert (Heibl & Renner 2012). However, the O. tuberosa alliance seems to have radiated along the Andes (Emshwiller & Doyle 2002), perhaps as little as 10-6 m.y.a. (Heibl & Renner 2012). New World species that are bulbous have scaly bulbs, or fleshy scales are borne along a rhizome; these scales may be equivalent to stipules or to whole leaves (Emshwiller et al. 2009). There are few other non-monocot bulbous taxa. Some species are shrubs to vines.

Pollination Biology & Seed Dispersal. There has been parallel evolution of distyly from tristyly within the New World bulbous species of Oxalis, and distyly is particularly common in a North American clade (Gardner et al. 2012).

The mucilaginous testa is often mistaken for an aril; the turgor pressure that builds up in it forces the rest of the seed out explosively, rather like squeezing a grape pip.

Genes & Genomes. Diploid plants with x = 5 had far larger genomes that polyploid clade with x = 6 in a group of Oxalis (Vaio et al. 2013).

Economic Importance. For Oxalis tuberosa (oca) and its relatives, see Emswhiller (2002).

Chemistry, Morphology, etc. Averrhoa is rather different from other members of the family. It has sieve tube plastids with protein crystalloids + fibres and starch, the ovules are weakly but definitely crassinucellate (but there is an endothelium) (Boesewinkel 1985b; Chung & Lim 1998), and the testa is multiplicative (Corner 1976). The leaves of Averrhoa carambola are two-ranked; the two species of the genus differ considerably in how they grow (Keller 1994).

The pollen of Oxalidaceae often contains starch. Link (1992a) describes the nectary glands as being opposite the calyx, but they are opposite the corolla at the bases of the filaments (e.g. Rama Devi 1991).

Some information is taken from Govindappa and Boriah (1956), Herr and Dowd (1968), L. L. Narayana (1970), and Rosenfeldt and Galati (2012), all embryology, etc., Robertson (1975: general) and Cocucci (2004: general); for cork position, see Averrhoa bilimbi.

Phylogeny. Heibl and Renner (2012) found the relationships [Oxalis [Biophytum [Dapania [Averrhoa + Sarcotheca]]]] in the family. Oberlander et al. (2004, esp. 2011) discuss relationships within some southern African species of Oxalis. The ca 210 African species of the genus, all bulbous and largely from the Cape region, form a clade with small, basal pectinations and then two major subclades (Oberlander et al. 2011). For a preliminary phylogeny of the genus as a whole, see Emshwiller et al. (2009).

Classification. See Lourteig (2000, and references) for extensive monographic work on Oxalis.

Previous Relationships. Cronquist (1981) placed Oxalidaceae in Geraniales, and he included Hypseocharis (here Geraniaceae-Geraniales), Lepidobotrys (Lepidobotryaceae-Celastrales) and Dirachma (Dirachmaceae-Rosales) in the family.

Synonymy: Averrhoaceae Hutchinson.

[Cunoniaceae [Elaeocarpaceae [Brunelliaceae + Cephalotaceae]]]: K valvate, postgenitally coherent by hairs, (C fringed/lobed); (antepetalous A shorter than the others).

Age. Estimates for the age of this node are (70-)66, 64(-60) m.y. (Wikström et al. 2001) or (64-)50, 46(-34) m.y. (Bell et al. 2010).

Platydiscus peltatus (Schönenberger et al. 2001a; Schönenberger & von Balthazar 2006), perhaps a member of Cunoniaceae, has been used to date the crown age of this clade (i.e. as stem Cunoniaceae) at (84.2-)83.5(82.8) m.y. (see Heibl & Renner 2012).

CUNONIACEAE R. Brown, nom. cons.   Back to Oxalidales

Cunoniaceae

Woody, branching from the current flush; plants often Al-accumulators; ellagic acid + or 0 [Bauera, Eucryphia]; wood with crystals; vessel elements with (simple to) mixed or scalariform perforation plates; sieve tubes with non-dispersive protein bodies; young stem with vascular cylinder; (nodes 1:3 [Bauera], 5:5; split laterals; etc.); petiole bundles (arcuate) annular (adaxial or medullary bundles +); stomata variable; leaves opposite, (palmate), leaflet margins gland-toothed, 2ndaries proceeding to the teeth, or not, (stipels +), stipule single, interpetiolar, rounded (acicular), (2, cauline-intrapetiolar - Lamanonia; 1, intrapetiolar), colleters +; flowers rather small, (4-)5(-10)-merous; C (0), ± = K in size (large); A (obdiplostemonous; in a single whorl), (-many, centripetal, with trunk bundles), (= and opposite sepals), (= and opposite C - Spiraeanthemum), (anthers basifixed; not articulated), filaments incurved in bud, often longer than the petals; tapetal cells binucleate; pollen dicolp(or)ate; (nectary +); G (?1-(Hooglandia)[2 (3-)5(-many)] (free; inferior), opposite petals [?always], placentae intruding, styluli common, (style hollow), stigmas punctate to capitate or decurrent; ovules (1-)2 epitropous erect -several pleurotropous/carpel, micropyle various, inc. zig-zag, outer integument 2-3 cells across, inner integument 4-5 cells across, parietal tissue 1-5 cells across, (nucellar cap 2 cells across), chalaza ± columnar; obturator +; archesporium multicellar, postament ± +; fruit a septicidal capsule, or follicle (drupe); exotestal and endotegmic cells tangentially elongated; endosperm (0), starchy (not Davidsonia); n = (12, 14-)16.

27[list]/280: Weinmannia (160), Pancheria (26). Largely temperate and tropical S. hemisphere, few African (map: from Good 1974). [Photo - Flower, Flower.]

Age. Fossil flowers of Platydiscus peltatus from the Late Cretaceous of Sweden ca 83 m.y.a. seem assignable to this family (Schönenberger et al. 2001a; Friis et al. 2011); the stamens are no longer than the petals. Flowers from Burmese amber dated at 110-97 m.y. old (Tropidogyne: K 5, spreading, A 10, G [3], inferior, styluli spreading) look rather like those of Ceratopetalum (Chambers et al. 2010).

Chemistry, Morphology, etc. There are numerous lignified cells in the bark of Cunoniaceae. That Bauera has 1:3 nodes may be connected with the fact that it sometimes lacks stipules, however, there is considerable vegetative variation in the genus: When the leaves are trifoliate, there are no stipules; when the leaves are simple, the stipules are foliaceous. Eucryphia and other Cunoniaceae have very small sieve tube plastids, those of the former have protein inclusions only and are about the smallest known (Behnke 1988b). The leaf teeth have a glandular apex: the lower branch of the main vein goes into the tooth, the other proceeds above it. Nodal anatomy is variable, as is stipule development; single interpetiolar stipules may be paired as primordia (Rutishauser & Dickison 1989). The flowers in an inflorescence often open almost simultaneously (Bradford & Barnes 2001) and sometimes centrifugally. The nectary varies in position from extrastaminal to intrastaminal. The pollen grains are typically very small. Cunonia has two oblique carpels (Engler 1930b). There are often five traces to each carpel. The endosperm is described as being oily by Cronquist (1981) and Mabberley (1997), but starchy by Hopkins and Hoogland (2002) and Bradford et al. (2004). It is not clear how common pachychalazal seeds are (see Doweld 1998a).

See also Jay (1968b) for chemistry, Hufford and Dickison (1992) for morphology, Gregory (1998) for general anatomy, Dickison (1980a) for wood anatomy, Dickison (1980b) and Rutishauser and Dickison (1989) for nodal anatomy, Rutishauser and Dickison (1989) and Dickison and Rutishauser (1990) for stipules, Mauritzon (1939a) for ovules, Dickison (1975) for floral anatomy of Bauera, Moody and Hufford (2000b) for Davidsonia, Mathews et al. (2001) and Schönenberger et al. (2001a) for floral morphology; Dickison (1989b) and Bradford et al. (2004) provide general information.

Phylogeny. Morphological phylogenetic analyses of Cunoniaceae in the old sense, i.e. including Aphanopetalum (now Saxifragales), do not signal the latter out as being anything particularly distinctive (Hufford & Dickinson 1992; Orozco Pardo 2002). Sweeney et al. (2004) placed the distinctive and then recently-discovered Hooglandia firmly within the family. Morgan and Soltis (1993) early associated Baueraceae and Cunoniaceae. the clade [Acsmithia + Spiraeanthemum] were sister to the rest of the family (see also Bradford & Barnes 2001; Hopkins et al. 2013: tree rooted by the latter genus). They have follicular fruits and vessel elements with scalariform perforation plates, but both features occur elsewhere in the family. Bauera, Davidsonia, and Hooglandia are probably all close to the base of the tree (Hopkins et al. 2013), although which genera, their immediate relationships, and with what support depended on the method of analysis. Bradford (2002) discussed evolution in Cunonieae.

Synonymy: Baueraceae Lindley, Belangeraceae J. Agardh, Callicomaceae J. Agardh, Davidsoniaceae Bange, Eucryphiaceae Gay, nom. cons., Spiraeanthemaceae Doweld

[Elaeocarpaceae [Brunelliaceae + Cephalotaceae]]: K/P valvate; inner integument 3-5 cells across.

ELAEOCARPACEAE Jussieu, nom. cons.   Back to Oxalidales

Elaeocarpaceae

Trees or (ericoid) shrublets; pyrrolizidine and tropane alkaloids, etc., ellagic acid +; growth rings common; vessel elements in radial multiples and with simple (scalariform) perforations; fibres often septate; (nodes 1:1); petiole bundle annular, often with medullary (and wing) bundles; (epidermis mucilaginous), stomata anomo- para-, actino- or cyclocytic; leaves spiral or opposite (two-ranked), simple, lamina vernation variable, margins toothed (entire), secondary veins pinnate or palmate, stipules lateral (0), (colleters +); inflorescence racemose or cymose or flowers axillary; flowers pendant, (4-merous), pedicels articulated (0); K (4-9), (connate), (± petal-like), C (0, 3-6), aestivation (induplicate-)valvate (cochlear), margins fringed/toothed (entire), with three traces; nectary large, androgynophore + (0); A (1)2 x K-many, centrifugal, (± in groups opposite sepals), anthers basifixed, filaments shorter than anthers, anthers tubular-porose or with short slits, (endothecium of stone cells - Elaeocarpus), (connective prolonged), with lignified hairs; G (1) [2-many], placenta various, lignified hairs in the loculi, style single, (apex shortly branched), stigma ± punctate; ovules 1-many/carpel, (epitropous), ± hairy, micropyle zig-zag, outer integument 2-6 cells across, inner integument 3-7(-17 - Tremandra et al.) cells across, parietal tissue 3-4 cells across, nucellar cap 0, endothelium + (?0), (hypostase +), (long supra-chalazal zone and sort-of-postament), (curved chalazal appendage +); (megaspore mother cells several); fruit a loculicidal capsule (loculicidal + septicidal), spiny or not, or drupe (berry); when capsules, seeds hairy, with chalazal, raphal or integumentary aril, or apical chalazal strophiole, or not, testal cells ± elongated, thickened and lignified (sarcotesta +; endotesta not crystalliferous), tegmen with vascular bundles, (multiplicative), (endotegmen lignified); endosperm ± copious, oily, initially starchy [Tremandra, etc.], embryo green [1 record], (curved - Sericolea, some Elaeocarpus); n = 12, 14, 15, 21.

12[list]/605: Elaeocarpus (350), Sloanea (150), Tetratheca (50). Tropical, esp. Papuasia-Australia, not mainland Africa (map: from Vester 1940; van Balgooy 1993: for early Tertiary fosssils [green], see Manchester & Kvacek 2009). [Photo - Flower, Fruit.]

Age. The age of this node has been estimated at (63-)59, 56(-52) m.y. (Wikström et al. 2001). Other estimates are (55-)42, 38(-27) m.y. (Bell et al. 2010) or over 100 m.y. (Crayn et al. 2006).

Fruits and leaves identified as Sloanea are known quite widely from the early Palaeocene (late Danian) onwards (Kvacek et al. 2001b), and the family may also occur in North America in the Late Cretaceous (Manchester & Kvacek 2009).

Evolution. Divergence & Distribution. Divergence of the distinctive xeromorphic Australian Tremandra et al. clade occurred some (42-)29, 26(-15) m.y.a. (Bell et al. 2010) or 64 m.y.a., diversification within it beginning some 37 m.y.a. (Crayn et al. 2006).

Genes & Genomes. Although there seems to have been elevated molecular divergence in the Tremandra et al. clade, it is distinctly less speciose than its sister clade, which includes Elaeocarpus, by far the largest genus in the family (Crayn et al. 2006).

Chemistry, Morphology, etc. The corolla is more or less (induplicate-)valvate, at least near its insertion, each petal enclosing a group of stamens, and the corolla is larger than the calyx in advanced bud (it is usually smaller in rosids). There are lignified hairs on the insides of the ovary loculi. These and many other similarities strongly link the old Tremandraceae and Elaeocarpaceae (Matthews & Endress 2002a).

Leaf teeth have a single vein running to an opaque (non)glandular deciduous apex. Juvenile leaves of Sloanea may be pinnate. The sepals may be more or less petaloid and the petals can vary considerably in width within the same flower; in some species they are connate. The androecium is very variable, and sometimes, when there are many stamens, they are clearly fasciculate; Venkata Rao (1953a) suggested that in Elaeocarpus there were antesepalous groups of stamens and single antepetalous stamens. Seeds and fruits are also very variable. Some species of Elaeocarpus have curved embryos.

Information on embryology is taken from Mauritzon (1934f) and Venkata Rao (1953a), on wood anatomy from Gasson (1996), and on seed anatomy, etc., of Tremandraceae from Boeswinkel (1999: similarity with that of Linaceae noted). See Coode (2004) for a general account of the expanded family.

Phylogeny. In Bradford and Barnes (2001) monophyly of Elaeocarpaceae was not established, but sampling in that part of Oxalidales was poor. However, monophyly is strongly supported in the more detailed analysis of Crayn et al. (2006: 88% bootstrap, 99% p.p.). The well-supported clade [Sloanea [Vallea + Aristotelia]] was sister to the rest of the family, [Crinodendron + Peripentadenia] and Dubouzetia perhaps being successively sister to [old Tremandraceae + [Sericolea, Aceratium, Elaeocarpus]], but there was little resolution of this latter group.

Previous Relationships. Elaeocarpaceae were previously usually placed either in (Cronquist 1981) or adjacent to (Takhtajan 1997) Malvales, but there are numerous differences (e.g. absence of mucilage, indumentum type). Tremandraceae have long been of very uncertain position, for example, they were placed in Rosidae-Vochysiales (Takhtajan 1997) or Pittosporales (Cronquist 1981).

Synonymy: Aristoteliaceae Dumortier, Tetrathecaceae R. Brown, Tremandraceae Candolle, nom. cons.

[Brunelliaceae + Cephalotaceae]: inflorescence cymose; P uniseriate; A 2 x P; G free, styles recurved, stigma decurrent; ovules ca 2 /carpel, basal; fruit a follicle.

Chemistry, Morphology, etc. An odd couple, but Cephalotaceae will make strange bed-fellows wherever they go, but see Matthews and Endress (2006b) for other characters possibly linking the two.

BRUNELLIACEAE Engler, nom. cons.   Back to Oxalidales

Brunelliaceae

Woody; chemistry?; cork?; vessel elements with simple and scalariform perforations; (nodes 5:5); petiole bundles annular or D-shaped, wing bundles +/0; stomata actinocyclic (anomocytic); hairs unicellular; leaves opposite, stipellate, leaflet vernation conduplicate, 2ndaries prominent, proceeding to the (doubly toothed) margin, stipules cauline; breeding system various; flowers small, 4-8-merous; A (3 x P), obdiplostemonous; pollen reticulate(-rugulate) to punctate; nectary +; G 2-8, carpels also alternating with C; ovules 2/carpel, epitropous, inner integument ca 4 cells across, obturator +; endocarp separating from the rest in fruit, K persistent; seeds shiny, raphe ± aril-like, coat with subepidermal sclerenchymatous layer and palisade innermost layer; endosperm mealy, cotyledons ?incumbent; n = 14.

1[list]/55. Central and South America and the Antilles; more or less montane (map: from Cuatrecasas 1970; note that Orozco Pardo 2002 does not include the easterly locations in South America). [Photo - Flower, Fruit.]

Chemistry, Morphology, etc. The nodes are described as being unilacunar (Orozco Pardo 2002; Orozco & Coba 2002), but there is some confusion here, and some nodes illustrated by Orozco Pardo (2002) certainly do not look unilacunar. The inner androecial whorl may have twice as many stamens as perianth members. There are pistillodes in staminate flowers and staminodes in carpellate flowers. The ovules are epitropous, unlike those of most Cunoniaceae. Pollen morphology is uninformative (Orozco 2001b). There are often five traces to each carpel. Orozco Pardo (2002) described the seeds as being arillate.

For general information, see Cuatrecasas (1970, 1985), Orozco Pardo (2002) and Kubitzki (2004b), for anatomy, Gregory (1998) and Orozco and Coba (2002), and for seed coat (which needs more study), Naranho and Huber (1971) and Danilova (1996).

Phylogeny. Orozco Pardo (2002) provides a morphology-based species level phylogeny of Brunelliaceae, together with comments on the biogeography of the genus.

CEPHALOTACEAE Dumortier, nom. cons.   Back to Oxalidales

Cephalotaceae

Herbs, carnivorous [insectivorous]; flavanols and ellagic acid +, tannin 0; cork?; vessel elements with ?scalariform perforations; true tracheids +; young stem with separate vascular bundles; nodes ?1:1; petiole bundles annular; stomata anomocytic; leaves spiral, simple, margins entire, some ascidiate, stipules 0; inflorescence scapose, racemose, branches scorpioid cymes; flowers 6-merous, hypanthium +, broad; P cucullate; nectary with glandular projections, esp. alternating with P; anthers ± incurved, anther connective with a glandular tip; G 6, carpels plicate, loculi filled with secretion, styles initially straight; ovules 1(2)/carpel, ?type, micropyle bi/endostomal, inner integument 3-5 cells across; hypanthium accrescent in fruit; seed coat mostly collapsed, exotesta papillate; endosperm development?, slight, embryo long, cotyledons accumbent; n = 10.

1[list]/1: Cephalotus follicularis. S.W. Australia (map: from FloraBase viii.2012). [Photo - Habit, Plant © H. Schneider.]

Evolution. Ecology & Physiology. There are nectar glands in the mouth of the pitcher which may faciltate the capture of insects (Bauer et al. 2008); Cephalotus produces enzymes in the pitcher (Peroutka et al. 2008b; Adlassnig et al. 2011).

Chemistry, Morphology, etc. Some information is taken from Diels (1930a), Jay and Lebreton (1973), Froebe and Baur (1988: the trap, a modified pinnate leaf), Danilova (1996), Gregory (1998: anatomy), Conran (2004: general) and the Carnivorous Plants Database; see also Lloyd (1942), Juniper et al. (1989) and McPherson (2010), all general.

Previous Relationships. Cephalotaceae were included in a heterogeneous Rosales by Cronquist (1981) where they were surrounded by families now included in Saxifragales; Cephalotales immediately followed Saxifragales in the system of Takhtajan (1997).