EMBRYOPSIDA Pirani & Prado
Gametophyte dominant, independent, multicellular, initially ±globular, not motile, branched; showing gravitropism; acquisition of phenylalanine lysase* [PAL], flavonoid synthesis*, microbial terpene synthase-like genes +, triterpenoids produced by CYP716 enzymes, phenylpropanoid metabolism [development of phenolic network], xyloglucans in primary cell wall, side chains charged; plant poikilohydrous [protoplasm dessication tolerant], ectohydrous [free water outside plant physiologically important]; thalloid, leafy, with single-celled apical meristem, tissues little differentiated, rhizoids +, unicellular; chloroplasts several per cell, pyrenoids 0; glycolate metabolism in leaf peroxisomes [glyoxysomes]; centrioles/centrosomes in vegetative cells 0, microtubules with γ-tubulin along their lengths [?here], interphase microtubules form hoop-like system; metaphase spindle anastral, predictive preprophase band + [with microtubules and F-actin; where new cell wall will form], phragmoplast + [cell wall deposition centrifugal, from around the anaphase spindle], plasmodesmata +; antheridia and archegonia +, jacketed*, surficial; blepharoplast +, centrioles develop de novo, bicentriole pair coaxial, separate at midpoint, centrioles rotate, associated with basal bodies of cilia, multilayered structure + [4 layers: L1, L4, tubules; L2, L3, short vertical lamellae] (0), spline + [tubules from L1 encircling spermatid], basal body 200-250 nm long, associated with amorphous electron-dense material, microtubules in basal end lacking symmetry, stellate array of filaments in transition zone extended, axonemal cap 0 [microtubules disorganized at apex of cilium]; male gametes [spermatozoids] with a left-handed coil, cilia 2, lateral; oogamy; sporophyte +*, multicellular, growth 3-dimensional*, cuticle +*, plane of first cell division transverse [with respect to long axis of archegonium/embryo sac], sporangium and upper part of seta developing from epibasal cell [towards the archegonial neck, exoscopic], with at least transient apical cell [?level], initially surrounded by and dependent on gametophyte, placental transfer cells +, in both sporophyte and gametophyte, wall ingrowths develop early; suspensor/foot +, cells at foot tip somewhat haustorial; sporangium +, single, terminal, dehiscence longitudinal; meiosis sporic, monoplastidic, MTOC [MTOC = microtubule organizing centre] associated with plastid, sporocytes 4-lobed, cytokinesis simultaneous, preceding nuclear division, quadripolar microtubule system +; wall development both centripetal and centrifugal, 1000 spores/sporangium, sporopollenin in the spore wall* laid down in association with trilamellar layers [white-line centred lamellae; tripartite lamellae]; nuclear genome [1C] <1.4 pg, main telomere sequence motif TTTAGGG, KNOX1 and KNOX2 [duplication] and LEAFY genes present, ethylene involved in cell elongation; chloroplast genome with close association between trnLUAA and trnFGAA genes [precursors for starch synthesis], tufA, minD, minE genes moved to nucleus; mitochondrial trnS(gcu) and trnN(guu) genes +.
Many of the bolded characters in the characterization above are apomorphies of 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.
Sporophyte well developed, branched, branching apical, dichotomous, potentially indeterminate; hydroids +; stomata on stem; sporangia several, terminal; spore walls not multilamellate [?here].
TRACHEOPHYTA / VASCULAR PLANTS
Sporophyte long lived, cells polyplastidic, photosynthetic red light response, stomata open in response to blue light; plant homoiohydrous [water content of protoplasm relatively stable]; control of leaf hydration passive; plant endohydrous [physiologically important free water inside plant]; PIN[auxin efflux facilitators]-mediated polar auxin transport; (condensed or nonhydrolyzable tannins/proanthocyanidins +); xyloglucans with side chains uncharged [?level], in secondary walls of vascular and mechanical tissue; lignins +; roots +, root hairs and root cap +; stem apex multicellular [several apical initials, no tunica], with cytohistochemical zonation, plasmodesmata formation based on cell lineage; vascular development acropetal, tracheids +, in both protoxylem and metaxylem, G- and S-types; sieve cells + [nucleus degenerating]; endodermis +; stomata numerous, involved in gas exchange; leaves +, vascularized, spirally arranged, blades with mean venation density ca 1.8 mm/mm2 [to 5 mm/mm2], all epidermal cells with chloroplasts; sporangia adaxial, columella 0; tapetum glandular; ?position of transfer cells; MTOCs not associated with plastids, basal body 350-550 nm long, stellate array in transition region initially joining microtubule triplets; archegonia embedded/sunken [only neck protruding]; suspensor +, shoot apex developing away from micropyle/archegonial neck [from hypobasal cell, endoscopic], root lateral with respect to the longitudinal axis of the embryo [plant homorhizic].[MONILOPHYTA + LIGNOPHYTA]
Sporophyte growth ± monopodial, branching spiral; roots endomycorrhizal [with Glomeromycota],lateral roots +, endogenous; G-type tracheids +, with scalariform-bordered pits; leaves with apical/marginal growth, venation development basipetal, growth determinate; sporangium dehiscence by a single longitudinal slit; cells polyplastidic, MTOCs diffuse, perinuclear, migratory; blepharoplasts +, paired, with electron-dense material, centrioles on periphery, male gametes multiciliate; nuclear genome size [1C] = 7.6-10 pg [mode]; chloroplast long single copy ca 30kb inversion [from psbM to ycf2]; mitochondrion with loss of 4 genes, absence of numerous group II introns; LITTLE ZIPPER proteins.
Sporophyte woody; stem branching lateral, meristems axillary; lateral root origin from the pericycle; cork cambium + [producing cork abaxially], vascular cambium bifacial [producing phloem abaxially and xylem adaxially].
Growth of plant bipolar [roots with positive geotropic response]; plants heterosporous; megasporangium surrounded by cupule [i.e. = unitegmic ovule, cupule = integument]; pollen lands on ovule; megaspore germination endosporic [female gametophyte initially retained on the plant].
EXTANT SEED PLANTS / SPERMATOPHYTA
Plant evergreen; nicotinic acid metabolised to trigonelline, (cyanogenesis via tyrosine pathway); microbial terpene synthase-like genes 0; primary cell walls rich in xyloglucans and/or glucomannans, 25-30% pectin [Type I walls]; lignin chains started by monolignol dimerization [resinols common], particularly with guaiacyl and p-hydroxyphenyl [G + H] units [sinapyl units uncommon, no Maüle reaction]; root stele diarch to pentarch, xylem and phloem originating on alternating radii, cork cambium deep seated; stem apical meristem complex [with quiescent centre, etc.], plasmodesma density in SAM 1.6-6.2[mean]/μm2 [interface-specific plasmodesmatal network]; eustele +, protoxylem endarch, endodermis 0; wood homoxylous, tracheids and rays alone, tracheid/tracheid pits circular, bordered; mature sieve tube/cell lacking functioning nucleus, sieve tube plastids with starch grains; phloem fibres +; cork cambium superficial; leaf nodes 1:1, a single trace leaving the vascular sympodium; leaf vascular bundles amphicribral; guard cells the only epidermal cells with chloroplasts, stomatal pore with active opening in response to leaf hydration, control by abscisic acid, metabolic regulation of water use efficiency, etc.; axillary buds +, exogenous; prophylls two, lateral; leaves with petiole and lamina, development basipetal, lamina simple; sporangia borne on sporophylls; spores not dormant; microsporophylls aggregated in indeterminate cones/strobili; grains monosulcate, aperture in ana- position [distal], primexine + [involved in exine pattern formation with deposition of sporopollenin from tapetum there], exine and intine homogeneous, exine alveolar/honeycomb; ovules with parietal tissue [= crassinucellate], megaspore tetrad linear, functional megaspore single, chalazal, sporopollenin 0; gametophyte ± wholly dependent on sporophyte, development initially endosporic [apical cell 0, rhizoids 0, etc.]; male gametophyte with tube developing from distal end of grain, male gametes two, developing after pollination, with cell walls; female gametophyte initially syncytial, walls then surrounding individual nuclei; embryo cellular ab initio, suspensor short-minute, embryonic axis straight [shoot and root at opposite ends; plant allorhizic], cotyledons 2; embryo ± dormant; chloroplast ycf2 gene in inverted repeat, trans splicing of five mitochondrial group II introns, rpl6 gene absent; whole nuclear genome duplication [ζ - zeta - duplication], two copies of LEAFY gene, PHY gene duplications [three - [BP [A/N + C/O]] - copies], 5.8S and 5S rDNA in separate clusters.
ANGIOSPERMAE / MAGNOLIOPHYTA
Lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, apigenin and/or luteolin scattered, [cyanogenesis in ANA grade?], lignin also with syringyl units common [G + S lignin, positive Maüle reaction - syringyl:guaiacyl ratio more than 2-2.5:1], hemicelluloses as xyloglucans; root cap meristem closed (open); pith relatively inconspicuous, lateral roots initiated immediately to the side of [when diarch] or opposite xylem poles; origin of epidermis with no clear pattern [probably from inner layer of root cap], trichoblasts [differentiated root hair-forming cells] 0, hypodermis suberised and with Casparian strip [= exodermis]; shoot apex with tunica-corpus construction, tunica 2-layered; starch grains simple; primary cell wall mostly with pectic polysaccharides, poor in mannans; tracheid:tracheid [end wall] plates with scalariform pitting, wood parenchyma +; sieve tubes enucleate, sieve plate with pores (0.1-)0.5-10< µm across, cytoplasm with P-proteins, not occluding pores of plate, companion cell and sieve tube from same mother cell; ?phloem loading/sugar transport; nodes 1:?; dark reversal Pfr → Pr; protoplasm dessication tolerant [plant poikilohydric]; stomata randomly oriented, brachyparacytic [ends of subsidiary cells level with ends of pore], outer stomatal ledges producing vestibule, reduction in stomatal conductance with increasing CO2 concentration; lamina formed from the primordial leaf apex, margins toothed, development of venation acropetal, overall growth ± diffuse, secondary veins pinnate, fine venation hierarchical-reticulate, (1.7-)4.1(-5.7) mm/mm2, vein endings free; flowers perfect, pedicellate, ± haplomorphic, protogynous; parts free, numbers variable, development centripetal; T +, petal-like, each with a single trace, outer members not sharply differentiated from the others, not enclosing the floral bud; A many, filament not sharply distinguished from anther, stout, broad, with a single trace, anther introrse, tetrasporangiate, sporangia in two groups of two [dithecal], each theca dehiscing longitudinally by a common slit, ± embedded in the filament, walls with at least outer secondary parietal cells dividing, endothecium +, cells elongated at right angles to long axis of anther; tapetal cells binucleate; microspore mother cells in a block, microsporogenesis successive, walls developing by centripetal furrowing; pollen subspherical, tectum continuous or microperforate, ektexine columellate, endexine lamellate only in the apertural regions, thin, compact, intine in apertural areas thick, pollenkitt +; nectary 0; carpels present, superior, free, several, spiral, ascidiate [postgenital occlusion by secretion], stylulus at most short [shorter than ovary], hollow, cavity not lined by distinct epidermal layer, stigma ± decurrent, carinal, dry; suprastylar extragynoecial compitum +; ovules few [?1]/carpel, marginal, anatropous, bitegmic, micropyle endostomal, outer integument 2-3 cells across, often largely subdermal in origin, inner integument 2-3 cells across, often dermal in origin, parietal tissue 1-3 cells across, nucellar cap?; megasporocyte single, hypodermal, functional megaspore lacking cuticle; female gametophyte lacking chlorophyll, four-celled [one module, nucleus of egg cell sister to one of the polar nuclei]; ovule not increasing in size between pollination and fertilization; pollen grains bicellular at dispersal, germinating in less than 3 hours, siphonogamy, pollen tube unbranched, growing towards the ovule, between cells, growth rate (20-)80-20,000 µm/hour, apex of pectins, wall with callose, lumen with callose plugs, penetration of ovules via micropyle [porogamous], whole process takes ca 18 hours, distance to first ovule 1.1-2.1 mm; male gametophytes tricellular, gametes 2, lacking cell walls, ciliae 0, double fertilization +, ovules aborting unless fertilized; P deciduous in fruit; mature seed much larger than fertilized ovule, small [<5 mm long], dry [no sarcotesta], exotestal; endosperm +, ?diploid, cellular, development heteropolar [first division oblique, micropylar end initially with a single large cell, divisions uniseriate, chalazal cell smaller, divisions in several planes], copious, oily and/or proteinaceous, embryo short [<¼ length of seed]; plastid and mitochondrial transmission maternal; Arabidopsis-type telomeres [(TTTAGGG)n]; nuclear genome [1C] <1.4 pg [mean 1C = 18.1 pg, 1 pg = 109 base pairs], whole nuclear genome duplication [ε/epsilon event]; ndhB gene 21 codons enlarged at the 5' end, single copy of LEAFY and RPB2 gene, knox genes extensively duplicated [A1-A4], AP1/FUL gene, paleo AP3 and PI genes [paralogous B-class genes] +, with "DEAER" motif, SEP3/LOFSEP and PHYA/PHYCgene pairs.
[NYMPHAEALES [AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]]: wood fibres +; axial parenchyma diffuse or diffuse-in-aggregates; pollen monosulcate [anasulcate], tectum reticulate-perforate [here?]; ?genome duplication; "DEAER" motif in AP3 and PI genes lost, gaps in these genes.
[AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]: phloem loading passive, via symplast, plasmodesmata numerous; vessel elements with scalariform perforation plates in primary xylem; essential oils in specialized cells [lamina and P ± pellucid-punctate]; tension wood + [reaction wood: with gelatinous fibres, G-fibres, on adaxial side of branch/stem junction]; anther wall with outer secondary parietal cell layer dividing; tectum reticulate; nucellar cap + [character lost where in eudicots?]; 12BP [4 amino acids] deletion in P1 gene.
[[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]] / MESANGIOSPERMAE: benzylisoquinoline alkaloids +; sesquiterpene synthase subfamily a [TPS-a] [?level], polyacetate derived anthraquinones + [?level]; outer epidermal walls of root elongation zone with cellulose fibrils oriented transverse to root axis; P more or less whorled, 3-merous [?here]; pollen tube growth intra-gynoecial; extragynoecial compitum 0; carpels plicate [?here]; embryo sac monosporic [spore chalazal], 8-celled, bipolar [Polygonum type], antipodal cells persisting; endosperm triploid.
[MONOCOTS [CERATOPHYLLALES + EUDICOTS]]: (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], x = 21, 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 , (G [3, 4]), whorled, 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).
[BERBERIDOPSIDALES [SANTALALES [CARYOPHYLLALES + ASTERIDS]]] / ASTERIDS ET AL. / SUPERASTERIDS : ?
[SANTALALES [CARYOPHYLLALES + ASTERIDS]]: ?
[CARYOPHYLLALES + ASTERIDS]: seed exotestal; embryo long.
Age. The age of this node may be Albian, some 111-104 m.y.a. (Wikström et al. 2001) or 116-114 m.y.a. (Anderson et al. 2005). Magallón and Castillo (2009) estimated ca 110.7 and 111.3 m.y. for relaxed and constrained penalized likelihood ages, Moore et al. (2010: 95% HPD) proposed a somewhat younger (104-)100(-95) m.y. age, Naumann et al. (2013) ages of around 107.1-103.2 m.y., Xue et al. (2012) the youngest ages of about 97.6 or 93.5 m.y., while Foster et al. (2016a: q.v. for details) estimated an age of about 125 m.y. and Tank and Olmstead (2017) and Z. Wu et al. (2014) the oldest ages of (149.4-)132.2(-115.8) and around 153 m.y. respectively.
Evolution. Ecology & Physiology. There is a variety of companion cell morphologies in the phloem. Transfer cells, companion cells with few plasmodesmata but numerous wall ingrowths, and intermediary cells, characterized by having numerous plasmodesmata that branch in the outer part of the walls adjacent to the bundle sheath cells, seem to be notably common in taxa found in this part of the tree (Turgeon et al. 2001; Turgeon 2010: Santalales and Berberidopsidales i.a. not included in study, see also Fabaceae, etc.). There seems to be a correlation between the presence of intermediary cells (see especially Lamiales) and the presence of raffinose and stachyose in the translocate, and active phloem loading of sugars is to be expected with such companion cell morphologies. This has a number of physiological consequences, while also keeping mesophyll tissue low in sugars that might otherwise attract and/or benefit herbivores (Turgeon 2010).
Phylogeny. See the Dilleniales page for discussion on the relationships around here; it is increasingly likely that Caryophyllales are sister to the asterids, whether (e.g. Bell et al. 2010) or not Dilleniales are sister to Caryophyllales, although the former is unlikely.
CARYOPHYLLALES Berchtold & J. Presl Main Tree.
(Odd ecology and/or physiology); plant often not mycorrhizal; root hair cells in vertical files [sampling!]; (tracheids +); (cork pericyclic); perforation plates not bordered; only alternate vascular pitting; scanty vasicentric parenchyma; rays both uni- and multiseriate; ?nodes; lamina margins entire; anther wall with outer secondary parietal cell layer developing directly into the endothecium, inner secondary parietal layer dividing, [i.e. the wall is described as being 4 cells across]; pollen colpate, tectum spinulose; G , when G = K or P, opposite them, style branches long; ovules with outer integument 2-3(-4) cells across, innner integument 2(-3) cells across; fruit a loculicidal capsule; seed testal; embryo long. - 37 families, 749 genera, 11,600 species.
Age. Crown-group Caryophyllales have been dated to 90-83 m.y.a. (Wikström et al. 2001: see position of Rhabdodendraceae); Anderson et al. (2005) suggests figures of 102-99 m.y., while Moore et al. (2010: 95% HPD, based on only two taxa) estimated a mere (71-)67(-63) m.y. and Xue et al. (2012) the still younger ages of ca 64.4 or 50.4 (the lowest estimate) m.y., Magallón and Castillo (2009) ca 94.35 m.y., Bell et al. (2010: Rhabdodendraceae sister to the rest) an age of (115-)106, 99(-91) m.y., and Naumann et al. (2013) an age or around 78.7 m. years. Sun et al. (2013) thought that the crown-group age was only 76-60 m.y.a., Z. Wu et al. (2014) suggest an age of around 119 m.y.a., ca 107.1 m.y.a. is the age suggested by Magallón et al. (2015), and ca 101 or 103 the ages in Hernández-Hernández et al. (2014). However, since some estimates of ages for nodes within Polygonaceae are more than 110 m.y. (Schuster et al. 2013), if these are confirmed, many ages elsewhere in the order will be called into question.
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. Caryophyllales contain ca 6.3% of eudicot diversity (Magallón et al. 1999). Maherali et al. (2016) note that the clade - or at least parts of it - have a high speciation rate, perhaps associated with the herbaceous habit and the absence of mycorrhizae that are common here.
The fossil record of just about the whole of the order is poor. However, X. Wang (2010a: p. 22) was inclined to the idea that Caryophyllales represented a very ancient clade: "Caryophyllales should represent, or at least is close to, the most primitive angiosperms". He compared their flowers to the reproductive structures of the coniferous Voltziales. Less cosmically, Doyle (2012) suggested that tricolpate pollen was "retained" in Caryophyllales.
Cuénoud (2002a, b) summarizes variation in Caryophyllales. There are many unusual characters scattered in the order, but their phylogenetic significance is unclear, partly because of sampling problems; e.g. sampling for anther wall development is not good (Dahlgren & Clifford 1982). Furthermore, members of the basal pectinations in the clade immediately below core Caryophyllales are particularly poorly known. Similarities in sieve tube plastids between Triplarieae (Polygonaceae) and core Caryophyllales are here treated as parallelisms (c.f. Judd & Olmstead 2004). Ronse de Craene (2013: see Table 1) summarized aspects of perianth and androecium morphology and development in the order, optimizing a number of characters. Pantoporate pollen is scattered throughout the order, having evolved at least 14 times here, but only (in this context!) 66 times in all angiosperms (Prieu et al. 2017). Given the variation in carpel number in the clade, it is with some hesitation that three carpels is suggested as the plesiomorphic condition.
S. A. Smith et al. (2017) found that the 13 genome duplications (see below) on which they focussed were quite often associated with shifts in climatic preferences, but there was no tight link between these duplications and increases in diversification rates.
Ecology & Physiology. Caryophyllales - especially Chenopodiaceae s. str. but also the [[Frankeniaceae + Tamaricaceae] [Plumbaginaceae + Polygonaceae]] clade - are notable for the number of taxa that are halophytes, tolerating salt concentrations of 200mM (Flowers & Colmer 2008; Flowers et al. 2010; Bromham 2015; Saslis-Lagoudakis et al. 2016; see also articles in Ann. Bot. 115(3). 2015; White et al. 2017: Na accumulation in both saline and non-saline environments). It is noteworthy that sulphated phenolic compounds occur in the [[Frankeniaceae + Tamaricaceae] [Plumbaginaceae + Polygonaceae]] part of the tree in particular, plants with such compounds often being halophytic - and this combination also includes seagrasses (McMillan et al. 1980). Furthermore, families scattered through this clade - Plumbaginaceae, Caryophyllaceae, Chenopodiaceae s. str., Tamaricaceae and Nyctaginaceae are examples (see also Douglas & Manos 2007) - include a number of species that are gypsophiles (gypsum = hydrous calcium sulphate) and so have to be able to handle sulphur (Escudero et al. 2014; Moore et al. 2016; C. T. Muller et al. 2017). Perhaps associated with theae ecological features, Lee et al. (2011) found that genes involved in metabolic processes involving sulphur compounds clustered at this node. Interestingly, Caryophyllales are often not associated with arbuscular mycorrhizal fungi (AMF - but see Newman & Reddell 1987), yet such fungi seem to be distinctive in gypsum-derived soils (Escudero et al. 2014 and references) - and there is perhaps a parallel here with Brassicales...
Cornwell et al. (2014) found that plants in Caryophyllales were characterized by being relatively small and having relatively high leaf nitrogen. S. A. Smith et al. (2017) noted that relatively very few Caryophyllales were to be found in wet ecosystems, the majority prefering (much) drier conditions. Taxa with other distinctive habits (e.g. grapnel climbers) or physiology (carnivory, C4 pathway, CAM) or both are also common in this clade. Perhaps associated with this ecological diversity are various distinctive anatomical features that are notably common here (see also Carlquist 2010), these include anomalous secondary thickening (Carlquist 2013) and rayless wood (Carlquist 2015b).
Plant-Animal Interactions. Some chrysomelid beetles - Alticinae, Cassidinae-Hispinae - seem notably more common here than elsewhere (Jolivet & Hawkeswood 1995), and some insects eat taxa in both main groups of this clade (Tempère 1969).
Bacterial/Fungal Associations. Landis et al. (2002) and Trappe (1987) suggested that both Polygonales and Caryophyllales (here just the one order) commonly lacked arbuscular mycorrhizal (AM) fungal associates, although there are exceptions, e.g. some Nyctaginaceae and Amaranthaceae (see e.g. Brundrett 2017b). Indeed, the distinction between non-mycorrhizal and AM condition may not be that clear cut here, as elsewhere. Thus Dianthus deltoides may have AM fungi, vesicles sometimes being produced but arbuscules only rarely, and there may be some movement of carbon from plant to fungus (Lekberg et al. 2015).
Purple-spored smuts and Uromyces rusts parasitize several families, including Plumbaginaceae, Polygonaceae and core Caryophyllales (Savile 1979b: he considered this to be a strong sign that the groups were close).
Genes & Genomes. For possible genome duplications here, see Y. Yang et al. (2015, 2017) and S. A. Smith et al. (2015, 2017). Of the 26 duplications found by Yang et al. (2017), double the number found by Yang et al. (2012), almost half were quite shallow in the tree, characterising species or small groups of species. Some duplications are placed obelow, but these papers should be consulted for the full picture.
The ribosomal rpl23 gene is a pseudogene in the few Caryophyllales examined (Logacheva et al. 2008).
Chemistry, Morphology, etc. Isoflavonoids are scattered in the group (Mackova et al. 2006), perhaps especially in the core Caryophyllales. Flavonol sulphates occur in Plumbaginaceae, Polygonaceae, and Amaranthaceae (Chenopodiaceae s. str.), and sulphated betalains in Phytolaccaceae.
For root hair development, see Dolan and Costa (2001). Carlquist (2010) suggests that few families in Caryophyllales have "truly adult" wood patterns. Placement of several features of wood anatomy on the tree need checking, although Carlquist (e.g. 2002b, 2003a, 2010) has provided a vast amount of detail (see also Core Caryophyllales). Non-bordered perforation plates may be a synapomorphy for Caryophyllales or Caryophyllales and Santalales (Carlquist 2000a; see also Carlquist 2010). Anomalous secondary thickening by successive cambia is widespread - it often occurs in lianes - and there is considerable variation in the morphology of these cambia (Carlquist 2010, much discussion), and such cambia may also occur in the root (see also Bailey 1980). Maximally biseriate rays are also widespread, including in Asteropeiaceae, but not in core Caryophyllales (Nandi et al. 1998). For the leaf and stem anatomy of a number of halophytes of this clade, see Grigore et al. (2014), for general discussion on wood anatomy, see Schwallier et al. (2017).
The outer stamens are often initiated in pairs, especially in core Caryophyllales, but also elsewhere in the order (Ronse Decraene & Smets 1993). A petal and adjacent (antepetalous) stamen are developmental units in Plumbaginaceae and Caryophyllaceae (Friedrich 1956; Ronse Decraene et al. 1998). Tricellular pollen grains are common. Long style branches, or separate styles more or less joining at the apex of the ovary, are widespread. Carpels that are open in development are known both from Polygonaceae and core Caryophyllales (Tucker & Kantz 2001).
It is unclear where the character of starchy endosperm is to be put on the tree. The condition is unfortunately not known for taxa in the pectinations just below core Caryophyllales. Netolitzky (1926), however, noted that taxa that he knew about (and here included in core Caryophyllales) lacked starchy endosperm, and starch was not recorded from the thin endosperm found in the seeds e.g. of some Amaranthaceae (Rocén 1927; Shepherd et al. 2005b and references), while its absence in the endosperm of Phytolacca (Woodford 1924) and Trianthema (Aizoaceae: Cocucci 1961) was also specifically noted. However, Bhargava (1935) recorded starch in the endosperm of Trianthema (Aizoaceae), Narayana and Lodha (1963) reported starch in the young endosperm of Orygia (and Corbichonia: Lophiocarpaceae), Kajale (1940b) noted dense starch grains in the mature endosperm of Amaranthaceae, and Kajale (1954) starch in the endosperm of Rivina humilis (Phytolaccaceae). Although several families of core Caryophyllales are reported to have starchy endosperm in the Flora of China (e.g. Dequan & Gilbert 2003), this is likely to reflect confusion with the starchy perisperm. Those reports aside, the nature of any endosperm reserves in the Rhabdodendraceae to Cactaceae clade remains an open issue, and starchy endosperm is provisionally placed as an apomorphy for the Droseraceae to Polygonaceae clade alone.
Phylogeny. Hilu et al. (2003: matK analysis alone) suggest that Caryophyllales are sister to Asterids, a relationship that has been found in some other studies (e.g. Soltis et al. 1997, c.f. also Nandi et al. 1998). A relationship between Caryophyllales and Dilleniales has also been suggested (D. Soltis et al. 2003a). However, Caryophyllales alone (or perhaps with Santalales) now seem to be sister to the asterids, although the support is still only moderate; see the Pentapetalae page for further discussion.
It has been suggested that there are two main clades within Caryophyllales, one includes the core Caryophyllales, the old Centrospermae, and four small families immediately basal to them, and the other includes Polygonaceae, etc., and a number of carnivorous taxa like Nepenthaceae and Droseraceae. This latter clade is well-supported (Morton et al. 1997b; Soltis et al. 2011), although it was not recovered in the mitochondrial analysis of Qiu et al. (2010) and relationships within it are scrambled in Bell et al. (2010). However, relationships around Polygonaceae now seem stable, but not those in the rest of the clade. This latter includes four carnivorous families that have attracted a lot of attention (see also Albert et al. 1992; Meimberg et al. 2000; Cuénoud et al. 2002; Cameron et al. 2002; Renner & Specht 2010) and other families with distinctive vegetative morphologies (see also Heubl et al. 2006). Metcalfe (1952a) suggested relationships between members of this group based on anatomical similarities. S. Williams et al. (1994) drew atttention to connections between Dioncophyllaceae and Drosophyllum in particular, and Drosophyllum and Nepenthaceae were also found to be weakly associated (Morton et al. 1997b). Soltis et al. (2011) found Drosera and Nepenthes to be sister taxa, but the support was only moderate and sampling not extensive. For detailed relationships, see Meimberg et al. (2000) and Cameron et al. (2002); Drosophyllaceae are sister to Dioncophyllaceae + Ancistrocladaceae, with good support, in an analysis of matK sequences, the position of Nepenthaceae being uncertain (Cuénoud et al. 2002). Indeed, Crawley and Hilu (2013: two genes) found either a weakly supported [Nepenthaceae + Droseraceae] clade, or Nepenthaceae were sister to the rest of the group, depending on the method of analysis, and the latter grouping was also recovered by Brockington et al. (2015). The position of Drosophyllaceae was particularly unstable in the 10-transcriptome study of Walker et al. (2017), while Y. Yang et al. (2017) recovered the relationships [Drosophyllaceae [Nepenthaceae + Droseraceae}}.
Relationships in this immediate area certainly need clarification, but there may be more general problems. Walker et al. (2017) recovered the relationships [Chenopodiaceae [[Frankeniaceae + Tamaricaceae] [[Plumbaginaceae + Polygonaceae] [the carnivorous clade]]]] in some analyses, although a monophyletic group including the first five families was also obtained, as were yet other topologies. Although the focus of this study was on the carnivorous taxa, other sampling being exiguous in the extreme, the basic topology of Caryophyllales used below is clearly called into question here.
Within the other major clade, Rhabdodendraceae were sister to the other members in an early rbcL analysis of Fay et al. (1997b), in the Bayesian analysis of Soltis et al. (2007a) and also in Bell et al. (2010). Cuénoud et al. (2002) found that Simmondsia was grouped with Rhabdodendron in a matK analysis, but with only weak support, but in two- and four-gene analyses (with poorer sampling) it was associated with core Caryophyllales; in trees shown by Drysdale et al. (2007) and Brockington et al. (2007, esp. 2009, 2015) a position of Rhabdodendron as sister to the rest of core Caryophyllales was again found in most analyses, and is adopted here (see also Hilu et al. 2003: matK analysis; Soltis et al. 2011). Relationships around Rhabdodendraceae, etc., are somewhat jumbled in the tree presented by Qiu et al. (2010). Asteropeiaceae and Physenaceae form a well supported pair, in turn showing a well-supported sister group relationship to core Caryophyllales (e.g. Källersjö et al. 1998; Brockington et al. 2015). Similarly, Asteropeiaceae and Simmondsiaceae, the only two taxa from this part of the order that were included, were successively sister groups to the core (D. Soltis et al. 2000). The tree below is based largely on those presented by Meimberg et al. (2000), Cameron et al. (2002: 4 genes) and Cuénoud et al. (2002: matK alone). For relationships within the core Caryophyllales, which are still not fully understood, see below.
Classification. For a classification of Caryophyllales at the family level, including complete generic symonymy, see Hernández-Ledesma et al. (2015). The main difference is that Amaranthaceae and Chenopodiaceae are kept separate there - indeed, no recent progress has been made in understanding major relationships in this clade - and a broad concept of Phytolaccaceae is adopted.
Previous Relationships. Takhtajan's (1997) Plumbaginanae are monotypic; Nepenthanae included Droseraceae and some other Caryophyllales, but also families now in Ericales, etc.. Many of the families in Caryophyllales were included in Cronquist's (1981) Caryophyllidae. Plumbaginaceae are rather similar in a few respects to Primulaceae and relatives and the two have been considered close in the past (see Cronquist 1981 for discussion); Friedrich (1956) had effectively discounted such ideas.
Includes Achatocarpaceae, Aizoaceae, Amaranthaceae, Anacampserotaceae, Ancistrocladaceae, Asteropeiaceae, Barbeuiaceae, Basellaceae, Cactaceae, Caryophyllaceae, Didiereaceae, Dioncophyllaceae, Droseraceae, Drosophyllaceae, Frankeniaceae, Gisekiaceae, Halophytaceae, Kewaceae, Limeaceae, Lophiocarpaceae, Macarthuriaceae, Microteaceae, Molluginaceae, Montiaceae, Nepenthaceae, Nyctaginaceae, Physenaceae, Phytolaccaceae, Plumbaginaceae, Polygonaceae, Portulacaceae, Rhabdodendraceae, Petiveriaceae, Sarcobataceae, Simmondsiaceae, Stegnospermataceae, Talinaceae, Tamaricaceae.
Synonymy: Aizoineae Doweld, Basellineae Doweld, Cactineae Bessey, Caryophyllineae Bessey, Chenopodiineae Engler, Nyctaginineae Doweld, Phytolaccineae Engler, Portulacineae Doweld, Simmondsiineae Reveal, Stegnospermatineae Doweld - Aizoales Boerlage, Alsinales J. Presl, Amaranthales Berchtold & J. Presl, Ancistrocladales Reveal, Atriplicales Horaninow, Cactales Berchtold & J. Presl, Chenopodiales Berchtold & J. Presl, Dioncophyllales Reveal, Droserales Berchtold & J. Presl, Frankeniales Link, Illecebrales Berchtold & J. Presl, Mesembryanthemales Link, Nepenthales Dumortier, Nyctaginales Berchtold & J. Presl, Opuntiales Willkom, Paronychiales Link, Petiveriales Link, Physenales Takhtajan, Phytolaccales Link, Plumbaginales Berchtold & J. Presl, Polygonales Berchtold & J. Presl, Portulacales Berchtold & J. Presl, Reaumuriales Martius, Rhabdodendrales Doweld, Riviniales Martius, Scleranthales Link, Silenales Lindley, Simmondsiales Reveal, Staticales Link, Stellariales Dumortier, Tamaricales Link, Telephiales Link - Caryophyllanae Takhtajan, Nepenthanae Reveal, Plumbaginanae Reveal, Polygonanae Reveal, Rhabdodendranae Doweld, Simmondsianae Doweld - Caryophyllidae Takhtajan, Plumbaginidae C. Y. Wu, Polygonidae C. Y. Wu - Amaranthopsida Horaninov, Cactopsida Brogniart, Caryophyllopsida Bartling, Opuntiopsida Endlicher, Polygonopsida Brongniart, Plumbaginopsida Endlicher
[[Droseraceae [Nepenthaceae [Drosophyllaceae [Ancistrocladaceae + Dioncophyllaceae]]]] [[Frankeniaceae + Tamaricaceae] [Plumbaginaceae + Polygonaceae]]]: acetogenic naphthoquinones + [inc. plumbagin]; endosperm starchy.
Age. The age of this clade is perhaps 75-67 m.y. (Wikström et al. 2001); the crown group age in Bell et al. (2010: [Frankenia + Tamarix] sister to the rest) is (100-)91, 86(-77) m.y., while ca 99.3 m.y.a. is the age in Magallón et al.( 2015).
Evolution: Divergence & Distribution. For gland morphology and vascularization in this part of the tree, see T. Renner and Specht (2011); optimisation is not easy. Although sessile, stalked and pit glands are found in the [Plumbaginaceae + Polygonaceae] clade, how similar they are to stalked glands found in some members of the carnivorous clade, and also to the sessile to depressed salt glands in the [Frankeniaceae + Tamaricaceae] clade is unclear; T. Renner and Specht (2011) did not include the latter clade in their study. Conran et al. (2007) noted that Frankeniaceae, Tamaricaceae and Plumbaginaceae all have flat, multicellular glands of subepidermal origin. This is perhaps an apomorphy there (or still higher), with a loss in Polygonaceae.
Genes & Genomes. Walker et al. (2017; see also S. A. Smith et al. 2017) found seven genome duplications in this clade, six being at the family level or within families; they also mention a genome duplication shared by the entire clade, but this seems to refer to the the γ triplication event of the core eudicots.
Chemistry, Morphology, etc. The acetogenic naphthoquinone plumbagin is known from Plumbaginaceae, Droseraceae, Nepenthaceae, and Dioncophyllaceae, and related compounds are found in Polygonaceae (Culham & Gornall 1994; Kovácik & Repcák 2006).
The Carnivorous Clade, = [Droseraceae [Nepenthaceae [Drosophyllaceae [Ancistrocladaceae + Dioncophyllaceae]]]]: plants carnivorous [insectivorous], forming rosette at least when young; inflorescence ± cymose; C contorted; anthers extrorse, dorsifixed; ovary unilocular.
Age. The age of this node in Bell et al. (2010) is (90-)77, 72(-60) m.y., but note the topology there; ca 83 m.y.a. is the age suggested by Magallón et al. (2015) and 83-68 m.y.a. the age in Walker et al. (2017).
Evolution: Divergence & Distribution. For a synapomorphy scheme for the whole group, see in part Albert and Stevenson (1996), Meimberg et al. (2000: the floral characters listed are mostly plesiomorphies), but especially Heubl et al. (2006).
Heubl et al. (2006) suggest that fly-paper traps are the plesiomorphic condition for the group, but where features like this or the possession of circinate leaves and pollen tetrads are placed on the tree will depend on the model of character optimisation used.
Ecology & Physiology. The acquisition of carnivory may have happened more than once here, or it occurred once and then was lost, perhaps more likely given the topologies found (Meimberg et al. 2000; Cameron et al. 2002: see also Schlauer 1997). T. Renner and Specht (2011) suggest scenarios for the evolution of digestive glands, and find that novel chitinase genes - otherwise involved in anti-fungal activities - have become involved in the extracellular degradation of the chitin of arthropods in this clade (Rottloff et al. 2011; T. Renner & Specht 2012). Other digestive enzymes involved seem to be coopted stress-responsive proteins, as is the case in other carnivorous plants like Sarraceniaceae and Cephalotaceae (Fukushima et al. 2017 and references). For much on carnivory, see papers in Ellison and Adamec (2018).
Chemistry, Morphology, etc. For the vegetative morphology of carnivorous members of this clade, see Kaplan (1997, vol. 2: chap. 18). For roots in carnivorous taxa, see Adlassnig et al. 2005).
Heubl and Wistuba (1997) suggested that both Droseraceae and Nepenthaceae had ploidy levels of 8 or 16, based on x = 5 or thereabouts.
For information on acetogenic quinones and alkaloids, see Hegnauer (1986), Bringmann and Pokorny (1995) and Bentley (1998), for carnivory, see Lloyd (1942) and Juniper et al. (1989), and for general information, especially photographs, see McPherson (2010).
DROSERACEAE Salisbury, nom. cons. Back to Caryophyllales
Rosette herbs, (woody; climbers); endomycorrhizae +; flavonols, ellagic acid +; cork?; young stem with separate bundles in one or two rings, medullary rays broad; cambium 0; (medullary vascular bundles +); (spirally-thickened fiber-sclereids +); nodes 1:1; petiole bundles various; stomata also tetracytic or actinocytic; stalked glands with phloem only [Drosera], sessile glands +; leaves adaxially circinate, long-stalked glands or trigger hairs adaxial, leaf moves, stipules +, intrapetiolar, ± fimbriate, or 0; inflorescence terminal, cyme monochasial, (bracts/bracteoles 0); K often connate at base, C ± marcescent; stamens = and opposite sepals (-15 - Dionaea), (introrse), (connective expanded); (tapetum amoeboid); pollen in tetrads, bi- or tricellular, 3-multiporate, pores equatorial [stephanoporate], aperture large and complex, protrusions along the borders of adjoining grains, operculate or not, (with orbicules); G [3(-5)], median member abaxial, styles separate, often bifid, (multifid), (style connate - Dionaea), stigmas expanded, papillate; placentation parietal (basal - Dionaea); ovules 3-many/carpel, parietal tissue often absent, nucellar endothelium +, column of cells in suprachalazal zone; (fruit indehiscent); exotesta palisade or not, (endotesta with U thickenings), endotegmic cells small, ± sclerotic, or mucilaginous; endosperm nuclear, (embryo short); (germination cryptocotylar; cotyledons 0); nuclear genome duplication, n = 5, 5-17, 19, chromosomes <1.5µm (<6µm - Dionaea), (holocentric - some Drosera); chloroplast rpl2 intron 0 [one species!].
3 [list]/205: Drosera (200). World-wide (map: from Hultén 1971; Fl. Austral. 8. 1982; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; Correa A. & Silva 2005). [Photos - Collection, Collection.]
Evolution: Divergence & Distribution. The beginning of diversification within Drosera may date to ca 42 m.y.a., although a pre-continental drift time has also been suggested (Yesson & Culham 2006 and references). Drosera is exceptionally diverse in S.W. Australia, where about one third of the species in the genus grow; diversification may be linked to the onset of the Mediterranean climate there some 15-10 m.y.a.; all told, 163 Australian species are described by Lowrie (2013: vols 1, 2). The Australian pygmy sundew clade includes D. meristocaulis, a plant from Guyana (Rivadavia et al. 2012).
Ecology & Physiology. Aldrovandra and Dionaea both have snap-traps with multicellular trigger hairs. More is known about the functioning of the trap of D. muscipula, Venus's flytrap, which can catch catches spiders, beetles and ants (Younstaedt et al. 2018). Gibson and Waller (2009; see also Williams 2002) discuss the evolution of the these traps in Dionaea , which are unique in angiosperms; they perhaps allow the plant to capture larger prey than it could otherwise utilize. The traps close in 100-300 ms after the trigger hairs have been stimulated twice, i.e. after the leaf senses two action potentials resulting from stimulation of the hairs by the prey, and the movement is aided by the leaf blades changing from concave to convex in shape; the trap becomes hermetically sealed and the prey is then bathed in digestive enzymes after five such action potentials (Forterre et al. 2005; Volkov et al. 2008; Böhm et al. 2016a, b; Heldrich & Neher 2018: general summary). Kreuzwieser et al. (2014) noted that the leaves have a sweet scent, perhaps mimicking the smell of fruit that would attract fruit flies to the leaves, however, Williams and Hartmeyer (2017) found that in the wild its prey is largely other than flies, 70% consisting of spiders, ants and beetles. Escalante-Pérez et al. (2011), Volkov and Markin (2014), Böhm et al. (2016a, b) and Bemm et al. (2016) provide details of the physiological changes occuring during closing and the post-closing digestive processes. Scherzer et al. (2017) noted that the contents of the secretory vesicles released follow a sequence that optimizes digestion of the animal - the first vesicles have H+ and Cl-, so the contents of the trap become acid, and later enzymes, etc., are secreted in a process that takes hours or days.
The response is limited to a single leaf, as in Drosera (c.f. Mimosa pudica), and is identical to that caused by wounding with a needle - perhaps not surprising since carnivory is thought to have evolved from plant defence mechanisms, activated by, for instance, damage/chewing by a herbivore (Pavolvic et al. 2017; Heldrich & Neher 2018). In particular, the touch hormone jasmonic acid that is involved in defence responses of the plant, e.g. to herbivory, has been coopted into the process of carnivory in Dionaea. Normally it is involved in signalling cascades that can result in cell death, the production of toxins, etc., while in carnivory it is involved in responses that result in the digestion of the prey (Bemm et al. 2016).
There is quite a variety of hair types in Drosera, and some of these may be comparable with the marginal spines of Dionaea (Hartmeyer & Hartmeyer 2010; Hartmeyer et al. 2013). Thus the leaves of D. glanduligera have rapidly-moving eglandular marginal hairs that can snap tight in as little at 75 ms and that pin the prey against glandular hairs in the centre of the blade (Poppinga et al. 2012). The glandular hairs of Drosera move, sometimes quite quickly, and the whole leaf may bend and envelop the prey, although rather more slowly. Some species of Drosera are sweetly scented (c.f. Dionaea above!), perhaps thereby attracting their prey, indeed, as many as 35 butterflies and moths have been found stuck to a single plant of the large, sprawling D. finlaysoniana (Fleischmann 2016). Dicyphine mirid bugs are able to negotiate the sticky leaf surfaces of Drosera, and this may have implications for nitrogen uptake and plant defence, as in other carnivorous plants like Roridulaceae, since the bugs may eat the trapped insects, nitrogen from bug excreta rather that directly from the prey moving into the plant (see Wheeler & Krimmel 2015 for mirids). The glands of at least some species of Drosera produce a ribonuclease which may aid the plant in obtaining phosphorus from its prey, and perhaps also in defence against viruses (Okabe et al. 2005), and they also secrete a chitinase on stimulation that is involved in insect digestion (Jopcik et al. 2017 and references). However, Wheeler and Carstens (2018) found few changes in gene expression categories in D. capensis compared with non-carnivorous plants, while the proteases in D. capensis that Butts et al. (2016) examined, while homologous to those in other plants, differed in ways that suggested that they might have new functionalities - perhaps new substrate recognition patterns. For further literature, see Peroutka et al. (2008b).
How the traps of Aldrovanda vesiculosa work has been clarified recently. Smaller than the the traps of Dionaea, they are also 3-5 times as fast. Rather than the leaf blades deforming during closure, as in Dionaea, stress accumulates along the midrib (Poppinga & Joyeux 2011; Volkov et al. 2008; see also Adamec 2011b) and there are changes in cell turgor, altogether rather different than what goes on in Dionaea (Westermeier et al. 2018). Given that the smaller leaves of young Dionaea do not have a snap-buckling closure mechanism, the uncertainty of the relationships between Drosera and the other two genera, and the diversity in movement within Drosera itself, there is still much to do to clarify the evolutionary contexts of the various trap mechanisms in the family (see also Gibson & Waller 2009).
Pollination Biology & Seed Dispersal. Dionaea muscipula, at least, rarely eats its pollinators, which are mostly bees and beetles (Youngstaedt et al. 2018).
Bacterial/Fungal Associations. Endomycorrhizae have been reported from Drosera (Fuchs & Haselwandter 2004).
Genes & Genomes. There is a nuclear genome duplication here (Y. Yang et al. 2017; S. A. Smith et al. 2017). For holocentric chromosomes, see Cuacos et al. (2015 and references).
Chemistry, Morphology, etc. Root hais can be up to 15 mm long (Adlassnig et al. 2005). Metcalfe and Chalk (1950) describe distinctive vascular patterns in the inflorescence axis and petiole here. In Drosera aliciae young inflorescences (before flower buds are evident) appear to be abaxially circinate, but this is probably a reflection of the way the monochasial cyme is developing.
The pollen of Drosera and Dionaea is remarkable. When it is hydrated, protrusions develop along the borders of adjoining grains of the tetrad, and in Dionaea and Drosera regia these protrusions persist in the dehydrated state and are operculate (Halbritter et al. 2012).
See Le Maout and Decaisne (1868), Baillon (1887), Kubitzki (2002d), McPherson (2008), papers in Ellison and Adamec (2018), esp. Fleischmann et al. (2018), and the Carnivorous Plants Database for general information, Hegnauer (1966, 1989) for chemistry, Schlauer et al. (2018) for naphthoquinones and hairs, Gregory (1998) for general anatomy, Conran et al. (2007) for gland morphology, Pace (1912), Takahashi and Sohma (1981) for a pollen survey, Venkatasubban (1950) and Boesewinkel (1989) for ovule and seed anatomy, and Hoshi and Kondo (1998) for chromosomes.
Phylogeny. Aldrovandra and Dionaea may be sister taxa; both have snap-traps, although rather different in how they function, n = 6, etc. (Cameron et al. 2002; Rivadavia et al. 2003: little support for the relationship); see also Williams et al. (1994) for phylogeny. Rivadavia et al. (2003) discuss the phylogeny of Drosera. The position of Drosera regia is unclear: In both chromosome number and pollen morphology (it has operculate protrusions in the pollen, rather like Dionaea) it is rather different from other species of Drosera. It may be sister to the rest of the genus, or even closer to the other genera in the family (Rivadavia et al. 2003).
Synonymy: Aldrovandaceae Nakai, Dionaeaceae Rafinesque
[Nepenthaceae [Drosophyllaceae [Ancistrocladaceae + Dioncophyllaceae]]]: fibriform vessel elements +; rays 1-2 cells wide; petiole bundle(s) surrounded by massive sclerenchymatous ring with embedded vascular bundles, wing bundles +; leaves abaxially circinate; anthers basifixed.
Age. This node can be dated to 67-55 m.y. (Wikström et al. 2001).
Chemistry, Morphology, etc. Heubl et al. (2006) place a character, "petiole with cortical vascular bundles" at this node - see above!
NEPENTHACEAE Dumortier, nom. cons. Back to Caryophyllales
Plant a liane, climbing by twining portion of leaves, (± a rosette plant); endomycorrhizae +; flavonols +, ellagic acid 0; cork pericyclic; (medullary vascular bundles +); (vessel elements with scalariform perforation plates); true tracheids +; large spirally-thickened fiber-sclereids [in pith, pericycle, etc.]; SiO2 bodies +; pith lignified; nodes 5-9:5-9; cortical bundles in stem; petiole bundle arcuate; peltate glands +; leaves sessile, base broad, blade in lower half, vernation involute, then narrow twining portion (0), pitcher terminal [epiascidiate],; plant dioecious; inflorescence a raceme, bracts and bracteoles 0; P +, uniseriate, (3-)4, decussate, large flat nectariferous glands adaxially; staminate flowers: A connate into a central column, (4-)8-25; pollen in tetrads, tricellular, apertures 0/indistinct; pistillode 0; carpellate flowers: staminodes?; G [(3-)4(-6)], placentation axile, style short, stigma broad, papillate; ovules many/carpel, bistomal, outer integument becoming very long, parietal tissue 1 cell across, chalazal projection +; seeds numerous, spindle-shaped, minute; chalaza with hair-pin bundle, exotesta with much thickened inner walls; endosperm +, nuclear; n = 40.
1 [list]/160. Madagascar to New Caledonia (map: see Meimberg & Heubl 2006). [Photo - Leaf; Collection.]
Age. Nepenthes is known fossil as pollen from Europe in the Eocene (Krutzsch 1989).
Evolution: Divergence & Distribution. For the biogeography of Nepenthes, see Meimberg and Heubl (2006); some analyses suggest that Malesian Nepenthes (including species from New Caledonia and Australia) are derived from a stock represented by the extant taxa found to the west of Malesia, but different relationships are suggested by different genes. Speciation in the genus is discussed by Clarke and Moran (2016).
Ecology & Physiology. Pavlovic et al. (2007) discuss the physiology of lamina and trap (see also Mithöfer 2011 and references). The liquid in the tank tends to be acid, and contains enzymes from the plant (Peroutka et al. 2008b; Adlassnig et al. 2011). Chitinases involved in the digestion of the insect exoskeleton have also been isolated (Rottloff et al. 2011 and references).
How insects become trapped in the pitchers has long been unclear. Nectar is produced by the pitchers and attracts insects and other animals. Recent work suggests that the rim (peristome) of the pitcher is extremely wettable (see Chen et al. 2016 for a description of how this happens at the nanoscale level), and insects may aquaplane when they step on it, falling in to the pitcher below where they die and get digested; when the rim is dry insects can walk on it easily, but they still may get trapped if the plant has wax-covered inner pitcher walls (Bohn & Federle 2004). The main capture mechanisms correlate with climate, species with epicuticular waxes growing in drier climates (Moran et al. 2013). In another variant of insect capture, insects on the underside of the lid of Nepenthes gracilis are catapulted at high velocity into the pitcher when raindrops fall on the lid; this is because the lids are stiff, but thin, and the cuticle waxes on the lower surface do not provide a good hold for the insects (Bauer et al. 2015). For the fauna living in the liquid in the pitchers, see Kitching (2000) and Bittleson (2018), and for other information, see Adamec (2011b).
On the whole the pitchers seem not to be very efficient at capturing insects (Joel 1988), and the plants may acquire nitrogen in other ways (Moran et al. 2018 for a summary). Thus the ant Camponotus schmitzi lives in domatia on Nepenthes bicalcarata, and it can run across the wetted rim and swim in the fluid in the pitcher; substantial amounts of nitrogen from the excreta of the ant are taken up by the plant (Bazile et al. 2012). Some montane species of Nepenthes with particularly large pitchers capture the faeces of tree shrews (Tupaia montana) and other animals as they feed from glands on the inner surfaces of the lids (Chin et al. 2010; Rice 2011). Similarly, the pitchers may serve as bat roosts, N. rafflesiana var. elongata getting about one third its nitrogen from the faeces of Hardwicke’s woolly bats (Kerivoula hardwickii hardwickii) and having particular modifications so the bat "fits" properly in the picher (Grafe et al. 2011); here the upper part of the pitcher wall reflects bat calls and so orients the animal (e.g. Lim et al. 2015). Finally, nutrients from litter that falls into the trap may be taken up by the plant (Adlassnig et al. 2011; Thorogood et al. 2017 and reference).
Mimicry with flowers has sometimes been invoked as an explanation of the distinctively coloured and shaped pitcher-rims, but this is unlikely (Joel 1988; Ruxton & Schaefer 2011).
Plant-Animal Interactions. For the invertebrates, etc., living in the pitchers and their interactions, see Beaver (1983).
Bacterial/Fungal Associations. Endomycorrhizae have been reported from Nepenthes (Séjalon-Delmas in Delaux et al. 2014).
Chemistry, Morphology, etc. The expanded part of leaf is developed from the leaf base, as in many monocots, the twining petiole and the pitcher from the rest (e.g. Troll 1932); the leaf is epiascidiate, i.e. the inside of the pitcher is developmentally equivalent to the adaxial surface of the lamina, the outside to the abaxial surface (see also Franck 1976).
The outer integument develops greatly after fertilization and forms an exostome (Goebel 1933); there is a hair-pin bundle in the testa (Takhtajan 1988).
For general information, see Cheek and Jebb (2001: almost a monograph), Kubitzki (2002d), McPherson (2008), papers in Ellison and Adamec (2018), esp. Clarke et al. (2018), and the Carnivorous Plants Database, for chemistry, see Hegnauer (1966, 1990), for anatomy, Metcalfe (1952a), Pant and Bhatnagar (1977) and Schwallier et al. (2016, esp. 2017) and for pollen, see Takahashi and Sohma (1981).
Phylogeny. For some relationships within Nepenthes, see Meimberg and Heubl (2006). Nepenthes pervillei, from the Seychelles, and N. madagascariensis were successively sister to the rest of the genus, although support was weak (Alamsyah & Ito 2013).
[Drosophyllaceae [Ancistrocladaceae + Dioncophyllaceae]]: ?
Age. The age of this node is estimated to be around 57.9 m.y. (Magallón et al. 2015).
DROSOPHYLLACEAE Chrtek, Slavíkovà & Studnicka Back to Caryophyllales
Plant woody, small; mycorrhizae?; chemistry?; cortical bundles in stem +, inverted; ?nodes; ?stomata; petiole bundles inverted, three, arcuate, sclerenchyma ring?; stalked and sessile glands with xylem and phloem; leaves linear, stalked glands abaxial, in lines, abaxially circinate, vernation revolute; flowers large, (C contorted), ± marcescent; A 10, attachment?; pollen grains tricellular, tectate, pantoporate, not spiny; G , opposite the K, placentation basal, styles separate, stigmas capitate; ovules several/carpel, parietal tissue ca 1 cell across, funicle long; fruit septicidal; seeds operculate, few; exotesta not palisade, endotesta crystalliferous, with U thickenings, exotegmen thick-walled; endosperm ?, embryo short; n = 6, chromosomes ³15 µm long; germination epigeal, ± cryptocotylar.
1 [list]/1: Drosophyllum lusitanicum. Southern Iberian Peninsula, Morocco (map: from Ortega et al. 1995). [Photos - Collection.]
Evolution. Ecology & Physiology. For carnivory in Drosophyllum, see Plachno et al. (2009) and Bertol et al. (2015); the leaf produces a sweet (?attractive to fruit flies and their like) scent, and catches insects even at night.
Although Drosophyllum looks quite delicate, it grows in very dry conditions and does not dry out fast. The mucilage on the tentacles is hygroscopic and may help the plant maintain a positive water balance (Adamec 2009).
Chemistry, Morphology, etc. Stem/leaf anatomy would repay investigation; both the cortical and petiole bundles appear to be inverted (Metcalfe & Chalk 1950, as Droseraceae).
The flowers are relatively large; the stamens opposite the calyx are longest. Dehiscence of the fruit is down the ribs of the capsule and the valves are opposite the calyx.
For some anatomy, see Metcalfe (1952a), for pollen, see Takahashi and Sohma (1981), for ovule and seed, see Boesewinkel (1989), and for general information, see Kubitzki (2002d), McPherson (2008), papers in Ellison and Adamec (2018), and the Carnivorous Plants Database.
[Ancistrocladaceae + Dioncophyllaceae]: plants woody, lianes; ?mycorrhizae; (acetogenic naphthylisoquinoline alkaloids +); cork deep seated; petiole with inverted bundles in sclerenchyma ring; stomata actinocyclic; A introrse; pollen grain nuclei?; embryo short; germination epigeal, cryptocotylar.
Age. Bell et al. (2010) suggested an age for this clade of (61-)41, 37(-20) m.y., Wikström et al. (2001) an age of 47-29 m.y.; around 36.2 m.y.a. is the age in Magallón et al. (2015) and ca 49.5 m.y. in Tank et al. (2015: Table S2).
Chemistry, Morphology, etc. The cotyledons of Ancistrocladaceae are shown as being recurved structures about the length of the stout hypocotyl/radicle (Gilg 1925), but they have also been described as being "remarkably folded" (Porembski 2002; c.f. Keng 1967). Indeed, the cotyledons as shown in Gilg (1925) are not that dissimilar from those of the three genera in Dioncophyllaceae (Airy Shaw 1952).
For general information, see Airy Shaw (1951), for the distinctive napthyl isoquinoline alkaloids of the clade, see Bringmann (1986), Bringmann and Pokorny (1995), and Bringmann et al. (2008, and references) - since they are synthesised from polyketide precursors, not from aromatic amino acids, so are barely alkaloids in the strict sense, for growth patterns see Cremers (1974) and for anatomy, see Gottwald and Parameswaran (1968) and Metcalfe.
ANCISTROCLADACEAE Walpers, nom. cons. Back to Caryophyllales
Climber, sympodially constructed, stem hooks borne in series, not carnivorous, ?rosette forming; myricetin +, ellagic acid?; spirally-thickened cells in axial parenchyma; nodes 3:3; SiO2 bodies in ray cells [African taxa]; xylem parenchyma apotracheal, banded; cortex with with elongated pitted sclereids, sclereid band indistinct; petiole bundle annular; lamina surface with wax-secreting pit glands [lepidote hairs in crypts], vernation supervolute, ?stipules; pedicels articulated; K quincuncial, unequal in size, (with abaxial glands), C basally connate or not, (imbricate); A (5) 10, whorl opposite petals larger, filaments widened and ± connate basally and adnate to C; nectary narrow raised ring; G [3(-4)], half or more inferior, style short, branches long, stigmas capitate-hippocrepiform or pinnatifid, ?type; ovule single [per flower], basal, hemitropous, outer integument "thick", ?nucellus; fruit a nut, K much enlarged; seed ruminate; exotesta "thin membranaceous"; endosperm cellular, hypocotyl/radicle stout, cotyledons ± recurved; n = ?.
1 [list]/12 (21). Tropical Africa to W. Borneo and Formosa (map: from van Steenis 1949a; Freson 1967; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003, 6. 2011). [Photo - Fruits, Grapnels.]
Chemistry, Morphology, etc. 1/3 species tested had fluorescing wood.
The branching and inflorescence structure are at first sight difficult to understand - however, Ancistrocladus robertsoniorum was flowering at MoBot iv.2017. Here neither inflorescences nor the complex series of hooks are immediately axillary to leaves, and the individual hooks themselves are also not subtended by leaves, although there are what are apparently very reduced leaves considerably below the hooks and the hooks may subtend buds. Massart (1896) early clarified the vegetative architecture of Ancistrocladus, noting appropriately that "few plants have a vegetative body of which the morphology is as complicated" (ibid.: p. 133). The climbing stem is built up of units consisting of two leaves (= prophylls), the axis of the unit then bending laterally and terminating in a hook, a series of sympodial hook units are then produced along this axis, the leaves on them being small. The growth of the climber continues via an orthotropic axillary shoot, and the whole process repeats itself. Cremers (1974) suggested that the upper leaf on the orthotropic module may have as many as five axillary buds, which end up in a variety of positions because of the strange growth of the plant. Most photosynthetic leaves are borne along short shoots. Whether or not the plant has stipules, and what these might be, is unclear (e.g. Taylor et al. 2005).
Porembski (2002: p. 25) described the inflorescences as being "racemes, spikes or dichasially branched panicles". The inflorescence, which is terminal, may have some branches that are hooks (c.f. "mixed" inflorescences in some Vitaceae). The flowers in the branched inflorescences of Ancistrocladus robertsoniorum are not immediately subtended by bracts, although there are small, bract-like structures along the branches of the inflorescences. Interestingly, here it is the stamens opposite the sepals that are longer. The pollen is like that of Dioncophyllaceae (Cronquist 1981).
For for general information, see Keng (1967a), Porembski (2002), Taylor et al. (2005), Heubl et al. (2010), and papers in Ellison and Adamec (2018), for anatomy, see Metcalfe (1952a) and van Tieghem (1903b), and for chemistry, see Hegnauer (1989).
Previous Relationships. In the past Ancistrocladaceae have often been included in Violales or in Theales or Theanae (Cronquist 1981; Takhtajan 1997).
DIONCOPHYLLACEAE Airy Shaw, nom. cons. Back to Caryophyllales
Climbers, (shrubs); cyclopentenoid cyanogenic glycosides +, ellagic acid?; successive cambia +; xylem with included phloem; true tracheids +; wood parenchyma vasicentric or apotracheal-diffuse; nodes ?; cortex with massive band of fibrous tissue; petiole bundles 1-3, arcuate; (stalked and sessile vascularized glands +); (first leaves linear, adaxially circinate, lamina with parallel venation - Triphyophyllum), lamina apex with paired recurved hooks; K valvate or open; A 10-30; pollen not spiny; G [2, 5], placentation parietal, (connate style short), stigmas punctate, capitate (feathery - Triphyophyllum); ovules several/carpel, ?morphology, funicles long; capsule opening before maturity; seeds flattened, broadly winged, green when young; seed coat thick; endosperm ?nuclear, embryo with spreading semicircular cotyledons; n = 12, 18 [both Triphyophyllum peltatum].
3 [list]/3. Tropical West Africa (map: from Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003).
Evolution. Ecology & Physiology. Some leaves in young plants of Triphyophyllum peltatum have a short blade and glandular hairs on the abaxial surface of the midrib, which is prolonged beyond the blade (Green et al. 1979) - and they are abaxially circinate when young, just like the leaves of Drosophyllum. It is at this stage that the plant may capture insects (Bringmann et al. 2001). The paired hooks at the ends of the leaves are apparently sensitive and thus are tendrils (Sousa-Baena et al. 2018b).
Chemistry, Morphology, etc. The report of cyclopentenoid cyanogenic glycosides from Dioncophyllum (Spencer & Seigler 1985b) should be confirmed for the family as a whole.
Androecial variation in Dioncophyllum is considerable - there may be five stamens opposite the petals, ten stamens, or ca 27 stamens... (Airy Shaw 1952).
For anatomy, see Metcalfe (1952a) and Miller (1975), for growth (the curved hooks are series of sympodial units) and seedlings, see Cremers (1974), for chemistry, Hegnauer (1966, as Flacourtiaceae, 1989) and Spencer and Siegler (1985), and for general information, see Airy Shaw (1952), Schmid (1964), Porembski and Barthlott (2002), McPherson (2008: excellent photographs), and the Carnivorous Plants Database.
Previous Relationships. See Airy Shaw (1952) for a summary - the families with which Dioncophyllaceae have been associated are placed in seven orders from Magnoliales to Asterales here... Dioncophyllales were included in Theanae by Takhtajan (1997) and in Violales by Cronquist (1981).
[[Frankeniaceae + Tamaricaceae] [Plumbaginaceae + Polygonaceae]]: vessel elements with minute lateral wall pits +; sulphated flavonols, ellagic acid +; pollen not spiny; ovary 1-locular; outer and inner integuments 2-3 cells across; seed exotestal.
Age. This node is about 93.3 m.y.o. (Magallón et al. 2015).
Evolution. Ecology & Physiology. Evolution of the halophytic habit (e.g. Liphschitz & Waisel 1982; Saslis-Lagoudakis et al. 2016), tolerance of dry conditions, etc., would repay attention here (see also articles in Rajakaruna et al. 2016). Sulphated phenolic compounds are common; plants with such compounds are often halophytic.
Plant-Animal Interactions. There are about 1,000 species in the straight-snouted weevil clade Brentidae-Apioninae-Apionini most of which are to be found on Fabaceae-Faboideae, however, their ancestral aniosperm hosts may have been in this clade (Winter et al. 2016).
Chemistry, Morphology, etc. Whether or not this whole clade is rayless is unclear. There are few records from Polygonaceae, and in Frankenia there may be rays (Carlquist 2015b).
[Frankeniaceae + Tamaricaceae]: halophytic; bisulphated flavonols +, myricetin 0; wood storied; nodes ?; salt glands +; (rhomboidal crystals +); (stomatal orientation transverse); leaves small [<1 cm long], with salt-excreting glands; flowers small, 4-6-merous, C with basal adaxial appendages; pollen not spinulose; G with median member abaxial, placentation (intruded) parietal, (basal), style +, branched, stigmas capitate-clavate; fruit a loculicidal capsule; exotestal cells bulging or as hairs; endosperm +.
Age. This node is dated to 43-30 m.y. (Wikström et al. 2001), ca 49.7 m.y. (Tank et al. 2015: Table S2), or 53.8 m.y. (Magallón et al. 2015).
Evolution: Divergence & Distribution. It is equally parsimonious to assume that petal appendages are apomorphies for the family pair as it is to assume that they have evolved independently. In Tamaricaceae members of the Reamuria, sister to the rest of the family, clade have these appendages. Seeds with copious endosperm have the same distribution.
Chemistry, Morphology, etc. For salt glands, see Fahn (1979 and references) and the discussion above, for ovules, etc., see Mauritzon (1936b).
Phylogeny. The monophyly of the two families and their sister-group relationship were confirmed by Gaskin et al. (2004).
Previous Relationships. Both Frankeniaceae and Tamaricaceae were placed in Violales by Cronquist (1981) and in Violanae by Takhtajan (1997), probably because of their parietal placentation.
FRANKENIACEAE Desvaux, nom. cons. Back to Caryophyllales
Herbs to shrubs; cork pericyclic or subepidermal; fibriform vessel elements +; wood rayless; cuticle wax crystalloids 0; leaves opposite, often ericoid; flowers also 7-merous, K connate, lobes induplicate-valvate, C clawed; A (3-)6(-24), (inner whorl staminodial), slightly connate at the base or not, extrorse, versatile, tapetal cells binucleate; ?nectary; pollen grains tricellular; G [(2-)3(-4)]; ovules (1-)2-6(-many)/carpel, parietal tissue 0, nucellar cap +, funicles long; exotestal cells large, papillate, papillae with terminal nail-like thickenings, endotestal cells thin-walled [?fibers], endotegmen with thick cuticle, tanniniferous; (polyembryony +), coenocytic micropylar endosperm haustorium +; n = 10, 15.
1 [list]/90. ± World-wide in warm, dry areas, but scattered (map: from Fl. Austral. 8. 1982; Whalen 1987; Jäger 1992; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; FloraBase 2004). [Photos - Collection]
Chemistry, Morphology, etc. Some information is taken from Walia and Kapil (1965), Whalen (1987: taxonomy of Old World Frankenia) and Olson et al. (2003: anatomy); for general accounts, see Surgis (1921) and and Kubitzki (2002d).
Phylogeny. For relationships within Frankenia, see Gaskin et al. (2004).
TAMARICACEAE Link, nom. cons. Back to Caryophyllales
Woody, also xeromorphic; (gypsum crystals +); cuticle waxes as tubes or curled rodlets; leaf bases often broad; inflorescence racemose, (flowers solitary, terminal), bracteoles 0; K connate below or not, (C lacking appendages); stamens = or 2x C or more, most connate at base into 5 bundles, development centrifugal, anthers extrorse to introrse, variously attached; nectary ± disciform, with C and A on top, or inside or outside A (0); G [(2-)3-4(-5)], opposite petals, (style short), stigmas wet; ovules 2-many/carpel, parietal tissue 1-2 cells across; embryo sac tetrasporic [a variety of types, even in one species, often 16-nucleate bipolar]; seed with hairs at chalazal end [on chalazal prolongation]; exotestal cells periclinally elongated and thick-walled, endotestal cells thin-walled, crystalliferous; endosperm usu. scanty, oil and protein as reserves, perisperm +, thin (0); n = (11) 12, nuclear genome size [1C] 1.53-1.6 pg.
5 [list]/90: Tamarix (55). Eurasia and Africa, esp. Mediterranean to Central Asia (map: from Hultén & Fries 1986; Meusel et al. 1978; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003), commonly naturalised in North America and elsewhere. [Photos - Collection]
Evolution. Ecology & Physiology. Halophytes are common in Tamaricaceae, perhaps evolving only once (Moray et al. 2015); see also articles in Ann. Bot. 115(3). 2015. In common with some other groups inhabiting saline conditions (Chenopodiaceae, Cactaceae), a number of taxa have very fast germination, i.e. they germinate within one day of imbibition beginning - Salix and Populus also do this, and some are pioneers in along with Tamarix, for example (Parsons 2012; Parsons et al. 2014). S. A. Smith et al. (2017) discuss the evolutionary context of the whole genome duplication here.
Genes & Genomes. A genome duplication is reported here (Y. Yang et al. 2017: Fig. 3; see also S. A. Smith et al.2017).
Chemistry, Morphology, etc. Reaumuria is distinctive in having single terminal flowers, a contorted corolla, and basal adaxial scales on the petals, c.f. Frankeniaceae. It also has many centrifugal stamens arising from 10 primordia, it lacks a nectary, and its seeds have endosperm (Ronse Decraene 1990).
See Frisendahl (1912), Joshi and Kajale (1936) and Johri and Kak (1954) for embryology, Hegnauer (1973, 1990) for chemistry, Czaja (1978) for seed storage, Zhang et al. (2001) for pollen and Gaskin (2002) for a general account.
Phylogeny. Relationships within the family are [[Holachna + Reaumuria] [Myricaria + Tamarix]] (Gaskin et al. 2004). For a phylogeny of Myricaria, see Y. Wang et al. (2009).
Synonymy: Reaumuriaceae Lindley
[Plumbaginaceae + Polygonaceae]: plants herbaceous; O-methylated flavonols, myricetin, quinones +; (SiO2 bodies +); (wood storeyed); cortical and/or medullary vascular bundles +; nodes 3:3; leaf base broad; inflorescence racemose; pollen usu. starchy; G with median member adaxial; stalked, sessile and pit glands +; ovule single [per flower], basal; fruit surrounded by accrescent calyx [usually part of the dispersal unit]; other than ± persistent exotesta, seed coat undistinguished; mitochondrial coxII.i3 intron 0.
Age. This node is dated variously at (125-)118.7, 110.9(-90.7) m.y. (Schuster et al. 2013), (93.3-)76.9(-67.9) m.y. (Magallón et al. 2018), ca 67.9 m.y. (Magallón et al. 2015), (72-)60, 58(-44) m.y. (Bell et al. 2010), ca 59.5 m.y. (Tank et al. 2015: Table S1, S2), or as little as 52-37 m.y. (Wikström et al. 2001).
Evolution: Divergence & Distribution. This whole clade may show an increase in diversification rate (Magallón et al. 2018); it seems to be most diverse immediately away from the tropics (see Kostikova et al. 2014b for Polygonaceae).
Plant-Animal Interactions. Lycaeninae caterpillars are quite commonly found on this family pair, probably because of the polyphenolics in their leaves (Fielder 1995).
Chemistry, Morphology, etc. For sterol composition in comparison to that of core Caryophyllales, see Wolfe et al. (1989). There are early reports that both families have perisperm (see Rocén 1927, p. 169).
For anatomy, see Carlquist and Boggs (1996), for pollen, see Nowicke and Skvarla (1979), and for seed hairs, see Hildebrand (1872).
PLUMBAGINACEAE Jussieu, nom. cons. Back to Caryophyllales
Choline-O-sulphate +, little oxalate accumulation; cork subepidermal or cortical; secondary thickening odd; rays multiseriate; petiole bundles arcuate; vascularized mucilage glands, epidermal salt glands; cuticle wax crystalloids 0 (irregular platelets); stomata also paracytic; distyly common; K connate, ribbed, C contorted; stamens = and opposite petals; pollen with irregular columellae, tectum continuous, itself with columellae, with rather coarse blunt spines; nectary on adaxial side of filament bases (elsewhere); G ; ovule anatropous, parietal tissue 1-3 cells across, funicle long and curled, obturator from wall at apex of ovary; embryo sac tetrasporic, 4-8-nucleate; K green in fruit; endotegmen persistent; endosperm 4n or 5n, little persisting, embryo green; nuclear genome duplication.
Ca 29 [list]/836 (725) - three groups below. Predominantly Mediterranean to Central Asia, scattered elsewhere. [Photos - Collection.]
Age. Crown-group Plumbaginaceae are dated to 40-27 m.y. (Wikström et al. 2001) or 19-17 m.y.a. (Lledó et al. 2005); Bell et al. (2010) suggest a crown-group age of (57-)43(-27) m.y. old.
1. Plumbaginoideae Burnett
Perennial herbs or shrubs; glycine betaine + [plumbaginin]; stems angled and striate; lamina (deeply lobed), petioles often short, (cauline stipules - Plumbago); distyly not associated with major morphological differences between morphs; K herbaceous, glandular, C (connate), lobes truncate-emarginate and then apiculate; style single, stigmatic receptive areas in bouquet-like aggregations along branch; (nucellar cap ca 2 cells across - Plumbagella); fruit a basally circumscissile capsule; n = 6, 7.
4/36. East Asia and Africa, Plumbago pantropical (map: from Baker 1948, probably over-optimistic), Plumbago commonly cultivated.
2. Limonioideae Reveal
Plant often salt tolerant; lamina cartilaginous, with 5-10 marginal rows of whitish cells; C connate; stamens basally adnate to corolla; styles separate.
Age. Crown-group Limonioideae are some 17-16 m.y.o. (Lledó et al. 2005).
2A. Aegialitideae Peng
Shrublet; ellagic acid +; successive cambia +; cortical vascular bundles +; branched sclereids +; leaf base surrounding stem, lamina vernation involute; ?distyly type; stigma punctiform-capitate; fruit much elongated, slender, pentagonal, longitudinally dehiscent [?type]; n = ?
1/2. Indo-Malesia, N. Australia, in mangroves (map: blue, from van Steenis 1949c).
Synonymy: Aegialitidaceae Linczewski
2B. Limonieae Reveal
Perennial herbs or shrubs; glycine betaines usu. 0, then beta-alanine betaines (and other quaternary ammonium compounds) +; leaves ± basal, (lamina margin deeply lobed), petioles often short; inflorescence capitate or branched, cymose, axis channelled, inflorescence scapose, or leaves reduced; distyly accompanied by morphological differences, (plant heterostylous); K scarious (also petal-like); pollen often dimorphic, columellae regular, tectum incomplete, reticulate; style +, branched, or styluli, stigma peltate-capitate or filiform (clavate); fruit an achene or circumscissile capsule; n = 8, 9, 17, 18, etc.; deletion of rpl16 intron.
14/800: Limonium (350), Acantholimon (165), Armeria (100). Mostly Irano-Turanian (Mediterranean), but also S. Africa, S. South America, and W. Australia (map above, red: from Hultén; Baker 1948; FloraBase 2004; Australia's Virtual Herbarium xii.2012).
Synonymy: Armeriaceae Horaninow, Limoniaceae Seringe, nom. cons., Staticaceae Cassel
Evolution: Divergence & Distribution. Lledó et al. (2005, see also 2011) suggest a number of ages for nodes in Limonioideae; calibration was on the age of the island on which the endemic Limonium endroides grew - used as a maximum age.
Limonieae are most diverse in the area from the western Mediterranean to Central Asia. About half the 90 species of Armeria are from the Iberian Peninsula alone. In Limonium there is hybridization, polyploidy (some species are triploids), and hundreds of microspecies, some apomictic, Brullo and Erben (2016) recently describing 39/98 species they recognized from Greece as new. Limonium may originally have been from the Macaronesian-Mediterranean area and it is now most speciose in Eurasia in particular, but odd species are also to be found in Australia, Brazil, etc. (Malekmohammadi et al. 2017). In the Near East to Central Asia genera like Acantholimon are common, and there are 164 species of that genus recognized in the Flora iranica alone (Lledó et al. 2005, 2011; Moharrek et al. 2017).
Ecology & Physiology. Members of the family prefer saline and sometimes rather dry conditions. Species of Limonium and some other Limonieae are succulent halophytes and may grow in salt marshes (Hanson et al. 1994; Flowers & Colmer 2008; Ogburn & Edwards 2010), while Aegilitis of the Aegalitideae is a mangrove plant (Findlay et al. 1967: osmoregulation). For some literature on the halophytic species, see Liphschitz and Waisel (1982) and articles in Ann. Bot. 115(3). 2015. The quaternary ammonium compounds of one sort or another that have been found in practically all members of the family examined are involved in salt excretion, while choline O-sulphate may be involved in sulphate detoxification (Hanson et al. 1994). A number of species (e.g. Armeria, Acantholimon) are cushion plants, which tend to prefer cold and dry climates (Boucher et al. 2016b). Indeed, Acantholimon often grows in dry conditions in the mountains of the Irano-Turanian area and typically is shrubby, more or less tussock-forming, with narrow, rigid leaves and a short inflorescence; interestingly, many of the small segregate genera recently included in Acantholimon look more like Limonium with their broad leaf blades and elongated inflorescences (Moharrek et al. 2017).
Pollination Biology & Seed Dispersal. For distyly in Plumbaginaceae, which reduces selfing, see Costa et al. (2017 and references). It is very variable in expression, for instance, in Plumbago the two floral morphs are quite similar while in Limonium there is very evident heterostyly. For apomixis in Limonium, which has a geographical component, see D'Amato (1949) and Róis et al. (2016 and references).
In a number of Limonieae the calyx becomes scarious in fruit and helps in wind dispersal; in Plumbago the calyx with its sticky glands persists in fruit and attaches to a passing animal.
Genes & Genomes. For a genome duplication, see Y. Yang et al. (2017) and S. A. Smith et al. 2017).
Chemistry, Morphology, etc. Glycine betaine is known from only a very few species of Limonium (and from Plumbago, etc.), but not from Aegalitis and Armeria and other Limonieae (Rhodes & Hanson 1993; Hanson et al. 1994); see Hanson et al. (1994) for choline-O-sulphate distribution.
For wood anatomy, which may be paedomorphic, the family perhaps having a more or less herbaceous ancestry, see Carlquist and Boggs (1996). There is extensive gross anatomical variation that probably can be integrated with the tribes/subfamilies - for example, there is a continuous ring of sclerenchyma outside the phloem in Plumbaginoideae, separate fascicles in Limonioideae, etc. (see Maury 1886). Williams et al. (1994) suggested that it was not known if the mucilage glands were vascularized, although in their data matrix the family was scored as having vascularized glands (see also the discussion above). Leaf vernation is variable, being flat, convolute or involute.
The style branches of Armeria are papillate all around for their entire lengths. Many Plumbaginoideae seem to lack a protruding obturator (Dahlgren 1916). According to Dahlgren (1916), the embryo sac is tetrasporic but eight-nucleate, but Maheshwari (1947) suggested it was tetrasporic and four-celled, three of the megaspores fused and the mature embryo sac consisted of an egg cell, a single synergid, a tetraploid polar nucleus and a three-nucleate antipodal cell... Aegalitis is little known.
There is much general information in Kubitzki (1993b); see Hegnauer (1969, 1990) for chemistry, Ruhland (1915) for salt-excreting glands, Baker (1948, 1953) variation in floral morphology (pollen, stigmas, etc.), de Laet et al. (1995) floral development, and Dahlgren (1937), Fagerlind (e.g. 1938b) and D'Amato (1940) for embryo sac development.
Phylogeny. Lledó et al. (1998, 2001) suggest phylogenetic relationships within the group, however, Aegialitis is placed as sister to all the rest of the family in some analyses (Savolainen et al. 2000: rbcL only).
For the phylogeny of Limonium, see Lledó et al. (2005: relatives unclear) and especially Malekmohammadi et al. (2017). Moharrek et al. (2014) found the relationships [Acantholimon [Limonium + Armeria]]; focussing on Acantholimon, they found that the old sections of Acantholimon were pulverized. Moharrek et al. (2017) confirmed these earlier findings and noted that there were two major clades within the genus.
Classification. The classification here is based in part on the phylogeny in Lledó et al. (1998, 2001); see also Hernández-Ledesma et al. (2015). There are a number of monotypic genera in Limonieae and generic limits need attention (Hernández-Ledesma et al. 2015); Moharrek et al. (2017) synonymized eight of these small gerea in ,i>Acantholimon.
Previous Relationships. Plumbaginaceae used to be associated with Primulaceae-Primuloideae. Both have stamens opposite the petals, common petal-stamen primordia, and a ± connate corolla (the latter especially in Limonioideae), but the two are not close - for Primulaceae, see Ericales.
POLYGONACEAE Jussieu, nom. cons. Back to Caryophyllales
Shoots monopodial, branching from previous flush; cork subepidermal (pericyclic); dark-staining deposits, esp. in rays; stem bundles distinct, persistent; pits vestured; nodes also 5 or more:5 or more; petiole with a (D-shaped) ring of bundles, (wing bundles +); mucilage cells common; soluble calcium oxalate accumulation; cuticle waxes as platelets or rodlets; (stomata dia- aniso- or paracytic); lamina vernation revolute, (margins lobed), secondary veins also palmate, colleters +; inflorescences with flowers in fascicles; flowers small, pedicels articulated; hypanthium ± developed; P +, uniseriate, basally ± connate, usu. some or all members with a single trace; stamens = to and alternate with P to 3 x P; pollen tricolporate to pantoporate; nectary disc-like, or between A (0); G [(2) 3 (4)], (common style short), stigma ± penicillate or capitate; ovule straight, (unitegmic), nucellar beak +, hypostase +, funicle short; (megaspore mother cells several); fruit an achene, trigonous (lenticular); seed ruminate; embryo straight to curved, lateral or not; nuclear genome duplication; expansion of the chloroplast inverted repeat.
55 [list]/1,110 - four groups below. World-wide. [Photos - Collection]
Age. This age of this node has been estimated at (122.5-)105.5, 97.8(-78.2) m.y. (Schuster et al. 2013), and (97.3-)90(-73.7) m.y.a. (Kostikova et al. 2014b: p. 1862, it "split from Plumbaginaceae") - or 41-34 m.y.a. (Forest & Chase, see Doorenweerd et al. 2016).
1. Symmerioideae Meisner
Tree; petiole winged, wing ± surrounding stem, stipule not forming closed tube; plant dioecious; P 5; staminate flowers: A 20+; carpellate flowers: ovary with basal septum; achenes pyramidal, 3 P adnate to wall; n = ?
1/1: Symmeria paniculata N. South America, West Africa (map: from Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; Tropicos i.2013).
[Afrobrunnichia [Polygonoideae + Eriogonoideae]]: stipule +, adaxial, tubular, ensheathing stem [= ochrea].
2. Afrobrunnichia Hutchinson & Dalziel
Liane, climbing with bifid, axillary tendrils; pedicel winged on both sides; P 5, basally connate; A usu. 8; funicle large; fruit a ?drupe ["turgid"], P lobes accrescent; seed deeply longitudinally 3-sulcate, irregularly ruminate; n = ?; germination epigeal, phanerocotylar
1/2. Tropical West Africa, Liberia to the Congo (map: from Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003).
[Polygonoideae + Eriogonoideae]: (seed not ruminate).
(Map: from Hultén 1971; Frankenberg & Klaus 1980; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; FloraBase i.2013; Australia's Virtual herbarium i.2013; Tanya Schuster, pers. comm.; Indo-Malesia incomplete).
Age. This node has been dated to 32-28 m.y. (Wikström et al. 2001), (122.5-)105.5, 97.8(-78.2) m.y. (Schuster et al. 2013), and (90.5-)83(-65.7) m.y.a. (Kostikova et al. 2014b) - c.f. details of tree.
3. Polygonoideae Eaton
Herbaceous (annuals), shrubby, lianes or vines [with ?leaf tendrils]; (extrafloral pit nectaries at petiole base); (leaves convolute - Muhlenbeckia), stipule ± scarious; P (3-6); A (3-9); (nectary 0); funicle long or short; (cotyledons folded - Fagopyrum, Pteroxygonum); n = 7 and up.
15/590: Persicaria 150), Rumex (200), Calligonum (80), Koenigia (60), Rheum (60). Especially (warm) north temperate.
Age. Crown Polygonoideae have been dated to (111.3-)93.5, 85.9(-68.4) m.y. (Schuster et al. 2013: Persicarieae + The Rest).
Synonymy: Calligonaceae Khalkuziew, Persicariaceae Martinov, Rumicaceae Martynov
4. Eriogonoideae Arnott
Lianescent and with branch tendrils [?plesiomorphic], or trees to perennial or annual herbs; (petiole bundles scattered - some Coccoloba); stipules massive, scarious, or 0; (plant dioecious); (inflorescence ± cymose, with involucre - Eriogonum et al.); (inner P clawed), n = ?
28/520: Eriogonum (250, but paraphyletic), Coccoloba (120). Largely tropical, America and the Antilles (West Africa), Eriogonum and relatives esp. W. North America.
Age. Crown Eriogonoideae have been dated to (104.7-)76.4, 69.1(-43.0) m.y. (Schuster et al. 2013: Brunnichieae + The Rest]).
Synonymy: Eriogonaceae G. Don
Evolution: Divergence & Distribution. For the fossil record, which includes fossils from the late Maastrichtian ca 68 m.y.o., see Manchester et al. (2015), and for wing-fruited fossils, see Manchester and O'Leary (2010).
If Oxygonum is sister to [Polygonaceae + Eriogonoideae], it may suggest that Polygonaceae were originally African/Gondwanan, and if age estimates here are accurate, then continental drift can be implicated in some distributions here (Schuster et al. 2011b, see also 2013).
Eriogonum and relatives are very diverse in the drier regions of southwest North America (and there are also some species in southern South America), and it may represent a relatively recent radiation (Sanchez & Kron 2008). See Schuster et al. (2013) for more dates within the family.
Schuster et al. (2013) provide a detailed discussion on the biogeography of [Polygonoideae + Eriogonoideae], especially Muehlenbeckia, with additional ages. Diversity within the family as a whole peaks in more temperate regions rather than increasing towards the tropics; reduced extinction rates in temperate clades may be an explanation (Kostikova et al. 2014b). Diversification within Rheum occurred along with the uplift of the Tibetan Plateau in the last (16.1)-12.0, 9.9(-6.8) m.y., most species living in this area (Sun et al. 2012; see also Hughes & Atchison 2015). For the evolution of extra-floral nectaries in some Polygoneae - no real effect on diversification rates - see Weber and Agrawal (2014).
Ecology & Physiology. Basal Polygonaceae tend to be found wetter (tropical) environments, although the family as a whole includes numerous taxa that prefer cooler conditions, a shift to these conditions being associated with the whole genome duplication (S. A. Smith et al. 2017). Calligonum is a clade of C4 plants growing in the halophilic vegetation in Asian Turanian deserts otherwise dominated by C4 Chenopodiaceae (Winter 1981; Sage et al. 2011; Christin et al. 2011b for dates). Calligonum can grow to 8 m tall (Winter 1981). Indeed, woodiness seems to have evolved several times from the herbaceous habit (Lamb Frye & Kron 2003; Tian et al. 2011).
The speciose Eriogonum is a feature of drier areas of western North America, and perennial species may have broader niches than annual species, despite a contrary expectation based on the shorter generation times of the latter (Kostikova et al. 2013: focus on Californian species; see also Kostikova et al. 2016: evolution of climatic tolerances). However, the perennial species have to be able to put up with fluctuating environmental conditions over the course of their lives, while an annual can live its entire life under suitable conditions. For adaptive evolution and parallelism/convergence in Californian Eriogonum and relatives, see Kostikova et al. (2014a).
Polygonum (Bistorta) viviparum is a common perennial herbaceous ECM plant of the tundra, both as a pioneer and as a component of more established vegatation (e.g. Gardes & Dahlberg 1996; Michelsen et al. 1998; Brevik et al. 2010). Another ECM plant, Coccoloba uvifera, may form monodominant stands in Antillean coastal forests (Séne et al. (2017).
Desert rhubarb (Rheum palaestinum) may survive in the arid conditions in which it grows in part by condensing soil moisture on the underside of its very wrinkled leaves that form a tight seal with the ground (Lev-Yadun et al. 2017) - does this happen in other species of the genus?
Pollination Biology. Remarkable "glasshouse bract" inflorescences with large white recurved inflorescence bracts covering the flowers have evolved twice within Rheum growing at high altitudes in Southeast Asia (Sun et al. 2012), a parallelism evident at the molecular level (Liu et al. 2015). In Rheum nobile the fungus gnat Bradysia pollinates the flowers, also laying eggs at the same time; the association is mutualistic - pollination is effected, but some of the developing fruits are eaten by the developing larvae (Song et al. 2014).
Plant-Animal Interactions. Lycaena and Heliophorus (Lycaenini) are found on Polygonaceae throughout their extratropical range (Ehrlich & Raven 1964), and caterpillars of the lycaenid Euphilotes eat a number of species of Eriogonum (Shields & Reveal 1988). Enteucha, leaf miners belonging to the monotrysian Nepticulidae, are known only from here, and their crown age (84-51 m.y.) is encompassed by the suggestions above (Doorenweerd et al. 2016: stem 135-102 m.y.o.).
For insect vein cutting (trenching) in Rumex crispus and its effect of the photosynthesis of the leaf, see Delaney and Higley (2006).
Triplaris has an association with the ant Pseudomyrmex, but if the ant does not keep neighbouring vegetation away more aggressive ants may invade and usurp the association (see Davidson & McKey 1993). The Pseudomyrmex species involved form a small clade unrelated to other myrmecophytic species in the genus, and there it little specificity in the plant-ant interactions (Davidson & McKey 1993; Sanchez 2015); ascomycete fungi, Chaetothyriales, are also involved in the association (Vasse et al. 2017). The ants eat pearl bodies produced by the plants (Davidson & McKey 1993). The ant clade is significantly younger that that of the clade of Triplaris it inhabits, the latter being dated to ca 13.6 m.y.a. (Chomicki et al. 2015; Chomicki & Renner 2015: ?sampling). The ant initially associated with the plant was perhaps Azteca (Chomicki et al. 2015), although this cannot be discerned in the more extensive study of Sanchez (2015).
Bacterial/Fungal Associations. Interestingly, in view of the general paucity of mycorrhizae in Caryophyllales, endomycorrhizae are reported from Eriogonum and ectomycorrhizae from both the tropical Coccoloba (Malloch et al. 1980; Tedersoo et al. 2010a) and the tundra-dwelling Polygonum (Bistorta) viviparum (e.g. Gardes & Dahlberg 1996; Brevik et al. 2010), and perhaps also Gymnopodium (see also Brundrett 2017a; Tedersoo 2017b; Tedersoo & Brundrett 2017 for literature, ages, etc.). ECM fungi on Coccoloba form a very distinct group (Tedersoo et al. 2014a). Newsham et al. (2009) also noted the frequency of arbuscular mycorrhizae in polar Polygonaceae.
Genes & Genomes. A genome duplication characterises this clade (Y. Yang et al. 2017; S. A. Smith et al. 2017: ?the whole family). Some species of Rumex have an X-Y system determining the 'sex' of the plant (Hough et al. 2014: R. hastulus); polyploids may have only a single Y chromosome (Cuñado et al. 2007).
See Logacheva et al. (2008) for the expansion of the inverted repeat.
Chemistry, Morphology, etc. Williams et al. (1994) noted that although no plumbagin had been reported from the family, other quinones were known there.
Sieve tube plastids with protein fibres are reported from Triplarieae (Behnke 1999). The climber Antigonon has leaf tendrils and successive cambia (Carlquist 2003a; Rajput 2015; Sousa-Baena et al. 2018b: inflorescence tendrils, also see other taxa). There are often subepidermal strands of collenchyma or sclerenchyma in the stem in Polygonaceae (see also Plumbaginaceae).
There have been suggestions that the perianth of Polygonaceae is basically 3-merous and two-whorled; the carpels are opposite the outer perianth whorl (e.g. Galle 1977 for floral diagrams, etc.; see also Laubengayer 1937; Ronse Decraene 1989a; Vautier 1949: comprehensive survey of floral vasculature). Flowers with five tepals would then be derived from those with six, perhaps by fusion of two of the members. Recent work, however, suggests that the basic condition for the family is to have five perianth members (Lamb Frye & Kron 2003; Burke et al. 2009, esp. 2010; Ronse de Craene & Brockington 2013). However, the extensive earlier work on floral vascularization is not integrated into this scenario, and floral vascularization in Symmeria, Afrobrunnichia and Oxygonum, phylogenetically critical taxa (see below), is unknown.
Stamens in Fagopyrum are both introrse and extrorse (Le Maout & Decaisne 1868), while in Persicaria campanulata five stamens are adnate to the perianth and three are completely free (Ronse Decraene & Akeroyd 1988). Since a nucellar beak is usually (?always) developed, there are several (4+) layers of parietal tissue. The chalazal end of the seed, i.e. the part below the point of junction of the integuments, van be quite massive (Cocucci 1957). The exact nature of the funicle is unclear; it might be a reduced basal placenta.
For more information, see Haraldson (1978) and Brandbyge (1993), both general, Hegnauer (1969, 1990: chemistry), Carlquist (2003a: wood anatomy), Ronse Decraene and Smets (1991c: nectaries), Hong and Hedberg (1990: pollen, very variable), Ronse Decraene et al. (2000c: fruits in some Polygonoideae), Woodcock (1914: seeds), and Hutchinson and Dalziel (1928: general) and Cremers (1974: growth), both Afrobrunnichia.
Phylogeny. In the past, the largely herbaceous Eriogonoideae s. str., i.e. Eriogonum and its immediate relatives, were separated from Polygonoideae, variable in habit. The former lack a sheathing stipule, their inflorescence is cymose and involucrate, while the latter have a sheathing stipule and a racemose inflorescence that lacks an involucre. However, recent work suggests that there are two moderately/well supported major clades in the family, one largely woody, Eriogonoideae s.l., Eriogonoideae s. str. being derived within that clade, and the other, Polygonoideae, largely herbaceous (Cuénoud et al. 2002; Lamb Frye & Kron 2003; Burke et al. 2010; Sanchez et al. 2011).
Some genera are basal to these two clades. Symmeria and Afrobrunnichia - the position of latter is not so clear - may be immediately below the [Antigonon + Brunnichia] clade in Eriogonoideae (Sanchez et al. 2009a; Sanchez & Kron 2009; see also Burke et al. 2009; Schuster et al. 2015). However, Sanchez et al. (2009b) using chloroplast data placed Symmeria as sister to the whole of the rest of the family and Afrobrunnichia sister to Eriogonoideae, while ITS data suggested that Afrobrunnichia was sister to Polygonoideae and Symmeria sister to Eriogonoideae; in a combined analysis the relationships were [Symmeria [Afrobrunnichia [the rest of the family]]]. Not all support values were high, but this set of relationships was found by Schuster et al. (2011b), who also noted that the position of Oxygonum was uncertain, although it, too, might be part of a basal pectination (see also Burke et al. 2010 and Sanchez et al. 2011 for the position of Symmeria).
Eriogonoideae s. l. include the woody "Coccolobeae" which are both basal and paraphyletic (e.g. Cuénoud et al. 2002; Lamb Frye & Kron 2003); [Antigonon + Brunnichia] (Brunnichieae), both lianes, are sister to the rest of the woody clade (Sanchez & Kron 2008; Burke et al. 2010; Schuster et al. 2013: Symmeria etc. not included). Within the rest of Eriogonoideae are clades with 5 and 6 perianth members, although the 5-membered Podopterus may be sister to the 6-membered clade (Burke et al. 2010). Eriogonum is paraphyletic and includes taxa like Chorizanthe and Dedeckera (Sanchez & Kron 2006, 2008; Kempton 2012; Kostikova et al. 2016). For relationships in the Neotropical Triplaris and Ruprechtia, see Chomicki and Renner (2015) and Sanchez (2015).
The African Oxygonum is sister to other Polygonoideae (Schuster et al. 2015), and then genera like Persicaria and Bistorta make up Persicarieae, sister to the remainder (Schuster et al. 2013, 2015). Schuster et al. (2015) discuss relationships between the other tribes here; the addition of taxa necessitated the description of two more clades as tribes, and Fallopia was highly pluphyletic. The mostly viney Muehlenbeckia is to be included in Polygonoideae; most species are sister to Fallopia s. str. (Schuster & Kron 2008; Schuster et al. 2011a, esp. 2013, 2015). For Chinese Polygonoideae, see Z.-D. Chen et al. (2016), and for a molecular phylogeny of Polygoneae, see Schuster et al. (2011b, 2015, also below). Rheum shows substantial morphological variation but little molecular variation, at least in the markers analysed (Wang et al. 2005).
Classification. See Hernández-Ledesma et al. (2015). For a tribal classification of Polygonoideae, see Sanchez et al. (2011) and for that of Eriogonoideae (and a subfamilial classification, too), see Burke and Sanchez (2011); although tribal limits in the old Eriogonoideae are holding up, subtribes and below are in somewhat of a state of disrepair (Kempton 2012). Generic limits around Polygonum are difficult, and the tendency now is to split the genus into an increasing number of pieces (e.g. Ronse Decraene & Akeroyd 1988; Brandbyge 1993; Ronse de Craene et al. 2004; Kim & Donoghue 2008; Kim et al. 2008; Galasso et al. 2009: comprehensive treatment; Yurtseva et al. 2010; D.-M. Fan et al. 2013).
Thanks. I thank Adriana Sanchez for comments.
[Rhabdodendraceae [Simmondsiaceae [[Asteropeiaceae + Physenaceae] [Caryophyllaceae, Nyctaginaceae, Cactaceae, etc.]]]]: (successive cambia +); styles stigmatic their entire length; ovules 1-2/carpel; fruit 1-seeded; endosperm slight.
Age. Rhabdodendron may have diverged from all other Caryophyllales 90-83 m.y.a. (Wikström et al. 2001), ca 87.4 m.y.a. (Tank et al. 2015: Table S2) or ca 108.9 m.y.a (Magallón et al. 2015).
Evolution: Divergence & Distribution. Few (1-2) ovules per carpel may be an apomorphy for the whole clade (see also Sukhorukov et al. 2015: "Core Caryophyllales"; other distinctive characters to be placed at this or the next four nodes), but the position of these ovules varies - apical in Simmondsiaceae, and basal in Rhabdodendraceae, just for starters. Basifixed anthers and stamens with very short filaments are common outside core Caryophyllales; their optimisation on the tree is difficult; taxa with such stamens also lack floral nectaries, perhaps wind pollination. Basal members of this clade outside core Caryophyllales lack a compitum, as far as is known (Armbruster et al. 2002).
Genes & Genomes. Y. Yang et al. (2015) found 10 or so genome duplications in this clade, including in Simmondsia and Physena.
Chemistry, Morphology, etc. For successive cambia, see Robert et al. (2011), and for the anatomy, etc., of single-seeded fruits, see Sukhorukov et al. (2015).
The morphology, embryology and in particular chemistry (see Fig. 4 in Brockington et al. 2015) of the basal members of this clade are poorly known, but the plants are rather different from members of core Caryophyllales.
Phylogeny. For relationships in this part of the tree, see above.
RHABDODENDRACEAE Prance Back to Caryophyllales
Woody; ellagic acid +; cork?; successive cambia + (0); true tracheids +; dark-staining deposits esp. in rays; SiO2 bodies +; pits vestured; sieve tube plastids with protein crystalloids and starch; nodes 5:5 or 7:7; (cortical bundles +); ?pericycle; secretory cavities with resin; sclereids +; petiole bundle annular, bundles separate or not, (medullary vascular bundles +), wing bundles +; foliar (branched) fibre-like sclereids +; hairs peltate, cells with SiO2 bodies; lamina punctate, vernation revolute, secondary veins looping close to margin, petiole base rather broad-cordate; inflorescence axillary, branched, ?with a terminal flower; hypanthium +, short; K ± connate, short, C rather thick; A many, development ± simultaneous, anthers much longer than filaments, basifixed, articulated, anther wall with outer parietal layer of anther wall producing endothecium only, the inner the middle layer and tapetum [monocotyledonous type], exodermis tanniniferous; nectary 0; G 1, stylulus basal, stigma much elongated, ?type; compitum necessarily 0; ovules 1-2/carpel, basal, campylotropous, bitegmic zone short, outer integument 4-5 cells across, inner integument 2-5 cells across, parietal tissue 10+ cells across, nucellar cap 0; megaspore mother cells several; fruit a drupelet, basally surrounded by K/swollen receptacular area, filaments persistent, pedicel swollen; seed single, exotestal cells tangentially elongated, underlying cells short-tracheidal [with bar thickenings]; perisperm +, slight, endosperm slight, embryo chlorophyllous, with large cotyledons; n = 10.
1 [list]/3. Tropical South America (map: see Prance 1972c; Aymard et al. 2016). [Photo - Flower.]
Chemistry, Morphology, etc. The leaves are often rather congested and may grade into much smaller undifferentiated leaves at the beginning of each innovation. I have not seen stipules (see also Puff & Weber 1976; c.f. Prance 1972c), but the rather broad petiole base can be confused with them.
The ovule is often described as being unitegmic (e.g. Nandi et al. 1998, following Puff & Weber 1976), but see Tobe and Raven (1989). The stylulus may be stigmatic for only part of its length. The embryo is surrounded largely by testa that develops from the unitegmic part of the ovule, and the description above refers to this (Tobe & Raven 1989).
For general information, see Prance (2002), for some chemistry, see Wolter-Filho et al. (1989). .
Previous relationships. The position of Rhabdodendraceae has long been uncertain. Thus they were placed in Rutales by Takhtajan (1997), although Prance (1968) had much earlier suggested a position around Caryophyllales; Cronquist (1983) placed them at the end of his Rosales after Surianaceae.
[Simmondsiaceae [[Asteropeiaceae + Physenaceae] [Caryophyllaceae, Nyctaginaceae, Cactaceae, etc.]]]: nodes 1:1; P +, uniseriate, 5.
Age. The age of this node may be around 100.9 m.y. (Magallón et al. 2015), about 97 m.y. (Hernández-Hernández et al. 2014), (102-)93, 88(-79) m.y. (Bell et al. 2010), ca 83.8 m.y. (Tank et al. 2015: Table S2) or 72-67 m.y. (Wikström et al. 2001).
Evolution: Divergence & Distribution. A uniseriate perianth is tentatively pegged to this node, the implication being that petal-like structures common in members of this clade are in fact staminodial or calycine in origin (Ronse de Craene 2007); see also Brockington et al. (2009), Ronse de Craene and Brockington (2013), and the discussion below under Core Caryophyllales.
Chemistry, Morphology, etc. For variation in seed size, see Moles et al. (2005a).
SIMMONDSIACEAE van Tieghem Back to Caryophyllales
Evergreen shrubs; ellagic acid 0, seeds with C36-C46 long straight-chain wax ester [jojoba oil - a wax]; successive cambia +; pericyclic fibres +; cork pericyclic; true tracheids +; petiole bundle ± C-shaped; stomata anomoytic, cyclocytic and laterocytic; hairs uniseriate; leaves opposite, articulated near stem, lamina vernation flat, secondary veins ascending from near base; plant dioecious; flowers small, (4, 6-merous); nectary 0; staminate plant: inflorescence usu. terminal, cymose; A 2x P, extrorse, anthers much longer than filaments, basifixed; pollen ± porate, central part operculoid, spinules minute; carpellate plant: flowers single axillary; G , styluli papillate all around; compitum 0; ovule 1/carpel, subapical, pendulous, apotropous, outer integument 6-10 cells across, inner integument 3-5 cells across, parietal tissue to 10 cells across, (nucellar cap to 2 cells across), obturator 0; fruit a capsule, exocarp of radially elongated sclereids, columella persistent, K accrescent, spreading; seeds 1-3, testa multiplicative, vascularized, exotestal cells palisade, walls thickened, mesotesta aerenchymatous, rest collapsed, cells tanniniferous; endosperm nuclear, reserve?, cotyledons incumbent; germination hypogeal; n = 13.
1 [list]/1: Simmondsia chinensis (!: note the epithet). S.W. North America, the Sonoran Desert (map: see Sherbrooke & Haase 1974). [Photos - Collection.]
Chemistry, Morphology, etc. Thulin et al. (2016) detected anthocyanins but not betalains here. The vessels have simple apertures and the root has anomalous secondary thickening (Bailey 1980).
The large embryo contains liquid wax made up of esters of high molecular weight, mono-ethylenic acids. The stamens are described as being latrorse (Takhtajan 1997).
For general information, see van Tieghem (1897), Mathou (1939) and Köhler (2002), for chemistry, see Hegnauer (1989, as Buxaceae), for wood anatomy, see Carlquist (2002b), for embryology, see Wiger (1935), and for testa anatomy, etc., see Tobe et al. (1992b) and Sukhorukov et al. (2015).
Previous Relationships. Simmondsiaceae have usually been included in Buxaceae or placed in a separate family, but close to Buxaceae. However, a monotypic Simmondsiales have been included in Hamamelididae (Takhtajan 1997).
[[Asteropeiaceae + Physenaceae] [Caryophyllaceae, Nyctaginaceae, Cactaceae, etc.]]: ?
Age. The age of this node is estimated at 61-52 m.y. (Wikström et al. 2001), (95-)83, 79(-68) m.y. (Bell et al. 2010) or about 96.2 m.y. (Magallón et al. 2015).
[Asteropeiaceae + Physenaceae]: young stem with vascular cylinder; wood parenchyma aliform-confluent; vasicentric tracheids +, fibre tracheids +; rays 1-2 cells wide; successive cambia ?0; A latrorse; exocarp of radially elongated sclereids; cells of seed coat tanniniferous; endosperm at most slight.
Age. This node is estimated to be about 61.7 m.y.o. (Magallón et al. 2015) or about 34.1 m.y.o. (Tank et al. 2015: Table S1).
Chemistry, Morphology, etc. Some information on the general anatomy of these two families is taken from Harms (1893) and on fruit and seed anatomy from Sukhorukov et al. (2015); Carlquist (2006) compared their wood anatomy.
ASTEROPEIACEAE Reveal & Hoogland Back to Caryophyllales
Evergreen trees or scrambling shrubs; plant ectomycorrhizal; ellagic acid?; rays uniseriate; pericyclic fibres +; petiole bundle annular; cortical and mesophyll sclereids +; hypodermis several layered; ?stomata; inflorescence terminal, branched, pedicels with many bracteoles; C +, deciduous; A 9-15, ?obdiplostemonous, anthers dorsifixed, filaments basally connate; (pollen 6-rugate); G [(2) 3], (style short, with lobed stigma), stigma continuous across G; compitum 0; ovules 2-many/carpel, ± apical, ?micropyle, nucellar cap 0; fruit nutlike, (several-seeded), K accrescent, spreading, forming wings, A persistent; seed coat 2-5 cells across; endosperm reserve?, embryo curved, cotyledons spirally coiled; n = ?
1 [list]/8. Madagascar. [Photos - Collection.]
Evolution. Bacterial/Fungal Associations. Asteropeia has both ecto- and arbuscular mycorrhizae (Bâ et al. 2011a, b: Henry et al. 2016; see also Brundrett 2017a; Tedersoo 2017b; Tedersoo & Brundrett 2017 for literature, ages, etc.).
Chemistry, Morphology, etc. Some information is taken from Morton et al. (1997b), Schatz et al. (1999), and Kubitzki (2002d), all general, Beauvisage (1920: anatomy), and Miller (1975: wood anatomy).
Previous Relationships. Asteropeiaceae were previously often included in Theaceae or Theales (Cronquist 1981; Takhtajan 1997), but are very different in wood anatomy (Baretta-Kuipers 1976).
PHYSENACEAE Takhtajan Back to Caryophyllales
Shrub or tree; triterpene glycosides, oxohexadecanoic acid + [keto fatty acid]; ellagic acid?; pericyclic sclereids +; cuticle wax crystalloids?; ?petiole bundle; leaves two-ranked; plant dioecious; inflorescence axillary, racemose, pedicels long; P 5-9; staminate flowers: A (8-)10-14(-25), anthers much longer than filaments, long, basifixed; carpellate flowers: G , septae incomplete; ?compitum; ovules 2/carpel, ± subbasal, campylotropous, funicle long; fruit subdrupaceous?; seed single, large, (with hair-like outgrowths), coat vascularized, 16-20 layers thick, cell walls not notably thickened; endosperm reserve?, cotyledons unequal; n = ?
1 [list]/2. Madagascar. [Photos - Collection.]
Chemistry, Morphology, etc. The petiole is often described as being articulated; it commonly breaks transversely above the base, but there is no evidence that the leaf is derived from a compound leaf. The vascular bundles in the lamina are completely surrounded by mechanical tissue. There are brachysclereids in the secondary phloem and the placental bundles are inverted (Dickison & Miller 1993).
General information is taken from Morton et al. (1997b) and Dickison (2002); for triterpene glycosides, see Inoue et al. (2009), for fruit anatomy, see Sukhorukov et al. (2015.
Previous Relationships. Physenaceae were included in Urticales by Cronquist (1981) and placed in a monotypic Physenales in Dilleniidae by Takhtajan (1997).
[Caryophyllaceae, Nyctaginaceae, Cactaceae, etc.] / Core Caryophyllales / Centrospermae: plant herbaceous; (CAM [especially pervasive in succulents] and C4 photosynthesis common); unlignified cell walls fluorescing blue under UV, green with NH3 [ferulic acid ester-linked]; (O-methylated) flavonols, quinones, triterpenoid saponins +, tannins, myricetin 0 or slight; (phytoferritin +); sieve tube plastids with a ring of proteinaceous filaments and a central angular crystalloid (also with starch); pericyclic fibres 0, phloem-derived fibres quite widespread; (mucilage cells +); (stomatal orientation transverse); lamina often succulent; inflorescence cymose; pollen grains tricellular, (polyaperturate), foot layer thin; nectary on adaxial bases of stamens, (abaxial), (on hypanthium); G opposite P [so the median member adaxial], stigmas papillate, little expanded; ovules campylotropous, (space between the bases of the inner and outer integuments), (placental obturator +, papillate/with short hairs), (funicles long); fruits with more than one seed, seeds black; both exotestal and endotegmic cells with bar-like thickenings; endosperm 0, perisperm +, starchy, starch grains clustered, embryo curved, not central, cotyledons incumbent; germinal epigeal, phanerocotylar; no dark reversal Pfr → Pr; mitochondrial rps10 gene lost, introns lost in chloroplast rpl2 [present in some Portulaca] genes.
Age. Molecular estimates of the crown age of this clade in Bell et al. (2010) are (83-)71, 66(-57) m.y.a. [actual node?].
Evolution: Divergence & Distribution. For ages of various clades in core Caryophyllales, see Hernández-Hernández et al. (2014); not all have been added below.
Core Caryophyllales contain ca 5.3% of eudicot diversity (Magallón et al. 1999).
The evolution of petals, betalains and anomalous secondary thickening in this group has long been of interest, but our understanding of phylogenetic relationships in this area is still uncertain in places (see below). Detailed sampling of Phytolaccaceae as well as Molluginaceae is critical if we are to understand relationships and evolution within core Caryophyllales. Even if only some of the new placements mentioned below are confirmed - and confirmation is badly needed - character evolution may be affected, and clarifying the basic phytochemical, morphological, anatomical and embryological variation of the migratory taxa is essential. Sukhorukov et al. (2015: p. 2) suggest a number of features common to "most representatives" of what they call the core Caryophyllales clade. This clade includes everything from Rhabdodendraceae on up, and is made up of earlier diverging lineages (including Microteaceae), the "Globular Inclusion" clade and taxa here placed in the [Caryophyllaceae [Achatocarpaceae + Amaranthaceae]] clade, both monophyletic; a few families are not accounted for (Sukhorukov et al. 2015: Fig. 1). They optimise characters like embryo orientation (not applicable if 2 or more seeds/fruit or loculus) and fruit succulence and pericarp layering on the tree.
Betalains may have been acquired once in this clade and then been lost at least twice (Cuénoud et al. 2002; Cuénoud 2002a; Brockington et al. 2015, c.f. 2011; Thulin et al. 2016; see also Clement & Mabry 1996), although there are no data on betalain presence for a few families (see Thulin et al. 2016; Lopez-Nieves et al. 2017). Betalain acquisition may have been preceded by duplications of some of the genes involved, probably along the stem of core Caryophyllales, and the genes may be included in an operon (Brockington et al. 2015). Another important step in the evolution of the betalain pathway is the evolution (also by duplication) of an enzyme (BvADHα) insensitive to tyrosine concentrations that is involved in the synthetic chain immediately prior to the production of tyrosine, which thus accumulates (Lopez-Nieves et al. 2017). Tyrosine is a major component of betalains, and after modification to betalamic acid, tyrosine is part of the chromophore of both betacyanins and betaxanthins, reddish and yellowish pigments respectively, the former acquiring another modified tyrosine unit (Tanaka et al. 2008; Pichersky & Lewinsohn 2011; Gandía-Herrero & García-Carmona 2013; Brockington et al. 2015; Khan & Giridhar 2015). Interestingly, although the differences between betalain and anthocyanin (phenyalanine is a major component of the latter) synthesis pathways may not be that great (Strack et al. 2003; Shimada et al. 2007; Khan & Giridhar 2015), the two have never been found in the same organism (references in Lopez-Nieves et al. 2017), although, somewhat complicating the issue, Shimada et al. (2005) found that anthocyanidin synthase genes were expressed in the seeds of both Phytolacca and Spinacia. The BvADHα enzyme is known from Simmondsiaceae (?betalains), but not Physenaceae, while Asteropeiaceae and Rhabdodendraceae have not been tested, and the duplication that gave rise to it may have happened somewhere along stem Caryophyllales or perhaps even earlier, so much earlier than the first duplications mentioned above (Lopez-Nieves et al. 2017). For betalains as possible defence against herbivory, etc., see Berardi et al. (2013).
Other features with rather spotty distributions are anatomical. These include the presence of wide-band tracheids. Here the cells have narrow lumina because of the height of the wall thickenings, and such tracheids are found in more or less desert-dwelling members of this clade (see below. The vascular anatomy of the lamina is quite often three-dimensional, with a ring of vascular bundles (peripheral vascular bundles) surrounding the midrib that have the xylem either internal (endoscopic) or external (exoscopic) (Ogburn & Edwards 2013; Melo-de-Pinna et al. 2014). These features are connected with the succulence, shape and photosynthetic pathway of the leaf and are particularly common in Chenopodioideae, Aizoaceae and Portulacinae. In other taxa the lamina is more or less flattened and the orientation of the vascular bundles is normal.
Details of timing/pattern of intiation of both the perianth and androecial members vary, and this variation may be of phylogenetic interest (Ronse de Craene 2013: much information). The evolution of corolla-like structures ("C"/"petals" below) is not simple (see Ronse de Craene 2010 for numerous floral diagrams of this group, esp. 2012 and 2013). Any "corolla" present, as in Caryophyllaceae, is usually described as being of staminal origin (e.g. Ronse Decraene & Smets 1993; Leins et al. 2001), although Greenberg and Donoghue (2011) noted that it was perhaps surprising that such apparently staminodial petals in Caryophyllaceae are found in a clade in which stamen number is supposed to have increased from 5 to 10 irrespective of the presence/absence of staminodes: Caryophyllaceae with 5 stamens only rarely have petals (but c.f. Ronse de Craene 2013). In a number of taxa, including Dianthus, there appear to be two pairs of bracetoles below the flower, and these are sometimes described as an epicalyx. When there is a single perianth whorl, perhaps equivalent to the "calyx" of some Caryophyllaceae, this is quite often attractive and corolline, bracteoles then often being functionally calycine and borne immediately under the perianth. "Petals" may have evolved perhaps nine times or so in the clade and in a variety of ways (Brockington et al. 2009; see also Ronse de Craene & Brockington 2013; Ronse de Craene 2013; Glover et al. 2015). Brockington et al. (2012) showed that the numerous "petals" of Aizoaceae-Ruschioideae and -Mesembryanthemoideae were of probable staminal origin and B-class genes were expressed during their development, the sepals of Sesuvioideae, for example, were also petal-like in part, but B-class genes (AP3, PI) were not involved in their development (c.f. Ronse de Craene 2013), and they suggested that this might be the case throughout the core Caryophyllales.
When the stamens are equal in number to the perianth members they are usually opposite to them. When there are many stamens the initial primordia may alternate with the perianth members (Aizoaceae) or continue the spiral of the perianth (Pereskia - Cactaceae, Leins & Erbar 1994a, b: there may not be a perianth here); development is often centrifugal (see also Ronse de Craene et 2013).
Ovule number is also very labile. Thus a single ovule/gynoecium could be a synapomorphy for all Core Caryophyllales minus Macarthuria, but two or more ovules/gynoecium would have evolved more than once, and the single ovule condition regained. The clade [Rhabdodendraceae + The Rest] could be characterized by its low ovule number, but, as mentioned elsewhere, Rhabdodendraceae and members of the next four pectinations are poorly known.
Ecology & Physiology. 1. Succulents, both of leaf and/or stem, are common and many taxa have CAM photosynthesis or its variants or precursors; expression of CAM may depend on the developmental stage the plant is at and it may also be facultative and depend on environmental conditions (Ehleringer et al. 1997; Sage et al. 2012, 2014; Winter & Holtum 2014; Christin et al. 2015; Winter et al. 2015; esp Bräutigam et al. 2017; see also Ocampo & Colombus 2010; Christin et al. 2011b for dates); the PEPC enzymes involved in both C4 and CAM photosynthesis are members of the ppc-1E1 family (Christin et al. 2014b). See also Bräutigam et al. (2017) for the evolution of CAM photosynthesis and Males and Griffiths (2017) for the stomatal biology of CAM plants. 2. Outside Poales, C4 photosynthesis is most common in core Caryophyllales, indeed, there are about one half (33/62) of all evolutionary origins of the syndrome in angiosperms here (Sage et al. 2011). See also Sage et al. (1999), Muhaidat et al. (2007 and references) and Christin and Osborne (2014) for the C4 pathway, also papers in Ann. Bot. 115(3). 2015.
Robert et al. (2011) noted that woody taxa with successive cambia often (86% of cases, lianes/vines not included) grow in conditions in which there is some kind of water stress, and in at least some core Caryophyllales both xylem and phloem are organized to form a three-dimensional network.
Plant-Animal Interactions. Core Caryophyllales are little liked by butterfly caterpillars (Ehrlich & Raven 1964), however the largely leaf mining yponomeutoid moth Heliodinidae are found here, especially on Nyctaginaceae (Sohn et al. 2013). Tempère (1969) discussed herbivory patterns that involve different members of this clade.
Bacterial/Fungal Associations. The oomycetous white blister rust, Wilsoniana is parasitic on taxa scattered throughout this clade (Thines & Voglmayr 2009 and references).
Genes & Genomes. In comparisons between herbaceous and woody clades, substitution rates at all sites in protein-coding genes were much higher in herbaceous lineagesthan in their woody relatives (Y. Yang et al. 2015).
For the mitochondrial rps10 gene, see Adams et al. (2002b); eact position of loss?
Chemistry, Morphology, etc. For tannin (both hydrolysable and non-hydrolysable) distribution, see Mole (1993). Sterol composition may be of systematic interest (Wolfe et al. 1989; Patterson & Xu 1990), with distinctive sterols common or dominant in Caryophyllaceae, Phytolaccaceae, Amaranthaceae, and "Portulacaceae". Isoflavonoids (Reynaud et al. 2005), sometimes quite diverse, and phytoecdysones are scattered in the Core Caryophyllales, but perhaps not in the Cactaceae area. For unlignified cell wall fluorescence, seeHartley and Harris (1981). Diferulic and p-coumaric acids are less commonly involved than in monocots, and alsthough sampling was quite extensive, neither the first two clades in core Caryophyllales nor members of the three clades basalo to them were investigated.
Stomatal morphology is variable, but anomocytic stomata are common in nearly all families. However, in Cactaceae and relatives, parallelocytic and other kinds of stomata are found; some families in this area have predominantly paracytic stomata. Stomatal orientation on stem and/or leaf is commonly transverse throughout the order (Butterfass 1987, Amaranthaceae s. str.?), however, it is unlear which taxa have vertically or which unoriented stomata. Variation in structures associated with the leaf base, whether hairs/colleters or "stipules", is considerable (Rutishauser 1981) and would repay further study; note that the basic nodal anatomy of the clade is one trace-one gap, unusual for plants with stipules as commonly accepted.
For a good general survey of floral morphology, see Hofmann (1994). Sepals with an abaxial crest are described from Caryophyllaceae, Amaranthaceae, Aizoaceae, and Portulacaceae (Ronse de Craene & Brockington 2013). If there is a "corolla", it develops at the same time or after the androecium, not before it, and the "petals" and stamen(s) opposite them may form a developmental unit (e.g. Eichler 1875; Wagner & Harris 2000). The corona - in Lychnis viscaria, at least - arises from two bulges on the adaxial side of the "corolla", perhaps representing anther thecae.
The carpels are quite commonly open in development, as in Polygonaceae (Tucker & Kantz 2001). Placentation is quite variable, although one commonly thinks of this group as typically having free-central placentation or its variants. A subepidermal layer of cells in the inside of the ovary wall may have calcium oxalate sand, as in some Amaranthaceae and Polygonaceae, while in Nyctaginaceae a ring of cells immediately below the ovary havs conspicuous raphides (Guéguen 1901); there is little information on this feature. The integuments are often separated by a small space at their bases, but this seems to vary within Portulacaceae and Caryophyllaceae, and the space may be absent in Phytolacca and Amaranthaceae (e.g. Meunier 1890; Hakki 1973; c.f. Bittrich 1993). The apical cells of the nucellus are commonly elongated radially, as in Cactaceae, "Portulacaceae", Aizoaceae, Phytolaccaceae, and Amaranthaceae (see Johri et al. 1992; also Narayana 1962: e.g. Aizoaceae, Gisekiaceae, Molluginaceae), i.e., they form a nucellar pad, but it is unclear if this feature is of systematic significance. This seems to vary within Portulaca and Mesembryanthemum and there may be confusion with radially elongated and periclinally divided nucellar epidermal cells, which would represent a nucellar cap (Meunier 1980). There are often short hairs on the funicle that are directed towards the micropyle (Neumann 1935).
Seeds of a number of taxa have an operculum, although not necessarily identical in morphology (Bittrich & Ihlenfeldt 1984). There are commonly bar-like thickenings on the walls of the endotegmic cells (e.g. Netolitsky 1926; Bittrich 1993a; perhaps shown in Narayana 1962a; Sukhorukov et al. 2015). Zheng et al. (2010) note that the starchy perisperm tissue is formed not from the parietal tissue surrounding the embryo sac, but from tissue immediately below the embryo sac, i.e., it is technically chalazosperm. For the loss of the intron of the rpl2 gene, see Logacheva et al. (2008).
Additional general information is taken from Bittrich (1993a: useful summary) and Cuénoud (2006), also, see Hegnauer (1989: chemistry), Wolfe et al. (1989) and Patterson & Zu (1990), both sterols, Steglich and Strack (1990) and Strack et al. (2003), both betalains, Shimida et al. (2007: control of anthocyanin/betalain production), Barthlott (1994: waxes), Behnke et al. (1983a: sieve tube plastids), Behnke (1994a: sieve tube plastids, phytoferritin), Gibson (1994), Jansen et al. (2000c) and Timonin (2011), anatomy, esp. successive cambia, Rutishauser (1981: "stipules" and similar structures), Kendrick and Hillman (1971: ?sampling, dark reversal Pfr → Pr), Zandonella (1977) and Erbar (2014), both nectaries, the latter, no distinction between androecial and receptacular nectaries, Nowicke and Skvarla (1979) and Nowicke (1994: pollen), Rocén (1927: embryology), Meunier (1890: ovules and testa), Werker (1997: seed coat) and Sukhorukov et al. (2015: seed and fruit anatomy, also embryo orientation, etc.).
Phylogeny. Understanding where taxa from the old Phytolaccaceae and Molluginaceae, both polyphyletic, are to be placed in the tree is critical for our understanding of relationships and evolution in core Caryophyllales. [Amaranthaceae [Achatocarpaceae + Caryophyllaceae]] were early found to form a moderately well supported clade, the rest of the core Caryophyllales another (Källersjö et al. 1998), however, although 13 families were included in this study, sampling within them was poor. Similar relationships were suggested by Savolainen et al. (2000a). D. Soltis et al. (2000) found that Phytolaccaceae, Nyctaginaceae and Delosperma (Aizoaceae) formed a group, also [Amaranthaceae + Caryophyllaceae], but again the sampling was very sparse; for the position of Achatocarpaceae, see also K. Müller and Borsch (2005b). For other ideas of relationships, see Rodman (1994) and Downie and Palmer (1994: structural variation in chloroplast DNA).
Many of the relationships in the tree here are similar to those shown by Cuénoud et al. (2002: the Delosperma sequence was excluded, sampling still a bit sketchy), and these in turn are largely similar to relationships found by Källersjö et al. (1998) and other workers. Cuénoud et al. (2002) found two quite well supported clades within core Caryophyllales. There have been recent improvements in our understanding of relationships along the backbone of core Caryophyllales. Schäferhoff et al. (2009) found that the poorly-known Microtea, one of whose previous resting places was Phytolaccaceae, was sister to the rest of core Caryophyllales (see also Y. Yang et al. 2015: Microtea the only problem genus included). In another study, Macarthuria, previously included in Limeaceae (and before that in Molluginaceae), occupied that position, and with strong support (Christin et al. 2011a: Microtea not included); Limeum itself (as the monogeneric Limeaceae) remained in its old position well embedded in core Caryophyllales.
Cuénoud et al. (2002) found that Aizoaceae were monophyletic, albeit with only slightly better than marginal (52% bootstrap) support in an analysis of matK sequences, the only gene for which they had moderately good sampling; Gisekia moved position in analyses of rbcL sequences; and Sarcobatus was sister to Nyctaginaceae, albeit with only weak support, in matK analyses, while in a rbcL analysis it grouped with Agdestis. Corbichonia (Lophiocarpaceae) and most of Hypertelis (now as Kewaceae, the type species remains in Molluginaceae) were well supported as successive sister clades at the base of the [Aizoaceae [Gisekiaceae [Sarcobataceae, Phytolaccaceae, Nyctaginaceae]]] clade (Christin et al. 2011a); Hypertelis was also found to be in this general area of the tree in Schäferhoff et al. (2009: included only in their petD analysis). Here both Macarthuria and Hypertelis are placed separately on the tree (see also Brockington et al. 2011), although it is not clear exactly what the support values for these positions are. Arakaki et al. (2011) found that Gisekiaceae and Aizoaceae reversed positions, but with little support; that area was not the focus of their study. There is further discussion on relationships in the Gisekiaceae to Nyctaginaceae part of the tree below.
Portulacineae, which include Cactaceae, have been associated with Molluginaceae (e.g. Nyffeler & Eggli 2010; Arakaki et al. 2011). However, in a recent transcriptome study support for this clade was weaker (Y. Yang et al. 2017). Relationships around Cactaceae, themselves a monophyletic group, remained difficult, and although progress has recently been made here (Brockington et al. 2009; Nyffeler & Eggli 2009; Ocampo & Columbus 2010; Soltis et al. 2011), some relationships are still uncertain. However, Arakaki et al. (2011: see below) produced a largely resolved tree for that area.
Other relationships have been suggested, but sampling is usually poor, support poor, or the markers are unreliable. Thus Harbaugh et al. (2010) found that Molluginaceae were sister to Caryophyllaceae, rather than Amaranthaceae, although two taxa from both families were all that were included in their study, which focused on Caryophyllaceae. Stegnospermataceae were sister to all other core Caryophyllales (support quite strong) and Limeum was placed with Amaranthaceae (support also quite strong) in a mitochondrial analysis by Qiu et al. (2010); however, Caryophyllaceae were not included. Support for the grouping [Stegnospermataceae [Caryophyllaceae + Amaranthaceae]] was found by Moore et al. (2011; see also Y. Yang et al. 2017: six small families along the spine of the tree around here not included). Crawley and Hilu (2012) examined the effect of missing data and missing taxa on phylogenetic reconstructions here. Later they obtained trees that differ in several details from the one here, but support values were mostly low (see Crawley & Hilu 2013). Thus there were clades [Achatocarpaceae + Amaranthaceae] and [Stegnospermataceae + Limeaceae] or Stegnospermataceae were sister to all other core Caryophyllales examined and Limeaceae were in about the same position as in the tree above, etc.. The summary tree in Hernández-Ledesma et al. (2015) suggests some rather different relationships, perhaps most notably that Microteaceae and Macarthuriaceae are outside the [Asteropeiaceae + Physenaceae] clade.
Classification. For generic synonymies of the families of this group, see Hernández-Ledesma et al. (2015), and for taxonomic problems in its German representatives, see Kadereit et al. (2016).
Previous Relationships. Most of this group was included in the old Centrospermae (so named because of the basal or free-central placentation that is common in the clade) or Caryophyllales in the strict sense. The shikimic acid pathway, particularly phenylalanine, is a starting point for the synthesis of nitrogen-containing benzylisoquinoline alkaloids and the betalains of core Caryophyllales, and Kubitzki (1994) suggested a relationship between core Caryophyllales, Magnoliidae and monocots because all contained such compounds.
MACARTHURIACEAE Christenhusz Back to Caryophyllales
±Rigid, rush-like shrubs; O-glycosylflavonoids; cork?; secondary growth abnormal; sieve tube plastids with cubic crystalloid and starch grains; nodes?; leaves spiral, at least some reduced to scales, stipules 0; ("C" 5, adnate to base of staminal tube; 0); A 8, connate basally, anthers basifixed; pollen grains finely punctate; G [3(-7)], loculus 1 (3); ovules 1-3/carpel, embryology?; fruit a leathery loculicidal capsule; seeds with funicular aril; n = ?
1 [list]/10. Australia, the periphery, esp. S.W. Australia (map: from Lepschi 1996; Australia's Virtual Herbarium xi.2013).
Evolution: Pollination Biology & Seed Dispersal. The seeds of Macarthuria are myrmecochorous (Lengyel et al. 2010).
Chemistry, Morphology, etc. For further information, see M. Endress and Bittrich (1993: as Molluginaceae), Lepschi (1996) and Christenhusz et al. (2014), all general, Hofmann (1973: flower, growth), Behnke et al. (1983b: pollen, sieve tube plastids, etc.), and Sukhorukov et al. (2015: fruit anatomy).
The genus is poorly known.
Previous Relationships. In earlier versions of this site (pre vi.2011) Macarthuria was included in Limeaceae; M. Endress and Bittrich (1993) placed it in Molluginaceae.
[Microteaceae [[Caryophyllaceae [Achatocarpaceae + Amaranthaceae]] [Stegnospermataceae [Limeaceae [[Lophiocarpaceae [Kewaceae [Barbeuiaceae [Aizoaceae [Gisekiaceae [[Sarcobataceae + Phytolaccaceae] [Petiveriaceae + Nyctaginaceae]]]]]]] [Molluginaceae [Montiaceae [[Halophytaceae [Didiereaceae + Basellaceae]] [Talinaceae [Anacampserotaceae [Portulacaceae + Cactaceae]]]]]]]]]]]: anthocyanins 0, betalains + [chromoalkaloids]; (pollen grains annular-punctate); placentation free-central or basal.
Evolution: Divergence & Distribution. It is unclear whether the acquisition of betalains is to be placed at this or a deeper node (see also Brockington et al. 2011, 2015).
MICROTEACEAE Schäferhoff & Borsch Back to Caryophyllales
Annual herbs; betalains?; cork?; secondary growth normal; sieve tube plastids lacking protein crystalloid, with a central starch grain; nodes?; calcium oxalate crystals 0; leaves spiral; inflorescence racemose, flowers in groups of up to 3; P (4), basally connate; A (2-)5-9, anthers globose; pollen pantoporate; G [2-4], orientation variable, unilocular, styluli diverging; ovule single [per flower], ?embryology, funicle quite long; fruit a muricate to spiny achene; seed single, black, shint, coat?; n = ?
1 [list]/9. Central and South America, Antilles (Map: from TROPICOS, vi.2011).
Chemistry, Morphology, etc. Some information is taken from Nowicke (1969: as Phytolaccaceae), Rohwer (1993a; as Phytolaccaceae); for sieve tube plastids, see Behnke (1993), and for fruit and seed, see Sukhorukov et al. (2015).
Microtea is very poorly known.
Phylogeny. See Schäferhoff et al. (2009).
Previous Relationships. In Amaranthaceae (early versions of this site), as Phytolaccaceae-Microteoideae, sometimes with Lophiocarpus in Phytolaccaceae (Rohwer 1993a) or as separate Lophiocarpaceae.
[[Caryophyllaceae [Achatocarpaceae + Amaranthaceae]] [Stegnospermataceae [Limeaceae [[Lophiocarpaceae [Kewaceae [Barbeuiaceae [Aizoaceae [Gisekiaceae [[Sarcobataceae + Phytolaccaceae] [Petiveriaceae + Nyctaginaceae]]]]]]] [Molluginaceae [Montiaceae [[Halophytaceae [Didiereaceae + Basellaceae]] [Talinaceae [Anacampserotaceae [Portulacaceae + Cactaceae]]]]]]]]]: sieve tube plastids with polygonal crystalloid.
Age. The age of this node has been estimated at 47-39 m.y. (Wikström et al. 2001), ca 62.2 m.y. (Tank et al. 2015: Table S2), about 89.5 m.y. (Magallón et al. 2015), or about 88 m.y. (Hernández-Hernández et al. 2014).
Evolution: Divergence & Distribution. There is a fair bit of diversification here.
[Caryophyllaceae [Achatocarpaceae + Amaranthaceae]]: (phytoecdysteroids +); stamens = and opposite P; ovule single [per flower], parietal tissue ca 4 cells across, nucellar cap 2-4 cells across; esp. outer wall of exotesta thickened and with stalactite-like projections; mitochondrial rps1 and 19 genes lost.
Age. The crown age of this clade is estimated at 38-29 m.y. (Wikström et al. 2001), (72-)59, 55(-44) m.y. (Bell et al. 2010), ca 57.6/52.6 m.y. (Tank et al. 2015: Table S2), or about 70.1 m.y. (Magallón et al. 2015).
Chemistry, Morphology, etc. For phytoecdysteroids, see Báthori et al. (1987), Dinan et al. (1998), and Zibareva et al. (2003). Mickesell (1990) listed both Amaranthaceae and Caryophyllaceae as having endosperm haustoria. Sukhorukov (2007) described the exotegmic cells of Chenopodiaceae s. str. as often having tannin deposits in the outer walls of the exotegmic cells that projected into the cell lumen (see also Kadereit et al. 2010). See also Sukhorukov et al. (2015: fruit and seed).
Since Achatocarpaceae are poorly known, most of the features mentioned above as possibly characterising the clade need to be confirmed.
CARYOPHYLLACEAE Jussieu, nom. cons. Back to Caryophyllales
Herbs, annual to perennial, (shrubs, lianes); cyclopeptides, anthocyanins, glycoflavones, anthraquinones +; cork cambium usu. deep-seated; true tracheids, fibres +; (wood rayless); pericyclic fibres +; nodes often swollen; stomata often diacytic; (cuticle waxes as rodlets); lamina vernation conduplicate or ± flat, stipules +, ± scarious; flowers 4-5-merous; hypanthium +; A (1-4); outer secondary parietal cell dividing, tapetal cells 2-nucleate; (pollen 6(+) pantoporate); (nectary surrounding or abaxial to [esp. antesepalous] A on receptacle); G [2-5], both alternate with and opposite "C", when 3 odd member adaxial, placentation ± axile, styles impressed [distribution?]; ovules with funicle longish to short, parietal tissue 3-10(-30) cells across, (in radial rows), (nucellar cap 2 cells across), (nucellar epidermis dividing along sides of ovules), obturator +, placental, hairy; fruit an utricle/achene/nutlet; (endotesta thickened; endotegmen ± thickened), ?tegmen bar thickenings; post-fertilization embryo sac with (chalazal) haustorium/diverticulum during early development, (suspensor massive), embryogeny solanad[!]; n = 7-15, 17; protein bodies in nuclei; mitochondrial coxII.i3 intron 0; sporophytic self-incompatibility system present.
101 [list]/2,200 (2,625) - 11 groups below. Mostly temperate, esp. Eurasian (map: from Vester 1940; Frankenberg & Klaus 1980; Hultén 1971; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; FloraBase i.2013; Australia's Virtual Herbarium i.2013). [Photos - Collection, Minuartia Habit, Microphyes Flower.]
1. Corrigioleae Dumortier
[Stipules auriculate]; leaves spiral; P with scarious margins; G with incomplete septae; fruit utricle or nutlet, or many seeded capsule; endotegmic cells lacking bar-like thickenings; genome size [1C] ca 0.49 pg.
2/16. Mediterranean to Pakistan, Africa, Chile; Corrigiola litoralis widely distributed.
Synonymy: Corrigiolaceae Dumortier, Telephiaceae Martynov
[Paronychieae [Polycarpaeae [Sperguleae [[Sclerantheae + Sagineae] [[Arenarieae + Alsineae] [Sileneae [Caryophylleae + Eremogeneae]]]]]]]: leaves opposite.
2. Paronychieae Dumortier
[Stipules paired, subadaxial to petiole; paired, connate, adaxial; single, concave, adaxial or interpetiolar]; P hooded, with subapical abaxial awn, (with scarious margins), ("C" +, filiform); (staminodes +); (pollen pantoporate); fruit a nutlet.
15/190: Paronychia (110), Herniaria (45). Worldwide, esp. Paronychia, many genera Mediterranean to Middle Eastern.
Synonymy: Herniariaceae Martynov, Illecebraceae R. Brown, nom. cons., Paronychiaceae Jussieu
[Polycarpaeae [Sperguleae [[Sclerantheae + Sagineae] [[Arenarieae + Alsineae] [Sileneae [Caryophylleae + Eremogeneae]]]]]: anthocyanins +, betalains 0 [?here, not in "Paronychioideae"]; "C" +; joint A-"C" primordium + [how common?].
3. Polycarpaeae de Candolle
Stipules + [interpetiolar fimbriae, from common primordium]; K usu. hooded, awned, (with scarious margins), ("C" deeply lobed to entire); (pollen pantoporate); styles basally connate; (fruit a capsule, seeds ³2/fruit).
Polycarpaea (50), Drymaria (48). Almost worldwide.
Synonymy: Ortegaceae Martynov, Polycarpaeaceae Schur
[Sperguleae [[Sclerantheae + Sagineae] [[Arenarieae + Alsineae] [Sileneae [Caryophylleae + Eremogeneae]]]]] / Plurcaryophyllaceae [sic]: wood rayless [?here]; hypanthium 0; A 10(+), (staminodes +, alternating with P); (placentation axile at least basally when ovary young); fruit a septicidal and loculicidal capsule, ³2 seeds/fruit.
4. Sperguleae Dumortier
[Stipules single, interpetiolar, connate and encircling stem below leaves]; K with scarious margin.
Spergula (60). ± worldwide.
Synonymy: Spergulaceae Bartling
[[Sclerantheae + Sagineae] [[Arenarieae + Alsineae] [Sileneae [Caryophylleae + Eremogeneae]]]]: stipules 0; nuclear genome duplication [or next node up].
[Sclerantheae + Sagineae]: ?
5. Sclerantheae de Candolle
(Hypanthium +); (K with membranous margins); ("C" 0); (nectary); A 1-10, (5 staminodes); (fruit a nut, 1-seeded).
Schiedea (34). Northern Hemisphere, Australasia, Ethiopia.
Synonymy: Scleranthaceae Berchtold & J. S. Presl
6. Sagineae J. Presl
(Hypanthium +); (K awned; with scarious margins); (A = "C"); (fruit a nut, 1-seeded).
Sabulina (65), Minuartia (55). Northern hemisphere, tropical montane, temperate southern hemisphere.
Synonymy: Minuartiaceae Martinov, Saginaceae Berchtold & Presl, Sabulinaceae Döll
[[Arenarieae + Alsineae] [Sileneae [Caryophylleae + Eremogeneae]]]: capsule often with 2X teeth as styles; embryogeny caryophyllad.
[[Arenarieae + Alsineae]]: ?
7. Arenarieae Kitt.
(Oily funicular aril - Moehringia); cotyledons incumbent.
Arenaria (135). Northern hemisphere, Central and west South America.
Synonymy: Sarcocaceae Adanson [?status]
8. Alsineae Lamarck & de Candolle
(Hypanthium +); (K with scarious margins), "C" ± retuse; micropyle endostomal, parietal tissue ca 3 cells across; (fruit a nut, 1-seeded); seed exotestal + endotegmic, or testal.
Stellaria (175), Cerastium (100), Odontostemma (65). Northern Hemisphere, esp. Eurasian, some cosmopolitan.
Synonymy: Alsinaceae Bartling, nom. cons., Cerastiaceae Vest, Stellariaceae Berchtold & J. Presl
[Sileneae [Caryophylleae + Eremogeneae]]: veins at apex of lamina intramarginal; K ± connate; (anthophore [prolongation between K and the rest of the flower] +); "C" clawed, contorted, apex retuse or not, venation closed, coronal scale +/0.
9. Sileneae de Candolle
(Plant dioecious); K with commissural veins, "C" (imbricate), ?direction contorted; (placentation axile basally); n = ?
?6/738: Silene (700). North Temperate, African montane.
Synonymy: Lychnidaceae Döll, Ortegaceae Martynov, Silenaceae Bartling
[Caryophylleae + Eremogeneae]: ?
10. Caryophylleae Lamarck & de Candolle
("Epicalyx" +); K (with membranous commissures), commissural veins 0 (scarcely evident); "C" right-contorted (imbricate), (ligulate); G [2 (3)]; 2-many ovules/carpel; capsule with 4 (6) teeth; (seeds peltate, embryo straight); n = 6, 10, 12-15, 17-18.
14/645: Dianthus (300<), Gypsophila (150), Acanthophyllum (95). Eurasia, N. Africa, few North America, Pacific Islands, Gypsophila australis Australia and New Zealand.
Synonymy: Dianthaceae Vest
11. Eremogoneae Rabeler & W. L. Wagner
Plant ± rosette-forming; leaves linear to graminoid; hypanthium poorly (well) developed; K not connate, often with scarious margins, often hardened at base, "C" not clawed, ?contorted, coronal scale 0; cotyledons accumbent; n = 11.
2/97: Eremegone (90). (Eur)Asian, W. North America.
Age. The earliest fossils associated with Caryophyllaceae seem to be of the pollen Periporopollenites polyoratus, from the Late Campanian ca 73 m.y.a.. This has been linked with the macrofossil Caryophylliflora paleogenica from the Eocene of Tasmania, but these fossils cannot be identified as any known member of the family (Jordan & McPhail 2003).
Evolution: Divergence & Distribution. The diversification rate in European Dianthus is surprisingly high, 2.2-7.6 species/m.y., and (at the time) the highest rate recorded for either plants or terrestrial vertebrates (Valente et al. 2010a: see also Espeletia and Lupinus). The genus is summer-flowering (i.e. it flowers during the dry season) and contains many narrow endemics (Valente et al. 2010a).
Schiedia forms a substantial radiation on Hawaii, species being herbs to shrubs or vines, and some have become wind pollinated and dioecious (Sakai et al. 1997). Relatives appear to include Honckenya and co., from the Arctic and subarctic (Harbaugh et al. 2009a; see also Shaw & Gillespie 2016).
The phylogenetic structure now evident in the family has considerable implications for character evolution, and for optimisation of characters in the context of a well-sampled phylogeny, see Greenberg and Donoghue (2011, but c.f. Fig. 5c).
Ecology & Physiology. Caryophyllaceae include numerous species that prefer cool/cold environments, movement to areas with such conditions perhaps being associated with the genome duplication recorded in the family (S. A. Smith et al. 2017), and there are over 100 species that are cushion plants adapted to cold, dry environments and often growing at higher altitudes (Boucher et al. 2016b).
Pollination Biology & Seed Dispersal. There is an association between some species of Silene and its relatives, mostly from the Medierranean, and Hadena, a largely Eurasian noctuid moth; Hadena lays eggs on the ovary/calyx, and the larvae eat at least some of the seeds, but the moth (both sexes) is also a pollinator - this is an obligate relationship for Hadena, rather like the yucca-yucca moth association (Kephart et al. 2006 for literature, also other papers in the New Phytologist 169(4). 2006; Prieto-Benítez et al. 2017). Some 70 species of Caryophyllaceae in over 10 genera and some 22 species of Hadena are involved (Prieto-Benítez et al. 2017), but these figures are likely ot be underestimates. Flowers are also pollinated by other moths whose caterpillars do not eat ovules or seeds (Kula et al. 2013). See also Ranunculaceae, Saxifragaceae, Phyllanthaceae, Moraceae and Asparagaceae-Agavoideae for similar relationships; Hembry and Althoff (2016) and Kawakita and Kato (2017f) review diversification and coevolution in these groups.
Bacterial/Fungal Associations. Ectomycorrhizae have been reported from the family (Wang & Qiu 2006), while Newsham et al. (2009) noted the frequency of arbuscular mycorrhizae in polar Caryophyllaceae and Lekberg et al. (2015) found that Dianthus deltoides might be associated with AM fungi, there being some movement of carbon from plant to fungus.
For anther smut fungi, see Ngugi and Scherm (2006); pollen is replaced by teliospores of Microbotryum violaceum s.l. (Uredinomycota - see also Montiaceae) and tranported by would-be pollinators to other plants. Microbotryum is common on the family, especially on perennial Sileneae (ca 80% of the species), but not much on the annuals or on members of the old Paronychioideae; strict cospeciation is not involved (Refrégier et al. 2008; Mena-Ali et al. 2009; Hood et al. 2010).
Genes & Genomes. Genome duplications in the family are quite common, and many of them are quite shallow (Y. Yang et al. 2017; S. A. Smith et al. 2017).
There has been a massive increase in the rate of synonymous substitutions in the mitochondrial genome of Silene noctiflora, but not in that of the chloroplast genome, nor in the substitution rates of its immediate relatives (Mower et al. 2007). The mitochondrial genome S. conica is, at 11.9 mb, bigger than the whole nuclear genome of some eukaryotes, while S. latfolia has quite a small mitochondrial genome of only 0.25 mb. Species of Silene with such huge mitochondrial genomes may have over a hundred micro-chromosomes, as least from the evidence of the mapping procedures used (Sloan et al. 2012). At around 7 Mb in size (over 7 x 106 base pairs) the genome of Silene noctiflora is arranged in over 50 chromosomes, not all of which have functional genes - and which are thus easily lost (Wu et al. 2015).
Mutation rates of some chloroplast genes, even in the inverted repeat region, have greatly accelerated, and there is variation in the position of the IR boundary and other structural changes in the chloroplast genome of some species of Silene, and similar changes seem to have occurred in parallel (Sloan et al. 2014; Zhu et al. 2015).
For the evolution of dioecy in Silene, which happened three times or so, see Desfeux et al. (1996) and Zluvova et al. (2008). Species of Silene subgenus Elisanthe have an X-Y 'sex' determination system (Lebel-Hardenack et al. 2002; Charlesworth 2008), also Papadopulos et al. (2015: rapid change in the Y chomosome of S. latifolia) and Hu and Filatov (2016) and references.
Chemistry, Morphology, etc. Variation in stipule morphology in Caryophyllaceae is considerable, even during the course of development of a single plant, as in Paronychia argentea (Rutishauser 1981).
In Pseudostellaria, at least, the stamens are initiated before the corolla (Luo et al. 2012). The long, curved nectary in some species of Schiedia develops on the abaxial bases of the stamens opposite to the calyx (Wagner & Harris 2000; esp. Harris et al. 2012). Weberling (1989 and references, esp. Thompson 1942) discusses placentation, which varies from axile, as in some species of Silene, perhaps the common condition in the family, to free central to the single, basal ovule of Uebelinia (this latter looks rather like a circinotropous basal ovule). For fruit morphology (dehiscent?) and anatomy of Corrigioleae, see Sukhorukov et al. (2015). A "chalazal" haustorium or diverticulum develops on the inside of the curved embryo sac in many species and the nucellus in Agrostemma is massively thick (Rocén 1927). Members of the old Paronychioideae in particular have solanad rather than caryophyllad embryo development.
Some general information is taken from Bittrich (1993b) and McNeill (1962: the old Alsinoideae, also maps), for Sileneae, see Oxelman et al. (2013 onwards), for chemistry, see Hegnauer (1964, 1989), for the distribution of phytoecdysteroids, see Zibareva et al. (2003) and Zibareva (2009) and for that of cyclopeptides, see Jia et al. (2004), for stomata, see Rohweder et al. (1971: correlation between stomatal apparatus and leaf width), for stem anatomy, see Schweingruber (2007), for floral morphology, etc., see Thompson (1942), Rohweder (1967b, 1970a), Rohweder and Urmi-König (1975) and Rohweder and Urmi (1978), for stamens or nectaries as corolla, see Mattfeld (1938) and Leins et al. (2001), for ovules and seeds, see Meunier (1890), Dahlgren (1940a), L. Wang et al. (2017) and Arabi et al. (2017: external morphology, Alsineae), and for much information on ovules and early embryogenesis, see Rocén (1927), also Cook (1909), Perotti (1913).
Phylogeny. Of the old subfamilies, Paronychioideae - classically defined by the presence of stipules, lack of a corolla, and utricular fruit - form a basal grade, with Corrigioleae (Telephium, Corrigola) sister to all the rest of the family. Dicheranthus, Polycarpon, etc., may form the next clade, Paronychia, etc., the next. Drymaria and Pycnophyllum, both morphologically distinctive taxa, may be sister (Smissen et al. 2002 - they noted that Pycnophyllum [and Pentastemonodiscus] were not to be included in Caryophyllaceae-Alsinoideae, but they did not suggest where they should go; Fior et al. 2006). In the erstwhile Alsinoideae the calyx is free and the corolla has ± open venation. Alsinoideae for the most part break down into two groups: one, including Cerastium, Stellaria, etc. (Alsineae), has capsules with split valves, and the other, including much of Minuartia, Sagina, etc. (Sagineae), is very diverse, but has capsules with entire valves; the corolla is often bilobed. Caryophylloideae, with their connate calyx and a clawed corolla with more or less closed venation and adaxial appendages (ligules), are holding up better phylogenetically. The tribes Sileneae and Caryophylleae are perhaps monophyletic, and together are sister to or form a polytomy with part of Arenaria (Nepokroeff et al. 2002; Fior et al. 2006). Relationships in Harbaugh et al. (2010) - on the whole well supported - from a three-gene analysis are [Corrigolieae [Paronychieae [Polycarpeae [Sperguleae [[Sclerantheae + Sagineae] [[Arenarieae + Alsineae] [Sileneae [Caryophylleae + Eremogeneae]]]]]]]]. Greenberg and Donoghue (2011) sampled more extensively but found a largely similar topology; a novel clade that they found, [[Sclerantheae + Sagineae] [[Arenarieae + Alsineae]], did not have much support. The position of the newly described Eremegoneae was uncertain in Harbaugh et al. (2010), but support was stronger in Greenberg and Donoghue (2011); in its current position its apomorphies are losses of the apomorphies of the whole [Sileneae [Caryophylleae + Eremogeneae]] clade, or, alternatively, these features arise independently in Sileneae and Caryophylleae... For relationships among Chineae taxa, see Z.-D. Chen et al. (2016).
Some genera are highly polyphyletic, so members of Arenaria ended up in Arenarieae, Alsineae and Eremogeneae (Sadeghian et al. 2015). Fior and Karis (2007 and references) looked at relationships in Moehringia (Arenarieae) and its allies and the evolution of its strophiole. Within Caryophylleae, Pirani et al. (2014) discuss the phylogeny of Acanthophyllum, and Valente et al. (2010a) the phylogeny of Dianthus in Eurasia, while Madhani et al. (2018) provide a comprehensive phylogeny of the tribe. Within Sagineae, Drypis, previously placed in Caryophylloideae because of its connate calyx, etc., is in the same immediate clade as Habrosia (ex Alsinoideae), so the variation there is considerable (Harbaugh et al. 2010; see also Greenberg & Donoghue 2011). In a comprehensive study, Dillenberger and Kadereit (2014) demonstrate the extensive polyphyly of Minuartia (Sagineae). For the phylogeny of Silene and its relatives (Sileneae), perhaps not monophyletic, see Desfeux and Lejeune (1996), Erixon and Oxelman (2008) and especially Naciri et al. (2017), for that of Viscaria, etc., see Frajman et al. (2009), and for relationships around Pseudostellaria, see M.-L. Zhang et al. (2017).
Classification. The old tripartite division of the family into Silenoideae, Alsinoideae and Paronychioideae was based on the presence of a hypanthium, whether or not the petals were emarginate, whether on not the calyx was fused, etc., and is not confirmed by recent work. Here I follow the tribal classification of Harbaugh et al. (2010, see also 2012: ?Drypidae Fenzl?). These authors did not sample a number of genera, so tribal compositions were uncertain, but the situation was considerably improved by Greenberg and Donoghue (2011). The tribal implications of the study by Dillenberger and Kadereit (2014) are unclear.
Features like number of styles and whether there is obviously a common stylar region often provided generic characters in the past, yet they turn out to be of little use (e.g. Dillenberger & Kadereit 2014). Thus the limits of Silene, historically characterised by having three styles, need to be expanded to include some taxa with five styles (Desfeux & Lejeune 1996); for a sectional classification of the genus, see Naciri et al. (2017). Genera like Arenaria and Minuartia are polphyletic (Harbaugh et al. 2009); indeed, many generic limits need attention (Greenberg & Donoghue 2011). Sadeghian et al. (2015) made some nomenclatural adjustments because of the polyphyly of Arenaria, while Dillenberger and Kadereit (2014) have dismembered Minuartia, necessary because the genus in its old, broad circumscription was hopelessly polyphyletic, and they note that several other genera are para- or polyphyletic - yet more nomenclatural changes are needed (see also Kadereit et al. 2016). See Madhani et al. (2018) for genera in Caryophylleae.
Botanical Trivia. There are reports of placental tissue from 30,000 year old material of Silene stenophylla (or perhaps from another species of the genus) trapped in permaforst being persuaded to form whole plants (Yashina et al. 2012a, b).
[Achatocarpaceae + Amaranthaceae]: pollen pantoporate; ovule single, basal.
Age. The age of this node may be around (94-)67.2(46) m.y. (Masson & Kadereit 2013), ca 64.2 m.y. (Magallón et al. 2015), or ca 52.6 m.y. (Tank et al. 2015: Table S2).
ACHATOCARPACEAE Heimerl, nom. cons. Back to Caryophyllales
Woody; C-glycosylflavonoids +, betalains 0; secondary growth normal; nodes ?; cuticle waxes as ± lobed platelets in clusters; (P 4); A 10-20, basally connate or not; pollen 6-pantoporate; G , collateral or superposed; ovules (2), details?; fruit a 1-seeded berry; seeds with small aril; n = ?
2 [list]/7. S.W. USA to South America (map: from Fl. N. Am. 4: 2003; GBIF 2008). [Photo © C.E. Hughes - Fruits, Fruiting branch.]
Evolution. Bacterial/Fungal Associations. Achatocarpus may be ectomycorrhizal (see also Brundrett 2017a; Tedersoo 2017b; Tedersoo & Brundrett 2017 for literature, ages, etc.).
Chemistry, Morphology, etc. Some information is taken from Bittrich (1993b); for wood anatomy, see Carlquist (2000c), Sukhorukov et al. (2015: p. 13) describe the perisperm as having distinctive "starch-granule conglomerates".
AMARANTHACEAE Jussieu, nom. cons. Back to Caryophyllales
Succulent, herbaceous or shrubby (lianes), often in saline conditions; anthraquinones, (isoquiniline alkaloids), 6-7-methylene-dioxyflavonols, isoflavonoids +, soluble calcium oxalate accumulation; successive cambia +, inc. roots; wood storied, rayless, esp. when young; vessels in multiples; pericyclic fibres few (0); cork cambium pericyclic [esp. chenopods; and elsewhere]; crystal sand + [less common in chenopods]; cortical and/or medullary vascular bundles + [less common in amaranths s. str.]; sieve tube plastids lacking protein crystalloids, (starch grain +); nodes often swollen, (1:3, 1:5: C/A); petiole bundles ± annular; stomata also paracytic (dia- and anisocytic); hairs variable, often uniseriate; (leaves opposite), lamina margins often toothed; P (1-8); stamens joining nectariferous disc, anther wall development monocotyledonous; tapetal cells 2(-5)-nucleate, (amoeboid); pollen often starchy, foot layer well developed; G [1-3(-6)], (subinferior), annular and open early in development, (median member abaxial), placentation basal, (apical), style ± developed, stigmas various; ovule also amphitropous, etc., with parietal tissue 2-9 cells across, in radial rows or not, nucellar cap 2-4 cells across, (chalazal region ± digested by the embryo sac); (antipodal cells persist); fruit indehiscent, or circumscissile capsule, (berry; drupe); exotesta with stalactite thickenings, endotegmen ± thickened and lignified, tanniniferous; (perisperm 0), (embryo sac haustorium during early development), embryo chlorophyllous or not.
183 - 104 chenopods and 79 amaranths - [list]/2,050-2,500. ± World-wide, esp. warm and dry temperate and subtropics and saline habitats (map: from Hultén & Fries 1986; Jalas et al. 1999; Culham 2007). [Photo - flowers, fruits, Collection.]
Age. An age for the clade of 87-47 m.y. is possible (Kadereit et al. 2012: note topology).
Amaranth-type taxa/Amaranthaceae s. str.: cuticle waxes lacking platelets; inflorescence branched or not, spike-like or capitate, ultimate units cymes; bracteoles ± papyraceous/scarious; P scarious, white or pigmented; A basally connate, with pseudostaminodes; pollen metareticulate; embryogeny chenopodiad[!]; n = (6-)8-9(-13, etc.).
[Celosioideae + Amaranthoideae]: ?
nuclear genome duplication [?here].
[Aervoideae [Achyranthoideae + Gomphrenoideae]]: gene duplication.
[Achyranthoideae + Gomphrenoideae]: ?
(P hairs branched); (A 5> - inc. 1, + 4 staminodes); (style excentric, curved).
Anthers bisporangiate, monothecal, (androecial tube intercalary in origin), (pseudostaminodes +, unvascularized); pollen with orbicules, metareticulate, mesocolpium raised; (G stipitate); nuclear genome duplication.
Gomphrena (120), Alternanthera (100), Iresine (70).
Chenopod-type taxa/Chenopodiaceae s. str.: isoflavonoids common; wood usually rayless; cuticle waxes as platelets; bracteoles 0; bracts and P ± fleshy/herbaceous, red to ± green; P quincuncial; carpellate flowers: P unequal, 3 smaller; disseminule an anthocarp, bract, perianth variously accrescent, (with spines, hooks, etc.), fruit an utricle/(capsule, circumscissile); (embryo chlorophyllous); x = 9; 300 bp deletion in chloroplast DNA inverted repeat.hairs adaxial to the leaf base - Anabasis
[[Suaedoideae + Salicornioideae] [Camphorosmoideae + Salsoloideae]]: ?
Age. The age of this node is around 41.3-37.6 m.y. (Kadereit et al. 2006); another estimate is 55.5-46.8 m.y. (Kadereit & Freitag 2011).
[Suaedoideae + Salicornioideae]: plants often of saltmarshes; lamina not developed; P basally connate.
Age. This node was dated to 38.2-28.7 m.y. (Kadereit et al. 2006) or ca 39 m.y. (Piirainen et al. (02017).
Annual to perennial herbs to shrubs; plant usually glabrous; lamina usually terete; inflorescence spicate, loose, leafy, bracteoles +; G [2-3], (inferior), (styles impressed), (connate and ± infunduliform), (capitate), filiform, papillate all around; P ± enlarged/winged in fruit, diaspores commonly heteromorphic; perisperm 0, embryo spiral.
2/83: Suaeda (82). ± worldwide, especially Central to East Asia, not forests.
Annual to perennial herbs, to shrubs and small trees; stem usu. articulated; leaves usu. opposite, ± terete or scaly, (reduced to a rim, etc.), base (semi-)amplexicaul, (decurrent, connate); inflorescence dense, spike-like, leafless; P (2-)3-4(-5), ± connate; A (1-)2-3(-4); G [2-3]; perisperm (0), endosperm ?copious.
15/110: Tecticornia (44), Sarcocornia (30). ± Worldwide, esp. temperate and tropics, not humid tropics, most in the Australian region.
Age. Crown-group Salicornioideae are 35-25.3 m.y.o. (Kadereit et al. 2006) or ca 29.1 m.y.o. (Piirainen et al. 2017).
Synonymy: Salicorniaceae Martynov
[Camphorosmoideae + Salsoloideae]: often plants of deserts and steppes; hairs long, jointed, multicellular [young plant at least]; leaves often isobifacial; fruiting perianth often with wings; exotestal stalactite thickenings 0.
Age. The age of this node is some 43.6-32.2 m.y. (Kadereit & Freitag 2011).
Often shrubby (herbaceous, annual); hairs with swollen bases, with "prickles"; leaves terete, (C4 photosynthesis); (flowers unisexual); pollen usu with >70 pores; styles filiform, with papillae all around; fruiting perianth also fleshy, spiny.
22/180: Sclerolaena (64), Maireana (57). Northern Temperate to subtropical, to the Sahara, W. North America, southern Africa, esp. Australia (map: from Kadereit & Freitag 2011).
Age. The age of crown-group Camphorosmoideae has been estimated at 27-17.3 m.y. (Kadereit & Freitag 2011).
Annual herbs or shrubs (trees); C4 photosynthesis [?in all]; leaves (opposite), terete; bracteoles +; P separate, quincuncial; anther appendages coloured, vesicular [Caroxyloneae]; stigmas flattened, papillae adaxial; (capsule circumscissile); diaspores commonly heteromorphic; seed compressed, coat often thin; perisperm 0, embryo spiral, (cotyledons terete), (chlorophyllous).
32/300-400: Salsola (100). Esp. central to southwest Asia, northern and southern Africa, Australia.
Age. The age of crown-group Salsoloideae is some 43.6-36.1 m.y. (Kadereit & Freitag 2011).
Synonymy: Salsolaceae Menge
[Betoideae [Corispermoideae + Chenopodioideae]]: ?
Annual to perennial herbs (subshrub; vine); bracteoles +[?]; (G semi-inferior); (T persistent, accrescent - Beta); capsule circumscissile.
6/14. N. India to maritime Europe, California (Map: from Hohmann et al. 2006).
Age. The age of crown-group Betoideae is about 48.6-35.4 (including Acroglochin) or 38.4-27.5 (excluding it) m.y. (Hohmann et al. 2006).
Synonymy: Betaceae Burnett
[Corispermoideae + Chenopodioideae]: ?
Annual herbs; hairs stellate or branched; inflorescence spicate, (flowers unisexual); fruits/seeds monomorphic; pericarp parenchymatous outside ["uppermost"], sclerenchymatous internally ["below"], no crystal layer; testa thin, tanniniferous, exotestal stalactite thickenings 0.
Synonymy: Corispermaceae Link [?status]
(C4 photosynthesis); (cuticle waxes 0); gland or bladder hairs +; (flowers unisexual); (carpellate flowers: P 0); (fruit a pyxidium); (diaspores heteromorphic); pericarp usu. thin, evascularized; testa tanniniferous, exotesta much enlarged, with tannin stalactites (0); x = (8) 9.
10/500: Atriplex (300), Chenopodium (150), Dysphania (40).
Synonymy: Atriplicaceae Jussieu, Blitaceae Kuntze, Chenopodiaceae Ventenat, nom. cons., Dysphaniaceae Pax, nom. cons., Spinaciaceae Menge
Annual to perennial herbs or small shrubs; habitat often ± saline; flowers axillary, bracteoles large; P petaloid; A basally connate, 5 (3, 2); (anthers unilocular); pollen smooth, (with microspines - Surreya); stigma ± capitate, papillate; G ; exotesta with stalactites; n = 9.
4/11(-13). Widely scattered, ± Temperate (map: see Masson & Kadereit 2013; Australia's Virtual Herbarium vii.2013).
Age. Crown-group Polycnemoideae are dated to (54.0-)35.6(-19.5) m.y.a. (Masson & Kadereit 2013).
Synonymy: Polycnemaceae Menge
Evolution: Divergence & Distribution. There may have been an increase in the diversifictaion rate at this node that is dated to (64.1-)51.0(-43.7) m.y.a. (Magallón et al. 2018).
Chenopodioideae s.l. probably originated in Eurasia, perhaps in environments close to the shore, with subsequent movement around the northern hemisphere and then into the southern hemisphere (e.g. Hohmann et al. 2006; G. Kadereit et al. 2010, 2012). For instance, there have been some nine invasions of Australia, mostly since the late Miocene so within the last 10 m.y. (Kadereit et al. 2005), and there have probably been two invasions by C4 Atriplex into North America and then to South America, and two invasions of Australia (Prideaux et al. 2009; Kadereit et al. 2010 - for further details, see Ecology and Physiology below). Within Betoideae, California-Mediterranean disjunctions have been dated to 15.4-8.1 m.y.a., perhaps via Beringia (Hohmann et al. 2006).
Ecology & Physiology. Amaranthaceae include some 500 species with the C4 photosynthetic syndrome, fully one third of all BLA species with the syndrome (Osmond et al. 1980; Sage et al. 2012; Bena et al. 2017). There have been 15 or more independent acquistions of the C4 pathway, perhaps with reversals (e.g. Pyankov et al. 2001; Kadereit et al. 2012). The first acquisition of C4 photosynthesis in Amaranthaceae can be dated to the early Miocene ca 24 m.y.a., while the age of a major C4 clade in Atriplex (Chenopodioideae) can be dated to 14.1-10.9 m.y., and other acquisitions may be a quarter of that age or less (Kadereit et al. 2003; Kadereit et al. 2010; Kadereit & Freitag 2011: Christin et al. 2011b for many dates), however, Kadereit et al. (2012) estimated that the first acquisition was a little earlier (47-22 m.y.a.) at the Eocene/Oligocene boundary. Two thirds of the C4 acquisitions are in the old Chenopodiaceae (Akhani et al. 1997; Pyankov et al. 2001; Kadereit et al. 2003, 2012; Sage et al. 2007, 2011; Kadereit & Freitag 2011). Within North American Atripliceae, Atriplex s. str., there has been a single origin of C4 photosynthesis (Zacharias & Baldwin 2010). For parallel evolution of C4 leaf types in Camphorosmeae, see Kadereit et al. (2014). There are several types of C4 photosynthesis and ca 17 different kinds of leaf anatomy, not all C4, in the family (e.g. Edwards & Voznesenskaya 2011; Freitag & Kadereit 2014). For summary comparisons of the chloroplast types of C3 and C4 taxa, see Koteyeva et al. (2011b), and for comparisons of two C4 species, see Koteyeva et al. (2011c). In Gomphrenoideae C4 photosynthesis has arisen three times or so probably in species growing in warm and more or less humid environments, and C4 species tend to occur more in drier and winter-cool habitats (Bena et al. 2017). However, the literature is extensive, and I have not done it justice, but the references below should serve as an entrance.
Voznesenskaya et. al. (2013) discuss in detail transitions between photosynthetic types in the predominantly C4 Salsoleae. For the evolution of enzymes involved in C4 photosynthesis in Alternanthera, where there are also C2 intermediates, see Gowik et al. (2006); C4 photosynthesis seems to have originated once here (Sánchez-del Pino et al. 2012). Rosnow et al. (2014b) noted that different amino acids were to be found in Suaedoideae in a position thought to be critical in determining affinity for phospoenolpyruvate in the carboxylase enzyme. In at least four Suaedeae s.l. all the different elements of C4 photosynthesis are to be found within a single cell, and although there is no conventional Kranz anatomy, the chloroplasts involved in different parts of the carbon fixation process are distinct and spatially segregated; this condition has evolved independently at least twice (Kapralov et al. 2006: Bienertia, Suaeda). Partitioning of the plastids within the cell is maintained by the distinctive organization of the cytoskeleton (Chuong et al. 2006), although plasticity is induced by the light environment (Lara et al. 2008). The different plastids in Beinertia may be either proximal and distal (with respect to adjacent veins) in elongated cells, or peripheral and central, the latter domain including most chloroplasts and being where the C3 part of the pathway occurs (Offerman et al. 2011); Rosnow et al. (2014a) explore how the chloroplasts differentiate.
Chenopods in general are most diverse in deserts from Sahara to Central Asia, and there are links between drought and salt tolerance and C4 photosynthesis. C4 species developed in lineages that were already adapted to drought and could tolerate salt, and they moved in to yet more arid environments (Kadereit et al. 2012). Many succulent chenopod C4 halophytes grow in the Irano-Turanian region (Ogburn & Edwards 2010) and they make up a major element of the vegetation there. In the rather cold Gobi deserts 15-17% of the species are C4 plants (they are only 3.5% of the total Mongolian flora), and they contribute 30-90% of the biomass there (Vostokova et al. 1995; Pyankov et al. 2000). Over 50% of the total C4 flora in the Gobi Desert is made up of fast-growing C4 chenopods (there are also some Polygonaceae), some of which are arborescent. A similar combination of plants also dominates the halophytic vegetation of the Central Asian Turanian deserts (Winter 1981); these are somewhat warmer than the Gobi deserts. Some of these C4 plants get quite large, Haloxylon aphyllum (Amaranthaceae) attaining 10 m in height and with a trunk 1 m across (Winter 1981). Succulent C3 chenopods are common in the Gobi in true desert conditions, and also in moist, saline soils (Pyankov et al. 2000).
The largest concentration of halophytes - plants that can tolerate conditions in which the electrical conductivity of the soil solution is equivalent to ca 80 mM NaCL or more (Bromham & Bennett 2014) - in flowering plants occurs here, with ca 510 halophytic species, mostly chenopods (381 spp.), in this clade (see also Saslis-Lagoudakis et al. 2016: also in Cyperaceae and Juncaceae). Halophytes here show "extreme conservation of salt tolerance" (Bromham 2015: pp. 334-335), arising only once or twice and salt tolerance being retained (Kadereit et al. 2012; Moray et al. 2015), and this is unlike the "tippy" (highly polyphyletic) distribution in other families that have a substantial number of halophytes, for instance, in Poaceae, where there is also frequent loss (Kadereit et al. 2012; Bennett et al. 2013; Bromham & Bennett 2014; Bromham 2015; Piirainen et al. 2017). A number of these halophytes, perhaps ca 43%, are also C4 plants, and there is a connection between these two features (Sage & Monson 1999; Jacobs 2001; Sage 2002; Flowers & Colmer 2008; Kadereit et al. 2012; Bromham & Bennett 2014), and also with heavy metal tolerance (Lutts & Lefève 2015), as in other families like Poaceae (see Rajakaruna et al. 2016 for extreme physiologies in general). Adaptations to salt tolerance like succulence, and also drought tolerance, may have first appeared in coastal plants of Eurasia in the Eocene and have later facilitated the subsequent adoption of C4 photosynthesis.
Furthermore, in common with some other groups inhabiting dry and/or saline habitats (including Tamaricaceae and Cactaceae), a number of Amaranthaceae s.l., mainly Chenopodiaceae s. str., have very fast germination. Here seeds usually have thin seed coats and long embryos and germinate within a single day from the start of imbibition, and this may begin when rain decreases salinity, temperatures are appropriate, etc. - quick establishment is of the essence (Parsons 2012; Parsons et al. 2014; esp. Kadereit et al. 2017). However, Chenopodiaceae-Salicornioideae and -Salsoloideae in particular can tolerate very high salt concentrations at germination, even saltier than seawater, and they may not germinate so quickly, while in taxa with heteromorphic diaspores (see also below), diaspores of one morph may show fast germination while those of the other morph enter the seed bank (Parsons 2012; Kadereit et al. 2017 for many details). C4 taxa may tolerate higher temperatures at germination, while in Australian Camphorosmoideae in particular the perianth part of the anthocarp is persistent and causes the seed to remain dormant (Kadereit et al. 2017).
Most work on salt tolerance has been carried out on a few species of Atriplex, with some on genera like Suaeda and Chenopodium, and knowledge of other genera is sketchy. The salt glands are epidermal hairs consisting of a stalk one to a few cells long and a head. Chloroplasts are reported from the stalk cells, at least (Kelley et al. 1962), and the plant gets rid of the accumulated salt when the heads break off or abscise (Schirmer & Breckle 1982). The hairs are commonest on younger parts of the plant where the problem of salt accumulation is most severe, although a number of other functions have also been ascribed to the salt glands (Karimi & Ungar 1989). For additional information on salt tolerance in Chenopodioideae, see articles in Ann. Bot. 115(3). 2015.
Chenopods are also very diverse in dry and/or saline conditions in Australia, with 279 species (as of 2004) endemic there (Kadereit et al. 2004). Aridification in Australia began early in the Miocene ca 22 m.y.a., and almost 150 species of shrubby drought- and salt-tolerant - and C3 - Camphorosmoideae began radiating there (11.5-)7.5(2.1) m.y.a., and these Australian Camphorosmoideae are sister to the Central Asian Grubovia, with a mere three species (Kadereit et al. 2004; Kadereit & Freitag 2011; Cabrera et al. 2012 for numerous dates; Freitag & Kadereit 2014; Mosyakin & Iamonico 2017). The diversity in Australian Salicornioideae is also great (Wilson 1980; Piirainen et al. 2017). Finally, C4 taxa like Atriplex (Chenopodioideae) also diversified extensively in Australia, mostly after 6.3-4.8 m.y.a. (Kadereit et al. 2010).
Some taxa of the amaranth Ptilotus, with around 90 species in Australia, accumulate high levels of phosphorus (Hammer et al. 2015).
Pollination Biology & Seed Dispersal. In Chenopodioideae s.l. in particular the perianth may become accrescent and envelop the fruit, being variously fleshy, winged or spiny and involved in dispersal, that is, the fruits are anthocarps (e.g. see illustrations in von Mueller 1889-1891; Fl. Austral. 4. 1984; Cabrera et al. 2009). Taxa with heteromorphic diaspores are quite common in Chenopodioideae (see Imbert 2002, also above), indeed, they are probably relatively more common here than in any other group of comparable size/age, and the diaspore types differ in their optimal conditions for germination, longevity, etc. (Song & Wang 2015; see also L. Wang et al. 2010; Gul et al. 2013; Kadereit et al. 2017).
Plant/Animal Interactions. Cecidomyiid midges (Asphondylia) form galls on chenopods like Sarcocornia and Tecticornia in Australia; fungi also live in the galls, although the relationship between the fungi and the midge larvae (the former are food for the latter?) is unclear (Teresa Lebel, pers. comm.).
Atriplex was probably a major item in the diet of the extinct giant (ca 230 kg) kangaroo Procoptodon goliah, and most of these species of Atriplex are in a clade that has diversified within the last 6.3-4.6 m.y. (Prideaux et al. 2009; Kadereit et al. 2010).
Bacterial/Fungal Associations. Although the family is apparently largely without mycorrhizae (see Delaux et al. 2014 for Beta and Spinacea), vesicular-arbuscular mycorrhizae have been reported from chenopods in the Red Desert of Wyoming - but only on native taxa and under undisturbed conditions (Miller 1979); c.f. also Zygophyllaceae.
Vegetative Variation. Nodal anatomy is nearly always unilacunar, but there is considerable variation in the number of traces that enter the leaf (e.g. Wilson 1924). For a discussion about the cortical vascular system and leaves of Salicornia and relatives, see Fahn and Arzee (1959), James and Kyhos (1961) and Beck et al. (1982), etc. (more literature in Piirainen et al. 2017). The question: Is the fleshy cortex of the stem of foliar or cauline origin?
Genes & Genomes. For genome size - small in the family as a whole - and evolution in Chenopodium s.l., see Kolano et al. (2015) and Mandák et al. (2016: ?sampling), and for that in Amaranthus see Stetter and Schmid (2017). For a gene duplication at the Aerva/Alternanthera node, see Y. Yang et al. (2015, 2017; S. A. Smith et al. 2017); there is also a duplication pegged to Amaranthus (S. A. Smith et al. 2017; Yang et al. 2017).
Economic Importance. For the American grain amaranths, see Clouse et al. (2016) and Stetter and Schmid (2017) and references - there are also some nasty glyphosate-resistent weedy amaranths, the pigweeds.
Chemistry, Morphology, etc. Triterpenoid saponins are common enough in flowering plants, but 30-noroleanane triterpenoids are distinctly less commen, and they have been found in two amaranth and four chenopod genera (Lyu et al. 2018; for saponins here, see Mroczek 2015). Fron (1899) looked at the anatomy of stem and root in young chenopods, i.a. noting that the arrangement of the vascular tissue could be spiral, although there could be variation here within a genus. Polycnemum and Nitrophila have been reported to have ordinary secondary thickening, but c.f. Heklau et al. (2012) and Masson and Kadereit (2013). The absence of rays in the wood is pervasive in the chenopods, with a few exceptions, and some amaranths also lack them (Carlquist 2015b; see also Carlquist 2003c). Stem collenchyma is well developed; there are nucleated xylem fibres (Rajput 2002). Stem-borne roots of Polycnemum seem to have a superficial cork cambium (Heklau et al. 2012). In 1:1 nodes in some Salicornioideae there are two lateral branches that diverge, descend, and enter the stem cortex (Wilson 1980).
The flowers of Chenopodioideae s.l. show a considerable amount of variation, partly because of the involvement of the perianth in fruit dispersal, and partly because the flowers may be quite reduced. In the reduced perianth of the Australian Tecticornia (Salicornioideae) the odd member is abaxial (for floral development, see Shepherd et al. 2005b). The flowers of Beta become semi-inferior during development (Flores Olvera et al. 2008) and the "bracteoles" enveloping the flower and fruit in some Atripliceae are modified perianth members (Flores-Olvera et al. 2011). Whether or not the flower parts of Chenopodium are spiral or whorled has occasioned much discussion (Sokoloff et al. 2018 and references).
Pollen of Amaranthaceae (inc. Chenopodiaceae) is fairly homogeneous (Nowicke 1975; Skvarla & Nowicke 1976), having a similarly thickened tectum, apertures with reduced pointed flecks of exine underlain by lamellar plates, and a thickened endexine; Pseudoplantago has cuboid pollen. However, there is quite a bit of variation beyond this (e.g. Borsch 1998; Borsch & Barthlott 1998). K. Müller and Borsch (2006c) discuss the evolution of the distinctive stellate pore ornamentation of the pollen of some Amaranthaceae s. str. - there are several independent gains and losses, and Sánchez-del Pino et al. (2016 and references) discusses the distinctive metareticulate pollen of Amaranthus.
2-carpellate members of the family usually have collateral carpels, but occasionally they are superposed. The chalazal region of the ovule is more or less digested by the embryo sac in at least some Amaranthaceae - and this is also once recorded from Nyctaginaceae (Maheshwari 1950). For fruit wall and seed coat anatomy in Chenopodioideae, see Sukhorukov and Zhang (2013); heteromorphism of diaspore type may be accompanied by variation in whether the embryo is chlorophyllous or not (Imbert 2002).
All in all, Amaranthaceae are morphologically heterogeneous, e.g. Pleuropetalum: Plant fleshy; leaves spiral; inflorescence racemose; A 8, connate basally; G [5-6], several basal ovules/carpel, fruit ± fleshy; n = 8, 9 - A paired in development (Ronse Decraene et al. 1999). Placed in Amaranthoideae by Townsend (1993); 3 spp. Tropical America, Galapogas.
Additional general information can be found in Eliasson (1988: Amaranthaceae), Robertson (1981: Amaranthaceae), Kühn (1993: Chenopodiaceae), Townsend (1993: Amaranthaceae), Judd and Ferguson (1999: Chenopodiaceae), Sukhorukov et al. (2014: Corispermoideae) and Zhu and Sanderson (2017: Chenopodiaceae). See also Blunden et al. (1999: betaine distribution, widespread), Hegnauer (1964, 1989: chemistry), Hu and Yang (1994), Rajput (2002), Carlquist (2003c) and Grigore et al. (2014), various aspects of anatomy, Joshi (1931: medullary bundles), Acosta et al. (2009: Ama) and Urmi-König (1981: Chen), inflorescence morphology, Payer (1857), Sattler (1973), Choob and Yurtseva (2007) and Flores Olvera et al. (2008, 2011), all Chen floral morphology, Hakki (1972, 1973: floral morphology, embryology: Chen), Meunier (1890), Kajale (1940b: extensive, amaranths), Wilms (1980), and Naidu (1984 and references), ovules and seeds, Shepherd et al. (2005b) and Sukhorukov et al. (2015: fruits and seeds, the former esp. chenopods), and Sukhorukov (2007, 2008: fruit wall anatomy); Flores Olvera et al. (2006), Tsymbalyuk (2008) and Zhu and Sanderson (2017) provide information on pollen.
Phylogeny. Cuénoud et al. (2002) found Amaranthaceae s. str. to be monophyletic, with very strong (97%) support, and Chenopodiaceae s. str. were perhaps monophyletic, but the branch collapsed in a strict consensus tree; the sampling was moderately good, but only the matK gene was analysed. In an extensive rbcL analysis, much of the old Chenopodiaceae were again monophyletic, but with little bootstrap support, ditto the old Amaranthaceae (incl. Polycnemoideae), while Betoideae were paraphyletic (G. Kadereit et al. 2003). Other studies had suggested that Chenopodiaceae were paraphyletic and perhaps even that Amaranthaceae were polyphyletic (Pratt 2003; Pratt et al. 2001). In an analysis of matK/trnK sequences, K. Müller and Borsch (2005b, c) found that Polycnemum and Nitrophila (100% support) were sister to the rest. Masson and Kadereit (2013) found a clade [other Amaranthaceae + Chenopodiaceae] had <70% bootstrap support and still lower PP values, while Amaranthaceae s. str. had 100% support and Chenopodiaceae s. str. again <70% bootstrap support yet 1.0 PP.; Amaranthaceae s. str. and Chenopodiaceae s. str. had similar support values in Kadereit et al. (2017), Polycnemoideae being placed sister to Chenopodiaceae, but support for this position was not strong. See also Z.-D. Chen et al. (2016) for relationships between the Chineae taxa, where these two main clades were not very well supported.
Within Amaranthaceae s. str. - at least some flowers are imperfect - Bosea and Charpentiera were successively sister to the rest, but Amaranthoideae, Amarantheae and Amarathineae were paraphyletic (e.g. Ogundipe & Chase 2009). Amaranthus is sister to Beta, etc., in ORF 2280 phylogenies, and this whole group is in turn sister to the [Celosia [(some Celosieae), Froelichia, etc. + Gomphreneae/Gomphrenoideae]] clade (Cuénoud et al. (2002). Amaranthoideae: for relationships in Amaranthus see Stetter and Schmid (2017). Gomphrenoideae: see Downie et al. (1997) and Sánchez-del Pino (2007). Within Gomphrenoideae are the iresinoids (Iresine should be circumscribed broadly), and the [gomphrenoids (Gomphrena is polyphyletic) + alternantheroids (Alternanthera is monophyletic)] (Sánchez-del Pino 2007; Sánchez-del Pino et al. 2009; see also Bena et al. 2017). The monophyly of Alternanthera has been confirmed (Sánchez-del Pino et al. 2012); for relationships in the Australian Ptilotus, see Hammer et al. (2015).
Relationships within the old Chenopodiaceae are having to be much reworked because the often highly reduced and modified flowers and fruits have been difficult to understand and interpret and previous taxon delimitations are unsatisfactory; see G. Kadereit et al. (2005) for relationships in Australian chenopods, Australia being a centre pof diversity for the group. Betoideae: Hohmann et al. (2006) found that Acroglochin, with circumscissile capsules like other members of the subfamily, tended to wander around the tree; they did not place it. Camphorosomoideae; Cabrera et al. (2009) looked at relationships in the Australian Camphorosmoideae, a monophyletic group, and Kadereit and Freitag (2011) at Camphorosmoideae as a whole. Chenopodioideae: Kadereit et al. (2010) examined relationships in Atripliceae, and Chenopodium as included there turned out to be polyphyletic; Fuentes-Bazan et al. (2012a) found that Atriplex and other genera were nested within Chenopodium s.l. - in fact, members of four tribes were intermingled (see also Kolano et al. 2015; Mandák et al. 2016 for Chenopodium s.l.). Relationships between Dysphanieae Pax (plant aromatic, with stalked or subsessile glands), Atripliceae Duby (inc. Chenopodieae), Axyrideae and Anserineae (inc. Spinacieae) are unclear, although the tribes seem to be monophyletic (Fuentes-Bazan et al. 2012b for a summary). For Atripliceae, see also Zacharias and Baldwin (2010: North American taxa). Salicornioideae: see G. Kadereit et al. (2006), for relationships in the Australian Tecticornia and its relatives, see Shepherd et al. (2004, 2005a) and for the relationships between the paraphyletic Sarcocornia and Salicornia, see Steffen et al. (2015). For a general phylogeny of the subfamily, see Piirainen et al. (2017). Salsoloideae: Wen et al. (2010) found that Salsoleae s.l. were monophyletic, Akhani et al. (2007) looked at relationships in Old World Salsoleae and Salsoloideae in general. Suaedoideae: See Schütze et al. (2003) for relationships.
Classification. For the classification of Chenopodiaceae, see Hernández-Ledesma et al. (2015) and Zhu and Sanderson (2017), for that of Suaedoideae, see Schütze et al. (2003), of Salsoloideae, see Akhani et al. (2007), of Chenopodioideae, see Fuentes-Bazan et al. (2012b), of Camphorosmoideae, Kadereit and Freitag (2011), and for that of Salicornioideae, see Piirainen et al. (2017 - a new genus still to be described). Thus in the last two subfamilies, for example, there is much variation in fruit and seed, the former in particular involving apparent adaptations for dispersal, and genera based on this variation are not holding up, even though some have only recently been described (Shepherd & Wilson 2007, c.f. Wilson 1980; Kadereit & Freitag 2011).
Cabrera et al. (2009) found generic problems in the Australian Camphorosmeae, Maireana being in a particular mess (see also Kadereit & Freitag 2011). Zacharias and Baldwin (2010) divided the C3 North American Atriplex and relatives, which are quite variable, into a number of genera, while Fuentes-Bazan et al. (2012b) made the needed nomenclatural changes for the dismemberment of Chenopodium s.l. into seven genera (see also Kadereit et al. 2016) although the limits of Chenopodium in Australia have been expanded (Mosyakin & Iamonico 2017).
Within Gomphrenoideae, Iresine should be circumscribed broadly and Gomphrena is polyphyletic (Sánchez-del Pino 2007; Sánchez-del Pino et al. 2009). Some of the extreme halophytic genera are morphologically much modified, and generic limits are difficult. However, a comprehensive classification of Amaranthaceae s.l. - assuming the family stays in its broad circumscription - is badly needed.
Synonymy: Achyranthaceae Rafinesque, Celosiaceae Martynov, Deeringiaceae J. Agardh, Gomphrenaceae Rafinesque, Sabulinaceae Döll [?here], Sarcocaceae Adanson [?status]
[Stegnospermataceae [Limeaceae [[Lophiocarpaceae [Kewaceae [Barbeuiaceae [Aizoaceae [Gisekiaceae [[Sarcobataceae + Phytolaccaceae] [Petiveriaceae + Nyctaginaceae]]]]]]] [Molluginaceae [Montiaceae [[Halophytaceae [Didiereaceae + Basellaceae]] [Talinaceae [Anacampserotaceae [Portulacaceae + Cactaceae]]]]]]]]]: ?
Age. The age of this node may be around 86.8 m.y. (Magallón et al. 2015) or 60.2 m.y. (Tank et al. 2015: Table S2).
STEGNOSPERMATACEAE Nakai Back to Caryophyllales
Woody, ± scandent; ?betalains; successive cambia +; true tracheids +; plant glabrous; leaves fleshy; inflorescence racemose; "C" (2-)5; A (5) 8-10, connate basally; nectaries in depressions at base of G; G [2-5], alternate with P, placentation becoming free-central, stigma/styles ± spreading; ovule 1/carpel, basal, epitropous, amphitropous, obturator +; fruit a capsule; seeds arillate; exotesta ± palisade, unlignified, endotegmen enlarged, persistent; n = ?
1 [list]/3. Central America, the Antilles (map: from Bedell 1980). [Photo - Fruit]
Chemistry, Morphology, etc. Like Caryophyllaceae, there are special cells in the wood that contain sphaerites; there is only diffuse axial xylem parenchyma. There is no nucellar cap. Are the seeds endospermic?
For more information, see Hofmann (1977), Bedell (1980) and Rohwer (1993a), all general, Horak (1981) and Carlquist (2012c), secondary thickening, Friedrich (1956: c.f. carpel position), Narayana and Narayana (1986: embryology) and Sukhorukov et al. (2015: fruit and seed, sometimes 2 seeds/loculus).
Previous Relationships. Stegnospermataceae have often been included in Phytolaccaceae. The two look rather similar, and have a somewhat similar gynoecium, but they are most obviously distinguishable by their flowers which have petals. They also have pollen with a prominent foot layer and massive endexine - this is thin in Phytolaccaceae. The ovules are epitropous, while in pluricarpellate Phytolaccaceae they are apotropous (Rogers 1985).
[Limeaceae [[Lophiocarpaceae [Kewaceae [Barbeuiaceae [Aizoaceae [Gisekiaceae [[Sarcobataceae + Phytolaccaceae] [Petiveriaceae + Nyctaginaceae]]]]]]] [Molluginaceae [Montiaceae [[Halophytaceae [Didiereaceae + Basellaceae]] [Talinaceae [Anacampserotaceae [Portulacaceae + Cactaceae]]]]]]]]: ovules apotropous.
Age. This node is around 85 m.y.o. (Magallón et al. 2015) or 58.3 m.y. (Tank et al. 2015: Table S2).
LIMEACEAE Reveal Back to Caryophyllales
Herbs or subshrubs; anthocyanins +, betalains 0; cork?; (secondary thickening normal); sieve tube plastids with cubic crystalloida; nodes?; leaves spiral; inflorescence leaf-opposed or not; P quincuncial; "C" +, clawed (0), A 5(-7), basally connate; G , (abaxial member alone fertile), septate, styles 2; ovule 1/carpel, pendulous, obturator +; antipodal cells persist; fruit a schizocarp; seeds pale yellow/brown; exotesta with anticlinal walls strongly raised/laciniate [wax deposits]; n = 9.
1 [list]/21. Southern Africa (most species), to Ethiopia, S. Asia (map: from Culham 2007; esp. Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003, 6. 2011).
Chemistry, Morphology, etc. The "petals"/petaloid staminodes are described as coming from the base of the outer stamens (Ronse de Craene 2013). The nature of the gynoecium is unclear, but there are certainly two stigmas and sometimes (at least) clearly two styles that are very close together at the base (e.g. Jeffrey 1961).
For further information, see M. Endress and Bittrich (1993: general, as Molluginaceae), Behnke (1976) and Behnke et al. (1983a), both plastid morphology, Sharma (1963: floral morphology), Hofmann (1973: flower, growth), and Hassan et al. (2005a: seed).
Previous Relationships. Limeum is another member of the old Molluginaceae (M. Endress & Bittrich 1993).
[[Lophiocarpaceae [Kewaceae [Barbeuiaceae [Aizoaceae [Gisekiaceae [[Sarcobataceae + Phytolaccaceae] [Petiveriaceae + Nyctaginaceae]]]]]]] [Molluginaceae [Montiaceae [[Halophytaceae [Didiereaceae + Basellaceae]] [Talinaceae [Anacampserotaceae [Portulacaceae + Cactaceae]]]]]]]: (wide-band tracheids +); sieve tube plastids with globular crystalloids.
Age. This node is variously estimated at 40-30 m.y. (Wikström et al. 2001), (74-)61, 58(-47) m.y. (Bell et al. 2010: note position of Mollugo), 55-53 m.y. (Arakaki et al. 2011), and 83 m.y. (Magallón et al. 2015).
Evolution: Divergence & Distribution. There may have been an increase in diversification at this node (S. A. Smith et al. 2017).
Physiology & Ecology. Wide-band tracheid pith cells are scattered in succulent members of this clade, e.g. Aizoaceae, Cactaceae, and Portulacaceae. They are also found in the leaf away from the midrib in Aizoaceae; bands are narrow but very tall (= "wide"), so the cell lumen is locally very narrow (Mauseth et al. 1995: similar in Hectorella [Montiaceae]; Carlquist 1998b). In a recent study of Ariocarpus fissuratus (Cactaceae), it was found that as the rays expanded these tracheids could contract, so allowing the whole root to contract, and the plant remained closer to the rocky ground where the temperatures were cooler (Garrett et al. 2010).
Chemistry, Morphology, etc. Limeaceae, Cactaceae and "Portulacaceae" have cells in rows along the dorsal junction of the seed.
[Lophiocarpaceae [Kewaceae [Barbeuiaceae [Aizoaceae [Gisekiaceae [[Sarcobataceae + Phytolaccaceae] [Petiveriaceae + Nyctaginaceae]]]]]]]: ?
Age. This node is about 79.6 m.y.o. (Magallón et al. 2015).
Phylogeny. Corbichonia (Lophiocarpaceae) and most of Hypertelis (the type species is in Molluginaceae) were well supported as successive sister clades at the base of this clade (Christin et al. 2011a). However, the whole clade still needs study to confirm relationships along its backbone.
LOPHIOCARPACEAE Doweld & Reveal Back to Caryophyllales
?Betalains; lamina not bifacial; K/P quincuncial; pollen trinucleate; obturator of hairs.
2 [list]/6. Africa to western India (map: approximate, from floras and florulas; Jeffrey 1961; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003).
1. Lophiocarpus Turczanowicz
Lamina ± terete; inflorescence indeterminate, with 3-flowered cymules; flowers sessile; C 0; A 4; tapetal cells 4-5-nucleate [2-nucleate by fusion]; G , oblique, 1-locular, stigmas very strongly bilobed; ovule single [from abaxial carpel], basal, obturator funicular; fruit an achene, surface verrucose to ribbed; exotestal cells much elongated radially; n = ?
1/4. Southern Africa.
2. Corbichonia Scopoli
Inflorescence a leaf-opposed cyme [terminal inflorescence evicted]; "C" staminodial, many, ± connate; A many, centrifugal; tapetal cells 2-3-nucleate; G , opposite P, placentation axile; ovules many/carpel, obturator placental; fruit a loculicidal capsule, surface smooth; seeds arillate; exotestal cells papillate, pores on anticlinal walls; n = 9.
1/2. Africa to tropical Asia.
Synonymy: Corbichoniaceae Thulin
Chemistry, Morphology, etc. The gynoecium of Corbichonia has 8 vascular bundles in its walls, with four that are diagonal to the carpels are notably larger than the others (Eckardt 1974). Its exotestal cells are described as being strongly elongated radially (Hakki 2013), which does not seem to be obviously consistent with the image in Sukhorukov et al. (2015: see fig. 8B), where they are described as being "alveolate", compared to "sinus-like, triangular in cross-sections" for Corbichonia, and other differences between the two such as orientation of stalactites in the exotestal cells are mentioned.
For general information, see Adamson (1958), Hofmann (1973), Rohwer (1993a: Lophiocarpus) and M. Endress and Bittrich (1993: Corbichonia), for Corbichonia flowers, see also Ronse de Craene (2007), for embryology, see Narayana (1962a) and Narayana and Lodha (1963: as Orygia, ovules shown as almost anatropous), and seeds, see Hassan et al. (2005a).
Classification. Corbichoniaceae are not recognized, pending development of a consensus; two families for two genera seems a bit much, despite their differences (c.f. Thulin et al. 2016).
Previous Relationships. Previously included in Phytolaccaceae (Lophiocarpus: Rohwer 1993a) and Molluginaceae (Corbichonia: M. Endress & Bittrich 1993).
[Kewaceae [Barbeuiaceae [Aizoaceae [Gisekiaceae [[Sarcobataceae + Phytolaccaceae] [Petiveriaceae + Nyctaginaceae]]]]]]: "C" absent.
KEWACEAE Christenhusz Back to Caryophyllales
(Annual) herbs or subshrubs; anthocyanins +, betalains 0; cork?; secondary thickening?; (stout glandular hairs +); leaves ± fasciculate, linear, terete, stipules adnate to base, ± sheathing; inflorescence pseudo-umbellate, pedunculate; P 5, up to 3-4 becoming petal-like; A (3-)5-15(-20), developmental centrifugal; G [3-5], opposite sepals, placentation axile, style 0, stigmas crests; ovules many/carpel; fruit a membranous loculicidal capsule or schizocarp; seeds operculate; n = 8.
1 [list]/8. South Africa (most), to Ethiopia, Madagascar, and St Helena (map: from Adamson 1958a; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003, 6. 2011).
Chemistry, Morphology, etc. The inflorescence is interpreted as being terminal and cymose (Hoffmann 1973). In bud, the perianth members enclose the rest of the flower and are sepal-like; in the open flower three or four expand and are petal-like, and the anthers and stigmas are also brightly colored.
For further information, see M. Endress and Bittrich (1993: general, as Molluginaceae), Adamson (1958a: general, South African species), Behnke et al. (1983a: sieve tube plastids), and Ronse de Craene (2013: floral morphology). In these references, Kewa is very largely equivalent to Hypertelis, see Christenhusz et al. (2014).
Phylogeny. The exclusion of Hypertelis spergulacea, the type of the genus (see Molluginaceae), makes morphological sense.
Classification. For the classification of this little family, see Christenhusz et al. (2014).
Previous Relationships. Another member of the old Molluginaceae (M. Endress & Bittrich 1993).
[Barbeuiaceae [Aizoaceae [Gisekiaceae [[Sarcobataceae + Phytolaccaceae] [Petiveriaceae + Nyctaginaceae]]]]]: successive cambia +.
Age. This node is around 77.8 m.y.o. (Magallón et al. 2015) or ca 52/48.1 m.y. (Tank et al. 2015: Table S1, S2).
BARBEUIACEAE Nakai Back to Caryophyllales
Lianes; betalains?; libriform fibers, diffuse axial parenchyma, true tracheids +; sieve tube plastids with polygonal crystalloids; cortical fibres +; druses +; leaves spiral; infloresecence axillary, fasciculate; A many; pollen tricolporoidate; G , septate; ovule 1/carpel; fruit a loculicidal capsule; seeds 1 or 2, arillate; testa cells elongated, with sinuous anticlinal walls, ?tegmen bar thickenings; n = ?.
1[list]/1: Barbeuia madagascariensis. Madagascar (map: from Culham 2007).
Chemistry, Morphology, etc. The plant dries black. See Hofmann (1977: general), Rohwer (1993a: general, under Phytolaccaceae) and Carlquist and Schneider (2000: anatomy).
Previous Relationships. And this is a refugee from the old Phytolaccaceae (Cronquist 1981).
[Aizoaceae [Gisekiaceae [[Sarcobataceae + Phytolaccaceae] [Petiveriaceae + Nyctaginaceae]]]]: soluble oxalate accumulation; raphides +; anther wall from both secondary parietal layers.
Age. The crown age of this clade is estimated at (47-)38, 36(-27) m.y. (Bell et al. 2010) or about twice that, ca 74.9 m.y. (Magallón et al. 2015); ca 45.1 m.y. is the figure in Tank et al. (2015: Table S2).
Evolution. Ecology & Physiology. Christin et al. (2014b) noted that ppc-1E1 genes in some Aizoaceae and Nyctaginaceae C4 plants did not have a Ser780, as is usual in such cases.
Chemistry & Morphology. For soluble oxalate accumulation, see Zindler-Frank (1976); Hartmann (2017) suggested that Aizoaceae-Sesuvioideae and -Aizooideae both had druses, which if true, might confuse the optimization of this feature.
AIZOACEAE Martynov, nom. cons. Back to Caryophyllales
Leaf succulents; growth sympodial; C-glycosylflavonoids -; cork from inner cortex or endodermis; wood storied, wood rayless; fibres ± in bands; cuticular waxes as ribbons or rodlets; stomata also para- and anisocytic; leaf trace bundles forming reticulum in cortex; leaves opposite, lamina with bladder-like cells in epidermis [also elsewhere on plant], leaf base broad, margins membranous; inflorescence with well-developed bracts/bracteoles; hypanthium +; P coloured adaxially and basally, with subapical abaxial appendage [= "horn" - ?here]; nectary annular, on hypanthium; A many, centrifugal, primordia 5, wall 5 cells across; tapetal cells 2-nucleate; pollen tricolp(oroid)ate; G septate; ovules apical to median, parietal tissue 1-3 cells across, epidermal cells radially elongated; exotesta tanniniferous, ± palisade, or tangentially elongated, inner periclinal walls not/less thickened; (suspensor massive); x = 8.
Ca 124 [list: subfamilies assigned]/ca 1,180 (1,900) - four subfamilies below. Esp. southern Africa, also Australia, etc., tropical and subtropical, arid. [Photos - Collection.]
Age. Aizoaceae are (56.4-)41.5(-38.7) m.y.o. (Klak et al. 2016).
1. Sesuvioideae Lindley
(C4 photosynthesis common); (nodes 3:3); (lamina with peripheral vascular bundles, xylem external [exoscopic]); prophylls often prominent; petiolar stipules +; flowers with two small pairs of bracts; (A 1-5, alt. P), primordia opposite P, or development rather chaotic; G (1-)[2(-5]), 2-many ovules/carpel, (nucellar cap +); capsule circumscissile, (indehiscent, winged), (compound, fused with spiny bracts - Tribulocarpus); seeds arillate (not); (n = 7).
5/65: Trianthema (32), Sesuvium (14). Tropics and Subtropics; Sesuvium portulacastrum is pantropical on beaches (map: see Fl. Austral. 4. 1984; Hartmann 2001a, b; Hartmann et al. 2011; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; Fl. N. Am. 4: 2003). [Photos - Habit, Flower.]
Age. Crown-group Sesuvioideae are around (40.7-)29.6(-17.9) m.y.o. (Klak et al. 2016).
Synonymy: Sesuviaceae Horaninow
[Aizooideae [Acrosanthoideae [Mesembryanthemoideae + Ruschioideae]]]: CAM photosynthesis common; (leaves spiral); inflorescence often not distinct from vegetative plant, bracteoles foliaceous; A primordia alternating with P; G opposite P; fruit loculicidal, a hygrochastic capsule, with expanding keel; seeds brown.
Age.This clade is (43.6-)35(-26.1) m.y.o. (Klak et al. 2016).
2. Aizooideae Arnott
Annual to perennial herbs or shrubs; leaves with mesomorphic epidermis [outer periclinal walls little thickened; no thickened cuticle; stomata not sunk]; accessory lateral branches + [?]; P horn?; A (5, 10); nectary apically on the hypanthium; G [2-10], to inferior; ovule 1/carpel, apical, apotropous, or many, (nucellar cap +), funicular obturator +, of glandular hairs; fruit (septicidal - Gunniopsis), (expanding keel 0), (nut-like - Tetragonia), (drupe); (cell walls of seed coat little thickened), (endotegmen palisade - Tetragonia).
5/116: Tetragonia (51), Aizoon (45). Drier parts of S. Africa, also Australia (Gunniopsis), few N. Africa and Asia Minor, N. America, etc. (Aizoon) (map: see Frankenberg & Klaus 1980; Fl. Austral. 4. 1984; Hartmann 2001a, b; also Klak et al. 2015, c.f. Klak et al. 2017 - to the Caspian Sea, not in China). [Photo - Flower.]
Age. This node is estimated to be (15.8-)9.5, 7.9(-3.0) m.y.o. (Valente et al. 2014) or (43.6-)35(-26.1) m.y.o. (Klak et al. 2016).
Synonymy: Galeniaceae Rafinesque, Tetragoniaceae Lindley
[Acrosanthoideae [Mesembryanthemoideae + Ruschioideae]]: lamina trigonous or terete, base expanded, connate, forming a sheath.
Age. This node is (45.4-)36.4(-23.8) m.y.o. (Klak et al. 2016).
3. Acrosanthoideae Klak
Shrublets; ?anatomy; A 8-many, in groups; ?nectary; G , ovary incompletely septate; ovules 1-2/carpel, basal, funicle short; capsule with parchment-like walls, expanding keel 0, ?dehiscence how; seeds black to dark brown.
1/6. Fynbos, Western Cape, South Africa (map, see Klak et al. 2017).
Age. Crown-group Acrosanthes is (10.7-)5.3(-1.9) m.y.o. (Klak et al. 2016).
[Mesembryanthemoideae + Ruschioideae]: leaves very succulent, with peripheral vascular bundles, xylem internal [= endoscopic]; hypanthium 0; P green, sepal-like, horn 0; "C" = staminodia, many, linear; G more or less inferior, nectary interrupted; x = 9.
Age. This node has been dated to about 6.0 m.y.o. (Valente et al. 2014) or (37.2-)29(-19.4) m.y.o. (Klak et al. 2016).
4. Mesembryanthemoideae Ihlenfeldt, Schwantes & Straka
Distinctive alkaloids [in Phyllobolus, etc.] +; cortical bundles +; (stem succulents; succulent persistent green cortex in stem); leaves with mesomorphic epidermis, stomata on both stem and leaf transversely (vertically) oriented; leaves to cylindric; flowers 4-5-merous; (A and "C" basally connate); nectary hollow and ± shell-shaped [koilomorphic] (flat); G [(3-)4-5(-6)], placentation axile, stigma wet [Aptenia]; parietal tissue 7-9 cells across, in radial rows or not; expanding keels of fruit purely septal; (n = 18, 27).
1/105. S. Africa, esp. succulent Karoo, a few species also W. South America, Australia, N. Africa, the Mediterranean and the Near East, naturalised in W. North America (map: see Fl. Austral. 4. 1984; Pascale Chesselet, pers. comm. 2004; also Klak et al. 2015).
Synonymy: Mesembryaceae Dumortier, Mesembryanthaceae Philibert, nom. cons.
5. Ruschioideae Schwantes
Leaves flat; (inflorescence distinct); A from ring primordium; nectary flat, annular, broad; G [(3-)5-15(-25)], placentae basal or parietal; expanding keels of fruit largely valvar, not reaching centre of fruit, with covering membranes [= inner part of fruit wall].
111/1,585 - three groups below. Southern and eastern Africa, esp. Karoo, south Madagascar and southwest Arabia (map: Pascale Chesselet, pers. comm. 2004).
Age. Crown-group Ruschioideae are about 4.5 m.y.o. (Valente et al. 2014), perhaps a little more, 8.7-3.8 m.y. (Klak et al. 2004) - or (37.5-)33.0(-28.5) m.y. (Arakaki et al. 2011).
5A. Apatesieae Schwantes
Annuals to perennial; leaves with mesomorphic epidermis, bladder cells much reduced/0, (central chlorophyll-free water-storing tissue +); nectary a flat, broad nectariferous ring; style-stigma funnel-shaped to pointed; fruit schizocarpic, expanding tissue much reduced.
7/11[!]. South Africa, mostly southwest (see Klak et al. 2015).
Age. This node is about 6.0 m.y.o. (Valente et al. 2014) - or (21.6-)17.1(-12.6) m.y.o. (Arakaki et al. 2011). ?Right place.
[Dorotheantheae + The Rest]: ?
Age. This node is estimated to be (12.6-)7(-3.4) m.y.o. (Klak et al. 2016).
5B. Dorotheantheae Chesselet, G. F. Smith & A. E. van Wyk
Annuals; vascular anatomy anomalous; peripheral vascular bundles 0; leaves with mesomorphic epidermis; nectary segmented.
1/10. Southwest South Africa.
Age. Crown-group Dorotheantheae can be dated to (6.6-)3.9, 3.3(-1.1) m.y.a. (Valente et al. 2014).
5C. The Rest / Core Ruschioideae.
(Annuals); wide-band tracheids + (0); bladder cells 0; (lamina hemispherical) (connate) [plant stone-like], vernation curved to flat, (apex with teeth), base expanded, ± connate, central chlorophyll-free water-storing tissue +; filaments (basally connate), papillate or hairy at base; (pollen tri(syn)colpate); nectaries usu. crest-like [lophomorphic, bulging]; G [5-many]; embryo sacs often other than monosporic, 8-nucleate; (fruit persistent), (ordinary capsule = no closing bodies or covering membranes); (chloroplast PEP subunit β' rpoC1 intron lost), ARP gene duplicated.
Ca 96/ca 1,565: Ruschia (290-350), Conophytum (87-290), Lampranthus (180-220), Delosperma (140-165), Phyllobolus (150), Drosanthemum (100-110), Psilocaulon (65), Antimima (6-100), Lithops (37-50+), Cheiridopsis (38). Southern Africa, esp. the western coastal Succulent Karoo. [Photos - Flower; Flower.]
Age. This node is about (3.8-)2.0, 1.5(-0.35) m.y.o. (Valente et al. 2014).
Evolution: Divergence & Distribution. The "meganiche" dominated by the family in southern Africa - rather arid winter-rainfall areas with moderate temperatures - may be only some 5 m.y. old (Ihlenfeldt 1994a). Klak et al. (2004) suggested that the radiation in Ruschioideae in S.W. Africa, at least, was both recent (3.8-8.7 m.y.a.) and very fast, splash dispersal leading to relatively limited dispersal and facilitating geographical speciation (see also Ihlenfeldt 1994a). (Age estimates in Arakaki et al. (2011) are about twice as old, while those in Valente et al. (2014) are somewhat younger - and after the origin of the Greater Cape Floristic Region in which core Ruschioideae in particular are so common; see also ages in Klak et al. 2016, focus on Aizooideae.) Apatesieae and Dorotheantheae are successively sister to the remainder of Ruschioideae, they are not very speciose. Core Ruschioideae, which include over 1,500 species, often have crest-like (lophomorphic) nectaries and hygrochastic and sometimes long-persistent capsules with a distinctive anatomy (for which, see Kurzweil 2006) that release only a few seeds at a time (see above for other characters). Klak et al. (2013, 2015) discussed the phylogeny of Ruschieae, indeed, of the Aizoaceae as a whole, in the context of adaptations to different rainfall regimes - there is much diversity in winter-rainfall areas - and geography. Kellner et al. (2011) looked at genetic differentiation in Lithops in the context of morphology and geography.
Bittrich and Hartmann (1988) started the process of delimiting the famly and assigning apomorphies to the main groups. See also Klak et al. (2015, 2016) for some apomorphies.
Ecology & Physiology. Aizoaceae, in particular Mesembryanthemoideae and Ruschioideae, dominate much of the Succulent Karoo of southwestern Africa, making up more than 50% of the species and up to an astounding 90% of the biomass. Members of these groups may be either salt-tolerant (see articles in Ann. Bot. 115(3). 2015) or drought-avoiders, and such variation in quite closely related species is unusual (Ogburn & Edwards 2010). Edaphic specialization - soils can vary considerably locally - seems to be involved in the diversification of the family (Ellis & Weis 2006), and core Ruschioideae in particular flourish under such conditions (Valente et al. 2014). Although some work has been carried out on details of anatomy and cell micromorphology and possible links to ecophysiology (see Vegetative Variation below; Melo-de-Pinna et al. 2014), much more needs to be done. Large amounts of Na+ and Cl- are accumulated in the large epidermal bladder cells of Mesembryanthemum crystallinum that may have a volume of up to 5μl; although they are epidermal in origin, they have functional chloroplasts (Barkla et al. 2016; see Adams et al 1998 for a detailed account of the species; White et al. 2016 for Na accumulation even in non-saline conditions). Hartmann (1993) suggested that such hairs were involved in water storage, or they may be involved with water uptake from dew or mist (Ihlenfeldt & Hartmann 1982). Interestimgly, bladder cells are not found in the great majority of the succulent Ruschioideae (see Hartmann 1993 for possible evolutionary sequences here).
C4 photosynthesis occurs in some Sesuvioideae (Sage et al. 1999); some origins may be as much as (27-)22.1(-17.2) m.y.a., others are much younger (Christin et al. 2011b), and there appear to have been reversals from C4 to C3 photosynthesis here (Bohley et al. 2015). C3/CAM intermediates are also known, as in Mesembryanthemum crystallinum (Winter & Holtum 2014; see also Mioto et al. 2014), and CAM is common in the three other subfamilies (Bohley et al. 2015).
Pollination Biology & Seed Dispersal. Aizoaceae in the drier areas of southwestern Africa are much visited by bees, which also visit Asteraceae there (Kuhlmann & Eardley 2012) - the two do have grossly similar flowers.
Straka (1955), Ihlenfeldt (1983) and Hartmann (1988) have described the intricate morphology of the capsules of the [Aizooideae [Mesembryanthemoideae + Ruschioideae]] clade, which are often hydrochastic. There are septal keels that reach from the central axis to the valve tips that expand when they absorb water. Seed dispersal is by "jet action" using the kinetic energy of falling raindrops (= ombro[hydro]chory: Parolin 2006; see also Kurzweil 2006), and how far the seeds are dispersed depends on the details of the capsule morphology. The ease of ejection of the seeds is inversely correlated with the distance the seed travels - if easily ejected, the seeds are not propelled far, and in Ruschioideae only a few seeds at a time leave the capsule, but in general dispersal distances are low. In a few taxa mericarps are the units of dispersal. There is also considerable variation in the establishment "strategies" of the seeds. Many Sesuvioideae, with more conventional fruits, have arillate seeds and are myrmecochorous (Lengyel et al. 2009).
Vegetative Variation. Variation in features such as leaf size and shape and internode elongation is considerable (Ihlenfeldt 1994a). Although species with foliaceous bracts or bracteoles in which the inflorescence is not distinct from the rest of the plant are sometimes distinguished from those with smaller bracts and distinct inflorescences (e.g. Hartmann 1993), it is unclear to me what the real growth characters are and where they go on the tree. However, details of initial growth and subsquent inflorescence development along with the switch from C3 to CAM photosynthesis are fascinating (for Mesembryanthemum crystallinum, see Adams et al. 1998) and would repay synthesis (for swirches to/from CAM photosynthesis, see Bräutigam et al. 2017).
In addition to the taxa with bladder-like cells on the leaf surface (see above, "idioblasts"), other taxa have an epidermis with massively-thickened outer cell walls that contain layers of calcium oxalate crystals (e.g. Ihlenfeldt & Hartmann 1982; see also Hartmann 1993). In addition, individual cells may be variously papillate or the surface otherwise sculpted and/or with epicuticular waxes, the stomatal openings may be deeply sunken, etc. (e.g. Ihlenfeldt & Hartmann 1982; Hartmann 2002; Opel 2005a). This syndrome of characters may be compared with the mesomorphic epidermis found in some taxa, where the outer epidermis walls and cuticle are not thickened and the stomata are not sunk (e.g. Jürgens et al. 1986; Klak et al. 2015)
The leaves of many core Ruschioideae, i.e., not including Drosanthemeae and Ruschieae, are more or less flush with the surface of the ground; they can be almost invisible in the stony habitats in which they grow, being greyish or brownish and looking like pebbles except when they flower - hence "flowering stones". These leaves are prophylls or bracteoles, the flower is terminal, and renewal shoots, the next flowering units, develop in the axils of the prophylls (Hartmann 2004, 2006 for a summary). In some species of Conophytum the leaves are almost completely connate except for a slit across the top out of which the flower and next pair(s) of leaves appear.
The leaves of Mesembryathemoideae and core Ruschioideae are cylindrical or trigonous, not more or less flattened (Klak et al. 2004; Chesselet et al. 2004; Melo-de-Pinna et al. 2014), and there is a system of peripheral vascular bundle surrounding the more or less arcuate midrib (3D vascular tissue - see Ogburn & Edwards 2013); these vascular bundles have internal xylem, and it is as if the lamina had been abaxialized (Melo-de-Pinna et al. 2014). In core Ruschioideae the leaves lack the bladder-like epidermal cells of the rest of the family, although the epidermal cells may be papillate or with hairs (Powell et al. 2017: the two intergrade). The exposed surfaces of the leaves sometimes have distinctive "windows", and in Lithops this window patterning may reflect venation reticulation or the position of huge, tannin-containing, subepidermal cells (Korn 2011). A duplication of the ARP gene, involved elsewhere in leaf development, is correlated with the diversification of core Ruschioideae, and it may be involved in the evolution of the diverse leaf morphologies of this group, although there is currently no more than a simple correlation on which to go (Illing et al. 2011, c.f. the phylogenetic interpretation there).
Chemistry, Morphology, etc. Studies of the wood anatomy of Aizooideae and Sesuvioideae are needed to clarify wood evolution there, and to confirm the extent of rayless wood in the family (Carlquist 2007a); see Rajput and Patil (2008) for a study of vascular development in Sesuvium portulacastrum. Melo-de-Pinna et al. (2014) note a possible correlation between expanded, more or less connate leaf bases and a system of peripheral vascular bundles in the blade which have internal xylem.
The petal-like basal part of the perianth (= sepals) in Sesuvioideae is equivalent to the sheathing vegetative leaf base while the apical "horn" represents the rest of the leaf, rather as in monocot leaf development (c.f. Vorlaüferspitze!). B-class floral genes were expressed neither in the petaloid basal part nor in the petal-like staminodes of Aizooideae and Ruschioideae (Brockington et al. 2012; for the latter c.f. in part Frohlich et al. 2007). The androecium may arise as a ring meristem or as five separate primordia.
Smets (1986) recorded the presence of a receptacular nectary disc. Although Niesler and Hartmann (2007) suggested that the correlation of nectary morphology with major clades was not that strong, noting that the nectaries in Glottiphyllum (Ruschioideae) were more or less flat, they occur in (are restricted to? - see above) the two basal clades in that subfamily.
The nature of the inferior ovary may repay investigation. In Tetragonia, at least, flowers may develop in the axils of bracts on the outside of the ovary (Prakash 1967), rather like the situation in some Cactaceae. Hartmann (1993) recorded a nucellar cap in Aizoaceae, but by this she meant the radially elongated cells of the nucellar epidermis; Cocucci (1961) noted that the radially elongated epidermal cells of the ovule divide anticlinally; Prakash (1967) perhaps implies there is a nucellar cap in Tetragonia. Sesuvioideae often have arillate seeds, although Tribulocarpus has an indehiscent fruit and so hardly surprisingly it lacks arillate seeds. Fruit morphology and anatomy in Mesembryanthemoideae and Ruschioideae in particular is very complex (e.g. Ihlenfeldt & Gerbaulet 1990).
For general information, see Bittrich (1986: esp. Mesembryanthemoideae), Chesselet et al. (1995, 2002) and Frandsen (2017: photographs), esp. Mesembryanthemoideae and Ruschioideae), Hartmann (1993, 2001a, b, 2017: thousands of photographs, enumeration of taxa), Klak (2010), and Interactive Mesembs, also Cole and Cole (2005: Lithops); see also Hegnauer (1964, 1989: chemistry), Klak and Linder (1998) and Klak et al. (2006: esp. stomata), Jürgens (1986) and Ihlenfeldt and Gerbaulet (1990), all general anatomy, Landrum (2001: wide-band tracheids), Bhambie et al. (1977: nodal anatomy in Sesuvioideae - confirm), Opel (2005a: leaf anatomy of Conophytum), Niesler and Hartmann (2004: some leaf morphology), Hofmann (1973: morphology), Haas (1976: esp. flower and fruit), Leins and Erbar (1993: floral development), Hartmann and Niesler (2009: detailed survey of nectaries), Meunier (1890), Schmidt (1925), Raghavan and Srinivasan (1940b) and Kajale (1940c), all ovules and seeds, Schwantes (1957: esp. fruit dehiscence), Hassan et al. (2005a: seed morphology), and Dupont (1968: seedlings, also stomata).
Acrosanthes is especially poorly known.
Phylogeny. I follow Klak et al. (2003) for basic groupings in the family; Aizoaceae s. str. (e.g. Chesselet et al. 1995) would seem to be paraphyletic. Acrosanthes has been included in Aizooideae, however, Klak et al. (2016, 2017) found that it was sister to [Mesembryanthemoideae + Ruschioideae], and with quite good support.
Sesuvioideae. For a phylogeny of Sesuvioideae, see Hassan et al. (2005b). Tribulocarpus, which used to be in Tetragonioideae (for which, see Aizooideae), is sister to other Sesuvioideae (Klak et al. 2003; Thulin et al. 2012a); relationships are [Tribulocarpus [Trianthema + The Rest]] (Bohley et al. 2015). Sesuvium has separate African and American clades (Sukhorukov et al. 2018a). Tetragonia is embedded in Aizooideae (Klak et al. 2003), however, it has wood rays, it lacks the bands of xylem fibres of other Aizoaceae, and there is vasicentric parenchyma adjacent to these fibres (Carlquist 2007).
Ruschioideae. Within Ruschioideae, Apatesieae and Dorotheantheae are successively sister to the remainder (see above for morphology, etc.; Klak & Bruyns 2012 for a phylogeny of Dorotheantheae). The remainder, core Ruschioideae, have also lost the chloroplast PEP subunit β' rpoC1 intron (Thiede et al. 2007) - c.f. Cactoideae. There is a detailed phylogeny of Ruschieae in Klak et al. (2013), while Powell et al. (2016) also look at relationships in the clade. See Opel (2005b) for a morphological phylogenetic analysis of Conophytum, while Powell et al. (2017) looked at relationships around here and particularly at the circumscription of Cheiridopsis.
Classification. Many generic boundaries are uncertain. Thus in the early twentieth century Mesembryanthemum included the whole of the Ruschioideae and Mesembryanthemoideae, and until recently Mesembryanthemoideae s. str., much the smaller of the two subfamilies, was divided into several genera. However, Klak et al. (2007) in a comprehensive study of the subfamily, obtained quite detailed phylogenetic resolution within it. Mesembryanthemum s. str., although quite a small genus, was polyphyletic, and any attempt to maintain current genera would, Klak thought, have caused the recognition of numerous and often poorly characterised taxa; only one genus was recognised, as here (see also Hernández-Ledesma et al. 2015). Others think that clades there can be characterised (V. Bittrich, pers. comm.; Liede-Schumann & Hartmann 2009).
Klak et al. (2013) note that there are problems with generic limits in Ruschieae, and there are major problems with species limits, too. Hammer in 1993 observed that there were then about 1,800 known populations of Conophytum (Ruschioideae) - for which there were 450 names; current estimates of species numbers for this genus range from 87 to 290 (see also Hernández-Ledesma et al. 2015 for the extent of generic problems in Ruschioideae). There are also problems with generic limits in Aizooideae (Klak et al. 2016). For an infrageneric classification of Drosanthemum, see Hartmann (2007).
[Gisekiaceae [[Sarcobataceae + Phytolaccaceae] [Petiveriaceae + Nyctaginaceae]]]: ovule 1/carpel, basal, funicle short; K persistent to ± accrescent and filaments persistent in fruit; seeds not the dispersal units; ORF 2280 sequence similarity, 210 bp deletion in chloroplast genome.
Age. This node is estimated to be ca 73.7 m.y.o. (Magallón et al. 2015) or about 43.2 m.y.(Tank et al. 2015: Table S2).
Phylogeny. Relationships in this area are still somewhat unclear. Douglas and Manos (2007) found only moderate support for the monophyly of Nyctaginaceae and vanishing little support for the monophyly of Phytolaccaceae (including Sarcobataceae). Similar relationships were found by Brockington et al. (2009), but with Gisekia strongly supported as sister to the whole clade (see also Bissinger et al. 2014). Indeed, Gisekia has been thought to be "discordant" wherever it is put, and in some phylogenies it came out in or near Phytolaccaceae-Rivinioideae (see Cuénoud et al. 2002; Christin et al. 2011b), althouth this seems to be an unlikely position.
Douglas and Manos (2007) found the relationships [Nyctaginaceae [Sarcobataceae [Phytolaccaceae + Petiveriaceae]], Brockington et al. (2009) the relationships [Phytolaccaceae [Nyctaginaceae [Sarcobataceae + Petiveriaceae], although support was generally weak (see also Crawley & Hilu 2013). Ronse de Craene (2013) suggested that relationships in this area were [[Petiveriaceae + Nyctaginaceae] [Phytolaccaceae s. str. + Sarcobataceae]], and these relationships were also found by Y. Yang et al. (2015), although the position of Sarcobatus, which had a very long branch, was unclear. Some relationships in Sukhorukov et al. (2015) were poorly supported, but overall the topology was [Phytolaccaceae [Agdestidaceae + Sarcobataceae] [Nyctaginaceae [Seguieraceae, Galesia [Petiveriaceae + Rivinaceae]]]]. Y. Yang et al. (2017) found the relationships [Sarcobataceae [Phytolaccaceae [Petiveriaceae + Nyctaginaceae]]], although Gisekiaceae were not sampled.
Petiveriaceae and Nyctaginaceae both have gynoecia with just a single carpel (Cuénoud et al. 2002), and the carpels of Mirabilis and Rivinia do look remarkably similar to each other (Leins & Erbar 1994). If Sarcobataceae are placed somewhere around here their carpel number is a reversal. Indeed, Brockington et al. (2011) found some support for an [Agdestis + Sarcobatus] clade, in turn sister to Phytolaccaceae s. str., but with little support there.
GISEKIACEAE Nakai Back to Caryophyllales
Prostrate annual (short-lived perennial) herbs; ?betalains; successive cambia 0; C4 photosynthesis +; leaves opposite; inflorescence dichasial to subumbellate; P quincuncial; A 5 or 10-15, alternating with P; G (3-)5(-15), pseudapocarpous, opposite P, styluli +; ovule with parietal tissue 2-3 cells across, nucellar cap 2-3 cells across, cells of nucellus expanded radially, funicle short; antipodal cells ± persistent; plant heterocarpic [?always], mericarps smooth to ± muricate or winged, K ± accrescent; exotestal cells tangentially elongated, exotegmic cells also thickened; n = 9.
1 [list]/1-7. Africa, southerm Asia (map: from Frankenberg & Klaus 1980; Flora Ethiopia Eritrea 2(1). 2000; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003, 6. 2011; Flora of China 5; Bissinger et al. 2014).
Age. Crown Gisekiaceae are (8.4-)4.8(-1.2) m.y.o. (Christin et al. 2011b: c.f. outgroups) or (25.7-)14.9(-6.20 m.y.o. (Bissinger et al. 2014).
Evolution: Divergence & Distribution. The origin of Gisekia may be southern African (Bissinger et al. 2014).
Ecology & Physiology. Bissinger et al. (2014) provide details of C4 photosynthesis in the family; the pathway may not be fully optimized.
Chemistry, Morphology, etc. See Hofmann (1973) for floral morphology, growth, Behnke (1976) and Behnke et al. (1983a) for sieve tube plastids, Gilbert (1993) for a review, Joshi and Rao (1936) for embryology, the suspensor apically curved and beak-like, Narayana (1962a) and Hassan et al. (2005a) for seed morphology, and Narayana and Narayana (1988) for a little chemistry.
Phylogeny. For relationships in this clade as shown by a well sampled study with quite a lot of resolution, see Bissinger et al. (2014); species as currently recognised are not monophyletic.
[[Sarcobataceae + Phytolaccaceae] [Petiveriaceae + Nyctaginaceae]]: cork subepidermal; protein bodies in nuclei; fruit indehiscent; nuclear genome duplication [?Gisekia].
Age. The age of this clade is estimated to be 28-21 m.y. (Wikström et al. 2001: Delosperma included), ca 37.1 m.y. (Tank et al. 2015: Table S2) or about 71.4 m.y. (Magallón et al. 2015).
Phylogeny. See above.
Genes & Genomes. A gene duplication may have occurred at this node (Y. Yang et al. 2015, 2017; S. A. Smith et al. 2017). For the rate of molecular evolution and woody/herbaceous clade comparisons, see Yang et al. (2015); three of the four (within Nyctaginaceae, Phytolaccaceae and Petiveriaceae) showed increases associated with the adoption of the herbaceous habit, the fourth (Sarcobatus) did not.
Classification. Family limits in this area may need adjusting. However, if there is a [[Agdestis + Sarcobatus] Phytolaccaceae s. str.] clade (Brockington et al. 2011), one might as well include Sarcobataceae in Phytolaccaceae.
[Sarcobataceae + Phytolaccaceae]: inflorescence racemose.
Age. This node is about 70.3 m.y.o. (Magallón et al. 2015) or very much younger, ca 36 m.y. (Tank et al. 2015: Table S2).
SARCOBATACEAE Behnke Back to Caryophyllales
Shrub, with short shoots, thorns; much Na and K oxalate; cork etc.?; wood rayless; ?stomata; leaves fleshy, sessile; plant monoecious; bracteoles 0; P 0; staminate plant: inflorescence densely spicate; flowers with peltate scales ["bracts"]; A 1-4, anthers much longer than filaments; pollen pantoporate, pore margins raised; carpellate plant: flowers single; bracteoles connate, tubular, bilobed; G , [?position], style bilobed; funicle?; fruit an achene, winged; ?tegmen bar thickenings; perisperm 0/scarious, embryo flattened, spiral, green; n = 18, 36, 54, ?protein bodies in nuclei.
1 [list]/2. S.W. North America (map: from Fl. N. Am. vol. 4: 2003). [Photos - Collection.]
Evolution. Physiology & Ecology. Sarcobatus is an important component of the vegetation of saline areas in southwest North America; sodium and potassium oxalate concentrations can reach 20% dry weight.
Genes & Genomes. Despite its woody habit, Sarcobatus is on a notably long branch and has a high substitution rate (Y. Yang et al. 2015: protein-coding genes).
Chemistry, Morphology, etc. Some information is taken from Carlquist (2000a); for fruit, see Sukhorukov et al. (2015).
Previous Relationships. Sarcobatus used to be included in Chenopodiaceae, but sieve tube plastids with globular inclusions, etc., suggest that it goes somewhere around here (Behnke 1997).
Classification. Is Sarcobatus really worth placing in a separate family (c.f. Behnke 1997)?
PHYTOLACCACEAE R. Brown, nom. cons. Back to Caryophyllales
Cuticular waxes as platelets; lamina vernation conduplicate; (inflorescence with cymose clusters of flowers); pollen tricolpate; funicular hair-type obturator +; ?tegmen bar thickenings.
5 [list]/32 - two groups below. Tropical and warm temperate, esp. America. [Photos - Collection.]
1. Phytolaccoideae Arnott
Herbs, vines or soft-wooded trees; saponins +; fibers vasicentric; nodes 1:3; inflorescence a raceme, (cymes at the base - Phytolacca), (leaf-opposed); P (4-)5; A 5-30, development centrifugal; tapetal cells multi-nucleate; G [3-17], (opposite P), free to connate, often pseudapocarpous, styluli broadly separate to ± connate, stigmas punctate; ovules apotropous, (outer integument ca 5 cells across), nucellar epidermal cells palisade, parietal tissue ca 2 cells across, nucellar cap 3-14 cells across, hypostase +; fruit a berry; embryo white; n = 9, 18, etc.
4/31: Phytolacca (25). Chile, Mexico, few in Old World, also weedy (Phytolacca) (map: from Fl. N. Am. v. 4. 2003; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003).
Synonymy: Sarcocaceae Adanson
2. Agdestidoideae Nowicke
Liane; root massively swollen; diffuse axial parenchyma, true tracheids +; wood rayless; Ca oxalate crystals 0; cuticle waxes with ± rounded platelets; lamina venation palmate; inflorescence branches cymose; P 4 (5); A 12-30, in groups alternating with P; nectary +; G [(3-)4], semi-inferior, septate, style branches becoming broadly recurved; ?ovule; fruit 1-seeded, achene, P forming wings; n = ?
1/1: Agdestis clematidea. South U.S.A. to Nicaragua (map: from Fl. N. Am. v. 4. 2003; Culham 2007).
Synonymy: Agdestidaceae Nakai
Evolution: Divergence & Distribution. Fossil fruits from the Upper Cretaceous (late Campanian) of Mexico are similar to those of Phytolacca, Cevallos-Ferriz et al. (2008) noting a palisade exotesta and also a palisade layer in the tegmen.
Chemistry, Morphology, etc. Phytolacca is reported, probably incorrectly, to have glucosinolates (Fahey et al. 2001 for literature).
The carpels of Phytolacca are initiated as a ring around the apex of the axis (Zheng et al. 2004).
See also Rohwer (1993a: general), Hegnauer (1969, 1990: chemistry), Carlquist (2000b: anatomy), Balfour and Philipson (1962: nodes of Phytolacca), Meunier (1890: ovules and seeds), Mauritzon (1934c) and Kajale (1954), both embryology, Rohweder (1965: gynoecium), Nowicke (1969) and Bortenschlager (1973), pollen, Hofmann (1977, 1994), Leins and Erbar (1993), Zheng et al. (2010) and Ronse de Craene (2013), all floral morphology/development.
[Petiveriaceae + Nyctaginaceae]: stomata also paracytic; G 1, stigma expanded, capitate.
PETIVERIACEAE Meissner Back to Caryophyllales
Herbs to trees or lianas; saponins 0, (plant smelling of garlic); (secondary growth normal); (spines +, prophyllar); styloids, elongate crystals +; inflorescence raceme or spike, branched or not (flowers terminal - Seguieria); (bracteoles slightly abaxial); (flowers weakly monosymmetric); P 4, (diagonal), (5 - Seguieria); A alternate with P, -many, whorls centrifugal, (anthers extrorse - Hilleria), anthers H-shaped; pollen tricolpate, also 6-12 colpate or 7-many pantoporate; nectary 0; style ± 0, stigma penicillate, fimbriate and basal [?: Petiveria]; outer integument 3-4 cells across [thicker towards chalaza], inner integument ca 2 cells across, parietal tissue 2-18 cells across, nucellar cap 2-9 cells across, placental obturator +; fruit winged [wings = P], utricle, or drupe; exotestal cells radially elongated, lumen ± obscure to obvious; perisperm +/± 0, micropylar endosperm haustorium [Petiveria alliacea], suspensor massive, cotyledons (complexly folded), (convolute - Petiveria); n = 18, 54; seedling epigeal, phanerocotylar.
9 [list]/13. Southern U.S.A. to South America, the Antilles, Australia, New Hebrides and New Caledonia (Monococcus) (map: from Rohwer 1982; Fl. Austral. 4. 1984; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; Fl. N. Am. v. 4. 2003).
Chemistry, Morphology, etc. Petiveria and Gallesia smell of onions. Nowicke (1969) described some Petiveriaceae as having "stipular thorns" up to 5 cm long; these are probably prophyllar.
Both Monococcus and Petiveria have four perianth parts that are diagonally arranged but their bracteoles are strictly lateral, while the perianth of the other genera is orthogonally arranged and the bracteoles are slightly adaxial (e.g. Vanvinckenroye et al. 1997). I am unclear about the stigma morphology here. Ovules of Petiveria have a nucellar beak.
See also Rohwer (1982, 1993a: general), Hegnauer (1969, 1990: chemistry), Carlquist (2000b, c) and Jansen et al. (2000c), both wood anatomy, Mauritzon (1934c: embryology), Rocén (1927: endosperm, in discussion), Rohweder (1965: gynoecium), Nowicke (1969: general, also pollen), Bortenschlager (1973: pollen), Hofmann (1977), Ronse De Craene and Smets (1991d), and Leins and Erbar (1993), all floral morphology/development, and Sukhorukov et al. (2015: fruit and seed).
Classification. Petiveriaceae are recognised because it has turned out that Phytolaccaceae, in which they were included, are not monophyletic; for a discussion, see above.
Synonymy: Hilleriaceae Nakai, Rivinaceae C. Agardh, Seguieriaceae Nakai
NYCTAGINACEAE Jussieu, nom. cons. Back to Caryophyllales
Annual herbs to shrubs, often rather weak-stemmed trees, or lianes; (isoflavonoids +); (cork cortical); wood storied, often rayless; (vessel elements with reticulate perforations); leaf wax crystalloids 0; P connate, petal-like, lobes induplicate-valvate or contorted; tapetal cells multinucleate, (massive); (nectary on receptacle); style long, slender, stigma asymmetric, also fimbriate; ovule with outer integument ?4 cells across, inner integument ?2 cells across, parietal tissue 2-7 cells across, (nucellar cap 2 cells across); antipodal cells enlarged, >3; exotesta lacking stalactites; embryo sac haustorium +; fruit surrounded by P, achene or nutlet, pericarp usu. thin; ?tegmen bar thickenings; perisperm [in t.s.] two lobed or two-partite, embryo green; n = (8-)11(-13+).
31 [list]/405 - seven groups below. Tropical to warm temperate (map: see Stemmerik 1964; Fl. Austral. 4. 1984; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; Fl. N. Am. v. 4. 2003; Culham 2007). [Photo - Fruit, Collection.]
1. Caribeeae Douglas & Spellenberg
Perennial, with taproot; leaves opposite, connate by expanded bases, blade <3 mm long; flower single, terminal, with 3-6 "bracteoles"; P constricted above the ovary, apically suburceolate; A 2, exserted, basally adnate to P; stigma capitate; "fruit" smooth; ?testa; ?embryo; n = ?
1/1: Caribea litoralis. Cuba.
[Leucastereae [Boldoeae [Colignonieae, Nyctagineae [Bougainvilleeae + Pisonieae]]]: flowers in cymose clusters; A often connate at the very base.
2. Leucastereae Bentham & Hooker
Trees; styloids, etc.; indumentum ± stellate; A 2, 3 (10-20); style thick/0, stigma crest-like; (P accrescent in fruit - Ramisia); (pericarp well developed); exotestal cells large; embryo hooked; n = ?
4/5. S.E. South America, esp. Brasil.
[Boldoeae [Colignonieae, Nyctagineae, [Bougainvilleeae + Pisonieae]]]: ?
3. Boldoeae Heimerl
Bracteoles 0; A free; stigma inconspicuous (style 0, stigma fimbriate); exotesta with stalactites; perisperm entire; n = ?
3/3. Mexico to Bolivia, the West Indies.
[Colignonieae, Nyctagineae, [Bougainvilleeae + Pisonieae]]: (gypsophily); leaves opposite; (involucre +); P bipartite, tube stout, limb thin; A 1-many, of varying lengths; pollen pantoporate, also tricolpate, etc.; (ovule unitegmnic); basal part of P tube accrescent, often mucilaginous, rest withering; (cotyledons unequal).
4. Colignonieae Heimerl
P only basally connate; exotestal ells large; n = 16, 17.
1/6. Andean South America
[Nyctagineae [Bougainvilleeae + Pisonieae]] (if there is such a clade): pollen grains spherical, starch as reserve; stigmatic papillae multiseriate/multicellular; carpel with dorsal vascular bundle; seed coat thin, cells tangentially elongated.
5. Nyctagineae Horaninow
(Medullary vascular bundles +); (C4 photosynthesis +); pollen pantoporate; stigmatic transmitting tissue compact, enclosed by a ring of cells, in two tracts; (outer integument 5-7 cells thick - Mirabilis), obturator +; (endotesta thickened [Mirabilis]); embryo hooked; genome duplication; n = 13, 20, 21, 22, 26, 27...
11/194: Boerhavia (50), Mirabilis (55), Abronia (33). Tropical to warm temperate, esp. herbs and shrubs in arid southwestern North America.
Synonymy: Allioniaceae Horaninow, Mirabilidaceae W. Oliver
[Bougainvilleeae + Pisonieae]: pollen grains tricolpate; stigmatic transmitting tissue diffuse; outer integument 4-6 cells across, (integument single - 3-6 cells across), parietal tissue ca 4 cells across, obturator 0.
Age. The crown age of a clade including Bougainvillea and Mirabilis is estimated at 19-13 m.y.a. (Wikström et al. 2001) or (32-)23, 22(-13) m.y. (Bell et al. 2010).
6. Bougainvilleeae Choisy
(Lianes, climbing by branch hooks); nodes 1:3; leaves spiral; pollen reserve lipids; style lateral; carpel also with median lateral vascular bundles; ovule sub-basal [Bougainvillea]; (pericarp well developed); n = 10, 17.
3/16: Bougainvillea (14-18). Central and tropical South America; southwest Africa.
Age. Bougainvillea-type pollen is reported from late Campanian deposits ca 70 m.y.o. in Sakhalin (Manchester et al. 2015 for references).
Synonymy: Bougainvilleaceae J. Agardh
7. Pisonieae Meisner
Plant ectomycorrhizal; pollen grains prolate, (pantocolpate); (testa multiplicative, unstructured [Pisonia]); embryo straight, cotyledons unequal; n = 68 [two counts].
7/200: Neea (85), Guapira (70), Pisonia (40). Pantropical, but especially New World.
Synonymy: Pisoniaceae J. Agardh
Evolution. Ecology & Physiology. A xerophytic clade in S.W. North America is noted for its abundance in dry or desert conditions, diversification beginning in the Oligocene or Miocene. A number of species also tolerate gypsum-rich soils (Escudero et al. 2014; for Abronia, see Saunders & Sipes 2011), gypsum tolerance having evolved perhaps four times in the (Pliocene and) Pleistocene (Drummond et al. 2012). See also S. A. Smith et al. (2017) for a genome duplication here (in the ancestor of Nyctagineae), its effect on diversification, and its association with a shift of the plants to drier, cooler conditions.
The origin of C4 photosynthesis in Boerhavia and Allionia has been dated to within the last 7 m.y. (Christin et al. 2011b).
Pollination Biology & Seed Dispersal. The single-flowered inflorescences of some species of Mirabilis can look remarkably like individual flowers: The green inflorescence bracts appear to be a calyx, and the brightly-coloured connate perianth looks like a sympetalous corolla. Taxa that flower in the evening or night (hence the name, the "four o'clock family") are quite common (Douglas & Manos 2007); Nores et al. (2013) summarize pollination biology in the family.
The subepidermal cells of the perianth may produce mucilage when the fruit is wetted, and this is especially notable in disseminules of the xerophytic North American clade. In species like Pisonia the pericarp becomes viscid and very sticky indeed; it is used as bird lime to catch birds (Western 2012).
Plant-Animal Interactions. Leaf mining or webbing caterpillars of the yponomeutoid moth Heliodinidae are notably common here (Sohn et al. 2013).
Bacterial/Fungal Associations. Pisonieae like Neea, Guapira and Pisonia are recorded to form ectomycorrhizal associations with various basidiomycetes perhaps especially Thelephoraceae; in forests, individual ECM plants are often quite dispersed in the vegetation and only a single species of fungus may be involved in the association. Furthermore, ectomycorrrhizae are imperfectly developed in species that have only long roots, not long + short, root hairs may be present, and in Pisonia the epidermal cells have what appear to be multicellular protrusions (Haug et al. 2005; Tedersoo et al. 2010a). The specificity of the association between fungus and plant is quite high (Tedersoo et al. 2010a). In some Pisonia, at least, although a fungal sheath is formed, there is no Hartig net, but the outer and radial walls of the plant epidermal cells develop transfer cell morphology (Cairney et al. 1994: see also Brundrett 2017a; Tedersoo 2017b; Tedersoo & Brundrett 2017 for literature, dates, etc.).
Genes & Genomes. For a gene duplication in Nyctagineae, see Y. Yang et al. (2015).
Chemistry, Morphology, etc. Primary stem anatomy can be complex in those species with medullary vascular bundles (e.g. Pant & Mehra 1963); I am not totally clear what is going on at the nodes, but secondary thickening may also be involved. Carlquist (2004) examined secondary thickening in Nyctaginaceae in detail: There is a lateral meristem that produces secondary cortex to the outside, and to the inside rays, conjunctive tissue, and a succession of vascular cambia, from which the more or less isolated areas of vascular tissue (but not rays) are derived. Hernández-Ledesma et al. (2011) looked at anatomical variation within Mirabilis in some detail.
Some Nyctagineae have pollen grains ca 200 µm long, about the largest in angiosperms outside the aquatic Cymodoceaceae (Alismatales). For nectaries in the family, see Nores et al. (2013). The single ovule seems to terminate the apex of the floral axis (Sattler & Perlin 1982). Abronia has only a single well-developed cotyledon. Cytologically Nyctaginaceae are poorly known.
See Bittrich and Kühn (1993) for general information, Hegnauer (1968, 1990) for chemistry, Vanvinckenroye et al. (1993) for floral development, Nores et al. (2015) for information about pollen and gynoecium, Rocén (1927) and Woodcock (1929) for ovules, and Sukhorukov et al. (2015: fruit and seed).
Phylogeny. The South American Leucastereae and Mexican-Central American Boldoeae are successively sister taxa to the remainder of the family, positions that have moderate to strong support. Within the remainder of the family a North American xerophytic clade has very strong support. Here Bougainvilleeae and Pisonieae (with minor additions) form a clade, while Abronieae are embedded in a highly paraphyletic Nyctagineae plus Boerhavieae complex, all three included in Nyctagineae above (Douglas & Manos 2007; see also Levin 2000 for a more limited study; Y. Yang et al. 2017).
Classification. For the tribal classification, see Douglas and Spellenberg (2010); they also recognised a monotypic Caribeeae, but this was unplaced in the phylogeny.
[Molluginaceae [Montiaceae [[Halophytaceae [Didiereaceae + Basellaceae]] [Talinaceae [Anacampserotaceae [Portulacaceae + Cactaceae]]]]]] / portullugo clade: fruit a loculicidal capsule [?level].
Age. This node is estimated to be 35-24 m.y.o. (Wikström et al. 2001), about 50.2 m.y. (Tank et al. 2015: Table S2), ca 51.9 (± 4.7) or 56.1 (± 5.8) m.y. (Christin et al. 2011a), (55.4-)53.3(-51.2) m.y. (Arakaki et al. 2011), or as much as around 73.1 m.y. (Magallón et al. 2015).
Evolution. Ecology & Physiology. Edwards and Ogburn (2012) discuss the evolution of CAM and C4 photosynthetic syndromes in this clade.
Ecology & Physiology. Ocampo and Columbus (2010) discuss the evolution of different photosynthetic pathways in this clade, which they reconstruct as being plesiomorphically C3. For CAM in the old Portulacaceae s.l., now scattered through this clade, see Guralnick and Jackson (2001) and especially Ocampo and Columbus (2010). CAM cycling is common; this occurs when plants do not completely shut their stomata during the day, and carbon is fixed at night from respiratory, not atmospheric, CO2.
Nyffeler and Eggli (2010b) offer estimates of the numbers of succulent species in the various families. Taxa with fleshy roots are scattered throughout the clade, being found in all families (except the monotypic Halophytaceae) as well as in all subfamilies of Cactaceae (e.g. Nyffeler et al. 2008).
Genes & Genomes. For a genome duplication here, see S. A. Smith et al. (2017) and Y. Yang et al. (2017); the sister clade (Molluginaceae) is hardly very diverse.
Chemistry, Morphology, etc. Variation within this clade is complex (see also Nyffeler 2007, especially Ogburn 2007; Nyffeler et al. 2008; Ogburn & Edwards 2009; Nyffeler & Eggli 2010b; Ocampo & Columbus 2010). Most taxa have mucilage cells, but there may be interesting variation within the group as to exactly where such cells occur in the plant (Ogburn & Edwards 2009). For the distribution of peripheral vascular bundles in the leaf, i.e., the leaf venation is three dimensional, see Ogburn and Edwards (2013).
Interpretation of the parts surrounding the flowers is complicated by how they have been described. Often there are paired structures - often more than a single pair - borne immediately below the flower and more or less completely surrounding it. Called bracteoles here, they have also often been called sepals. The inner/upper pair of bracteoles is in the median plane (e.g. Eichler 1878), as is the sole pair of bracteoles in Montia (Ronse de Craene 2010) and Halophyton (Pozner & Cocucci 2006), although they do not comment on the orientation. The transverse outer bracteoles may have flowers in their axils, the inner median bracteoles always lack them. In at least some species of Anacampseros the inner bracteoles are in the same plane as the bud-subtending bracteoles (Vanvinckenroye & Smets 1999), in species of Portulaca such as P. oligosperma there are two quite large bracteoles immediately underneath the flower and then four smaller bracteoles - ?= perianth - in a whorl separated from the first pair by a short internode (Geesink 1969), while in Lewisia there are lateral bracteoles and inner median bracteoles forming the involucel (Dos Santos & Ronse De Craene 2016). The whorl inside the bracteoles, usually 4- or 5-parted - called a perianth here - is like that of other core Caryophyllales. Its members are often more or less brightly coloured and have been described as petals or petal-like. In Claytonia their development is much retarded relative to that of the androecium, and a theory is that the perianth proper has been lost and the apparent perianth is a modified part of the androecium (Dos Santos et al. 2012). The lateral members of the perianth in Montia develop first, and the median members, sometimes as many as 11, develop after the androecium (Dos Santos et al. 2016).
Portulaca has an androecial ring primordium, as in some Cactaceae and in species of Anacampseros, sometimes also with centrifugal initiation of stamens; other species have fewer stamens, which may be initiated in pairs (facing each other!) opposite the perianth members, or as single stamens alternating with them (Vanvinckenroye & Smets 1999). When there is the same number of stamens as perianth members, their position relative to the carpels varies. Nowicke (1996) summarized a number of pollen characters that are shared in the group (her Portulacinae), although they might also occur outside it: Columellae either narrowed towards the middle or expanded towards the base, sometimes fused; pollen with granular internal surfaces; perforated foot layer; non-apertural endexine "thread-like" - the latter term unclear from the descriptions provided.
For chemistry, see Hegnauer (1969, 1990), for anatomical information about the old Portulacaceae, see Becker (1895), for pollen, see Nilsson (1967), for general information, see Carolin (1987 [also a phylogenetic analysis], 1993). For information on the vegetative plant, see Nyffeler et al. (2008).
Phylogeny. Relationships between members of this clade were for some time rather uncertain, but it was also clear that they were not reflected by the then-current classifications. Hershkovitz and Zimmer (1997) realized that if Cactaceae were recognised, Portulacaceae would be paraphyletic (see also Appelquist & Wallace 1999, 2001). Later they found little major phylogenetic structure in a study of American Portulacaceae (Hershkovitz & Zimmer 2000: ribosomal DNA, Cactaceae not included). Hershkovitz (2006) found the same general pattern as he focused on W. American "Portulacaceae" from the Andean region - there were perhaps half a dozen clades in that region, but no major groupings beyond that. Cactaceae, Didiereaceae and Portulacaceae remained a closely entwined complex (Appelquist & Wallace 2000), indeed, they can all be intergrafted (Anderson 1997). See also Cuénoud et al. (2002) for relationships in this area, e.g. of Halophytum. Many of the relationships found by Ocampo and Columbus (2010) were poorly supported, and Halophytaceae wandered around the tree.
A number of studies since 2007 have clarified relationships around here. Cactaceae + Talinum + Portulaca + Anacampseros, etc., were found to make up a major and rather well supported clade (Hershkovitz & Zimmer 1997; Appelquist & Wallace 2001). Nyffeler (2007: three genes, two compartments) found some support for a topology [Talinum and relatives [Portulaca [Anacampseros and relatives + Cactaceae]]], although the topology was different when the mitochondrial nad1 data were analyzed alone. Support for the [Anacampseros and relatives + Cactaceae] clade was appreciable in the combined analysis (78% bootstrap), where the chloroplast signal predominated.
Details of relationships immediately around Cactaceae remain unstable. Brockington et al. (2009; large amounts of data, rather skimpy sampling) found a clade [Portulacaceae + Talinaceae] with 98% boostrap support, and Claytonia (Montiaceae) was sister to the whole clade, which included Halophytaceae. Nyffeler and Eggli (2010a) found few resolved relationships except in the Talinaceae-Cactaceae area, and support for the monophyly of Didieraceae and Montiaceae was not strong; and Butterworth and Edwards (2008) found the relationships [Anacampserotaceae [Talinacaeae [Portulacaceae + Cactaceae (weak support)]]], although there was no outgroup, so Anacampserotaceae appeared to be paraphyletic. Portulaca and Pereskia (but not Claytonia) share a 500 bp chloroplast DNA deletion in the rbcL gene (Wallace & Gibson 2002 for details and references), a potentially informative molecular marker. Crawley and Hilu (2013) recovered the clade [Portulacaceae [Anacampserotaceae + Cactaceae]], as did Hernández-Hernández et al. (2014). Y. Yang et al. (2017) found that Portulacaceae and Anacampserotaceae were sister taxa. Ogburn and Edwards (2015) recovered a [Portulacaceae + Anacampserotaceae] clade, and this was also recovered - although not always - by Moore et al. (2018) using a targeted enrichment approach, which should be consulted for a discussion on the conflicting signals found here and elsewhere in this clade.
Using the nuclear PHYC and chloroplast trnK/matK genes and ca 250 species of this clade, Arakaki et al. (2011) confirmed with strong support the position of Molluginaceae as the sister taxon to Portulacinae (see also Soltis et al. 2011: support only moderate; Ogburn & Edwards 2015). There was strong support for relationships along the spine of this clade, but "only" 78% likelihood bootstrap support for the [Anacampserotaceae [Portulacaceae + Cactaceae]] clade, although that also has some morphological support. Support for the monophyly of all families is strong. The only exception is the [Halophytaceae [Didiereaceae + Basellaceae]] clade; Didiereaceae are not monophyletic, Basellaceae being sister to the Portulacaria group, and Halophytaceae are only weakly associated with the other two families (Arakaki et al. 2011). Soltis et al. (2011) found only weak support for the [Didiereaceae + Basellaceae] clade, but Anton et al. (2013) found some support for a [Didiereaceae [Halophytaceae + Basellaceae]] clade. There was weak support for a [Halophytaceae + Basellaceae] clade but stronger support for a [Didiereaceae [Talinaceae + the rest]] clade (Moore et al. 2018).
Classification. Basellaceae and Didiereaceae are kept separate; there are a few African genera that used to be included in Portulacaceae in the latter, so making them less distinct, although morphology is largely consistent with their new position. Portulacaceae s.l. are strongly paraphyletic, their erstwhile members being placed in Portulacaceae s. str. (now a small group), Talinaceae, Anacampserotaceae and Montiaceae below. The morphologically rather distinctive and Antipodean Hectorellaceae are included in Montiaceae.
MOLLUGINACEAE Bartling, nom. cons. Back to Caryophyllales
Barely succulent (annual) herbs (shrubs), growth sympodial, modules with definite numbers of leaves; hopane saponins, C-glycosylflavonoids, (anthocyanins +, betalains 0); wood rayless; (C4 photosynthesis +); cork?; (secondary growth normal); (sieve tube plastids with starch grains); pericyclic fibres +; (raphides +); (also rhomboidal crystals +); plant glabrous (hairs glandular or stellate); cuticle waxes as platelets or rodlets; stomata anomocytic; prophylls prominent; leaves often pseudoverticillate, opposite or spiral, stipules membranaceous (0); P quincuncial, ("C" bifid to laciniate, -20 [Glinus]); A (2-)5-10(-30), alternate with P, (centrifugal), (filaments ± connate basally); (pollen pantoporate); G (1) [2-5(more)], opposite sepals/perianth or the median member adaxial, placentation axile, style single, or styles ± separate, stigmas linear (capitate); ovules 1[basal]-many/carpel, parietal tissue 1(-2) cells across, epidermal cells radially elongated, nucellar cap to 2 cells across, obturator +, funicles short to long; fruit (dehiscing by transverse slits), (nutlet); seeds arillate or not, (operculate); exotestal cells undistinguished in shape, (outer periclinal walls perforated - Glinus); n = 9.
11 [list]/87: Mollugo (35), Pharnaceum (25). Tropical, especially southern Africa, to warm temperate, some weedy (map: from Frankenberg & Klaus 1980; Jalas & Suominen 1980; Fl. N. Am. 4: 2003; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003, 6. 2011; Australia's Virtual Herbarium vii.2013 - incomplete, and South America rather notional). [Photos - Habit & Flower]
Age. The age of crown group Molluginaceae is estimated at ca 46.7 (± 4.8) or 50.3 (± 5.8) m.y. (Christin et al. 2011a).
Evolution: Divergence & Distribution. The rate of diversification of the Adenogramma-Pharnaceum clade is notably less than many others in this general area of Caryophyllales (Arakaki et al. 2011).
Ecology & Physiology. C4 photosynthesis probably arose more than once here (Christin et al. 2010b, 2011, q.v. for dates). There are also a few C3/C4 intermediates with C2 photosynthesis in Mollugo, and species such as Mollugo verticillata that photosynthesize like this may be some 10-20 m.y. old (Christin et al. 2011a). Adoption of the new photosynthetic pathway is accompanied by an increase of tolerance of drier conditions (Christin & Osborne 2014).
Chemistry, Morphology, etc. For pigments, see Thulin et al. (2016). The apparent anomalous occurrence of vascular rays in genera like Macarthuria (M. Endress & Bittrich 1993) is less anomalous when these genera are removed from the family; there has been a similar clarification of apparent variation in sieve tube plastid type. Para- dia- and anisocytic stomata are all recorded; stomatal type should be checked against the new circumscription of the family. The stipule-like structures need examination.
The androecium may be fasciculate; Adamson (1958a) noted that the 20-30 stamens of Hypertelis spergulacea, which belongs here (the rest of the genus is in Kewaceae), are in groups.
Some information is taken from Adamson (1960), Bogle (1970), M. Endress and Bittrich (1993) and Thulin et al. (2013), all general, Richardson (1981: flavonoids, but c.f. Behnke et al. 1983b), Vincken et al. (2007: saponins), Hegnauer (1964, 1989, as Aizoaceae: chemistry), Behnke (1976) and Behnke et al. (1983a), both sieve tube plastids, Payne (1933, 1935: Mollugo), Sharma (1963: floral morphology, includes segregates), Hofmann (1973: flower, growth), and Raghavan and Srinivasan (1940), Narayana and Lodha (1972), Bhargava (1934), Narayana (1962a) and Hassan et al. (2005a) all embryology, seeds and ovules.
Phylogeny. Nepokroeff et al. (2002) found that Mollugo and relatives and Pharnaceum and relatives each formed a well-supported clade, but the two were only weakly linked. However, support for a monophyletic Molluginaceae was strong both in Christin et al. (2011a) and Arakaki et al. (2011), and resolution of relationships within the clade was also good; branches in the Adenogramma-Pharnaceum clade were notably long (Arakaki et al. 2011). Thulin et al. (2016) provide a pretty compehensive tree for the famil, with all the major banches well supported. Mollugo is strongly para/polyphyletic (Christin et al. 2010b, 2011a; Arakaki et al. 2011; Thulin et al. 2016).
Classification. Thulin et al. (2016) provide a generic level classification for the family.
Previous Relationships. The limits of the family have long been unclear. Most Molluginaceae as circumscribed in M. Endress and Bittrich (1993) are included here, but Limeum, Corbichonia (Lophiocarpaceae), and Macarthuria, are elsewhere in the core Caryophyllales as separate monogeneric families, as is Kewa, which includes species that used to be in Hypertelis, which remains here. Polpoda is not incorporated in any description. It has P 4, A alternating with the perianth, G , basally connate styles, and scarious stipules (Hoffman 1994). There have been suggestions that Gisekia might be included in Phytolaccaceae-Rivinioideae (see Cuénoud et al. 2002), although here it is in its own family (Brockington et al. 2009).
Synonymy: Adenogrammaceae Nakai, Glinaceae Martius, Pharnaceaceae Martynov, Polpodaceae Nakai
[Montiaceae [[Halophytaceae [Didiereaceae + Basellaceae]] [Talinaceae [Anacampserotaceae [Portulacaceae + Cactaceae]]]]] / Portulacineae Engler: (plants with tuberous roots) [at least some species in all families]; (CAM +); phloem parenchyma cells with phytoferritin [crystalline iron-protein complex in plastids]; Ca oxalate crystals in stem epidermis; mucilage cells +; stomata paracytic; (lamina with peripheral vascular bundles, phloem internal [orientation normal]); lamina ± succulent, amphistomatic [?Basellaceae]; two pairs of bracteoles, inner pair in the median plane, lacking subtending buds, ± enclosing the flower; P petal-like, (-13), first two developing in the transverse plane; A (3) 5(opposite P)-8(-many); pollen pantocolpate; G ( - lateral),  [2 abaxial], style +, branches spreading; ovule lacking funicular/placental obturator; nuclear genome duplication, 6-bp deletion in chloroplast ndhf gene.
Age. An estimate of the age for this clade is (33.7-)18.8(-6.7) m.y., not very old (Ocampo & Columbus 2010), around 36.2 m.y. (Tank et al. 2015: Table S2), (47.6-)44.9(-42.2) m.y. (Arakaki et al. 2011), or about 42.6 m.y. (Magallón et al. 2015).
Evolution: Divergence & Distribution. This clade seems to be New World in origin (Ocampo & Columbus 2010). Hershkovitz and Zimmer (2000) suggested that there must have been a number of major dispersal/colonization events.
For family limits and characterisations, see Nyffeler and Eggli (2010b).
MONTIACEAE Rafinesque Back to Caryophyllales
Annual to perennial herbs, often with swollen roots and basal rosette leaves, internodes short (subshrubs); ?betalains; photosynthesis?; cork cambium initiation delayed; secondary growth little; vessel elements?; plant glabrous; stomata longitudinally oriented; cuticle waxes as procumbent platelets; leaves often with broad clasping bases, flat to terete with an adaxial impressed line (not succulent); inflorescences terminal or axillary, (monochasial) cymose, or single (axillary) flower; (transverse bracteoles absent, or -9 "sepaloids"); P 4-5(-19), (basally connate); A equal and opposite perianth members, (or 1 fewer, alternating with P - Hectorella, Lyallia), (-100, development centrifugal), basally connate or not; tapetal cells multinucleate; pollen also tricolpate, pantoporate; G [2-8], (placentation free central, with 4-7 ovules), style ± developed, branches diverging, stigma papillate; ovules (1/carpel), with medium funicle, inner integument protruding considerably, parietal tissue 1-5 cells across, in radial rows; fruit also circumscissile, or 1-seeded, indehiscent; outer wall of exotesta thickened and with stalactite-like projections, ?tegmen bar thickenings; n = 5-13, etc.
14 [list]/225: Parakeelya (40-70), Montiopsis (40), Claytonia (27), Phemeranthus (25-30). Especially western North and South America, also the Antilles and the Subantarctic Islands (map: approximate, from Hultén & Fries 1986; Fl. N. Am. 4: 2003; Miller & Chambers 2006; M. Ogburn, pers. comm. ix.2012; Australia's Virtual Herbarium i.2013 - much naturalization, so not easy). [Photo - Collection, but not all.]
Age. The age for crown-group Montiaceae is (25.4-)13(-3.4) m.y. (Ocampo & Columbus 2010: 95% highest posterior density) or (43.0-)39.9(-36.8) m.y. (Arakaki et al. 2011).
Evolution. Ecology & Physiology. Within Portulacineae, Montiaceae are noted for their ecological expansion into both colder and more seasonally variable habitats, and there have been several habit/habitat shifts, many being between the annual and perennial habit, the latter occurring in taxa that had moved into cooler environments - hardly notable niche conservatism (Ogburn & Edwards 2012, 2014; S. A. Smith et al. 2017). On the other hand, Montiaceae are not very speciose and are sister to a clade with almost ten times the number of species - most being in Cactaceae, of course.
Calandrinia polyandra (= Parakeelya) is a facultative CAM plant (Winter & Holtum 2014, see also 2011).
Pollination Biology & Seed Dispersal. The seeds may be forcibly ejected as the margins of the valves incurve during capsule dehiscence (Carolin 1993). The seeds of some Montiaceae are myrmecophytic (Lengyel et al. 2010).
Bacterial/Fungal Associations. The South American Calandrinia is a host of the anther smut Microbotryum (Uredinomycota), also found on Silene, etc. (Hood et al. 2010).
Genes & Genomes. There can be considerable infraspecific variation in chromosome numbers - thus the diploid number in Claytonia virginica varies between 12 and 191 (e.g. Lewis et al. 1967; Bogle 1969; see also McIntyre & Strauss 2017). There are suggestions that there has been a genome duplication in the ancestor of Claytonia (S. A. Smith et al. 2017; Y. Yang et al. 2017).
Chemistry, Morphology, etc. Hectorella has both spiral phyllotaxis and a closed vascular system, a very unusual combination (Beck et al. 1982). The lamina of Phemeranthus has peripheral vascular bundles with the xylem external (Ogburn & Edwards 2013).
The inflorescence of Hectorella and Lyallia may be a reduced cyme; there are alternate/2-ranked bracts below the flower, and the latter genus may have more than one flower per axil (Skipworth 1961; Wagstaff & Hennion 2007). The paired bracteoles below the flower in these two genera are clearly described and illustrated as being transverse (lateral) by Skipworth (1961), but later described as being ad/abaxial (median) by Philipson and Skipworth (1961). Cave et al. (2010) described the lower two bracteoles of Calandrinia as developing successively, the upper pair being lateral(-abaxial). Montiopsis can have trilobed bracteoles. Nyffeler and Eggli (2010b) described the flower of Lewisia as having up to 9 "sepaloids" (= perianth members). Dos Santos et al. (2012) noted that the petaloids in Claytonia appeared well after the androecium was initiated; however, they thought that they were calycine, but with very delayed growth, rather than outgrowths of the filaments.
Schnizlein (1843-1870: fam. 206) showed carpels alternating with the perianth members, or the median member in the abaxial position, as in Claytonia. Seed coat anatomy needs more study. Rocén (1927) thought that the endotegmen of Calandrinia (it looks like the exotegmen) had rod-like rhickenings; the tegmen was multiplicative.
Some additional information is taken from Philipson (1993) and Lourteig (1994), general, for Claytonia see Miller and Chambers (2006); see Meunier (1890) for ovules and seeds, for pollen, see Nilsson (1967); see Carolin (1993), Eggli (2002) and Nyffeler and Eggli (2010b) for general accounts.
Phylogeny. For the circumscription of Montiaceae, see above. West American members of the old Portulacaceae to be included in Montiaceae include Montia, Lewisia, Phemeranthus (this used to be included in Talinum - Talinaceae here), etc. (e.g. Hershkovitz 1993, 2006; Hershkovitz & Zimmer 2000). The whole clade has strong support, as does the sister group relationship between Phemeranthus, with pantoporate pollen, and the rest of the clade (Applequist et al. 2006; see also Ocampo & Columbus 2010; Ogburn & Edwards 2015). Ogburn and Edwards (2015) found two main clades apart from Phemeranthus, one largely South American and the other, within which relationships between Parakeelya and Calandrinia (also pantoporate pollen) were unclear, was largely North American.
Applequist et al. (2006: ndhf analysis, see also e.g. Nepokroeff et al. 2002; Ogburn & Edwards 2015) also included the New Zealand-Antarctic Hectorellaceae, previously of uncertain relationships, as a new tribe of Portulacaceae. Although flower position (axillary) and bracteole and stamen position of Hectorellaceae differ from that of other Montiaceae and the gynoecium is unilocular, the anatomy of the two is very similar (Carlquist 1998b).
O'Quinn and Hufford (2005) outlined the phylogeny of Claytonia (tricolpate pollen) and its sister taxon, Montia (pantocolpate).
Classification. See Nyffeler and Eggli (2010b) for included genera.
Synonymy: Hectorellaceae Philipson & Skipworth
[[Halophytaceae [Didiereaceae + Basellaceae]] [Talinaceae [Anacampserotaceae [Portulacaceae + Cactaceae]]]]: plant mucilaginous.
Age. Arakaki et al. (2011) suggested an age of (45.3-)42.5(-39.7) m.y. for this node, Magallón et al. (2015) an age of about 39.5 m. years.
[Halophytaceae [Didiereaceae + Basellaceae]]: fruit indehiscent, single-seeded.
Age. This node is around 38.1 m.y.o. (Magallón et al. 2015) or 34.6 m.y. (Tank et al. 2015: Table S2).
Evolution: Divergence & Distribution. At what level around here pantoporate pollen is an apomorphy is unclear (c.f. Prieu et al. 2017).
[Halophytaceae + Basellaceae] [if this clade exists]: stomata paracytic; ovule single [per flower]; n = 12.
Evolution: Divergence & Distribution. For possible apomorphies, some of which depend on the outcome of optimisation procedures, see Anton et al. (2014).
HALOPHYTACEAE A. Soriano Back to Caryophyllales
Annual herb, swollen roots 0; successive cambia +; wood rayless; ?mucilage; stomata paracytic (cyclocytic, parallelocytic); lamina with peripheral vascular bundles, phloem internal; plant monoecious, pedicels 0; nectary 0; staminate inflorescence: densely spicate; transverse bracteoles absent; P 4, barely petal-like, valvate-decussate; stamens alternate with perianth members, anthers extrorse, dehiscing by pores by contraction of the connective, endothecium with frame-shaped thickening on anticlinal walls; pollen cuboid, hexapantoporate; pistillode 0; carpellate inflorescence: fasciculate, several flowers embedded in swollen axis bearing leaves; P 0; staminodes 0; G , only adaxial carpel fertile, style +, short, stigmas spreading; ovule single [per flower], ?morphology; fruit a nutlet, swollen axis becoming hard, breaking up; ?tegmen bar thickenings; n = 12.
1 [list]/1: Halophytum ameghinoi. Argentina (map: from Zuloaga & Morrone 1999).
Evolution. Ecology & Physiology. CAM photosynthesis is likely here, the plant having fleshy leaves and growing in dry to very dry habitats - and its δ13C values agree (Holtum et al. 2018).
Chemistry, Morphology, etc. There are no endothecial thickenings at all on cells adjacent to the openings of the anthers (Pozner & Cocucci 2006).
Some information is taken from Bittrich (1993b) and Nyffeler and Eggli (2010b), general; for stomata, see Di Fulvio (1975); Pozner and Cocucci (2006) describe the staminate flower in considerable detail, including the distinctive endothecial thickenings and anther dehiscence.
Details of embryology and female flower and fruit development are poorly understood.
Previous Relationships. Halophytaceae were included in Chenopodiaceae (Cronquist 1981). Relationships with Aizoaceae - also with rayless wood - have also been suggested (Gibson 1978).
[Didiereaceae + Basellaceae]: ?
Age. The age of this node is (28.5-)14.9(-3.9) m.y. (Ocampo & Columbus 2010: 95% HPD), ca 33.9 m.y. (Tank et al. 2015: Table S2) or about 36.8 m.y. (Magallón et al. 2015).
DIDIEREACEAE Radlkofer, nom. cons. Back to Caryophyllales
Woody, (± stem succulent), often thorny, deciduous (evergreen); short shoots + (0); "tannin" common, methylated flavonoids +; (wide-band tracheids +); cork cambium initiation precocious; tanniniferous cells +; mucilage ducts +; leaf stomata parallelocytic, transversely oriented; cuticular waxes as ribbons or rodlets; short shoots common, (persistent paired prophylls); leaf vernation flat, (lamina terete, vascular bundles lateral); plant (gyno)dioecious, (inflorescence fasciculate); (transverse bracteoles absent); P 4-5, annular nectary at base; A 5 [alternating with P]-12 in a single whorl (many - Calyptrotheca), from ring primordium, basally connate; (with adaxial nectaries); pollen also tricolpate, (5-7-zonocolpate), aperture finely spinulate; G [(2-4)], stigmas ± peltate, fringed; ovules 1(-2)/carpel; fruit achenial, (circumscissile capsule, K strongly accrescent - Calyptrotheca); (seeds 2-3), with funicular strophiole or aril (0 - Ceraria); tegmen with bar thickenings; perisperm ± absent; n = 22, 24, often wildly polyploid.
7 [list]/16. Madagascar, South Africa, E. Africa (Map: from Coates Palgrave 2002; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; Bruyns et al. 2014b). [Photos - Collection.]
Age. The age for crown-group Didiereaceae is (24.4-)12.1(-2.4) m.y. (Ocampo & Columbus 2010).
Evolution: Divergence & Distribution. Portulacaria has tricolpate pollen and Calyptrotheca polypantoporate pollen, so the distinctive 5-7-zonocolpate of Didiereaceae s. str. is not an apomorphy for Didiereaceae s.l. (c.f. Nyffeler & Eggli 2010a b) and at what level pantoporate pollen is an apomorphy around here is unclear.
Ecology & Physiology. CAM or facultative CAM occurs here.
Chemistry, Morphology, etc. Rauh (1983) calls the spiky structures of Didiereaceae s. str. spines, being either leaves on short shoots or paired and stipular. However, Alluaudia has leaves subtending an axillary spiky structure, and later paired and apparently prophyllar leaves develop from an axillary bud below it. This suggests that the spiky structure is a modified axillary shoot, a thorn.
The bracteoles immediately associated with each flower are in the median plane, and large bracteoles of the inflorescence ("large bracts") may be obvious, as in Portulacaria. In Didiereaceae s. str. there are four stamens clearly alternating with the perianth members.
See Rauh and Schölch (1965 and references), Kubitzki (1993b), Schatz (2001) and Nyffeler and Eggli (2010b), all general, Hegnauer (1966, 1968, 1989: chemistry), Erbar and Leins (2006: floral ontogeny), and Sukhorukov et al. (2015: fruit and seed).
Phylogeny. This clade includes a morphologically distinctive monophyletic group of four Madagascan genera, Didiereaceae in the old sense, and immediately basal to them are some African ex-Portulacaceae. Relationships are [Portulacaria [Calyptrotheca + Didiereaceae s. str.]], and within the last group, Allaudiopsis is sister to the rest, while the position of Decarya has only weak support (see e.g. Bruyns et al. 2014b).
Classification. Didiereaceae are expanded to include some ex-Portulacaceae (see Appelquist & Wallace 2000, 2003); Appelquist and Wallace (2003) provide a rather overelaborate subfamilial classification. See also Bruyns et al. (2014b) for genera.
Synonmy: Portulacariaceae Doweld
BASELLACEAE Rafinesque, nom. cons. Back to Caryophyllales
Vines/lianes, with swollen rhizomes or tubers; successive cambia +; cork cambium initiation timing?, in outer cortex; vascular bundles separate, bicollateral; leaf stomata paracytic, ?oriented; cuticle wax crystalloids 0; leaves (also opposite), vernation curved to ± conduplicate, (lamina margins serrate, with glands - Tournonia); inflorescence racemose, (cymose - Tournonia); flowers small; P (4-)5(-13), ± connate; (nectary +) [also inside A]; A 4-9, often equal and opposite P, adnate to them, basally connate, (reflexed in bud); tapetal cells multi-nucleate; pollen hexapericolpate/porate, (cuboid), (pantoporate - 3 spp.); (style single, branches short), stigma ± capitate or lobed; ovule single [per ovary], basal, funicle stout, shortish; outer integument ca 2 cells across, inner integument 2-4 cells across, parietal tissue 2-8(?-16) cells across, nucellar beak +, no space between the integuments, placental obturator +; fruit an utricle, P persistent, (inner bracteoles surrounding fruit, fleshy, or dry, winged); testa in particular multiplicative, also tegmen, exotesta tanniniferous; perisperm scanty, starch grains clustered, embryo (spirally twisted), green; n = 12, 22, nuclear genome size [1C] ca 1.46 pg.
4 [list]/19. Africa, New World, apparently introduced into India-East Asia (map: from Sperling 1987; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; Fl. N. Am. 4: 2003). [Photos - Collection]
Evolution. Ecology & Physiology. For CAM photosynthesis in Anredera baselloides, which occurs only when the plant is water stressed, see Holtum et al. (2018).
Chemistry, Morphology, etc. Sperling (1987) reports both bracteoles and large, paired structures immediately surrounding the perianth (see also Eriksson 2007). The interpretation of floral morphology differs - c.f. Friedrich (1956), LaCroix and Sattler (1988) and Sperling and Bittrich (1993).
For general information, see Bogle (1969), Sperling (1987), Eriksson (2007), and Nyffeler and Eggli (2010b). For chemistry, see Hegnauer (1964, 1989), for wood anatomy, see Carlquist (1999), for successive cambia, see Jansen et al. (2000c), for leaf development, see Hernandes-Lopes et al. (2015), for ovules, see Rocén (1927: outer integument "viel" cells across).
Classification. Eriksson (2007) includes a synopsis of species included in the family.
Synonymy: Anrederaceae J. Agardh, Ullucaceae Nakai
[Talinaceae [Anacampserotaceae [Portulacaceae + Cactaceae]]]: plant mucilaginous; secondary growth normal; pericyclic fibres 0; stomata parallelocytic; A development from a ring primordium, many; fruit covered by dried P, pericarp 2-layered, exocarp ± caducous.
Age. Arakaki et al. (2011) suggested an age of (42.1-)39.4(-36.7) m.y., Magallón et al. (2015) an age of about 33.3 m.y., and Tank et al. (2015: Table S2) an age of around 30.8 m.y. for this node.
Chemistry, Morphology, etc. Ex-Portulacaceae in the pectinations basal to Cactaceae have the pericarp strongly differentiated into two layers.
For anatomy, see Ogburn (2007) and Ogburn and Edwards (2009).
TALINACEAE Doweld Back to Caryophyllales
Herbs to (lianescent) shrubs, underground parts often tuberous; cork cambium initiation timing variable, (cortical); tanniniferous cells +; C3/CAM cycling; petiole bundle arcuate, with wing bundles; stem stomata parallel to stem axis, leaf stomata un- or weakly transversely oriented, morphology variable; leaf vernation revolute; P quincuncial; A ca 15 to many, anther wall with two secondary parietal cell layers, inner producing the middle layer [monocot type]; archesporial cells uniseriate; pollen pantoporate [Talinum]; G , ovary at least initially septate; ovules with parietal tissue 1-2 cells across, epidermal cells radially elongate, nucellar cap to 4 cells across; fruit (baccate, mucilaginous, indehiscent - Talinella), epidermis papillate; seed strophiolate [= funicle?], exotesta well developed, endotegmen thickening slight; n = 8.
3 [list]/27. America and Africa, including Madagascar (map: from Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; Fl. N. Am. 4. 2003; Tropicos iii.2014). [Photo - Collection, but not all.]
Age. The age of crown-group Talinaceae is estimated at (18.3-)9.1(-2) m.y. (Ocampo & Columbus 2010) or the very different (33.2-)29.9(-26.3) m.y. (Arakaki et al. 2011).
Evolution. Ecology & Physiology. Talinum triangulare is a facultative CAM plant (Winter & Holtum 2014).
Chemistry, Morphology, etc. The roots are apparently polyarch (von Poellnitz 1934). Young leaves may have paired, axillary scales; these are the very tips of the prophylls.
See von Poellnitz (1934) and Nyffeler and Eggli (2010b), general, also Hernandes-Lopes et al. (2015: leaf development), Vanvinckenroye and Smets (1996: floral development), Meunier (1890: ovules and seeds), and Maheswari Devi and Pulliah (1975) and Veselova et al. (2012), both embryology.
Phylogeny. Talinella is nested within Talinum (Nyffeler 2007; Nyffeler & Eggli 2010b).
Classification. See Nyffeler and Eggli (2010b).
[Anacampserotaceae [Portulacaceae + Cactaceae]]: (sclereids in stem cortex); stem stomata 0[?]; leaves with axillary bi- or multiseriate hairs/scales; A development centrifugal; outer integument ca 2 cells across, inner integument 2(-3) cells across.
Age. The age for this clade is some (26.6-)14.3(-5.1) m.y. (Ocampo & Columbus 2010) or (39.6-)37(-34.4) m.y. (Arakaki et al. 2011).
Genes & Genomes. There is variation in the chloroplast infA gene in this clade, with both insertions and duplications occuring (Ocampo 2009).
Chemistry, Morphology, etc. The axillary hairs in the first two families are often bi- or oligoseriate, while those of the few Cactaceae examined - but from three subfamilies - are uniseriate, although those of Pereskiopsis are biseriate at the base. Chorinsky (1931) remains a useful early study on these structures, which are never vascularized (see also Rutishauser 1981). There are scattered stomata on the peduncle of Portulaca and on the stem of Anacampseros (pers. obs.).
ANACAMPSEROTACEAE Eggli & Nyffeler Back to Caryophyllales
Subshrubs with ± tuberous roots, (stems fleshy), (rosette plants), internodes short; cork cambium initiation precocious, (cortical); (wood rayless); (wide-band tracheids +); (sclereids +); (spirally-thickened fiber-sclereids in rays); facultative CAM, ?C4 photosynthesis; (lamina with peripheral vascular bundles), leaf stomata transversely oriented; leaves (opposite), lamina ± terete, (axillary hairs 0, but then concave adaxial scale - Avonia); upper and lower bracteoles in same plane; A 5-many, (outer 5 stamens alternating with P members), basally connate; G [(2) 3], septate, style solid, stigmas papillate, receptive on both surfaces; parietal tissue ca 2 cells across, nucellar cap 0; (exocarp and endocarp not separating - Grahamia); seeds pale-coloured, (winged), exotesta ± separating from endotesta, cells large, thin walled, unlignified, (bullate to long-papillate); embryo only slightly (much) curved, not surrounding the poorly developed perisperm; n = x = 9.
3 [list]/36: Anacampseros (34). Very scattered: C. and S. Australia, Somalia to South Africa (most species), S. South America, N. Mexico and S.W. U.S.A. (map: from Gerbaulet 1992a, 1993; Fl. N. Am. 4: 2003).
Age. The age of crown-group Anacampserotaceae is (22.6-)11.4(-3.2) m.y. (Ocampo & Columbus 2010: Talinopsis sister to Grahamia, etc.) or (34.2-)31(-27.8) m.y. (Arakaki et al. 2011).
Evolution: Divergence & Distribution. For the biogeography of this widely scattered clade, see Gerbaulet (1992b).
Ecology & Physiology. For the ecology of African Anacampserotaceae, see Gerbaulet (1993). Facultative CAM photosynthesis occurs here (Winter & Holtum 2017).
The seeds have very thin testas, so it would be no surprise if at least some of the family have very fast germination (<1 day: Kadereit et al. 2017 and references).
Chemistry, Morphology, etc. For general information, see von Poellnitz (1933), Gerbaulet (1992a), Rowley (1994), Eggli (2002), Nyffeler and Eggli (2010a, b) and Frandsen (2017: images); for anatomy, etc., see von Poellnitz (1933), for floral development, see Vanvickenroye and Smets (1999), and for some ovule morphology, see Rocén (1927).
Phylogeny. Nyffeler (1997) included six species of Grahamia (old style) in his study, and they formed a perfect pectination; at least some of the nodes had good support. Talinopsis frutescens is sister to the rest of the family (Nyffeler & Eggli 2010b; Ocampo & Columbus 2010
Classification. For genera, see Nyffeler and Eggli (2010a, b).
[Portulacaceae + Cactaceae]: unlignified parenchyma cells in wood; (hypanthium ± developed); G half inferior; pericarp not 2-layered.
Age. the age of this node is estimated at 18-11 m.y. (Wikström et al. 2001), (26.5-)13.9(-4.9) m.y. (Ocampo & Columbus 2010), (33-)22, 21(-11) m.y. (Bell et al. 2010), about 28.8 m.y. (Magallón et al. 2015), ca 29.1 m.y. (Tank et al. 2015: Table S2), or (37.6-)35(-32.4) m.y. (Arakaki et al. 2011).
Chemistry, Morphology, etc. Non-lignified parenchyma cells, often in bands, occur in the wood of at least some Portulaca and in Cactaceae (Melo-de-Pinna 2009).
PORTULACACEAE Jussieu, nom. cons. Back to Caryophyllales
Succulent (annual) herbs; cork cambium initiation delayed; (wood rayless); C4 photosynthesis; leaf stomata transversely oriented/unoriented, (paracytic); (internodes short); leaves (opposite), vernation flat to revolute, (blade terete, vascular bundles peripheral), (axillary hairs 0); inflorescences terminal, ± capitate (cymose), (flowers single), with involucre; (transverse bracteoles absent); (P 4-8), (connate), with a single trace; tapetal cells multi-nucleate; G [(2-)5(-8)], to semi-inferior, placentation parietal/basal; ovules with parietal tissue ca 5 cells across, in radial rows, or ca 8 cells across, not in rows [P. pilosa], (nucellar cap 2 cells across); embryo sac with chalazal haustorium; bracts and K deciduous in fruit, capsule circumscissile; seed with hilar aril; anticlinal walls of testa sinuous; n = (8-)10, x = 9; five copies of the ppc-1E1 gene lineage [?or whole Portulacineae].
1 [list]/40-115. Worldwide, but especially tropical and subtropical North and South America, weedy (map: approximate, from Legrand 1962; Geesink 1969; Frankenberg & Klaus 1980; Gilbert & Phillips 2000; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; FloraBase ii.2010). [Photo - Collection, but not all.]
Age. Ages suggested for crown-group Portulaca are (18.5-)9.6(-2.0) m.y. (Ocampo & Columbus 2010) and (43-)23(-6.9) m.y. (Ocampo & Columbus 2012: improved sampling, calibration on Hawaiian islands), or (21-)17.6(-14.3) m.y. (Arakaki et al. 2011).
Evolution. Ecology & Physiology. There have been several switches to C4 photosynthesis at a maximum of ca (33.8-)28.8(-23.8) m.y.a. (Ocampo & Columbus 2009) and at a minimum about 1/3 this time (Christin et al. 2011b). Ocampo et al. (2013) subsequently suggested perhaps a single origin there that could be dated to ca 23 m.y.a.; C3-C4 intermediates may be derived. They noted that there were two C4 subtypes and three anatomical variants in the genus (see also Voznesenskaya et al. 2010), and there are also facultative CAM/C4 plants (Winter & Holtum 2014, see also 2017). Christin et al. (2014b, q.v. for ppc-1E1 duplication) suggested that CAM evolved before C4 photosynthesis here.
Cushion plants are disproportionately common in this clade (Boucher et al. 2016b).
Genes & Genomes. For the increased rate of molecular evolution in the herbaceous Portulacaceae compared to the woody Cactaceae, see Y. Yang et al. (2015).
Chemistry, Morphology, etc. For leaf anatomy and development, where there is consderable variation connected only in part with photosynthetic pathways, see Voznesenskaya et al. (2010) and Hernandes-Lopes et al. (2015).
The development of the perianth is much retarded relative to that of the androecium (dos Santos et al. 2012).
See Sharma (1954) for floral anatomy (the single traces to the P members divide into three), Meunier (1890), Rocén (1927), Kajale (1940c) and Ocampo (2013) for ovules and seeds, and Nyffeler and Eggli (2010b) for general information.
Phylogeny. Relationships within Portulaca are discussed by Ocampo and Columbus (2009). The genus consists of a clade with opposite leaves, in turn made up of Australian and African-Asian clades, and a clade with spiral leaves (Ocampo & Columbus 2012; Ocampo et al. 2013).
Previous Relationships. For taxa included in earlier circumscriptions of Portulacaceae, see e.g. Carolin (1993) and Nyffeler and Eggli (2010b).
CACTACEAE Jussieu, nom. cons. Back to Caryophyllales
Plant ± woody; (alkaloids +); C3/CAM cycling; rays wide and tall; calcium oxalate as whewellite [CaC2O4.H2O]; cork cambium initiation precocious; extensive primary expansion of the pith; (sclereids in phloem); nodes often 1:2-10; epidermis (inc. cuticle) thick-walled, hypodermis + (0), with druses (0), numerous; leaf stomata unoriented; cuticular waxes as ribbons or rodlets, also thick prostrate plates; short shoots + [areoles], with leaves = spines, photosynthetic leaves, and uni- or biseriate hairs, (areoles long-lived, spines and sometimes expanded leaves continuing to be produced); long shoot leaves large, flattened, petiolate; median bracteoles 0; "P" several-numerous [modified bracts], spiral, outer sepaline and inner petaline; A development initially from five separate primordia; nectary rather disc-like; G [5-many], surrounded by stem tissue [with areoles, etc.], (inflorescence proliferating from bracts on ovary); placentation ± "parietal", incompletely septate, stigma wet; ovules in two ranks, many/carpel, parietal tissue ca 1 cell across, nucellar cap +, nucellar epidermal cells radially elongated, lateral epidermal cells anticlinally divided [?all], funicle with short hairs apically (not), long; (archesporium multicellular); fruit baccate; seed ?colour, funicles fleshy; endotegmic cell walls thickened or not; n = x = 11, chromosomes <3 µm long; 6 kb inversion in large single copy region of plastid genome.
139[list]/1,866 - five groups below. Nearly all New World, esp. arid conditions. [Photos - Collection.]
Age. Diversification in Cactaceae is thought to have begun in the mid-Caenozoic ca 30 m.y.a. (Hershkovitz & Zimmer 1997, q.v. for other estimates) or ca 29.1 m.y.a. (Tank et al. 2015: Table S1). Ocampo and Columbus (2010) suggest very much younger ages of (19.1-)10(-3.1) m.y. while Arakaki et al. (2011) estimated (30.5-)28.6(-26.7) m.y.; (37-)27(-16.5) m.y. is the estimate in Hernández-Hernández et al. (2014).
1. Leuenbergioideae Mayta & Molinari
± Lianescent; cork cambium initiation precocious, cortical; no stem stomata; (P laciniate); pollen colpate; (ovary inferior).
1/8. Mexico and the Caribbean, Brasil. (map: from Leuenberger 1986, 2008; Edwards et al. 2005)[Photo - Leaf, Flower, Fruit.]
Age. The crown-group age may be (28.1-)25.8(-23.5) m.y. (Arakaki et al. 2011).
[Pereskioideae [Opuntioideae [Maihuenioideae + Cactoideae]]] / caulocacti: cork cambium initiation delayed; cortical sclereids 0; stem mucilage cells +; stem epidermis persistent [?level], cuticle often thick, stomata numerous, parallel, opuntioid [subsidiary cells distinct, but apart from the innermost pair of cells more or less randomly arranged].
Age. Arakaki et al. (2011) suggested an age of (28.7-)27(-25.3) m.y. and Hernández-Hernández et al. (2014) an age of (28.5-)20.5(-16.5) m.y. for this node.
2. Pereskioideae Engelmann
± Lianescent; phloem sclereids +; lamina supervolute; A centrifugal, from 5 primordia; pollen tri- -polycolpate; endotegmen tanniniferous.
1/9. Andean, S. South America (map: from Leuenberger 1986, 2008; Edwards et al. 2005).
Age. Arakaki et al. (2011) suggest an age of around 27-25 m.y.a. for the crown group.
[Opuntioideae [Maihuenioideae + Cactoideae]]: stems succulent; CAM or facultative CAM +; (primary root growth determinate); extensive primary expansion of the cortex[?]; internodes short; wide-band tracheids in secondary xylem [at least in seedlings]; hypodermal collenchyma +; cortical chlorenchyma forming mesophyllar tissue with intercellular spaces; leaves small, terete, soon deciduous; inflorescences axillary [in areoles], flowers "solitary"; A from ring primordium; stigma commissural [?Maihuenoideae]; ovary inferior; perisperm ± 0 [?here].
Age. Arakaki et al. (2011) suggest an age of around (26.5-)25.3(-24.1) m.y. for this node.
3. Opuntioideae Burnett
Plant ± shrubby, (tree-like); stems usu. articulated, often flattened, (terete); vascular bundles lacking cap of phloem fibres; calcium oxalate hypodermal, as druses or spherical clusters; (cork cambium initiation precocious); (no stem stomata); leaf stomata parallel; leaves deciduous, lamina ± terete, (leaves subpersistent, large, with blade - Pereskiopsis); areoles with minute, retrorsely-barbed bristle-spines [glochids]; (hypanthium +, short); pollen pantoporate; seeds white, ± covered by bony funicle ["aril"]; testa lignin with guaiacyl/syringyl units [= normal], outer periclinal wall of testa little thickened; (cotyledons are storage organs of seed); much polyploidy, deletion of the chloroplast accD gene.
16/349: Opuntia (200). Canada, almost the Arctic Circle, to Patagonia. (map: see Thorne 1973; F. N. Am. vol. 4. 2003.) [Photo - Flower, Flower.]
Age. Crown-group Opuntioideae have been dated to (18-)15.1(-12.1) m.y. (Arakaki et al. 2011) or (13.8-)9.3(-5.9) m.y. (Hernández-Hernández et al. 2014).
Synonymy: Nopaleaceae Schmid & Curtman, Opuntiaceae Desvaux
[Maihuenioideae + Cactoideae]: inflorescence not proliferating; testa interstitially pitted or cratered, exotesta with outer periclinal wall much thickened.
Age. An age for this node is some (25.4-)24.4(-23.4) m.y. (Arakaki et al. 2011).
4. Maihuenioideae P. Fearn
Plant densely caespitose; cork cambium initiation precocious; large mucilage reservoirs in stem medulla and cortex; photosynthetic parenchyma at base of areolar crypts, stem stomata in areolar crypts; leaf stomata transverse; (areoles producing leaves), leaves to ca 1 cm long, subdeciduous, lamina terete, with cylindrical reticulum of bundles, the external xylem surrounding central mucilage reservoir; pollen tricolpate; funicles in fruit long, mucilaginous.
1/2. Argentina and Chile (map: from Leuenberger 1997, 2008).
Age. Crown-group Maihuenoideae are (2-8-)1.4(-0.3) m.y.o. (Hernández-Hernández et al. 2014).
5. Cactoideae Eaton
Plant essentially leafless [leaves up to 1.5(-2.5) mm long when mature]; calcium oxalate also as weddellite [CaC2O4.2H2O]; stem stomata unoriented [transverse - epiphytic taxa]; pollen 3-pantocolpate(-porate), (in tetrads); (outer integument 3-4 cells across - Cereus); funicle length?; (fruit dehiscing laterally); seeds with a conspicuous spongy hilum-micropyle region; loss of intron in the chloroplast PEP subunit β' rpoC1 gene.
112/1,498. New World, S. Canada to S.W. U.S.A. southwards; v. few in Africa, Madagascar, and Sri Lanka.
Age. Crown-group Cactoideae are (23.5-)21.8(-20.1) m.y.o. (Arakaki et al. (2011) or (24.5-)17.1(-12.7) m.y.o. (Hernández-Hernández et al. 2014).
5A. Blossfeldieae Crozier
Tuberous roots 0; spines absent; vascular bundles lacking cap of phloem fibres; calcium oxalate druses 0; hypodermal collenchyma 0; epidermis (inc. cuticle) thin-walled, soon replaced by cork cambium; photosynthetic parenchyma at base of areolar crypts; stem stomata few, in areolar crypts, leaf stomata 0; ?pollen; seeds with a funicular aril [strophiolate]; testa with one short narrow projection per cell ["hairy"]; n = 33 [hexaploid].
1/2. Bolivia to Argentina, eastern Andes (map: from Leuenberger 2008).
5B. Cacteae Reichenbach / The Rest.
(Plant epiphytic [ca 1/10 spp.]), (lianes); (tetrahydroisoquinoline alkaloids +); primary root growth determinate (not); (stem dichotomising); stem ribbed and/or tuberculate (not); (growth determinate); calcium oxalate usually as weddellite (and/or whewellite), (raphides +); (wide-band tracheids 0); cortical vascular bundles +; cortex broad, succulent, inner cortical cells collapsible/not; medullary vascular bundles +; (areoles dimorphic); (flowers monosymmetric); hypanthium + (0); pollen 3-pantocolpate(-porate), (in tetrads); (ovules circinotropous); seeds black to brown, (arillate), funicles?; testa lignin usu. with catechyl units (guaiacyl/syringyl; 5-hydroxyguaiacyl [5H] units), (hypocotyl storage organ); chloroplast PEP subunit β' rpoC1 intron lost.
91/1250: Mammillaria (145-180), Echinopsis (50-100), Aylostera (10-100), Echinocereus (44-71), Gymnocalycium (50), Rhipsalis (40). New World (S. Canada to S. W. U.S.A. southwards), esp. Mexico, Brasil, Peru-Bolivia; Rhipsalis with a few spp. in Africa, Madagascar, Sri Lanka; also rain forest climbers and epiphytes (map: see Thorne 1973; Barthlott 1983 and Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003 [Rhipsalis]; Fl. N. Am. vol. 4. 2003.). [Photo - Plant, Flower.]
Age. Arakaki et al. (2011) suggest an age of (21.7-)19.7(-17.7) m.y. and Hernández-Hernández et al. (2014) an age of 21.9-)15.3(-10.9) m.y. for this node.
Synonymy: Cereaceae de Candolle & Sprengel
5. Hylocereeeae Buxbaum
8/73: Selenicereus (31).
Evolution: Divergence & Distribution. Arakaki et al. (2011) suggested a number of clade ages; see also Nyffeler and Eggli (2010a) for some dates.
The diversification rate may have increased around here some (33.3-)30.1(-28.8) m.y.a. - or maybe ca 4 m.y. earlier in a clade including Portulacaceae (Magallón et al. 2018).Many diversification rates within Cactaceae are quite high, with significant radiations occuring in the late Miocene-Pliocene, ca 8-3 m.y.a. (Arakaki et al. (2011). Tank et al. (2015: Table S1) also note a notable increase in diversification in Cactaceae. Hardly surprisingly, the monotypic Blossfeldia, sister to all other Cactoidaeae (see below), represents a lineage with notably lowered diversification rates of 0 or 2.27 x 10-17/ma, depending on the particular measure used (Arakaki et al. 2011)! Pachycereeae, which include the North American columnar cacti, also began diversifying in the Late Miocene ca 8.5 m.y.a. (Barba Montoya et al. 2011), although it is difficult to understand details of evolution here because of gene/species tree discordance - independent lineage sorting (ILS) is coupled with very long generation times, and hemiplasy connected with this ILS accounts for about 60% of the apparent homoplasy (Copetti et al. 2017). Cereeae began diversifying ca 3 m.y.a. or less, the central Brazilian Cerrado being the center for the group (Franco et al. 2017). Crown group Opuntia in the narrow sense, with 150-180 species, may be (7.5-)5.6(-3.6) m.y. old (Araki et al. 2011), and originating in southwest South America, it may have moved to North America by long-distance dispersal, subsequently diversifying there considerably (Majure et al. 2012).
Hernández-Hernández et al. (2014) examined diversification in the family from various points of view. Although the initial adaptation to dry conditions, probably in the central Andean region around 30 m.y.a., was important, subsequent diversification occurred rather later, 15-10 m.y.a., and a substantial component of this was in clades that had moved to North America. In Cactoideae in particular, the evolution of a diversity of growth forms and adaptations to various pollinators, particularly bats and birds, also played major roles (Hernández-Hernández et al. 2014: more on ages, diversification rates, etc.). For wood evolution, etc., in Cacteae, see Vásquez-S&nchez et al. (2017).
Cactaceae are an iconic family of the New World, but Rhipsalis, epiphytic and bird-dispersed, has a few species growing in Africa, Madagascar, and Sri Lanka; there have been questions as to whether the Old World species are native, or not (Barthlott 1983). Korotkova et al. (2011) emphasized the differences found by Barthlott (1981) between Old World R. baccifera and other taxa and suggested a long history in the Old World. Grosse-Veldmann et al. (2016a) thought that the evolution of autogamy in the genus might have facilitated its wide distribution.
For distribution maps of all the genera, see Barthlott et al. (2015b).
Hybridization is quite common in Cactaceae, with genera like Discocactus being of possible hybrid origin, although how important it has been the diversification of the family is unclear (Machado 2008, but see Capetti et al. 2017).
Ecology & Physiology. Edwards and Donoghue (2006; see also Edwards 2006; Edwards & Diaz 2006; Ogburn & Edwards 2010) discuss the eco-physiological evolution of Cactaceae (for which, also see Nobel 1982, 1988 and references). They emphasize that the leafy Pereskia and Rhodocactus clades have high photosynthetic water use efficiency, very high minimum leaf water potentials (water movement is easy), and conservative stomatal behaviour, the stomata opening only when there is available water, i.e. at night or after rain. Other features of potential functional interest include the production of large amounts of water conducting tissue relative to leaf area, and also CAM-type photosynthesis. This latter is poorly developed in Pereskia, etc., but is well developed in succulent cacti (Martin & Wallace 2000; Edwards & Donoghue 2006), as it is in a number of other xerophytic plants.
Calcium oxalate metabolism in Cactaceae and relatives is potentially interesting. There is variation in the degree of hydration of calcium oxalate, with two crystal forms, weddellite (CaC2O4.2H2O) and whewellite (CaC2O4.H2O); Cactoideae alone have weddellite (Rivera and Smith 1979: they note only druses were examined; Monje & Baran 2002; esp. Hartl et al. 2007). Some Cactaceae accumulate positively massive amounts of calcium oxalate crystals, for example, they make up ca 85% of the dry weight of Cactus senilis. The recent finding (Tooulakou et al. 2016) that in the eudicots studied (no Cactaceae, but two other Caryophyllales were) such crystals are broken down to produce CO2 during the day when the plant is stressed, reforming at night, so providing a reserve of CO2 for the plant - it is a kind of CAM-cycling (see Kuo-Huang et al. 2007 for other possible functions of druses). When the cactus dies, the calcium oxalate in the plant returns to the soil as calcite, resulting in appreciable amounts of carbon being stored in the soil (Garvie 2006).
Most Cactaceae have a broad and shallow rooting system that allows quick uptake of water after rain. In a number of Cactaceae, especially Cactoideae but not Pereskia s.l., the primary root is determinate in growth (Dubrovsky & North 2002; Shishkova et al. 2013 for the rather erratic distribution of this feature), perhaps facilitating the rapid development of lateral roots (Rodríguez-Rodríguez et al. 2003). "Rain roots", water-absorbing roots, develop quickly after rains and die when the soil dries up. Here, too, the main root usually aborts (Shishkova et al. 2008; Ogburn & Edwards 2010), but a skeletal root system of perennial, cork-covered roots persists (Gibson & Nobel 1986). Contraction of the roots, so keeping the plant close to the ground surface, is known or suspected for some Cactoideae (Garrett et al. 2010). Roots in at least some Cactaceae have rhizosheaths surrounding and adherent to the root and perhaps protecting it against dessication; they are formed by mucilage from the root, soil grains, etc. (Huang et al. 1993; Dubrovsky & North 2002).
Fleshy, water-storing roots are scattered in Cactaceae, including Pereskia (e.g. Rauh 1979); the taxa involved are usually small plants. The tissue involved is not always the same, suggesting the independent origin of such roots, but it is some kind of modified secondary vascular tissue (Stone-Palmquist & Mauseth 2002). These swollen roots seem to be particularly common in the taxa of the basal pectinations of Opuntioideae (Griffith & Porter 2009), and they are also scattered in families in the clades immediately basal to Cactaceae (see also Griffith 2004).
Diversification of the "leafless" Cactaceae may be as much connected with the development of a cauline water storage system as with the evolution of the other ecophysiological features just mentioned (and of course one would like to know much more about the physiology and anatomy of the clades immediately basal to Cactaceae). The ribbed and/or tuberculate stems of most Cactoideae allow the loss and gain of large amounts of water as the stem can easily contract or expand (see also Mauseth 2006a). Few cacti are really dessication tolerant, although the diminutive Blossfeldia is an exception (Barthlott & Porembski 1996; Griffith 2009). Finally, although Cactaceae are pre-eminently a group of drier climates in the New World and a notable component of seasonally dry tropical forests (Pennington et al. 2009), a number of Cactoideae grow in more or less humid forest as lianes and epiphytes, several having flattened and leaf-like stems; the epiphytic habit may have evolved four times or so there (Korotkova et al. 2010). Some species of cacti can also stand extreme cold (to -200C), cold hardening remarkably quickly in a matter of a very few days (Nobel 1982). Interestingly, however, unlike several other group that grow in drier habitats, salt tolerance is uncommon (Flowers et al. 2010).
There is considerable variation in growth form in "leafless" Cactaceae, which range from often bizarrely-branched trees to tall and unbranched to flat-discoid to tussock-forming to stoloniferous ("Wandersprosse", Creeping Devils) and occasionally even rhizomatous plants (see e.g. Rauh 1979), and this is discussed in a phylogenetic context by Hernández-Hernández et al. (2011). For details of the ecology of columnar cacti, including drought tolerance, photosynthetic rate, germination and seedling establishment, see papers in Fleming and Valiente-Banuet (2002) and Williams et al. (2014).
In common with some other groups inhabiting saline conditions (including Tamaricaceae, Chenopodiaceae), some Cactaceae have very fast germination, i.e. they germinate within one day of imbibition beginning (Parsons 2012; Parsons et al. 2014).
On a totally different subject, grafts between taxonomically widely distant taxa are easy to make in Cactaceae. For instance, Blossfeldia can be grafted onto Pereskiopsis, and contamination of Blossfeldia DNA by that of its stock was fingered as a possible cause of early conflicts over the phylogenetic position of that remarkable genus (Gorelick 2004).
Pollination Biology & Seed Dispersal. The evolution of a sort of hypanthium and so the possibility of developing a long floral tube may have been a key innovation for Cactoideae allowing a greater diversity of pollinators for the flowers; Cactoideae are much more speciose than other clades in this phylogenetic area (Schlumpberger 2012). Bee pollination is probably plesiomorphic in Cactaceae, and there have been perhaps ten bee-to-humming bird pollinator shifts and half as many bee-sphingid moth shifts, mostly in Cactoideae (Schlumpberger 2012). A variety of other pollinators also visit cacti flowers. Thus about 200 species in 51 genera are pollinated by bats (Dobat & Peikert-Holle 1985); Fleming et al. (2009) conservatively list 42 species in 26 genera (for bat pollination in columnar cacti, see Arizmendi et al. 2002 and references: also other papers in Fleming & Valiente-Banuet 2002). Some 390 species have reddish flowers, and these flowers were notably often tubular (ca 20%); there are perhaps 120 (Gorostiague & Ortega-Baes 2015: cautions should be heeded!) or 187 (Mutke et al. 2015) species with flowers that might be considered bird-pollinated, and many are found in the east Brazilian caatinga. Almeida et al. (2013) looked at nectary morphology and nectar concentration in some Cactoideae with very different floral morphologies; species with more exposed nectaries had greater sugar concentrations, perhaps being bee-pollinated, while Grosse-Veldmann et al. (2016a) examined various aspects of pollination in Rhipsalis. The senita cactus, Lophocereus/Pachycereus schottii, is actively pollinated by a pyralid moth Upiga virescens that lays eggs in some flowers leading to the loss of the fruit; other animals that are potential pollinators also visit the flowers (Fleming & Holland 1998; Holland & Fleming 1999).
Animal - mostly bird - dispersal of the fruits is very common in the family; Rhipsalis (see above for its distribution) has mistletoe-like fruits and in South America Cactaceae with such fruits are dispersed by the mistletoe specialist friar birds (Euphoniinae, near Fringillidae: Snow 1981; Restrepo 1987). In some Cactoideae in particular the seeds may germinate while still in the fruit, a form of vivipary (Cota-Sánchez et al. 2007).
Plant/Animal Interactions. The cactus-feeding habit may have evolved only once in the pyralid phycitine moths, although support is weak (Simonsen 2008: morphology only). The phycitines include the famous/infamous (it depends on where you live) Cactoblastis cactorum, unfortunately now introduced into the U.S.A. (see also Ervin 2012).
The Drosophila repleta species group, with over 100 species, has radiated on Cactaceae, the larvae growing on fermenting cactus tissues, whether cactus pads or the stems of columnar cacti (Oliveira et al. 2012); they moved on to this habitat from fermenting fruits perhaps 16-12 m.y.a. and have colonized columnar cacti several times (López-Olmos et al. 2017). The chemistry of the cacti is complex, and they contain numerous potentially toxic compounds which the insects have to tolerate (López-Olmos et al. 2017 and references). Some Drosophila will grow on only a single host, the latter containing sterols that can stand in for essential sterols missing from the ecdysone pathway of the insect (Lang et al. 2012). Rotting cacti in general provide habitats for numerous insects in the Sonoran desert region (Pfeiler et al. 2013).
Bacterial/Fungal Associations. Endophytic bacteria have been isolated from Cactoideae growing in the Sonora desert. These may help the cacti grow on rocks, and in vito fixation of nirtogen has also been observed (Puente et al. 2009; Lopez et al. 2011).
Vegetative Variation. The stout, more or less succulent stems that characterises members of Cactaceae - even Pereskia has quite thick stems - results from primary or secondary thickening/expansion in the cortex, less often the pith (for which, see Troll & Rauh 1950; Boke 1954, 1980). Branched columnar cacti (and Opuntioideae) have constrictions where the branch joins the stem, which would seem to be rather hazardous biomechanically. However, Schwager et al. (2013) show how details of thickening pattern, fibre orientation, etc., make this constriction in the three Cactoideae that they studied biomechanically more plausible. Interestingly, these species may not have tension wood. See also Schwager and Neinhuis (2015, 2016) for branching.
The rather ordinary-looking leaves of Leuenbergioideae and Pereskioideae represent the plesiomorphic condition for the family (but c.f. Griffith 2004, 2008). In Opuntioideae, the leaves of Pereskiopsis are rather similar, while those of Quiabentia (the two may be sister taxa - e.g. Butterworth & Evans 2008) are terete, unifacial but also persistent; such large leaves have probably been derived more than once in the subfamily (Griffith 2009; Griffith & Porter 2009; Ritz et al. 2012). Stomata are restricted to leaves and the stem adjacent to areoles in leafy Opuntioideae (Griffith 2008). In most other Opuntioideae the leaves are small, terete and deciduous. These leaves lack a blade meristem but have an hypodermal meristen around the periphery of the leaf, and Boke (1944) rather hesitantly reported stipules associated with these leaves. Although one commonly thinks of Cactoideae in particular as being leafless, Mauseth (2007) showed that most do have leaves, although they are up to only 1.5(-2.5) mm long when mature and so are mostly shorter even than the small, terete leaves of Opuntioideae. Despite their small size, Cactoideae leaves may have a rudimentary lamina with vascular tissue, stomata, etc. The leaf base is early distinguishable from the rest of the leaf, and its subsequent development results in the ribs and tubercles along the stem that are characteristic of so many Cactaceae (Boke 1954). The spines are modified leaves, there are intermediates between spines and glochids, and both are initiated in spirals surrounding the areole apex - areoles represent aggregations of leaves, variously modified (Boke 1944, 1980; de Arruda and Melo-de-Pinna 2016).
The spines and hairs that make up the areoles of Cactaceae represent a short shoot, and areoles may keep on growing and adding spines and even photosynthetic leaves, as in Pereskia. Mammillaria appears to have dimorphic areoles: There are normal spiny areoles borne on tubercules (hence the generic name) and spineless areoles that bear flowers that are found in the axils of the tubercules; see also Rauh (1979) and Boke (1980) for inflorescence development. In Echinocereus the areole meristem, whether vegetative or floral, becomes enclosed, and breaks through the stem when it develops (Sáncgez et al. 2015).
Genes & Genomes. For the loss of the inverted repeat and the chloroplast ndh genes in Carnegiea gigantea, see Sanderson et al. (2015); the ndh function may be taken over by a nuclear gene.
Castro et al. (2016) discuss variation in the heterochromatic banding of the chromosomes, which may be of some systematic interest. For chromosome counts in the family, see Ross ().
There is likely to have been ancient hybridization in Opuntia (Majure et al. 2012), and tardy coalescence can cause major problems when inferring relationships (Copetti et al. 2017).
Economic Importance. The cochineal insect, the sternorrhynchid Dactylopius, grows on species of Opuntia. The genus also provides food, fodder for livestock, and includes some seriously invasive species (e.g. Ervin 2012 for references). Goettsch et al. (2015) found that about 30% of all cacti, a very high level, were threatened because their habitats were being converted for other uses and the plants themselves collected by cactus-fanciers.
Chemistry, Morphology, etc. Lignin in the testa of Cactaceae-Cactoideae is variable in composition, many members having otherwise rare catechyl units (F. Chen et al. 2013: other lignin units as well). The amount of lignin there is moderate, taxa with "normal" guaiacyl/syringyl units either have substantially more (Opuntioideae) or sometimes much less (some Cactoideae) (Chen et al. 2013), and there is also a correlation with seed colour. The survey of lignin composition could usefully be extended.
The roots of at least some Cactoideae have an open type of apical meristem (Rodríguez-Rodríguez et al. 2003). Root hairs sometimes develop from all cells in the root, unusual for seed plants (Dubrowsky & North 2002). Wide-band tracheids are most frequently present in the seedlings, and they may persist in the adult plant if it is small and globular, but if it grows erect they may no longer be produced, the plant needing stronger support tissue (e.g. Mauseth 2006). Given the width of their stems, it is not surprising that many Cactaceae have very broad apical meristems 400-1500 µm across, rather broader than those of other flowering plants (Gifford 1954; Clowes 1961: sampling poor; Boke 1980), although they are only 80-329 µm across in Pereskia (Boke 1954). The cortex is particularly variable in Cactoideae. Mauseth and Landrum (1997) commented on the apparently very long-lived epidermis in many Cactaceae, which may remain functional for hundreds of years (see also Mauseth 2006a). Cork cambium may eventually develop, nearly always in the epidermis and nowhere else, and in some cases the plant may die if it is extensively developed (Evans & Cooney 2015), while development of a hypodermal cork cambium may be defence against attack by the loranthaceous Ligaria in Corryocactus (Mauseth et al. 2015). Cuticle waxes in the form of spiral rodlets occur in Cereeae.
There is potentially interesting variation within the parallelocytic stomata "type" so common here. Wallace and Dickie (2002) thought that the stomata of Opuntioideae were unique; in both Pereskia and Opuntioideae the subsidiary cells do not, or only barely, overlap the ends of the guard cells, the "opuntioid" stomatal type (it could be called brachyparallelocytic), while in other Cactaceae subsidiary cells successively more broadly invest the poles of the whole stomatal apparatus. There is also variation in stomatal orientation. The stomata on the stems of Pereskia and Opuntioideae are oriented parallel to the long axis of the stem, while in Cactoideae they tend to be unoriented (Eggli 1984).
The inferior ovary of Cactaceae is a text-book example of receptacular epigyny, the tissue investing the ovary being of axial origin (Boke 1964; see also Tiagi 1963 and references). Thus in genera like Opuntia areoles arranged in spirals cover the inferior ovary; it is as if the ovary had sunk into the stem. In Pereskia nemorosa and a few other Cactaceae additional flowers may arise from the axils of the leaves or from areoles on the ovary, the proliferating infliorescences in the characterization above (Rauh 1979; Leuenberger 2008 - see also Tetragonia-Aizooideae-Aizoaceae). The hypanthium so conspicuous in some Cactoideae in particular is an elaboration of this axial tissue, while "petals" show all intergradations with arole-subtending leaves on the axial tissue surrounding the ovary. The evolution of this inferior ovary needs to be re-examined given the paraphyly of Pereskia s.l. and the probable position of Portulacaceae as sister to Cactaceae; some species of Pereskia s. str. have superior ovaries (see Rauh 1979; Boke 1980; Edwards et al. 2005). Tiagi (1963) noticed that in Pereskia aculeata and P. sacharosa the course of the vascular tissue in the hypanthium was S-shaped, while in P. bleo and P. grandifolia it took the course of an inverted U, however, the significance of this is unclear [nomenclature to be updated]. Vascularization of "prophylls", bracts and perianth members of the flowers varies (Tiagi 1963).
The initial stages of androecial development may be as either separate, more or less spirally-arranged primordia, or as a single ring primordium (Leins & Erbar 1994b). Ovary placentation is variable. Placentae may alternate with septae, and/or be more or less basal; Leins and Schwitalla (1988) interpret the condition in which ovules are associated with incomplete septae proceeding from the ovary wall as the plesiomorphic condition for Cactaceae (see also Leins & Schwitalla 1986). The nucellus in Parodia may protrude through the micropyle (Rauh 1979). Cisneros et al. (2011) suggest that the inner integument of species of Hylocereus may be 4-5 cells across, but this is not readily to be seen in the images they provide.
For general information, see Boke (1980), Barthlott and Hunt (1993), Anderson (2001), Nobel (2002) and Schumannia 7. 2015 (= Barthlott et al. 2015a); Hunt et al. (2006) provides an excellent summary of the family, including a volume of superb photographs of nearly all species taken mostly in the wild (see also Lodé 2015a, b). For chemistry, see Hegnauer (1964, 1989) and Gibson et al. (1986: alkaloids), for spines, see Schlegel (2009 and literature, morphology and structure), for general anatomy, see Terrazas and Arias (2003: esp. Cactoideae) and Terrazas Salgado and Mauseth (2002), for nodes, see Bailey (1960) for cortical bundles, see Mauseth and Sajeva (1982), and for wide-band tracheids in particular, see Mauseth (2004a), Godofredo and Melo-de-Pinna (2008) and Arruda and Melo-de-Pinna (2010). For Pereskia s.l., see Boke (1968 and references), Leuenberger (1986: general), and Mauseth and Landrum (1997: "relictual" anatomical characters), Neumann (1935: pollen, etc., development), and Jiménez-Duran et al. (2016: embryology). For Opuntioideae, see Hunt and Taylor (2002: general) and Stuppy (2002: morphology); for leaf anatomy, see Boke (1944), for general anatomy see Mauseth (2005), for wood anatomy, see Mauseth (2006c). For Maiheunia some information is taken from Gibson (1977) and Mauseth (1999), anatomy, and Leuenberger (1997), general; Taylor (2005) is a good introduction. For Blossfeldia, see Barthlott and Porembski (1996). For floral morphology, see Ross (1982), for pollen, see Cuadrado and Garralla (2009), Leuenberger (1976: general) and Garralla and Cuadrado (2007: Opuntioideae), for ovules, etc., see Mauritzon (1934d) and Maheshwari & Chopra (1955), for seed morphology, see Barthlott and Voigt (1979), Bregman (1992), and Barthlott and Hunt (2000: Cactoideae).
For revisions of critical taxa, see in particular work by Leuenberger, e.g. Leuenberger and Eggli (1999: Blossfeldia) and Leuenberger (1986: Pereskia and Rhodocactus, 1997: Maiheunia, 2008: update on the literature of all three). Calvente (2012) enumerated the taxa in Rhipsalis. Rowley (2004) listed names of nothogenera, and these had doubled in number in the preceding ten years.
As Edwards et al. (2005) note, the anatomy of the outgroups to Cactaceae is poorly known, as is the occurrence of proliferating inflorescences in Portulaca, also with a more or less inferior ovary and now thought to be sister to Cactaceae (c.f. Edwards et al. 2005).
Phylogeny. The basic phylogenetic relationships within Cactaceae are still rather uncertain, and chloroplast and nuclear genes can suggest different major clades (see Butterworth 2006a and Nyffeler & Eggli 2010a for summaries; Moore et al. 2018). A study by Nyffeler (2002) found rather weak support for the subfamilies and that perhaps rather distressingly Pereskia was not clearly monophyletic. Edwards et al. (2005) confirmed that Pereskia s.l. was paraphyletic, which allowed them to shed new light on the evolution of the cactus habit (c.f. Butterworth & Wallace 2005 - topology different). For more details on the relationships of the major clades in Cactaceae, now all individually quite well supported, see Butterworth and Edwards (2008), Hernández-Hernández et al. (2011: position of Maihuenoideae unclear, 2014 [Maihuenoideae [Opuntioideae + Cactoideae]]) and especially Arakaki et al. (2011); details of relationships in Bárcenas et al. (2011) were less clear, but only the trnK-matK region was examined.
For relationships within Opuntioideae, see Griffith (2002), Wallace and Dickie (2002), Butterworth and Edwards (2008), Hernández-Hernández et al. (2011, 2014) and especially Griffith and Porter (2009). The latter found the well-supported set of relationships [Maihueniopsis et al. [Pterocactus [terete-stemmed species + flat-stemmed species]]]; the leafy Pereskiopsis is in a derived position in the clade (c.f. e.g. Mauseth 2005 on its apparently plesiomorphous features). Ritz et al. (2012) examined the phylogeny and evolution of Andean species of Opuntia with terete stems, and Bárcenas (2016) relationships in the Cylindropuntia area..
Within Cactoideae, the distinctive Blossfeldia liliputana (= Blossfeldioideae Crozier) is sister to all other Cactoideae (Crozier 2004), and despite some initial controversy over this position, it has been confirmed (e.g. Gorelick 2004; Mauseth 2006b; Butterworth 2006b; Arakaki et al. 2011). Hernández-Hernández et al. (2011, see also 2014) provide a quite detailed phylogeny of Cactoideae, although for the most part maximum likelihood bootstraps were low and maximum parsimony support still lower; earlier studies of Cacteae (Butterworth et al. 2002) and Mammillaria (Butterworth & Wallace 2004) faced the same problem. Vázquez-Sánchez et al. (2013, 2017) discussed the phylogeny of Cacteae. For the phylogeny and evolution of columnar Cactoideae, see Wallace (2002: Calymmanthium is odd); Franco et al. (2017) studied relationships in Cereeae, Tapia et al. (2017) relationships in Echinocereeae, especially around Cephalocereus, for Echinocereus itself, see Sánchez et al. (2014), and Korotkova et al. (2018 relationships in Hylocereeae; for relationships of South American mountain cacti, see Ritz et al. (2007), for Gymnocalycium (Trichocereeae), see Meregalli et al. (2010) and Demaio et al. (2011). For Rhipsalidae, see Calvente et al. (2011a, b: also character evolution) and Korotkova et al. (2011: Hatiora polyphyletic), for Pfeifferia and relatives, see Calvente et al. (2011), and for Rhipsalis itself, see Calvente (2012) and Korotkova et al. (2011). Cruz et al. (2016) looked at relationships within some Hyloceridae, several epiphytic and with flattened stems. For Echinopsis see Schlumpberger and Renner (2012). Disentangling relationships among North American columnar cacti presents major problems because of the consequences of slow coalescence (Copetti et al. 2017, also S. Hartmann et al. 2002). See Wallace and Cota (1996) for the PEP subunit β' rpoCI intron and Wallace and Gibson (2002) for a general study.
Classification. Metzing and Kiesling (2008) summarize early (pre-DNA) studies in the family, and include reproductions of some remarkable evolutionary trees. For a recent classification of the whole family, genera and tribes being listed, see Nyffeler and Eggli (2010a).
Over the years, there have been major disagreements over generic limits (e.g. Gibson et al. 1986), and depending on the author, the number of genera occurring in the family varies by a factor of ten, and of the species by a factor of two. For example, in 1903 there were a mere sixteen genera in Cactoideae in 1903, but now as many as 116 genera may be recognized (Hunt 2002). Bárcenas et al. (2011) sampled quite extensively in the family and found that many tribes and genera in both the big subfamilies were not monophyletic: Only 4/6 and 14/36 genera of Opuntioideae and Cactoideae respectively for which two or more species were sampled turned out to be monophyletic, that is, only half the genera that had more than a single species were monophyletic. Floral traits often reflect pollinator preferences rather than clades, and growth habit is also labile (Schlumpberger & Renner 2012: Echinopsis area). Much phylogenetic work explicitly or implicitly has taxonomic implications (e.g. Korotkova et al. 2010; Calvente et al. 2011; and especially Bárcenas et al. 2011), although the latter in particular were appropriately conservative. For generic limits in Cacteae, see also Vázquez-Sánchez et al. (2013) and for those in Hylocereae, see Korotkova et al. (2018). For a discussion on generic limits in the whole family, confirming that the situation is indeed chaotic at all levels, see Hern&ndez-Ledesma et al. (2015); Lodé (2015a, b) presents a new classification.
Opuntia has been broadly delimited, but Wallace and Dickie (2002) have suggested that it should be dismembered, Opuntioideae then including sixteen genera. The situation in Opuntioideae is indeed a mess, as is clear from the study by Griffith and Porter (2009). Hunt (1999, 2002) had earlier proposed the recognition of about eight broadly-delimited genera, roughly equivalent to tribes of other workers, which certainly makes sense pending sorting out the phylogeny of the group as a whole - and might also be a sensible final solution. Whether or not the stakeholders (Griffith & Porter 2009) can agree might be another matter.
Previous Relationships. Despite the distinctive appearance of the "leafless" cacti, the relationships of the family with other Caryophyllales has generaly been recognized.