LIGNOPHYTA

Plant a shrub or tree; true roots +, origin endogeneous, root cap +, apex multicellular; endodermis +; shoot apical meristem multicellular; lateral meristems +, cork cambium producing cork abaxially, vascular cambium producing phloem abaxially and xylem adaxially; lamina with mean venation density 1.8 mm/mm² (to 5 mm/mm²).

EXTANT SEED PLANTS/SPERMATOPHYTA

Plant woody, 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, thus containing p-hydroxyphenyl and guaiacyl lignin units, so no Maüle reaction; root xylem exarch, cork cambium deep seated; arbuscular mycorrhizae +; shoot apical meristem interface specific plasmodesmatal network; stem with vascular tissue around central pith [eustele], vascular bundles with interfascicular tissue, ectophloic, endodermis 0, xylem endarch; 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"]; vascular bundles collateral [stem: phloem external; leaf: phloem abaxial]; stomata morphology?, pore opening controlled by abscisic acid; leaves with petiole and lamina, spiral, 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 tetrahedral, only one megaspore develops, megasporangium indehiscent; male gametophyte development first endo- then exosporic, tube developing from distal end of grain, to ca 2 mm from receptive surface to egg, gametes two, developing after pollination, with cell walls, flagellae numerous; ovules increasing considerably in size between pollination and fertilization, female gametophyte endosporic, initially syncytial, walls then surrounding individual nuclei; seeds "large" [ca 8 mm³], but not much bigger than ovule, with morphological dormancy; embryo cellular ab initio, endoscopic, plane of first cleavage of zygote transverse, suspensor +, short-minute, embryo straight, shoot and root at opposite ends [allorrhizic], white, cotyledons 2; plastid transmission maternal; ycf2 gene in inverted repeat, two copies of LEAFY gene, PHY gene duplications [three - [BP [A/N + C/O]] - copies], nrDNA with 5.8S and 5S rDNA in separate clusters; mitochondrial nad1 intron 2 and coxIIi3 intron and trans-spliced introns present.

MAGNOLIOPHYTA

Lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, non-hydrolysable tannins, quercetin and/or kaempferol +, 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 unilacunar [1:?]; stomata brachyparacytic [ends of subsidiary cells level with ends of pore], outer stomatal ledges producing vestibule; lamina formed from the primordial leaf apex, margins toothed, development of venation acropetal, secondary veins pinnate, overall growth ± diffuse, venation hierarchical, fine venation reticulate, 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 not sharply differentiated, with a single trace, outer members not enclosing the rest of the bud, often smaller than inner members; 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 columellar, endexine thin, compact, lamellate only in the apertural regions; nectary 0; G superior, free, several, ascidiate, with postgenital occlusion by secretion, stylulus short, hollow, cavity not lined by distinct epidermal layer, stigma ± decurrent, 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, megaspore tetrad linear, functional megaspore chalazal, lacking sporopollenin and cuticle; female gametophyte four-celled [one module, nucleus of egg cell sister to one of the polar nuclei]; ovule not increasing in size between pollination and fertilization; pollen binucleate at dispersal, male gametophyte trinucleate, germinating in less than 3 hours, pollination siphonogamous, tube elongated, growing between cells, growth rate 20-20,000 µm/hour, outer wall pectic, inner wall callose, with callose plugs, penetration of ovules via micropyle [porogamous], whole process takes ca 18 hours, distance to first ovule 1.1-2.1 mm; male gametes lacking cell walls, flagellae 0, double fertilization +, ovules aborting unless fertilized; P deciduous in fruit; seed exotestal, becoming much larger than ovule at time of fertilization; endosperm diploid, cellular [micropylar and chalazal domains develop differently, first division oblique, micropylar end initially with a single large cell, divisions uniseriate, chalazal cell smaller, divisions in several planes], copious, oily and/or proteinaceous; embryogenesis cellular; germination hypogeal, seedlings/young plants sympodial; Arabidopsis-type telomeres [(TTTAGGG)_n]; whole genome duplication, 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]]]]]: vessels +, elements with elongated scalariform perforation plates; 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]]]]: essential oils in specialized cells [lamina and P ± pellucid-punctate]; tension wood 0; 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 +; 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 positiion]; embryo sac bipolar, 8 nucleate, antipodal cells persisting; endosperm triploid; ?germination.

[MONOCOTS [CERATOPHYLLALES + EUDICOTS]]: (veins in lamina often 7-17mm/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 scattered, asarone 0 [unknown in some groups, + in some asterids]; root epidermis derived from root cap [?Buxaceae, etc.]; 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?; palaeohexaploidy [gamma triplication], PI-dB motif +, small deletion in the 18S ribosomal DNA common.

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

[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, if evident only early in development and then petals often appearing to be free); anthers dorsifixed?; (nectary gynoecial); style +, long; ovules unitegmic, integument thick, endothelium +, nucellar epidermis does not persist; exotestal 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); (pollen with orbicules); style short[?]; duplication of the PI gene.

ASTERID I / LAMIIDAE: G [2], superposed; loss of introns 18-23 in d copy of RPB2 gene.

[BORAGINACEAE + VAHLIACEAE + GENTIANALES + LAMIALES + SOLANALES]: (8-ring deoxyflavonols +); vessel elements with simple perforation plates; C forming a distinct tube, initiation late [sampling!]; A epipetalous; [vascularized] nectary at base of G; style long.   Back to Main Tree

Evolution. Divergence & Distribution. Magallón and Castillo (2009) offer estimates of ca 81 m.y. for both relaxed and constrained penalized likelihood datings for this clade - but note topology; Boraginaceae are included, Vahliaceae excluded.

Morphology, Anatomy, etc. There are several characters of potential phylogenetic interest in this group. 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. 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 do 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. Lamiales and Boraginaceae have in common similar hydroxycinnamic acid derivatives, i.e. disaccharide esters of rosmarinic/lithospermic/caffeic acids (Mølgaard & Ravn 1988).

Boraginaceae s. str. have callose plugs in the pollen tube, as do Solanales, but they are both present and absent in Hydophylloideae, and absent in Heliotropioideae, Cordioideae, and monosymmetric-flowered Lamiales (Cocucci 1983).

Phylogeny. Vahlia is placed sister to Lamiales, but with only 63% bootstrap support by Albach et al. (2001b), or is associated more specifically 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). However, Qiu et al. (2010: mitochondrial genes) did not find Boraginaceae and Gentianales to be immediately associated, although they are not strongly separated. In general, relationships between Gentianales, Lamiales and Solanales are unclear (Albach et al. 2001b; B. Bremer et al. 2002; Janssens et al. 2009, Boraginaceae s.l. not included; J. Li & Zhang 2010). Even the analysis of all 79 protein-coding plastid genes and four mitochondrial genes did not clarify relationships in this area (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 s.l. were included.

Unplaced:  Back to Main Tree

BORAGINACEAE Jussieu, nom. cons.

Plant ± herbaceous; pyrrolizidine alkaloids; cork superficial to mid-cortical (pericyclic); (silicon concentration high [?level]); (vessel elements with scalariform perforation plates); sieve tubes with nuclear non-dispersive protein bodies; nodes 1:1; petiole bundle(s) arcuate; plant ± roughly hairy, hairs with a basal cystolith or cystolith-like body, and/or walls calcified; leaves spiral; inflorescences terminal, cymose, cyme scorpioid, ± circinate, (bracteoles 0); K free, C tube formation late; anther placentoid 0; (pollen with pseudocolpi); nectary not vascularized; placentation parietal, (heterostyly +), stigma dry; fruit a loculicidal capsule, K persistent; micropylar endosperm haustoria +, cotyledons accumbent[?].

148[list]/2755 - in six groups below. Temperate to tropical. [Photos - Collection]

1. Boraginoideae Arnott

?

112/1600. Largely (warm) north temperate, a few tropical montane.

Codoneae

Subshrubs; ?chemistry; plant prickly-hairy; flowers 10-12-merous; K deeply linear-lobed, C broadly campanulate, with flaps near filament bases; pollen without pseudocolpi; G [2], placentation strongly intrusive parietal, style deeply bilobed; ovules many/carpel; testa reticulate-papillate; endosperm copious; n = ?.

1/2. S.W. Africa (map: see Retief et al. 2005).

Synonymy: Codonaceae Weigend & Hilger

Wellstedieae + The Rest: ovules 2/carpel, apical, pendulous.

Wellstedieae

Plant small, subshrub; ?chemistry; peltate glands +; flowers in two serried ranks along the stem; flowers four-merous; C lobes three-veined, C tube eight veined; pollen 12-25 x 8-15 µm, exine perforate to reticulate, pseudocolpi +, mesocolpium coarse-reticulate [c.f. hydrophylloids]; nectary 0; G [2], stigma bifid, wet; ovule one/carpel; fruit septae may separate from the walls; seed with fringe of downwardly-pointing hairs from near the apex; embryo curved, cotyledons accumbent, endosperm 0; n = ?

1/5. S.W. and N.E. Africa (map: see Thulin & Johansson 1996; Reteif & van Wyk 2008).

Synonymy: Wellstediaceae Novák

The Rest.

(Shrubs); prenylated naphthoquinones [e.g. alkannin, reddish or purple dye], gamma-linolenic acid +, stem storage polysaccharides isokestose and higher inulin oligosaccharides [fructans] (with starch; none in annuals); (pits vestured); one (or both) bracteoles 0; corolla often rotate, mouth with inpushings of corolla tube [fornices, morphology variable] (0), anther connective produced or not; tapetal cells multinucleate (uninucleate - Cynoglosseae); pollen trinucleate, (4- or more colporate), tube with callose; ovary with secondary septae, style gynobasic, hollow, (style branched), stigma punctate to capitate; ovule with integument 7-12 cells across, (nucellar cap +), endothelium 0, placental obturator +; fruit a schizocarp, with (1-)4 nutlets, exocarp sclerified; testa (vascularized), exotestal cells with outer walls thickened and lignified (other patterns of thickening, or unthickened), most other cells disappear; endosperm oily or 0, also nuclear, haustoria 0; n = (4-)12(-13).

110/1595: Cryptantha (160), Onosma (150), Myosotis (90), Cynoglossum (75), Paracaryum (70), Plagiobothrys (70), Lithospermum (70), Echium (60), Amsinckia (50), Mertensia (50), Trigonotis (50). Largely (north (warm) temperate, some on mountains in the tropics (map: see Wickens 1976; Meusel et al. 1978; Hultén & Fries 1986; Böhle et al. 1996; Långström & Chase 2002; FloraBase 2005; Wiegend et al. 2010: still incomplete).

Synonymy: Anchusaceae Vest, Buglossaceae Hoffmannsegg & Link nom. illeg., Cerinthaceae Berchtold & Presl, Cynoglossaceae Döll, Echiaceae Rafinesque, Onosmaceae Martynov

[Hydrophyllaceae [Heliotropioideae + Cordioideae + Ehretioideae + Lennooideae]]: (plant smells unpleasantly); tapetal nucleus number?; endothelium +; testa with single layer of transfer cells [cells with labyrinthine ingrowths of the wall].

2. Hydrophylloideae Burnett

(Shrubs); tannins 0, inulin?, alkaloids?; (mycorrhizae 0); leaves (opposite; compound), margins lobed, toothed (entire), secondary veins pinnate to palmate; bracts and bracteoles usu. 0; (K free); C tube formation late [Nemophila]; A usu. with small scales at each side of the base; pollen also colpate, tubes with callose (0 - Phacelia); nectary 0; G (seminferior), style ± deeply divided, stigma punctate; ovules 2-many carpel, (pleurotropous), (crassinucellate), integument 5-10 cells across; (fruit a loculicidal + septicidal capsule), (indehiscent); (seeds ruminate by inpushings of the exotestal cells), exotestal cells thickened on inner and radial walls, (largely disappearing - Nemophila), endotestal cells persistent, walls esp. the inner periclinal ± thickened; endosperm also nuclear, copious to scanty, chalazal and micropylar haustoria +/0, with lateral projections, (reserve hemicellulose), embryo (short), green or white; n = 5, 9-13, 19.

17[list]/240: Phacelia (150), Nama (60). New World, esp. drier areas of southwestern North America (map: see Brummitt 2007). [Photo - Undetermined Flower.]

Synonymy: Ellisiaceae Berchtold & J. S. Presl [?status], Eutocaceae Horaninow, Hydrophyllaceae R. Brown, nom. cons., Sagoneaceae Martynov

[Heliotropioideae + Cordioideae + Ehretioideae + Lennooideae]: bark oxidises; pollen tubes lacking callose; ovary with secondary septae, transfer cells in funicle and placenta also; ovules 2/carpel; fruit a schizocarp, or indehiscent, with a multilayered lignified endocarp; endosperm cellular.

3. Heliotropioideae Arnott

(Trees or lianes); cambium not storied; pericyclic sheath 0 [?always]; pits not vestured (+); petiole bundles arcuate; (tetrahedral crystals +); leaves usu. conduplicate [Tournefortia]; C imbricate or with involute margins; A connate at apex via papillae, connective not produced; tapetal cells binucleate; (4 colporate); style much swollen apically (0), stigma receptive only basi-laterally, discoid, then conical and ± bilobed at sterile apex, or hemispherical, with a ring of hairs, stigma wet; ovules with integument (?3-)8 cells across, parietal tissue ca 1 cell across [?], nucellar cap ca 2 cells across, obturator +; fruit a schizocarp, (drupe with 4, 1-seeded stones); seed exotestal; endosperm 0 (slight) at maturity, ?haustoria, embryo curved or straight, cotyledons large, suspensor long; n = 5, 7-9, 11-14, etc.

5/405: Heliotropium (250), Tournefortia (150, salicylic acid: polyphyletic - see Diane et al. 2002a). Tropical to warm temperate (map: see Frankenberg & Klaus 1980; Flora of China; Gottschling et al. 2004; Flora Base 2005). [Photo - Flower.]

Synonymy: Heliotropiaceae Schrader, nom. cons.

4. Cordioideae Beilschmied

Trees, shrubs or lianes; terpenoid-based quinones +; cambium storied; secondary phloem stratified; nodes 3:3 [Cordia, see below]; petiole bundles (invaginated) annular and with (cortical and) rib bundles; crystal sand and prismatic or columnar crystals +; lamina margins toothed to entire; bracteoles usu. 0; (cymes subdichasial); K valvate to open, persistent to accrescent, C contorted (imbricate); anther connective usu. not produced; pollen often spiny, pseudocolpi 0, (3-porate - Varronia); styles twice divided, stigmas punctate to capitate; ovules straight, tenuinucellate, nucellar cap [Cordia] +; fruit often a drupe, stones 1 (2, 4) (K accrescent [an anthocarp!]); testa vascularized [Cordia], 3-4 layers of transfer cells; endosperm haustoria?, 0, cotyledons plicate, toothed; n = 9, 14-16, 19.

3/330: Cordia (300+: esp. West Indies, heterostylous, inc. Varronia - 100+). Tropical, especially South America (map: see Gottschling et al. 2004; Flora Base 2005; green, Hoplestigma, from Brummitt 2007). [Photo - Flower, Fruit.]

Synonymy: Cordiaceae Dumortier, nom. cons., Hoplestigmataceae Gilg, Sebestenaceae Ventenat, nom. illeg.

5. Ehretioideae Arnott

?Smell; also trees or shrubs; inulins?; cambium storied; (pits vestured - e.g. Ehretia, Rochefortia); petiole bundle arcuate; lamina margins toothed (entire); bracteoles?, flowers (4-)5-merous; K (5-15; valvate), C imbricate or inwards-folded, ± rotate; anther connective usu. not produced; tapetal cells multinucleate; (pollen 3-porate), mesocolpium coarse-reticulate; placentation apical to axile, styles ± well developed, stigmas capitate or elongate; ovules (1/carpel), integument ca 10-12 cells across, parietal tissue 1 cell across, nucellar cap ca 2 cells across, epidermal cells anticlinally elongated, placental obturator +; embryo sac bisporic, 8-nucleate [Allium type]; K accrescent or not, fruit a drupe, stone (1-)2-(4-)seeded, or a schizocarp; endosperm copious to 0, embryo curved, suspensor long; n = 5, 7-11, 13, 16, etc.

8/170: Ehretia (75), Bourreria (50). Mostly tropical (map: see Gottschling et al. 2004; Flora Base 2005).

Synonymy: Ehretiaceae Martius, nom. cons.

6. Lennooideae Craven

Plant echlorophyllous, root parasite; chemistry?; cork?; mycorrhizae 0; sieve tubes with nuclear non-dispersive protein bodies?; stem with cortical bundles; nodes?; leaves reduced to scales; inflorescence capitate; flowers 5-10-merous; K long, narrow, free; pollen tube callose?; nectary 0; G [5-16], placentation axile, style stout, stigma capitate or lobed; ovule type?; fruit a drupe, irregularly schizocarpic, (± circumscissile), K and C persistent; exotesta with fine reticulate thickening; endosperm starchy, ?haustoria, embryo minute, undifferentiated; n = 9.

3[list]/7. S.W. U.S.A. to N. South America (map: from Brummitt 2007).

Synonymy: Lennoaceae Solms-Laubach, nom. cons.

• Many Boraginaceae have rough to hispid, spiral, exstipulate leaves, the inflorescence is cymose, scorpioid and spirally coiled when the flowers are in bud, and the flowers are radially symmetric, the corolla is often more or less rotate, and the gynoecium is often clearly 4-lobed, 4-ovulate, and bicarpellate. Major groupings within the family are easy enough to recognise.

• Boraginoideae - the "typical" borage - are usually herbs that can be recognised by their often spiral leaves the hairs on which have distinctive white bases and by their coiled, cymose inflorescences. The flowers lack one or both bracteoles and often have rotate corollas; the style is gynobasic, and the fruit has four nutlets which may be ornamented with various kinds of hooks and other projections.

• Heliotropioideae are often vegetatively like Boraginoideae and also have similar inflorescences and flowers, but the style is terminal and the stigmatic head is almost plug-like. The fruit is often a schizocarp. The stem may oxidise, the slash turning reddish.

• Cordioideae and Ehretioideae are both woody, and sterile members can be hard to identify, although quite often the bark is fibrous, the stem is oxidising, and the twigs are whitish in color. Both subfamilies have cymose inflorescences, but the flowers of Cordioideae can often be recognised by their branched styles and capitate stigmas; the style in Ehretioideae is once-divided. The fruits are drupes, surrounded by a persistent and more or less accrescent calyx.

• Hydrophylloideae are mostly herbs, again often hispid and with helicoid cymes, but the corolla is more open than in Boraginoideae, the style is terminal, the placentation parietal, and the fruit is a capsule.

• Lennooideae are echlorophyllous root parasites with congested inflorescences; the flowers are rather boraginoid, although 5-10 merous.

Evolution. Divergence & Distribution. The diversification of primarily woody taxa may have taken place in the mid-Cretaceous, some 90 m.y.a., in South America (Gottschling et al. 2004); Wikström et al. (2001) estimate divergence of the whole Boraginaceae at 81-77 m.y., i.e. rather later and some time in the Ypresian-Thanetian ([Vahliaceae + Lamiales] are the sister clade), with Hydrophylloideae and Boraginoideae separating 59-56 m.y.a.. Moore and Jansen (2006) also suggest rather later dates, with the very end Cretaceous at 67-63 m.y. being a date for the diversification of the woody taxa. Magallón and Castillo (2009: note topology; Gentianales sister, Vahliaceae excluded) suggest an age of ca 77.5 m.y. for both relaxed and constrained penalized likelihood stem datings for this clade.

Divergence within Boraginoideae [Ogastemma + [Lithospermeae, etc.]] is estimated to have occurred some 43 m.y. (56-30) ago (Weigend et al. 2009). Luebert et al. (2011a) suggest Heliotropoideae diversified in the Paleocene or earlier, and within Heliotropium (inc. Tournefortia) diversification began about 45 m.y.a., stem node age is ca 60.7 m.y.a. in the Middle Eocene (see Luebert et al. 2011b for many more details).

The South American Moritzia and Thaumatocaryon, the only Boragineae in the New World are sister taxa, and they in turn are sister to all other Boragineae, which are largely Eurasian; interestingly, there are fossils from North America of late Miocene age that are assignable to this clade, so filling the distributional gap (Weigend et al. 2010). Moore and Jansen (2006) and Moore et al. (2006) outline speciation and distribution in the amphitropical disjunct desert genus, Tiquilia (Ehretioideae), in some detail; it may have originated in the Palaeocene ca 58 m.y. before present but began to diversify only rather later, some 33-38 m.y.a., and with repeated dispersal from W. North America to W. South America. Heliotropium sect. Cochranea is also a notable endemic group of the Atacama Desert (Luebert & Wen 2008). There have been a number of New World intercontinental dispersal events within Cryptantha s.l., again nearly all in the north->south direction (Hasenstab-Lehman & Simpson 2012, see also Guilliams & Baldwin 2011); the lopsided directionality of such events seems to be connected with the behaviour of the migrating birds that are likely to have dispersed the fruits.

Echium is a good example of "island woodiness". Woody, more or less tree-like (up to 3 m tall) and sometimes monocarpic species have evolved on Macaronesia from herbaceous ancestors. Divergence within Echium may have begun some 20.6 m.y.a., but the Macaronesian diversification - there seem to have been two reversions to the herbaceous habit, and the majority of the species are on the Canary Islands - can be dated to a mere (6.3-)3.9(-1.5) m.y.a. (Böhle et al. 1996; Stöcklin 2011; García-Maroto et al. 2009: see Mansion et al. 2009 for other Mediterranean insular endemic Boraginoideae).

Pollination Biology & Seed Dispersal. Floral evolution shows much of interest in this group, although lacking both a comprehensive phylogeny as well as developmental studies of the more distinctive flowers, details remain poorly known. Several taxa have flowers that are not the normal 5-merous asterid flower. These include Codon (10-12-merous, ex Hydrophyllaceae; the only African member of that family in its old circumscription), Hoplestigma, and Lennooideae (see also the [asterid I + asterid II] clade). The first two of these have many more stamens and petals than normal, but a simple bicarpellate gynoecium; Lennooideae also show an increase in carpel number. Both the petals and stamens of Hoplestigma are described as being in several series (Goldberg 1986), and its floral morphology and development would clearly repay investigation.

Boraginoideae are well known to have a gynobasic style, but the terminal style of Heliotropoideae, at least, may be derived from the gynobasic condition. In the latter the pollen transmitting tissue proceeds to the base of the gynoecium (e.g. Hanf 1935).

Pollination is predominantly by insects. North temperate megachilid osmiine bees like Hoplitis species of the Annonosmia-Hoplitis group collect pollen from concealed-pollen flowers of this family and/or members of Fabaceae-Faboideae. This odd pairing is perhaps because both groups of plants have pyrrolizidine alkaloids and/or nutrients that are essential for larval development of the bees (Sedivy et al. 2013). Basal Halictidae pollinate both Boraginoideae and Hydrophylloideae (Patiny et al. 2008).

In Boraginoideae the corolla often shows color changes on aging, pink to blue, yellow to pink to blue, yellow to white; p.H. changes of the cell sap are involved in the shift pink to blue, and perhaps cell turgor changes in the shift of the colour of the "eye" of the flower from yellow to white (Weiss 1995; Nuttman & Wilmer 2008). Such changes seem to affect pollinator behaviour (Casper & La Pine 1984; Nuttman & Wilmer 2008 and references). In a number of Boraginoideae buzz pollination occurs; nectar is also produced by these flowers (Teppner 2011). Heterostyly also occurs in some Boraginoideae (e.g. Cohen et al. 2012); in one of the genera showing heterostyly, Lithospermum, there have also been spectacular increases and decreases in corolla tube length (Cohen 2012).

Nutlets of Boragineae may have elaiosomes and are then dispersed by ants, while in taxa like Cynoglossum the nutlets have glochids and are dispersed in the fur of larger animals (Selvi et al. 2011). Some species of the large genus Cryptantha, especially diverse in western North and South America, have inflorescences with basal, cleistogamous flowers and non-dispersing fruits (Grau 1983). Wellstedia is a tumbleweed (?all species), and its capsules open only when wetted (Thulin & Johansson 1996).

Ecology & Physiology. Heliotropium, especially section Orthostachys, contains perhaps ca 150 species with C₄ photosynthesis, and also intermediates between C₃ and C₄ photosynthetic pathways with C₂ photosynthesis (Vogan et al. 2007; Sage et al. 2011).

The holoparasitic Lennooideae may be sister to - or even a clade within - Ehretioideae (see below). It has been suggested that they parasitize their close relatives (Smith et al. 2000), but their hosts are various. More work is needed to clarify the evolution of this distinctive parasitic clade.

Plant-Animal Interactions. Boraginaceae (including Hydrophylloideae) are not often eaten by caterpillars (Ehrlich & Raven 1964). However, wilting plants and/or flowers of Boraginoideae and Heliotropoideae, especially the latter, are visted by adult butterflies (Danainae, Ithomiinae) and moths (Ctenuchidae, Arctiidae); the pyrrolizidine alkaloids the plants contain are used in their pheromones or are deterrents to feeding by other animals (see also Crotalaria and some Apocynaceae and Asteraceae-Asteroideae: Edgar et al. 1974; Ackery & Vane-Wright 1984 [considerable detail for the danaines]; Boppreé 1986; Brown 1987). Cordia (Cordioideae) is also sometimes visited, although it is not known to contain these alkaloids. 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).

Bacterial/Fungal Associations. Holm (1979) noted that some Boraginoideae and Hydrophylloideae have similar rusts.

Vegetative Variation. For secondary woodiness in Echium, see above. Leaves subtending branches are sometimes displaced up the branches they subtend in Tournefortia. The growth pattern of some species of Cordia, including the myrmecophilous species, is distinctive: the apex of the stem aborts, some branches are plagiotropic, while one becomes orthotropic and forms the renewal shoot. The inflorescence can also be oddly placed.

Chemistry, Morphology, etc. The hydroxycinnamic acid depside, rosmarinic acid, is known from Boraginoideae and Hydrophylloideae (as well as some Lamiaceae: Mølgaard & Ravn 1988). Taxa with root trichoblasts in radial files are quite common in Boraginaceae s.l.

There are usually many veins diverging in the corolla lobes of Boraginaceae s.l., but not in Wellstedia. There is considerable variation in ovule and endosperm development, conveniently summarized by Khaleel (1985). A variety of septal structures are produced in this group (see Gottschling 2004). There is controversy as to whether the ovules in some Boraginaceae s.l. are crassinucellate or tenuinucellate. Given that ovules with even a single layer of parietal tissue are crassinucellate by some definitions, Boraginoideae, for example are tenuinucellate, while Ehretioideae and Heliotropoideae are crassinucellate, Hydrophyllaceae s. str. may have both conditions (e.g. Di Fulvio 1981, 1987; c.f. Gottschling 2004; Berg 2009). The style in at least some Boraginoideae and Hydrophylloideae apears to be hollow (Guéguen 1901). Suspensor size in the embryo varies considerably in this group; I have not attempted to see if variation correlates with clades. The relationships of the several-seeded capsules of Hydrophylloideae to the few-seeded indehiscent/schizocarpic fruits of most of the rest of the group are unclear, but parallelisms and/or reversals would seem to be the order of the day. There is variation in the presence of the mitochondrial coxII.i3 intron (two species sampled...).

Within Boraginoideae, fructans are absent in annual species but also in the perennial Alkanna; starch may sometimes also be present (Bourdu 1957; Meier & Reid 1982). Trichodesma has opposite leaves and the pendulous and campanulate flowers are borne in a congested inflorescence at the end of a rather long peduncle. Echium has obliquely monosymmetric flowers, while the flowers of some species of Nonea may be vertically monosymmetric, the abaxial stamen being much longer than the others (the flowers of Echiochilon are also monosymmetric - I would guess obliquely so); the flowers of Cerinthe have an oblique plane of symmetry (Selvi et al. 2009), although the flowers are functionally polysymmetric. With pollen grains at ca 4.1 µm long, Cryptantha clevelandii has about the smallest grains of any flowering plant (Hargrove & Simpson 2003). Amsinckia has very strongly bilobed cotyledons. Thulin and Johansson (1996) described the capsule of Wellstedia as being septifragal, Reteif and van Wyk (2008) as being loculicidal; the latter appear to be correct. The ovule here has a distinctive shape caused by a chalazal projection (e.g. Reteif & van Wyk 2008).

Acicular protein bodies are found in the nucleus of sieve elements in Hydrophylloideae. The mesocolpium is coarse-reticulate, as in some Boraginaceae s. str. (Wagenitz 1992). Di Fulvio (1989a) described the ovules of Nama as being crassinucellate, but the tenuinucellate condition seems to be common (e.g. Berg 2009); for seed coat morphology in Nama, see Chance and Bacon (1984). For details of embryogenesis, seed coat, etc., see also Berg (2009 and references) and di Fulvio (1987, 1990). Tournefortia astrotricha (Heliotropoideae) lacks inulin. Details of embryology are taken from DiFulvio (1978). The central foliar trace of Cordia (Cordioideae) is at least sometimes a striking inverted "C" when it joins the central stele, but I do not know how widespread this character is (see Neubauer 1977 for nodal anatomy of Cordia myxa - also modified 1:3). Ehretioideae are heterogeneous in wood anatomy; both Antrophora and Lepidocordia have vessels in radial groups, apotracheal parenchyma, and fibre tracheids with bordered pits (Gottwald 1982). In embryology Ehretioideae are perhaps closest to Heliotropioideae (Diane et al. 2002a). The embryology of Lennooideae is largely unknown.

For general information on Codon in particular, see Retief and van Wyk (2005), Retief et al. (2005) and Weigend and Hilger (2010). For other information, see Gürke (1891: general), Svensson (1925: embryology), K. A. Wilson (1960: Hydrophyllaceae, general), Khaleel (1977: testa anatomy), Prósperi and Cocucci (1979: callose, in Boraginoideae, variable in Hydrophylloideae, sampling needs to be extended), Gottwald (1982), Fisher et al. (1989: sieve tubes with nuclear non-dispersive protein bodies), Heubl et al. (1990: esp. Cordia), Al-Shehbaz (1991: general), Thulin and Johansson (1996), Di Fulvio (1997: protein inclusions in nucleus), Hartmann and Witte (1995), pyrrolizidine alkaloids, Gunstone (1992) and Velasco and Goffman (1999: fatty acids, esp. gamma linolenic acid, but not restricted to Boraginoideae, see Gunstone 1992), Förther (1998: esp. Heliotropioideae), Diane et al. (2002b: transfer cells), Buys and Hilger (2003: inflorescence morphology), Gottschling et al. (2004: diversification), Aniszewski (2007: alkaloids), and Guignard (1893: ovules vascularized), Millsaps (1940), Venkateswarlu and Atchutaramamurti (1955), and Johri and Vasil (1956) - all embryology, etc. For floral morphology in Hydrophylloideae, see Hilger (1987) and Hofmann (1999). For Boraginoideae, see Y. Heslop-Harrison (1981) and Bigazzi and Selvi (2000) for the morphology of stigma papillae, Hilger (1985) for fruit development, Seibert (1978: Lithospermeae), Ovczinnikova (2007) and Simpson and Hasenstab (2009: Cryptantha, see the cover photograph!) for fruit morphology, and Rabaey et al. (2010: vestured pits, ± correlations with clades within Boraginoidae). For pollen morphology of Boraginoideae, see Weigend et al. (2009), for Boragineae, Bigazzi and Selvi (1998), for Cordioideae, see Nowicke and Miller (1990), and for Ehretioideae, see J.-X. Liu et al. (2003). See The Parasitic Plant Collection for general information about Lennooideae.

Phylogeny. Boraginoideae are sister to rest of the group, and this latter clade may include Codon (ex Hydrophyllaceae) and Wellstedia, both African, as clades successively sister to the remainder (e.g. Luebert & Wen 2008). However, the position of Wellstedia - and Codon - must be confirmed; the former linked with the other two Boraginoideae in the analysis in Moore and Jansen (2006). Two groups of ex Hydrophyllaceae also are successive sister taxa within the other major clade in some reconstructions; Nameae in particular may be sister to the [Cordioideae + Heliotropoideae + Ehretioideae] clade (Olmstead & Ferguson 2001; Moore & Jansen 2006, low bootstrap but high posterior probabilty; Luebert & Wen 2008). Nameae include the only woody and tropical members of Hydrophyllaceae s. str. (i.e., excluding Hydrolea, see below). However, Gottschling et al. (2001), looking at the secondary structure of the ITS1 transcript, found Hydrophyllaceae s. str. to be monophyletic (the position of Codon is uncertain) and sister to [Heliotropoideae [Cordioideae + Ehretioideae]] - in the discussion above I follow this topology. Boraginaceae and Hydrophylloideae also have meroterpenoids, rusts (see above) and very variable endosperm development in common - all plesiomoprphic?? Nazaire and Hufford (2012) sampled the whole Boraginaceae in the course of placing Mertensia. Support was quite good for the structure [Boraginoideae [Hydrophylloideae + the rest]], further major relationships were similar to those of Gottschling et al. (2001), but again support was weak. Lennoa and relatives were sister to Cordioideae, the two being embedded in a paraphyletic Heliotropoideae in a nuclear gene analysis, but embedded in Ehretioideae in the chloroplast and combined analyses (Nazaire & Hufford 2012). They will probably be included in Ehretioideae. See also Ferguson (1999) for relationships.

Långström and Chase (2002) discuss tribal relationships within Boraginoideae. Within Lithospermeae, the limits of Lithospermum itself are to be extended (Weigend et al. 2009; Cohen & Davis 2009a, esp. b, 2012), however, the tree was poorly supported and the addition of relatively few (22) morphological characters had a major effect on support values and some on topology (Cohen & Davis 2011). Vegetative and floral features are highly homoplastic when optimised on the tree (Cohen & Davis 2011). For the limits of Lithospermeae, see also Saadati et al. (2011); Lithodora is polyphyletic (Thomas et al. 2008). Trigonotidae are to be completely dismembered, its two South American genera being sister to the Eurasian Boragineae (Weigend et al. 2010). For the phylogeny of insular Echium, see García-Maroto et al. (2009). Cynoglossum is likely to be paraphyletic (Selvi et al. (2011), indeed, although the monophyly of Cynoglosseae is quite well supported, it includes representatives of just about all tribes of Boraginaceae ever described (Nazaire & Hufford 2012). Nazaire and Hufford (2012: Wellstedia not included; see also Cohen 2011a) found quite good support for the relationships [Codoneae [Echiochileae [Cynoglossseae [Boragineae + Lithospermeae]]], the position of Echiochileae having the least support.

For the phylogeny of Cordioideae, see Gottschling et al. (2003); Coldenia is sister to the rest of Cordioideae and Saccelium is included in Cordia s. str. For Cordia s. str. and its immediate relatives, see Miller and Gottschling (2007) and Weeks et al. (2010).

For relationships and evolution of habit, etc., in neotropical Heliotropium, see Luebert et al. (2011b).

The distinctive West African Hoplestigma belongs around here (see e.g. Hallier 1911). It has been placed near Boraginaceae because of its scorpioid cymose inflorescence, absence of bracts, pollen with pseudocolpi (as in Ehretioideae: Nowicke & Miller 1989; see also Takhtajan 1997). Molecular data place it close to Cordia (K. Wurdack, pers. comm.). Hoplestigma is little known, but there appear to be three vascular traces in the base of the petiole; its nodal anatomy may be similar to that of Cordia.

Lennooideae are often associated with Boraginaceae and/or Hydrophyllaceae (Cronquist 1981; Takhtajan 1997; esp. Yatskievych et al. 1986). rps2 data even suggest a position within Ehretioideae (see also Nazaire & Hufford 2012). Both Ehretia + Lennoaceae have a shared intron in the mitochondrial gene cox1, and Tiquilia in particular is sister to Pholisma in Smith and dePamphilis (1998; Smith et al. 2000; Olmstead & Ferguson 2001; Hardy & Cook 2012). (Tiquilia and immediate relatives, mostly plants of American deserts, are unusual within Ehretioideae in being herbs, or shrubs that flower very quickly, and their inflorescences may be crowded. Their fruits are dry, and secondary veins in the leaves go to the sinuses [Richardson 1977]). However, until there is further resolution of phylogenetic relationships, I have retained Lennooideae as separate from Ehretioideae. For other relationships within Ehretioideae, see Gottschling and Hilger (2001).

• Hoplestigma: deciduous tree, buds perulate, calyx connate, irregularly-splitting, petals 11-14, basally connat, stamens 20-35, adnate to the base of the corolla, carpels two, four ovules borne on intrusive parietal placentae, and long style branches that are bent outwards, then inwards, and terminated by U-shaped, expanded stigmas.

Classification. Family names are being described in this part of the tree (e.g. Weigend & Hilger 2010), so the classification of the group is somewhat in limbo. Gottschling et al. (2005) equivocate as to whether Coldenia should be included in their Cordiaceae - if it is, as here, the clade has few apomorphies. Luebert and Wen (2008) suggest a narrow circumscription for Cordiaceae (see below), their Hydrophyllaceae are paraphyletic, and they of course do not include the distinctive Hoplestigma.... If narrow family limits are adopted, then, depending on the phylogeny, there could be some 11 families in this clade - hardly a desirable outcome, perhaps. Hence I largely follow Nazaire and Hufford (2012) who recognise a broadly circumscribed Boraginaceae that includes five subfamilies, as well as five tribes within Boraginoideae, the focus of their study (for tribes, see also Långström & Chase 2002).

Generic limits in Boraginoideae need much attention. Hasenstab-Lehman and Simpson (2012) adjust the limits of Cryptantha; genera like Lithosperma, Trigonotis and Anchusa are polyphyletic (e.g. Nazaire & Hufford 2012). The limits of Lithospermum have been adjusted, but the relationships of names to clades around there is still unclear (Cohen & Davis 2009b; Cohen 2011b). For generic limits in Cordioideae, see Gottschling et al. (2003); Saccelium is included in Cordia s. str.; Miller and Gottschling (2007) segregated Varronia from Cordia, although since the two are sister taxa, strictly speaking this is not necessary, even if the split is supported by morphology. Generic limits in Heliotropoideae also need attention (Diane et al. 2002a; Hilger & Diane 2003; Luebert et al. 2011a, b); Craven (2005) suggested that the whole lot were best placed in Heliotropium s.l. - a suggestion not without merit. For genera in Ehretioideae, see Miller (2003).

Previous Relationships. Boraginaceae have sometimes been associated with Lamiaceae (Lamiales) because both often have gynobasic styles and fruits with four separate nutlets, but the latter have iridoids, opposite leaves, square (not rounded) stems, monosymmetric flowers usually with 4 stamens, endosperm with haustoria and embryo with a long suspensor, and the two are not close. Furthermore, the radicle in Boraginaceae points upwards in fruit, while in Lamiaceae it faces downwards. No putative relative of Boraginaceae s. l. has alkannin or pyrrolizidine alkaloids. Pteleocarpa, with vestured pits, is usually included in Boraginaceae s.l., but it is here placed in Gelsemiaceae (Gentianales). Hydrolea, ex Hydrophyllaceae but with axile placentation, is here to be found in Solanales. Hoplestigmataceae were included in the Violales by Cronquist (1981), perhaps because of their parietal placentation.

Thanks. I am grateful to Mark Gottschling for discussion, and also the tree used here.

Synonymy: Boraginales Berchtold & J. Presl, Cordiales Martius, Echiales Lindley, Ehretiales Martius, Hydrophyllales Martius - Boraginanae Doweld

VAHLIACEAE Dandy   Back to Unplaced

Herbs or subshrubs; iridoids +; nodes 1:1; petiole bundle arcuate; hairs uniseriate-glandular; leaves opposite; flowers small; K valvate, C free; nectary +; G inferior, [2(-3)], 1-locular, placentae apical, confluent, styles distinct, diverging, stigmas ± capitate; ovules many/carpel, bitegmic, micropyle endostomal, outer integument 2-3 cells across, inner integument 2-3 cells across, endothelium 0, parietal tissue 1 cell across; fruit a septicidal capsule, K persistent; exotestal cells ± elongated, outer or all walls thickened, endotestal cells with well-developed U-thickenings, neither lignified, raphe disappears; endosperm slight; n = 6, 9.

1[list]/8. Africa and Madagascar to India (map: from Bridson 1974; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003).

• Vahliaceae are densely glandular-pubescent herbs or subshrubs with opposite entire leaves and rather spreading basically cymose inflorescences bearing small flowers with inferior ovaries; the fruit dehisces at the apex inside the sepal lobes. Vahliaceae look rather like some Rubiaceae, however, there are no stipules, the relatively large, persistent calyx is valvate, the petals are free, and the gynoecium has a single loculus with apical placentae.

Evolution. Divergence & Distribution. Magallón and Castillo (2009) offer estimates of ca 83 m.y. for relaxed and constrained penalized likelihood datings for stem group Vahliaceae - but note topology.

Friis and Skarby (1982) described two species of Scandianthus from the Upper Cretaceous of Sweden which they tentatively associated with Vahlia (see also the morphological analysis in Martínez-Millán 2010); they all have an unilocular gynoecium with apical-lateral placentae and free styles and fruits with septicidal dehiscence. Friis and Skarby (1982) also noted a phenetic similarity to some Hydrangeaceae, Phyllonomaceae, Escalloniaceae, and even some Saxifragaceae s. str. However, Scandianthus has ten stamens, a decidedly unusual number for any member of the [asterid I + asterid II] clade - if indeed it is to be placed here.

Chemistry, Morphology, etc. Although the ovary has only a single locule, dehiscence of the fruit occurs between the styles, and this is normally equivalent to dehiscence along the septal radii.

Some information is taken from Thouvenin (1890), Mauritzon (1933: ovules), and Cutler and Gregory (1998: anatomy).

Classification. Bridson (1974) monographed the family.

Previous relationships. Vahliaceae were included in Saxifragales by Cronquist (1981) and Takhtajan (1997).

Synonymy: Vahliales Doweld

[GENTIANALES + SOLANALES]: non-hydrolysable tannins usu. 0; nodes 1:1; x = 11 or 12.

GENTIANALES Berchtold & J. Presl  Main Tree, Synapomorphies.

Iridoids [different pathways!], monoterpene indole alkaloids, (O-methylated) flavones and flavonols +, myricetin rare; 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.

Note: Possible apomorphies are now being added throughout the site; they 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 because there is very considerable homoplasy, with variation within and between clades, for most characters. Furthermore, the basic information for all too many characters is very incomplete, often 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...

Evolution. Divergence & Distribution. Gentianales may be some 89-83 m.y. old (Wikström et al. 2001), but timing of diversification within the clade is unclear since Dialypetalanthus is shown sister to the rest - here it is included well within Rubiaceae. Janssens et al. (2009) date stem group Gentianales to 101±7.9 m.y.a. and the crown group to 79±10.2 m.y.; comparable figures are 108 and 78 m.y. in Bremer et al. (2004) and (97-)76(-56) and (75-)52(-35) m.y. in Lemaire et al. (2011b: [Gentianales + Solanales]). Magallón and Castillo (2009) suggest an age of ca 81 m.y. for stem Gentianales; Boraginaceae are included in its sister clade, Vahliaceae excluded.

Endress (2011a) suggested that a key innovation in Gentianales was tenuinucellate ovules.

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.

Chemistry, Morphology, etc. 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, plasmodial tapeta being known from some species of Gentianaceae, Rubiaceae and Apocynaceae (Furness 2008a). Most families have taxa with bi- or trinucleate pollen grains. 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) found rather different relationships - Rubiaceae are sister to Loganiaceae, Gentianaceae, Gelsemiaceae and Apocynaceae. Relationships between these last four families are still not clear. M. Endress et al. (1996) found the relationships Gelsemiaciaceae [[Strychnaceae + Geniostomaceae (well supported)] Apocynaceae], see also B. Bremer and Struwe (1992). In other analyses, as in the tree below, there is weak support for a relationship between Gelsemiaceae and Apocynaceae (Backlund et al. 2000; Jiao & Li 2007: for the tree, see also B. Bremer 1999; Rova et al. 2002), while Soltis et al. (2011: sampling) found some support for a sister group pair [Gentianaceae + Apocynaceae].

Previous Relationships. The circumscription and relationships of Loganiaceae are a key to understanding the both the past and present circumscription and relationships of Gentianales. 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 separate clades in Lamiales (Scrophulariaceae, near Gesneriaceae, Plocospermataceae, Stilbaceae and Tetrachondraceae respectively), while Desfontainia (Desfontainiaceae) is in Bruniales, a campanulid/asterid II (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, Voyria.

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, (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), (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, suspensor haustorium +; 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]

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 articulated; heterostyly esp. common; C valvate; (pollen grains 3-celled); (ovules campylotropous), (micropyle 0), integument 1-14 cells across; (antipodal cells persist); (testa ca 14 cells across - Schradera; (suspensor haustorium +); loss of atpB promoter.

Psychotria s. str. (1400: ?inc. Myrmecodia, Hydnophytum [55]), Galium (400), Spermacoce (inc. Borreria: 275), Palicourea (250: inc. Cephaelis [100]), Oldenlandia (250), Hedyotis (200), Lasianthus (180), Argostema (100), Morinda (80), Gaertnera (70), Schradera (55), Margaritopsis (50). Worldwide. [Photo - Fruit.]

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[?].

2. [Luculia [Acranthera + Coptasapelta]]

(Raphides +).

3/53: Acranthera (35). Himalayas, China, to Malesia.

3. Cinchonoideae Rafinesque

Corynanthean and complex indole alkaloids +; (raphides + - Hillieae, Hamelieae); C left contorted; ovules often numerous; fruits usu. dry.

Timonius (150), Guettarda (80). Predominantly Neotropical.

Synonymy: Catesbaeaceae Martynov, Cephalanthaceae Rafinesque, Cinchonaceae Batsch, Coutareaceae Martynov, Guettardaceae Batsch, Henriqueziaceae Bremekamp, Naucleaceae Wernham

4. Ixoroideae Rafinesque

(Latex +); (calycophylls +); C contorted or cochleate; (pollen buds +); (placentation parietal), (stigma not bilobed - e.g. Gardenia); ovule number variable; fruits often fleshy; embryo short [?distribution].

Pavetta (400), Ixora (300), Mussaenda (200), Coffea (125), Randia (100), Tricalysia (90), Gardenia (60), Bertiera (55). Pantropical.

Synonymy: Coffeaceae Batsch, Dialypetalanthaceae Rizzini & Occhioni, nom. cons., Gardeniaceae Dumortier, Hameliaceae Martius, Randiaceae Martynov, Sabiceaceae Martynov

• Members of the family can be recognised in the vegetative state by their opposite, sometimes whorled, and entire leaves that often dry blackish and interpetiolar stipules that have axillary colleters. The ovary is inferior, the flowers are polysymmetric, often with a narrow corolla tube and spreading lobes, and are quite often rather small and aggregated into heads.

Evolution. Divergence & Distribution. Antonelli et al. (2009) suggest that divergence within Rubiaceae began a mere (68.8-)66.1(-63) m.y.a. K. Bremer et al. (2004) suggest an age for stem Rubiaceae of (88-)78(-68) m.y., Bremer and Eriksson (2009) also provide a comprehensive dated phylogeny for the family, but with rather older dates. They suggest ages of some 90.4 m.y. for stem and about 86.6 m.y. for crown Rubiaceae; stem ages in Lemaire et al. (2011b: [Gentianales + Solanales]) are (86-)73(-60) (ages in Rubiaceae table) or (75-)52(-35) m.y. (ages in asterid table) and crown ages (77-)62(-50) or (70-)62(-55) m.y. As a final estimate, crown Rubiaceae are dated to (87.9-)84.9(-80.8) m.y. by Manns et al. (2012).

Graham (2009) summarized the fossil history of Rubiaceae - there are no certain records from the Cretaceous or Palaeocene.

Bremer and Eriksson (2009) suggested that the split of Ixoroideae and Cinchonoideae was approximately 73.1 m.y.a., with subsequent divergence within those two subfamilies beginning some 59.6 and 34.7 m.y.a. respectively. Manns et al. (2012: HPD estimates) give many dates for the family, focusing on Cinchonoideae; they date the divergence of Ixoroideae and Cinchonoideae at (84.5-)78.5(-71.7) m.y.a. Divergence within Cinchonoideae was dated to (65.6-)57.4(-50.3) m.y. (ca 38.7 m.y. in Bremer & Eriksson 2009), while Luculia had diverged from [Coptosapelta + Acranthera] (see below) back in the Late Cretaceous (Manns et al. 2012). There are also many dates in Lemaire et al. (2011b: Luculia, etc. not included in family tree): The divergence of Cinchonoideae and Ixoroideae happened (68-)60(-54) m.y.a, crown Cinchonideae are (52-)36(-24) m.y. old and crown Ixoroideae (60-)55(-51) m.y.; crown Rubioideae are (60-)53(-48) m.y. old. However, Lemaire et al. (2011b), also unaccountably note "more recent stem node ages" of 26 m.y. for Cinchonoideae, all rather confusing.

Antonelli et al. (2009) date Cinchonoideae at some (54.6-)51.3(-47.8) m.y.; Rubiaceae had moved into South America from the Old World via a North Atlantic land bridge; they also date divergences within the South American members of the family, especially within Isertieae and Cinchoneae. Manns et al. (2012), however, suggested that Ixoroideae and Cinchonoideae started off 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 in the Eocene (Manns et al. 2012). Tosh (2009) summarized biogeographical studies on Madagascan Rubiaceae.

The minimum divergence time of Rubieae is (37.6-)28.6(-20.2) m.y.a. (Bremer & Eriksson 2009) and their origin is Old World (Soza & Olmstead 2010a), although Graham (2009) suggested that Galium is known from rocks at least 55 m.y. old. Coprosma may have originated in New Zealand a mere 15-10 m.y.a., whence it was dispersed by animals maybe some 16 times widely across the Pacific, including Hawaii (Cantley & Keeley 2012).

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).

Pollination Biology & Seed Dispersal. Many Rubiaceae have rather small flowers but make them attractive to pollinators in a variety of ways. Large, coloured calyces (calycophylls) are particularly common in Ixorodinae and help to attract the pollinator. The Old World Mussaenda is an example with its its 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), while in the New World Warsewiczia has similarly conspicuous individual sepals. 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 Cephalanthus and Naucleeae have flowers aggregated into spherical heads, while Cephaelis (= Palicourea: Rubioideae) has a condensed inflorescence immediately subtended by paired and coloured inflorescence bracts.

Henriquezia has a monosymmetric corolla. 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, pollen being catapulted onto the pollinating insect; the flowers are monosymmetric and may be inverted (Delprete 2009). Secondary pollen presentation is notably common in Cinchonoideae (Nilsson et al. 1990; Puff et al. 1996; de Block & Igersheim 2001), but it also occurs in Ixoroideae (e.g. Vanguerieae - see Tilney et al. 2011); pollen is presented on tips of the styles. Hundreds of Rubioideae in particular are heterostylous, and there have been several reversals to homostyly (Ferrero et al. 2012). Dioecy occurs in Vanguerieae, but with apparent reversals to hermaphroditism (Razafimandimbison et al. 2009), and also in New World Galium, here with reversals to polygamy (Soza & Olmstead 2010b). Taxa like the sister genera Gaertnera (see Malcomber 2002) and Pagamea have secondarily superior ovaries (Igersheim et al. 1994).

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/animal-dispersed fruits, and herbs/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). 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 root spines arising from the stem, inflorescence, end even the torn and eaten surfaces of the leaves (Huxley 1978; Jebb 1991; Huxley & Jebb 1991 for the taxonomy of the group). Myrmecophily has 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, and their presence is correlated with development of distinctive colleters (Lersten 1974 and references). Bacteria of the ß-proteobacterium Burkholderia have been isolated from the nodules (van Oevelen et al. 2004). Burkholderia is a nitrogen-fixing symbiont in the root nodules of some Faboideae, but 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).

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, being 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).

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. 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).

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 [asterid I + asterid II] clade). 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). 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 the odd cylcotide proteins, scattered in Rubioideae, see Gruber et al. (2008), for alkaloids, see Aniszewski (2007) and Berger et al. (2012), 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, and Rutishauser (1984: stipules). See also Lloyd (1902: esp. suspensor, very variable), Fagerlind (1937: embryology and much else), Weberling (1977: inflorescences), Rogers (1984: Gleasonia, etc.), Puff et al. (1993a: pollen, fruits in Mussaenda et al., 1993b, much detail about Schradereae), Huysmans et al. (1997: orbicules in Cinchonioideae), Vinckier et al. (2000: orbicules in Ixoroideae), Verstraete et al. (2011: orbicules, not integrated with earlier observations?), Jansen et al. (2002a, 2003: Al accumulation), Delprete (2004: morphology), Dessein et al. (2005a) and Verellen et al. (2007), both pollen, not really a great help taxonomically, Gamalei et al. (2008: phloem), Lersten and Horner (2011: calcium oxalate crystal morphology in Naucleeae [Cinchonoideae], interesting variation), 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 the three genera do form a clade in Manns et al. (2012), it is sister to Rubioideae. Luculia and Coptasapelta differ considerably in morphology: 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 is sister to Coptasapelta (see also Bremer & Eriksson 2009), these two have little morphologically in common (Rydin et al. 2009a). 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 (Rydin et al. 2009a). 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; relationships within Spermacoceae have been investigated further by Groeninckx et al. (2009a, esp. 2009b), Rydin et al. (2009b) and Guo et al. (2013: Asian taxa). Wikström et al. (2013) is an 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.

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). Morinda, with its apparently distinctive capitate inflorescences, is in fact polyphyletic (Razafimandimbison et al. 2009b).

For phylogenetic relationhips within Cinchonoideae, see Andreasen and Bremer (1996), Rydin et al. (2009), and especially 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 the more comprehensive analysis in Manns et al. (2012). For relationships in Naucleeae, see Razafimandimbison & Bremer (2002).

Within Ixoroideae, Ixora (Ixoridinae) is paraphyletic (Mouly et al. 2009a, b, see also Andreasen & Bremer 2000). Sipanea and Posoqueria form a clade (Razafimandimbison et al. 2011). Condamineae, a basal clade, are circumscribed by Kainulainen et al. (2010); they are very heterogeneous, and include Mastixiodendron, the morphologically even more distinctive Dialypetalanthus, several genera with calycophylls (see above), 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 monotypic clades; see Razafimandimbison et al. (2009a) for the phylogeny of dioecious Vanguerieae. Tosh et al. (2009) have adjusted the limits of the African Tricalysia (see also Tosh 2009), Cortés-B. et al. (2009) looked at Retiniphylleae, Kainulainen et al. (2009) at Alberteae, and Alejandro et al. (2011) at Octropeae.

Two genera are particularly odd morphologically:

• Dialypetalanthus: cork cortical, phloem stratified; K free, C free, opposite K, both in two decussate pairs; A (8-)16-17(-25), not epipetalous, basally connate, anthers basifixed, dehiscing by pores (see Rizzini & Occhioni 1949), bracteoles apparently ad/abaxial (Piesschaert et al. 1997). Oil glands are described as being pervasive (Goldberg 1986). RbcL data suggest that its inclusion in Ixoroideae (e.g. Fay et al. 2000b; esp. Kainulainen et al. 2010).

• Theligonum: iridoids and raphide sacs +; plant monoecious, anemophilous; staminate flowers: paired, opposite, not subtended by leaves; P tubular, ridged, splitting into 2-5 segments; A 2-30, development variable; pollen 4-8-zonoporate; carpellate flowers: G pseudomonomerous, bilocular, 1-locular by suppression, with 1 campylotropous ovule; testa single-layered, walls thin, endosperm with starch, embryo curved (Wunderlich 1971; Rutishauser et al. 1998). Vegetatively Theligonum is a good match with Rubioideae, where it was included by B. Bremer (1996). The differences between it and other Rubiaceae are those that might be expected of a wind-pollinated plant, i.e., breeding system, reduced and modified perianth, many stamens, and only a single-seeded fruit (see Wunderlich 1971 for floral details).

Classification. Robbrecht and Manen (2006) and B. Bremer (2009) should be consulted for a detailed discussion on taxon limits, formal classification, etc. Manns and Bremer (2010) provide a tribal classification of Cinchonoideae and assign nearly all genera to those tribes, at least provisionally.

Bremer (2009) notes that of the ca 611 genera in the family, 1/3 are monotypic - and some are very large and are turning out to be paraphyletic. 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 being described in the context of local phylogenetic analyses... (Groeninckx et al. 2010a, b). Guo et al. (2013) described three new genera from the Asian part of the complex, but another 10-17 names (several already exist) will then be needed to describe this part of the tree... 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 Nepokroeff et al. (1999) 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). 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 are also maintained as separate by Takhtajan (1997) but are included in Rubiales.

Thanks. I am grateful to Elmar Robbrecht for help with the synonymy.

[Gentianaceae [Loganiaceae + Gelsemiaceae + Apocynaceae]]: route I secoiridoids +; internal phloem + [bicollateral vascular bundles]; C tube formation late; syncarpy postgenital; testa with anticlinal walls thickened.

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.

GENTIANACEAE Jussieu, nom. cons.   Back to Gentianales

Herbs to shrubs (trees), mycorrhizal (and echlorophyllous); (plants Al-accumulators), no starch, but oligosaccharides +, monoterpene indole alkaloids, tannins 0; cork?; (vessel elements with scalariform perforation plates); rays often 0; parenchyma septate; nodes 1(-3 or more):1(-3 or more), (+ split laterals); mucilage cells + (0); plant glabrous; (stomata anisocytic); leaves sessile, usu. connate basally, lamina vernation variable, secondary veins ± palmate (pinnate), (stipules +); flowers 4-5(-16)-merous, "disc-like" structure between K and C, C right-contorted, marcescent, (tube formation intermediate), petal epidermal cells elongated and flat; A (extrorse; placentoids +), basally connate; 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 multinucleate - Halenia; diploid to polyploid; multiplying, persistent); fruit a septicidal capsule, calyx often prominent; seeds small to minute; testa multiplicative, 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.]

1. Saccifolieae Struwe, Thiv, V. A. Albert & Kadereit

(Echlorophyllous myco-heterotrophic herbs), (shrubs); chemically unknown; (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]]]]]: ?

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); ovary ± bilocular; (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.

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 connate basally), colleters +/0; (A extrorse); pollen variously clumped, (asymmetric), 1-6-porate with smooth to scabrate exine, 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 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 +.

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; (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; 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

• Gentianaceae often lack vegetative indumentum; many are bitter-tasting herbs. Their almost sessile, entire, opposite leaves are joined at the base and have ascending venation, and their rather large flowers have a relatively large, persistent calyx, an often marcescent corolla with right-contorted lobes and a bicarpellate gynoecium with parietal placentation. The placentae are deeply bilobed and protrude into the ovary cavity. The saprophytic taxa look very different at first sight!

Evolution. Divergence & Distribution. 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., the age of the node Exaceae + the rest} some 57.4-)49.1, 48.6(-40.1) m.y., and that of [Voyrieae + the rest] some (65.2-)54.0, 46.8(-40.1) (Merckx et al. 2013, q.v. for other dates). 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).

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. Similarly, there was an increase in diversification of Halenia after it moved into Central and South America within the last 1 m.y.; there are 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 "normal" and myco-heterotrophic species are found in genera like Exochaenium and Exacum. Voyriella and Voyria are other myco-heterotrophs, which generally lack root hairs. 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).

Bacterial/Fungal Associations. Paris-type endomycorrhizae involving Glomeromycota are common in Gentianaceae, including the myco-heterotrophic members (Imhoff 1999; Franke et al. 2006).

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. 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, and the pollen is in clumps, whether 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).

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 - are they modified nectaries? Chassot and von Hagen (2008) discuss variation in pollen in Swertia. 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 180^o, 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). Some of these taxa have very reduced cotyledons

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 [asterid I + asterid II] clade), 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 the morphology, etc., of myco-heterotrophic taxa, see Oehler (1927); for information on Voyria in particular, see Johow (1889 and references: anatomy, seed, etc.), Oehler (1927: general), Wood & Weaver 1982; Maas & Ruyters 1986), Bouman and Devente (1986), Bouman and Louis (1990) and Bouman et al. (2002), seed, the latter also ovules, Albert and Struwe (1997; morphological phylogenetic analysis), Struwe et al. 2002, and Franke 2002 (Voyria flavescens).

For information on nodal anatomy, see Post (1958); for seeds, Bouman and Devente (1986) and Bouman et al. (2002); general embryology, see Hakki (1997); for ovule development, see Shamrov (1996), Bouman and Schrier (1979), Bouman et al. (2002), and Vijayaraghavan and Padmanaban (1968); for orbicules, see Vinckier and Smets (2000a); for a summary of pollen variation, see Nilsson (2002) and Nilsson et al. (2002); for chemistry, see Jensen and Schripsema (2002); for the gynoecium, see Shamrov and Gevorkyan (2010b); and for general information, see Struwe and Albert (2002) and the Gentian Research Network.

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 is still somewhat uncertain - it may have diverged before Exaceae, not after it, as suggested above. We also need basic anatomical, chemical and developmental knowledge of Saccifolieae, Exaceae and Voyrieae if the evolution of Gentianaceae is to be understood. The Guayanan Saccifolium, with its distinctive ascidiate leaves, is in a clade with the mycoheterotrophic Curtia, Voyriella, etc., that is sister to all other Gentianaceae (Thiv et al. 1999; Struwe et al. 2002; 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). 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 and there are 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.

Previous Relationships. Although there is evidence from pollen, etc., that Voyria is not particularly similar to the myco-heterotropic Voyriella, etc., its immediate relationships are unclear, although it has bicollateral vascular bundles like many other Gentianales in this part of the tree.

[Loganiaceae + Gelsemiaceae + Apocynaceae]: ?

LOGANIACEAE Martius, nom. cons.   Back to Gentianales

Annual herbs to shrubs or lianes; tryptophane-derived alkaloids, quercetin, kaempferol +; nodes 1:1 or 3:3 (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 valvate (imbicate, contorted, quincuncial), often hairy at the mouth; (A 1, abaxial - Usteria); nectary 0, poorly developed, or on walls of G; G often partly inferior and partly apocarpous (congenitally syncarpous; stylar fusion postgenital), collateral, placentation axile, styles branches +/0, stigma capitate, long-clavate, 2-lobed, or punctate; ovules 1-many/carpel, integument 4-6 cells across; fruit a follicle, loculicidal and/or septicidal capsule, drupe or berry; (seeds embedded in pulp), (placentae fleshy - Gelsemium), exotestal cells papillate or hairy, ± thick-walled and lignified except outer wall; endosperm starchy or hemicellulosic, horny; 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 unique (in this group) to Strychnos and its immediate relatives. The ovules of Mitrasacme have an endothelium and the endosperm is "intermediate" in development. 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 Hasselberg (1937: nodes and stipules), Leeuwenberg (1980: general), Keller (1996: "stipules"), Hakki (1998: Usteria), and Aniszewski (2007: alkaloids).

,b>Phylogeny. For relationships in Loganieae, see Gibbons et al. 92012); generic limits will have to be adjusted.

Synonymy: Antoniaceae Hutchinson, Gardneriaceae Perleb, Geniostomataceae L. Struwe & V. Albert, Spigeliaceae Berchtold & J. Presl, Strychnaceae Perleb

[Gelsemiaceae + Apocynaceae]: nodes 1:1; seeds ± flattened.

Phylogeny. Backlund et al. (2000) note that C17 indole alkaloids, the number of tapetum layers, and cytology support this relationship - and that the presence of quercetin and kaempferol, imbricate corolla, and horny (starchy) endosperm might support a close relationship between Gelsemiaceae and Loganiaceae.

GELSEMIACEAE L. Struwe & V. Albert   Back to Gentianales

Shrubs or lianes; quercetin, kaempferol +; true tracheids +; stomata?; (stipules 2, interpetiolar or short sheathing); flowers heterostylous; A extrorse [Gelsemium] or latrorse; style twice branched; fruit a loculicidal and/or septicidal capsule, K persistent; seeds winged or hairy; testa?; endosperm horny, starchy; n = 8, 10.

2[list]/11. ± Pantropical (map: from Leeuwenberg 1961; van Steenis & van Balgooy 1966). [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). Pteleocarpa has not been incorporated into the description.

• Pteleocarpa - a poorly known west Malesian genus. It has i.a. vestured pits, spiral leaves, largely separate style branches, two ovules/carpel, and a single-seeded, more or less orbicular samara; when in flower, the whole branch is yellow, the leaves being yellow like the corolla. Brummitt (2007) recognized this as a separate family (he described it formally in 2011).

Previous Relationships. Pteleocarpa has been included in Boraginaceae-Ehretioideae, e.g. by Takhtajan (1997); the other genera are ex Loganiaceae.

Synonymy: Pteleocarpaceae Brummitt

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, indole alkaloids, cardenolides + [cardiac glycosides], 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); (petioles also with adaxial bundles); stomata also paracytic (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, 0; G apocarpous, (-8); collateral), style branches elongated, apex alone postgenitally syncarpous, stylar head swollen, adhesive, wet or dry; ovules (hemitropous), integument 6-9 cells across, endothelium 0; (seeds rounded); testa multiplicative, exotestal cells with all walls thickened, (flattened mesotestal crystalliferous cells); extensive polyploidy including triploids, protein crystalloids in the nuclei; also sporophytic incompatibility system present.

415[list]/4555: in 21 groups below, numbering follows subfamilial names cocommonly in use; first two are wildly paraphyletic. Largely tropical to warm temperate (map: from Hultén 1968; see also maps below). [Photo - Flower, Fruit]

1. "Rauvolfioideae"

(Pollen porate), G apocarpous, if syncarpous, placentation axile or parietal; fruit berry, drupe or follicle; (seed with coma - Haplophyton); n = (9) 10, 11, (23).

84/980. Tropical.

Aspidospermeae

Alstonieae Trees.

[Vinceae [Willughbeieae + Tabernaemontaneae]] = Rauvolfioideae Kosteletzky s. str.: ?

Vinceae = Rauwolfieae - 9/100: Rauvolfia (110).

Synonymy: Vincaceae Vest

[Willughbeieae + Tabernaemontaneae]: ?

Willughbeieae - (G connate). 18/130: Landolphia (60).

Synonymy: Willughbieaceae J. Agardn

Synonymy (not checked): Cerberaceae Martynov, Ophioxylaceae Martius, Pacouriaceae Martynov

Tabernaemontaneae G. Don

K with several to many basal colleters; A sessile, anthers with thick, lignified guide rails; nectaries paired; (ovary fusion congenital), stigmatic head complex with a five-lobed upper crest and a thickened basal flange (not); fruit a berry; (seed with aril, ± ruminate, with long hilar groove - Tabernaemontaninae).

15/150: Tabernaemontana (100-120). Northern South America (Ambelaniinae) and pantropical (Tabernaemontaninae).

[Alyxieae, Melodineae, Hunterieae]

Alyxieae

Alyxia (120). n = 9.

Melodineae

Melodinus (75).

Hunterieae

Plumerieae

Synonymy: Plumeriaceae Horaninow

Carisseae (ovary fusion congenital)

Synonymy: Carissaceae Bertolini

["Apocynoideae", Periplocoideae [Baisseeae [Secamonoideae + Asclepiadoideae]]] - APSA Clade: iridoids 0 [this level?]; C right-contorted; anthers with lignified basal appendages [guide rails]; pollen porate; anthers adnate to style head [forming gynostemium], retinaculum formed by trichomes [region of stamen by which it attaches to style head]; stylar head radially differentiated, with a thickened basal flangs; fruit a follicle; seeds comose, coma chalazal, hairs unicellular.

Chemistry, Morphology, etc. See especially Livshulz et al. (2007: general) and Lens et al. (2009: wood characters, not all incorporated in this tree).

2. "Apocynoideae" Burnett

A inserted well below bases of corolla lobes; n = (6-)10, 11 (12).

77/860. Largely tropical.

Wrighteae

C left contorted.

3/29: Wrightia (23). Old World tropics.

Nerieae

4/47: Strophanthus (38). Africa (most) and Europe to Japan and Malesia.

Maloutieae

[Rhabdadenia, Periplocoideae, [Asian clade + New World clade], [Baisseeae [Secamonoideae + Asclepiadoideae]]] - Crown Clade: few wide vessels and several narrow vessels in clusters; vasicentric tracheids +; fibres [not tracheids] in ground tissue; nectary surrounding base of ovary [?level].

Rhabdadenia

Wood fibres very thin-walled, parenchymatous.

1/4. Tropical America.

[Apocyneae + New World clade] = Apocynoideae s. str.: ?

Often lianes; stamen-corolla tube very short; (pollen in tetrads); style head fusiform (with strap-like bands of adhesive), no basal collar.

22/ Largely Malesian-South East Asian, also North Temperate (Apocynum).

[Echiteae, Mesechiteae, Odontadenieae] / New World clade: (pyrrolizidine alkaloids + [inc Anodendron, Alafia])

Echiteae

19/ Parsonsia (120), Prestonia (65). New World, tropical, also New Caledonia (two genera) to Australasia and South East Asia (Echites).

Mesechiteae

5/ Mandevilla (115), Forsteronia (50). New World.

Odontadenieae

7/ New World.

3. Periplocoideae Endlicher

Plants with tuberous roots; C (valvate), tube formation intermediate; stamen-corolla tube very short, staminal feet erect, connate, forming tube around ovary; nectar secreted on margins of staminal feet, rceptacular nectary 0; anthers without lignified guide rails; pollen in tetrads, 4-16 porate, surface smooth; pollen collected on spoonlike 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 leaves; stamen-corolla tube very short; G initially half inferior, style head without basal flange.

Baisseeae

Large lianes; (trichomes branched); (leaves with domatia); (style head with strap-like bands of adhesive).

4/ . Africa. Inc. Dewevrella

[Secamonoideae + Asclepiadoideae]: (fructans/inulin +), monoterpene indole alkaloids 0; C tube formation intermediate; A inserted well below bases of corolla lobes, corona usually staminal, filaments 0, anthers inserted on top of fused tube [specialized ring corona, staminal feet], alternistaminal sections of tube nectariferous, the nectaries behind guide rails; pollinaria erect, pollinia of the one pollinarium from half anthers of adjacent stamens, translator of hardened resinous mostly stigmatic secretion [retinaculum], translator arms [caudicle] 0, corpusculum apical, adhesive; pollen in tetrads when mature, grains inaperturate, surface smooth, orbicules 0; endosperm nuclear (cellular), embryo green; n = 11.

4. Secamonoideae Endlicher

Lianes, climbing by twining; C also left-contorted; pollinia 4, lacking outer wall; granular layer of exine thick.

9/170: Secamone (100). Old World, esp. Madagascar, tropics to temperate.

5. Asclepiadoideae Burnett

(Included phloem +); (leaves spiral); C also valvate; anthers bisporangiate, dithecal, pollinia 2, microsporogenesis simultaneous [pollen tetrads linear during development], granular layer of exine thin; nectar usually accessible at or near base of guide rails; n = (9-14).

214/2365. Tropics to temperate, drier areas esp. in Africa (map: see Good 1952). [Photo - Flower, Flower, Flower, Fruit.]

5a. Fockeeae

Plants with tuberous roots; connective appendages +, inflated; no pollinium wall [?: Cibirhiza].

2/9. Drier parts of southern and eastern Africa, Arabia.

5b. The Rest = Asclepiadeae, Marsdenieae, Ceropegieae

(Lianes); (phenathroindolizidine alkaloids); (latex clear - Marsdenieae and esp. Ceropegieae); anther secretes wall around pollinium, pollinia with translator arms [caudicles], (orbicules + - Riocreuxia); pollen as monads when mature; (exotestal cells with outer walls unthickened - Hoya).

212/2356: Cynanchum (200), Matalea (180), Ceropegia (160), Asclepias (100), Gonolobus (100), Marsdenia (100), Brachystelma (100), Hoya (90[-200+]), Oxypetalum (90), Dischidia (80), Ditassa (75), Stapelia (70), Orbea (55), Huernia (50), Tylophora (50), Caralluma (47). Tropics to temperate, drier areas esp. in Africa.

Synonymy: Asclepiadaceae Borkhausen, nom. cons., Cynanchaceae G. Meyer, Stapeliaceae Horaninow

• Apocynaceae usually have copious latex and the leaves are often opposite and with colleters; the venation of the dry lamina is not very prominent. A number of taxa are climbers. The corolla is often contorted and the stylar head is swollen and closely associated with the more or less connivent anthers. The two carpels are usually held together only by the stylar head; in fruit, they often diverge (if both are fertilised); follicles containing seeds with tufts of unicellular hairs at either end are common. The inflorescence may appear extra-axillary, being borne in the axils of scale leaves themselves borne after a reduced internode, or they may be lateral-axillary, as in many Asclepiadoideae.

Evolution. Divergence & Distribution. Rapini et al. (2007) calibrated the age of crown-group Apocynaceae at ca 54 m.y., but Bell et al. (2010) suggest ages of only ca 21 m.y. The Asclepiadoideae-Secamonoideae split was dated to ca 42 m.y. and crown group Asclepiadoideae to ca 37 m.y. (Rapini et al. 2007, q.v. for more dates; also in 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. 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. 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).

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 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). 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. 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 arrangement of the androecium is the same as that in Asclepiadoideae (see also Schick 1982). Note that in Tabernaemontaneae several features - an androecium with thick, lignified guide rails, a stigmatic head with a five-lobed upper stigmatic 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 distinct nectaries at the base of the gynoecium, but in Secamonoideae and Asclepiadoideae in particular it 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 of Apocynaceae in general 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 lobes narrow 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 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). 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., are 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, where 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). At least some Asclepiadoideae have no compitum developed at all, one of the reasons for the frequent occurrence of fruits in which only a single carpel has developed.

Fruit and seed morphology in the old Apocynoideae is quite variable, but follicular fruits with comose seeds characterise a clade that encompasses most of the diversity of the family. At least some Asclepiadoideae have no compitum developed at all, one of the reasons for the frequent occurrence of fruits in which only a single carpel has developed.

Plant-Animal Interactions. Caterpillars of Nymphalidae-Danainae-Danaini (often as Danainae) 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 (Janz et al. 2006; c.f. Wahlberg et al. 2009), although many New World Ithomiini eat Solanaceae (q.v.); the danaine clade diverged from other butterfly clades ca 89 m.y.a. (Wahlberg et al. 2009). The cardenolides in the leaves are noxious and may protect both larva and adult (e.g. Malcolm 1991; see also Dobler et al. 2011).

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). The monarch butterfly is one example of an insect involved in this cardenolide syndome, although the adult also sequesters pyrrolizidine alkaloids for defence (Hartmann & Witte 1995). 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 are found in some Apocynaceae, so the plants attract practically all Danaini butterflies, mostly males, which use these compounds as the basis of their pheromones (but not the monarch) and for defence (Boppreé 2005; Brehm et al. 2007); Ithomiini are also attracted. These alkaloids also occur in Crotalaria, some Boraginaceae and Asteraceae-Asteroideae. Interestingly, Ithomiini preferentially visit bait with withered flowers, while Arctiidae moths prefer crushed roots, and Brehm et al. (2007) suggested that the pyrrolizidine alkaloids of Prestonia (Echiteae) may have been originally involved in the pharmacophagous behaviour of Ithomiini butterflies (Wilmott & Freitas 2006).

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). Hosts of seed-eating bugs of Hemiptera-Lygaeidae-Lygaeinae are concentrated in the old Apocynaceae (Slater 1976).

For the possible co-evolution of the longicorn beetle Tetraopes with Asclepias, see Farrell and Mitter (1998), and for a study of the different defence syndromes of Asclepias, see Agrawal & Fishbein (2006). Although the resprouting ability of the plant - or simply its tolerance of herbivory - may be an effective defence against specialist herbivores in particular in Asclepias (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). Indeed, 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 were 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); Moles et al. (2011b) suggest that generally such protective compounds decresase at lower latitudes.

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).

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). Epiphytes are not uncommon.

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. 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, withcentes of distribution in Arabia, East Africa and southern Africa (Meve et al. (2004).

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. 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: see also Woodson 1935; Holm 1950; Nolan 1969; Liede & Weberling 1985; Steck & Weberling 1982, etc.).

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 some variation in the direction of overlap of the corolla lobes (Eichler 1874); how the corolla tube is initiated in Periplocoideae is unknown. Much has been written about the homology of the various structures associated with the corolla, stamens, and stigmatic head; deciding which structures on different flowers are directly comparable (see Remane's criteria) can indeed be very difficult. Thus 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). Again, 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. There has been considerable discussion about the nature of the paired nectaries of Vinca, and because of their vasculature, etc., it has been suggested that they are carpels (Fahn 1979 for literature); this is unlikely. 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 Glück (1919: colleters), Andersson (1931: embryology), Leeuwenberg (1983: Plumerioideae), 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), Sennblad and Bremer (1996: rbcL phylogeny, morphology), Swarupanandan et al. (1996: flowers of Asclepiadoideae, classification), Civeyrel et al. (1998: pollinaria variation), Omlor (1996: translator structure in Periplocoideae and Secamonoideae, 1998: floral morphology and testa anatomy), M. Endress and Bruyns (2000, much general information), Albers and Meve (2001: karyology), Aniszewski (2007: alkaloids), Demarco et al. (2006: laticifer type), Lens et al. (2009c: wood anatomy, to be integrated), Meve et al. (2009: floral morphology of Marsdenieae) and Shamrov and Gevorkyan (2010b: gynoecium). 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 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). Of the other tribes, Tabernaemontaneae have an androecium with lignified guide rails and a stigmatic head complex like that of "Apocynoideae" in particular, there being a five-lobed upper crest and a thickened basal flange (Simões et al. 2010). Simões et al. (2010) have clarified relationships within the tribe, i.a. circumscribing Tabernaemontana broadly to include Stemmadenia; major clades within that genus are correlated with geography. Alyxieae have irregularly-shaped 2-3-porate pollen grains the ectoapertures having thickened margins (Lens et al. 2008b and references); 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 Tabernaemontaneae, see Simões et al. (2006a, 2010), of Alyxieae, M. Endress et al. (2007) and of "Rauvolfioideae" as a whole, see Simões et al. (2007a).

Apocynoideae, as well as the old Asclepidaceae and Periplocoideae, form the APSA clade, relationships within which are being clarified. A small African clade, Baisseeae (Dewevrella, with coiled filaments [?; Livshultz 2009], is included here, although it does not have the morphological features of the other genera), has strong support as sister to [Secamonoideae + Asclepiadoideae], and 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 [Baissaaeeae [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). How relationships play out will of course affect the optimization of characters on the tree...

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.

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) appear to be separable by morphological features, possibly apomorphies, such as pollinarium morphology, inner guide rail presence/absence, and nectary position (Wanntorp & Kunze 2009); estimates of species numbers in these two genera in particular vary widely. Hoya is particularly speciose; see 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 classification here is based on that of M. Endress et al. (2007a; see also Endress & Bruyns 2000; summary in Nazar et al. 2013), however, it will be clear that any classification of the entire family must for now be rather provisional (e.g. M. Endress 2004).

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 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). 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.