EMBRYOPSIDA Pirani & Prado
Gametophyte dominant, independent, multicellular, thalloid, with single-celled apical meristem, showing gravitropism; rhizoids +, unicellular; flavonoids + [absorbtion of UV radiation]; protoplasm dessication tolerant [plant poikilohydric]; cuticle +; cell walls with (1->4)-ß-D-glucans [xyloglucans], lignin +; several chloroplasts per cell; glycolate metabolism in leaf peroxisomes [glyoxysomes]; centrioles in vegetative cells 0, metaphase spindle anastral, predictive preprophase band of microtubules, phragmoplast + [cell wall deposition spreading from around the spindle fibres], plasmodesmata +; antheridia and archegonia jacketed, stalked; spermatogenous cells monoplastidic, centrioles develop de novo, associated with basal bodies of flagellae, multilayered structure +, proximal end of basal bodies lacking symmetry, stellate pattern associated with doublet tubules of transition zone; spermatozoids with a left-handed coil; male gametes with 2 lateral flagellae; oogamy; diploid embryo initially surrounded by haploid gametophytic tissue, plane of first division horizontal [with respect to long axis of archegonium/embryo sac], suspensor/foot +, cell walls with nacreous thickenings; sporophyte multicellular, sporangium +, single, with polar transport of auxin, dehiscence longitudinal; meiosis sporic, monoplastidic, microtubule organizing centre associated with plastid, cytokinesis simultaneous, preceding nuclear division, sporocytes 4-lobed, with a quadripolar microtubule system; spores in tetrads, sporopollenin in the spore wall, wall with several trilamellar layers [white-line centred layers, i.e. walls multilamellate]; close association between the trnLUAA and trnFGAA genes on the chloroplast genome.
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 common ancestor of the group.
Abscisic acid, ?D-methionine +; sporangium with seta, seta developing from basal meristem [between epibasal and hypobasal cells], sporangial columella + [developing from endothecial cells]; stomata +, anomocytic, cell lineage that produces them with symmetric divisions [perigenous]; underlying similarities in the development of conducting tissue and in rhizoids/root hairs; spores trilete; polar transport of auxins and class 1 KNOX genes expressed in the sporangium alone; MIKC, MI*K*C* and class 1 and 2 KNOX genes, post-transcriptional editing of chloroplast genes; gain of three group II mitochondrial introns.
[Anthocerophyta + Polysporangiophyta]: archegonia embedded/sunken in the gametophyte; sporophyte long-lived, chlorophyllous, nutritionally largely independent of the gametophyte; sporophyte-gametophyte junction interdigitate, sporophyte cells showing rhizoid-like behaviour.
Sporophyte well developed, branched, free living, sporangia several; spore walls not multilamellate [?here]; apical meristem +.
EXTANT TRACHEOPHYTA / VASCULAR PLANTS
Photosynthetic red light response; water content of protoplasm relatively stable [plant homoiohydric]; control of leaf hydration passive; (condensed or nonhydrolyzable tannins/proanthocyanidins +); vascular tissue +, sieve cells + [nucleus degenerating], tracheids +, in both protoxylem and metaxylem; endodermis +; root xylem exarch [development centripetal]; stem with an apical cell; branching dichotomous; leaves spirally arranged, blades with mean venation density 1.8 mm/mm2 [to 5 mm/mm2]; sporangia adaxial on the sporophyll, derived from periclinal divisions of several epidermal cells, wall multilayered [eusporangium]; columella 0; tapetum glandular; gametophytes exosporic, green, photosynthetic; stellate pattern split between doublet and triplet regions of transition zone; placenta with single layer of transfer cells in both sporophytic and gametophytic generations, embryonic axis not straight [root lateral with respect to the longitudinal axis; plant homorhizic].[MONILOPHYTA + LIGNOPHYTA]
Branching ± monopodial; lateral roots +, endogenous, root apex multicellular, root cap +; tracheids with scalariform-bordered pits; leaves with apical/marginal growth, venation development basipetal, growth determinate; sporangia borne in pairs and grouped in terminal trusses, dehiscence longitudinal, a single slit; cells polyplastidic, microtubule organizing centres not associated with plastids, diffuse, perinuclear; male gametes multiflagellate, basal bodies staggered, blepharoplasts paired; chloroplast long single copy ca 30kb inversion [from psbM to ycf2].
Plant woody; lateral root origin from the pericycle; branching lateral, meristems axillary; cork cambium + [producing cork abaxially], vascular cambium bifacial [producing phloem abaxially and xylem adaxially].
EXTANT SEED PLANTS / SPERMATOPHYTA
Plant evergreen; nicotinic acid metabolised to trigonelline, (cyanogenesis via tyrosine pathway); primary cell walls rich in xyloglucans and/or glucomannans, 25-30% pectin [Type I walls]; lignins derived from (some) sinapyl and particularly coniferyl alcohols [hence with p-hydroxyphenyl and guaiacyl lignin units, so no Maüle reaction]; root stele with xylem and phloem originating on alternate radii, not medullated [no pith], cork cambium deep seated; arbuscular mycorrhizae +; shoot apical meristem interface specific plasmodesmatal network; stem with vascular cylinder around central pith [eustele], phloem abaxial [ectophloic], endodermis 0, xylem endarch [development centrifugal]; wood homoxylous, tracheids and rays alone, tracheid/tracheid pits circular, bordered; mature sieve tube/cell lacking functioning nucleus, sieve tube plastids with starch grains; phloem fibres +; stem cork cambium superficial; branches exogenous; leaves with single trace from vascular sympodium [nodes 1:1]; stomatal pore with active opening in response to leaf hydration, control by abscisic acid, metabolic regulation of water use efficiency, etc.; leaves with petiole and lamina, development basipetal, blade simple; axillary buds +, (not associated with all leaves); prophylls two, lateral; plant heterosporous, sporangia borne on sporophylls; microsporophylls aggregated in indeterminate cones/strobili; true pollen +, grains mono[ana]sulcate, exine and intine homogeneous; ovules unitegmic, parietal tissue 2+ cells across, megaspore tetrad linear, functional megaspore single, chalazal, lacking sporopollenin, megasporangium indehiscent; pollen grains landing on ovule; male gametophyte development initially endosporic, lacking chlorophyll, tube developing from distal end of grain, gametes two, developing after pollination, with cell walls; female gametophyte endosporic, initially syncytial, walls then surrounding individual nuclei; seeds "large" [ca 8 mm3], but not much bigger than ovule, with morphological dormancy; embryo cellular ab initio, endoscopic, plane of first cleavage of zygote transverse, suspensor +, short-minute, embryonic axis straight [shoot and root at opposite ends; plant allorhizic], white, cotyledons 2; plastid transmission maternal; ycf2 gene in inverted repeat, whole nuclear genome duplication [zeta duplication], two copies of LEAFY gene, PHY gene duplications [three - [BP [A/N + C/O]] - copies], nrDNA with 5.8S and 5S rDNA in separate clusters; mitochondrial nad1 intron 2 and coxIIi3 intron and trans-spliced introns present.
ANGIOSPERMAE / MAGNOLIOPHYTA
Lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, apigenin and/or luteolin scattered, [cyanogenesis in ANITA grade?], S [syringyl] lignin units common [positive Maüle reaction - syringyl:guaiacyl ratio more than 2-2.5:1], and hemicelluloses as xyloglucans; root apical meristem intermediate-open; root vascular tissue oligarch [di- to pentarch], lateral roots arise opposite or immediately to the side of [when diarch] xylem poles; origin of epidermis with no clear pattern [probably from inner layer of root cap], trichoblasts [differentiated root hair-forming cells] 0, exodermis +; shoot apex with tunica-corpus construction, tunica 2-layered; reaction wood ?, associated gelatinous fibres [g-fibres] with innermost layer of secondary cell wall rich in cellulose and poor in lignin; starch grains simple; primary cell wall mostly with pectic polysaccharides, poor in mannans; tracheid:tracheid [end wall] plates with scalariform pitting, wood parenchyma +; sieve tubes enucleate, sieve plate with pores (0.1-)0.5-10< µm across, cytoplasm with P-proteins, cytoplasm not occluding pores of sieve plate, companion cell and sieve tube from same mother cell; sugar transport in phloem passive; nodes 1:?; stomata brachyparacytic [ends of subsidiary cells level with ends of pore], outer stomatal ledges producing vestibule, reduction in stomatal conductance to increasing CO2 concentration; lamina formed from the primordial leaf apex, margins toothed, development of venation acropetal, overall growth ± diffuse, venation hierarchical-reticulate, secondary veins pinnate, veins (1.7-)4.1(-5.7) mm/mm2, endings free; most/all leaves with axillary buds; flowers perfect, pedicellate, ± haplomorphic, parts spiral [esp. the A], free, numbers unstable, development in general centripetal; P +, members each with a single trace, outer members not sharply differentiated from the others, not enclosing the floral bud; A many, filament not sharply distinguished from anther, stout, broad, with a single trace, anther introrse, tetrasporangiate, sporangia in two groups of two [dithecal], ± embedded in the filament, with at least outer secondary parietal cells dividing, each theca dehiscing longitudinally, endothecium +, endothecial cells elongated at right angles to long axis of anther; (tapetum glandular), cells binucleate; microspore mother cells in a block, microsporogenesis successive, walls developing by centripetal furrowing; pollen subspherical, tectum continuous or microperforate, ektexine columellate, endexine +, thin, compact, lamellate only in the apertural regions; nectary 0; carpels present, superior, free, several, ascidiate, with postgenital occlusion by secretion, stylulus short, hollow, cavity not lined by distinct epidermal layer, stigma ± decurrent, carinal, dry [not secretory]; ovules few [?1]/carpel, marginal, anatropous, bitegmic, micropyle endostomal, outer integument 2-3 cells across, often largely subdermal in origin, inner integument 2-3 cells across, often dermal in origin, parietal tissue 1-3 cells across [crassinucellate], nucellar cap?; megasporocyte single, hypodermal, functional megaspore, chalazal, lacking cuticle; female gametophyte four-celled [one module, nucleus of egg cell sister to one of the polar nuclei]; supra-stylar extra-gynoecial compitum +; ovule not increasing in size between pollination and fertilization; pollen grains landing on stigma, bicellular at dispersal, mature male gametophyte tricellular, germinating in less than 3 hours, pollination siphonogamous, tube elongated, growing between cells, growth rate (20-)80-20,000 µm/hour, apex of pectins, wall with callose, lumen with callose plugs, penetration of ovules via micropyle [porogamous], whole process takes ca 18 hours, distance to first ovule 1.1-2.1 mm; male gametes lacking cell walls, flagellae 0, double fertilization +, ovules aborting unless fertilized; P deciduous in fruit; seed exotestal, much larger than ovule at time of fertilization; endosperm diploid, cellular, heteropolar [micropylar and chalazal domains develop differently, first division oblique, micropylar end initially with a single large cell, divisions uniseriate, chalazal cell smaller, divisions in several planes], copious, oily and/or proteinaceous; dark reversal Pfr → Pr; Arabidopsis-type telomeres [(TTTAGGG)n]; 2C genome size 1-8.2 pg [1 pg = 109 base pairs], whole nuclear genome duplication [epsilon duplication]; protoplasm dessication tolerant [plant poikilohydric]; ndhB gene 21 codons enlarged at the 5' end, single copy of LEAFY and RPB2 gene, knox genes extensively duplicated [A1-A4], AP1/FUL gene, paleo AP3 and PI genes [paralogous B-class genes] +, with "DEAER" motif, SEP3/LOFSEP and three copies of the PHY gene, [PHYB [PHYA + PHYC]].
[NYMPHAEALES [AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]]: wood fibres +; axial parenchyma diffuse or diffuse-in-aggregates; pollen monosulcate [anasulcate], tectum reticulate-perforate [here?]; ?genome duplication; "DEAER" motif in AP3 and PI genes lost, gaps in these genes.
[AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]: vessel elements with scalariform perforation plates in primary xylem; essential oils in specialized cells [lamina and P ± pellucid-punctate]; tension wood +; tectum reticulate; anther wall with outer secondary parietal cell layer dividing; carpels plicate; nucellar cap + [character lost where in eudicots?]; 12BP [4 amino acids] deletion in P1 gene.
[[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]] / MESANGIOSPERMAE: benzylisoquinoline alkaloids +; sesquiterpene synthase subfamily a [TPS-a] [?level], polyacetate derived anthraquinones + [?level]; outer epidermal walls of root elongation zone with cellulose fibrils oriented transverse to root axis; P more or less whorled, 3-merous [possible position]; pollen tube growth intra-gynoecial; embryo sac bipolar, 8 nucleate, antipodal cells persisting; endosperm triploid.
[MONOCOTS [CERATOPHYLLALES + EUDICOTS]]: (extra-floral nectaries +); (veins in lamina often 7-17 mm/mm2 or more [mean for eudicots 8.0]); (stamens opposite [two whorls of] P); (pollen tube growth fast).
[CERATOPHYLLALES + EUDICOTS]: ethereal oils 0.
EUDICOTS: (Myricetin, delphinidin +), asarone 0 [unknown in some groups, + in some asterids]; root epidermis derived from root cap [?Buxaceae, etc.]; (vessel elements with simple perforation plates in primary xylem); nodes 3:3; stomata anomocytic; flowers (dimerous), cyclic; K/outer P members with three traces, ("C" +, with a single trace); A few, (polyandry widespread, initial primordia 5, 10, or ring, ± centrifugal), filaments fairly slender, anthers basifixed; microsporogenesis simultaneous, pollen tricolpate, apertures in pairs at six points of the young tetrad [Fischer's rule], cleavage centripetal, wall with endexine; G with complete postgenital fusion, stylulus/style solid [?here]; seed coat?
[PROTEALES [TROCHODENDRALES [BUXALES + CORE EUDICOTS]]]: (axial/receptacular nectary +).
[TROCHODENDRALES [BUXALES + CORE EUDICOTS]]: benzylisoquinoline alkaloids 0; euAP3 + TM6 genes [duplication of paleoAP3 gene: B class], mitochondrial rps2 gene lost.
[BUXALES + CORE EUDICOTS]: ?
CORE EUDICOTS / GUNNERIDAE: (ellagic and gallic acids +); leaf margins serrate; compitum + [one place]; micropyle?; whole nuclear genome duplication [palaeohexaploidy, gamma triplication], PI-dB motif +, small deletion in the 18S ribosomal DNA common.
[ROSIDS ET AL. + ASTERIDS ET AL.] / PENTAPETALAE: root apical meristem closed; (cyanogenesis also via [iso]leucine, valine and phenylalanine pathways); flowers rather stereotyped: 5-merous, parts whorled; P = calyx + corolla, the calyx enclosing the flower in bud, sepals with three or more traces, petals with a single trace; stamens = 2x K/C, in two whorls, internal/adaxial to the corolla whorl, alternating, (numerous, but then usually fasciculate and/or centrifugal); pollen tricolporate; G , G  also common, when [G 2], carpels superposed, compitum +, placentation axile, style +, stigma not decurrent; endosperm nuclear; fruit dry, dehiscent, loculicidal [when a capsule]; RNase-based gametophytic incompatibility system present; floral nectaries with CRABSCLAW expression.
[SANTALALES [BERBERIDOPSIDALES [CARYOPHYLLALES + ASTERIDS]]] / ASTERIDS ET AL. / SUPERASTERIDS : ?
[BERBERIDOPSIDALES [CARYOPHYLLALES + ASTERIDS]]: ?
[CARYOPHYLLALES + ASTERIDS]: seed exotestal; embryo long.
ASTERIDS / Sympetalae redux? / ASTERIDAE / ASTERANAE Takhtajan: nicotinic acid metabolised to its arabinosides; (iridoids +); tension wood decidedly uncommon; C enclosing A and G in bud, (connate [sometimes evident only early in development, petals then appearing to be free]); anthers dorsifixed?; (nectary gynoecial); G , style single, long; ovules unitegmic, integument thick, endothelium +, nucellar epidermis does not persist; exotestal [!: even when a single integument] cells lignified, esp. on anticlinal and/or inner periclinal walls; endosperm cellular.
[ERICALES [ASTERID I + ASTERID II]]: (ovules lacking parietal tissue) [tenuinucellate].
[ASTERID I + ASTERID II] / CORE ASTERIDS: ellagic acid 0, non-hydrolysable tannins not common; sugar transport in phloem active; inflorescence basically cymose; A = and opposite sepals or P, (numerous, usu. associated with increased numbers of C or G); style short[?]; duplication of the PI gene.
ASTERID I / LAMIIDAE: loss of introns 18-23 in d copy of RPB2 gene.
[GARRYALES [GENTIANALES [[VAHLIACEAE + SOLANALES] [BORAGINALES + LAMIALES]]]]: G , superposed; loss of introns 18-23 in RPB2 d copy.
[GENTIANALES [[VAHLIACEAE + SOLANALES] [BORAGINALES + LAMIALES]]]: (8-ring deoxyflavonols +); vessel
elements with simple perforation plates; nodes 1:1; C forming a distinct tube, initiation late [sampling!]; A epipetalous; (vascularized)
nectary at base of G; style long; several ovules/carpel; fruit
a septicidal capsule, K persistent. Back to Main Tree
Age. Magallón and Castillo (2009) offer estimates of ca 81 m.y. for both relaxed and constrained penalized likelihood datings for this clade - but Vahliaceae are excluded. The age for the same node in Bell et al. (2010) is (96-)87, 83(-77) m.y. (again, Vahlia excluded) or (102-)92, 86(-79) m.y. (Vahlia included), in Bremer et al. (2004) it is ca 108 m.y., in Xue et al. (2012) it is only 60.4 or 57.6 m.y. and Naumann et al. (2013) 80.8(Boraginales excluded)-76.5 m.y., while in Nazaire et al. (2014) it is (102.1-)89.1(-73.3) m.y. - but c.f. topologies.
Evolution. Divergence & Distribution. There are several characters of potential phylogenetic interest in this group. The hydroxycinnamic acid depside, rosmarinic acid, is known from Boraginaceae and Hydrophyllaceae, as well as some Lamiaceae (Mølgaard & Ravn 1988). Lamiales and Boraginaceae have in common similar hydroxycinnamic acid derivatives, i.e. disaccharide esters of rosmarinic/lithospermic/caffeic acids (Mølgaard & Ravn 1988). Oleaceae, Lamiaceae, and Solanaceae have (arabino)xyloglucans and some (galacto)xyloglucan hemicelluloses in the cell wall; the plesiomorphic condition for seed plants is to have (fuco(galacto))xyloglucans (O'Neill & York 2003; Harris 2005), but the sampling is very poor. Boraginaceae have callose plugs in the pollen tube, as do Solanales, but they are both present and absent in Hydophyllaceae, and absent in Heliotropiaceae, Cordiaceae, and monosymmetric-flowered Lamiales (Cocucci 1983). Protein crystals in nuclei are common, but are apparently not known from Avicennia, etc. (Speta 1977, 1979), and information is needed for groups recently moved to Lamiales. Whether or not such crystals characterise both Lamiales and also Boraginaceae s. str. (see also Wagstaff & Olmstead 1997) needs to be confirmed. Although some Boraginaceae have protein bodies in their nuclei, they are of two very different kinds, and many Boraginaceae entirely lack them; there is also variation within Lamiales.
González and Rudall (2010) thought that a bicarpellate gynoecium might be an apomorphy for this clade, and it was perhaps derived from a pseudomonomerous gynoecium like that of Metteniusa (Metteniusaceae) - see also for gynoecial evolution.
Pollination Biology & Seed Dispersal. These lamiids in particular include many large- and monosymmetric-flowered taxa that have dry fruits with many seeds. However, Convolvulaceae, Lamiaceae, and Verbenaceae, for example, have four seeds/fruit at a maximum). But even when each flower has only one or two seeds, these are generally small, indeed, many euasterids have rather small seeds (Linkies et al. 2010).
Plant-Animal Interactions. Nylin et al. (2014) noted that members of all four orders were hosts for nymphalid butterfly larvae, three (Boraginales not included) being "important" hosts - only seven orders in this category were mentioned.
Phylogeny. Relationships in this part of the tree have long been unclear. Bell et al. (2010) suggested the grouping [Lamiales [Gentianales [Boraginaceae + Solanales]]], Lens et al. (2008a: Bayesian analyses) and Magallón and Castillo (2009) that of [Gentianales [Lamiales [Boraginaceae + Solanales]]], and Lens et al. (2008a: maximum parsimony) found the relationships [[Solanales + Gentianales] [Lamiales + Boraginaceae]]. Qiu et al. (2010: mitochondrial genes) did not find Boraginaceae and Gentianales to be immediately associated, although they were not strongly separated, while the two were sometimes linked, if with weak support, by Ruhfel et al. (2014: there were other positions for Boraginales). In general, relationships between Gentianales, Lamiales and Solanales remained uncertain (Albach et al. 2001b; B. Bremer et al. 2002; Janssens et al. 2009, Boraginaceae s.l. not included; J. Li & Zhang 2010). Even an analysis of all 79 protein-coding plastid genes and four mitochondrial genes did not clarify them (Moore et al. 2008) nor did the 17-gene 640-taxon study of Soltis et al. (2011). Finet et al. (2010) found quite good support for a [Gentianales + Solanales] clade, but no Boraginaceae were included.
Weigend et al. (2013b), sampling four plastid loci and 134 taxa (81 Boraginaceae s.l.), found the very weakly supported sets of relationships [Boraginaceae [Lamiales [Solanales + Gentianales]]] (see also Nazaire et al. 2014: Suppl. Fig. 4A, ITS + 4 plastid markers) and [Lamiales [Gentianales [Solanales + Boraginaceae]]] in different analyses. Cassinopsis was strongly supported as sister to the whole lot. On the other hand, Refulio-Rodriguez and Olmstead (2014), sampling 1 mitochondrial and 9 plastid genes and 129 terminals (75 in Lamiales), recovered the relationships [Gentianales [Solanales [Boraginales + Lamiales]]]; the whole clade had very strong support, as did the monophyly of the orders, but bootstrap support for the two nodes along the spine was only moderate (maximum likelihood) or very weak indeed (maximum parsimony). The amount of data analyzed seems to have allowed this improved set of relationships, and there is support enough to use the topology that they found and to explore its morphological, etc., consequences. However, Maia et al. (2014), in one alignment using 18S/26S nuclear ribosomal data, retrieved a polyphyletic Boraginaceae within the Solanales, although support was not strong, while another alignment suggested a clade [Boraginaceae + Gentianales]. One factor driving these conflicting relationships are different signals in nuclear ([Solanales + Gentianales]) and chloroplast ([Solanales + [Lamiales + Gentianales]]) genes (Xi et al. 2014).
The position of Vahlia remains unclear. Magallón and Castillo (2009) and Bell et al. (2010) suggested that it was sister to all other lamiids (except Garryales, etc.) The genus was placed as sister to Lamiales, but with only 63% bootstrap support, by Albach et al. (2001b; see also Lens et al. 2008a: Bayesian analyses; Nazaire & Hufford 2012: plastid genes; Weigend et al. 2013b; Nazaire et al. 2014: Suppl. Fig. 4A), or it links with Boraginaceae in other analyses (Lundberg 2001e; B. Bremer et al. 2002). Only in ndhF analyses was there some support for a linkage with Solanales (Olmstead et al. 1999, 2000; see also Savolainen et al. 2000a; Lundberg 2001e). Refulio-Rodriguez and Olmstead (2014) also found this position, but despite the large amount of data in this study, there was substantial support only in the Bayesian analyses, while in both analyses of combined 18S/26S nuclear ribosomal data, Maia et al. (2014) found remarkably strong - given the weak support for most relationships in their study - support for the position of Vahliaceae as sister to all the other taxa under consideration here. However, the genus is provisionally placed on the Solanales page.
GENTIANALES Berchtold & J. Presl Main Tree.
Route I iridoids [mostly derived from secologanin or secologanic acid], monoterpene indole alkaloids, (O-methylated) flavones and flavonols +, non-hydrolysable tannins [e.g. myricetin] usu. 0; nodes 1:1; glandular hairs 0; pits vestured; nodes?; petiole bundle(s) arcuate; branching from current flush; leaves opposite, joined by a line across the stem, (stipules +), colleters +; (corolla swollen at the apex in bud); pollen orbicules +; ovules many/carpel, endothelium 0; endosperm nuclear. - 5 families, 1118 genera, 16637 species.
Age. Crown-group Gentianales may be some (75-)71, 68(-65) or (68-)64, 61(-57) m.y. old (Wikström et al. 2001: the first age is with Dialypetalanthus sister to the rest, the second ignores D.). Janssens et al. (2009) date them to 79±10.2 m.y.; comparable figures are 108 and 78 m.y. in Bremer et al. (2004). Estimates of crown group ages are (86-)73(-60) (ages in Rubiaceae table) or (75-)52(-35) m.y. (ages in asterid table) in Lemaire et al. (2011b) and (78-)69, 65(-54) m.y. (Bell et al. 2010); Bremer and Eriksson (2009) suggest rather greater ages of (104.7-)90.4(-76.5) m. years.
Note: Possible apomorphies are in bold. However, the actual level at which many of these features, particularly the more cryptic ones, should be assigned is unclear. This is partly because many characters show considerable homoplasy, in addition, basic information for all too many is very incomplete, frequently coming from taxa well embedded in the clade of interest and so making the position of any putative apomorphy uncertain. Then there is the not-so-trivial issue of how ancestral states are reconstructed (see above).
Evolution. Divergence & Distribution. Endress (2011a) suggested that a key innovation in Gentianales was tenuinucellate ovules.
Chemistry, Morphology, etc. For iridoid synthesis, see Jensen et al. (2002) and references. Wink (2008) noted that the enzyme strictosidine synthase, a key intermediary in the formation of the monoterpene indole alkaloids commonly found in this clade, is in fact quite widely distributed in flowering plants. The monoterpene indole alkaloid camptothecin is scattered through Gentianales, e.g. it is found in Opiorrhiza (Rubiaceae), Mostuea (Gelsemiaceae) and Ervatamia (Apocynaceae) (see Lorence & Nessler 2004).
Colleters range from secretory palisade cells surrounding an elongated axis to much smaller, simpler, hair-like structures (some Gentianaceae, Apocynaceae-Asclepiadoideae). They are borne on leaves, the calyx or corolla (Renobales et al. 2001), or even in a ring below the leaves and encircling the stem, as well as in their normal axillary position.
Tapetal variation is considerable, amoeboid tapeta being known from some species of Gentianaceae, Rubiaceae and Apocynaceae (Furness 2008a). Most families have taxa with bi- or tricellular pollen grains; for further discussion, see Williams et al. (2014). There is substantial variation in the presence of the mitochondrial coxII.i3 intron in this clade.
Some information is taken from Rogers (1986: general), Erbar and Leins (1996: corolla development), Conn et al. (1997: general), Jansen and Smets (1998: wood anatomy, 2000: vestured pits), and Vinckier and Smets (2002a, c: orbicules).
Phylogeny. Struwe et al. (1995) suggested that Loganiaceae, even when more narrowly circumscribed, were extremely paraphyletic, with clades including about 1,300 genera and 15,500 species (Rubiaceae, Gentianaceae, Apocynaceae + Asclepiadaceae) coming from within them; they delimited families accordingly. However, B. Bremer (1996a), Potgeiter et al. (2000) and Backlund et al. (2000) and authors since found rather different relationships - Rubiaceae are sister to Loganiaceae, Gentianaceae, Gelsemiaceae and Apocynaceae.
However, relationships between these last four families are still not entirely clear. M. Endress et al. (1996) found the relationships [Gelsemiaceae [Apocynaceae [Strychnaceae + Geniostomaceae (well supported)]], see also B. Bremer and Struwe (1992). In other analyses there is weak support for a relationship between Gelsemiaceae and Apocynaceae (Backlund et al. 2000; Jiao & Li 2007; see also B. Bremer 1999; Rova et al. 2002). However, B. Bremer et al. (2002) and Soltis et al. (2011: sampling) found some support for a sister group pair [Gentianaceae + Apocynaceae], as did Refulio-Rodriguez and Olmstead (2014: not the maximum likelihood analysis); the latter also found the pair [Gelsemiaceae + Loganiaceae], and this topology is provisionally folowed here (see also Struwe et al. 2014: weak support).
Previous Relationships. The circumscription and relationships of Loganiaceae are a key to understanding the both the past and present circumscription and relationships of Gentianales. Classically, Loganiaceae seemed to show relationships with many sympetalous groups, and Bentham (1856) compared a broadly delimited Loganiaceae to a less-wooded area from which obvious forests representing more distinctive families such as Rubiaceae, Solanaceae, etc., had been removed. Loganiaceae in this sense (e.g. Leeuwenberg 1980) had ca 22 genera and 310 species. Of these genera, Buddleja s.l. and Androya (not immediately related), Peltanthera and Sanango (not immediately related), Plocospermum, Nuxia and Retzia, and Polypremum, are now in five or more separate clades in Lamiales (Scrophulariaceae, near Gesneriaceae, Plocospermataceae, Stilbaceae and Tetrachondraceae respectively), while Desfontainia (Desfontainiaceae) is in Bruniales, a campanulid (for references, see those families), so it is not surprising that Loganiaceae seemed to be such a "central" family. Chemical variation within Loganiaceae s.l. strongly supports its break-up (e.g. Jensen 1999). However, Loganiaceae are morphologically quite heterogeneous even in their much more restricted circumscription.
Includes Apocynaceae, Gelsemiaceae, Gentianaceae, Loganiaceae, Rubiaceae.
Synonymy: Apocynales Berchtold & J. Presl, Asclepiadales Berchtold & J. Presl, Chironiales Grisebach, Cinchonales Lindley, Galiales Bromhead, Loganiales Lindley, Lygodisodeales Martius, Rubiales Berchtold & J. Presl, Strychnales Link, Theligonales Nakai, Vincales Horaninow
RUBIACEAE Jussieu, nom. cons. Back to Gentianales
Plant woody; tanniniferous, anthraquinones from shikimic acid; (cork cambium deep-seated); true tracheids +; nodes 1(-3 or more):1(-3 or more), (+ split laterals); crystal sand +/0; secretory sacs widespread; stomata paracytic; lamina vernation usu. flat, stipules interpetiolar (sheathing; intrapetiolar; two pairs; toothed or not), innervated from circumferential vascular ring; inflorescences often thyrsoid, flowers often aggregated; flowers 4- or 5-merous, (heterostyly +); K small, aestivation open, (free), (0), C with early tube formation, C often left-contorted (valvate); ovary inferior, nectary on top, placentation axile (to parietal), style usually well developed, stigma wet or dry; ovules (apotropous), (parietal cells +), (nucellar epidermal cells anticlinally elongated), (endothelium +), (obturator +); megaspore mother cells several, (embryo sacs several, ± haustorial); fruit baccate, drupaceous or capsular, laterally dehiscent, etc., (G largely superior in fruit); seeds 1-many, (pachychalazal; ruminate), exotesta alone persisting, papillate/short hairy or not, cells variously thickened, (mesotestal cells thickened); endosperm cellular or nuclear, often hemicellulosic, embryo straight to curved, (medium), suspensor haustorium + [?all]; n = 11 (10-16).
611[list]/13150 - in four groups below. World-wide, but largely tropical, especially Madagascar and the Andes (map: from Hultén 1958, 1971; Brummitt 2007). [Photo - Flower.]
Age. Antonelli et al. (2009) suggest that divergence within Rubiaceae began (68.8-)66.1(-63) m.y.a., although Bremer and Eriksson (2009) provided rather older dates of (100.8-)86.6(-72.9) m.y.. Crown group ages in Lemaire et al. (2011b) are around (77-)62(-50) m.y., and ages are (60-)56, 55(-51) m.y. in Wikström et al. (2001), (69-)57(-45) m.y. in Bell et al. (2010: note topology), and (87.9-)84.9(-80.8) m.y. in Manns et al. (2012).
Graham (2009) summarized the fossil history of Rubiaceae - there are no certain records from the Cretaceous or Palaeocene, the earliest being vegetative fossils from the Eocene of North America (Roth & Dilcher 1979) which had previously been placed in seven families and four orders. These fossils are a little odd in that Roth and Dilcher (1979), who compared them with members of Cinchonoideae and Ixoroideae, suggested that the stipules on the petiole bases might be single, and at least sometimes they are minutely serrulate, perhaps because of hydathodes on their margins.
1. Rubioideae Verdcourt
Commonly herbs; (cylcotide proteins +), (monofluoracetates +), shikimic-acid derived anthraquinones +, plants Al-accumulators [esp. woody taxa]; (root with superficial cork cambium - Paederia); raphides + [square in transverse section]; hairs septate, articulated; heterostyly esp. common; C often valvate; (pollen grains 3-celled); (ovules campylotropous), (apex of nucellus exposed), integument 1-14 cells across; (megaspore mother cells 2-15), (antipodal cells persist); (testa ca 14 cells across - Schradera; (suspensor haustorium +); loss of atpB promoter.
/7600: Psychotria s. l. (1600), Palicourea (800), Galium (400), Spermacoce (275: inc. Borreria), Oldenlandia (250), Notopleura (210), Hedyotis (200), Rudgea (200), Lasianthus (185), Chassalia (140), Coprosma (105), Argostemma (100), Gynochthodes (95), Margaritopsis (80), Gaertnera (70), Schradera (55), Morinda (40). Worldwide. [Photo - Fruit.]
Age. Bremer and Eriksson (2009) suggested ages of (90.7-)77.9(-65.3) m.y. and Lemaire et al. (2011b) ages of (60-)53(-48) m.y. for crown-group Rubioideae.
Synonymy: Aparinaceae Hoffmannsegg & Link, Asperulaceae Spenner, Cynocrambaceae Endlicher, nom. illeg. Galiaceae Lindley, Hedyotidaceae Dumortier, Houstoniaceae Rafinesque, Hydrophylacaceae Martynov, Lippayaceae Meisner, Lygodisodeaceae Bartling, Nonateliaceae Martynov, Operculariaceae Perleb, Pagamaeaceae Martynov, Psychotriaceae F. Rudolphi, Spermacoceaceae Berchtold & J. Presl, Theligonaceae Dumortier, nom. cons.
Luculia, etc., Cinchonoideae, Ixoroideae: plants woody; route II carboxylated iridoids +, indole alkaloids +; hairs mostly cylindrical; secondary pollen presentation common; exotestal cells with perforations[?].
Age. Manns et al. (2012: HPD estimates) suggest an age of (84.5-)78.5(-71.7) m.y.a. for this node.
2. [Luculia [Acranthera + Coptasapelta]]
3/53: Acranthera (35). Himalayas, China, to Malesia.
Age. Luculia diverged from [Coptosapelta + Acranthera] in the Late Cretaceous (Manns et al. 2012).
[Cinchonoideae + Ixoroideae]: shrubs or trees.
Age. Bremer and Eriksson (2009: Luculia, etc. not included, stem age of this node not the crown age for the family, c.f. Fig. 1) suggested that the split of Ixoroideae and Cinchonoideae was approximately (88.7-)73.1(-58.4) m.y.a.; Manns et al. (2012: HPD estimates) give an age of (84.5-)78.5(-71.7) m.y.a., and Lemaire et al. (2011b: Luculia, etc. not included) an age of (68-)60(-54) m.y.a. - but see below for topological uncertainty around here.
3. Cinchonoideae Rafinesque
Corynanthean and complex indole alkaloids +; (raphides + - Hillieae, Hamelieae); C imbricate, valvate, (right contorted); ovules often numerous, (straight); fruits usu. dry.
/1,500. Timonius (150), Guettarda (80), Rytigynia (70), Fadogia (45). Tropical, predominantly New World.
Age. Bremer and Eriksson (2009) estimated that divergence within Cinchonoideae began (52.5-)38.7(-28.1) m.y.a., Manns et al. (2012: HPD estimates) gave an age of (65.6-)57.4(-50.3) m.y., and Lemaire et al. (2011b) an age of (52-)36(-24) m.y. old - but they also note "more recent stem node ages" of 26 m.y. for Cinchonoideae, all rather confusing. Antonelli et al. (2009) dated crown Cinchonoideae at some (54.6-)51.3(-47.8) m.y..
Synonymy: Catesbaeaceae Martynov, Cephalanthaceae Rafinesque, Cinchonaceae Batsch, Coutareaceae Martynov, Guettardaceae Batsch, Henriqueziaceae Bremekamp, Naucleaceae Wernham
4. Ixoroideae Rafinesque
Subshrubs to trees (herbs); (latex +); (calycophylls +); secondary pollen presentation common; (K lobe/lobes expanded, petal-like); C also valvate (cochleate, open, etc.); (pollen in tetrads), (with buds); (placentation parietal), (stigma not bilobed - e.g. Gardenia); ovule number variable, integument ca 9 cells across; fruits often fleshy; (seed ruminate); embryo medium (short); n = 11.
/4000: Pavetta (400), Ixora (300), Mussaenda (200), Coffea (125), Randia (100), Tricalysia (90), Wendlandia (80), Gardenia (60), Bertiera (55). Pantropical.
Age. Bremer and Eriksson (2009) suggested that crown-group Ixoroideae were some 59.6 m.y. old, while Lemaire et al. (2011b) suggested ages of (60-)55(-51) m.y..
Synonymy: Coffeaceae Batsch, Dialypetalanthaceae Rizzini & Occhioni, nom. cons., Gardeniaceae Dumortier, Hameliaceae Martius, Randiaceae Martynov, Sabiceaceae Martynov
Evolution. Divergence & Distribution. A number of studies have discussed the evolution of Rubiaceae is considerable detail, see e.g. Bremer and Eriksson (2009). Antonelli et al. (2009) thought that Rubiaceae had a boreo-tropical origin and had moved into South America from the Old World via a North Atlantic land bridge; they also date divergences within the South American Cinchonoideae, especially within Isertieae and Cinchoneae. Manns et al. (2012), however, suggested that Ixoroideae and Cinchonoideae originated in South America ca 78.5 m.y.a., with substantial subsequent long distance dispersal - not so much by land bridges - of taxa with both wind- and animal-dipersed seeds. In particular, the palaeotropical [Hymenodictyeae + Naucleeae] probably moved there from the New World in the Eocene (Manns et al. 2012). In apparent long-distance dispersal in the family, the plants involved seem often to have had drupaceous fruits (B. Bremer & Eriksson 1992).
The minimum divergence time of Rubieae has been dated to (37.6-)28.6(-20.2) m.y.a. (Bremer & Eriksson 2009) with the Old World as a possible place of origin (Soza & Olmstead 2010a), although Graham (2009) suggested that Galium is known from rocks at least 55 m.y. old. Coprosma, with around 110 species, may have originated in New Zealand (or perhaps New Guinea) a mere 15-10 m.y.a., whence it was dispersed by animals perhaps some 16 times widely across the Pacific; it seems to have arrived twice in Hawaii, and multiple dispersal events to the one island are common here (Cantley & Keeley 2012; Cantley et al. 2014). Psychotria s.l. represents another major diversification in the New Guinea-Pacific area, with 250+ species there (Andersson 2002; Barrabé et al. 2013 and references). Psychotria s.l. in New Caledonia, with some 85 species, represents a major radiation (Barrabé et al. 2013). Interestingly, relationships were not with the speciose Pacific Psychotria, and most New Caledonian species belonged to a clade that had diversified within the last ca 7 m.y. and that is sister to an Australian clade (Barrabé et al. 2013, q.v. for many dates). Sedio et al. (2013) examined the movement of Palicourea and Psychotria in the New World around about the time of the biotic interchange between North and South America ca 3 m.y.a. and noted that the ecological preferences of taxa that moved did not change, and that in Central America in particular the ecological diversity of these genera was increased by immigrants from South America with ecological preferences other than those of the natives. Tosh (2009) summarized biogeographical studies on Madagascan Rubiaceae, however, looking at relationships in the pantropical Lasiantheae, Smedmark et al. (2014) emphasized how difficult it was to reconstruct biogeographical events if more than one resolution was allowed for nodes whose support was weak - not too much could be said.
Endress (2011a) thought that the inferior ovary of Rubiaceae might be a key innovation.
Ecology & Physiology. Rubiaceae are an important component of the understory vegetation of tropical forests in Malesia and the New World. They are not uncommonly epiphytic, indeed, Rubiaceae represent an appreciable component of the woody epiphytic flora (see also Ericaceae-Vaccinioideae-Vaccinieae). The family is the fourth most speciose in trees recorded from plots throughout the Amazonian forests, but it has disporportionally few (1/277) of the species that make up half the stems 10 cm or more d.b.h. in those forests (ter Steege et al. 2013). Razafimandimbison et al. (2012) looked at the evolution of growth habit in Morindeae; lianes are plesiomorphic, with independent evolution of the self-supporting habit, perhaps connected with diversification of the clade in the neotropics.
Pollination Biology & Seed Dispersal. Many Rubiaceae have rather small flowers but make them attractive to pollinators in a variety of ways. The flowers are often more or less closely aggregated, and Claßen-Bockhoff (1996a) has surveyed the more flower-like inflorescences that are quite common in the family. Taxa like Cephalanthusmany Morindeae and Naucleeae have flowers aggregated into spherical heads, and in Morindeae there has been evolution of simple fruits from mutliple fruits in which the individual fruis are fused (Razafimandimbison et al. 2012). Cephaelis (= Palicourea: Rubioideae) has a condensed inflorescence immediately subtended by paired and coloured inflorescence bracts. Large, coloured calyces (calycophylls) are particularly common in Ixoroideae and help to attract the pollinator. The Old World Mussaenda is an example with large petal-like calyx lobes usually occurring singly on a few flowers in the quite lax inflorescence (the genus may be polyphyletic - see Alejandro et al. 2005) - and see also Nematostylis, while in the New World Warsewiczia has similarly conspicuous individual sepals - and see also Wittmackanthus, Calycophyllum, etc..
In some species of Spermacoce (Rubioideae) the apices of the corolla lobes are incurved and extensively modified, and pollination is explosive (Vaes et al. 2006); palynological variation here is extreme, being almost equivalent to that in the whole of the rest of the family (Dessein et al. 2002). Explosive pollination is also known from Posoquerieae (Ixoroideae), pollen being catapulted onto the pollinating insect; the flowers are monosymmetric and may be inverted (Delprete 2009). Henriquezia has a monosymmetric corolla. Secondary pollen presentation is notably common in Cinchonoideae (Nilsson et al. 1990; Puff et al. 1996; de Block & Igersheim 2001), but it is also quite common in Ixoroideae (e.g. Vanguerieae - Tilney et al. 2011; see also Kainulainen et al. 2013); pollen is presented on tips of the styles. Hundreds of Rubioideae in particular, and overall, perhaps half the whole family (Robbrecht 1988), are distylous, and there have been several reversals to homostyly (Ferrero et al. 2012). Dioecy occurs in a number of neotropical Gardenieae (Ixoroideae) like Randia that have large fleshy fruits (C. Taylor pers. comm.). In Vanguerieae there are apparent reversals to hermaphroditism (Razafimandimbison et al. 2009), and in New World Galium there may have been reversals to polygamy (Soza & Olmstead 2010b).
In South East Asia - and probably elsewhere - Rubiaceae are important food resouces for frugivores because they produce crops of sugar-rich fruits more or less aseasonally (Leighton & Leighton 1983).
Within Rubiaceae there may be a correlation between fruit types, plant habit, and diversification. Thus clades that are shrubs or trees and in which winged seeds are apomorphic, shrubs with animal-dispersed fruits, and herbs with abiotic dispersal (but not winged seeds) are notably speciose (Eriksson & Bremer 1991; B. Bremer & Eriksson 1992). Fleshy fruits may have evolved about twelve times in the family, especially during the Eocene-Oligocene period (B. Bremer & Eriksson 1992), although this figure is likely to be an underestimate, fleshy fruits having evolved at least four times in a New World clade of Galium alone (Soza & Olmstead 2010b, q.v. for other fruit morphologies there); for the evolution of schizocarpous fruits in Psychotria, see Razafimandimbison et al. 2014). In cases of apparent long-distance dispersal in the family, the plants involved seem often to have had drupaceous fruits (B. Bremer & Eriksson 1992).
Plant-Animal Interactions. Rubiaceae are not often eaten by caterpillar larvae of butterflies (Ehrlich & Raven 1964), although some sphingids (Semanophorae) do prefer members of the family (Forbes 1956).
Myrmecodia, Hydnophytum and related Malesian genera (Hydnophytinae) are highly modified epiphytic ant plants. The ants live in chambers in the grossly swollen stem (hypocotyl) base, and nutrients from the material brought in by the ants and stored in chambers with a distinctive morphology are taken up by the plant. Some species have more or less branched spines arising from the root, stem, inflorescence, and even the torn and eaten surfaces of the leaves (Huxley 1978; Jebb 1991; Huxley & Jebb 1991 for the taxonomy of the group). Close associations with ants have arisen several other times in Rubiaceae. Thus there are several myrmecophytic Naucleeae, the ants living in hollowed stems in plants with a much more "normal" appearance than that of many Hydnophytinae; interestingly, some of these myrmecophytic clades have diversified notably slowly and/or have very limited distributions (Razafimandibison et al. 2005).
Psychotria is largely divided up into Old and New World clades. There are hundreds of species of Psychotria s.l. throughout the Pacific, including on Hawaii (Nepokroeff et al. 2003; Givnish et al. 2008b). The genus is abundant throughout Malesia and in New Guinea (Nepokroeff et al. 1999; Andersson 2002), and a Pacific-Malesian clade of Psychotria includes the ant plants Myrmecodia and Hydnophytum mentioned above (Andersson and Nepokroeff et al. have different taxonomies). In a subclade of New World Psychotria (= subgenus Psychotria) older species tend to occupy larger areas than younger species (Paul et al. 2009); c.f. J. C. Willis's "age and area" hypothesis (e.g. Willis 1922), but the conceptual baggage is presumably very different in the former.
Bacterial/Fungal Associations. Bacterial leaf nodules are known from some African species of Psychotria (Rubioideae), and their presence is correlated with development of distinctive colleters (Lersten 1974 and references). Leaf nodulation seems to have originated in mainland taxa which then moved to Madagascar and the Comoros independently, but not to the Mascarenes; nodulation has sometimes been lost, and also independently acquired in the Malagasy P. bullata (Razafimandimbison et al. 2014). Bacteria of the ß-proteobacterium Burkholderia have been isolated from the nodules (van Oevelen et al. 2004). Although Burkholderia is a nitrogen-fixing symbiont in the root nodules of some Fabaceae-Faboideae, early studies failed to detect nitrogen fixation in Psychotria (Miller 1990). Pavetta and Sericanthe also have leaf nodules, for a total of about 440 species with nodules; transmissal of Burkholderia is largely vertical, although there is also horizontal movement, and the association is not of very long standing (Lemaire et al. 2011b). Members of two groups of Burkholderia also grow free in the leaf between mesophyll cells in some African Vanguerieae (Ixoroideae), an association that seems largely specific from the plant's point of view but not from that of the bacteria (Verstraete et al. 2013a, b). The association seems to have evolved three times, although any benefits to the partners are unclear (Verstraete et al. 2013b), all told, some 150 species of Vanguerieae may be involved.
Vegetative Variation. Although most Rubiaceae can be recognised by a distinctive combination of vegetative characters (see above), vegetative variation in the family is quite extensive, even apart from the distinctive morphologies of the myrmecophytic taxa just mentioned. Herbaceousness has evolved most notably in Rubioideae, where some Spermacoceae may be secondarily woody while Knoxeae are both primarily and secondarily woody (Lens et al. 2009a, b). Genipa and Posoqueria have a deeply lobed lamina; "latex" is not uncommon. Anisophylly is well known in the family, occurring also in herbaceous taxa like Theligonum and Argostemma, where it is especially marked in taxa like A. humilis.
Rubiaceae are a classic case of a family with stipules. Stipule morphology and position in general shows considerable variation; there are sometimes two pairs of stipules, one more or less intrapetiolar, the other interpetiolar. Most taxa have 1:1 nodal anatomy, branches of the single traces separating and forming a vascular collar around the stem from which the stipular bundles themselves diverge (Majumdar & Pal 1958). A number of genera are trilacunar (Neubauer 1981; Robbrecht & Puff 1986); this does not seem to correlate with phylogeny. In angiosperms, unilacunar nodes are unusual in taxa with stipules, trilacunar nodes being the norm (Sinnott & Bailey 1914).
The exact nature of the whorled "leaves" of Galium has been a a matter of some dispute. Here there are no clearly distinct stipules, but there are only two opposite branches per node, suggesting that the basic construction of the plant is of paired, opposite leaves; this is confirmed by the pattern of vascularization in most species (e.g. Neubauer 1981). Soza and Olmstead (2010a) found the basic condition in Rubieae to be six leaves per whorl, although there was frequent evolution of four-membered whorls (and even reversal to six again). Taxa like Galium rubioides have four large leaves at the node all of which are directly vascularized from the stele (Rutishauser 1999); this is likely to be a derived condition (Soza & Olmstead 2010a). However, leaves and stipules may develop from different primordia (e.g. Pötter & Klopfer 1987), and it has even been suggested that "leaf-like stipules are independent structures, not part of the leaf" (Soza & Olmstead 2010a). At the same time species like G. paradoxa sometimes have opposite leaves with paired, interpetiolar stipules - and there is similar variation in the unrelated Limnosipanea (C. Taylor, pers. comm.).
Genes & Genomes. Molecular evolution in the herbaceous Rubioideae seems to be speeded up compared to that in the woody members (Rydin et al. 2009b: note the laggard woody Dunnia within the herbaceous clade!).
Chemistry, Morphology, etc. For cyclotide proteins, found in Oldenlandia, Psychotria, and relatives in Rubioideae, see Gruber et al. (2008) and Koehlbach et al. (2013). Petiole anatomy is variable, and although the vascular bundles are often more or less arcuate, in some Ixoroideae they are annular (Martínez-Cabrera et al. (2009).
In some taxa the calyx begins to develop after the corolla, but this is only when the calyx lobes are much reduced; the calyx tube does develop later (de Block & Vrijdaghs 2013). Taxa like the sister genera Gaertnera (see Malcomber 2002) and Pagamea have secondarily superior ovaries (Igersheim et al. 1994). A few Rubiaceae like Theligonum and Dialypetalanthus have more than twice the number of stamens as perianth/sepals/petals (e.g. Endress 2003a; for further discussion, see the euasterids). For pollen variation in the paraphyletic Spermacoce, see Dessein et al. (2005b). There is considerable variation in ovule morphology and development (Maheshwari 1950; de Toni & Mariath 2008, 2010; Figueiredo et al. 2013). Ronse Decraene and Smets (2000) discuss floral development in the family, emphasizing variation in the relative development of a stamen-corolla tube with a common meristem and a corolla tube s.s.; filaments may fuse postgenitally with the corolla tube proper. There is considerable variation in the pattern of thickening of the exotestal cells; as might be expected, taxa with drupaceous fruits have a less well developed exotesta (Robbrecht & Puff 1986).
For additional information on Rubiaceae, see Verdcourt (1958), Robbrecht (1988, 1993), Robbrecht et al. (1996), and Rogers (2005), all general, for alkaloids, see Aniszewski (2007) and Berger et al. (2012), for Al and Si accumulation, see Jansen et al. (2002a, 2003), and for toxic monofluoracetates, see Lee et al. (2012); also see Koek-Noorman & Hogeweg (1974), Koek-Noorman (1977), Martínez-Cabrera et al. (2010), and León H. (2013), all wood anatomy, Rutishauser (1984: stipules), Gamalei et al. (2008: phloem), and Lersten and Horner (2011: calcium oxalate crystal morphology in Naucleeae [Cinchonoideae], interesting variation). See also Weberling (1977: inflorescences), Rogers (1984: Gleasonia, etc.), Puff et al. (1993a: pollen, fruits in Mussaenda et al., 1993b, much detail about Schradereae), Martínez-Cabrera et al. (2013: floral morphology of Hamelieae, etc.), Huysmans et al. (1997: orbicules in Cinchonioideae), Vinckier et al. (2000: orbicules in Ixoroideae), Verstraete et al. (2011: orbicules, not integrated with earlier observations?), Delprete (2004: morphology), Dessein et al. (2005a) and Verellen et al. (2007), both pollen, not really a great help taxonomically, Rakotonasolo and Davis (2006: some odd placentation types), Lloyd (1899, 1902: embryology), Fagerlind (1937: embryology and much else), Takhtajan (2013: esp. seeds), and for chromosomes of Rubioideae, see Kiehn (2010).
Phylogeny. B. Bremer (2009) summarizes phylogenetic work on the family (see also Bremer 1996b). The basic phylogenetic structure is [Rubioideae [[Luculia [Acranthera + Coptasapelta]] [Cinchonoideae + Ixoroideae]] (see B. Bremer 1995, 1999; Rova et al. 2002; Robbrecht & Manen 2006; Rydin et al. 2009a; etc.). The clade of Luculia and Coptosapelta - and now Acranthera - seems moderately well supported. However, Bremer and Eriksson (2009) suggest that the three may not form a single clade, and while they do form a clade in Manns et al. (2012), it is sister to Rubioideae. Refulio-Rodriguez and Olmstead (2014) found moderate support for the placement of Luculia as sister to the other four Rubiaceae they examined (these included representatives of all three subfamilies).
Luculia and Coptasapelta are not close morphologically: As Robbrecht and Manen (2006) emphasize, these two genera differ in having, as in Coptosapelta, or not, as in Luculia, raphides, accumulating (or not) aluminium, having T-shaped hairs (not), pororate, acolumellate (tricolporate) pollen grains, and distyly (secondary pollen presentation) (Verellen et al. 2004; for pollen presentation, see Puff et al. 1996). Although Acranthera may be sister to Coptasapelta (see also Bremer & Eriksson 2009), these two also have little morphologically in common (Rydin et al. 2009a). Thus assigning polarity to many features in the family becomes rather tricky.
Within Rubioideae, relationships are becoming clarified. Opiorrhiza has the atpB promoter region that is lacking in other Rubioideae (Manen & Natali 1996; Natali et al. 1996) and was thought to be sister to the rest of the subfamily. Rydin et al. (2009a) found it was close to Urophylleae, mainly because of support from ITS, not chloroplast genes, and relationships between major clades in Urophylleae are clarified by Smedmark and Bremer (2011: note, species-level relationships unclear). Sister to the whole of Rubioideae, and with strong support, is the monotypic African genus Colletoecema (Piesschart et al. 2000: near basal, but actual position uncertain; esp. Rydin et al. 2009a); does it have an atpB promoter region? Rydin et al. (2008) discuss the placement of some other small and little-kmown genera of Rubioideae; they considerably affect our understanding of the evolution and diversification of the clade. Both morphology and molecular data strongly support the monophyly of Rubieae (Rogers 2005 for literature). There is now considerable phylogenetic resolution within the tribe, with relationships between seven strongly-supported (both bootstrap and posterior probabilities) major clades themselves being well supported (Soza & Olmstead 2010a, also 2010b for New World Galium; see also Manen & Natali 1995; Manen et al. 1994; Natali et al. 1996). De Toni and Mariath (2011) found that flowers and fruits suggested that Galium and Relbunium were sister taxa and both worthy of generic status. However, Soza and Olmstead (2010b) noted that their fleshy fruits were distinctive (but not unique) in Galium, and the Relbunium group is embedded in a larger South American clade that is firmly part of Galium.
Relationships within the ca 1000 species of Spermacoceae are a major problem area. Kårehed et al. (2008) investigated the phylogeny of Spermacoceae; they suggested that Hedyotis was to be resticted to Asian taxa; further studies were carried out by Groeninckx et al. (2009a, esp. 2009b), Rydin et al. (2009b) and Guo et al. (2013: Asian taxa), while Wikström et al. (2013) is another important step forwards. Psychotria and relatives also pose problems. The Psychotria and Palicourea complexes are sister taxa, and the former, often having caducous stipules, is largely divided into Old and New World clades, while the latter includes some species of Psychotria. A Pacific-Malesian clade of Psychotria includes myrmecophytes as well as genera like Amaracarpus (Nepokroeff et al. 1999; Andersson 2002: the important optimisation of marginal preformed germination slits on the pyrenes is questionable); Cephaelis groups with Palicourea, and overall there is considerable geographical signal in the clades. Barrabé et al. (2012) focused on relationships of a clade of the Palicourea group, the Malesian-Pacific-American Margaritopsis, while Smedmark et al. (2015) examined relationships within the pantropical Lasiantheae.
For further information on the phylogeny of Rubioideae, see Andersson and Rova (1999), B. Bremer and Manen (2000: phylogeny and classification in Rubioideae), Backlund et al. (2007), Kårehed and Bremer (2007: Knoxieae), Smedmark (2008: Urophylleae), and Razafimandimbison et al. (2008: relationships around Psychotrieae, many-seeded carpels evolve from one-seeded carpels in Schradereae, esp. 2014). Morinda, with its distinctive capitate inflorescences and compound fruits, is in fact polyphyletic (Razafimandimbison et al. 2009b, 2012).
For phylogenetic relationhips within Cinchonoideae, see Andreasen and Bremer (1996), Rydin et al. (2009), and especially Manns et al. (2012) and Manns and Bremer (2010); the latter recognise nine tribes within the subfamily, all of which are strongly supported as being monophyletic, however, some of the relationships between groups of tribes are as yet poorly resolved (Manns & Bremer 2010). For relationships within these tribes, see Manns and Bremer (2010) and Manns et al. (2012), also, within Vanguerieae, see Lantz and Bremer (2005) and references and Razafimandimbison et al. (2009). For relationships in Sabiceeae, see Khan et al. (2008). [Naucleeae + Hymenodictyeae] are a well supported clade sister to the only moderately (jacknife) supported remainder of Cinchonoideae (Andersson & Antonelli 2005: Luculia and Coptasapelta excepted); see also Razafimandimbison & Bremer (2002) and especially Löfstrand et al. (2014) for Naucleeae and Hymenodictyeae.
The six-plastid gene study of Kainulainen et al. (2013: Dialypetalanthus not included) has provided substantial support for relationships throughout Ixoroideae, although those in the "basal" Condamineeae-Mussaendeae area remain somewhat unclear, as do those in the Pavetteae area. Condamineeae as circumscribed by Kainulainen et al. (2010) are very heterogeneous and include Mastixiodendron, the morphologically even more distinctive Dialypetalanthus (see also Feng et al. 2000), several genera with calycophylls, etc. For the circumscription of Coffeeae, see A. Davis et al. (2007), Maurin et al. (2007) and Novak et al. (2012) for the phylogeny and biogeography of Coffea. Razafimandimbison et al. (2011) found that at the base of the clade encompassing the ca 1100 species of Vanguerieae there were successively four monogeneric clades (three in Kainulainen et al. 2013, Glionettia unplaced); see Razafimandimbison et al. (2009a) for the phylogeny of dioecious Vanguerieae. Relationships within the old Gardenieae are becoming clarified, and Pavetteae, Gardenieae, and two small tribes may form a clade, although without bootstrap support (Mouly et al. 2014: chloroplast data); Alejandro et al. (2011) look at relationships within Octotropideae. Ixora (Ixoridinae) is paraphyletic (Mouly et al. 2009a, b, see also Andreasen & Bremer 2000; Tosh et al. 2013: Afro-Madagascan species). Tosh et al. (2009) have adjusted the limits of the African Tricalysia (see also Tosh 2009), Cortés-B. et al. (2009) looked at Retiniphylleae and Kainulainen et al. (2009) at Alberteae. Sipanea and Posoqueria form a basal clade (Razafimandimbison et al. 2011; Mouly et al. 2014). The Madagascan Melanoxerus (Gardenieae) links with African taxa in plastid and ribosomal analyses, neotropical taxa in nuclear gene analyses (Kainulainen & Bremer 2014).
Two genera are particularly odd morphologically:
Classification. Robbrecht and Manen (2006) and B. Bremer (2009) should be consulted for a detailed discussion on taxon limits, formal classification, and the like. Manns and Bremer (2010) provide a tribal classification of Cinchonoideae and assign nearly all genera to those tribes, at least provisionally. There is a tribal classification of Ixoroideae in Kainulainen et al. (2013) where genera in 21 of the 24 tribes are enumerated; one genus (Glionettia) is unplaced. See Govaerts et al. (2013) for a World Checklist of Rubiaceae.
Bremer (2009) noted that of the ca 611 genera in the family, 1/3 were monotypic - and some are very large and are turning out to be paraphyletic. Not surprisingly, generic limits are problematic in a number of places, indeed, if preserving the names of these small genera seems desirable, then wholseale dismemberment of larger genera and ever more small genera will be the logical if unfortunate result. Within Rubieae, the circumscriptions of both Asperula and Galium are currently a mess (Soza & Olmstead 2010a). Spermacoceae are very difficult with both considerable lumping and considerable splitting having occurred in the past. Oldenlandia appears to be wildly polyphyletic, and Spermacoce very paraphyletic (Kårehed et al. 2008; Groeninckx et al. 2009a, esp. 2009b; Wikström et al. 2013), and new genera are unfortunately being described in the context of local phylogenetic analyses (Groeninckx et al. 2010a, b). Thus Guo et al. (2013) described three new genera from the Asian part of the Spermacoce complex, but another 10-17 names (several already exist) will then be needed to describe this part of the tree alone. For generic limits in Urophylleae, see Smedmark and Bremer (2011: nine of Bremekamp's small genera still unsampled). Generic limits around the polyphyletic Morinda have been adjusted (Razafimandimbison et al. 2009). A Pacific-Malesian clade of Psychotria also includes myrmecophytes like Myrmecodia and Hydnophytum as well as genera like Amaracarpus (Andersson 2002); Andersson (2002) seemed inclined to split the clade, while e.g. Nepokroeff et al. (1999) and particularly Razafimandimbison et al. (2014) would include them in Psychotria s.l.. The limits of Ixora have been formally adjusted (Mouly et al. 2009a, b), while Coffea is to include Psilanthus (Maurin et al. 2007). Generic and tribal limits are diffficult around Rondeletieae and Guettardeae (Rova et al. 2009); Guettarda itself is polyphyletic (Achille et al. 2006). See Löfstrand et al. (2014) for a discussion on generic limits in Naucleeae. In Galium in particular, fruit morphology is a poor indicator of sectional relationships (Soza & Olmstead 2010b; see also Abdel Khalik et al. 2009).
Previous Relationships. Rizzini and Occhioni (1949) were sure Dialypetalanthaceae were in Myrtales, while Cronquist (1981) placed Dialypetalanthaceae adjacent to Pittosporaceae in his Rosales, and Theligonaceae was in his Rubiales. Both families were also maintained as separate by Takhtajan (1997) but were included in Rubiales.
Thanks. I am grateful to Elmar Robbrecht for help with the synonymy and to Charlotte Taylor for many useful comments.
[[Loganiaceae + Gelsemiaceae] [Gentianaceae + Apocynaceae]]: route I secoiridoids +; internal phloem + [bicollateral vascular bundles]; K valvate or imbricate; C tube formation late; syncarpy postgenital; testa with anticlinal walls thickened.
Age. Bell et al. (2010) give an age of (69-)61, 57(-47) m.y. for this clade, although relationships within it are very different from those followed here.
Chemistry, Morphology, etc. Bouman and Schrier (1979) noted that exotestal cells with thickenings on their anticlinal walls are common around here; Gelsemiaceae and Loganiaceae were not mentioned.
[Loganiaceae + Gelsemiaceae]: quercetin, kaempferol +; C imbricate; placentation axile; endosperm horny (starchy/hemicellulosic).
Phylogeny. Backlund et al. (2000) noted that C17 indole alkaloids, the number of tapetum layers, and cytology supported the relationship [Gelsemiaceae + Apocynaceae], but that the presence of quercetin and kaempferol, imbricate corolla, and horny (starchy) endosperm might support a close relationship between Gelsemiaceae and Loganiaceae.
LOGANIACEAE Martius, nom. cons. Back to Gentianales
Annual herbs to shrubs or lianes; tryptophane-derived alkaloids +; nodes also 3:3 (and split laterals); stomata?; lamina vernation ± flat, (secondary veins palmate), (sheathing stipule +); flowers 4- or 5-merous, (median K abaxial - Logania), (monosymmetric - Usteria); K basally connate or not, (C also contorted, quincuncial), often hairy at the mouth; (A 1, abaxial - Usteria); tapetum (amoeboid), polyploid [Strychnos]; pollen grains tricellular [?all]; nectary 0, poorly developed, or on walls of G; G collateral, (-5), often partly inferior and partly apocarpous (congenitally syncarpous), (placentae massive), (stylar fusion postgenital), styles branches +/0, stigma capitate, long-clavate, 2-lobed, or punctate; ovules (1-)many/carpel, epitropous [?always], integument 4-6 cells across; fruit a follicle, loculicidal and/or septicidal capsule, drupe or berry; (placentae fleshy - Gelsemium), (seeds embedded in pulp), seeds ruminate - Spigelia); exotestal cells papillate or hairy, ± thick-walled and lignified except outer wall; n = 10, 12, 16; seedings epigeal and phanerocotylar.
13[list]/420: Strychnos (190), Mitrasacme (55), Geniostoma (55). Pantropical, esp. Australia and New Caledonia (map: from Leenhouts 1962; van Steenis & van Balgooy 1966; Leeuwenberg 1969). [Photo - Flower, Fruit]
Chemistry, Morphology, etc. The wood of Strychnos has included phloem; the plant has branch tendrils.
Colporate pollen without lateral extensions at the endocolpus is reported to be a character restricted (in this group) to Strychnos and its immediate relatives. The ovules of Mitrasacme have an endothelium and the endosperm is "intermediate" in development, while Mitreola oldenlandioides has straight ovules and cellular endosperm (Reddy et al. 1999). The herbaceous Spigelia is distinctive. Its leaves are often pseudoverticillate; the inflorescence is a cincinnus; it has late corolla tube formation; and its fruit is a septicidal+loculicidal capsule, the valves all falling off.
For information, see Leeuwenberg (1980: general), Aniszewski (2007: alkaloids), Keller (1996: "stipules"), Hasselberg (1937: nodes and stipules), Dahlgren (1922), Bendre (1975) and Maheshwari Devi and Lakshminarayana (1960: ?Strychnos with an endothelium), all embryology, and, Hakki (1998: Usteria).
Phylogeny. For relationships in Loganieae, see Gibbons et al. (2012); generic limits will have to be adjusted.
Synonymy: Antoniaceae Hutchinson, Gardneriaceae Perleb, Geniostomataceae L. Struwe & V. Albert, Spigeliaceae Berchtold & J. Presl, Strychnaceae Perleb
GELSEMIACEAE L. Struwe & V. Albert Back to Gentianales
Trees, shrubs or lianes; quercetin, kaempferol +; true tracheids +; stomata?; (leaves spiral), (margins serrate), (stipules 2, interpetiolar or short sheathing); (flowers single); flowers heterostylous (not); A latrorse (extrorse - Gelsemium); pollen pores with distinct lateral extensions [?level], surface striate to reticulate; ?nectary; (G stipitate - Pteleocarpa), style twice (once) branched, stigma puctate (capitate); (ovules 2/carpel); fruit a loculicidal and/or septicidal capsule, (muricate), (1-seeded samara - Pteleocarpa), K usu persistent; seeds winged or hairy, flattened, or rugose, (not); testa?; n = 8, 10.
2[list]/11. ± Pantropical (map: from Leeuwenberg 1961; van Steenis & van Balgooy 1966; Sobral & Rossi 2003). [Photo - Gelsemium Collection © M. Dirr, Flower (Pin), Flower (Thrum).]
Evolution. Divergence & Distribution. For the phylogeny and biogeography of the family (Pteleocarpa not included), see Jiao and Li (2007).
Chemistry, Morphology, etc. Vascular pits in Gelsemium are not vestured (Rogers 1986), those of Pteleocarpa are. The latter also has mainly apotracheal parenchyma in unilateral, uniseriate bands and fibre tracheids with bordered pits (Gottwald 1982).
How nectar is secreted in Pteleocarpa is unclear (Struwe et al. 2014).
Phylogeny. The association of Pteleocarpa with this clade is strongly supported Refulio-Rodriguez and Olmstead (2014) suggested that it was sister to the two other genera, Struwe et al. (2014) did not place it.
Classification. Although Pteleocarpa is a distinct genus - Brummitt (2007) recognized it as a separate family, describing it formally later (Brummitt 2011) - it is best included in Gelsemiaceae (see Struwe et al. 2014).
Previous Relationships. Pteleocarpa has been included in Boraginaceae-Ehretioideae, e.g. by Takhtajan (1997); the other genera are ex Loganiaceae.
Synonymy: Pteleocarpaceae Brummitt
[Gentianaceae + Apocynaceae]: monoterpene indole alkaloids; (interxylary phloem); C contorted; testa multiplicative,
Age. The age of this clade is around 62 m.y. (Naumann et al. 2013).
GENTIANACEAE Jussieu, nom. cons. Back to Gentianales
Herbs to shrubs (trees), mycorrhizal (and echlorophyllous); (plants Al-accumulators); starch 0, oligosaccharides +, tannins 0; cork?; (vessel elements with scalariform perforation plates); rays often 0; parenchyma septate; nodes 1:3 (3 or more:3 or more), (+ split laterals); mucilage cells + (0); plant glabrous; (stomata anisocytic); leaves sessile, usu. connate basally, lamina vernation variable, secondary veins ± palmate (pinnate); flowers 4-5-merous, "disc-like" structure between K and C, C right-contorted, marcescent, (tube formation intermediate), petal epidermal cells elongated and flat; A basally connate, (extrorse), (placentoids +); tapetum (amoeboid), cells uninucleate; nectary 0; G ?collateral, style often short, stigma broadly 2-lobed (capitate), wet; funicle with at best poorly developed vascular tissue, integument 2-20 cells across, (outer epidermal cells early massive), hypostase +; (antipodal cells diploid to polyploid), (multiplying, persistent); fruit a septicidal capsule, calyx often prominent; seeds small to minute; exotestal cells (± elongated), inner walls variously thickened (not), other layers ± disappear; embryo white or green; 100 bp deletion in trnL gene.
88[list]/ca 1675 - 7 tribes below. World-wide, but especially temperate (map: from Gillett 1963; Hultén 1958, 1971; van Steenis & van Balgooy 1966; Klackenberg 1985; Ho & Liu 2001; Struwe & Albert 2004; Kissling 2012). [Photo - Flower, Flower.]
Age. The crown age of the family may be some 50 m.y. (Yuan et al. 2003) or (78.6-)66.2, 57.8(-47.3) m.y. (Merckx et al. 2013).
Although fossils with pollen like that of Macrocarpaea are reported from the Eocene ca 45 m.y.a., their identity is questionable (Stockey & Manchester 1985; Struwe et al. 2002).
1. Saccifolieae Struwe, Thiv, V. A. Albert & Kadereit
(Echlorophyllous myco-heterotrophic herbs), (shrubs); ?chemistry; (leaves spiral); flowers (heterostylous), (4-)5(-6)-merous; placentation parietal; (dust seeds +); (endosperm cellular - Voyriella), (cotyledons 0); n = 10-14.
4/19. tropical South America, Panama.
Synonymy: Saccifoliaceae Maguire & Pires
[Exaceae [Voyrieae [Chironieae [Potalieae [Helieae + Gentianeae]]]]]: ?
Age. This node was date to some (57.4-)49.1, 48.6(-40.1) m.y. by Merckx et al. (2013).
2. Exaceae Colla
(Echlorophyllous myco-heterotrophic herbs); (flowers monosymmetric/enantiostylous - Exacum, Orphium); (median petal adaxial); K connate or not, usu. prominently keeled; petal epidermal cells rounded and convex; (anther with appendages), (endothecium 0 - Exacum); ovary ± bilocular; (ovule straight), (endothelium + - Exacum); anticlinal walls of exotestal cells sinuous or not; x = 7, n = 9, 11, 15, etc.
8/165: Exacum (70, inc. Cotylanthera), Sebaea (65). Africa, esp. Madagascar, Indo-Malesia, and to Australia and New Zealand (some Sebaea).
[Voyrieae [Chironieae [Potalieae [Helieae + Gentianeae]]]]: placentation parietal, (placentae bilobed).
Age. The age of this node was estimated at (65.2-)54.0, 46.8(-40.1) m.y. (Merckx et al. 2013).
3. Voyrieae Gilg
Small, echlorophyllous myco-heterotrophic herbs; ?chemistry; axis may lack nodes but bear roots and shoots; roots and shoots both exogenous, or both endogenous; vascular bundles separate; (leaves not connate basally), colleters +/0; (A extrorse); pollen variously clumped, (asymmetric), 1-6-porate, exine smooth to scabrate, orbicules 0; placentae strongly bilobed, stigma expanded, infundibular; ovules straight, no integument, or anatropous, one integument, endothelium +, nucellar cap +; seeds dust-like, embedded in the swollen placenta or not; exotesta +; endosperm cellular or initially nuclear, present to almost absent, embryo undifferentiated; n = 16-20.
1/19. Tropical America, Voyria primuloides in Africa (map: from Maas & Ruyters 1986; Raynal-Roques 1967).
[Chironieae [Potalieae [Helieae + Gentianeae]]]: xanthones, L-(+)-bornesitol +; (interxylary phloem +).
4. Chironieae Endlicher
(Shrubs); distinctive 6-substituted xanthones; flowers (2-)4-5(-12)-merous; K connate, (pollen in tetrads); n = 10, 13-15, 17, etc.
23/159: Centaurium (50). Tropics and warm N. temperate.
Synonymy: Chironiaceae Berchtold & J. Presl, Coutoubeaceae Martynov
[Potalieae [Helieae + Gentianeae]]: nectary +.
5. Potalieae Reichenbach
Trees to lianes or herbs; C-glucoflavones +; nodes 5 or more:5 or more; epidermal and cortical sclereids + [?all]; (massive sheathing stipule-like structure); flowers 3-16(-24)-merous; K basally connate; pollen porate; syncarpy congenital [?all]; (fruit a berry); n = ?
13/154: Fagraea (75), Lisianthus (30). Pantropical.
Synonymy: Potaliaceae Martius
[Helieae + Gentianeae]: ?
6. Helieae Gilg
(Shrubs); vessels often in multiples; (inter/intrapetiolar sheaths, stipules +); flowers (4-)5(-6)-merous; (corona at adaxial base of A); pollen usu. in tetrads, polyads; style often long, twisted and flattened when dry; n = ?
22/205: Macrocarpaea (110), Symbolanthus (30). Tropical Central and South America, Caribean.
7. Gentianeae Colla
Distinctive xanthones, C-glucoflavones +, (fructans/inulin +); (nectary on C - Swertia et al.); style often short or 0; (antipodal cells multinucleate - Halenia); seeds larger; n = ³5, very variable.
17/950: Gentiana (360), Gentianella (250: polyphyletic), Halenia (80), Swertia (135: ?polyphyletic). North temperate, to the Celebes (some Tripterospermum) and Africa and Madagascar (some Swertia).
Synonymy: Obolariaceae Martynov
Evolution. Divergence & Distribution. Merckx et al. (2013) give other dates, etc., for the family. Since Voyria primuloides, the only African species of the otherwise neotropical genus, diverged from the others somewhere between 28-12 m.y.a., LDD across the Atlantic is probably responsible for its disjunction (Merckx et al. 2013). Von Hagen and Kadereit (2001) suggested that Gentianella moved into South America from the north and diversified considerably in the Andean region; there are ca 170 species in South America, of which ca 48 are restricted to the páramo (Sklenár et al. 2011), versus 42 in the whole of the northern hemisphere. From the Andes it moved on to New Zealand by long distance dispersal. There was an increase in diversification of Halenia only after it moved into Central and South America within the last 1 m.y., not when it first acquired spurs; there were three separate colonizations of South America. The genus may originally have been from Central or East Asia, and its stem group age is ca 11.8 m.y. (von Hagen & Kadereit 2003). The wide distribution of Exacum was also probably attained by dispersal (Yuan et al. 2005).
Ecology & Physiology. Root hairs are generally absent in Voyria, but they are present in V. primuloides and also in V. aphylla where its roots abut those of other plants and also litter; fungal penetration occurs in the former situation (Imhof 1999). Even if the roots of these other plants are described as being decomposed, this is apparently only locally, and carbon exchange may occur (Imhoff 1999), so perhaps parasitism occurs.
Both autotrophic and myco-heterotrophic species are found in genera like Exochaenium and Exacum; Voyriella is another myco-heterotroph. Some species of Exochaenium may be parasites (Kissling 2012). It is interesting that myco-heterotrophic taxa have evolved in the three basal clades in the family (Merckx et al. 2013).
Pollination Biology. Swertia and other Gentianeae sometimes have fimbriate appendages and nectaries on the petals. Halenia has flowers with five nectar spurs, uncommon in angiosperms (von Hagen & Kadereit 2003). Sebaea s. str. has a pair of collateral secondary stigmas at the base of the style (Kissling et al. 2009b), apparently unique in the angiosperms.
Pollination of the myco-heterotrophic Voyria is mostly by bees. The pollen is clumped, the clumps being held together by the tubes of pollen grains that have already germinated and/or by secretions from the anthers; the anthers are borne close together around the style or stigma (Hentrich 2008; Hentrich et al. 2010a).
Bacterial/Fungal Associations. Paris-type endomycorrhizae involving Glomeromycota are common in Gentianaceae, including the myco-heterotrophic members (Imhoff 1999; Franke et al. 2006).
Chemistry, Morphology, etc. The plants are often bitter-tasting because of the iridoids they contain, while Exacum may be foetid. Flavone-O-glycosides are known from two species of Exacum, alone in the family. The wood of Helieae shows paedomorphic characteristics (Carlquist & Grant 2005). 1:3 nodes are scattered through the family, e.g. Exacum, Gentiana and Sabatia. Although Gentianaceae are not supposed to have stipules, Potaliinae in particular, and especially Fagraea, have inter/intrapetiolar sheaths and auriculate structures at the nodes; for the diversity of stipule-like structures in Macrocarpaea (Helieae), see Grant and Weaver (2003).
Corolla tube formation for some taxa has been described as being late-early. Exacum has an imbricate corolla (and calyx), and the flower is monosymmetric because of the orientation of the androecium and style and curvature of the pedicel (Ronse de Craene 2010). There are sometimes two almost stamen-like appendages on either side of the ovary of Voyria, perhaps modified nectaries. Gentiana has ovules over almost the entire inner surface of the loculus. An endothelium is sometimes reported from Gentianaceae (Kapil & Tiwari 1978), however, as Shamrov (1996) describes this, it consists of one or two layers of cells of the integument that are elongated periclinally, not more or less anticlinally enlarged, as is common. The multiplicative integument of Orphium frutescens it is about 6 cells across at anthesis (Hakki 1999). The considerable variation in integument thickness in the family needs to be put into a phylogenetic context.
Cotylanthera (= Exacum) has straight, ategmic ovules, as have some Voyria. The polarity of the embryo sac in such cases is reported to have been inverted 180o, the egg cell being near the chalaza (Bouman et al. 2002). However, it is perhaps more likely that the ovule is anatropous, but the ovules are so highly reduced that few landmarks are left to be able to tell. The funicles of these taxa also lack vascular tissue (Bouman et al. 2002). The embryos of some of these taxa have very reduced cotyledons. From illustrations in Johow (1895) there appear to be two parietal cells in Voyria, and although he emphasized that the embryo sac developed from the uppermost (micropylar) megaspore, he illustrated the lowermost cell in that role.
Potalieae-Potaliinae are timber trees (secondarily woody?) with multilacunar nodes and cortical sclereids; the flowers of Anthocleista and Potalia are up to 16-merous (for further discussion, see the euasterids), the corolla is deciduous, the pollen porate, carpellary fusion is congenital, and the fruits are berries. Young plants of Anthocleista have leaves over 2 m long. The group is palynologically heterogeneous (Nilsson et al. 2002).
For general information about Gentianaceae, see Wood and Weaver (1982), Struwe and Albert (2002), Struwe et al. (2002), and the Gentian Research Network, for information on chemistry, see Jensen and Schripsema (2002); for nodal anatomy, see Post (1958); for seeds, Bouman and Devente (1986) and Bouman et al. (2002); general embryology, see Maheswari Devi (1963) and Hakki (1997); for ovule development, etc., see Stolt (1921: variation of integument thickness within Gentiana; postament or basal projection of embryo sac), Shamrov (1996), Bouman and Schrier (1979), Bouman et al. (2002), and Vijayaraghavan and Padmanaban (1968); for orbicules, see Vinckier and Smets (2000a); for pollen, see Nilsson (2002), Nilsson et al. (2002) and Chassot and von Hagen (2008: Swertia); and for the gynoecium, see Shamrov and Gevorkyan (2010b).
For the morphology, etc., of myco-heterotrophic taxa, see Oehler (1927); for information on Voyria in particular, see Johow (1885, 1889: anatomy, seed, etc.), Maas and Ruyters (1986), Bouman and Devente (1986), Bouman and Louis (1990) and Bouman et al. (2002), seed, the latter also ovules, and Franke 2002 (Voyria flavescens).
We need basic anatomical, chemical and developmental knowledge of Saccifolieae, Exaceae and Voyrieae if the evolution of Gentianaceae is to be understood.
Phylogeny. Relationships between some of the tribes are still not well supported (Molina & Struwe 2009; Merckx et al. 2013), in particular, the position of Voyria remains somewhat uncertain - it may have diverged before Exaceae, not after it, as suggested above. Indeed, although there is evidence from pollen, etc., that Voyria is not particularly similar to the myco-heterotrophic Voyriella, etc., its immediate relationships are unclear, although it has bicollateral vascular bundles like many other Gentianales in this part of the tree. See Albert and Struwe (1997) for a morphological phylogenetic analysis of Voyria. The Guayanan Saccifolium, with its distinctive ascidiate leaves, is in a clade with the myco-heterotrophic Curtia, Voyriella, etc., that is sister to all other Gentianaceae (Thiv et al. 1999; Struwe et al. 2002; see also Refulio-Rodriguez & Olmstead 2014, c.f. Struwe et al. 1998); the glandular bodies in the leaf axils of Saccifolium are best interpreted as colleters.
For the phylogeny of Exaceae, see Yuan et al. (2003) and Kissling et al. (2009a: Sebaea s.l. is paraphyletic). For relationships in neotropical Helieae, see Struwe et al. (2009). Relationships within Fagraea (Potalieae) have recently been clarified, and the variation in tree architecture there makes more sense (Wong & Sugumaran 2012). Within Gentianeae, Gentianella seems to be polyphyletic (von Hagen & Kadereit 2001), while Swertia, too, may be polyphyletic (Chassot et al. 2001; Kadereit & von Hagen 2003), indeed, relationships in the Swertia/Halenia area are poorly understood (H.-C. Xi et al. (2014). Relationships within Gentianineae are being clarified, with Metagentiana probably being polyphyletic (Chen et al. 2005b; Favre et al. 2010), but more work is needed before the biogeography of this largely alpine group can be understood.
Classification. For an infra-familial classification of Gentianaceae, see Struwe et al. (2002), also the Gentian Research Network. Kissling et al. (2009a) and Kissling (2010) have divided the polyphyletic Sebaea into three genera, but there are even suggestions that the monophyletic Fagraea should be dismembered (Wong 2012 and references).
Previous Relationships. Anthocleista, Fagraea, and Potalia used to be in Loganiaceae (Struwe & Albert 2000), but details of their iridoid chemistry are very gentianaceous and they are well embedded in the family (e.g. Backlund et al. 2000). Emblingia has been placed here (Savolainen et al. 2000a), but a position in Brassicales in its own family (q.v.) is justified on both molecular and morphological grounds.
APOCYNACEAE Jussieu, nom. cons. - hierarchy below below very much under construction - Back to Gentianales
Lianes, climbing by twining, to evergreen trees (herbs); tryptophane-derived, steroidal [pseudoalkaloids, pregnane skeleton], indolizidine alkaloids,
route II decarboxylated iridoids +, tanniniferous; (cork cambium deep-seated - Rhazya);
pericyclic fibres 0 [always?]; (vessel elements with scalariform perforation plates), vessels single or in radial groups; tracheids in ground tissue; laticifers +,
not articulated (articulated), latex white; (petioles also with adaxial bundles); stomata usu. paracytic (anomocytic, actinocytic); leaves (spiral), lamina vernation usu. flat or conduplicate, ("stipules" +, cauline); K with basal adaxial colleters, C left-contorted, postgenital connation forming the upper tube [above the insertion of the A], (corona from C); anthers ± connivent, filament short; secondary pollen presentation +, pollen transported in foam; nectary separate lobes,
on outer wall of ovary, or 0; G apocarpous, (-8), (collateral),
415[list]/4555: 5 subfamilies and 25 tribes below; of the subfamilies, the first two in particular are wildly paraphyletic. Largely tropical to warm temperate (map: from Hultén 1968; see also maps below). [Photo - Flower, Fruit.]
Age. Rapini et al. (2007) calibrated the age of crown-group Apocynaceae at ca 54 m.y., but Bell et al. (2010) suggested an age of only ca 21 m.y..
1. "Rauvolfioideae" Kosteletzky - this includes the next 11 tribes.
1A. Aspidospermeae Miers
Trees or shrubs; (leaves spiral); calycine colleters 0; (C right-contorted); stylar head usu. undifferentiated (basal collar - Haplophyton); fruit a drupe or follicle, seeds winged, (with micropylar and chalazal coma - Haplophyton).
1B. Alstonieae G. Don
Trees or shrubs; calycine colleters 0/+; C also right-contorted; (stylar head differentiated); fruit a follicle; seeds with coma at both ends, winged, or hairy.
[Vinceae [Willughbeieae + Tabernaemontaneae]]: ?
1C. Vinceae D. Don.
Trees, shrubs (lianes, herbs); calycine colleters 0; (C right-contorted); anthers free from stigma, all fertile or with apical appendage; (only one G develops), stylar head differentiated, with basal collar; fruit a drupe, moniliform with several drupelets, or follicle; seeds (1-2), warty, hairy or winged, or unremarkable.
9/100: Rauvolfia (110).
Synonymy: Ophioxylaceae Martius, Vincaceae Vest
[Willughbeieae + Tabernaemontaneae]: G  [could be placed here].
1D. Willughbeieae A. de Candolle
Lianes, branches with terminal tendrils, trees, or shrubs (rhizomatous); calycine colleters +/0; G , placentation axile to parietal, stylar head not differentiated; fruit a berry, (seed 1).
18/130: Landolphia (60).
Synonymy: Pacouriaceae Martynov, Willughbieaceae J. Agardh
1E. Tabernaemontaneae G. Don
Shrubs or trees (lianas); calycine colleters several to many, basal; A sessile, anthers with thick, lignified guide rails; nectaries paired; G , placentation axile to parietal, or apocarpous, stylar head differentiated, complex, with a five-lobed upper crest and a thickened basal flange (not); fruit a berry/berrylet, or [Tabernaemontaninae], follicular; seed with aril, ± ruminate, with deep hilar groove.
15/150: Tabernaemontana (100-120). Northern South America (Ambelaniinae) and pantropical (Tabernaemontaninae).
[Melodineae, Hunterieae, Amsonieae, Alyxieae]: ?
1F. Melodineae G. Don
Trees, or shrubs; calycine colleters usu. 0; G , placentation axile, or apocarpous, stylar head usu. undifferentiated; fruit a berry, or follicle; seeds winged.
5/. Melodinus (75).
1G. Hunterieae Miers
Shrub or small trees (lianas); calycine colleters usu. +; G 2-5, stylar head not differentiated; fruit berrylets.
1H. Amsonieae M. E. Endress
Small shrubs to perennial herbs; leaves spiral; calycine colleters 0; anthers free, entirely fertile; stylar head differentiated, with basal collar; fruit a follicle; seeds not flattened.
1I. Alyxieae G. Don
Shrubs, trees or lianes; indole alkaloids 0; (leaves spiral); calycine colleters 0; pollen grains irregularly-shaped, 2-3-porate, ectoapertures with thickened margins, (inaperturate, in tetrads - Condylocarpon); G also [3-5], stylar head not differentiated; fruit a berry or drupe, moniliform with several drupes, or follicular; seed with aril, ± ruminate, with deep hilar groove, or winged at both ends, (ruminate); n = 9.
7/. Alyxia (120).
[Plumerieae, Carisseae ["Apocynoideae", Periplocoideae [Baisseeae [Secamonoideae + Asclepiadoideae]]]]]:
1J. Plumerieae E. Meyer
Shrubs, trees (lianes); iridoids, cardenolides [cardiac glycosides] +; leaves spiral (opposite); calycine colleters 0/+; (corona +); anther (sagittate, adnate to style head), (apex sterile, plumed); (G  - postgenitally), placentation parietal), stylar head differentiated; 2 ovules/carpel; fruit a drupe or samaroid, or follicle; seeds winged.
Synonymy: Cerberaceae Martynov, Plumeriaceae Horaninow
[Carisseae ["Apocynoideae", Periplocoideae [Baisseeae [Secamonoideae + Asclepiadoideae]]]]:
1K. Carisseae Dumortier
Shrubs to trees; indole alkaloids 0, (cardenolides [cardiac glycosides] +); (branched thorns +); calycine colleters usu. 0; C also right-contorted; A well above stylar head; G , placentation parietal to axile, or apocarpous, stylar head not differentiated; fruit a berry.
2/12. Old World tropics.
Synonymy: Carissaceae Bertolini
["Apocynoideae", Periplocoideae [Baisseeae [Secamonoideae + Asclepiadoideae]]] / APSA Clade: iridoids 0 [this level?], (cardenolides + [cardiac glycosides]); anthers with sagittate lignified basal appendages [guide rails]; pollen porate; anthers firmly adnate to style head [forming gynostegium], retinaculum formed by trichomes [region of stamen by which it attaches to style head]; stylar head differentiated both radially and vertically [or put at level of whole family], with a thickened basal flange, receptive basally; fruit a follicle; micropylar coma +.
2. "Apocynoideae" Burnett
A inserted well below bases of corolla lobes; n = (6-)10, 11 (12).
2A. Wrighteae G. Don
C left- or right-contorted; corona +/-; ([G 2]); chalazal coma + (and micropylar, deciduous).
3/29: Wrightia (23). Old World tropics.
[Nerieae + The Rest]: C right-contorted.
2B. Nerieae Baillon
(Succulent) shrubs or trees, (lianas); (pyrrolizidine alkaloids + - Alafia); (leaves spiral); (corona +); anthers with long apical appendage; G free to connate); coma also chalazal.
6/47: Strophanthus (38). Africa (most) and Europe to Japan and Malesia.
[Maloutieae + The Rest]: ?
2C. Malouetieae Müller Argovensis
Plant cactus-like, with spines; leaves spiral; calycine colleters 0; anthers weakly attached to stylar head; G free, stylar head with five basal projections; chalazal coma +.
[Rhabdadenieae, Periplocoideae, [Asian clade + New World clade], [Baisseeae [Secamonoideae + Asclepiadoideae]]] / Crown Clade: plant vine/liane; few wide vessels and several narrow vessels in clusters; vasicentric tracheids +; fibres [not tracheids] in ground tissue; nectaries 5, (basally connate), surrounding base of ovary [?level].
2D. Rhabdadenieae M. E. Endress
Slender lianas to perennial herbs; wood fibres very thin-walled, parenchymatous; calycine colleters 0; guide rails truncate, fused to filament; stylar head cylindrical, apically hairy, basal collar +.
1/4. Tropical America.
[Apocyneae + New World clade]: ?
Stamen-corolla tube very short; stylar head fusiform (with strap-like bands of adhesive), no basal collar. [goes where?]
2E. Apocyneae Reichenbach
Shrubs, lianes, or herbs; (pyrrolizidine alkaloids + - Anodendron); (leaves spiral); calycine colleters +; (C left-contorted); stylar head usu. broadest at the middle, basal collar 0 (+).
24/. Largely Malesian-South East Asian, also North Temperate (Apocynum).
[Echiteae, Mesechiteae, Odontadenieae] / New World clade: (pyrrolizidine alkaloids +).
2F. Echiteae Bartling
Woody lianes (small trees; herbs); (latex translucent); calycine colleters +, position variable; (C valvate), (corona +); guide rails narrow, (filaments spirally twisted - some Parsonsia); stylar head fusiform, basal collar narrow.
19/ Parsonsia (120), Prestonia (65). New World, tropical, also New Caledonia (two genera) to Australasia and South East Asia (Echites).
2G. Mesechiteae Miers
Colleters on adaxial surface of leaf.
5/ Mandevilla (115), Forsteronia (50). New World.
2H. Odontadenieae Miers
7/ New World.
3. Periplocoideae Endlicher
Plants with tuberous roots; C (valvate), tube formation intermediate, corona corolline; stamen-corolla tube very short, staminal feet erect, connate, forming tube around ovary; nectar secreted on margins of staminal feet [alternistaminal], receptacular nectary 0; anthers without lignified guide rails; tapetal cells uni(bi)nucleate; pollen in tetrads, inner and outer walls differentiated, grains 4-16 porate, surface smooth; pollen collected on spoon-like structure, basal sticky viscidium [translator]; retinaculum formed by cellular fusion; exotestal cells unthickened [Periploca]; embryo color?; n = 11 (mostly).
31/180. Old World, esp. Africa, tropics to dry temperate (map: Good 1952).
Synonymy: Periplocaceae Schlechter, nom. cons.
[Baisseeae [Secamonoideae + Asclepiadoideae]]: colleters on adaxial surface of leaf; stamen-corolla tube very short; G initially half inferior, stylar head without basal flange.
Baisseeae M. Endress
Large lianes; (trichomes branched); (leaves with domatia), (colleters axillary - Dewevrella; (filaments long, spirally twisted first in one direction and then the other - Dewevrella); (stylar head with strap-like bands of adhesive).
4/32: Baissea (20). Old World Tropics, esp. Africa.
[Secamonoideae + Asclepiadoideae]: (fructans/inulin +), monoterpene indole alkaloids 0; C tube formation intermediate; A inserted well below bases of corolla lobes, corona usually staminal [common vascular supply with A, filaments 0, anthers inserted on top of fused tube/specialized ring corona/staminal feet], nectar produced in alternistaminal sections of tube, the nectaries behind guide rails; endothecium not fibrous; pollinia of the one pollinarium from half anthers of adjacent stamens, erect, lacking outer walls, retinaculum formed by cellular fusion, translator with hardenened apical corpusculum [adhesive], translator arms/caudicles short; pollen in tetrads, outer and inner walls differentiated [inner walls have intine bridges], grains inaperturate, surface smooth, orbicules 0; endosperm nuclear (cellular), embryo green; n = 11.
Age. This node was dated to ca 42 m.y. (Rapini et al. 2007).
4. Secamonoideae Endlicher
Lianes, climbing by twining; (colleters on axaial surface of leaf); (C left-contorted); pollinia 4; granular layer of exine thick.
8/170: Secamone (100). Old World, esp. Madagascar, tropics to temperate.
5. Asclepiadoideae Burnett
(Interxylary phloem +); (leaves spiral), colleters on axaial surface; anthers bisporangiate, dithecal, pollinia 2; tapetal cells uninucleate; microsporogenesis simultaneous [pollen tetrads linear during development], granular layer of exine thin; nectar usually accessible at or near base of guide rails; mitochondrial rpoC2 pseudogene [from chloroplast]; n = (9-14).
214/2365. Tropics to temperate, drier areas esp. in Africa (map: see Good 1952). [Photo - Flower, Flower, Flower, Fruit.]
Age. Crown group Asclepiadoideae were estimated to be ca 37 m.y.o. (Rapini et al. 2007).
Plants with tuberous roots; connective appendages +, inflated; (anther secretes sporopollenin wall around pollinium, pollen appear to be in monads when mature - Cibirhiza).
2/9. Drier parts of southern and eastern Africa, Arabia.
[[Eustegieae + Asclepiadeae] [Marsdenieae + Ceropegieae]]: (lianes, often epiphytic); (phenathroindolizidine alkaloids); anther secretes sporopollenin wall around pollinium, pollinia with translator arms [caudicles], (orbicules + - Riocreuxia); outer and inner walls of tetrads not differentiated, pollen appear to be monads when mature.
[Eustegieae + Asclepiadeae]: ?
5B. Eustegieae Liede & Meve
Latex clear; leaves (spiral), lamina palmately lobed (margin with a few teeth).
2/6. The Cape, southeast Africa.
5C. Asclepiadeae Duby
87/. Cynanchum (200), Matalea (180), Asclepias (100), Gonolobus (100), Oxypetalum (90), Ditassa (75), Tylophora (50).
Synonymy: Asclepiadaceae Borkhausen, nom. cons., Cynanchaceae G. Meyer
[Marsdenieae + Ceropegieae]: ?
5D. Marsdenieae Bentham
(Latex clear); (pollinia with pellucid margin along proximal side); (exotestal cells with outer walls unthickened - Hoya).
26/. Hoya (90[-200+]), Marsdenia (100), Dischidia (80),
5E. Ceropegieae Orban
Latex clear; C valvate; pollinia with pellucid margin along distal side.
47/. Ceropegia (160), Brachystelma (100), Stapelia (70), Orbea (55), Huernia (50), Caralluma (47).
Synonymy: Stapeliaceae Horaninow
Evolution. Divergence & Distribution. For dates, etc., see Rapini et al. (2007) and Liede-Schumann et al. (2012).
Endress (2011a) thought that a key innovation within Gentianales was the possession of pollinaria, presumably to be optimized at the [Secamonoideae + Asclepiadoideae] node. Pollinia may have increased pollination efficiency by generalist pollinators in the rather small populations growing in these rather dry areas - a reduction of the Allee effect. Asclepiadoideae, often small herbs, represent the most derived members of this clade (Livschultz et al. 2011), and are diverse and highly endemic in southern Africa in particular (Ollerton et al. 2003).
Within "Apocynoideae" genera in major clades usually are from either the Old or the New World, with little overlap between the two (Livschultz et al. 2007). There is also substantial geographical structuring of clades within groups like e.g. Asclepiadoideae (Goyder 2006 for a summary).
Ecology & Physiology. Members of Asclepiadoideae are the most speciose scandent group in tropical New World forests, "Apocynaceae" somewhat less so, although in Africa the latter are perhaps the most prominent group with the scandent habit (Gentry 1991). Livschultz et al. (2011) proposed that [Asclepiadoidese + Secamonoideae] moved into drier habitats, the large rainforest lianes of Baisseeae representing the ancestral habit/habitat of the whole milkweed clade. More or less erect growth forms have evolved from lianes in Secamonoideae (Lahaye et al. 2005). The Hoya-Dischidia clade includes a large number of epiphytic climbers, unfortunately, details of the evolution of this distinctive habitat preference/habit are unclear (Wanntorp et al. 2014).
Succulence is widespread in the family, particularly in Periplocoideae (root succulents) and Asclepiadoideae (especially stem succulents). Nyffeler and Eggli (2010b) estimate that there are 74 genera containing 1151 species of succulents; 65 of these genera, mostly small, include only succulent taxa (Meve & Liede-Schumann 2010). There are about 400 species of stem succulent Cerpoegieae in the Old World alone, with centres of distribution in Arabia, East Africa and southern Africa (Meve et al. (2004).
Pollination Biology and Seed Dispersal. In all Apocynaceae, the anthers are closely associated with a swollen stigmatic head. In some perhaps plesiomorphic Apocynaceae like Plumeria and Alyxia cells of the stigmatic head secrete a sticky polysaccharide-terpenoid material to which the pollen adheres - basically, secondary pollen presentation; there are no localized receptive and secretory areas on the stigma. Such taxa are found in basal grade of "Rauvolfioideae", however, it is possible that such stigmas are derived, and more than once, and that the differentiated stigma described below is plesiomorphic for the whole family (Simõs et al. 2007a; see especially Schick 1980, 1982, also Shamrov & Gevorkyan 2010a, for the morphology of the stigmatic head). Taxa with an otherwise undifferentiated stylar head may have a pair of apical "stigmatic lobes", although these do not function as such (Albers & van der Maesen 1994). In taxa with spatial differentiation within the stigmatic head, pollen is deposited onto the apex of the swollen head; sticky material is secreted immediately below, and pollen germinates only at the base of the head (e.g. Albers & van der Maesen 1994). The gynostegium, formed by the post-genital fusion of anthers and stigma, develops when the connective tissue of the anther becomes adnate to the stigmatic head (the staminal retinacule of Simões et al. 2007b). Commonly in "Apocynoideae" pollen from thecae of adjacent anthers mixes, whereas pollen from the two thecae of the one anther does not mix because the intervening connective is adnate to the stigmatic head, that is, the basic spatial arrangement of the androecium is the same as that in Asclepiadoideae (see also Schick 1982). This is a very complex system, and in Tabernaemontaneae several features - an androecium with thick, lignified guide rails, a stylar head with a five-lobed upper crest and a thickened basal flange, and paired nectaries - are all associated, all being lost together some five times on the tree (Simões et al. 2010).
The intimate association of the androecium and gynoecium to form the gynostegium that characterizes Asclepiadoideae and Secamonoideae is postgenital. Within Periplocoideae, pollinia seem to have evolved at least three times (Ionta & Judd 2007). Since it is unlikely that Periplocoideae are sister to [Secamonoideae + Asclepiadoideae] (see esp. Livschultz et al. 2007), the evolution of the pollinarium that characterize the latter can be considered separately, although variation in the pollinarium of Fockeeae, sister to all other Asclepiadoideae, somewhat confuses the issue (see Verhoeven et al. 2003). In any event, the old idea of the evolution of the pollinia of Asclepiadaceae via Periplocaceae/Periplocoideae as some sort of intermediate needs to be revised (see also Potgeiter & Albert 2001; Sennblad & Bremer 2002; Ionta & Judd 2007; esp. Livschultz et al. 2007).
Nectar in many of the old Apocynaceae is secreted by nectaries at the base of the gynoecium; these vary in number and may be connate basally or free. In Secamonoideae and Asclepiadoideae in particular nectar may be secreted in "staminal outgrowths" from the petal-like staminal feet (i.e. the corolla + filament tissue below the anther) that completely surround the gynoecium. Kunze (e.g. 1991, 1997; Kunze & Wanntrop 2008b) show that it is secreted beneath the guide rails, although it may be accessible to the pollinator only elsewhere in the flower (Fahn 1979 suggested that the stigma itself might secrete nectar in Asclepias). A variety of floral volatiles has also been characterized (Jürgens et al. 2009).
The diversity of form produced by tissues from the corolla, stamens, and staminal feet in [Secamonoideae + Asclepiadoideae] is remarkable (see Liede & Kunze 1993 for terms used), indeed, flowers in many Apocynaceae develop a variety of petal-like appendages. These may develop from the corolla tube (Nerium, Allamanda) or from the apices of the anthers (Adenium, Nerium). Strophanthus can have appendages at the apices of the anthers or more or less bilobed appendages in the angles of the corolla lobes, while the corolla lobe narrows into a thin, dangling process that in some species is almost 30 cm long; there is no nectary. Within Asclepiadoideae, the corona develops very late and is clearly staminal, and this is consistent with the pattern of gene expression in the flower (Livshultz & Kramer 2009), although Kunze (2005b) suggests that it is an organ sui generis - which it is, from another point of view. There is much variation in the details of the gynostegium in Asclepiadoideae. Kunze and Wanntorp (2008a) discuss corona and anther skirt evolution while Kunze and Wanntorp (2008b) puzzle over the morphologically distinctive gynostegium of the molecularly unremarkable Hoya spartioides.
For a general survey of pollination in Apocynaceae, see Ollerton & Liede (1997). Hairs on the anthers or stigmatic head, or lignified guide rails at the bases of the anther, are all involved in pollen presentation and guiding the mouth parts of the pollinator (or trapping the pollinator...) so that effective pollination occurs (e.g. Fallen 1986). An annulus or flange around the middle of the head in many ex-Apocynaceae aids in the removal of the pollen from the proboscis of the pollinator, scraping it off, while the receptive stigma itself forms a ring around the base of the head. The stigmatic flange and the lignified guide rails on the anthers together form a trap-and-guide pollination mechanism.
In asclepiads the nectar may be physically associated with the guide rails, the proboscis of the insect being guided to the viscidium, which thus attaches the pollinia to the pollinator (e.g. Kunze 1991). In general, pollination is a rather precise process, although several species of insects may be effective pollinators of one species of plant (e.g. Ollerton et al. 2003); indeeed, in five species of Asclepias 41-185 species of floral visitors were recorded of which 17-116 were effective pollinators (Fishbein & Venable 1996). Fly pollination is quite widespread, particularly in Asclepiadoideae (see e.g. the photographs in Pilbeam 2010). It has been studied in detail in Ceropegia (Vogel 1961) where it is very common; in one study, about 60% of the some 60 species examined were each pollinated by a single genus of flies (Ollerton et al. 2009b: see below for the phylogeny of the genus). Meve and Liede (1994) surveyed pollination in stapeliads in general, while Ollerton et al. (2003) looked at pollination of asclepiads at a site in South Africa, some being pollinated by specialists and others by generalists. Yamashiro et al. (2008) studied details of pollination of Japanese species of Vincetoxicum; tipulids, other dipterans, moths, etc., were all involved.
Wyatt and Lipow (2007) suggest that the evolution of pollinia and the secondary apocarpy in Asclepiadoideae and Apocynaceae s.l. is connected with the post-zygotic incompatibility system that characterises Apocynaceae (?all) and at least some other Gentianales. In Ceropegieae, at least, the situation is rather like that in many Orchidaceae; natural hybrids are uncommon, but it is quite easy to make successful artifical crosses between species in different "genera" (Meve et al. 2004 for references).
Fruit and seed morphology in the old Apocynaceae is quite variable, but follicular fruits with comose seeds characterise a clade that includes the old Asclepiadaceae. At least some Asclepiadoideae have no compitum, one of the reasons for the frequent occurrence of fruits in which only a single carpel has developed.
Plant-Animal Interactions. 1,2-dehydropyrrolizidine alkaloids are found in some Apocynaceae, and plants with these alkaloids attract practically all Danaini butterflies, mostly males, which use these compounds as the basis of their pheromones and for defence (Boppreé 2005; Brehm et al. 2007). The monarch does not use these alkaloids in pheromones, but it does sequester them for defence (Hartmann & Witte 1995).
Caterpillars of Nymphalidae-Danainae-Danaini relish members of this family (Ehrlich & Raven 1964; see Ackery & Vane-Wright 1984 for a comprehensive treatment; Brower et al. 2010 for a phylogeny), but they also eat other plants with latex, including several Moraceae and Carica. Caterpillars of all three main clades of Danainae can be found on Apocynaceae, probably their ancestral host family (Edgar 1984; Janz et al. 2006; c.f. Wahlberg et al. 2009), although many New World Ithomiini eat Solanaceae (see below); the danaine clade diverged from other butterfly clades ca 89 m.y.a. (Wahlberg et al. 2009). The monarch butterfly is one example of an insect involved in this cardenolide syndome; the cardenolides are noxious and may protect both caterpillar and adult butterfly (e.g. Malcolm 1991; see also Dobler et al. 2011).
For a study of the different defence syndromes of Asclepias, see Agrawal & Fishbein (2006). Although the resprouting ability of Asclepias - or simply its tolerance of herbivory - may be an effective defence against specialist herbivores (Agrawal & Fishbein 2008), the situation is complex; production of a variety of phenolics also changed, showing an overall increase as cardenolide production decreased (Agrawal et al. 2009a). Herbivorous insects that eat cardenolide-containing Apocynaceae show convergence at the amino acid level that appears to promote cardenolide resistance; normally cardenolides inhibit the sodium pump by binding with a subunit of it (Zhen et al. 2012; Dobler et al. 2012; Whiteman & Mooney 2012 for a summary).
Larvae of a few species of ithomiine butterflies are found on Apocynaceae, especially on Echiteae (Edgar 1984, as Parsonsieae). In a comprehensive morphological analysis (Wilmott & Freitas 2006) these apocynaceous-eating ithomiines, which include Tellervo, the only Old World member of the group, came out at the base of the tree (unrooted); ithomiines otherwise eat mostly New World Solanaceae, q.v.. Adult ithomiini butterflies are also attracted to Apocynaceae from which they take up alkaloids, and Edgar (1984) and Brehm et al. (2007) suggested that the pyrrolizidine alkaloids of Echiteae may have been originally involved in their pharmacophagous behaviour; the alkaloids are the basis of the butterfly pheromones. These pyrrolizidine alkaloids are also found in Crotalaria, Heliotropaceae and Asteraceae-Asteroideae.
One interpretation of the initial diversification in North American Asclepias is that this was accelerated by reduced investment in defensive traits like latex and cardenolide production (Agrawal et al. 2009b). Furthermore, there is an inverse correlation between the presence of leaf surface waxes and that of indumentum, the presence of either making it more difficult for potentially noxious insects to alight, although other plant traits are also involved (Agrawal et al. 2009c). Finally, both induced and constitutive - amount and diversity - cardenolide production increases at lower latititudes (Rasmann & Agrawal 2011; Agrawal et al. 2012 for a summary), although Moles et al. (2011b) suggest that generally such protective compounds decrease at lower latitudes.
Milkweed caterpillars may be infected by protozoan parasites. The tolerance and resistance of the caterpillars to particular protozoan parasites depends on the Asclepias they are eating; tolerance and resistance are conferred separately by the plant (Sternberg et al. 2012).
Brightly-colored danaine caterpillars and bright orange aphids are to be found on Asclepiadoideae in both North America and southern Africa. Aphids may on occasion even induce cardenolide production (Martel & Malcolm 2004), but resistance of aphids to cardenolides may have evolved rather differently from that in other herbivores eating asclepiads (Zhen et al. 2012). These aposematic aphids seem to feed preferentially on internal phloem/adaxial phloem of leaf bundles, apparently the cardenolide transport system, so acquiring food and protection at the same time (Botha et al. 1977). However, which bundles are targeted may also depend on the age of the leaf (Botha et al. 1975).
Pyrrolizidine alkaloids and pentacyclic triterpene saponins variously sequestered and modified are found in the secretions of the defensive glands of some Chrysolina and Platyophora beetles (Chrysomelidae, both very speciose genera: Pasteels et al. 2001; Termonia et al. 2002; Hartmann et al. 2003). For the possible co-evolution of the longicorn beetle Tetraopes with Asclepias, see Farrell and Mitter (1998). Hosts of seed-eating bugs of Hemiptera-Lygaeidae-Lygaeinae are concentrated in the old Apocynaceae (Slater 1976).
Bacterial/Fungal Associations. Although Paris-type mycorrhizae are found in Gentianaceae, Loganiaceae, and Rubiaceae, Arum-type endomycorrhizae, or intermediates, are common in Apocynaceae, especially in Asclepiadoideae (Imhoff 1999).
Vegetative Variation. Seedlings of genera with opposite leaves, like Hoya, may have spiral leaves; Absolmsia, previously segregated from Hoya, has spiral leaves even at the flowering stage. In taxa such as Vallesia there are cauline "stipules", apparently colleters in a stipular position; Vallesia also has spiral leaves. Mandevilla has a distinctive ring of large, radiating, almost fleshy projections immediately below the leaves, and in other taxa there may be adaxial, scale-like structures on the petiole (Thomas & Dave 1991). A variety of stipule-like structures is also found in Stapelia and relatives; in Edithcolea grandis the "stipule" is represented by a single hair (Bruyns 2000, see also 2004), while there is a variety of hairs and other structures in the stipular position in Caralluma (Bruyns et al. 2010). In Apocynaceae like Alstonia there is an adaxial excavation at the base of the petiole in which the axillary bud is enclosed; this is often encased by secretions from the colleters.
Branching in a number of taxa is complex. The apical bud may abort, or be converted into an inflorescence, and there may be a pair/whorl of reduced leaves with a very short internode at the end of each innovation, and these reduced leaves subtend vegetative branches or inflorescences which then appear to be in an extra-axillary position (Troll & Weberling 1990). The "lateral" inflorescences of at least some stapeliads may be displaced-terminal (Bruyns 2004), and such inflorescences are also found in Apocynum, Asclepias, etc., however, Leptadenia (Asclepiadoideae) has axillary inflorescences. The literature is quite extensive, although there is no recent synthesis; see e.g. Woodson (1935), Holm (1950), Nolan (1969), Liede and Weberling (1985) and Steck and Weberling (1982).
Genes & Genomes. For the transfer of the rpll pseudogene from the mitochondrion to the nucleus in Asclepiadeae, including Eustegia and Astephanus, see Straub et al. (2013).
Chemistry, Morphology, etc. For distinctive fatty acids in the seed, see Badami and Patil (1981). Agrawal et al. (2011) summarize information on cardiac glycosides in the family; they note that the steroidal alkaloids found in Apocynaceae are strictly speaking pseudoalkaloids, since the nitrogen does not come from amino acids.
The cambium is occasionally storied. The leaves of Asclepiadoideae and many genera more basal to them have flat vernation (Cullen 1978). Cymose inflorescences of some sort are the norm in the family, and some Marsdenieae in particular have very long-lived but contracted inflorescences in which single flowers or whorls of flowers open at intervals over a year or more (Meve et al. 2009).
There is variation in the direction of contortion of the corolla lobes (e.g. Eichler 1874). How the corolla tube is initiated in Periplocoideae is unknown. There has been considerable discussion about the nature of the paired nectaries of Vinca in particular, and because of their vasculature, etc., it has been suggested that they are modified carpels (e.g. Woodson & Moore 1938; Rao & Ganguli 1963; Fahn 1979); this is unlikely. Much has been written about the homology of the various floral structures; deciding which structures on different flowers are directly comparable (see Remane's criteria) can indeed be very difficult. If the staminal feet in Periplocoideae are considered similar to the fused basal tube of [Secamonoidae + Ascleiadoideae], in that both are outgrowths of the stamen-corolla tube, then there is a potential synapomorphy for the larger group, or a parallelism if they do not form a single clade (Livshulz et al. 2007). Strap-shaped bands on the style head are scattered in ex-Apocynoideae, and may be similar to translators in Asclepiadoideae, Secamonoideae, and Periplocoideae; could this yield a high-level character in the whole APSA clade (Livshulz 2010)? There is quite a lot of variation in pollen morphology in Apocynaceae, independent of pollinarium formation. Alyxieae in particular have grains with large pores, and some species have remarkable barrel-like pollen grains, the pores forming the ends of the barrel (M. Endress et al. 2007a). For tetrad morphology, see Omlor (1998); Periplocoideae and Secamonoideae are reported to have T-shaped and tetragonal tetrads and successive microsporogenesis. When the carpels are connate, placentation may be axile or parietal (the latter, Allamanda, see Fallen 1985). Syncarpy seems to have evolved more than once in the family, it is congenital in Acokanthera and postgenital in Allamanda (Sennblad & Bremer 1996). The carpels may be collateral (Spichiger et al. 2002). An endothelium has been reported in the ovules of Apocynaceae s. str. (Kapil & Tiwari 1978; Cronquist 1981), but it is absent according to Rohwer (1996).
Apocynaceae are a much-studied group. See M. Endress and Bruyns (2000), Leeuwenberg (1994), and Livshulz et al. (2007), all general, Aniszewski (2007: alkaloids), Demarco et al. (2006: laticifer type), Lens et al. (2009c: wood anatomy, to be integrated), Cremers (1973: growth of some lianes), Glück (1919: colleters), Leeuwenberg (1983: Plumerioideae), Swarupanandan et al. (1996: flowers of Asclepiadoideae, classification), Meve et al. (2009: floral morphology of Marsdenieae), Kunze (1990, 2005a: corona), Nilsson et al. (1993), Verhoeven and Venter (1994, 2001), Van der Ham et al. (2001: Alyxieae), Vinckier and Smets (2002b: orbicules), van de Ven and van der Ham (2006: Melodinus, etc.), and Van der Weide and Van der Ham (2012: Tabernaemontaneae), all pollen, P. Endress (1994b: much floral morphology, esp. Asclepiadoideae), Kunze (1996: stamen), Sennblad (1997: general), Civeyrel et al. (1998: pollinaria variation), Omlor (1996: translator structure in Periplocoideae and Secamonoideae, 1998: floral morphology and testa anatomy), Albers and Meve (2001: karyology), Endress et al. (1983) and Shamrov and Gevorkyan (2010b: gynoecium), and Andersson (1931), Anantaswamy Rau (1940b), and Venkata Rao and Rama Rao (1954), all embryology. There is much information on Periplocoideae, Secamonoideae, and Asclepiadoideae at a site run by S. Liede-Schumann and U. Meve while F. d'Alessi and L. Viljoen provide information on stapeliads in particular.
Phylogeny. Both Rauvolfioideae and Apocynoideae are paraphyletic (Sennblad & Bremer 1996, 2002); see Livshultz et al. (2007) for the phylogeny of "Apocynoideae" and Simões et al. (2007) for that of "Rauvolfioideae", particularly paraphyletic. The relationships of seven tribes in the latter are more or less clear, but those of the remaining five tribes remain to be established; there is good support for Aspidospermeae and Alstonieae as successively sister to all other Apocynaceae (Simões et al. 2007), and both tribes more or less lack uniseriate rays, a feature uncommon in other "Rauvolfioideae" (Lens et al. 2008b). Simões et al. (2010, see also 2006a) have clarified relationships within Tabernaemontaneae, i.a. circumscribing Tabernaemontana broadly to include Stemmadenia; major clades within that genus are correlated with geography. All tribes can be more or less readily distinguished by a combination of features in their wood anatomy (Lens et al. 2008b). For a phylogeny of Alyxieae, M. Endress et al. (2007) and of "Rauvolfioideae" as a whole, see Simões et al. (2007a). Burge et al. (2013) clarified relationships within the much-cultivated Pachypodium.
Apocynoideae, as well as the old Asclepidaceae and Periplocoideae, form the APSA clade, relationships within which are being clarified. Parsonsia and Echites (Echiteae: Sennblad & Bremer 2002) are part of the New World clade, Mesechiteae. For phylogenetic relationships in Mesechiteae, see Simões et al. (2004, 2006b); in an earlier circumscription, the tribe was polyphyletic. There is small mostly African clade, Baisseeae, in which Dewevrella, with coiled filaments, is sister to the rest - and it is morphologically rather different from them (Livshultz 2009, esp. 2010). They are strongly supported as being sister to [Secamonoideae + Asclepiadoideae]. Below Baisseeae is a polytomy including a largely Asian clade (but including Apocynum) of ex-Apocynoideae, a largely American clade of that group, Rhabdadenia, and Periplocoideae (Livshultz et al. 2007; Livshulz 2010; see also Lahaye et al. 2007). Within Periplocoideae Phyllanthera is sister to the rest; pollinia seem to have evolved at least three times (Ionta & Judd 2007; see also Venter & Verhoeven 2001). It is currently unclear whether or not Periplocoideae are immediately related to [Baisseeae [Secamonoideae + Asclepiadoideae]], and relationships could be [Periplocoideae [[Asian clade + New World clade] [Baisseeae [Secamonoideae + Asclepiadoideae]]], with the position of Rhabdadenia unclear (e.g. Livshulz 2010, perhaps 8 times the current amount of parsimony-informative data will solve the problems).
Surveswaran et al. (2014) found that relationships within Asclepiadoideae were [Fockeeae [Eustephieae + Asclepiadeae] [Ceropegieae + Marsdenieae]], although support for the first pair is not very strong. Relationships within New World Asclepiadoideae have been clarified by e.g. Liede-Schumann (2005), Rapini et al. (2007) and Suilva et al. (2012: most genera of Metastelmatinae are not monophyletic). Yamashiro et al. (2004) found that Vincetoxicum was not monophyletic; Liede-Schumann et al. (2012) clarified relatioships in the whole Tylephorinae. Relationships around Astephaninae are unclear (Liede 2001). Hoya and Dischidia (Marsdenieae) are fairly close (Livshultz et al. 2013: outline of relationships within the tribe), and could be separated by morphological features, possibly apomorphies, such as pollinarium morphology, inner guide rail presence/absence, and nectary position (Wanntorp & Kunze 2009). However, whether Dischidia is sister to or embedded within Hoya remains unclear (Wanntorp et al. 2014). Estimates of species numbers in these two genera in particular vary widely, although Hoya is particularly speciose; see also Wanntorp et al. (2006a, b, 2009) for phylogenies, Wanntorp and Forster (2007: floral morphology in general), Kunze and Wanntorp (2008a: corona and anther skirt) and Kunze and Wanntorp (2008b: focus on Hoya spartioidea). Relationships along the backbone of Hoya remain poorly resolved (Wanntorp et al. 2011a). For relationships within Asclepias, polyphyletic, see Goyder et al. (2007); Asclepias in the New World is sister to an Old World clade of Asclepiadoideae within which the Old World Asclepias are embedded, however, support for the two clades is not strong, and basal relatiosnhips within the Old World clade also have little support. A study focusing on New World Asclepias found that Trachycalymma was sister to both the Old and New World clades, although none of these relationships had much non-parametric bootstrap support (Fishbein et al. 2011); in Goyer et al. (2007) Trachycalymma was embedded within the Old World clade. For the delimitation and relationships of Cynanchum, see Liede and Kunze (2002) and Liede and Täuber (2002). Within Ceropegieae relationships are complex, Ceropegia itself occurring all over the tree (Meve & Leide 2001, 2002; Meve & Liede-Schumann 2007). For the Gonolobus area, see Krings et al. (2008).
Classification. The suprageneric classification here is based on that of M. Endress et al. (2007a and in particular 2014; see also Endress & Bruyns 2000; summary in Nazar et al. 2013); for subtribes, see M. Endress et al. (2014).
In general, generic limits need attention (see e.g. Liede & Täuber 2000; Liede et al. 2002; Rapini et al. 2003; Goyder et al. 2007l; Meve & Liede-Schumann 2007). For generic limits in Tabernaemontaneae, see Simões et al. (2010). Generic limits in Asclepiadoideae are particularly difficult, and current genera can seem to be distinguished by floral minutiae. Asclepias itself is definitely polphyletic, the New World clade including the type of the genus (Goyder et al. 2007), but morphology alone is not clarifying relationships too much; Goyder (2009) provisionally included even Trachycalymma (see above) in an admittedly unsatisfactorily circumscribed African Asclepias. Ceropegieae are another very difficult area, indeed, various genera are embedded within Caralluma, in turn embedded in Ceropegia (Meve & Leide 2001, 2002; Meve & Liede-Schumann 2007; Bruyns et al. 2010: see de Kock & Meve 2007 for a checklist); one can only guess what the ultimate clade limits will be. For the circumscription of Sarcostemma, see Liede and Täuber (2000). For genera in the Asclepiadoideae-Marsdenieae, see Omlor (1998) and Meve et al. (2009); to make Marsdenia monophyletic, the tribe, which includes Hoya, etc., would become monogeneric (Livshultz et al. 2013). Liede-Schumann et al. (2012) extend the limits of the Old World genus Vincetoxicum.
For a magnificent revision of southern African stapeliads, see Bruyns (2004).
Thanks. I thank M. Endress for comments.