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 rich in p-parahydroxyphenyl and guaiacyl units; true roots present, apex multicellular, xylem exarch, 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 +; tracheid/tracheid pits circular, bordered; sieve tube/cell plastids with starch grains; phloem fibers +; 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, veins -5 mm/mm² [mean for all non-angiosperms 1.8]; axillary buds associated with at least 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, 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 duplication [N/O//A/C and P//BE lines], mitochondrial nad1 intron 2 and coxIIi3 intron and trans-spliced introns present.

MAGNOLIOPHYTA

Plant woody, evergreen; lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, non-hydrolysable tannins, quercetin and/or kaempferol +, apigenin and/or luteolin scattered, [cyanogenesis in ANITA grade?], lignins derived from sinapyl as well as coniferyl and p-coumaryl alcohols, containing syringyl units, S lignin [in positive Maüle reaction, syringyl:guaiacyl ratio less 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 2-layered tunica-corpus construction; wood fibers and wood parenchyma +; reaction wood ?, with gelatinous fibres; starch grains simple; primary cell wall mostly with pectic polysaccharides; tracheids +; sieve tubes eunucleate, with a sieve plate and cytoplasm with P-proteins, companion cells from same mother cell that gave rise to the sieve tube; nodes unilacunar [1:?]; stomata with ends of guard cells level with pore, paracytic, outer stomatal ledges producing vestibule; leaves with petiole and lamina [the latter 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 leaves with axillary buds; flowers perfect, polysymmetric, parts spiral [esp. the A], free, development in general centripetal, numbers unstable; P not sharply differentiated, outer members not enclosing the rest of the bud, smaller than inner members; A many, with a single trace, introrse, filaments stout, anther ± embedded in the filament, tetrasporangiate, dithecal, 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, binucleate at dispersal, trinucleate eventually, 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, [outer integument often largely subdermal in origin, inner integument dermal], inner integument 2-3 cells thick, micropyle endostomal, parietal tissue 1-3 cell layers; megasporocyte single, megaspore lacking sporopollenin and cuticle, chalazal, female gametophyte four-celled [one module, nucleus of egg cell sister to one of the polar nuclei]; P deciduous in fruit; seed exotestal; pollen germinating in less than 3 hours, siphonogamy, tube elongated, growing at 80-600 µm/hour, with callose plugs and callose-based walls, penetrating between cells, penetration of ovules 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, single copy of LEAFY and RPB2 gene, knox genes extensively duplicated [A1-A4], AP1/FUL gene, paleo AP3 and PI genes [paralogous B-class genes] +, with "DEAER" motif, SEP3/LOFSEP and PHYA + C/PHYB + E gene pairs.

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, because some taxa basal to the [magnoliid + monocot + eudicot] group have been surprisingly little studied, there is considerable variation between families 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 a 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), where on the tree a thicker nucellus and a stylar epidermal layer are acquired has not yet been indicated.

NYMPHAEALES [AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]: vessels + [one position], elements with elongated scalariform perforation plates; 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.

SAPINDALES [HUERTEALES [MALVALES + BRASSICALES]]: flavonols +; vessel elements with simple perforation plates; (cambium storied); petiole bundle(s) annular; inner integument thicker than outer, style +; endosperm scanty.

Chemistry, Morphology, etc. Based on a study of the genome of Arabidopsis, De Bodt et al. (2005, see also Maere et al. 2005) suggest there was a duplication of the whole genome some 109-66 million years before present, although given the uncertainty over the dating of this duplication and relationships within rosids, exactly where the duplication should go on the tree is unclear.

Phylogeny. The only recently established clade Huerteales is strongly supported as being monophyletic (Peng et al 2003: three gene analysis, sampling sketchy; Worberg et al. 2009: all genera included). However, relationships within other malvids are somewhat uncertain, and it remains unclear just what group is sister to Brassicales. The clade [Malvales + Sapindales] is a possible candidate as sister to Brassicales (Soltis et al. 2000; Peng et al 2003: both weak support), and Endress and Matthews (2006) note that there are some features perhaps more common in these first two families than elsewhere. [Malvales + Sapindales] may also be sister to [Brassicales + Tapisciales] (Soltis et al. 2007a: support weak for the latter pair). However, Bausher et al. (2006) in an analysis of whole chloroplast genomes found strong support for the clade [Brassicales + Malvales], but only one species from the three orders, and no Huerteales, were included (see also Jansen et al. 2007; Moore et al. 2007). There was also some support for this topology in analyses by Savolainen et al. (2000) and Hilu et al. (2003); Alford (2006) suggested that [Huerteales (Perrottetia not included) + Brassicales + Malvales] might be sister to Sapindales. Worberg et al. (2007b, 2009) recovered the relationships [Sapindales [Huerteales [Brassicales + Malvales]]], with strong support, and also for the monophyly of each of the four orders. In studies including the mitochondrial matR gene, although the malvid clade was recovered, relationships within it were unclear (Zhu et al. 2007), however, I follow Worberg et al. (2009) here.

SAPINDALES Dumortier  Main Tree, Synapomorphies.

Interesting secondary compounds, ethereal oils, myricetin +; (secretory cells/tissue +); silicified wood or wood with SiO₂ grains in all major families [esp. Anacardiaceae and Burseraceae]; tension wood +; mucilage cells with swollen layered inner periclinal walls [position varies]; branching from previous innovation, petioles leaving a prominent scar; leaves spiral, odd-pinnately compound, conduplicate; A 2x K, (exine distinctly striate); disc well developed; G opposite petals [therefore flowers obdiplostemonous...] or odd member adaxial; ovules few/carpel, epitropous; seed coat?; (embryo green). - 9 families, 460 genera, 5670 species.

Evolution. Wikström et al. (2001: relationships are [Brassicales [Malvales + Sapindales]]]) date the origin of stem Sapindales to (84-)80(-76) million years before present, diversification beginning (71-)67(-63) million years before present. The age of crown group Sapindales was estimated as (66-)63(-60) and (73-)71(-69) million years (two penalized likelihood dates), the stem group age being (102-)96(-90) and (80-)76(-72) million years; Bayesian relaxed clock estimates were only slightly different, to 76 million years for the first analysis and in the upper range of the second analysis (Wang et al. 2009), while Magallón and Castillo (2009) suggested ages of ca 98.1 and 98.4 million years for relaxed and constrained penalized likelihood datings for stem Sapindales, and ages of 70.6 and 70.7 million years (again relaxed and constrained ages) for the crown group.

Sapindales contain ca 3% eudicot diversity (Magallón et al. 1999) and show quite high diversification rates (Magallón & Catillo 2009).

Associated with the accumulation of noxious secondary metabolites in this group, specialised herbivores are found on many of them. Thus the hemipteran Calophya eats largely Anacardiaceae, Burseraceae, Simaroubaceae and Rutaceae (Burckhardt & Basset 2000) - plus a couple of records from entirely unrelated families. Galls are quite common, perhaps especially on Sapindaceae and Anacardiaceae (Mani 1964).

Chemistry, Morphology, etc. Biebersteiniaceae and Nitrariaceae are particularly poorly known morphologically, etc. Gums and resins occur in both the Rutaceae-Meliaceae-Simaroubaceae and Burseraceae-Anacardiaceae groups (Nair 1995). Stratified phloem may be quite widespread (in some Meliaceae, Burseraceae and Simaroubaceae, at least: M. Ogburn, pers. comm.), also Sapindaceae. Teeth, when present, have a clear glandular apex broadening distally and with a foramen and two accessory veins (or one, the other going above the tooth: Hickey & Wolfe 1975). The stipules may clearly be modified leaflets and have been described as pseudostipules or metastipules. The latter have been defined as structures having the morphology of true stipules, yet there was good reason to believe that they were derived from pseudostipules... (Weberling & Leenhouts 1965). The flowers are often imperfect, and staminate and carpellate flowers have well-developed pistillodes and staminodes respectively, so they can be difficult to distinguish. Bachelier and Endress (2009) suggest some floral development features found widely in this clade. Septal cavities have been noticed in Cneorum (Rutaceae) and Koelreuteria (Sapindaceae), but they do not secrete nectar (Caris et al. 2006, cf. septal nectaries in monocots). The style in at least some Rutaceae and Sapindaceae is hollow (Lersten 2004).

For embryology, see Mauritzon (1936).

Phylogeny. For general relationships, see Gadek et al. (1996), while Pell (2004) notes some deletions and insertions that may characterise groupings within the clade. Muellner et al. (2007) present a two-gene tree with quite good sampling; their results suggest the poorly supported basal relationships in the tree here, a fair bit of resolution elsewhere, excepting only a moderately-supported sister group relationship between Meliaceae and Simaroubaceae (cf. Gadek et al. 1996), so a trichotomy including Rutaceae is shown on the tree. Relationships are somewhat different in Wang et al. (2009), but support was weak and sampling poor. Molecular data place Biebersteinia in Sapindales, albeit with a long branch (Bakker et al. 1998).

Previous Relationships. In the past Bretschneideraceae and Akaniaceae have been associated with Sapindales, Bretschneidera in particular looking very like a member of Sapindaceae, even if the presence of myrosin cells in the former was recognised (Cronquist 1981; Takhtajan 1997). Morphological phylogenetic analyses may continue to suggest this position, however, they are to be included in Brassicales as Akaniaceae (e.g. Ronse de Craene & Haston 2006).

Includes Anacardiaceae, Biebersteiniaceae, Burseraceae, Kirkiaceae, Meliaceae, Nitrariaceae, Rutaceae, Sapindaceae, Simaroubaceae.

Synonymy: Acerales Lindley, Aesculales Bromhead, Amyridales J. Presl, Aurantiales Link, Burserales Baskerville, Cedrelales R. Brown, Citrales Dumortier, Cneorales Link, Diosmales J. Presl, Julianales Engler, Leitneriales Engler, Meliales Lindley, Nitrariales Doweld, Pteleales Link, Rutales Perleb, Spondiadales Kunth, Terebinthales Dumortier Zanthoxylales J. Presl - Burseranae Doweld, Rutanae Takhtajan, Sapindanae Doweld - Rutidae Doweld - Aceropsida Endlicher, Aesculopsida Brongniart, Rutopsida Meisner

BIEBERSTEINIACEAE Endlicher   Back to Sapindales

Perennial herbs; vessels?; nodes?; leaves (2-3 compound), odd-pinnate, leaflets lobed, toothed, stipules petiolar, lobed or not; inflorescence racemose; C clawed, nectary glands at base of antisepalous stamens, pollen 3-celled; styles separate, impressed, apically connate, stigma capitate; 1 ovule/carpel, micropyle endostomal; embryo sac tetrasporic, 16-celled [Penaea type] fruit a schizocarp, columella persisting, K ± accrescent; testa ± collapsed, exotegmen thick-walled, lignified, anticlinal walls sinuous, endotegmen lignified, cells polygonal; endosperm development?, embryo somewhat curved, cotyledons foliaceous; n = 5.

1/5. Greece to Central Asia (map: from Heywood 2007; Muellner et al. 2007). [Photos - Collection]

• Biebersteiniaceae are perennial, glandular-hairy herbs that have odd-pinnate leaves with lobed to compound leaflets and petiolar stipules. Ihe inflorescence is erect and racemose and the flowers are large. The fruit has a single seed per carpel and a persistent columella.

Chemistry, Morphology, etc. At least some species are foul-smelling. The petalline stamens are longest; Takhtajan (1997) described the ovules as being unitegmic. The anatomy of Biebersteinia is largely unknown.

The herbaceous habit of Biebersteinia is rather unusual in the order, but ethereal oils (no oxygenated sequiterpenes, high proportion of aliphatic hydrocarbons), single ovule/carpel, etc., are all congruent with a position here. Its exotegmen is rather like that of Ledocarpaceae and Vivianaceae (both Geraniales), especially when young, since both exotesta and endotegmen are tanniniferous (Boesewinkel 1988), but it has distinctive flavones and methyl ethers quite like Rutaceae in part, but unlike Geraniaceae (Bate Smith 1973; Greenham et al. 2001).

Additional information is taken from Baillon (1874), Kunth (1912), Hegnauer (1989, as Geraniaceae: chemistry), Boesewinkel (1997) and Tzakou et al. (2001: fatty acids).

Previous relationships. Previously Biebersteinia has been more or less closely associated with Geraniaceae (Geraniales) (e.g. Cronquist 1981; Takhtajan 1997).

Nitrariaceae [Kirkiaceae [Anacardiaceae + Burseraceae]] [Sapindaceae [Rutaceae + Meliaceae + Simaroubaceae]: stigmatic head from postgenitally united free carpel tips, papillate.

NITRARIACEAE Berchtold & J. Presl   Back to Sapindales

Shrubs; mycorrhizae absent [Peganum]; �-carbalin alkaloids +, ethereal oils?; cork in inner cortex; wood storied; nodes?; mucilage cells +, throughout plant or not; cuticle waxes 0 (platelets, rodlets); leaves two per node, adjacent (spiral), simple or multifid, ?ptyxis, stipules minute or foliaceous, ± cauline; A (10-)15, (antepetalous A in pairs; flower 3-4-merous; A 4, opposite sepals [Tetradiclis]), pollen stephanocolporate; nectaries antepetalous [Nitraria] or extra/intrastaminal disc; G [2-4], style long to rather short, basal [Nitraria, Tetradiclis], stigma as commissural[?] lines down part of its length, dry; 1 apotropous or 6-many ?epitropous ovules/carpel, outer integument 3-4 cells across, inner integument ?2-3 or 4-7 cells across, micropyle zig-zag or bistomal; fruit a capsule, drupe, or berry; exo- and endotesta short palisade, enlarged [cells inflated - Tetradiclis] or not, endotegmen ± fibrous [Peganum] or not [Tetradiclis]; (endosperm copious); n = 7, 12, 30.

3[list]/16. Usu. ± arid regions in N. hemisphere, but little in America, also Australia (map: Pan et al. 1999; Brummitt 2007; FloraBase 2007). [Photo - Flowers]

Chemistry, Morphology, etc. Basically, just about all features need careful examination throughout the group; I do not understand the variation in it. Nitraria often has two or three leaves at a node, although not all these have scarious stipules; the leaves are occasionally toothed or lobed. It also has apotropous ovules (Takhtajan 1997) and aliform-confluent xylem parenchyma.

Peganum also may have two much-divided leaves at a node, in this case also with more or less foliaceous and divided stipules - see also Malacocarpus; it has foliar raphides, but there are only a few mucilaginous cells. The androecium is described as being obdiplostemonous by Eckert (1966); the 15 stamens may be in groups of three opposite the sepals, or there may be paired stamens opposite the petals (Ronse Decraene & Smets 1991a, 1992, 1996a; Ronse Decraene 1992; Ronse Decraene et al. 1996). There are many ovules per carpel and the fruit a loculicidal capsule or berry.

The flowers of Tetradiclis are (3-)4-merous, the stamens equal in number to and opposite the sepals, and there is no nectary. there are usually four carpels, each divided into three parts; of the 6 ovules in each carpel, all borne on end of long placenta arising at base of ovary, four ovules are in a central locellus, and one each in lateral locelli; the style is more or less basal, stigmatic ridges extending down the expanded apical portion; n = 7. The distinctive fruit is a loculicidal capsule, but only the seeds in the central locelli are released when the capsule opens, the other two being retained. Takhtajan (1997) says that stipules there are absent; they are present, if small.

No endothelium has been recorded in members of Nitrariaceae (Kapil & Tiwari 1978), cf. Zygophyllaceae s. str. Batygina et al. (1985) provide details of endosperm development, etc., Danilova (1996), of seed anatomy, and Sheahan and Cutler (1993), of anatomy; for chemistry, see Hegnauer (1973, 1990: as Zygophyllaceae), and for general information, see Hussein et al. (2009).

Phylogeny. Molecular data suggest the relationships [[[Peganum + Malacocarpus] Tetradiclis] Nitraria] (Sheahan & Chase 1996), and place the group in Sapindales.

Previous Relationships. In general appearance, and also in features like wood anatomy, and perhaps also chemistry (Nag et al. 1995), there are similarities betweeen Nitrariaceae and Zygophyllaceae; since both grow in dry and warm habitats, this may account for some of these similarities. Indeed, the two families used to be together in Zygophyllalaceae (Cronquist 1981), although Takhtajan (1997) placed the genera here included in Nitrariaceae as three separate families in his Zygophyllales. Zygophyllales in A.P.G. II (2003) include Zygophyllaceae s. str. and the monogeneric Krameriaceae and are not remotely close to Nitrariaceae.

Synonymy: Peganaceae Doweld, Tetradiclidiaceae Doweld

[Kirkiaceae [Anacardiaceae + Burseraceae]] [Sapindaceae [Rutaceae + Meliaceae + Simaroubaceae]: leaves compound, odd-pinnate, leaflets opposite; pollen 2-nucleate; persistent remnant of floral apex in the center of the gynoecium [?this level]; ovules 2/carpel, epitropous, superposed, micropyle endostomal, inner integument elongated, S- or Z-shaped, nucellar cap +.

Kirkiaceae [Anacardiaceae + Burseraceae]: G adnate to central receptacular apex, synascidiate, stigma with uniseriate multicellular papillae, wet; fruits with 1 seed/carpel.

Chemistry, Morphology, etc. For some general information, see Bachelier and Endress (2008b).

KIRKIACEAE Takhtajan   Back to Sapindales

Tree or shrub; ellagic acid +; nodes?; petiole bundle annular, with medullary bundles; glandular hairs with multiseriate stalk; cuticle waxes 0; stomata ?anomocytic; leaves ± opposite to spiral, leaflets serrate; plants monoecious; inflorescence subdichasial, ultimate branches monochasial; flowers small, 4-merous, K basally connate, decussate, initially valvate, then open, C with adaxial-basal glandular hairs; staminate flowers: stamens = and opposite sepals, pollen syncolpate; disc broad, well developed, pistillode +; carpellate flowers: staminodes +; G [4 (8)], ?orientation, extra "loculus" ± developed, tip of receptacle apex convex, swollen, glandular, styles closely adpressed, erect, finally spreading, stigmas connate, ± punctiform; usu. 1 ovule/carpel, outer integument 2-3 cells across, inner integument 3-4 cells across, micropyle bistomal, long [1/2 length of ovule]; fruit a schizocarp, mericarps pendulous from columella; testa?; endosperm ?type, slight, embryo curved; n = ?

1/8. Tropical and S. Africa, Madagascar (map: from Brummitt & Stannard 2007).

• Kirkiaceae are woody plants that have often rather closely-set odd-pinnate leaves with toothed leaflets. Ihe inflorescence is dichasial, although the ultimate branches may be monochasial, and the flowers are small and 4-merous. The fruit is a ridged or angled schizocarp with persistent if slender columella strands.

Chemistry, Morphology, etc. The wood of Pleiokirkia is reported to smell like honey (Schatz 2001). The lower order branches have female flowers, higher order branches male (Bachelier & Endress 2008b). For some information on anatomy, see Jadin (1901) and on chemistry, see Nooteboom (1967); for the floral morphology of Kirkia, see Bachelier & Endress (2008a, esp. b).

Previous Relationships. Kirkiaceae were previously placed in (Cronquist 1983, but with some doubt) or near (Takhtajan 1997) Simaroubaceae, but they lack quassinoids and limonoids.

Anacardiaceae + Burseraceae: biflavonoids [alone in order]; (vessel elements with scalariform or reticulate perforations); vertical intercellular secretory canals in phloem, this surrounded by a light-coloured, sinuous, sclerenchymatous band [not easy to see]; glandular hairs wuith uniseriate stalk; cuticle waxes usu. 0; (plants dioecious); flowers rather small, K often connate, C little longer than K; palynologically indistinguishable; (disc extrastaminal); central receptacular apex ± exposed in the center of the flower; ovule pachychalazal; fruit an (operculate) drupe, endocarp cells in a mass, lignified, not oriented.

Evolution. Fossils assignable to Burseraceae/Anacardiaceae are known from the early Eocene in England ca 50 milliion years ago (Collinson & Cleal 2001).

Chemistry, Morphology, etc. Note that Anacardiaceae like Pachycormus have thin, brown, flaking bark and vegetatively look quite like Burseraceae... Bachelier and Endress (2009) discuss the floral morphology and anatomy of this clade in detail. The basic endocarp condition for [Anacardiaceae + Burseraceae] seems to be that of an unoriented mass of sclerified and often crystalliferous cells (Wannan & Quinn 1990). Such an endocarp characterises Spondiadoideae, and it is also found in Burseraceae as well as in Buchanania, Campnosperma and Pentaspadon, included in Anarcardioideae, as by Pell (2004: unfortunately, Campnosperma was not sequenced). Indeed, Buchanania is possibly sister to remaining Anacardioideae (Aguilar-Ortigosa & Sosa 2004), appropriate, given its endocarp anatomy. It has been suggested that an operculum may be derived twice in Anacardiaceae (Pell & Urbatsch 2001), but it is also found in fruits of Burseraceae and perhaps it, too, is plesiomorphic within the whole clade.

For chemistry, see Hegnauer (1964, 1989), for general developmental information, see Bachelier and Endress (2007a, especially 2008a, b).

ANACARDIACEAE R. Brown, nom. cons.   Back to Sapindales

Trees or shrubs (climbers); exudate black or becoming blackish; (cork cortical); pith loose, shining; vertical resin ducts +; wood often fluorescing; nodes usu. 3:3; petiole with annular wing bundles; leaflets not articulated, margins toothed or not, base of petiole often swollen; inflorescence cymose, flowers (3-)5(-7)-merous; (K, C 0); A (1-10<), when 5, opposite sepals, (stamens on disc; disc 0); (andro/gynophore +); styles separate (single), terminal to gynobasic, stigma capitate (lobed), dry; 1 ovule/carpel, usu. apotropous, ± anatropous, (perichalazal), uni- or bitegmic, micropyle zig-zag (endostomal), funicle often long, ponticulus +; chalazogamy +; seed often ± pachychalazal, (exotestal cells [and hypodermis] thickened), endotegmen usu. ± thickened, lignified; endosperm oily (and starchy), embryo often curved (cotyledons folded - Mangifera); n = 7-12, 14-16, 21.

70[list]/600. Tropical, also temperate (map: from Heywood 1976; George 1985; Meusel et al. 1978). Two groups below. [Photo - Flower, Fleshy fruit, Dry fruits.]

1. Spondiadoideae Link

Biflavonoids; also alkylcathechols and alkylresorcinols 0; A obdiplostemonous; G [(1-[pseudomonomerous?])4-5(-12)] and as many locules; ovule pendulous, (2/ovules carpel, one epitropous); exocarp thick.

10/115. Tropical.

Synonymy: Spondiadaceae Martynov

2. Anacardioideae Link

(Biflavonoids, 5-deoxyflavonoids, also alkylcathechols and alkylresorcinols [phenols with unsaturated side chains - allergenic] +); leaves simple (compound); A variable; G 1 [pseudomonomerous?], [3(-6, partly syncarpous, Buchanania)], antesepalous carpel alone fertile, symplicate zone?, (styles connate); ovule apical to basal, (unitegmic, funicle massive, with outgrowths - Pistacia, etc.); drupe often asymmetrical, ± flattened, (K much accrescent); exocarp thin, epidermis lignified, endocarp with up to three layers of palisade lignified sclereids, internal to these a crystalliferous layer [= stratified].

60/485: Semecarpus (60). Largely tropical, also temperate.

Synonymy: Blepharocaryaceae Airy Shaw, Comocladiaceae Martynov, Julianaceae Hemsley, Lentiscaceae Horaninow, Pistaciaceae Adanson, Podoaceae Franchet, Schinaceae Rafinesque, Vernicaceae Link

• Anacardiaceae may be fairly readily recognised because of their often black and/or rather resinous-smelling exudate; the leaves often have black discolorations and the blade may dry a distinctive grey colour. In herbarium specimens, the dry, black exudate may entirely cover the cut surface of the twig, or it may form a distinctive black ring around the periphery. The leaves are often odd-pinnate and the leaflets are opposite to alternate. The flowers are small, and the fruits are often flattened drupes with excentric style or styles.

Evolution. For the early Tertiary fossil history of what are now East Asian endemic Anacardiaceae, see Manchester et al. (2009) - Choerospondias has been found in Lower Eocene deposits of the London Clay. Middle Eocene deposits from Germany include fossils of the distinctive fruits of the New World Anacardium, with their much-swollen pedicels; the African Fegimanra, sister to Anacardium, also has swollen pedicels, although they are clearly different (Manchester et al. 2007b).

Anacardiaceae are noted for the sometimes extremely violent allergenic reactions their exudates cause; catechols, resorcinols and other types of phenolic compounds, often in a mixture, as in urushiol, are involved. About a quarter of the genera - all Anacardioideae - have such compounds.

Aphids (Fordinae) that form distinctive galls are closely associated with species of Pistacia (Inbar 2009), while a gall-forming jumping plant louse, the hemipteran Calophya, is notably common on Schinus, and other psyllids occur on Anacardiaceae (Burckhardt & Basset 2000; Burckhardt 2005).

There is a variety of winged fruit types in Anacardioideae. These include fruits adnate to broad bracts (Dobinea), samaras (Loxopterygium), a wing formed by the flattened peduncle of the inflorescence (Amphipterygium), much enlarged sepals (Parishia), and even much enlaged petals (Swintonia); the evolution of these fruit types seems to be correlated with the adoption of a drier habitat (Pell & Mitchell 2007). Other structures may be part of the dispersal unit, including a fleshy swollen pedicel, as in Anacardium, while in Cotinus hairs on the pedicels are involved in the wind dispersal of the fruits.

In Pistacia, and perhaps other genera, chalazogamy occurs, the pollen tube moving from the funicle via the ponticulus, an outgrowth of the funicle that bridges the gap between it and the chalaza (Martínez-Pallé & Herrero 1995; Bachelier & Endress 2009).

Chemistry, Morphology, etc. Branching in Anacardium may occur on the current flush. Wind-pollinated taxa often lack a disc, also petals. Mangifera has one or two stamens borne inside the disc. In Anacardium the single stamen is on an oblique plane of symmetry; more generally, the position of the carpel, when single, suggests that the flower has oblique symmetry. In Anacardioideae the floral/receptacle apex is sometimes quite short (Bachelier & Endress 2009). Pistacia and Amphipterygium (see Julianaceae below) both are wind pollinated, dioecious, and with reduced flowers. Their ovules are distinctive, being unitegmic and with a massive funicle, etc. (Bachelier & Endress 2007b).

For general information, see Ding Hou (1978), for fruit anatomy, Wannan and Quinn (1990), for floral morphology, Wannan and Quinn (1991), for general chemistry, Young (1976), for chemistry of Julianaceae, see Hegnauer (1966, 1989), for seed anatomy, see von Teichman (1991, 1994, and references), and for wood anatomy, see Gupta and Agarwal (2008). Pell (2004) covers the morphology of the whole family in a phylogenetic context, which she provides; Mitchell et al. (2006) focus more on Spondiadoideae.

Phylogeny. Spondiadeae and some Rhoeeae - the clade includes Pegia, Tapirira and Cyrtocarpa = Spondiadoideae (see Aguilar-Ortigosa & Sosa 2004 and Pell 2004, the latter with a list of included genera) - are sister to the rest of the family, Anacardioideae (Pell & Urbatsch 2000, 2001; Pell 2004 and Mitchell et al. 2006 for a list of genera, but see below); wind-dispersed taxa in this latter subfamily do not form a single group (Pell & Mitchell 2007, c.f. Pell & Urbatsch 2001). Buchanania in some analyses is quite well supported as sister to Anacardioideae (Aguilar-Ortigosa & Sosa 2004; Wannan 2006), consistent both with its chemistry, endocarp anatomy (see above), carpel number of 4-6, and different position of the fertile carpel, but its position is not fixed in others (Pell & Mitchell 2007, cf. abstract). Note that Campnosperma, so far included in only one study (Chayamarit 1997, sampling limited, relationships suggested are unlike those in other studies, no support values), has an endocarp similar to that of Buchanania and the fruit is sometimes two-locular. The morphology of neither of these genera is accounted for in the Anacardioideae as characterized here; if they are, the subfamily will probably lack much in the way of apomorphies.

For the limits of Rhus, which seem best narrowly drawn (i.e., restricted to ca 35 species in the genus), see Yi et al. (2006, and references).

Classification. A number of anacardiaceous genera have highly reduced flowers and inflorescences, and in the past they have been segregated in separate families. These include Blepharocaryaceae, with their compact, involucrate inflorescences, Julianaceae, dioecious, the staminate flowers with extrorse anthers and carpellate flowers that lack a perianth but are surrounded by an involucre, and finally Podoaceae, with opposite leaves and carpellate flowers that also lack a perianth.

BURSERACEAE Kunth, nom. cons.   Back to Sapindales

Trees or shrubs; bark often flaky, light grey; colorless to white resinous exudate common; tannins?; (pith cells heterogeneous); nodes usu. 5:5; secretory canals rare; sclereids in stem; snail glands [curled ± uniseriate glandular hairs] common; leaflets (with pellucid dots), ?ptyxis, margins often toothed, petiolules and petioles often pulvinate, stipules petiolar or cauline, laciniate to entire, or 0; flowers 3-5(-7)-merous; (hypanthium +), K induplicate-valvate, C induplicate-valvate; ventral carpel bundles fused bundles of adjacent placentae, style usu. short; ovules campylotropous, (integument 1), outer and inner integuments ca 4 cells across, nucellar cap quite massive, nucellus 6-12 cells across; (fruit septifragal), drupe often angled, stone with valves, K deciduous; (exotesta with shortly radially elongate but unthickened cells), endotesta lignified, ± tracheidal; embryo reserves hemicellulosic.

18[list]/550. Tropical. Two groups below.[Photo - Leaf, Flower, Fruit.]

1. Beiselieae Thulin, Beier & Razafimandimbison

(Vessel elements with scalariform perforation plates); leaf ?bases persistent, with a spine; K, C valvate; G [9-12], symplicate zone short, ovary strongly furrowed; pericarp splitting septifragally separately from the endocarp, columella with deep flanges, mericarps apically winged; n = ?

1/1: Beiselia mexicana. Mexico.

2. Bursereae DC, Garugeae Marchand, Protieae Marchand

(Cork cambium deeper - Santiria); petiole bundle often with medullary strands; (stamens = and opposite sepals; pollen psilate, striate); G [(2-)3-5], symplicate zone well developed, ovules collateral, receptacle enclosed bin the gynoecium; (pseudoaril [pericarpial in origin] +; mesocarp quite frequently splits down loculicidal radius; fruit with columella (pyrenes winged; often only one loculus developing); vascular bundle in outer integument; cotyledons folded, palmately lobed; n = (11-)13, 23.

17/550: Commiphora (190, 150 from Africa), Protium (85), Canarium (75), Bursera (50-100). Tropical, but esp. America and N.E. Africa (map: from Rzedowski 1978; D. C. Daly, pers. comm.).

• Burseraceae are recognisable by their often scented resinous exudate and smooth, flaking bark; compound, odd-pinnate leaves with opposite, often long-petiolulate and more or less pulvinate leaflets that have prominent fine venation especially when dry; and petioles, petiolules and rachis that tend to be brownish and more or less scurfy. The swollen leaf base is often concave adaxially. The calyx is often connate and 3- or 4-lobed, and the angled drupes have a wrinkled surface when dry. The resinous exudate often smells of almonds (myrrh, frankincense), and in some genera the leaflets are strikingly symmetrical.

Evolution. The split between Bursera and Commiphora has been dated to some 120 million years before present, with diversification within the former genus starting some 70 million years before present (Becerra 2005); these dates seem something of an overestimate. Weeks and Simpson (2007) suggest that divergence of Commiphora from the clade now represented by the E. Asian B. tonkinensis occured some 53-41.6 million years before present (Eocene). Commiphora itself did not diversify until 32.3-23.2 million years before present, Neogene aridification of Africa occuring more or less at that time (Weeks & Simpson 2007), while Bursera, of which some 85% of the species - often quite narrowly distributed - are found in dry, tropical, Mexican forests - diversified within about the last 25 million years (Becerra et al 2009: see Weeks et al. 2005 and Weeks & Simpson 2007 for further details on the complex biogeography of the family).

For possible coadaptive relationships between Burseraceae, especially Bursera itself, and herbivorous chrysomelid beetles (Blepharida) and how the latter deal with the toxic terpene-containing resins the plants contain, see Becerra (1997, 2003 and references) and Becerra et al. (2001: particularly interesting). Species with a squirt defence - toxic material is under pressure and when tissues are perforated it is ejected to a diastance of up to 2 m - have rather a rather simple terpenoid defence (Becerra et al. 2009). Locally, species of Bursera tend to be chemically more dissimilar than would be expected at random (Becerra 2007). Overall chemical diversity in Bursera has increased with time/speciation, if dropping off when considered from a per speciation point of view as variation seems to become permutational, terpene diversification occuring in the local ecological context (Becerra et al. 2009).

Chemistry, Morphology, etc. Some Burseraceae have foliaceous stipules; these are usually interpreted as being the reduced basal pair of leaflets of the compound leaf. A few genera (e.g. Garuga) have a well-developed hypanthium; the disc is rarely extrastaminal (Triomma). Odd carpel is abaxial in 4-merous Amyris (Schnizlein 1843-1870, fam. 244).

For general information, see Lam (1931, 1932), Leenhouts (1956), and Forman et al. (1989: esp. Beiselia), and for pollen morphology, see Harley and Daly (1995: Protieae) and Harley et al. (2005: considerable variation).

Phylogeny. Beiselia (B. mexicana is the only species) has simple cotyledons; molecular studies suggest that it is sister to the rest of the family (e.g. Clarkson 2002). This has considerable implications for character evolution, including cotyledon morphology; Beiselia also has several probably autapomorphic features like its gynoecium with its 9-12 carpels. Commiphora may be embedded in Bursera, but the support is weak (Weeks et al. 2005). A recent study suggested that the clades, Protieae, Bursereae, and Garugeae (the latter including Canarium, etc.) had strong support individually and also as sister to Beiselia, but relationships between the first three tribes were unclear (Thulin et al. 2008).

Synonymy: Balsameaceae Dumortier, Neomangenotioideae Leroy

Sapindaceae [Rutaceae + Meliaceae + Simaroubaceae] (if a clade): anthers with a pseudo-pit; tapetal cells multinucleate; hypostase +.

SAPINDACEAE Jussieu, nom. cons.   Back to Sapindales

Woody; quebrachitol [cyclitol], toxic saponins, cyclopropane [non-protein] amino acids +, ellagic acid 0 (+); cork also outer cortex (pericyclic - Dodonaea); latex of sorts not uncommon; (vessel elements with scalariform perforation plates; petiole bundle with cortical or adaxial bundles); cuticle waxes 0 (platelets, rodlets); leaves spiral, leaflets articulated [check basal pectinations], ptyxis also conduplicate-plicate, margins serrate, colleters common; inflorescence paniculate, the flowers often in clusters, imperfect; pedicels articulated; flowers 4-5-merous, [K5 C4; K4 C4; etc], C (0, 5+), often clawed, hairy, and with various ± complex appendages, nectary disc outside A; A (4-[Glenniea])8(-16), often hairy; G [(2) 3(-6)],(style hollow; style branches +), stigma strongly 3-lobed or not, dry or wet; ovules variously curved, sessile, often apotropous, (micropyle bistomal), outer integument thicker than the inner integument, funicular obturator +; fruit a capsule, or a schizocarp with 1-seeded samaras; seed often pachychalazal, chalazal/integumentary arils and sarcotesta common; testa (and tegmen) multiplicative, testa vascularised, exotesta palisade (not), unlignified, tegmen limited to radicular pocket, (mesotestal cell walls thickened and lignified; endotesta crystaliferous, exotegmen fibrous, lignified or not); endosperm 0, starchy, embryo curved, the radicle in a pocket of the testa, cotyledons spiral or not; n = esp. 10-12 [climbers] and 14-16 [non-climbers]; germination hypogeal or epigeal.

135[list]/1580: - four subfamilies below. ± World-wide. (map: from Herzog 1936; Meusel et al. 1978; George 1985). [Photo - Flower, Fruit, Fruit.]

1. Xanthoceroideae Thorne & Reveal

Phloem stratified; stomata anomocytic; leaves deciduous; flowers large; disc with golden, horn-like glands; pollen spiny; 6-8 ovules/carpel, outer integument 7-8 cells across, inner integument 4-5 cells across; aril 0; mesotestal cell walls thickened, tegmen multiplicative, with inner layers thick-walled.

1/1: Xanthoceras sorbifolia. N. China.

Synonymy: Xanthoceraceae Buerki, Callmander & Lowry

Hippocastanoideae [Dodonaeoideae + Sapindoideae]: flowers often strongly obliquely or vertically [Aesculus] monosymmetric, ovules apotropous, (archesporium multicellular).

2. Hippocastanoideae Burnett

Cuticle wax crystalloids quite common [Acer]; stomata actinocytic (anomocytic); leaves opposite, palmate (odd pinnate; simple), deciduous; (flowers large - Aesculus; polysymmetric); (nectary inside A - Acer); outer integument 3-5 [Acer or 8-10 cells across, inner integument 3-6 cells across, hypostase 0 - Handeliodendron), stigma dry; (fruit a samara); (aril +); n = 20.

5/130: Acer (110). North temperate, some tropical and usually montane.

Synonymy: Aceraceae Jussieu, Aesculaceae Berchtold & J. Presl, Hippocastanaceae A. Richard, Paviaceae Horaninow

Dodonaeoideae + Sapindoideae: leaves usu. spiral, even-pinnate, (bicompound; simple), leaflets opposite or not, (entire; rachis winged; petiolar stipules +); (seeds with physical dormancy, water gap near hilum).

3. Dodonaeoideae Burnett

Cork pericyclic; stomata cyclocytic [both Dodonaea]; (1 pendulous epitropous ovule/carpel), outer integument 8-10 cells across, inner integument 3-4 cells across.

16/135: Dodonaea (70). Pantropical-warm temperate, esp. Australia/Southeast Asia.

Synonymy: Dodonaeaceae Link

4. Sapindoideae Burnett

(Lianes with branch tendrils; secondary thickening anomalous;) stomata various; (pollen oblate, triporate - Serjania, etc.); often 1 ovule/carpel, outer integument 4-12 cells across, inner integument 2-6 cells across; chromosomes 0.62-4.36 µm long.

111/1185: Serjania (215), Paullinia (195), Guioa (65), Cupaniopsis (60). Pantropical.

Synonymy: Allophylaceae Martynov, Koelreuteriaceae J. Agardh, Ornithrophaceae Martynov

• Sapindaceae are recognisable by their often spiral, pinnately-compound leaves that often have subopposite leaflets and a terminal rhachis tip, although many taxa have ternately/palmately-compound leaves. The base of the petiole is quite strongly swollen and the stem is ridged. The leaflets may be coarsely serrate and the fine venation is often prominent when dry. The inflorescences are paniculate, and the flowers are often borne in congested groups along the axis. The flowers are often rather small and are conspicuously hairy inside; there are usually eight stamens and complex folds or scales on the petals. The fruits have only one or two seeds per carpel and are often deeply lobed, or a single carpel only may develop, the other one or two carpels persisting at the base; samaras of various types are common. The radicular pocket in the testa is distinctive.

Evolution. Cupaniopsis-type pollen is widespread in the fossil record, including several sites in Africa, although Sapindaceae with such pollen are no longer found there (Coetzee & Muller 1984). Fossils ascribable to Sapindaceae are known from the later Cretaceous, while Wehrwolfea, with striate pollen and a floral formula of K 4 C 4 A 10(?+) G 3-4, is known from the middle Eocene of western Canada (Erwin & Stockey 1990). The split between Acer and Dipteronia has been dated to (98-)78(-63.5) million years ago (Renner et al. 2007b). For the early Tertiary fossil history of what are now East Asian endemics, see Manchester et al. (2009). The very widespread Dodonaea viscosa has spread and diversified within the last two million years (Harrington & Gadek 2009).

The largely neotropical Paullineae (Sapindoideae), with 8 genera including Serjania and Paullinia, contain one third of the species in the family. Many are vines and have trunks with several vascular cylinders that soon become independent of one another (Tamaio & Angyalossy 2009). Sapindaceae, along with Bignoniaceae, are the major components of the viny vegetation of the Neotropics.

Species of Acer like A. rubrum are known for having very labile breeding systems; see Renner et al. (2007b) for a study of breeding systems in the genus, with dioecy evolving several times.

Chemistry, Morphology, etc. Aesculus has bud scales, Billia has naked buds, but both branch from previous flush. Radlkofer (1892-1900) shows Serjania as having strongly obliquely symmetrical flowers, with the odd gynoecial member abaxial on the plane of symmetry. The abaxial corolla member is absent, but the stamens are abaxial, the two adaxial(?)-lateral members being missing. In Acer, the samaras are oblique (Schnizlein 1843-1870). Ronse de Craene (2010) depicts gynoecial orientation as varying within an inflorescence in Acer. The petals of Sapindaceae are often rather complex, and have a similarly complex set of terms used to describe them. Brizicky (1963) reports that the ovules may be epitropous, while those of Koelreuteria and other taxa are both epitropous (the lower ovule) and apotropous (the upper ovule) in the same loculus (Mauritzon 1936; Danilova 1996). Corner (1976) noted that the outer integument of Nephelium lappaceum was slightly thinner than the inner integumnent, amd he recorded a definite funicle from Aesculus, at least after fertilization. The fruit looks like a follicle when only one carpel develops; dehiscence is, however, down the abaxial side. In many Sapindaceae (and some Anacardiaceae) the pericarp grows much faster than the seed, so what seem to be almost mature fruits can contain seeds that are still very small. It has been suggested that the base chromosome number for Sapindaceae is x = 7 (Ferrucci 1989).

For an early but still useful account of the family, see Radlkofer (1933, 1934), for seeds, see van der Pijl (1955) and Turner et al. (2009: germination), for chemistry, see Hegnauer (1964, 1966, 1973, 1989, 1990, also under Aceraceae and Hippocastanaceae), for pollen, see Muller and Leenhouts (1976), for wood anatomy, see Klaassen (1999) and Agarwal et al. (2005), for embryology, Tobe and Peng (1990), for chromosome numbers, Lombello and Forni-Martens (1998), for chromosome size, see Ferrucci (1989), for floral morphology of Koelreuteria, see Ronse Decraene et al. (2000b), of Handeliodendron, see Cao et al. (2008), and of Acer, etc., see Leins and Erbar (2010), for fruits of Paullineae, see Weckerle and Rutishauser (2005), for epidermal features, see Cao and Xia (2008), and for nectaries, which may have three vascular traces, see Solis and Ferucci (2009).

Phylogeny. Preliminary studies suggested that Xanthoceras, with simply 5-merous, polysymmetric flowers, ovules arrranged in parallel (see also Magonia), and complex, golden nectaries borne outside the eight stamens, might be sister to all other Sapindaceae, and that the genera included in the erstwhile Aceraceae and Hippocastanaceae formed monophyletic sister taxa, the combined clade being sister to the remainder of the family (see Klaassen 1999; Savolainen et al. 2000a; Soltis et al. 2007a). Recent two-gene studies (Harrington et al. 2005, 2009 - the latter incorporating information about secondary structure of the ribosomal DNA examined, extensive sampling in Dodonaeoideae but not including any Sapindoideae) have largely confirmed these results. Harrington et al. (2005) found that Xanthoceras was not sister to the rest of the family in single gene analyses, being somewhat embedded, but without strong support; it was only in the joint analysis that is was sister to all other Sapindaceae (70% bootstrap, ³95% posterior probability: see also Buerki et al. 2010a, 2010b, support for the position still very low). Early morphological analyses (Judd et al. 1994) suggested a rather different set of relationships. For extensive studies of the family - 81 and 104 genera respectively - see Buerki et al. (2009, 2010b); the limits of some tribes need re-evaluating. For the phylogeny of Acer, see Li et al. (2006) and Renner et al. (2007b).

Classification. The phenetically distinctive Aceraceae and Hippocastanaceae are here included in Sapindaceae, with which they have much in common; Buerki et al. (2010b) prefer to recognize them (and Xanthoceraceae) as families. For subfamilies, see Buerki et al. (2009). There is extensive polyphyly of the classicaly-recognized tribes (Buerki et al. 2010b).

Previous Relationships. Sapindaceae are chemically similar in some respects to Fabaceae (e.g. both have non-protein amino acids: for a summary of these, see Fowden et al. 1979), and both have compound leaves, but they are unlikely to be immediately related.

Rutaceae + Meliaceae + Simaroubaceae: alkaloids, limonoids/protolimonoids, pentanortriterpenes +; cuticle waxes 0; (leaves trifoliate, simple); inflorescence branches cymose.

Chemistry, Morphology, etc. The triterpenoid limonoids (see Rutaceae), meliacins (Meliaceae), cneorids (Rutaceae), and quassinoids (Simaroubaceae) are biosynthetically related (e.g. Connolly et al. 1970; Evans & Taylor 1983) and often have a bitter taste. For details of the distribution of limonoids and protolimonoids, see Yin et al. (2009), and for trans-octadecanoic acids in seed oils, see Stuhlfauth et al. (1985). Rutaceae and Simaroubaceae are reported to have embryo sac haustoria (Mickesell 1990). For some information on carpel development, see van Heel (1983).

Rutaceae + Meliaceae: tetranortriterpenes, flavones +; stigma capitate.

RUTACEAE Jussieu, nom. cons.   Back to Sapindales

Herbs to trees; furanocoumarins +; (vessel elements with scalariform perforation plates); wood often fluorescing; (nodes 1:1; cuticle waxes platelets, rodlets, etc.); stomata various; leaves spiral to opposite, (rhachis winged), leaflets (subopposite), usu. articulated, ptyxis also flat, margins entire to crenate (serrate), punctate because of schizogenous cavities, (stipules intrapetiolar - Metrodora); breeding system various; flowers (vertically or obliquely monosymmetric), (3-)5-merous; K (2-4), connate or free, C (0-4), often valvate?, (connate); (androgynophore +); A (2-many in a single whorl), obdiplostemonous, filaments ± flattened (connate); (gynophore +); G (1 [2-)5(-many)], variously connate to almost free, (opposite sepals - Zanthoxylum), style impressed to ± gynobasic, (connate only at apex; styluli [marginal] +), (stylar canals as many as carpels), stigma (lobed), dry or wet; ovules 1-many/carpel, (apical), micropyle also zig-zag; fruit a loculicidal and part septicidal capsule, often strongly lobed, or follicle, mesocarp and endocarp separating, or berry (drupe); exotesta often mucilaginous, irregularly palisade, or lignified and fibrous (mesotesta sclerotic), exo-(and meso- and endo-) tegmen tracheidal; (endosperm +), (embryo curved); n = (7-)9(-11+).

161[list]/1815: Zanthoxylum (250), Melicope (150). Largely tropical (map: from Meusel et al. 1978; Brummitt 2007).

1. Spathelioideae

Pyranochromones, (diterpenoid cneorubin X; quassinoids) +; (no oil cavities, but leaves with solitary oil cells); petiole bundle more or less cylindrical, of two opposed plates (arcuate - Bottegoa); stomata anomocytic to cyclocytic; (leaves simple; bicompound; stipules and stipular thorns); C valvate; A (4-5); pollen reticulate; ovules 1-2(-3)/carpel, apotropous or epitropous, campylotropous, micropyle endostomal, outer integument ca 2 cells across, inner integument ca 3 cells across, parietal tissue ca 5 cells across; fruit a loculicidal capsule, carpels opening adaxially and separating from columella; carpels separating in fruit; fruit a winged drupe; (testa multiplicative, exotestal cells large, outer walls thickened, exotegmen tracheidal - Harrisonia).

7/35: Spathelia (20). Tropical America and Africa, Madagascar, the Mediterranean.

Synonymy: Cneoraceae Vest, Ptaeroxylaceae J.-F. Leroy, Spatheliaceae J. Agardh

The rest: outer integument 3-6 cells across, inner integument 2-5(-6) cells across,

2. Rutoideae

3. Aurantioideae

G postgenitially united; (pulp of berrry of multicellular hairs).

[Photo - Flower, Flower, Fruit.]

Synonymy: Amyridaceae Kunth, Aurantiaceae Durande, Boroniaceae J. Agardh, Citraceae Roussel, Dictamnaceae Vest, Diosmaceae R. Brown, Diplolaenaceae J. Agardh, Flindersiaceae Airy Shaw, Fraxinellaceae Nees & Martius, Jamboliferaceae Martynov, Pilocarpaceae J. Agardh, Pteleaceae Kunth, Zanthoxylaceae Berchtold & J. Presl

• Rutaceae are recognisable because of their often opposite, compound and punctate leaves; their cymose inflorescences; their flowers, with the stamens often arranged in a ring, thick filaments, conspicuous disc at the base of the ovary, and expanded stigma, are quite distinctive. Although the fruits are variable, many have a glandular-punctate pericarp, while others are dry, deeply lobed, and dehisce to reveal the black and shiny seeds.

Evolution. For dates of diversification within Rutaceae, especially Aurantioideae, see Pfeil and Crisp (2008; cf. in part Muellner et al. 2007); the family is relatively young, and distributions are unlikely to be much affected by continental drift events. For the early Tertiary fossil history of what are now East Asian endemics, see Manchester et al. (2009).

Rutaceae have very diverse secondary metabolites, some of which (essential oils, coumarins, etc.) are similar to those in Apiaceae (Hegnauer 1971), while their alkaloids are like those found in some magnoliids - and are produced via nine or more different biosynthetic pathways. Caterpillers of Papilionidae-Papilioninae butterflies are notably common on Rutaceae, indeed, ca 1/3 of the records are from this family, and 80% of the ca 550 species of Papilio are found here (Zakharov et al. 2004). Like the magnoliids, on which closely related Papilioninae are also found, it is the alkaloids that attract the butterflies. It is possible that Rutaceae were the original food plants for Papilio, since even those caterpillars which now eat Magnoliales will eat Rutaceae if they have to.

Ca 250 species of Diosmeae are restricted to South Africa, largely to the Cape Floristic Region (Trinder-Smith et al. 2007).

Chemistry, Morphology, etc. Rutaceae as circumscribed here are a variable group. They are very diverse in their secondary metabolites, some of which (essential oils, coumarins, etc.) are similar to those in Apiaceae (Hegnauer 1971), while the alkaloids are like those found in some magnoliids and are produced via nine or more different biosynthetic pathways. Rutaceae and associated "families" once segregated from them all have pyranochromones. Da Silva et al. (1988) surveyed these secondary metabolites, suggesting that an overhaul of the infrafamilial classification was in order. Adsersen et al. (2007) note the value of prenylated acetophenones as a marker for Xanthoxyleae (inc. Melicope, etc.).

Rutaceae are also rather variable in flower and fruit, if less so vegetatively. Prickles of Zanthoxylum can be in the stipular position. Monosymmetry is scattered in the family, occuring in Dictamnus and Erythrochiton, for example. Kallunki (1992) illustrates the flowers of Erythrochiton fallax as having the median sepal adaxial, but their exact orientation, and how they are actually held, is unclear since the inflorescence can be pendulous and up to 1.5 m long. The flowers of Galipeinae, to which Erythrochiton belongs, may have only two stamens plus staminodes, a connate corolla, filaments connate and forming a tube, or a corolla that is connate only because of the adnation of the filaments (Pirani & Menezes 2007). Peltostigma has a floral formula K3 C3 A9 G [?5], and looks almost lauraceous; Pilocarpus has an erect raceme and the calyx is reduced to a rim. Carpel (stylar) fusion may be postgenital (Gut 1966). Ovules of Glycosmis are unitegmic, and both apotropous and epitropous ovules are recorded from the family. In bitegmic taxa, either integument may be slightly thicker than the other (Corner 1976). Nucellar polyembryony is widespread. Triphasia has G [3], with the odd member adaxial, and the same is true of Cneorum tricoccon, which has 3-merous flowers (see Caris et al. 2006 for floral development). �

For gynoecial morphology in particular, see Gut (1966), for general information, see van der Ham et al. (1995) and White and Styles (1966), for general chemistry, see Hegnauer (1973, 1990, also 1964, 1989 as Cneoraceae), Waterman and Grundon (1983), and Mulholland et al. (2000, "Ptaeroxylaceae" in particular), for alkaloid chemistry, see Waterman (1975, 1999), for floral development of Cneorum, Caris et al. (2006b), dor ovules of Harrisonia, see Wiger (1935), for a review of relationships, Araújo et al. (2003), for floral morphology, see Zhou et al. (2002), and for floral orientation, see Eichler (1878). See also Dahlgren and van Wyk (1988), van der Ham et al. (1995) and White and Styles (1966) for information about Kirkia.

Phylogeny. General relationships in a two-gene analysis: most of Rutaceae sister to [[Spathelia + Dictyoloma] [[Cneorum + Ptaeroxylum] Harrisonia]], both genus pairs with good support, but the position of Harrisonia, with sequences from only a single gene, was less clear (Chase et al. 1999; see also Groppo et al. 2008). Spathelia (chromones) and Dictyoloma (C valvate) are a strong pair; secretory cavities are reported from them (Groppo et al. 2008). Jadin (1901) had noted that anatomically Harrisonia was rather different from other Simaroubaceae in its heterogeneous pith and its lack of medullary secretory canals. Although it does not seem to have pellucid foliar gland dots, Fernando and Quinn (1992) found secretory cavities in the fruits and Fernando et al. (1995) suggested that its removal from Simaroubaceae was justified on both molecular and morphological grounds. Although these few genera form a fairly distinct group, inclusion within Rutaceae seems reasonable (Groppo et al. 2008). Razafimandimbison et al. (2010) found a small group of genera including those mentioned above that formed a weakly/moderately supported clade ([Spathelia + Dictyoloma] are sister to the rest) that included the old Ptaeroxylaceae; it is morphologically quite heterogeneous, like the rest of the family, and is recognised as Spathelioideae above.

Some of the fruit characters used to distinguish the classic subfamilies in Rutaceae are proving unreliable in delimiting major clades (e.g. Hartley 1981; But et al. 2009). However, within core Rutaceae, [Aurantioideae (distinctive fruit with fleshy hairs in the loculi; fibrous exotegmen; endosperm 0; x = 9) [Chloroxylon + Ruta]] do form a poorly to well-supported group (e.g. Groppo et al. 2008). Aurantioideae are monophyletic (e.g. see also Morton et al. 2003). For relationships within Aurantioideae, see Pfeil and Crisp (2008) and Bayer et al. (2009); Clauseneae may not be monophyletic (Morton 2009). For subtribal relationships, see Morton (2009), and forrelationships around Citrus, see Scott et al. (2000), Samuel et al. (2001) and Bayer et al. (2009). Salvo et al. (2008) found that Dictamnus is widely separate from the other members of Ruteae, linking with Casimoroa and Skimmia (Groppo et al. 2008). Most other Rutoideae are immediately unrelated, perhaps forming a clade sister to Dictamnus et al. (see Poon et al. 2007; Groppo et al. 2008), and subfamilies other than Aurantioideae are interspersed in this group, within which relationships are uncertain. Zanthoxylum may be sister to the rest (see also Muellner et al. 2007); it is certainly part of a well-supported clade with distinctive isoquinoline alkaloids that may be sister to Ptelea. Flindersia and relatives have secretory cells in the stem only and their capsule is septifragal, perhaps reminiscent of Meliaceae, but their furoquinoline alkaloids, schizogenous cavities, and subterete filaments are consistent with a position in Rutaceae. Euodia and relatives form a moderately supported clade, but other than that, relationships are unclear (Poon et al. 2007). For relationships in Galipeinae see Kallunki and Groppo (2007) and in the largely South African Diosmeae, see Trinder-Smith et al. (2007).

Classification. Tribal limits for the most part need overhauling (e.g. Salvo et al. 2008; Poon et al. 2008), and the same is true of generic limits, especially around Citrus (Scott et al. 2000; Samuel et al. 2001; Bayer et al. 2009), as also in Galipeinae (Kallunki & Groppo 2007) and Diosmeae (Trinder-Smith et al. 2007). Hartley (1981) suggested some generic realignments that largely ignored then then-conventional subfamilies; this work has since been confirmed by molecular data.

Previous Relationships. Cronquist (1981) included Cneorum in Sapindaceae; Airy Shaw (1966) associated Kirkia with Ptaeroxylaceae, but with hesitation. Hegnauer (1990) included Ptaeroxylum in Meliaceae, although he noted it was chemically more similar to Rutaceae. Harrisonia has also been included in Rutaceae, as by Thorne (1992: no reasons given).

Savolainen et al. (2000b) suggested that Lissocarpaceae should be included here, but a position in Ebenaceae-Ericales is now strongly supported (Berry et al. 2001).

MELIACEAE Jussieu, nom. cons.   Back to Sapindales

Trees; bark often rather bitter; secretory cells with resin, etc. +; nodes 5:5; (hairs stellate); (leaves even-pinnate), leaflets not articulated (alternate; articulated; toothed); plants often dioecious, but flowers apparently perfect, (3-)5(-8)-merous; K often connate, C (-14; connate); A 2x C, connate (5-30 in a single whorl); G (1) [2-6(-many)], postgenitally united, stigma wet; ovules ?anatropous, (micropyle exo/bistomal), outer integument 2-5 cells across, inner integument 2-4 cells across, placental obturator common; archesporium often multicellular; seeds often pachychalazal, coat vascularised, testa and tegmen multiplicative (not), testa undistinguished but thick, endotesta crystalliferous, exotegmen fibrous [Trichilia, Swietenia] (not); embryo white [green - Trichilia]; n = 10-14.

52[list]/621 - 2 groups below. Pantropical, but largely Old World; plants of the lowlands (map: see Wickens 1976; Pennington 1981; FloraBase 2006; GBIF x.2009).

1. Melioideae Arnott

Buds naked; (nodes 3:3); (leaves two-ranked - Turraea); 1-2 (-many) ovules/carpel, stigma capitate; fruit a loculicidal capsule (berry, drupe, nut); seeds unwinged (winged - Quivisianthe), usu. with aril [funicular in Naregamia] or sarcotesta.

37/571. Aglaia (110), Trichilia (85), Dysoxylum (80), Chisocheton (50), Guarea (50). Pantropical, but largely Old World.

Synonymy: Aitoniaceae Reveal & Hoogland

2. Swietenioideae Kostel.

Buds perulate (naked - Capuronianthus); (C connate; A at least partly free; nectary 0), (2 [Capuronianthus]) 3-many ovules/carpel, style-head discoid (capitate); fruit a septifragal capsule, valves falling off, columella persisting and seeds winged, or slight columella and seeds with massive woody or corky testa.

15/50: Entandophragma (15). Pantropical, but largely Old World.[Photo - Flower, Fruit.]

Synonymy: Cedrelaceae R. Brown, Swieteniaceae Berchtold & J. Presl

• Meliaceae are recognisable by their usually spiral and odd-compound leaves with well-developed leaf buttresses, i.e. the leaf bases are swollen and more or less elongated vertically. The leaflets are often opposite and dry thin and brittle, with little in the way of tertiary venation evident. The bark may smell - sweet, like garlic, etc. - and milky exudates occur sporadically. The flower buds are often longer than broad, with petals much longer than the sepals, and most members have a staminal tube and a large stigma. The fruits and seeds are usually quite large. [Photo - Flower, Fruit.]

Evolution. Muellner et al. (2006) discuss the biogeography of the family, suggesting its origin in Africa and subsequent dispersal; the family is ca 85-76 million years old, diversification within it beginning ca 75-67.5 million years before present. For the biogeography of Aglaia, see Muellner et al. (2008b).

Most species of Guarea (tropical America) and Chisocheton (Malesia), both Melioideae, have indefinitely growing leaves. In Guarea the apical part of the leaf is shoot-like in its gene expression (Tsukaya 2005), while in species of Chisocheton such as C. pohlianus the inflorescence may be epiphyllous (Fisher & Rutishauser 1990), flowers appearing between the leaflets (specimens have been misidentified as Rubiaceae!). In the latter genus the leaves can be rooted, and then they continue to grow for a long time, although I do not know of any case where a fertile tree has been produced from a leaf. Capuronianthus (Swietenioideae) has opposite, compound leaves, while the simple-leaved Vavaea and Turraea (both Melioideae) look rather unlike other Meliaceae, except when in flower; the leaves of the latter genus may even be two-ranked and lack articulations.

Most Meliaceae have a well-developed floral tube which is formed by the connation of the filaments - a rather uncommon way of forming the tube. The pistillode in staminate flowers is well developed, the result being that staminate and carpellate flowers are very similar functionally, although the former are often somewhat narrower. The whole apex of the style may be massively swollen and involved in secondary pollen presentation, as in Vavaea (Ladd 1994).

Economic Importance. Azadirachta indica (Melia azadirachta) is the neem tree (for an account, see Singh et al. 2009); the wood of Swietenia spp. provides the prized mahogany.

Chemistry, Morphology, etc. Munronia is ± herbaceous. Sieve tube plastids with protein crystalloids and starch occur in Melia and Azederach. The filaments of Vavaea are largely free, as are those of Cedrela and Toona (Swietenioideae-Cedreleae). Indeed, Cedreleae are rather different florally from other Meliaceae, but features found there such as more or less free stamens may be derived, not plesiomorphous as one might think a priori (cf. Gouvêa et al. 2008). Walsura often has leaflets with ± pulvinate petiolules and prominent reticulate venation, the stamens are also more or less free, and the fruit is often 1-seeded. Turner et al. (2009) document a water gap near the hilum in the hard seeds of Dodonaea.

For chemistry, see Hegnauer (1969, 1990) and Mulholland et al. (2000), and for embryology, etc., see Wiger (1935) and Nair (1970).

Phylogeny. Swietenioideae (Cedreloideae may be an earlier name, but it is currently not used) and Melioideae are clearly monophyletic clades (Oon et al. 2000: one gene, Cedreloideae not well supported; Muellner et al. 2003: three genes; Muellner et al. 2006: rbcL alone, sampling better). Although the two subfamilies can be separated chemically based on limonoid types, recent work on Quivisianthe suggests that the distinction may not be that simple (Mulholland et al. 2000). Two Malagasy genera previously segregated as separate subfamilies, Quivisianthe and in particular Capuronianthus, are embedded in Melioideae and Swietenioideae respectively (e.g. Muellner et al. 2003, 2006). Within Melioideae, Melieae (probably including Owenia) are sister to the rest, but with only moderate support; relationships along the backbone of the rest of the rather pectinate ITS tree are poorly supported, but rather better resolved by rbcL data (Muellner at al. 2008a). For relationships in Aglaia, see Muellner et al. (2005); see Fukuda et al. (2003) for a phylogeny of Chisocheton; for Neotropical Cedreleae, see Muellner et al. (2009).

Classification. For a generic monograph, see Pennington and Styles (1975), for a monograph of Neotropical Meliaceae, see Pennington (1981), and for a monograph of Aglaia, see Pannell (1992). I am grateful to David Kenfack for useful information.

SIMAROUBACEAE Candolle, nom. cons.   Back to Sapindales

Trees or shrubs; bark very bitter by simaroubilide quassinoids, ellagic acid +; wood often fluorescing; (nodes multilacunar); medullary secretory canals common; sclereids common, oil cells uncommon; (stomata paracytic); leaf ptyxis also supervolute-curved, leaflets not articulated, (flat surface glands +), margins coarsely toothed to entire, (stipules +, cauline [Picrasma, some Soulamea] or petiolar); flowers rather small, bisexual or not, (3-)4-6(-8)-merous; K connate or free (0), (C 0); A (5, opposite sepals, 10<), with lateral or basal-adaxial scales or 0; G 1-5(-8), ± free to connate, gynophore short and stout/0, style +/0, or styluli +, often ± basal, stigmas ± recurved, ± pointed, with elongated receptive zone, dry; ovule 1/carpel, micropyle (bistomal? - Samadera) zig-zag, outer integument 3-10 cells across, inner integument 2-8 cells across, parietal tissue 7-20 cells across, (ovule close to epidermis - Samadera); fruit 1-seeded drupelet (samara); seed (pachychalazal), with undistinguished testa (mesotegmen with reticulate thickenings) or scattered lignified cells, endotesta often slightly lignified, tegmen crushed; (endosperm with starch [Leitneria] or hemicellulose reserve); n = 8-13.

19-22[list]/110: Simaba (25). Largely tropical; a few (e.g. Ailanthus) temperate (map: from Nooteboom 1962; Heywood 1978; Thomas 1990; fossils of Ailanthus as black crosses, from Corbett & Manchester 2004 and Clayton et al. 2009, also Japan; fossils of Leitneria as blue crosses, from Clayton et al. 2009). [Photo - Flower, Fruit] [Photo - Fruit]

• Simaroubaceae can be recognised because the twigs have conspicuous pith - herbarium specimens are often notably light - and the bark is bitter, even when dry; the leaflets of the odd-compound leaves often have rather coarse, blunt, teeth and flat glands on the lower surface, sometimes close to the margin, and the leaf rhachis collapses at the nodes. The flowers are rather small, the petals usually barely exceeding the sepals. The fruits are often separate drupelets or samaras.

Evolution. Ailanthus is known as widespread fossils from the Eocene ca 52 million years before present; it has not been recorded from the Palaeocene (Corbett & Manchester 2004; see also Clayton et al. 2009 for the fossil history of this genus, Leitneria, and Chaneya, the latter not certainly to be included in Simaroubaceae). The age of crown group Simaroubaceae has been estimated as some 52 million years (Muellner et al. 2007), although better sampling in the family suggested a rather older date in the Cretaceous-Maastrichtian a little more than 65 million years ago. However, most diversification within the family has been in the Caenozoic (Clayton et al. 2009).

Despite (or because of?) the fairly good fossil history of the family in the northern hemisphere, the biogeographic hisory of Simaroubaceae is of considerable complexity with much disperal (and some extinction) needed to explain the current distribution of taxa (Clayton et al. 2009).

Chemistry, Morphology, etc. Although the carpels may be ± free, there is often only a single style. Even in taxa with unitegmic ovules, the axis of the embryo and the micropyle are offset at sharp angle, hence the latter is zig-zag. There are reports of other than porogamous fertilisation in the family (cf. Anacardioideae: Rao 1970).

For chemistry, see Hegnauer (1973, 1990, also 1966, 1989, as Leitneriaceae), and for other information, see Wiger (1935: embryology), Abbe (1974: floral morphology/anatomy of Leitneria), Fernando and Quinn (1992: pericarp anatomy), Jadin (1901: vegetative anatomy), Boas (1913: vegetative anatomy), and Webster (1936: wood anatomy).

Phylogeny. [Picrasma [Holacantha + Castela]] form a clade with rather weak support that is sister to the rest of the family, Ailanthus, [Leitneria, Soulamea, Brucea, etc.] and Picrolemma are successively sister to the remainder; much of the phylogenetic structure along the backbone of the family is well supported (Clayton et al. 2007a, esp. b; 2009). There are five major clades, and only Quassia and Nothospondias are of uncertain position, bracketing Picrolemma (Clayton et al. 2007b). Leitneria is well embedded in Simaroubaceae, being sister to all other members of clade III (Clayton et al. 2007b). In the past it has been separated in its own family (it was then the only family restricted to the U.S.A.!) - it is wind pollinated, the plant is more or less dioecious, and hardly surprisingly the flowers are much reduced and in short catkins: C 0?, pollen reticulate; G 1, stigma decurrent; mesotegmen with reticulate thickenings, endosperm starchy.

The very poorly-known Gumillea (ex Cunoniaceae) should perhaps be included in Simaroubaceae, although the stamens do not appear to have scales and there are many ovules per carpel - the latter feature in particular would be rather odd for any member of Sapindales. Its stamens alternate with its petals, so making membership in Picramniales unlikely (and ovule number also militates against this).

Previous Relationships. Simaroubaceae have been very difficult to delimit, and molecular data suggest the excision of Suriana and its relatives (here in Surianaceae - Fabales), Harrisonia (Rutaceae), and Picramnia and Alvaradoa (Picramniaceae - Picramniales, sister to [Sapindales [Huerteales etc.]]) (e.g. Fernando et al. 1995).

Synonymy: Ailanthaceae J. Agardh, Castelaceae J. Agardh, Holacanthaceae Engler, Leitneriaceae Bentham & J. D. Hooker, Quassiaceae Bertolini, Simabaceae Horaninow, Soulameaceae Endlicher