LIGNOPHYTA

True roots +; lateral meristems: cork cambium producing cork abaxially, vascular cambium producing phloem abaxially and xylem adaxially.

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, (lignins derived from p-coumaryl alcohol, i.e. S [syringyl] lignin units); true roots present, apex multicellular, xylem exarch, and branching endogenous; arbuscular mycorrhizae +; shoot apical meristem multicellular, interface specific plasmodesmatal network; stem with ectophloic eustele, endodermis 0, xylem endarch, branching exogenous; vascular tissue in t.s. discontinuous by interfascicular regions; vascular cambium + [xylem ("wood") differentiating internally, phloem externally]; wood homoxylous, tracheids and rays alone, tracheid/tracheid pits circular, bordered; mature sieve tube/cell lacking functioning nucleus, plastids with starch grains; phloem fibres +; stem cork cambium superficial, root cork cambium deep seated; leaves with single trace from sympodium ["nodes 1:1"]; stomata ?; leaf vascular bundles collateral; leaves megaphyllous [determinancy evolved first, then ad/abaxial symmetry], spiral, simple, lamina with vein density up to 5 mm/mm² [mean for all non-angiosperms 1.8]; axillary buds associated with at most some leaves; prophylls [including bracteoles] two, lateral; plant heterosporous, sporangia eusporangiate, on sporophylls, sporophylls aggregated in indeterminate cones/strobili; true pollen [microspores, i.e. no distal pore for release of gametes] +, grains mono[ana]sulcate, exine and intine homogeneous; ovules unitegmic, crassinucellate, 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, with many flagellae; female gametophyte endosporic, initially syncytial, walls then surrounding individual nuclei; seeds "large", first cell wall of zygote transverse, embryo straight, endoscopic [suspensor +], short-minute, with morphological dormancy, white, cotyledons 2; plastid transmission maternal; 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; shoot apex with tunica-corpus construction, tunica 2-layered; reaction wood ?, with gelatinous fibres; 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 cells from same mother cell that gave rise to the sieve tube; sugar transport in phloem passive; nodes unilacunar [1:?]; stomata with ends of guard cells level with pore, paracytic, outer stomatal ledges producing vestibule; leaves petiolate, lamina [formed from the primordial leaf apex], development of venation acropetal, 2ndary veins pinnate, fine venation reticulate, veins (1.7-)4.1(-5.7) mm/mm², endings free; most/all leaves with axillary buds; flowers perfect, pedicellate, polysymmetric, 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 by action of hypodermal endothecium, endothecial cells elongated at right angles to long axis of anther; tapetum glandular, 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 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]; P deciduous in fruit; seed exotestal; pollen binucleate at dispersal, trinucleate eventually, germinating in less than 3 hours, pollination siphonogamous, tube elongated, growing at 80-600 µm/hour, with pectic outer wall, callose inner wall and callose plugs, growing between cells, penetration of ovules via micropyle [porogamous] within ca 18 hours, distance to first ovule 1.1.-2.1 mm, tube moves between nucellar cells; double fertilisation +, endosperm diploid, cellular [micropylar and chalazal domains develop diffently, first division oblique, micropylar end initially with a single large cell, divisions uniseriate, chalazal cell smaller, divisions in several planes], copious, oily and/or proteinaceous, embryo cellular ab initio, minute; 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]].

Evolution. Possible apomorphies for flowering plants are in bold. Note that the actual level to which many of these features, particularly the more cryptic ones, should be assigned is unclear. This is because some taxa basal to the [magnoliid + monocot + eudicot] group have been surprisingly little studied, there is considerable homoplasy as well as variation within and between families of the ANITA grade in particular for several of these characters, and also because details of relationships among gymnosperms will affect the level at which some of these characters are pegged. For example, if reticulate-perforate pollen is optimized to the next node on the tree (see Friis et al. 2009 for a discussion), it effectively makes the pollen morphology of the common ancestor of all angiosperms ambiguous... For other features such as details of sugar transport in the phloem, their placement on the tree is frankly speculative. Finally, for features such as parietal tissue/a nucellus only one (Nymphaeales) to three cells thick above the embryo sac and a stylar canal lacking an epidermal layer, although plesiomorphous for basal grade angiosperms (Williams 2009), I am unsure where on the tree a thicker nucellus and a stylar epidermal layer are acquired.

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

[FABALES [ROSALES [CUCURBITALES + FAGALES]]] / the nitrogen fixing clade :   Back to Main Tree
(N-fixing by root-dwelling associates [usu. the actinomycete Frankia]); tension wood +; seed exotestal.

Evolution. Divergence & Distribution. Wikström et al. (2001) dates diversification in the clade to (91-)89(-87) million years before present, while Moore et al. (2010: 95% highest posterior density) suggest ages of (107-)104(-100) million years.

Bacterial/Fungal Associations. There are at least six independent establishments of symbioses with Frankia, a gram-positive actinomycete, in this clade that result in the plant being able to fix nitrogen, and at least two more associations with rhizobia (e.g. Swensen 1996; Clawson et al. 2004). Jeong et al. (1999) and Clawson et al. (2004) compared phylogenetic relationships within Frankia with those of its hosts; there is not a close parallel. Thus Clawson et al. (2004) suggested that all the three clades of Frankia that they recognised might have diverged before the evolution of the angiosperms.

Intercellular penetration of the root epidermis by Frankia may be the plesiomorphic route of infection, occurring in both Rosales and Cucurbitales; in Fagales infection is by root hairs (Clawson et al. 2004). However, given the absence of strong phylogenetic structure in the group, details of how infection patterns map on to phylogeny are unclear (see also Soltis et al. 2005a). The situation is yet more complex. In Mimosa and some Faboideae, at least, ß-proteobacteria like Burkholderia phymatum and Cupriavidus also form nodules that may effectively fix nitrogen, while the α-proteobacteria, rhizobia, that form nodules in other Fabaceae occur in four separate clades, over a dozen "species" being involved (J. J. Doyle 1998; Moulin et al. 2001; Sprent 2002; Elliott et al. 2007; Bontemps et al. 2010). Rhizobia themselves can fix nitrogen only when in association with their host, and one of the components of the cofactor of nitrogenase, which actually fixes the nitrogen, has been found to come from the host legume (Hakoyama et al. 2009). Haemoglobin is intimately involved in helping preserve the largely oxygen free micro-environment the bacteria need for nitrogen fixation; a variety of haemoglobins are involved, including haemoglobin synthesized by Frankia (Vessey et al. 2004).

Although there is considerable variation in morphology of the nodules, it does not correlate with bacterium type. In general in Fabaceae the nodules arise from the cortex and have peripheral vascular tissue with bacterial infected cells in the center (Franche et al. 1998), while in all other nodules, whether associated with Frankia or rhizobia, the nodules are modified lateral roots. There the vascular tissue is central, initiation of the nodule is pericyclic, and it is the cortical cells that contain bacteria (Gualtieri & Bisseling 2000; Vessey et al. 2004). However, recent work clearly shows that nodule origination in Faboideae occurs where lateral roots develop, although cortical cells may also be involved (op den Camp et al. 2011). Indeed, in Faboideae, there seems to have been cooption of genes originally involved in lateral root origination after a genome duplication event ca 54 million years ago (op den Camp et al. 2011), but N-fixing clades such as Chamaecrista do not have this duplication (Cannon et al. 2010).

Nitrogen fixation in this group of four orders is a classic example of a "tendency" or a predisposition (Vessey et al. 2004), and the possible molecular reasons for the restriction of these diverse bacterial associations to the N-fixing clade are being dissected. There is a relatively small plasmid-born "symbiosis island" that can be exchanged among bacteria and that enables nodulation to develop, although not all nodulation genes occur on these plasmids (Sullivan & Ronson 1998; J. J. Doyle 1998). A number of the genes involved in the establishment of both the actinomycete and Rhizobium symbiosis are the same as those involved in establishing vesicular-arbuscular mycorrhizal associations, the "SYM" (symbiosis) pathway being involved in all (Bonfante & Genre 2010; Hocher et al. 2011). One of these genes, the symbiosis receptor kinase gene, exists in a particularly distinctive form in the N-fixing clade - and also in Tropaeolum, but not rice, tomato or poppy. This gene in the latter genera rescued mycorrhizal formation in defective forms of the gene in Fabaceae, but not nodule formation, whereas the Tropaeolum gene restored the ability to form nodules (Markmann et al. 2008; see also Chen et al. 2007, 2009; Gherbi et al. 2008; Yano et al. 2008; Markmann & Parniske 2009). There are also connections betwen the signalling genes involved in arbuscular mycorrhizae symbioses and rhizobial Nod factors involved in nodulation in legumes (Maillet et al. 2010; Op den Camp et al. 2010; Streng et al. 2011), the rhizobia acquiring the nod gene by horizontal transfer (Suominen et al. 2001). Although Nod factors do not occur in actinorhizal associations, there is notable similarity at the transcriptional level in the genes involved in the establishment of endosymbioses in Casuarina, Alnus (both associates of actinorhiza), and legumes (Hocher et al. 2011).

Ecology & Physiology. Nitrogen-fixing plants are usually not plants of closed lowland tropical rainforst, often being members of more open vegetation, even of early successional communities, in both tropical and temperate regions of the world.

Perhaps connected (in some way) with nitrogen fixation is the fact that taxa scattered in the nitrogen-fixing clade form root clusters of varying morphologies; in some cases, at least, these have been shown to facilitate phosphorous uptake in phosphorous-poor soils (Lambers et al. 2006). Species forming ectomycorrhizal associations are also common in the nitrogen-fixing clade, being found throughout Fagales, for example, and this association has evolved at least seven times (but apparently not in Cucurbitales?). Plants with ectomycorrhizae do not fix nitrogen.

Plant-Animal Interactions. There may be associations of this clade with particular butterflies (as food sources for caterpillars), and within Fabales and Rosales in particular (Ackery 1988, 1991). Indeed, it has been suggested, as by Scott (1985) and Janz and Nylin (1998; see also Braby & Trueman 2006) that the ancestral food plant for larvae of butterflies as a whole may have been Fabales (but note that caterpillars are common only on Fabaceae) or perhaps in the rosid I group; Ackery (1991) also suggested Malvales as a possibility. Rosids as a whole are another possibility (e.g. Powell 1980; Berenbaum & Passoa 1999).

Chemistry, Morphology, etc. Whether or not the presence of stipules is plesiomorphic in the clade depends in part of its phylogeny, but there is clearly a variety of structures borne at the node - and nodal anatomy is also variable (see below: de Aguiar-Dias et al. 2011).

Phylogeny. For the limits of the N-fixing clade, a rather unexpected group, see Chase et al. (1993, 1999), Savolainen et al. (1997), Soltis et al. (1995b, 1997, 1998), and Swensen (1996). Although it is not recovered by some analyses in the complete chloroplast genome study of Bausher et al. (2006), the poor sampling - no other rosid I taxa were included - may well be reponsible, and the nitrogen-fixing clade was also found not to be monophyletic in Duarte et al. (2010) or in the genome-level analysis of Burleigh et al. (2011). The clade had little support in the mitochondrial matR analysis of Zhu et al. (2007), but support was much strengthened when two chloroplast genes were added (also monophyletic in the mitochondrial analysis of Qiu et al. 2010).

Relationships within the clade have been unclear (e.g. Qiu et al. 2010), and Zhu et al. (2007) could not even recover a monophyletic Rosales using the mitochondrial matR gene; the other three orders were, however, all strongly supported. Sytsma et al. (2002) recovered a topology [Cucurbitales [Fabales [Fagales + Rosales]]], while in Zhu et al. (2007: four genes) the position of the first two was reversed, albeit in both studies there was little support for the topologies found. However, Ravi et al. (2007) examining data sets including 61 protein-coding genes (only three of the orders) and four genes (Fagales, the missing order, included) found good support for [Fabales + Rosales] and some support for the broader grouping [Cucurbitales [Fagales [Fabales + Rosales]]]. Apart from Fabales (three Fabaceae-Faboideae included), the other orders were represented by single exemplars. A [Fabales + Rosales] clade was also obtained by Jansen et al. (2007) and Moore et al. (2007), but no Fagales were included in these studies. In other analyses there is some support for a [Cucurbitales + Fagales] clade (see Chase et al. 1993; Setoguchi et al. 1999; Schwarzbach & Ricklefs 2000; Soltis et al. 2000, 2003a; Zhang et al. 2006). The support for the topology in the Summary Tree is quite strong (Moore et al. 2008; Soltis et al. 2011; Moore et al. 2011), but confirmation after e.g. increased taxon sampling would be comforting.

FABALES Bromhead  Main Tree, Synapomorphies.

Ellagic acid 0; wood often fluorescing; nodes?; styloids +; K initiation helical; carpels free, embryo green. - 4 families, 754 genera, 20055 species.

Evolution. Fabales contain ca 9.6% eudicot diversity (Magallón et al. 1999), of which the bulk is made up of Fabaceae.

Evolution. Divergence & Distribution. Wikström et al. (2001: relationships are [Fabales [Rosales [Cucurbitales + Fagales]]]) date the origin of the clade to (91-)89(-87) million years before present, diversification beginning (77-)74(-71) million years before present - although Fabaceae themselves, which contain the bulk of the species in the order, may not have begun diversifying for another twenty million years or so. The age of crown group Fabales was estimated as (90-)87(-84) or (75-)72(-69) million years (two penalized likelihood dates), the stem group age being (109-)104(-99) and (92-)89(-86) million years; Bayesian relaxed clock estimates were slightly older, to 100 or 112 million years respectively (Wang et al. 2009: note that relationships are [Rosales [Fabales [Cucurbitales + Fagales]]]), while Magallón and Castillo (2009: relationships are [Fabales + Rosales] [Cucurbitales + Fagales]) gave ages of ca 101 and 101.3 million years for relaxed and constrained penalized likelihood estimates of stem Fabales.

Chemistry, Morphology, etc. The distribution of a number of features may be of systematic significance in this clade, but sampling is poor; the problem is compounded by the uncertain phylogenetic relationships within Fabales. Note the variation in nodal anatomy within the order; variation within Surianaceae is correlated with presence/absence of stipules. Although styloids are reported from Surianaceae, Quillajaceae and Fabaceae, details of their distribution within Fabaceae are unclear; they are certainly quite common in Faboideae (Lersten & Horner 2005), apparently less so in the rest of the family. Despite the floral differences between Polygalaceae and Fabaceae, there are some developmental similarities between the two (Prenner 2004d). The rpl22 gene is in the nucleus in Polygalaceae (check!) and Fabaceae (i.e. is absent from the chloroplast), but the condition in the rest of the order is unknown (J. J. Doyle et al. 1995). Some distinctive palynological features are scattered here: Quillajaceae and some Surianaceae have exine protruding at the apertures, and these and Fabaceae-Cercideae (although perhaps derived within that group?) have striate pollen (Banks et al. 2003; Claxton et al. 2005). It would be nice to know if Surianaceae or Quillajaceae had starchy endosperm, and more details of their chemistry are needed. Many Fabaceae-Faboideae have lost the rps16 gene, and it is also absent from Polygala (Downie & Palmer 1992: but again, sampling).

Phylogeny.Fabales were a rather unexpected group, but it is quite strongly supported - see Morgan et al. (1994), Källersjö et al. (1998), etc., however, Hilu et al. (2003) found Larrea (Zygophyllaceae) to be weakly associated with Fabaceae, the only member of Fabales included in their rbcL analysis.

Within Fabales, Persson (2001) suggested the relationships [Polygalaceae [Surianaceae [Quillajaceae + Fabaceae]]], but there was little support for this (see the tree in versions 1-6). Forest et al. (2002, see also Qiu et al. 2010) found weak support for the topology [Quillajaceae [Fabaceae [Surianaceae + Polygalaceae]]], and Banks et al. (2008) suggest that there is strong support for the relationship [Quillajaceae [the rest]] (see the tree here), although Wojciechowski et al. (2004, but sampling) suggested the possibility of a [Surianaceae + Quillajaceae] grouping... The unrooted topology in Bruneau et al. (2008a) is [Polygalaceae [Quillajaceae + Surianaceae] Fabaceae]. Bello et al. (2009) in a careful analysis on matK and rbcL data, preferred relationships obtained in a maximum parsimony analysis of [[Polygalaceae [Fabaceae [Surianaceae + Quillajaceae]]], however, support remained poor - and if anything was still poorer for any relationships obtained in Bayesian analyses of the same data. Wang et al. (2009) did not obtain well supported relationships in this clade in their twelve-gene analysis of the rosids, while in a megaphylogeny of angiosperms Smith et al. (2011) found some support for a clade [Quillajaceae + Fabaceae]. Relationships remained unclear in the study by Soltis et al. (2011).

Includes Fabaceae, Polygalaceae, Quillajaceae, Surianaceae.

Synonymy: Caesalpiniales Martius, Cassiales Link, Mimosales Link, Polygalales Berchtold & J. Presl, Quillajales Doweld, Surianales Doweld

QUILLAJACEAE D. Don   Back to Fabales

Small evergreen tree; saponins, proanthodelphinidin, flavone C-glycosides +; storying?; nodes 1:3; petiole bundles arcuate, no pericyclic fibres; mucilage cells +; hairs warty; leaves spiral, blade vernation conduplicate, margins toothed [hydathodal?], (entire), stipules petiolar; inflorescence terminal, cymose; hypanthium +; K valvate, nectary on lower half of K, C contorted, spathulate, clawed; A unidirectional in initiation, 5 opposite sepals above nectary + 5 opposite C below nectary; pollen striate; G becoming [5], opposite K, stigmatic zone elongated down styles; ovules several/carpel, pleurotropous, in two marginal rows, micropyle?, outer integument ?3 cells across, inner integument ? cells across; fruit strongly asymmetrically lobed, follicular, opening down both surfaces of the lobes, K moderately accrescent; seeds winged; testa with 3 outer layers thickened, sclerotic, tegmen disintegrating; endosperm type?, cotyledons investing radicle, conduplicate; n = 14, 17.

1/3. Temperate South America (map: from Donoso Z. 1994; Culham 2007). [Photo - Flower, Fruit.]

• Quillajaceae are vegetatively rather undistinguished with their spiral, serrate, stipulate leaves, although the conspicuous teeth appear to be hydathodal. They may be readily recognised by their distinctive flowers in which the antesepalous stamens are borne on the outer edge of the disc some way up the sepals and the antepetalous stamens are borne inside the nectary near the base of the ovary. The petals are clawed and the strongly lobed fruits open down both the inner and outer surfaces of the lobes and contain winged seeds.

Chemistry, Morphology, etc. The leaves are amphistomatous. The flowers of Quillajaceae, with their distinctive positioning of nectary and androecium, may be interpreted as having a hypanthium. Development of the androecium is unidirectional and is rather like that of Fabaceae (Bello et al. 2007/8). The carpels are definitely connate axially, but are largely free laterally, cf. earlier versions of this site. There appear to be only three traces to each carpel, although Sterling (1969) noted that there were also "intermediate" bundles. Robertson (1974) noted that n = 17. Embryologically the family is poorly known.

See also Péchoutre (1902, as Rosaceae) for seed morphology, Hegnauer (1973, 1990, as Rosaceae) for chemistry, Sterling (1969) and Kania (1973) for gynoecial morphology, Lersten and Horner (2005) for vegetative anatomy, particularly styloids, Kubitzki (2006b) for a general account, Bello et al. (2007, reprinted 2008) for floral development, and Marchiori et al. (2009) for wood anatomy (intercellular canals, included phloem). Additional data from: Aronson 7897 (anatomy, embryo).

Previous Relationships. Quillaja was included in Rosaceae as part of Quillajoideae (Takhtajan 1997) or, more usually, it has been included in Spiraeaoideae, e.g. as Quillajeae (Robertson 1974). It is indeed superficially quite similar to the South American Kageneckia, but wood anatomical data, etc., suggest that it should be removed from Rosaceae (Lotova & Timonin 1999; cf. Zhang 1992).

[Fabaceae [Surianaceae + Polygalaceae]]: ?

FABACEAE Lindley, nom. cons.//LEGUMINOSAE Jussieu, nom. cons. et nom. alt.   Back to Fabales

Trees to annual herbs; lectins [haemagglutinins] and gums esp. in seeds, 5-deoxyflavonoids, Cglycosylflavonoids, pinitol [cyclitol] +; cork also in outer cortex; cambium storied; secretory cells common, sieve tube plastids with protein crystals (and/or starch, or simply starch); nodes 3:3; cuticle wax platelets as rosettes; stomata various; branching from previous flush; colleters +, hairs often uniseriate (mesifixed); leaves (opposite), pari- or odd-pinnately compound (palmate, simple), leaflets pulvinate, stipellate or not, opposite (alternate), vernation conduplicate, (glandular-punctate), (margins lobed, toothed), (2ndary veins palmate); inflorescence racemose; flowers (3-)5(-6)-merous, floral developmental sequence K-G-C-outer whorl A-inner whorl A [G initiation/development much advanced]; hypanthium +, C clawed, adaxial-median member internal [descending cochleate]; A unidirectional in initiation, (2-)10(-many); G 1, stipitate, style long, (hollow), stigma expanded or not, wet; ovules several/carpel, one-ranked, micropyle zig-zag, outer integument 2-10 cells across, inner integument 2-3 cells across, parietal tissue to 2 cells across, nucellar cap ca 3 cells across, vascular bundle in antiraphe, funicle long; (megaspore mother cells several), chalazal embryo haustorium +; fruit follicular, dehiscing abaxially also; seed symmetrical, with pleurogram [area of cells with a deep-seated linea lucida] + (0), linea fissura [fine line delimiting pleurogram] ± circular/oval [closed; ?level], (0); exotesta palisade, linea lucida separating much thickened outer anticlinal walls from the thinner inner walls, mesotesta of stellate cells, (seed coat undistinguished), tegmen crushed; (thick-walled endosperm with galactomannans [Schleimendosperm]), chalazal endosperm/suspensor haustoria + [?level]; embryo ± straight, cotyledons investing radicle; rpl22 gene transferred from chloroplast to nucleus.

745/19500 - discussed in six or so groups below. World-wide.

1a. Cercideae

Trees to lianes; leaves apparently simple, bilobed or not; pollen striate; (funicle short); (seeds asymmetrical); n = 7, etc.

4-12/265: Bauhinia (250). Pantropical (temperate) (map: from Meusel et al. 1965; Sales & Hedge 1996). [Photo - Bauhinia]; [Photo - © D. Kimbler - Cercis]

Synonymy: Bauhiniaceae Martynov

1b. Duparquetia

Leaves once-compound; floral development acropetal ["normal"], K 4, petaloid, adaxial-median C external; A 4, opposite K, connate, anthers porose; pollen asymmetrical, ectoaperture encircling the equator, with two endoapertures; G initiation not advanced relative to other organs.

1/1: Duparquetia orchidacea. Tropical W. Africa.

1c. Detarieae

Plant ectomycorrhizal; resins with bicyclic diterpenes; leaf phloem transfer cells +; leaflets with crater-like glands on the abaxial surface, stipules deciduous, intrapetiolar; bracteoles well developed, deciduous; (pollen striate); endosperm 0, cotyledon cell walls thick, with amyloid and xyloglucans; x = 12.

Macrolobium (70-80)

Synonymy: Detariaceae J. Hess

1d. Dialiineae

?

14/56: Dialium (28). Tropical. (Poepiggia)

"Caesalpinioideae" + Mimosoideae + Faboideae: (N-fixation); (non-protein amino acids, esp. in seeds, +); vestured pits + (0); (fruit a drupe, samara, schizocarp, etc.).

2. "Caesalpinioideae" Candolle

Shrubs or trees (herbs); (N-fixing, rhizobia remain in infection threads), often with ectomycorrhizae; non-protein amino acids +; sieve tube plastids also with fibres; leaves bicompound or not; (G adnate to side of hypanthium); ovules usu. campylotropous, outer integument with vascular strand; seed with aril (0), funicle long and thin to stout and thick, (pleurogram +); (cotyledons with thick-walled cells [amyloid, xyloglucan]).

160[list]/1930: Senna (295-350), Chamaechrista (265). Predominantly tropical, esp. Africa and America. [Photos - Collection]

Synonymy: Caesalpiniaceae R. Brown, Cassiaceae Vest, Ceratoniaceae Link[?]

3. Mimosoideae Candolle

Shrubs or trees (herbs); N-fixing common; albizziine [non-protein amino acid] +; sieve tube plastids also with fibres; (septate fibres +; aliform axial parenchyma); rays usu. 20³ cells high; leaves often bicompound, petiolar extrafloral nectaries common; flowers often aggregated into heads, developing together, with all organs initiation in flowers of the one head beginning simultaneously; flowers rather small, polysymmetrical, bracteoles 0; C mmeber initiation simultaneous, corolla enclosing the flower in bud, hypanthium often 0, K connate, median member adaxial, valvate (imbricate; much reduced), C usu. connate, valvate, odd member abaxial, claws 0; A often connate, (many, from ring primordium); pollen polyads common; (G 1+ - e.g. Inga, if 5, opposite K - Archidendron lucyi]), stigma (dry - one record), cup-shaped, (peltate); nucellus naked); seed (arillate), funicle long, thin; testa with vascular strand, pleurogram + (0), linea fissura U-shaped [open], (0).

82[list]/3275: Acacia s. str. (960), Mimosa (480: some have sensitive leaves), Inga (350), Calliandra (200), Vachellia (161), Senegalia (85), Prosopis (45), Pithecellobium (40). Esp. tropical and warm temperate, esp. Africa and America (map: from Vester 1940; Maslin et al. 2003). [Photos - Collection]

Synonymy: Acaciaceae E. Meyer, Mimosaceae R. Brown

4. Faboideae Rudd / Papilionoideae Jussieu, nom. alt.

N-fixing common; isoflavonoids [pterocarpans and isoflavans], prenylated flavonoids, pyrrolizidine, indolizidine, and quinolizidine alkaloids +; (cork cambium deep seated); sieve tubes with spindle-shaped non-dispersive protein bodies [forisomes]; leaves once compound; K, C, A with unidirectional [abaxial to adaxial] initiation; ?hypanthium; (pollen porate); (G 1< - Swartzia); ovules usu. campylotropous, (endothelium; integumentary endothelium); seed pleurogram 0, linea fissura 0; testa (multiplicative), hour-glass cells [below palisade exotesta] +, raphe shorter than the antiraphe, hilum with a hilar groove, with tracheid bar [group of tracheids just below surface of hilum] and recurrent vascular bundles; embryo with well-developed suspensor [?not the basal condition], cotyledons accumbent, not investing radicle, cotyledon areole +, (xyloglucans +, starch in embryo), (endosperm 0); duplication of CYC gene.

4a. Swartzieae

Trees, shrubs; ?hypanthium, C 1; A many, from ring meristem; G 1; seed usu. arillate.

1/140. Central and South America.

4b. The Rest.

Herbs, vines (lianes, trees, shrubs); (nodes 1:1); (leaves 2+ compound), palmate or pinnate, (pulvini 0); ?hypanthium, adaxial-median C external [= ascending cochleate]; A usu. connate [e.g. 9 + 1]; (pollen porate); antiraphe bundle (+ Canavalia, Sophora), funicle short; seed asymmetrical, not arillate; hilum with counter palisade; embryo curved, radicle long.

475[list]/13715 (abbreviations - BAPH = baphioids, DAL = dalbergioids s.l., GEN = genistoids, IRLC = Inverted Repeat Loss Clade, MILL = Indigofereae + millettioids, MIRB = mirbelioids, ROB = robinioids): Astragalus (2400-3270: IRLC), Indigofera (700: aff. MILL, mesifixed hairs), Crotalaria (700: GEN), Mirbelia s.l. (450: MIRB), Tephrosia (350: MILL), Desmodium (300: MILL), Aspalathus (300: GEN), Oxytropis (300: IRLC), Adesmia (240-425: DAL), Trifolium (240: IRLC), Rhynchosia (230: MILL), Lupinus (200), Aeschynomene (160: DALB), Hedysarum (160: IRLC), Lathyrus (160: IRLC), Vicia (160: IRLC), Dalea (150: DALB), Eriosema (150: MILL), Millettia (150: MILL), Daviesia (135: MIRB), Machaerium (130: DALB), Onobrychis (130: IRLC), Ormosia (130: unplaced), Lotus (inc. Coronilla: 125: ROB), Lonchocarpus (120: MILL), Erythrina (110: MILL), Gastrolobium s.l. (110: MIRB), Mucuna (105: MILL), Lotononis (100: GEN), Pultenaea (100: MIRB), Vigna (90+: MILL), Genista (90: GEN), Medicago (inc. Trigonella, 85: IRLC), Swainsonia (85: IRLC), Caragana (75: IRLC), Jacksonia (75: MIRB), Ononis (75: IRLC), Phaseolus (75: MILL), Zornia (75: DALB), Argyrolobium (70: GEN), Arachis (70-80: DAL), Cytisus (65: GEN), Bossiaea (60: MIRB), Canavalia (60: MILL), Clitoria (60: MILL), Dolichos (60: MILL), Galactia (60: MILL), Lebordea (60: GEN) Sesbania (60: ROB), Brogniartia (55: GEN), Derris (55: MILL), Lessertia (50: IRLC), Psoralea (50: MILL), Sophora (50: GEN), Caragana (50: IRLC). Esp. (warm) temperate, but world-wide (map: from Vester 1940; Meusel et al. 1965; Hultén 1971). [Photo - Flower, Fruit, Collection.]

Synonymy: Aspalathaceae Martynov, Astragalaceae Berchtold & J. Presl, Ciceraceae W. Steele, Coronillaceae Martynov, Cytisaceae Berchtold & J. Presl, Dalbetrgiaceae Martinov, Daleaceae Berchtold & J. Presl, Galedupaceae Martynov, Geoffroeaceae Martius, Hedysaraceae Oken, Inocarpaceae Berchtold & J. Presl, Lathyraceae Burnett, Lotaceae Oken, Papilionaceae Giseke, Phaseolaceae Martius, Robiniaceae Vest, Sophoraceae Berchtold & J. Presl, Swartziaceae Bartling, Tamarindaceae Martinov, Trifoliaceae Berchtold & J. Presl, Viciaceae Oken

• Fabaceae may be recognised by their compound, stipulate leaves whose leaflets are entire and often have wrinkled pulvini, and flowers with a single carpel, free petals (or two may be connate), and stamens either all similar in length, or if dissimilar, not regularly alternating longer and shorter. The fruit is usually dry and elongated, the often flattened seeds being borne in a single rank.

• "Caesalpinioideae" and Cercis and its relatives are woody plants that may be recognised by their usually once-compound leaves and monosymmetric flowers with the odd petal adaxial and inside the others in bud; the hypanthium is often well-developed.

• Mimosoideae are also mostly woody plants that have leaves that are often bicompound and have extrafloral nectaries on the petioles. The flowers are rather small and are often borne in heads, all flowers opening more or less simultaneously; the long, coloured filaments form the visually attractive part of the inflorescence. Both the calyx and corolla are valvate, and both (and often the bases of the filaments) are connate. The seeds have a fine, U-shaped line on both sides.

• Faboideae are usually herbs or vines and often have once-compound leaves. The flowers are monosymmetric with the odd petal being adaxial and outside the others; the papilionoid flower consists of adaxial banner, paired wings and two connate petals forming the keel. The stamens have more or less connate filaments and the fruit is often explosively dehiscent, simultaneously splitting down both sides and the two valves twisting.

Evolution. Divergence & Distribution. Fabaceae are a notably speciose clade, particularly the branches with Mimosoideae and Faboideae (Magallón & Sanderson 2001), and contain ca 9.4% of eudicots; it has been estimated that some 16% of all woody species in neotropical rainforest are members of this family (Burnham & Johnson 2004). Indeed, Fabaceae are the most speciose family in lowland tropical rainforest and also drier forest types in America and Africa (Gentry 1988).

Fabaceae began diversifying in the Palaeocene only ca 60-64 million years ago (the stem group is little older), and the major clades had separated by 58-55 million years ago (e.g. Bruneau et al. 2008b; perhaps slightly younger in Bello et al. 2009, the Gondwanan age of Amherstieae suggested because of their distribution and common possession of ectomycorrhizae [Henkel et al. 2002] seems unlikely). Bruneau et al. (2008b) suggest that the crown age of the major clades in Fabaceae is 56-34 million years ago. The clade [part of "Caesalpinioideae" + Mimosoideae] may date to 54 ± 3.4 million years before present, stem group Mimosoideae to ca 55 million years before present, crown group Mimosoideae to 44 ± 2.6 million years before present (Lavin et al. 2005; not very dissimilar ages in Bouchenak-Khelladi et al. 2010b, although it deopends exactly what is included in the subfamily). Wikström et al. (2001) provided somewhat different dates: they date stem Fabaceae to 79-74 million years before present (Quillaja not included in the analysis), with diversification beginning some 68-56 million years before present; the Mimosoideae-Faboideae split is dated to 59-34 million years before present. Stem group Faboideae may date to 58.6 ± 0.2 million years before present, and the crown group may be about the same age (Lavin et al. 2005, the latter date is rather sensitive to the age of Fabaceae as a whole). Marazzi and Sanderson (2010) suggest an age of 53.04-47.45 million years for stem group Senna, 46.97-45.00(-41.72) million years for the speciose crown group.

Lavin et al. (2004) and Schrire et al. (2005) suggest that it is more profitable to think of diversification and distribution of Fabaceae in terms of vicariance of biomes rather than of the classic geographical areas; the North Atlantic land bridge may have been important in the Tertiary dispersal of the family (Lavin et al. 2000). Although there are a number of transoceanic disjunctions within Fabaceae, 51/59 of these are only 1-22 million years old (Schrire et al. 2005; see also Bouchenak-Khelladi et al. 2010b). Early divergence within Mimosoideae seems to have occurred in Africa (Bouchenak-Khelladi et al. 2010b). Soltis et al. (2009) think, although with some hesitation, that diversification in Faboideae may be connected to a genome duplication there that they place immediately basal to the split between Mirbelieae and the rest; this is the clade that is notable for the occurrence of the non-protein amino acid canavanine (see below). See also rate shifts in Smith et al. (2011) and discussion below under Ecology and Physiology.

Crisp and Cook (2009) suggest that apparent independent increases in the rate of diversification in clades in the [Mirbelieae + Bossieae] and Podalyrieae are rather the results of extinctions caused by cooling climates and increased seasonality ca 32-30 million years ago in the early Oligocene, and Crisp and Cook (2007) date the development of SW/SE Australian disjunctions to vicariant events caused by the development of aridity in the Nullarbor plane some 14-13 million years ago (other climatic events could also be implicated). On the other hand, for Schnitzler et al. (2011) diversification of the ca 128 species of Podalyrieae in the Cape Flora has to do with shifts in ways that plants survive fires and it began ca 33 million years ago at the end of the Eocene.

Within Faboideae, a number of divergences have been dated, including the separation of the speciose Astragalus from Oxytropis (the latter has a beak on its keel: see Wojciechowski et al. 1999 for the monophyly of Astragalus, etc.) 16-12 million years ago, although diversification in both is relatively recent. In particular, radiation in the speciose aneuploid New World neoastragalus clade (ca 500 species) started ca 4.4 million years ago (Wojciechowski 2004), with two invasions of west South America - there are over 100 species there - that occurred a mere 2.07-1.62 and 1.23-0.79 million years ago respectively (Scherson et al. 2008). Several major clades that are correlated with geography have been detected in Lupinus (Aïnouche & Bayer 1999, support not very strong; Aïnouche et al. 2004), and subsequent work has shown that within one of these clades there has been a recent (within the last two million years) Andean diversification that is now represented by over eighty species, the rate of diversification increasing as the genus moved into Andean South America from Central America (Moore & Donoghue 2009; see also Silvestro et al. 2011). This diversification was probably connected with the migration of bumble bees to South America, also from North America, which probably occured at most six million years ago (Hughes & Eastwood 2006). Ree et al. (2003) studied aspects of LEGCYC gene evolution in the context of variation of floral morphology in the genus.

Faboideae-Robinieae have been diversifying for some 30 million years in the neotropical seasonally dry tropical forest (Pennington et al. 2009). On the other hand, Inga (Mimosoideae), with some 350 species, seems to have diversified in the lowland trpical forests that it prefers within the last two million years (Richardson et al. 2001b; Pennington et al. 2009; Dexter et al. 2010 for some thoughts on species limits - extinction might also cause this pattern, see Crisp & Cook 2009). There has been much diversification of Indigofereae in succulent biomes, clades growing there tending to be geographically more restricted than those common in grassland biomes; ages of crown groups of the four clades into which species of Indigofera fall is ca 15.5 million years or less (Schrire et al. 2009).

Ecology & Physiology. - see also Plant-Animal Interactions. Fabaceae can grow in closed lowland tropical rainforst, but are also often members of more open vegetation, even of early successional communities, in both tropical and temperate regions of the world. They make up perhaps the second most immportant scandent family - both ecologically and in terms of number of species - in the New World (Gentry 1991).

Associations with nitrogen-fixing bacteria are very common in Fabaceae, and substantial amounts of nitrogen can be fixed [refs.]. However, the role of legumes in the nitrogen cycle of tropical forests is unclear. Some work suggests that N-fixation is facultative, and in old, relatively nutrient-rich forests, nitrogen fixation by legumes (in the example, species of Inga) decreases when compared with species growing in seasonally flooded forests and in light gaps (Barron et al. 2011); other species of Fabaceae also have low fixation rates in mature forests (Barron et al. 2011 and literature). It has also been suggested that N-fixing tropical forest legumes may have a competitive advantage over non-nodulators as atmospheric CO₂ concentration increases (Cernusak et al. 2011).

Detarieae in particular are often ectomycorrhizal. In New World rainforests they may be locally dominant; many species (one hundred +) of mostly basidiomycete fungi were involved in this association in three species of legumes - Dicymbe, Aldina - examined (Smith et al. 2011). In the Old World, ectomycorrhizal caesalpinoids like Isoberlinia and Brachystegia are very important components of the widespread deciduous miombo forests. These are to be found growing on often rather poor soils over large areas of east and south-central Africa (e.g. Högberg 1990 and Smith & Read 2008 for references).

As already mentioned, particular groups of Fabaceae are conspicuous elements of various vegetation types world-wide (Lewis et al. 2005; Schrire et al. 2005). Faboideae-Robinieae are an important component of the neotropical seasonally dry tropical forest (Pennington et al. 2009), while Inga (Mimosoideae), with some 350 species, is very conspicuous in neotropical lowland forests (Richardson et al. 2001b; Pennington et al. 2009). There has been much diversification within a number of geographically-restricted clades of Indigofereae that grow in succulent biomes (Schrire et al. 2009).

Plant-Animal Interactions. There are numerous and often quite specific associations of insects and Fabaceae. Caterpillars of Lycaenidae-Riodininae-Riodinini, Lycaenidae-Curetinae and especially Lycaeninae-Lycaenini butterflies are often found on Fabaceae (Ehrlich & Raven 1964; Fiedler 1991, 1995), as are larvae of the some 260 species in 15+ genera of Coliadinae and Dismorphiinae (Pieridae) butterflies (see also Brassicales and Santalales, Braby & Trueman 2006, about a quarter of the records), indeed, species of Fabaceae may be the original food plants of Pieridae (Braby & Trueman 2006; Wheat et al. 2007; Fordyce 2010). The diversity of caterpillars - especially that of "basal" butterfly groups, including Baronia, sister to all Papilionidae ((Heikkilä et al. 2011) - on Fabaceae is such that Janz and Nylin (1998) and Braby and Trueman (2006) suggested that Fabaceae might be the springboard for hostplant diversification of butterflies feeding on angiosperms in general (see also the introduction to Fabales). In another variant of insect-plant relationships, the flowers of Crotalaria are visted by Danainae and Ctenuchidae because the pyrrolizidine alkaloids they contain are used as the basis of the pheromones of these lepidoptera (also Asteraceae, and wilting plants of some Boraginaceae: Edgar et al. 1974; Pliske 1975; Boppreé 1986); Crotalaria is also involved with arctiid moths such as Utetheisa in that its secondary metabolites provide defence for the young, pheromones, etc., etc. (Eisner & Meinwald 1995).

The jumping plant lice Psyllidae-Arytaininae are often associated with Fabaceae-Faboideae, especially genistoids, and especially in the Mediterranean-Macaronesian region, while Psyllidae-Acizzinae are associated with Mimosoideae in the Southern Hemisphere (Percy 2003; Percy et al. 2004). In Acacia s. str., well over 200 species of Phlaeothripinae (thrips) form galls and other habitations on species of subgenera Juliflorae and Plurinerves in Australia, although not on species of subgenus Acacia; the latter subgenus has only a single main vein, unlike the others which have several (Morris et al. 2002; Mound & Morris 2005). Much of the diversification seems to have occurred subsequent to the radiation of of Acacia as aridification increased within the last 10 million years (McLeish et al. 2007).

Some 70% of seed beetles, bruchids (Chrysomeloidea-Bruchidae/Bruchinae), are associated with Fabaceae, the legume-feeding Bruchini perhaos diverging between 57.9-51 million years ago, quite soon after the origin of Fabaceae themselves (Kergoat et al. 2011); particular groups of bruchids maye be associated with particular groups of Fabaceae (e.g. Kergoat et al. 2011 and references). Bruchini are a large group with some 1700 species whose larvae are specialized seed-eaters. They have diversified considerably on Fabaceae; perhaps first associated with Faboideae, they then moved on to other groups following the chemistry of the plants involved (esp. Kergoat et al. 2005a, b; see also Johnson 1989, 1990 [Acanthoscelides], Birch et al. 1989 [chemistry of the interaction], and Janzen 1969 [the complexity of the association between plant and weevil]; Kato et al. 2010 [importance of oviposition preferences of females]); stem Bruchinae may be 85-82.6 million years old (age spread far greater) and have eaten the seeds of Arecaceae (Kergoat et al. 2011). Two clades, made up largely of New World Acanthoscelides and predominantly Old World Bruchidius, dominate, and they may have radiated contemporaneously with their hosts, largely Fabaceae-Mimosoideae and Faboideae (elsewhere also on some Malvaceae, in particular); they can detoxify the non-protein amino acid, L-canavanine. For some estimates of divergence of particular groups of bruchids on particular clades of Faboideae, see Kergoat et al. (2011). The pattern of association of bruchid groups with mimosoids is interesting; individual bruchid genera tend to be found on adajcent pectinations of the mimosoid phylogenetic tree (Kergoat et al. 2007).

Less widespread but very well known is the close association of ants with some members of the old Acacia subgenus Acacia (= Vachellia). These includes the swollen-thorn acacias such as V. sphaerocephala which provide protein-rich Beltian bodies at the ends of the leaflets (the leaves have many leaflets, even for Acacia s.l.) as food for the Pseudomyrmex ants, and there are swollen stipular thorns that serve as their homes (Janzen 1974b, see Webber & McKey 2009 for comments on our understanding of this system). The ants also take nectar from extrafloral nectaries, and in the case of these close associations, the nectar produced is sucrose-free, the ants lacking the invertase needed to break down sucrose (Kautz et al. 2009). Interestingly, species of Acacia with low rewards are derived from species with higher rewards and with ant mutualists that defend them; species that offer only low rewards are often colonized by exploiter ants that do not defend the plant (Heil et al. 2009). Other examples of close ant-plant relationships are scattered elsewhere in the family (McKey 1989 for a list). A recent study of the common African Leonardoxa africana details the importance of the third party in the relationships, an ascomycete (Defossez et al. 2009, 2011), indeed, nitrogen from the ants initially moves more into the fungus than the plant (for plant-ant signalling in this association, see Vittecoq et al. 2011).

More general legume/ant associations are mediated by extrafloral nectaries. These secrete nectar and attract ants that can protect the plant bearing them, and they have possibly evolved some 35 times in the family - and also been subsequently lost and even regained (e.g. Marazzi et al. 2011; see also McKey 1989). They are notably common in Mimosoideae, being found towards the base of the petiole and sometimes on petiolules, and the nectar they secrete usually contains sucrose. Such nectaries are less common in "Caesalpinioideae", or they are represented by tufts of hairs (Pascal et al. 2000), and they are still less common in Faboideae.

The presence of such extrafloral nectaries characterises a major clade within Senna. It has been suggested that they are a "key innovation" there that is involved in the diversification of that clade, which is both much more speciose than its sister clade (68, no nectaries/282, nectaries) and diversified significantly faster. Extrafloral nectaries attract ants that help defend the plant against insects. The extrafloral nectary-bearing clade may have exploited the new habitats that became available in South America after the Andean uplift (Marazzi et al. 2006; Marazzi & Sanderson 2008, esp. 2010). Marazzi and Sanderson (2010) suggest a crown-group age for the extrafloral nectary clade of some 40.79-30.56 million years, that is, slightly before the Andean uplift (ca 30 million years ago); cf. also Lupinus and Astragalus. At the same time, Marazzi and Sanderson (2010) noted that Simon (2008) had found that the loss of extra-floral nectaries characterized a large clade of Mimosa that was far more speciose than its sister clade - indeed, the ratio of species in the sister taxa with and without extrafloral nectaries there is 15:515 (Simon et al. 2011).

Herbivory by foliovorous insects is quite extensive in the family, Cassia fistulosa sometimes being close to defoliated by caterpillars of pierid butterflies, while up to one third or more of the developing foliage of species of Inga may be eaten by herbivores (Kursar et al. 2009). Pinzón-Navarro et al. (2010) discuss the weevils found on Inga; up to 43 species of this speciose genus may coexist at a single site, and this may in part be possible because species differ considerably in antiherbivore defences, the defences varying independently between the species (Kursar et al. 2009). The toxic indolizidine alkaloid, swainsonine, is found in Astragalus (species with it are called "locoweeds") and Swainsona itself, and it causes a serious, sometimes fatal, disease in cattle (for its synthesis by associated fungi, see Pryor et al. 2009; Ralphs et al. 2008). The non-protein amino acids found in many Fabaceae (see below) may also be toxic, while the Australian Gastrolobium (Mirbelieae) produces the toxic sodium monofluoroacetate (Chandler et al. 2001).

Indeed, the diversity of "secondary metabolites" in Fabaceae, perhaps especially in Faboideae, is remarkable; for instance, about 28% of all known flavonoids and about 95% of the isoflavonoid aglycone structures - over 1,000 alone - identified in plants are known from Fabaceae, and the isoflavonoids are restricted to Faboideae. Isoflavonoids may be phytoalexins (defence), and are perhaps also involved in nodulation (Hegnauer & Grayer-Barkmeijer 1993; Reynaud et al. 2004). Flavonoids lacking the 5-hydroxy group are characteristic of Fabaceae (Seigler 2003), but I do not know at what level they are apomorphic. In general Fabaceae have a very distinctive nitrogen metabolism. Non-protein amino acids are common (see e.g. Fowden et al. 1979), and nitrogen in the xylem sap is transported as a mixture of amino acids, amides, and sometimes also ureides; very little is transported as nitrate. Wojciechowski et al. (2003, 2004, see also Wojciechowski 2003) note that the evolution of some non-protein amino acids are systematically interesting, thus canavanine production seems to have originated in the ancestor of one major subgroup of Faboideae (it includes mirbelioids, millettioids, robinioids, and the large group lacking the inverted repeat in the chloroplast genome, and may date to 54.3 ± 0.6 million years before present - Lavin et al. 2005 - see tree above). L-canavanine, which can be taken up in place of the normal amino acid L-arginine, may have potent effects on herbivores (e.g. Rosenthal 1990, 2001 and references; see also Huang et al. 2011 for non-protein amino acids). L-canaline is rather like the amino acid ornithine; both L-canaline and L-canavanine serve as nitrogen reserves for the plant. Pea albumin, a small sulphur-rich peptide with insecticidal properties, is known only from Faboideae where it may be a synapomorphy for the [hologalegina + millettioid] clade, being lost in some/all robinioids (Louis et al. 2007). Canavanine and alkaloid production are mutually exclusive in legumes, while within the genistoid legumes the presence of quinolizine and of pyrrolizidine alkaloids seems to be mutually exclusive (Wink 2008).

More conventional chemical deterrents are also found in Fabaceae, and a number of species have cyanogenic glucosides. Host-insect interactions have been studied in detail, for instance, those between cyanogenic host (Lotus corniculatus) and herbivorous insect (Zygaena filipendulae) - the latter can also synthesize the cyanogenic compounds themselves (Zagrobelny & Møller 2011, also references to other systems).

Bacterial/Fungal Associations. Fabaceae are well known for their association with nitrogen-fixing bacteria which grow inside irregular, pinkish-coloured nodules on the roots (Sprent 2009 for a summary). Rhizobium is perhaps the best-known genus involved. Nodule formation is initiated by the exudation of flavonoids, isoflavonoids, and other attractants by the host and infection of a root hair by a bacterium, although there are other ways the plant becomes infected, including through cracks, perhaps the plesiomorphic condition, as in Dalbergieae and Genisteae within Faboideae (Cannon et al. 2010). (Vessey et al. 2004). Nodule formation involves the production of Nod factors by the bacterium, although in a few nodule-forming α-proteobacteria (see below) such as the photosynthetic Bradyrhizobium there is no nodABC gene (Giraud et al. 2007). Nod factors are lipochito-oligosaccharides (LCOs), made up of a chain of 3-5 N-acétyl-D-glucosamine units, variously substituted and with a 16-20 C fatty acid attached. The plesiomorphic infection morphology is to have persistent infection threads and long-lived nodules (see also Parasponia - Cannabaceae), while more derived is the absence of infection threads, the mitosis of infected cells, and a short life span for the nodules (de Faria & Sprent 1995; see also Corby 1988: survey of nodules and their various morphologies; Sprent 2005: for nodule distribution, see also J. J. Doyle 1994, 1998; J. J. Doyle et al. 1997; Lavin et al. 2001; Oono et al. 2010). Inside the plant the bacteria differentiate into bacteroids, either reversibly and without much morphological change or non-reversibly. In the latter case, which is much less common (Oono et al. 2010), they become swollen; N-fixing by these swollen bacteroids is more efficent than by non-swollen bacteroids (Oono & Denison 2010). One or a few bacteroids are enclosed by a plant membrane, the whole forming an organelle-like symbiosome (Streng et al. 2011, summary). The nodules themselves are anatomically rather like stems having peripheral vascular bundles, the bacteria being in the pith (Franche et al. 1998), although nodule origination occurs where lateral roots develop (op den Camp et al. 2011). Indeed, in Faboideae, there seems to have been cooption of genes originally involved in lateral root origination after a genome duplication event ca 54 million years ago (op den Camp et al. 2011) - after the divergence of Faboideae from N-fixing clades such as Chamaecrista, which do not have this duplication (Cannon et al. 2010).

Nodulation is especially widespread in Faboideae and Mimosoideae, but less common in "Caesalpinioideae" - although occurring in taxa like Chamaecrista. In many "Caesalpinioideae" persistent infection threads occur, although these are also to be found in some Faboideae (Naisbitt & Sprent 1992). Generally speaking, symbiont specificity is greatest in the IRLC clade (Faboideae, see below), although genera like Astragalus are exceptions (Howard & Wojciechowski 2006). Within Faboideae, the nodulating Swartzia (derived nodule morphology) and immediate relatives may form a clade sister to the rest of the subfamily (support is weak, see Ireland et al. 2000; Pennington et al. 2000; Lavin et al. 2005), although some other Faboideae that are also in clades that are separate from that including the bulk of the subfamily do not nodulate. However, most Faboideae are nodulators (Sprent 2000, 2001, 2007).

Details of the evolution of nodulation in Fabaceae are still not well understood. The ability to nodulate has been acquired more than once, perhaps even several times, within the family. Although most nodulating bacteria are members of the proteobacteria α-2 subclass, they do not form a monophyletic group, and several "species" are involved; Agrobacterium (crown gall tumour) and others are also members of this group (J. J. Doyle 1998; Sprent 2001). Yet other N-fixing bacteria are associated with Fabaceae. These include Burkholderia, a ß-proteobacterium not at all close to Rhizobium and relatives, however, it is also an effective nitrogen-fixing symbiont of at least some Faboideae and of Mimosa. Other ß-proteobacteria can form nodules, albeit ineffective, with Mimosoideae (Moulin et al. 2001; Sprent 2002; Elliott et al. 2007 and references), and an association with ß-proteobacteria may be quite common in the tropics (Sprent 2007). Thus the ß-proteobacterium Burkholderia and relatives (some of which are pathogenic, but these rarely nodulate) form two groups, one involved in symbioses with New World Mimosa and Mimosoideae, the other (B. tuberum) nodulating African Faboideae in Crotalarieae and Phaseoleae (Bontemps et al. 2010).

In Oxytropis kansuensis, at least, the toxic indolizidine alkaloid, swainsonine, is synthesised by the endophyte Undifilum (an ascomycete, imperfect stage of Pleosporaceae: Pryor et al. 2009). Swainsonine is also found in Astragalus and Swainsona itself; the related fungus Embellisia is also implicated in this association (Ralphs et al. 2008).

A number of Fabaceae, especially non-nodulated members and including Acacia s. str. and "Caesalpinioideae" like Dicymbe, are ectomycorrhizal (Sprent & James 2007 for literature; Smith & Read 2008); see introduction to the N-fixing clade, also above. Ectomycorrhizal caesalpinoids also include Isoberlinia and Brachystegia common in the widespread deciduous miombo forests of east and south-central Africa (e.g. Högberg 1990 and Smith & Read 2008 for references).

Rusts show an interesting pattern of distribution on Fabaceae. Uromyces is found predominantly on herbaceous Faboideae, but also on Bauhinia and one or two other woody taxa (being found, along with related genera, on Acacia in Australia alone), while Ravenelia is found on woody members of the family, i.e. "Caesalpinioideae", but also especially Mimosoideae (Savile 1976, 1979a, b; El-Gazzar 1979). In a number of species of Ravenelia the teliospores, thick-walled spores in which nuclear fusion and then meiosis occur, are aggregated into groups, and these telial heads may mimic the groups of pollen grains (polyads) that are common in Mimosoideae. Stingless Trigona bees may pick up the telial heads and polyads as they forage for pollen. However, Ravenelia is only very rarely found on Australian Acacia; the distributions of rusts, acacias and trigonid bees all break at about Wallace's Line.

Vegetative Variation. Although most Fabaceae have once or twice compound leaves, leaflets with entire margins, and pulvini associated with leaves and leaflets, there is extensive variation on this theme; thus palmate leaves occur in Lupinus and unifoliate leaves are scattered in the family. In Acacia s. str. (the old subgenus Phyllodinae), the leaves of the mature plant are much modified and are often called phyllodes, although seedlings and regeneration shoots may have once or twice compound leaves. Kaplan (1980) suggested that these "phyllodes" were not equivalent to the petiole of a compound leaf, but to the leaf as a whole. In the early development of normal leaves there are two adaxial meristems that go on to develop the leaflets/pinnae; the leaflets/pinnae become lateral in position by secondary reorientation. However, in Acacia there is a single, broader adaxial meristem that develops into the entire leaf, so the leaves are flattened at right angles to the plane of flattening of a normal leaf. Complicating the issue, in some species of Acacia these apparently phyllodinous leaves are densely set along the stem, but only some are associated with stipules and buds, others lack both. A number of Faboideae (e.g. Vicia, Pisum) are tendrillar vines, the tendrils being modified terminal leaflets; in Lathyrus aphaca the photosynthetic function of the leaf is taken over by the large stipules, the rest of the leaf being tendrillar, while L. nissolia lacks tendrils and has a phyllodinous leaf (see Kenicer et al. 2005 for a phylogeny). The leaves may be reduced to a single more or less connate pair of leaflets, as in Bauhinia, named after the botanical brothers Caspar and Jean Bauhin.

In general, angiosperm leaf development is associated with the activity of the KNOX1 gene, and this is true of plants with compound leaves, i.e. Fabaceae. However, in the inverted repeat loss clade (IRLC clade - Faboideae, see below) the KNOX1 gene is not expressed in the developing leaves, but the FLO/LFY gene, normally a floral regulatory gene, is expressed there, while it continues to be expressed in the flowers, too (Hofer et al. 1997). Interestingly, the leaves in the IRLC clade lack pulvini (Champagne et al. 2007; see also Rosin & Kraemer 2009).

Some species of Mimosa and other genera have leaves that are sensitive to touch, stimulus transmission occurring as membrane depolarisation is propagated down the petiole and along the stem; folding of the leaf is caused by tugor changes in the cells of the pulvini at the bases of the leaf and leaflets (for the anatomy of the pulvinus, which has an endodermis, see Rodrigues & Machado 2007). In taxa like Albizzia (Samanea) saman, similar movements occur as the leaflets fold towards the evening when the light is failing, or just when there is heavy cloud cover, this behaviour being responsible (in some tellings of the tale) for its name, the rain tree. In Desmodium gyrans the single pair of lateral leaflets move intermittently without being touched, the speed of movement increasing with the temperature. Simon et al. (2011) suggest that sensitive leaves have evolved ca six times in Mimosa alone, although a full understanding of the evolution of this feature depends on more extensive studies on this and related phenomena in legume leaves.

Floral Biology & Seed Dispersal. Lewis et al. (2000) summarize what is known about pollination in Fabaceae, especially in "Caesalpinioideae". The monosymmetric pea flower or papilionaceous floral morphology (see below) and its variants are common in "Caesalpinioideae" and especially Faboideae. However, papilionaceous flowers encompass a variety of morphologies; as Bruneau et al. (2005, p. 201) note of caesalpinioid legumes, "zygomorphy is expressed as a multitude of homoplasious morphs". Hardly surprisingly, flowers of Fabaceae attract a diversity of pollinators that visit the flowers for various rewards. Pollination in "Caesalpinioideae" is predominantly by polylectic bees, while oligolectic bees are commoner pollinators of Mimosoideae and Faboideae. However, this may be as much a reflection of where these subfamilies occur, since oligolectic bees are more speciose in (warm) temperate regions, especially Mediterranean climates (Michener 1979; Kuhlmann & Eardley 2012), and that is where the latter two subfamilies are particularly common. Interestingly, within the tropics bees seem to be commonest in the New World (Michener 1979), and woody Fabaceae are especially diverse there.

The monosymmetric papilionoid flower is characterised by the more or less erect ultraviolet-absorbing banner petal which sometimes has colour patterning, the two wing petals, and the paired interlocking keel petals enclosing the stamens; bee pollination is the norm. (For pollination in keel flowers in general, see Westerkamp [1996, 1997].) Although the flowers of Cercis are only superficially similar to those of Faboideae (Tucker 2002a), both are more or less papilionoid; they have keels and are quite similar functionally (but Cercis lacks the sculpturing on the wing petals that is common in Faboideae). In some Caesalpinia s.l. the abaxial sepal is coloured and more or less functions as a keel. Monosymmetry in Faboideae, at least, involves duplication of a CYC gene occured early in the diversification of Faboideae, if not before (Citerne et al. 2003), and consequent dorsalization of the flower (see also Fukuda et al. 2003; Feng & al. 2006; Wang et al. 2008). Polysymmetry in the African Cadia (Faboideae-genistoid), a "reversal", is the result of dorsalization of the flower, the same basic principle that results in peloric flowers in Antirrhinum (Citerne et al. 2006); Cadia is sister to a largely Cape group of genera of the Podalyrieae-genistoids (Boatwright et al. 2008a) that have ordinary papilionoid flowers. Mirror image flowers are common in Fabaceae except for Mimosoideae (Tucker 1996b), while Hesse (1986) noted that both Bauhinia and Cercis - and Caesalpinia and Delonix - had pollen-connecting threads made up of something other than sporopollenin.

Faboideae are pollinated in a variety of ways, their floral morphology varying accordingly (for a survey, see Arroyo 1981), although their pollen is relatively uniform (ref.?). Interestingly, variation in the micromorphology of the epidermis between different petals of a single flower has so far been observed only within Faboideae (Stirton 1981; Ojeda et al. 2009); the outer surfaces of the wing petals in particular are variously sculpted, or have pockets and folds that afford footholds for the bee pollinators. When the androecium is monadelphous, i.e. the filaments of all the stamens are connate, the pollinator reward is often pollen, and this can be delivered by a pump-type secondary pollen presentation mechanism. The bee lands on the keel, and the style then forces pollen out of the keel in a tooth paste-like strand, as in Lupinus. If diadelphous - nine stamens are connate and a single adaxial stamen is free - the reward is often nectar, the nectary lying between the filament tube and gynoecium, the nectary being quite variable in morphology (see also Vogel 1997 for nectar which is secreted in a variety of positions, Indigofera even has short nectar-secreting spurs; Davis et al. 1988). Other taxa like Cytisus, Desmodieae and Indigofera have explosive pollination. Here the style is held under tension which is released as the style curves when the pollinator lands; such flowers can be visited only once. Vicia is another genus that has secondary pollen presentation, and there the pollen is presented to the pollinator on a stigmatic pollen brush; such a brush is found in a number of other Faboideae, mostly with asymmetric flowers (see e.g. Lavin & Delgado-Salinas 1990), where it may also be involved in pushing the pollen up a tube-like keel. Erythrina is pollinated by perching (sun) and hovering (humming) birds, depending on where in the world it grows, and both floral morphology and how the flowers and inflorescences are held varies according the requirements of these different visitors (Bruneau 1997). The flowers of Swartzia, sister to all other Faboideae, are very different from those of all other Fabaceae in their connate sepals, (0-)1(-2) petal, numerous free and dimorphic stamens developing from a ring meristem, and absence of nectar; pollination here may be by euglossine bees (Tucker 2003b for floral morphology; Torke & Schaal 2008 for a phylogeny).

Buzz pollination is quite common, for example, it occurs throughout the large genus Cassia s.l. ("Caesalpinioideae": Lewis et al. 2000), now divided into three genera. As one might suspect, the Cassia s.l. clade has anthers dehiscing by pores, and these have four different modes of development (Tucker 1996b). The flowers of Senna are often enantiostylous and lack bracteoles (enantiostyly is likely to have been acquired once, although also subsequently lost); the anthers dehisce by pores and are basifixed. There are three (or more) stamen morphs: three abaxial staminodes, four middle medium-sized stamens from which pollen is taken by the bees, and three longer abaxial stamens pollen from which is actually involved in pollination (see Tucker 1996b; Marazzi & Endress 2008; Marazzi et al. 2007). Cassia s. str., with dorsifixed anthers, also has three stamen morphs. The filaments are curved and the anthers have slits or basal pores. Finally, the largely herbaceous Chamaechrista is also enantiostylous; the stamens have two morphs in different whorls, the filaments are short, and the basifixed anthers dehisce by pores and have a velcro-like line of hairs. There is considerable variation in stigma morphology; the stigmas are often porate, with an exudate (Dulberger et al. 1994; Marazzi et al. 2007 and references). Details of pollination are poorly known, but Westerkamp (2004) suggests that in some species of both Senna and Chamaechrista the orientation of some anthers is such that the pollen ejected when the flower is vibrated initially misses the bee entirely, but bounces off the petals and ultimately lands on the back of the bee - whence it is removed by the stigma; enantiostyly is an integral part of this remarkable pollination mechanism.

Many species of Cassia and its relatives have asymmetrical flowers, and these are also characteristic of Phaseolinae as a whole. in the latter, the labellum is twisted asymmetrically, forming a tube rather like an elephant trunk (cf. Pedicularis - Orobanchaceae), and pollen is pumped out of the end of the tube (Delgado-Salinas et al. 2011 for references; see also Lavin & Diego-Salinas 1990).

Mimosoideae have very different floral morphologies from other Fabaceae. Here numerous small and secondarily polysymmetric flowers are aggregated into attractive units, all flowers opening at about the same time. Pollen grains are frequently aggregated into polyads which are caught in the cup-shaped stigma that is of the appropriate size for the polyad of that species, and there are also about as many ovules in the ovary as there are pollen grains in the polyad (Banks et al. 2010; Kenrick 2003 for references and the implications of this pollination mechanism for the breeding system). Banks et al. (2011) note that all the pollen grains of a polyad form a single harmomegathic unit. In Calliandra s. str. the polyads have an associated sticky mucilage body by which they are attached to the pollinator, but the stigma is much larger and capitate and the polyads adhere to its surface (Prenner & Teppner 2005; Greissl 2006, cf. in part Teppner 2007). For more information on locellate anthers (scattered in the clade), polyads, anther dehiscence, etc., in Mimosoideae, see Prenner and Teppner (2005), Teppner (2007) and Teppner and Stabentheiner (2007, 2010) and references. Bats may also be pollinators, as in Parkia.

The legume s. str. is a single carpellate fruit that dehisces explosively along both sutures, the two valves twisting as they separate; such fruits have two layers of lignified fibres, at least one of which is oblique to the long axis of the fruit (Fahn & Zohary 1955). The legume is common in European-North American Faboideae, but it occurs also in the other subfamilies, including in Bauhinia and Duparquetia, both members of clades that may be sister to the rest of the family. The fruits of Cercis, in the same clade, are not explosively dehiscent, but are otherwise similar; they are also typologically rather similar to the fruits of Myristica, the nutmeg! However, overall there is a great diversity of fruit morphology in the family, including variously winged fruits, fleshy fruits, fruits breaking up into single-seeded units in different ways, and fruits modified for external animal transport with spines and hooks, for example, the velcro-like hooks on Desmodium (hence its common name, beggar's ticks). In Trifolium the calyx and corolla are both involved in fruit dispersal mechanisms. Arillate seeds are common and facilitate dispersal, which can be internal, and seeds that have red and black color patterns on the coat such as Abrus precatorius, Erythrina and the sometimes pluricarpellate Pithecellobium are well known mimic the color contrasts of red aril and black seed of some other Fabaceae, and also other plants (c.f. Corner's idea of transference of function - Corner 1958), but do not chew the seed of Abrus precatorius... There are also seeds with fleshy coats. However, in many taxa, especially those with explosively dehiscent fruits, the seed coat is very hard and may need scarification if germination is to occur (for fruits and seeds, see Corner 1951; van der Pijl 1956; Kirkbride et al. 2003; etc.). Close to a thousand Faboideae are myrmecochorous, and myrmecochory is also known from Australian Acacia (Mimosoideae: Mckey 1989; Lengyel et al. 2009, 2010); independent evolution of this dispersal mode has occurred several times within the family.

Other. Knoblauch et al. (2001) discuss the possible mode of action of the distinctive spindle-shaped non-dispersive protein bodies (= forisomes), found commonly in Faboideae (e.g. Behnke 1981b; Behnke & Pop 1981; Peters et al. 2010), in blocking the pores of the sieve plates when turgor pressure changes; the protein bodies change shape and volume very quickly depending on the concentration of Ca²⁺ ions, and ATP is not needed for this shape change (Peters et al. 2007, 2008, 2010). Within the Faboideae, forisomes are absent from a number of Galegeae, many members of which - including those species of Astragalus studied - also lack calcium oxalate crystals (Peters et al. 2010).

Cytisus purpureus forms a well-known graft hybrid with Laburnum anagyroides (+ Laburnocytisus adamii; see Herrmann 1951 for another example); the epidermis alone is Cytisus tissue, and any seeds, being derived from cells from deeper layers, will give Laburnum plants. However, the graft hybrid often breaks down, resulting in branches that are pure Laburnum anagyroides or pure Cytisus purpureus.

Economic Importance. For information on the domestication of soybean (Glycine max), common bean Phaseolus vulgaris, pea (Pisum sativum), the azuki bean (Vigna angularis) and relatives, see papers in Ann. Bot. 100(5). 2007, and for these taxa and lentil (Lens culinaris), see Fuller (2007). Weeden (2007) discusses the diversity of genetic changes involved in domestication of legumes. For the domestication of the peanut, Arachis hypogea, see Dillehay et al. (2007) and for its phylogeny, see Friend et al. (2010), and for the domestication of the lima bean, Phaseolus lunatus, see Serrano-Serrano et al. (2010).

Chemistry, Morphology, etc. Root nodule morphology may help delimit groups of genera in Faboideae (Wojciechowski 2003). Cluster roots have been reported in some Faboideae, including Lupinus, although they do not occur in all members of the latter genus, at least (Shane & Lambers 2005), while arbuscular mycorrhizal fungi occur in root nodules in several species, although their importance is unclear (Scheublin & van der Heijden 2006). The occurrence of galactomannans (storage polysaccharides) and the ratio of galactose to mannose that they contain in seeds of Fabaceae may be of phylogenetic interest (Buckeridge et al. 1995, 2000a, b). Some species of Mimosoideae and Faboideae have leaves that are rich in silica (Westbrook et al. 2009). Characters of woods of members of "Caesalpiniodeae" include rays that are usually more than 20 cells tall, presence of silica bodies, and axial canals (Evans et al. 2006); I do not know how these fit on to the current tree.

Details of hypanthial evolution within Fabaceae are unclear; it seems to have become much reduced and lost several times. The "normal" (for flowering plants) floral orientation of Mimosoideae with the median sepal adaxial and the median petal abaxial may be secondary; in some 4-merous Mimosoideae the median petal is adaxial (Prenner 2011). Although the normal orientation is also found in some caesalpinioids like Ceratonia, the inverted orientation occurs in both Cercis and Bauhinia (see Tucker 1989; Herendeen et al. 2003; Luckow et al. 2005), Duparquetia, many other caesalpinioids, and Faboideae. Note that the orientation of the single carpel is the same in all taxa.

For any understanding of floral development in Fabaceae, the numerous papers by Shirley Tucker are an essential starting point. The parts of the flowers of most Fabaceae develop in the unusual sequence sepals-carpels-petals-outer stamens-inner stamens, and there are other distinctive features of their development (e.g. Champagne et al. 2007; Feng et al. 2006; Wang et al. 2008; for variation in general patterns of floral development in Fabaceae, see Prenner and Klitgaard (2008b) who emphasize the diversity of developmental patterns even within the corolla whorl, and that although in Duparquetia and Faboideae the adaxial petal is in the outermost position, the two have developmentally different pathways. Even within Mimosoideae, the sepal-like whorl originates in various ways (Ramírez-Domenech & Tucker 1990), and particularly when there is complete loss of individual floral structures in development, overall floral morphology can be greatly changed (Tucker 1988, 2000).

For floral and inflorescence morphology, especially in Faboideae-Loteae, see Sokoloff et al. (2007a). In Hardenbergia violacea (Faboideae) the colour patterning on the standard may mimic an anther (Lunau 2006). For the adaxial sepal member in Mimosoideae, see Ramírez and Tucker (1990); they note that there are a variety of developmental pathways that result in the connate calyx of that subfamily. For more floral development in Mimosoideae, see Gemmeke (1982); the androecium may be centripetal when borne on five main primordia. Prenner (2004b) notes the distinctive cochlear-descending calyx aestivation, helically-initiated androecium, etc., of Calliandra s. str., rather isolated within Mimosoideae. For polyads, anther dehiscence, etc., in some Mimosoideae see Teppner (2007) and Teppner and Stabentheiner (2007) and references. n Bauhinia there are additional staminodial structures at the base of the ovary (Endress 2008c) - or perhaps they have something to do with colleters. Pennington et al. (2000) discussed floral evolution in "basal" Papilionoideae, some of which like Swartzia have flowers with very derived morphologies. The pattern of initiation of the sepals and stamens in Faboideae is variable, by no means always being unidirectional (e.g. Prenner 2004a; de Chiara Moço & de Araujo Mariath 2009 - cf. characterization). The flowers of some Amorpheae have a stemonozone rather than a hypanthium (McMahon & Hufford 2002). Prenner (2004c) suggested that a slight asymmetry in the early development of the androecium (the adaxial median stamen is initiated slightly off the median axis) occurs in more "basal" Faboideae and also some "Caesalpinioideae". Androecial initiation in Swartzia can be both centripetal and centrifugal (ref.?).

"Caesalpinioideae" have 4(-7)-nucleate tapetal cells, while those of Mimosoideae and Faboideae are 1-nucleate (Wunderlich 1954) - this character may have some systematic significance. Pollen variation in Fabaceae is quite considerable outside Faboideae (Bente Klitgaard, pers. comm.), that of Duparquetia being unique among that of angiosperms (Banks et al. 2006). The style is at least sometimes hollow, although the cavity arises in various ways, including by lysigeny (Lersten 2004). The carpels may have five traces and are quite often open during development in "Caesalpinioideae", but not, apparently, in Cercideae, Mimosoideae or Faboideae (Tucker & Kantz 2001). The embryo sac of some Faboideae (?elsewhere) more or less protrudes into the micropyle, as in Archevaletaia (Maheshwari 1950). There is a great deal of variation in the development of the embryo suspensor, even within Faboideae (Lersten 1983; see also Tucker 1987; Yeung & Meinke 1993; Rodriguez-Pontes 2008). Both a true endothelium and an integumentary endothelium may be present in Faboideae (Rodrigues-Pontes 2008 for discussion and references). For seed and embryo morphology in Faboideae, see Kirkbride et al. (2003); the two recurrent vascular bundles lateral to the hilum are absent in "basal" Faboideae (Lackey 2009). For the aborting plumule in seedlings of Lotus and Coronilla and their relatives, see Dormer (1945).

For general information see Polhill and Raven (1981), Ferguson and Tucker (1994), Crisp and Doyle (1995), Doyle and Luckow (2003), and Lewis et al. (2005: well-illustrated summary of geographic distribution, etc., of all the genera; some of the taxa recognised in the body of the book are para/polyphyletic). For general chemistry, about which a great deal is known, see Hegnauer (1994, 1996), Southon (1994), and Hegnauer and Hegnauer (2001), and for additional details, see also Frohne and Jensen (1992) and Waterman (1994: secondary metabolites), for the evolution of these secondary metabolites, see Wink and Waterman (1999), Wink and Mohamed (2003: particularly useful) and Wink (2003), for polysaccharides and flavonoids in particular, see Hegnauer and Grayer-Barkmeijer (1993) and Harborne and Baxter (1999), for terpenoids, see Langenheim (1981, 2003), for seed galactomannans, etc., see Buckeridge et al. (2000b) and Meier and Reid (1982: Lupinus has galactans in its cotyledons), for alkaloids, see Aniszewski (2007), and for glucosylceramides, see Minamioka and Imai (2009). For starch, see Czaja (1978) and , for epidermal wax crystals, see Ditsch et al. (1995).

For wood anatomy, see Baretta-Kuipers (1981), Gasson et al. 2003, 2009 ("Caesalpinioideae"-Caesalpinieae), and Evans et al. (2006: Mimosoideae). For information about seed coat anatomy, see e.g. Pammel (1899), Corner (1951), Gunn (1981), Kirkbride and Wiersema (1997), Lackey (2009) and on fruits and seeds in "Caesalpinoideae", see Gunn (1991); many features other than those noted in the characterisation above may be of systematic interest. Luckow et al. (2005) discuss variation in flower and seed in the Mimosoideae; for embryology, etc., Newman (1934), Dnyansagar (1970) and Guignard (1881), general floral and inflorescence morphology, Endress (1994b), carpel development, van Heel (1981, 1983), gene and intron loss, J. J. Doyle et al. (1995), floral development, Tucker (1996a, b and references, 2001 [Cynometreae], 2002b, c, 2003c [all Detarieae], 2003a [general], 2003b [Swartzia]), Endress (1994b [general], van Heel (1993: Archidendron, if five carpels, alternate with corolla), Mansano and Teixeira (2008: Lecointea clade ), Pedersoli et al. (2010: Copaifera, Detarieae), Song et al. (2011: Clianthus), and Paulino et al. (2011: Indigofera), pollen morphology, Banks and Klitgaard (2000), Banks et al. (2000), Kuriakose (2007). For cotyledon areole presence, the size of the areole being linked to the amount of endosperm, see Endo and Ohashi (1998) and Lackey (2011), for endosperm, see e.g. Rau (1953), for the pleurogram, esp. in Chamaechrista, De-Paula and Oliveira (2008), and for fruit anatomy in Crotalaria and relatives, see Le Roux et al. (2011).

Phylogeny. Fabaceae are monophyletic in both molecular and morphological analyses. However, relationships at the base of Fabaceae are currently unresolved; the classical Caesalpinioideae are paraphyletic, Mimosoideae and Faboideae are monophyletic. In addition to placing Cercideae as sister to the rest of Fabaceae, Wojciechowski et al. (2004) found that Dialiinae were sister to the remainder. There were then two main clades, the Mimosoideae, to which Ceratonia, Gleditsia, etc., Caesalpinieae, Cassieae, and Cercideae (all "Caesalpinioideae") are more or less successively sister taxa, and Faboideae; Bruneau et al. (2008a, b) found a somewhat similar set of relationships (see tree here). Cercis and Bauhinia may be sister to all other Fabaceae (e.g. J. J. Doyle et al. 2000 and references; Bruneau et al. 2001), although they are placed sister to Detarieae s.l. (inc. Cynometra) sometimes with only with moderate support (Wojciechowski et al. 2004; Lavin et al. 2005; Forest et al. 2007b). Detarieae include genera like Cynometra, Tamarindus and Amherstia and have also been placed by themselves as sister to all Fabaceae minus Cercideae. Duparquetia is also in this general area (Forest et al. 2002; Tucker et al. 2002), and was placed sister to Dialiinae in the study by Herendeen et al. (2003). Recent studies (Bruneau et al. 2008a, b) find that Cercideae, Duparquetia, and/or Detarieae s.l. all remain candidates for being sister to the rest of the family. Morphology and anatomy support such relationships. Thus all three lack vestured pits (they are also absent in Cassieae), but such pits are common in the rest of the family, i.e. their presence is largely congruent with phylogeny. Duparquetia is highly derived, and so although the carpel develops after the stamens are initiated, unlike all other Fabaceae studied (Prenner & Klitgaard 2008), there is only a single staminal whorl...

Within Cercideae, Cercis is sister to the rest (Sinou et al. 2009). Generic limits of Bauhinia itself are discussed by Sinou et al. (2008, 2009), and at least Bauhinia s. str. lacks the srp12 intron (Doyle et al. 1995; Lai et al. 1997) and also the rpl2 intron (Sinou et al. 2009). The standard of Duparquetia shows colour patterning. The parts of the flower show normal acropetal initiation, unlike the case in many other legumes (Prenner & Klitgaard 2008a, esp. b for details of floral development). Detarieae are well known for showing extensive loss of petals and/or stamens, or increase in the latter (Tucker 1992b, 2000, etc.): In Monopetalanthus durandii the flower is surrounded by bracetoles and the floral formula is K 1 (minute), C 1; A 10; G 1, Brachystegia glaucescens also has large bracteoles, K 5 (all small), C 0; A 10; G 1, while Dialium guineense has small bracteoles, and a floral formula of K 5, C 1 (small); A 2; G 1 (Tucker 2000). Many Detarieae have crater-like glands on the abaxial surfaces of the leaflets, they secrete resin, having secretory canals in the stem, and they also have caducuous stipules and bracteoles, etc. (Redden & Herendeen 2006: morphological phylogenetic analysis; Fougère-Danezan et al. 2003, 2007, 2010: molecular and morphological studies, characters of the group). The resins produced by Detarieae contain distinctive bicylic diterpenes, possibly an apomorphy for the tribe (Fougère-Danezan et al. 2007). Pollen is also extremely variable in this group (Banks & Klitgaard 2000; Banks 2003). Detarieae s. str. and Amherstieae have amyloid in their cotyledons, x = 12 (Hegnauer & Grayer-Barkmeijer 1993); amyloid is also found in Sclerolobieae (?different classifications?: see Kooiman 1960; Meier & Reid 1982). Redden et al. examined phylogenetic relationships in the Brownea clade, possible synapomorphies for it being an unchanneled leaf rachis, thread-like stipules, connate bracteoles, four sepals, and introrse anthers. Finally, in a classic study Léonard (1957) described seedlings of some African members (Cynometreae, Amherstieae) of this group.

Whatever the relationships among these clades, the rest of Fabaceae form a clade. Mimosoideae in the old sense are very largely monophyletic, as are Faboideae, but their recognition makes Caesalpinioideae paraphyletic. Umtiza is excluded from Detarieae and forms a clade with taxa like Gleditsia, Gymnocladus and Ceratonia, several of which are dioecious and have smallish, greenish flowers sometimes with a poorly differentiated calyx and corolla - not plesiomorphic features (Herendeen et al. 2003a; see also Forest et al. 2007b). For additional information on relationships in caesalpinioid legumes, see Herendeen et al. (2003b) and Lavin et al. (2005), for phylogenetic relationships within Senna, see Marazzi et al. (2006), for some pollen morphology, see Banks et al. (2003), and for relationships within Chamaecrista, see Conceição et al. (2009).

Some ex-caesalpinioids (e.g. Dimorphandra), which have small flowers in spikes or panicles, may have to be included in Mimosoideae (Wojciechowski 2003; Bruneau et al. 2008a, b), to which they show considerable similarity in wood anatomy (Evans et al. 2006) and also pollen, which is rather homogeneous although nearly always in monads (Banks & Lewis 2009), and/or Mimosoideae would have to be reduced to a tribe (Luckow et al. 2003). Genera like Pentaclethra are to be included (cf. Bouchenak-Khelladi et al. 2010b, but some confusion there?), while taxa like Dinizia, Pachyelsama and Erythrophleum with racemose inflorescence and small, more or less polysymmetric flowers with free sepals and petals (and ten stamens) form a basal grade (Bouchenak-Khelladi et al. 2010b). The Ingeae, derived, with a valvate calyx and many stamens connate and forming a tube, are embedded in Acacieae (e.g. Clarke et al. 2000; Robinson & Harris 2000; Miller & Bayer 2000, 2001; Luckow et al. 2003; Jobson & Luckow 2007; Brown 2008; Brown et al. 2008). The old Acacia subgenus Acacia, which includes the bull's horn acacias, seems to be monophyletic, but Acacia s.l. is polyphyletic (e.g. Bouchenak-Khelladi et al. 2010b). Murphy et al. (2000, 2003, 2010 [relationships still only moderately resolved]) and Miller et al. (2003) discuss the phylogeny of Acacia s. str., the old subgenus Phyllodinae, and Miller and Bayer (2003) that of Vachellia, the old subgenus Acacia, and Senegalia, the old subgenus Aculeiferum. Siegler (2003) summarized the phytochemistry of the complex, Evans et al. (2006) detailed wood anatomy, and Kergoat et al. (2007) noted what bruchids had to say about systematics of Acacia s.l.; see also Muelleria 26(1). 2008, a special issue on Acacia, and also World Wide Wattle website. Of other Mimosoideae, Mimosa may be monophyletic and sister to Piptadenia (Besseger et al. 2008); Simon et al. (2011) provide an extensive phylogeny of Mimosa, optimizing various characters on the tree. See Richardson et al. (2001b) for the diversification of Inga. Catalano et al. (2008) provide a phylogeny of the ecologically important New World genus Prosopis.

Faboideae are monophyletic. A topology (simplified) for Faboideae in general including [swartzioids: SWAR [Cladrastis, etc., [genistoids: GEN, [Amorpheae + dalbergioids = dalbergioids s.l.: DAL], [baphioids: BAPH [mirbelioids: MIRB [[Indigofereae + millettioids: MILL] [robinioids: ROB + Inverted Repeat Loss Clade: IRLC]]]]]]] seems moderately well supported (Wojciechowski 2003; McMahon & Sanderson 2006); the [robinioids + Inverted Repeat Loss Clade] clade is called the hologalegina clade. The tree here is based largely on Wojciechowski et al. (2004) and Peters et al. (2010). McMahon and Sanderson (2006) provide a supermatrix analysis of 2228 species of Faboideae. Within Faboideae, Swartzieae, woody, nodulators, lacking bracteoles, with very variable flowers and arillate seeds, may be sister to the rest, but support is weak and the exact circumscription of Swartzieae is unclear (Ireland et al. 2000; Pennington et al. 2000; Lavin et al. 2005); it may well be largely restricted to Swartzia. Swartzia has atypical seeds for Faboideae, for example, the testa being thin and cracking and the embryo straight, but these are likely to be derived features. Florally it is also distinctive: it has an entire calyx that is cast off as the flower opens, only a single petal, numerous free and dimorphic stamens, a strongly stalked ovary, and no nectary; some taxa have more than a single carpel (see Torke & Schaal 2008 for a phylogeny).

Many Faboideae have a 50kb inversion in the trnL intron in the large single-copy region of their chloroplast genome, however, taxa like Swartzieae, Sophora, and a few others, lack this inversion (J. J. Doyle et al. 1996, 1997; Pennington et al. 2001; Wojciechowski et al. 2004). There has also been the loss of the 25kb chloroplast inverted repeat; this characterises a largely temperate, epulvinate, herbaceous and very speciose group, the IRLC group (see Wojciechowski 2003 and references); the woody Wisteria is also a member of this clade. For relationships in Canary island Genisteae, see Percy and Cronk (2002), and in Loteae, see Allan et al. (2004). Desmodium and possibly related genera (MILL) have also lost the rps12 intron (it has moved to the nucleus) as well as the srp12 intron (Doyle et al. 1995; Bailey et al. 1997; Jansen et al. 2008). ORF84 has also been lost many times, and accD (= ORF512, zpfA) has also been lost (Doyle et al. 1995). Both the rps16 and ycf4 genes are lost in the majority of tribes of Faboideae (Doyle et al. 1995; Jansen et al. 2007). The IRLC clade is characterized not only by the loss of the inverted repeat, but the compound leaves lack pulvini and differ in details of development (see above), there are CA primordia in the flower, A initiation being bidirectional, and overlap in the timing of C, A, and G initiation (Naghiloo & Dadpour 2010). All members of the IRLC clade lack the clpP intron, while the rps12 intron has been lost from all members of the clade examined except Wisteria, Callerya and Afgekia - but not Glycyrrhiza - cf. the tree above (Jansen et al. 2008; Wojciechowski et al. 2008; see also Saski et al. 2007). Indeed, genome evolution in taxa that lack the inverted repeat has been considerable (Magee et al. 2010); overall, these and other changes in chromosomal organisation provide a considerable amount of phylogenetic structure.

For the phylogeny of dalbergioid legumes, see Lavin et al. (2000); desmodioid nodules, small oblate nodles of determinate growth that are always associated with a lateral root, are common there (Lavin et al. 2001). The large genus Machaerium is more related to Aeschyomene section Ochopodium (that genus is polyphyletic) than to Dalbergia, so the apparent similarities in habit, fruit, etc, need re-evaluating (Ribeiro et al. 2007). For relationships within Amorpheae and the floral evolution of the latter (petals may be lost, or all look rather similar; a stemonozone, a tube formed by the adnation of filaments to the corolla, may be developed; etc.), see McMahon and Hufford (2002, 2004, 2005) and McMahon (2005), for that of Robinia and its relatives, which include Lotus and Sesbania, which are quite close, see Lavin et al. (2003) and Farruggia and Wojciechowski (2009), of Crotalarieae, see Boatwright et al. (2008b, esp. c) and of Lotononis and relatives in particular, Boatwright et al. (2011: also character evolution), and for that of Psoraleae, see Egan and Crandall (2008). For diversification in Cape genistoids, see Edwards and Hawkins (2007), and for phylogenies or revisions of Mirbelia s.l., see Crisp and Cook (2003a, b), Gastrolobium, Chandler et al. (2001), Pultenaea, Orthia et al. (2005), Jacksonia, Chappill et al. (2007), Ononis, Liston (1995), Arachis, Krapovickas and Gregory (2007 - for the domestication of the peanut, see Dillehay et al. 2007), Cytisus, Cubas et al. (2002), on Bossiaea. Members of the millettioid clade have a pseudoracemose inflorescence with more than a single flower at each node (Tucker 1987a); Indigofereae, its sister clade, have true racemes (Wojciechowski et al. 2004), while the combined clade may share early expression of monosymmetry in floral development (Paulino et al. 2011). For the delimitation of Millettieae, see Lavin et al. (1998); Hu et al. (2000) studied their phylogeny, Kajita et al. (2001: rbcL) that of Millettieae and relatives. Stefanovic et al. (2009: eight chloroplast genes) concetrated on relationships among the some 2,000 species of Millettieae-phaseoloids, finding substantial resolution; they found that i.a. Mucuna was sister to Desmodium and its relatives, and the combined clade was sister to the rest of the group - which includes Cajanus, Vigna, Erythrina etc. For a phylogeny of Phaseolus itself, see Delgado-Salinas et al. (1999, 2006); Vigna has to be dismembered (Delgado-Salinas et al. 2011). Schrire et al. (2009) disentangle relationships within Indigofereae, finding considerable phylogenetic structure (i.a. there are four major clades within Indigofera) that can be linked with both morphology and ecology. Thompson et al. (2001) looked at relationships within Brongniartieae, members of which are Australian-South American.

Within the IRLC, Astragalus is an extremely speciose genus characterising drier areas of both hemispheres, and a number of taxa have leaf rhachis spines. Extensive phylogenetic studies (e.g. Wojciechowski 1993, 2004; Kasempour Osaloo et al. 2004; Scherson et al. 2004) show that most New World taxa are aneuploid (n = 11-15) and form a monophyletic group, other species are base 8; for relationships in Old World Astragalus, see Kasempour Osaloo et al. (2004), Kazemi et al. (2009) and Riahi et al. (2011). Oxytropis is sister to Astragalus. For phylogeny and diversification of Caragana in the context of the Qinghai-Tibetan Plateau uplift, see Zhang et al. (2009) and Zhang and Fritsch (2010). Within Trifolium the American species form a monophyletic group (Ellison et al. 2006; Liston et al. 2006). Phylogenetic relationships within Medicago have turned out to be highly reticulating (Maureira-Butler et al. 2008); Medicago probably includes Trigonella, and for its limits, see Bena (2001) and Steele et al. (2010). A preliminary phylogeny of Lathyrus suggested that the ca 20 South American species might represent a single clade derived from Northern hemisphere ancestors (Asmussen & Liston 1998; see also Kenicer et al. 2005 for a phylogeny of the genus).

Classification. See Pennington (1997) for a monograph of Inga and Dexter et al. (2010) for some species limits there. The old Acacia subgenus Acacia, which includes the bull's horn acacias, seems to be monophyletic, but Acacia s.l. is polyphyletic. As Maslin (2001) noted sadly of the 955 or so species then placed in Acacia for the Flora of Australia treatment, "we are obliged to present the flora treatment [i.e., everything in the one genus] in the absence of a more meaningful classification". However, things are changing (Maslin et al. 2003) - the argument now is over what names to call the bits into which Acacia s.l. is to be divided (see above). See Miller and Bayer (2003) for Vachellia, the old subgenus Acacia, and Senegalia, the old subgenus Aculeiferum; see also Siegler et al. (2006) for the American segregate Mariosousa. However, some are deeply unsatisified with this nomenclatural solution.

For a sectional classification of the neotropical Swartzia (Faboideae), see Torke and Mansano (2009). For generic limits around Gastrolobium, see Chandler et al. (2001), for those around Vigna, see Delgado-Salinas et al. (2011), and for those around Lotononis, see Boatwright et al. (2011),; in general, a fair bit of adjustment to generic limits seems to be need (e.g. see Percy & Cronk 2002; Allan et al. 2004; Ribeiro et al. 2007). Thompson (2001) provides a careful study of E. Australian Hovea (Brongniartieae).

Previous Relationships. Fabaceae s.l. are often referred to their own order, as in both Cronquist (1981) and Takhtajan (1997), and then they are usually divided into three families. They can be confused with Connaraceae (Oxalidales), although the latter lack stipules, their flowers are polysymmetrical and have stamens of two distinctly different lengths, and their gynoecium is frequently multicarpellate. However, in both the RP122 chloroplast gene has moved to the nucleus, and the ovaries of both have adaxial furrows (cf. the ventral slit: Matthews & Endress 2002). Fabaceae have also been linked with Sapindaceae (e.g. Dickison 1981b), here in the malvids, but there is little support other than the common possession of compound leaves - and none molecular - for such an association.

Botanical Trivia. There has been as much diversification of the ycf4 protein, involved in photosystem 1 assembly, within Lathyrus as there has been between cyanobacteria and other angiosperms (Magee et al. 2010).

[Surianaceae + Polygalaceae]: ?

SURIANACEAE Arnott, nom. cons.   Back to Fabales

Woody; ellagic acid?; cork also in inner cortex; storying +/0; wood fluorescing?; vessels in radial multiples; (sieve tube plastids with starch grains and protein filaments forming a peripheral shell); nodes 3:3 (1:1 - Suriana); (medullary vascular bundle - Recchia); sclereids +; petiole bundle arcuate to annular; leaves spiral or two-ranked, (unifacial; pinnate, leaflets alternate, articulated), (stipules 0 - Suriana); inflorescence cymose, usu. terminal; pedicels articulated; K connate basally or not, quincuncial, C (0), contorted, shortly clawed or not; ?receptacular tissue ± forming a ring around the C base; A obdiplostemonous (= and opposite sepals); pollen surface variable (vermiform - Cadellia); nectary 0; (gynophore +, nectariferous - Recchia), G 1-5, when 5 opposite C, styluli ± gynobasic, stigma clavate to capitate; ovules 1-5/carpel, campylotropous, surrounded by mucilage, unitegmic, integument 3-7 cells across, parietal tissue 4-5 cells across, (nucellar cap +), hypostase +; megaspore mother cells several, antipodal cells ± degenerate; fruit a berry, drupe or nut, endocarp with outer layer of palisade sclereids, other cells apart from the inner epidermis isodiametric, K persistent, accrescent or not; exotestal cells enlarged, cuboidal, tanniniferous, rest crushed [ca 7 cells thick]; chalazal endosperm haustorium +, endosperm 0, embryo green, curved or folded, cotyledons incumbent; n = ?; germination epigeal, phanerocotylar.

5[list]/8 Mostly Australian, also Mexico (Recchia), pantropical (Suriana maritima) (map: from van Steenis & van Balgooy 1966 [blue - Suriana maritima]; FloraBase xi.2010). [Photo - Flower]

Chemistry, Morphology, etc. The vegetatively "atypical" Suriana is the only genus whose embryology has been studied and the whole family is little known chemically. The family is vegetatively rather heterogeneous, although its wood anatomy is quite homogeneous (Webber 1936). The exotesta of Suriana is described as being green (Rao 1970). Both Cadellia and Recchia have thickened cell walls in the exocarp and sclereids in their bark parenchyma (Crayn et al. 1995).

For more information, see Jadin (1901) and Boas (1913: both vegetative anatomy), Mauritzon (1939: embryology), Gutzwiller (1961: general), Wiger (1935), Anantaswamy Rau (1940), Rao (1970) and Heo and Tobe (1994: all embryology, etc.), Hegnauer (1973, as Simaroubaceae: chemistry), Weberling et al. (1980: general); Gadek and Quinn (1992: pericarp), Crayn et al. (1995: relationships), Schneider (2006: general), and floral development (Bello et al. 2007/8: Suriana only). Additional data from: Cadellia - Benson s.n. = NSW 408528 (anatomy); Stylobasium - Latz 12864 (fruit), Strid 20708 (anatomy).

Phylogeny. For relationships, see Forest et al. (2007b); [[Recchia + Lundellia] [Suriana [Cadellia + Stylobasium]] seems to be the cladistic structure in the family. Although the sieve tube plastids of Stylobasium are distinctive, having sieve starch grains and protein filaments forming a peripheral shell (Behnke et al. 1996), there seems little reason to recognise Stylobasiaceae as a monotypic family since three more would be needed.

Previous Relationships. Surianaceae were included in Rosales-Simaroubaceae (here in Sapindales) by Cronquist (1981) and in Rutales as a separate family by Takhtajan (1997).

Synonymy: Stylobasiaceae J. Agardh

POLYGALACEAE Hoffmannsegg & Link, nom. cons.   Back to Fabales

Successive cambia +); saponin +; nodes 1:1; styloids 0; (stomata other than anomocytic); plant glabrous or with unicellular hairs; branching from previous flush; lamina entire, often paired glands [crateriform extrafloral nectaries] or thorns at nodes (elsewhere); inflorescence indeterminate; flowers monosymmetric, K quincuncial, caducous, C 5; A 8, connate, basally adnate to C, median adaxial A often absent; pollen polycolporate, surface psilate or foveolate; (disc excentric); G connate, style long, stigma dry; micropyle zigzag (endo-, exostomal), exostome often long, outer integument 2(-5) cells across, inner integument (1-)2(-3) cells across, parietal tissue ca 2 cells across, nucellar cap +, hypostase enlarged, (postament - Epirrhizanthes?); fruit a berry; seed often hairy, exotesta subsclerotic, endotestal cells ± palisade or not, U-thickened, crystalliferous (not); endosperm copious or not, starchy.

Ca 21[list]/940 - four tribes below. World-wide, except the Arctic and New Zealand. [Photo - Flower]

1. Xanthophylleae Chodat

Shrubs or trees; plants Al-accumulators; wood parenchyma apotracheal, diffuse; glands at nodes, (conspicuous domatia on leaves), K quincuncial, unequal, C contorted; A (7-10); G [2], placentation parietal, 2 or more apotropous ovules/carpel, in two rows, outer integument 4-12 cells across, stigma small, bilobed (capitate); (fruit irregularly dehiscent); testa multiplicative; hypostase massive; n = ?

1/95. Indo-Malesia (map: from van der Meijden 1982).

Although the seed coat anatomy is often undistinguished, some species have Polygala-type testa anatomy (see family characterisation); irregularly loculicidally dehiscent fruits also occur.

For a monograph, see van der Meijden (1982).

Synonymy: Xanthophyllaceae Reveal & Hoogland

[Polygaleae, Carpolobieae, Moutabeae]: inflorescence cymose; A ± adnate to petals, variously connate, often monadelphous; 1 epitropous ovule/carpel; exostomal/funicular aril + (0).

2. Polygaleae Chodat

Herbs (echlorophyllous mycoheterotrophs), lianes, shrubs; (ergoline alkaloids +), at least some smell of wintergreen, tannins 0 [Polygala]; pits vestured; banded paratracheal parenchyma +; (glands at nodes); two adaxial lateral K = wings, 2 abaxial lateral K, minute, two connate adaxial C = the standard, abaxial C = the keel, often fringed [with crest], 2 abaxial-lateral C minute; (A 2-7), anthers opening by apical pores; G [2] (adaxial member suppressed), stylar canal +, stigma bilobed, ± asymmetrical; fruit an often flattened capsule, drupe or samara, (K persistent, green - Polygala, etc.); caruncle + (chalazal aril +; no appendages)n = 6+, very variable.

Ca 13/830: Polygala (325, generic limits unclear), Monnina (180), Muraltia (120), Securidaca (80). World-wide, except the Arctic and New Zealand (Map: from GBIF 2009; FloraBase 2009; orange from Paiva 1998).

3. Carpolobieae Eriksen

(glands at nodes); (C contorted), abaxial C keeled; A (4) 5, anthers opening by short confluent apical slits; G [3], stigma capitate; n = 9-11.

2/6. Tropical Africa.

4. Moutabeae Chodat

Woody; plants Al-accumulators; banded apotracheal parenchyma +; glands on leaves (and at nodes); (inflorescence cymose); K adnate to C, abaxial C not keeled; A (6-10), anthers opening by short confluent apical slits; G [3-8], stigma capitate; funicular aril +; n = 14.

4/15. Tropical America, New Guinea to New Caledonia. [Photos - Flowers, Flower - Close-up, Petioles, Branch, Petioles with ants, Flower with moth]

For vegetative anatomy, see Styer (1977).

Synonymy: Diclidantheraceae J. Agardh, Moutabeaceae Pfeifferr

• Polygalaceae are woody or herbaceous plants that may be recognised by their often yellowish-drying simple and entire leaves; there are quite frequently paired glands at the nodes or glands or domatia on the leaf blades. The flowers are usually monosymmetric, and are more or less papilionaceous. They range from having five rather large sepals and five petals - not strongly papilionaceous - to having two of the sepals much enlarged and coloured (the "wings" of the flower), two of the petals much reduced, and the three remaining petals modified as "standard" and "keel" - strongly papilionaceous. There are two or more carpels and a single style.

Evolution. Divergence & Distribution. Wikström et al. (2001) date the origin of the clade to 68-66 million years before present (ca 84 million years in Bello et al. 2009 - but note topology), with diversification beginning in the Tertiary (65.5-)57.4(-49.3) million years ago (Bello et al. 2009). In the Cape region Muraltia started diverifying in the Fynbos (21.4-)18.5(-14.1) million years ago, and in the succulent karoo (4-)2.5(-1.3) million years ago (Verboom et al. 2009). The distinctive Paleosecuridaca curtisii has recently been described from the Palaeocene of North Dakota; although in gross morphology its fruits are remarkably like those of Securidaca and the seeds have a testa with a well developed palisade layer, there are two seeds per carpel (Pigg et al. 2008b).

Floral Biology & Seed Dispersal. The flower in Polygalaceae is quite differently constructed from that of Fabaceae (Westerkamp & Weber 1999; Bello et al. 2010, but see Prenner 2004d), although quite often both looking and being functionally very similar. Note that the flowers of Polygala, which in overall appearance are particularly like those of some Fabaceae, are unlikely to represent the plesiomorphic condition of the family, indeed, overall floral variation in Polygalaceae is very considerable.

In at least some North American species of Polygala pollen is presented on the sterile lobes of the asymmetrical stigma (secondary pollen presentation: Weekley & Brothers 1996; see Castro et al. 2008 for details; Bello et al. 2010 for details of stigma morphology).

In a study of ant dispersal in Polygalaceae, which is quite common in Polygaleae, it seems that caruncles may be an apomorphy of Polygaleae, although chalazal arils have also evolved more than once in this clade, and they and caruncles have been lost, too (Forest et al. 2007b; see also Lengyel et al. 2009, 2010 for myrmecochory). Evolution of these elaiosomes is suggested to have occurred (69.9-)54-50.5(-35.2) million years before present, well after initial diversification of the ant clades attracted to them. Muraltia, also myrmecochorous and with some 120 species found mostly in the Cape region of South Africa, appears to have diversified relatively recently, mostly within the last ca 10 million years (Forest et al. 2007a).

Bacterial/Fungal Associations. Epirixanthes is an echlorophyllous myco-heterotroph.

Vegetative Variation. Although genera like Xanthophyllum and some Moutabeae may have paired glands at the nodes, other genera seem to lack anything faintly comparable with stipules, and where stipules might be lost in this part of the tree is uncertain. De Aguiar-Dias et al. (2011) have recently suggested that the paired nectary glands at the base of the leaf in Polygala laureola are indeed stipules because they receive a vascular bundle from the single vascular trace.

Chemistry, Morphology, etc. In Polygala myrtifolia, with eight stamens, it is apparently the two stamens in the median plane - i.e., on opposite sides of the flower - that are lost (Prenner 2004d); see Bello et al. (2010) for other floral diagrams. For floral morphology and development of Polygaleae, see Krüger and Robbertse (1988) and Krüger et al. (1988), and for that of the family as a whole, see Bello et al. (2010). The tricolpate pollen of Balgooya is probably derived; some Polygalaceae such as Heterosamara have asymmetric, almost boat-shaped pollen grains (Banks et al. 2008).

Some general information is taken from Eriksen (1993a) and especially from Eriksen and Persson (2006), that on ovule and seed from Johow (1910: Epirrhizanthes), Verkeke (1985, inc. integument thickness, the inner integument of Securidaca is up to 9 cells across, 1991), Takhtajan (2000: ovule and seed), and Banks et al. (2008: pollen morphology and evolution). For chemistry, see Hegnauer (1969, 1990). Also see Polygalaceae website (Freire-Fierro 2001 onwards).

Phylogeny. Of the four groups mentioned above, Moutabeae may be paraphyletic (Persson 2001: trnL-F), although adding rbcL data suggests they are monophyletic (Forest, in Eriksen & Persson 2006), and morphology points in this direction (Eriksen 1993b); the other three groups appear to be monophyletic (although Carpolobieae are only weakly supported). However, all four tribes are strongly supported in a three-gene analysis (Forest et al. 2007b), and Xanthophylleae are sister to the other three tribes; relationships between the latter are unclear. Polygala and Bredemeyera are grossly paraphyletic (Persson 2001). See Eriksen (1993b) for a morphological phylogeny.

Classification. See Paiva (1998) for much information on Polygala, especially from Africa and Madagascar. Abbott (2011) split up Polygala in the North American flora.

Previous Relationships. The Polygalales of Cronquist (1981) included seven families, the mutual affinities of five of which were described as being "widely accapted". These include Xanthophyllaceae (= Polygalaceae), Vochysiaceae (Myrtales), Trigoniaceae (Malpighiales) and Tremandraceae (= Elaeocarpaceae, Oxalidales). For Emblingiaceae, often included in (e.g. Cronquist 1981; Mabberley 1997) or near (e.g. Takhtajan 1997) Polygalaceae, see Brassicales.