LIGNOPHYTA

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

EXTANT SEED PLANTS/SPERMATOPHYTA

Plant woody, evergreen; nicotinic acid metabolised to trigonelline, (cyanogenesis via tyrosine pathway); primary cell walls rich in xyloglucans and/or glucomannans, 25-30% pectin [Type I walls]; lignins derived from (some) sinapyl and particularly coniferyl alcohols, thus containing p-hydroxyphenyl and guaiacyl lignin units, so no Maüle reaction; root xylem exarch, cork cambium deep seated; arbuscular mycorrhizae +; shoot apical meristem interface specific plasmodesmatal network; stem with vascular tissue around central pith [eustele], vascular bundles with interfascicular tissue, ectophloic, endodermis 0, xylem endarch; wood homoxylous, tracheids and rays alone, tracheid/tracheid pits circular, bordered; mature sieve tube/cell lacking functioning nucleus, sieve tube plastids with starch grains; phloem fibres +; stem cork cambium superficial; branches exogenous; leaves with single trace from vascular sympodium ["nodes 1:1"]; vascular bundles collateral [stem: phloem external; leaf: phloem abaxial]; stomata morphology?, pore opening controlled by abscisic acid; leaves with petiole and lamina, spiral, development basipetal, blade simple; axillary buds +, not associated with all leaves; prophylls two, lateral; plant heterosporous, sporangia borne on sporophylls; microsporophylls aggregated in indeterminate cones/strobili; true pollen +, grains mono[ana]sulcate, exine and intine homogeneous; ovules unitegmic, parietal tissue 2+ cells across, megaspore tetrad tetrahedral, only one megaspore develops, megasporangium indehiscent; male gametophyte development first endo- then exosporic, tube developing from distal end of grain, to ca 2 mm from receptive surface to egg, gametes two, developing after pollination, with cell walls, flagellae numerous; ovules increasing considerably in size between pollination and fertilization, female gametophyte endosporic, initially syncytial, walls then surrounding individual nuclei; seeds "large" [ca 8 mm³], but not much bigger than ovule, with morphological dormancy; embryo cellular ab initio, endoscopic, plane of first cleavage of zygote transverse, suspensor +, short-minute, embryo straight, shoot and root at opposite ends [allorrhizic], white, cotyledons 2; plastid transmission maternal; ycf2 gene in inverted repeat, two copies of LEAFY gene, PHY gene duplications [three - [BP [A/N + C/O]] - copies], nrDNA with 5.8S and 5S rDNA in separate clusters; mitochondrial nad1 intron 2 and coxIIi3 intron and trans-spliced introns present.

MAGNOLIOPHYTA

Lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, non-hydrolysable tannins, quercetin and/or kaempferol +, apigenin and/or luteolin scattered, [cyanogenesis in ANITA grade?], S [syringyl] lignin units common, positive Maüle reaction [syringyl:guaiacyl ratio more than 2-2.5:1], and hemicelluloses as xyloglucans; root apical meristem intermediate-open; root vascular tissue oligarch [di- to pentarch], lateral roots arise opposite or immediately to the side of [when diarch] xylem poles; origin of epidermis with no clear pattern [probably from inner layer of root cap], trichoblasts [differentiated root hair-forming cells] 0, exodermis +; shoot apex with tunica-corpus construction, tunica 2-layered; reaction wood ?, associated gelatinous fibres [g-fibres] with innermost layer of secondary cell wall rich in cellulose and poor in lignin; starch grains simple; primary cell wall mostly with pectic polysaccharides, poor in mannans; tracheid:tracheid [end wall] plates with scalariform pitting, wood parenchyma +; sieve tubes enucleate, sieve plate with pores (0.1-)0.5-10< µm across, cytoplasm with P-proteins, cytoplasm not occluding pores of sieve plate, companion cell and sieve tube from same mother cell; sugar transport in phloem passive; nodes unilacunar [1:?]; stomata brachyparacytic [ends of subsidiary cells level with ends of pore], outer stomatal ledges producing vestibule; lamina formed from the primordial leaf apex, margins toothed, development of venation acropetal, secondary veins pinnate, overall growth ± diffuse, venation hierarchical, fine venation reticulate, veins (1.7-)4.1(-5.7) mm/mm², endings free; most/all leaves with axillary buds; flowers perfect, pedicellate, ± haplomorphic, parts spiral [esp. the A], free, numbers unstable, development in general centripetal; P not sharply differentiated, with a single trace, outer members not enclosing the rest of the bud, often smaller than inner members; A many, filament not sharply distinguished from anther, stout, broad, with a single trace, anther introrse, tetrasporangiate, sporangia in two groups of two [dithecal], ± embedded in the filament, with at least outer secondary parietal cells dividing, each theca dehiscing longitudinally, endothecium +, endothecial cells elongated at right angles to long axis of anther; tapetum glandular, cells binucleate; microspore mother cells in a block, microsporogenesis successive, walls developing by centripetal furrowing; pollen subspherical, tectum continuous or microperforate, ektexine columellar, endexine thin, compact, lamellate only in the apertural regions; nectary 0; G superior, free, several, ascidiate, with postgenital occlusion by secretion, stylulus short, hollow, cavity not lined by distinct epidermal layer, stigma ± decurrent, carinal, dry [not secretory]; ovules few [?1]/carpel, marginal, anatropous, bitegmic, micropyle endostomal, outer integument 2-3 cells across, often largely subdermal in origin, inner integument 2-3 cells across, often dermal in origin, parietal tissue 1-3 cells across [crassinucellate], nucellar cap?; megasporocyte single, hypodermal, megaspore tetrad linear, functional megaspore chalazal, lacking sporopollenin and cuticle; female gametophyte four-celled [one module, nucleus of egg cell sister to one of the polar nuclei]; ovule not increasing in size between pollination and fertilization; pollen binucleate at dispersal, male gametophyte trinucleate, germinating in less than 3 hours, pollination siphonogamous, tube elongated, growing between cells, growth rate 20-20,000 µm/hour, outer wall pectic, inner wall callose, with callose plugs, penetration of ovules via micropyle [porogamous], whole process takes ca 18 hours, distance to first ovule 1.1-2.1 mm; male gametes lacking cell walls, flagellae 0, double fertilization +, ovules aborting unless fertilized; P deciduous in fruit; seed exotestal, becoming much larger than ovule at time of fertilization; endosperm diploid, cellular [micropylar and chalazal domains develop differently, first division oblique, micropylar end initially with a single large cell, divisions uniseriate, chalazal cell smaller, divisions in several planes], copious, oily and/or proteinaceous; embryogenesis cellular; germination hypogeal, seedlings/young plants sympodial; Arabidopsis-type telomeres [(TTTAGGG)_n]; 2C genome size 1-8.2 pg [1 pg = 10⁹ base pairs], whole genome duplication, ndhB gene 21 codons enlarged at the 5' end, single copy of LEAFY and RPB2 gene, knox genes extensively duplicated [A1-A4], AP1/FUL gene, paleo AP3 and PI genes [paralogous B-class genes] +, with "DEAER" motif, SEP3/LOFSEP and three copies of the PHY gene, [PHYB [PHYA + PHYC]].

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

[AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]: ethereal oils in spherical idioblasts [lamina and P ± pellucid-punctate]; tectum reticulate-perforate, nucellar cap + [character lost where in eudicots?]; 12BP [4 amino acids] deletion in P1 gene.

[[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]] / MESANGIOSPERMAE: benzylisoquinoline alkaloids +; polyacetate derived anthraquinones + [?level]; outer epidermal walls of root elongation zone with cellulose fibrils oriented transverse to root axis; P more or less whorled, 3-merous [possible positiion]; embryo sac bipolar, 8 nucleate, antipodal cells persisting; endosperm triploid; ?germination.

[MONOCOTS [CERATOPHYLLALES + EUDICOTS]]: (veins in lamina often 7-17mm/mm² or more [mean for eudicots 8.0]); (stamens opposite [two whorls of] P); (pollen tube growth fast).

[CERATOPHYLLALES + EUDICOTS]: ethereal oils 0.

EUDICOTS: myricetin, delphinidin scattered, asarone 0 [unknown in some groups, + in some asterids]; root epidermis derived from root cap [?Buxaceae, etc.]; nodes 3:3; stomata anomocytic; flowers (dimerous), cyclic; K/outer P members with three traces, "C" with a single trace; A few, (polyandry widespread, initial primordia 5, 10, or ring, ± centrifugal), filaments fairly slender, anthers basifixed; microsporogenesis simultaneous, pollen tricolpate, apertures in pairs at six points of the young tetrad [Fischer's rule], cleavage centripetal, wall with endexine; G with complete postgenital fusion, stylulus/style solid [?here]; seed coat?

[PROTEALES [TROCHODENDRALES [BUXALES + CORE EUDICOTS]]]: (axial/receptacular nectary +).

[TROCHODENDRALES [BUXALES + CORE EUDICOTS]]: benzylisoquinoline alkaloids 0; euAP3 + TM6 genes [duplication of paleoAP3 gene: B class], mitochondrial rps2 gene lost.

[BUXALES + CORE EUDICOTS]: ?

CORE EUDICOTS / GUNNERIDAE: (ellagic and gallic acids +); leaf margins serrate; compitum + [one place]; micropyle?; palaeohexaploidy [gamma triplication], PI-dB motif +, small deletion in the 18S ribosomal DNA common.

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

[DILLENIALES [SAXIFRAGALES [VITALES + ROSIDS s. str.]]]: nodes 3:3; stipules + [usually apparently inserted on the stem].

[SAXIFRAGALES [VITALES + ROSIDS]] / ROSANAE Takhtajan / SUPERROSIDAE: ??

[VITALES + ROSIDS] / ROSIDAE: anthers articulated [± dorsifixed, transition to filament narrow, connective thin].

ROSIDS: (mucilage cells with thickened inner periclinal walls and distinct cytoplasm); embryo long; genome duplication; chloroplast infA gene defunct, mitochondrial coxII.i3 intron 0.

ROSID II / MALVIDAE / [[GERANIALES + MYRTALES] [CROSSOSOMATALES [PICRAMNIALES [SAPINDALES [HUERTEALES [MALVALES + BRASSICALES]]]]]]: ?

[CROSSOSOMATALES [PICRAMNIALES [SAPINDALES [HUERTEALES [MALVALES + BRASSICALES]]]]]: ?

[PICRAMNIALES [SAPINDALES [HUERTEALES [MALVALES + BRASSICALES]]]]: ovules 2/carpel, apical.

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

Evolution. Divergence & Distribution. A suggestion for the age of this node is (88-)71(-73) m.y. (N. Zhang et al. 2012). Other estimates are (102-)96(-90) and (80-)76(-72) m.y. (Wang et al. 2009) and ca 98.1 and 98.4 m.y. (Magallón & Castillo 2009).

Genes & Genomes. 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 m.y. 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. Placing it at this node is one possibility.

Chemistry, Morphology, etc. For integument thickness (which, however, reverses, and its condition is unclear in Huerteales, etc.), see Endress and Matthew (2006a).

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 (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 Berchtold & J. Presl  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, leaflets opposite, vernation conduplicate; A 2x K, (± obdiplostemonous); (exine distinctly striate); nectary well developed; G opposite petals or odd member adaxial, stigmatic head from postgenitally united free carpel tips; ovules few/carpel, epitropous; seed coat?; (embryo green). - 9 families, 471 genera, 6070 species.

Note: Possible apomorphies are now being added throughout the site; they are in bold. However, the actual level at which many of these features, particularly the more cryptic ones, should be assigned is unclear. This is because there is very considerable homoplasy for many characters, with with variation within and between clades. Furthermore, basic information for all too many characters is very incomplete, often coming from taxa well embedded in the clade of interest and so making the position of any putative apomorphy uncertain. Then there is the not-so-trivial issue of how ancestral states are reconstructed...

Evolution. Divergence & Distribution. Wikström et al. (2001: relationships [Brassicales [Malvales + Sapindales]]) date the crown group to (71-)67(-63) m.y.; the age was estimated as (66-)63(-60) and (73-)71(-69) m.y. (two penalized likelihood dates: Wang et al. 2009), while Magallón and Castillo (2009) suggested an age of around 70.7 m.y..

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

Plant-Animal Interactions. Associated with the accumulation of noxious secondary metabolites, specialised herbivores are found on many of this group. 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. 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 are sometimes clearly modified leaflets and have been described as pseudostipules or metastipules, the latter being 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).

Bachelier and Endress (2009) suggest some floral developmental features found widely in this clade. The flowers are often imperfect, but since staminate and carpellate flowers have well-developed pistillodes and staminodes respectively, they can be difficult to distinguish. Floral tubes formed by connate or closely adpressed and flattened filaments occur throughout Meliaceae, in a number of Rutaceae, in Boswellia disocorides (Burseraceae)... Pollen with striate exine is scattered through the order. Septal cavities have been noticed in Cneorum (Rutaceae) and Koelreuteria (Sapindaceae), but they do not secrete nectar (Caris et al. 2006, c.f. septal nectaries in monocots). For some details of embryology, see Mauritzon (1936). Biebersteiniaceae and Nitrariaceae are particularly poorly known morphologically.

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 (also poorly supported in Soltis et al. 2011), a fair bit of resolution elsewhere, excepting only a moderately-supported sister group relationship between Meliaceae and Simaroubaceae (c.f. Gadek et al. 1996; Soltis et al. 2011: sampling), 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, ex Geraniaceae, in Sapindales, albeit with a long branch (Bakker et al. 1998). Morphological phylogenetic analyses suggest that Bretschneidera and Akania are to be included in Brassicales (e.g. Ronse de Craene & Haston 2006, see below).

Previous Relationships. In the past Bretschneideraceae and Akaniaceae (= Akaniaceae [Brassicales] here) have been associated with Sapindales, Bretschneidera in particular looking very like a member of Sapindaceae; the presence of myrosin cells in the former was not considered to be all that important (Cronquist 1981; Takhtajan 1997).

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

Synonymy: Rutinae Reveal - Acerales Berchtold & J. Presl, Aesculales Bromhead, Amyridales J. Presl, Aurantiales Link, Biebersteiniales Takhtajan, Burserales Martius, Cedrelales Martius, Citrales Dumortier, Cneorales Link, Diosmales J. Presl, Hippocastanales Link, Julianales Engler, Leitneriales Engler, Meliales Berchtold & J. Presl, Nitrariales Martius, Pteleales Link, Rutales Berchtold & J. Presl, Simaroubales Berchtold & J. Presl, Spondiadales Martius, Terebinthales Dumortier, Zanthoxylales J. Presl

BIEBERSTEINIACEAE Schnitzlein   Back to Sapindales

Rhizomatous perennial herbs; vessels?; nodes?; hairs glandular; leaves (2-3 compound), leaflets lobed, margins toothed, stipules +, petiolar, lobed or not; inflorescence racemose; C clawed, (denticulate); nectary glands opposite K; pollen 3-celled, exine striate; gynophore +, short, G [5], styles separate, impressed, apically connate, stigma capitate; ovule 1/carpel, micropyle endostomal; embryo sac tetrasporic, 16-nucleate, 13-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. Biebersteinia is little known. At least some species are foul-smelling. The ante-petalous stamens are longest. Takhtajan (1997) described the ovules as being unitegmic.

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.

Additional information is taken from Baillon (1874), Kunth (1912: general), Hegnauer (1989, as Geraniaceae: chemistry), Boesewinkel (1997: seeds), Tzakou et al. (2001: fatty acids) and Muellner (2011: general).

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

[Nitrariaceae [[Kirkiaceae [Anacardiaceae + Burseraceae]] [Sapindaceae [Simaroubaceae [Rutaceae + Meliaceae]]]]]: stigma papillate.

NITRARIACEAE Lindley   Back to Sapindales

Annual to perennial herbs to shrubs; mycorrhizae absent [Peganum]; ß-carbalin alkaloids +, ethereal oils?; cork in inner cortex; wood storied; nodes?; petiole bundle arcuate, with wing bundles; stomata in longitudinal bands of small cells [not Nitraria]; mucilage cells +, throughout plant or not; cuticle waxes 0 (platelets, rodlets); leaves two per node, adjacent, (spiral), entire or pinnatifid, ?vernation, stipules minute or foliaceous, ± cauline; inflorescence terminal, cymose, or flower single. leaf-opposed; K (connate), (valvate - Peganum]; C protects the flower in bud; A (5-)15, in triplets opposite K, filament bases broad, flattened, [Nitraria, Peganum), or flower (3-)4-merous; A basically[?] haplostemonous, 4, opposite K [Tetradiclis]); nectaries antepetalous [Nitraria, Peganum], or 0 [Tetradiclis; G [2-4(-6)], (opposite C - Nitraria), style long to rather short, basal and ± impressed [Nitraria, ± hollow, Tetradiclis], stigma as commissural compital lines down part of its length, dry; ovules 1 apotropous or 6-many ?epitropous/carpel, micropyle zig-zag or bistomal, outer integument 2-4 cells across, inner integument 2-3 or 4-7 cells across, parietal tissue ca 3 cells across, funicle long [not Nitraria]; megaspore mother cells several [Peganum]; fruit a capsule, or drupe, 1-seeded. mesocarp woody [Nitraria], or berry [some Peganum]; (testa weakly multiplicative - Peganum), exotesta cells inflated or not, often mucilaginous; endotesta short palisade, or not, endotegmen ± fibrous [Peganum] or not [Tetradiclis]; endosperm copious (not Nitraria), (embryo green); n = 7, 12.

3[list]/16. Usu. ± arid regions from North Africa to East Asia, also S.W. Australia and E. Mexico (map: from Brummitt 2007; modified by Frankenberg & Klaus 1980; Pan et al. 1999; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; FloraBase 2007). [Photo - Flowers.]

Chemistry, Morphology, etc. The variation in this group is rather puzzling...

• Nitraria often has two or three leaves at a node (= ?short shoot), although only some 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 flowers are leaf opposed. 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 is 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 a 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 extend 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 are absent; they are present, if small.

No endothelium has been recorded in members of Nitrariaceae (Kapil & Tiwari 1978), c.f. 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, and Bachelier et al. (2011: nice study, all three genera) of floral morphology; for chemistry, see Hegnauer (1973, 1990: as Zygophyllaceae), and for general information, see Weberling and Leenhouts (1965), Hussein et al. (2009) and Sheahan (2011: as Nitrariaceae and Tetradiclidaceae). For the embryology of Peganum, see Kapil and Ahluwalia (1963).

Phylogeny. Molecular data suggest the relationships [Nitraria [Tetradiclis + Peganum (inc. Malacocarpus)]] (Sheahan & Chase 1996; Savoilainen et al. 2000; Muellner et al. 2007), and place the group in Sapindales.

Previous Relationships. Nitrariaceae and Zygophyllaceae agree in general appearance, wood anatomy, and perhaps also chemistry (Nag et al. 1995); 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 Zygophyllaceae (Cronquist 1981), although Takhtajan (1997) placed the genera here included in Nitrariaceae as three separate families in his Zygophyllales. Zygophyllales in A.P.G. III (2009) include Zygophyllaceae s. str. and the monogeneric Krameriaceae and are not remotely close to Nitrariaceae.

Synonymy: Peganaceae Takhtajan, Tetradiclidaceae Takhtajan

[[Kirkiaceae [Anacardiaceae + Burseraceae]] [Sapindaceae [Simaroubaceae [Rutaceae + Meliaceae]]]]: persistent remnant of floral apex in the center of the gynoecium [?this level], (styles postgenitally connate); ovules 2/carpel, superposed, micropyle endostomal, inner integument elongated, S- or Z-shaped, nucellar cap +.

[Kirkiaceae [Anacardiaceae + Burseraceae]]: inflorescence thyrsoid [panicle of cymes]; (pollen exine striate); G adnate to central receptacular apex, synascidiate, stigma with uniseriate multicellular papillae, wet; fruit a schizocarp, with 1 seed/carpel, endocarp well developed.

Chemistry, Morphology, etc. Syllepsis is uncommon in this clade (Keller 1994). For some general information, see Bachelier and Endress (2008b).

KIRKIACEAE Takhtajan   Back to Sapindales

Tree or shrub, often with tuberous roots; ellagic acid +; nodes?; petiole bundle with medullary bundles; glandular hairs with multiseriate stalk; cuticle waxes 0; stomata ?anomocytic; leaves ± opposite to spiral, leaflet margins 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; nectary broad, well developed; pistillode +; carpellate flowers: staminodes +; G [4 (8)], ?orientation, extra "loculus" ± developed, tip of receptacle apex convex, swollen, glandular, styluli closely adpressed, erect, finally spreading, apex postgenitally connate, stigmas ± punctiform; ovule usu. 1/carpel, micropyle bistomal, long [1/2 length of ovule], outer integument 2-3 cells across, inner integument 3-4 cells across; mericarps pendulous from columella; testa "very thin"; endosperm ?type, 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 columellar strands.

Chemistry, Morphology, etc. The family is chemically unexceptionable, lacking distinctive secondary metabolites found elsewhere in the order (Mulholland et al. 2003). The wood of Pleiokirkia is reported to smell like honey (Schatz 2001). The lower order branches have female flowers, while flowers on higher order branches are male (Bachelier & Endress 2008b). The endocarp of the fruit has elongated and variously oriented sclereids (Fernando & Quinn 1992).

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). For general information, see Muellner (2011).

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

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

Evolution. Divergence & Distribution. Fossils assignable to Burseraceae/Anacardiaceae are known from the early Eocene in England ca 50 m.y.a. (Collinson & Cleal 2001).

Chemistry, Morphology, etc. Anacardiaceae like Pachycormus have thin, brown, flaking bark and vegetatively look quite like Burseraceae; the wood anatomy of the two is very similar (Daly et al. 2011). 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), as found in Anacardiaceae-Spondiadoideae, and also in Buchanania, Campnosperma and Pentaspadon, included in Anarcardioideae, as by Pell (2004: unfortunately, Campnosperma was not sequenced), as well as in Burseraceae. 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 resinous, black or becoming blackish; (cork cortical); crystals in xylem; wood often fluorescing; pith loose, shining; nodes usu. 3:3; petiole with annular wing bundles; leaflets not articulated, margins toothed or not, base of petiole often swollen; breeding system various; flowers (3-)5(-7)-merous; (K, C 0); A (1-10<), when 5, opposite sepals; (stamens on nectary; nectary 0); (andro/gynophore +), styluli ± separate, terminal to gynobasic, (apex postgenitally connate), stigma capitate (lobed), dry; ovule 1/carpel, usu. apotropous, ± anatropous, (perichalazal), uni- or bitegmic, micropyle zig-zag (endostomal), funicle often long, ponticulus +; seed often ± pachychalazal, vascular bundles in this area, endotegmen usu. ± thickened, lignified; endosperm oily (and starchy), embryo often curved; n = 7-12, 14-16, 21.

81[list]/873. Tropical, also temperate (map: from Heywood 1976; modified by Barkley 1937; Fl. Austral. 25. 1985; Wickens 1976; Meusel et al. 1978; Arbonnier 2002; Nie et al. 2009; Trop. Afr. Fl. Pl. Ecol. Distr. 6. 2011). Two groups below. [Photo - Flower, Fleshy fruit, Dry fruits.]

1. Spondioideae Arnott

A obdiplostemonous; G (?1 - Solenocarpus)[2-)4-5(-12)]; ovule ± apical, (2/ovules carpel, one epitropous), hypostase +, funicle massive; exocarp thick, operculum +/0; exotestal cells (and hypodermis) thickened or not, ± persistent, tegmen ± 0, hypostase persistent, saddle-shaped.

10/115. Tropical [or 21/138: Lannea (40)].

Synonymy: Spondiadaceae Martynov

2. Anacardioideae Link

5-deoxyflavonoids, also alkylcathechols and alkylresorcinols [phenols with unsaturated side chains - allergenic] +; leaves (opposite), simple to compound; (flowers monosymmetric); (K and/or C 0); A (1 [+ staminodes]), 5, 10 (many), (basally connate); G 1 [pseudomonomerous?], [3(-6)], (highly) asymmetric, one carpel fertile, symplicate zone?, (stigma punctate); ovule apical to basal, (unitegmic, funicle massive, with outgrowths - Pistacia, etc.); (chalazogamy +); drupe often asymmetric, ± 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], (operculum 0); seed coat undifferentiated; (embryo green), (cotyledons folded - Mangifera).

60/735: Searsia (120), Semecarpus (72), Mangifera (68), Ozoroa (40[+]). Largely tropical, also temperate.

Synonymy: Blepharocaryaceae Airy Shaw, Comocladiaceae Martynov, Julianaceae Hemsley, Lentiscaceae Horaninow, Pistaciaceae Martinov, Podoaceae Franchet, Rhoaceae Sadler, Schinaceae Rafinesque, Vernicaceae Schultz-Schultestein

• 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 often have an excentric style or styles (e.g. Spondias!) and are often more or less flattened and single-seeded drupes.

Evolution. Divergence & Distribution. 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; Pell et al. 2011; Collinson et al. 2012 for this and other fossil records). On the other hand, distinctive fruits that have been identified as Dracontomelon, a genus now restricted to the Old World, are known from the Late Eocene of Panama in deposits some 40-37 m.y. old (Herrera et al. 2012).

Plant-Animal Interactions. 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 psyllid plant louse, the hemipteran Calophya, is notably common on Schinus, and other psyllids occur on Anacardiaceae (Burckhardt & Basset 2000; Burckhardt 2005).

Pollination Biology & Seed Dispersal. There is chalzogamy in Pistacia, and perhaps other genera, 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).

Anacardioideae have a number of different kinds of disseminules that have modifications for wind dispersal. These include fruits adnate to broad bracts (Dobinea), fruits with a wing formed by the flattened peduncle of the inflorescence (Amphipterygium), much enlarged sepals (Parishia) or petals (Swintonia), more ordinary samaras (Loxopterygium), while in Cotinus hairs on the pedicels help in the wind dispersal of the fruits. The evolution of these fruit types seems to be correlated with the adoption of a drier habitat (Pell & Mitchell 2007). In Anacardium the fleshy swollen pedicel is part of the attractive unit.

Chemistry, Morphology, etc. Schweingruber et al. (2011) emphasize the abundance of tension wood. 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 nectariferous disc; normally the stamens are outside the nectary. 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 is obliquely symmetric (Ronse de Craene 2010). 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 infraspecific variation in style number - 1, 3 - see Gonzàlez and Vesprini (2010). Although the fruits are commonly described as drupes, the origins of the various layers of the fruit wall do not correspond to those of a drupe in the strict sense (Gonzàlez & Vesprini 2010).

For general information, see Ding Hou (1978) and Pell et al. (2011), for fruit anatomy, Wannan and Quinn (1990), for ovules, fruit and seed, see von Teichman and van Wyk (1988 and references), 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; Mitchell et al. (2006) focus more on Spondiadoideae.

Phylogeny. Spondiadoideae - Spondiadeae and some Rhoeeae, including Pegia, Tapirira and Cyrtocarpa (see Aguilar-Ortigosa & Sosa 2004; Pell 2004: list of included genera) - are sister to the rest of the family. In Anacardioideae (Pell & Urbatsch 2000, 2001; Pell 2004 and Mitchell et al. 2006 for a list of genera) wind-dispersed taxa do not form a single group (Pell & Mitchell 2007, c.f. Pell & Urbatsch 2001). However, Pell et al. (2011) suggest that Spondiadoideae may be polyphyletic.

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 other analyses (Pell & Mitchell 2007, c.f. abstract). Campnosperma, so far included in only one study (Chayamarit 1997: sampling limited, relationships different from those in other studies, no support values), has an endocarp similar to that of Buchanania and the fruit is sometimes two-locular. Neither of these genera is accounted for in Anacardioideae as characterized above; 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. Pell et al. (2011) included 21 genera in their polyphyletic Spondiadoideae.

Previous Relationships. 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; exudate colorless to white, resinous; ellagic acid +; nodes usu. 5:5; sclereids in stem; petiole bundle annular; indumentum very various; epidermis with mucilage cells; leaflets (with pellucid dots), ?vernation, margins often toothed, petiolules and petioles often pulvinate; dioecy common; K induplicate-valvate, ± connate, C valvate; ventral carpel bundles fused bundles of adjacent placentae, style usu. short; ovules 2/carpel; fruit septifragal, drupe often angled, stone with valves, K deciduous; (exotesta with shortly radially elongate but unthickened cells), endotesta lignified, ± tracheidal; embryo reserves hemicellulosic.

19[list]/755. Tropical. Two groups below.[Photo - Leaf, Flower, Fruit.]

1. Beiselieae Thulin, Beier & Razafimandimbison

Plant deciduous; (vessel elements with scalariform perforation plates); pith cells heterogeneous; leaf bases much swollen, persistent, apex shriveling and forming a spine; G [9-12], symplicate zone short, ovary strongly furrowed, style ± 0; ovules superposed; pericarp splitting septifragally, columella strongly ribbed, pyrenes apically winged, between the ribs; cotyledons entire; n = 13.

1/1: Beiselia mexicana. Michoacan, Mexico (Map: in blue below).

2. Bursereae de Candolle, Garugeae Marchand, Protieae Marchand

(Plant deciduous); oleoresins with mono- and bicyclic monoterpenes, triterpenes with ursane and oleanane components; (cork cambium deeper - Santiria); (pith cells hetergeneous); petiole bundle with medullary strands, (not; arcuate - Commiphora); snail glands + [curled ± uniseriate glandular hairs]; stipules petiolar or cauline, laciniate to entire, or 0; (K with single trace), C also induplicate-valvate, etc., (connate); A (apparently in a single whorl), (connate - canarium), (stamens = and opposite sepals), tapetal cells binucleate; (pollen psilate or striate); G [(2-)3-5], (one carpel developing), symplicate zone well developed, receptacle enclosed by the gynoecium; ovules collateral, campylotropous, outer integument 3-5 cells across, inner integument 3-4 cells across (integument 1, ca 5 cells across), parietal tissue 5-20< cells across, nucellar cap 1-30 cellls across (?0); pyrenes (winged), usu. with pericarpial pseudoaril, or fruit indehiscent, seeds embedded in ± fleshy pericarp; mesocarp quite frequently splits down loculicidal radius; fruit with columella; vascular bundle in outer integument; cotyledons straight to variously folded, entire to palmately lobed; n = 11-13, 22-24.

Synonymy: Balsameaceae Dumortier

18/754: Commiphora (185, 150 from Africa), Protium (180), Canarium (120), Bursera (100), Dacryodes (70). Tropical, but esp. America and N.E. Africa (map: from Rzedowski 1978; Trop. Afr. Fl. Pl. Ecol. Distr. 6. 2011; 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 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 symmetric.

Evolution. Divergence & Distribution. Becerra et al. (2012) put the age of crown group Burseraceae at (110.6-)92.7(-74.8) m.y., Bursera and Commiphora splitting ca 60 m.y.a., and the age of crown group Bursera at (62.7-)57.1(-51.5) m.y. Earlier, Becerra (2005) had put the split between Bursera and Commiphora at some 120 m.y.a., i.e. distributions might be affected by continental drift, with diversification within the former starting some 70 m.y.a. However, De-Nova et al. (2012: Beiselia included) dated crown-group Burseraceae to the early Palaeocene (69.7-)64.9(-60.3) m.y. Weeks and Simpson (2007) suggested that divergence of Commiphora from the clade now represented by the E. Asian B. tonkinensis occurred some 53-41.6 m.y.a. in the Eocene; Commiphora itself did not diversify until 32.3-23.2 m.y.a., Neogene aridification of Africa occurring more or less at that time. De-Nova et al. (2012) dated the split between Bursera and Commiphora to (59.0-)54.7(-50.6) m.y., crown group Bursera being ca 49.4. m.y., although diversification within the genus did not really get going until (23-)20 m.y.a. Becerra et al. (2009) had suggested that Bursera, of which some 85% of the species - often quite narrowly distributed - are found in seasonally-dry, tropical forests (SDTF) of Mexico, has diversified most within about the last 25 m.y., and De-Nova et al. (2012) estimated the age of most species of the SDTF at ca 7.5 m.y. - old, but more or less as predicted for such forests (Pennington et al. 2009; Dick & Pennington 2011).

See Daly et al. (2011) for the fossil record of the family.

Weeks et al. (2005) and Weeks and Simpson (2007, q.v. for details) discuss the complex biogeographic relationships within Burseraceae.

Plant-Animal Interactions. 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). Becerra (2003) suggested that the two had been co-evolving for about 100 m.y.. Species with a squirt defence in which toxic material is under pressure and when tissues are perforated it is ejected to a diastance of up to 2 m have a rather simple terpenoid-based exudate (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, and terpene variation seems to have become a matter of permuting combinations of chemicals in the local ecological context (Becerra et al. 2009).

Chemistry, Morphology, etc. The remarkable leaf bases of Beiselia are described by Forman et al. (1989); the axillary bud is borne on the base a little way from the stem. Some Burseraceae have foliaceous stipules; these are usually interpreted as being the reduced basal pair of leaflets of a compound leaf.

A few genera (e.g. Garuga) have a well-developed hypanthium; the disc is rarely extrastaminal (Triomma). The odd carpel is drawn as being abaxial in 4-merous Amyris (Schnizlein 1843-1870, fam. 244). Srivastava (1968) thought that the ovules of Bursera delpechiana were straight, but they do not appear to be so from his illustration. The embryo sac is very deely seated in the ovule, and there may be up to 85 cells between it and the epidermis; the shape of the embryo sac at maturity is very variable (Wiger 1935).

For additional general information, see Lam (1931, 1932), Leenhouts (1956), and in particular, Daly et al. (2011). For some chemistry, see Khalid (1983), mebryology, Narayana (1960 and references), and for pollen morphology, see Harley and Daly (1995: Protieae) and Harley et al. (2005: considerable variation).

Phylogeny. The quite recently-described Beiselia is sister to the rest of the family (e.g. Clarkson 2002). This has considerable implications for character evolution; Beiselia also has several probably autapomorphic features. In some studies Commiphora was embedded in Bursera, but the support was weak (Weeks et al. 2005). The monophyly of Bursera, sister to Commiphora, was confirmed (Becerra et al. 2012; De-Nova et al. 2012, but c.f. some analyses in the latter). Protieae, Bursereae, and Garugeae (the latter including Canarium, etc.) all had strong support individually and also as sister to Beiselia, but relationships between them were unclear (Thulin et al. 2008); Becerra et al. (2012) suggested the relationships [Canarieae [Protieae + Bursereae]], although support for the position of Canarieae was not very strong.

[Sapindaceae [Simaroubaceae [Rutaceae + Meliaceae]]] (if a clade): anthers with a pseudo-pit; tapetal cells multinucleate, nuclei fusing to form polyploid mass; hypostase +; testa over five cells across, multiplicative.

Chemistry, Morphology, etc. The style in at least some Rutaceae and Sapindaceae is hollow (Lersten 2004). For an extensive tabulation of variation in anther, ovule and seed characters of this clade, see Tobe (2011a).

SAPINDACEAE Jussieu, nom. cons.   Back to Sapindales

Woody; quebrachitol [cyclitol], toxic saponins, cyclopropane amino acids + [non-protein amino acid], ellagic acid 0 (+); cork also outer cortical; latex of sorts not uncommon; (vessel elements with scalariform perforation plates); petiole bundle with cortical or adaxial bundles); (epidermal cells mucilaginous), cuticle waxes 0 (platelets, rodlets); leaves spiral, odd pinnate, leaflets articulated [check basal pectinations], vernation also conduplicate-plicate, margins serrate, colleters common; inflorescence paniculate, the flowers often in clusters, imperfect; pedicels articulated; flowers 5-merous, C clawed; nectary extrastaminal; A 8, hairy; tapetal cells 1-3-nucleate; G [(2) 3(-6)], (style hollow; 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, parietal tissue 4-15 cells across (?0); fruit a loculicidal capsule; seed often pachychalazal; testa (and tegmen) multiplicative, testa vascularized, exotesta palisade (not), unlignified, (mesotestal cell walls thickened and lignified; endotesta crystaliferous), tegmen limited to radicular pocket, (exotegmen fibrous, lignified or not); endosperm 0, starchy, embryo curved, radicle in pocket formed by testa.

140[list]/1630: - four subfamilies below. ± World-wide. (map: from Herzog 1936; Meusel et al. 1978; Fl. Austral. 25. 1985). [Photo - Flower, Fruit, Fruit.]

1. Xanthoceroideae Thorne & Reveal

Phloem stratified; stomata anomocytic; bud scales +; leaves deciduous; flowers large [ca 2.5 cm across]; nectary with golden, horn-like glands alternating with C; pollen spiny; ovules 6-8/carpel, campylotropous, outer integument 6-8 cells across, inner integument 3-4 cells across, hypostase +, obturator 0; aril 0; mesotestal cell walls thickened, tegmen multiplicative, with inner layers thick-walled; germination epigeal; n = ?

1/1: Xanthoceras sorbifolia. N. China.

Synonymy: Xanthoceraceae Buerki, Callmander & Lowry

[Hippocastanoideae [Dodonaeoideae + Sapindoideae]]: pericyclic sheath of phloem fibres and stone cells; flowers often strongly obliquely or vertically [Aesculus] monosymmetric, (4-merous); ovules apotropous, funicular obturator +/-; (megaspore mother cells several); (fruit septicidal, a schizocarp with 1-seeded samaras); cotyledons spiral or not; germination hypogeal or epigeal.

2. Hippocastanoideae Dumortier

Cyanogenic glucosides 0; (pericyclic sheath 0); cuticle wax crystalloids quite common [Acer]; stomata actinocytic (anomocytic); bud scales + (0); leaves opposite, usu. palmate (odd pinnate; simple), deciduous; (flowers large - Aesculus; polysymmetric); C (not clawed - Acer), (with appendages); A (5-)6-8(-12); (nectary - Acer); (style long-branched), stigma dry; outer integument 3-5 [Acer] or 8-10 cells across, inner integument 3-6 cells across - Handeliodendron), nucellar cap 8-10 cells layers across, (hypostase 0 - Handeliodendron); (aril + - Handeliodendron); n = 20.

5/143: Acer (126). North temperate, some tropical and then usually montane.

Synonymy: Aceraceae Jussieu, Aesculaceae Burnett, Hippocastanaceae A. Richard, Paviaceae Horaninow

[Dodonaeoideae + Sapindoideae]: leaves usu. evergreen, even-pinnate, (bicompound; simple), leaflets opposite or not, (margins entire), (rachis winged); seeds often with chalazal/integumentary arils and sarcotesta, (dormancy physical, water gap near hilum).

3. Dodonaeoideae Burnett

Cork pericyclic - Dodonaea; stomata cyclocytic - Dodonaea; C (0), (appendages uncommon); A 5-many; ovule (1/carpel, pendulous, epitropous), outer integument 8-10 cells across, inner integument 3-4 cells across; (seed arillate or with sarcotesta); n = 10, 12, 14-16.

22/145: Dodonaea (70). Pantropical-warm temperate, esp. Australia/Southeast Asia.

Synonymy: Dodonaeaceae Small

4. Sapindoideae Burnett

(Lianes, climbing by branch tendrils); (secondary thickening anomalous); stomata various; (stipules or petiolar pseudostipules +); C (0, 5+), with various ± complex appendages; A (4[Glenniea]-many), tapetal cells uninucleate; (pollen oblate, triporate - Serjania, etc.); ovule often 1/carpel, outer integument 4-12 cells across, inner integument 2-7 cells across; (antipodal cells persistent - Cardiospermum); fruit also a samara (indehiscent); seeds often arillate or with arillode or sarcotesta; (amyloid [xyloglucans] in seed - Cardiospermum); n = esp. 10-12 [climbers] and 14-16 [non-climbers]; chromosomes 0.62-4.36 µm long.

111/1340: Serjania (230), Paullinia (195), Allophylus (1-250), Guioa (65), Cupaniopsis (60), Talisia (42), Cupania (50), Matayba (50). Pantropical.

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

• Sapindaceae are recognisable by their often spiral, pinnately-compound leaves with 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 branched, and the flowers are often borne in congested groups along the axes. The flowers are often rather small and are conspicuously hairy inside; the nectary is outside the staminal ring and there are often 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 little pocket in the seed coat which encloses the radicle is distinctive.

Evolution. Divergence & Distribution. Fossils ascribable to Sapindaceae are known from the later Cretaceous, while Cupaniopsis-type pollen is widespread in the fossil record, including from several sites in Africa, although Sapindaceae with this pollen are no longer found there (Coetzee & Muller 1984). 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). For the early Tertiary fossil history of what are now East Asian endemics, see Manchester et al. (2009).

All subfamilies of Sapindaceae diverged in the mid Cretaceous between (very approximately) 116-98 m.y., spreading initially from Laurasia, with South East Asia remaining an important area in the evolution of the family (Buerki et al. 2010c). The split between Acer and Dipteronia has been dated to (98-)78(-63.5) m.y.a. (Renner et al. 2007b).

For the biogeography of the family, in which much dispersal is involved, see Buerki et al. (2010c: methodological comparisons). Sapindaceae seem to have moved into New Caledonia ca 10 times or more, or there is yet a more complex pattern of movement to and from the island; the relatives of the Mauritian Cossinia pinnata (Dodonaeoideae) grow in the New Caledonian area (Buerki et al. 2012a). The very widespread Dodonaea viscosa has spread within the last two m.y. (Harrington & Gadek 2009).

Ecology. 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 and Fabaceae, are the major components of the viny vegetation of the Neotropics (e.g. Gentry 1991).

Pollination Biology. Species of Acer like A. rubrum are known for having very labile breeding systems. Renner et al. (2007b) studied breeding systems in the genus and found that dioecy evolved several times.

Chemistry, Morphology, etc. Aesculus has bud scales, Billia has naked buds, but both branch from the previous flush. "Ordinary-looking" stipules are known only from climbing species like Serjania, but leaflets looking like stipules (pseudostipules) occur elsewhere in the family.

Radlkofer (1892-1900) shows Serjania as having strongly obliquely symmetric 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. The petals of Sapindaceae are often rather complex, and have a similarly complex set of terms used to describe them. In Acer, the samaras are shown as being oblique by Schnizlein (1843-1870); Ronse de Craene (2010) depicts gynoecial orientation as varying within an inflorescence here.

Brizicky (1963) reported that the ovules may be epitropous; 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 integument, and that there was a definite funicle in 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. Turner et al. (2009) document a water gap near the hilum in the hard seeds of Dodonaea. It has been suggested that the base chromosome number for Sapindaceae is x = 7 (Ferrucci 1989).

For an early tribal classification, see Radlkofer (1890), for general accounts, see Radlkofer (1933 to 1934) and Acevedo-Rodríguez et al. (2011), for chemistry, see Hegnauer (1964, 1966, 1973, 1989, 1990, also under Aceraceae and Hippocastanaceae), for wood anatomy, see Klaassen (1999) and Agarwal et al. (2005), for epidermal features, see Cao and Xia (2008) and Pole (2010), for floral morphology of Koelreuteria, see Ronse Decraene et al. (2000b), of Handeliodendron, see Cao et al. (2008), of Acer, etc., see Leins and Erbar (2010), and of Xanthoceras, see Zhou and Liu (2012), for nectaries, which may have three vascular traces, see Solis and Ferucci (2009), for pollen, see Muller and Leenhouts (1976), for embryology, Nair and Joseph (1960) and Tobe and Peng (1990), for chromosome numbers, Lombello and Forni-Martens (1998), for chromosome size, see Ferrucci (1989), for fruits of Paullineae, see Weckerle and Rutishauser (2005), for seeds, see Guérin (1901), van der Pijl (1955) and Turner et al. (2009: germination).

Phylogeny. Preliminary studies suggested that Xanthoceras, with simply 5-merous, polysymmetric flowers (but eight stamens), ovules arranged in parallel (see also Magonia), and complex, golden nectaries borne outside the eight stamens, might be sister to all other Sapindaceae, general relationships being [Xanthoceras [[erstwhile Aceraceae + Hippocastanaceae] 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: information about secondary structure of ribosomal DNA, extensive sampling in Dodonaeoideae but no 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 with 70% bootstrap and ³95% posterior probability (see also Buerki et al. 2010a, 2010b, support still very low). Early morphological analyses (Judd et al. 1994) suggested a rather different set of relationships. For extensive phylogenetic studies of the family - 81 and 104 genera respectively - see Buerki et al. (2009, 2010b). For the phylogeny of Acer, see Li et al. (2006) and Renner et al. (2007b), and for that of Dodonaea, see Harrington and Gadek (2010), and for relationships around Cupania, see Buerki et al.(2012a).

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 Xanthoceras, as Xanthoceraceae) as families. For subfamilies, see Buerki et al. (2009). There is extensive polyphyly of the classically-recognized tribes (Buerki et al. 2010b), while generic limits in the Cupania group (Sapindoideae) are unclear (Buerki et al. 2012a).

Previous Relationships. Sapindaceae are chemically similar in some respects to Fabaceae, e.g. both have non-protein amino acids (for a summary, see Fowden et al. 1979), and both have compound leaves, but they are not closely related.

[Simaroubaceae [Rutaceae + Meliaceae]]: 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; papers in Waterman & Grundon 1983; Waterman 1983, 1993) and often have a bitter taste. For additional 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). For some information on carpel development, see van Heel (1983).

Hartl (1958) sugested that there were similarities betwreen Rutaceae and Simaroubaceae in fruit (endocarp) anatomy; he did not include other Sapindales in his comparison. Rutaceae and Simaroubaceae are both reported to have embryo sac haustoria (Mickesell 1990).

SIMAROUBACEAE Candolle, nom. cons.   Back to Sapindales

Trees or shrubs; bark very bitter, simaroubilide quassinoids, carboline alkaloids and canthinones [with tryptophane nucleus), ellagic acid +; wood often fluorescing; (nodes multilacunar); pith conspicuous, medullary secretory canals common; sclereids common, oil cells uncommon; (stomata paracytic); leaflet not articulated, vernation also supervolute-curved, margins coarsely toothed to entire, (stipules +, cauline - some Soulamea - or petiolar); breeding system various; (pedicel articulated), flowers rather small, <1 cm across, (3-)4-6(-8)-merous; K connate or free; A (4, 5, opposite sepals, with 4-5 staminodes or 0); tapetal cells 3-12-nucleate; gynophore short and stout/0, G 1-5(-8), ± postgenitally connate [/level], style short, branches short, recurved, or separate, often ± basal, (apex postgenitally connate), stigmas ± recurved, ± pointed, with elongated receptive zone, dry; ovule 1(-2)/carpel, (hemitropous), micropyle (bistomal? - Samadera) zig-zag, (inner integument very long, folded), outer integument 3-10 cells across, inner integument 2-8 cells across, parietal tissue 6-22 cells across, (tissue below e.s. massive, with central elongated cells - Samadera), nucellar cap 2-7 cells across; fruitlets separate; 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), (perisperm +, thin); 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; Trop. Afr. Fl. Pl. Ecol. Distr. 5. 2010; 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]

Picrasmeae

(Plant all thorny; leaves scales); (stipules cauline); fruits drupelets.

3/22. Southern U.S.A. to Argentina, 2 spp. Southeast Asia-Malesia.

The Rest: (leaves with flat surface glands); (K, C, 0); A 10<; fruits 1-seeded drupelets or samaras.

........

[Quassia [Samadera + Simarouba etc.]]: (filaments with with lateral or basal-adaxial scales); (style long, with separate canals).

• 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. Divergence & Distribution. The age of crown group Simaroubaceae has been estimated as some 52 m.y. (Muellner et al. 2007); better sampling suggested a rather older date in the Cretaceous-Maastrichtian of a little more than 65 m.y., however, most diversification has been in the Caenozoic (Clayton et al. 2009).

Fossil Ailanthus is widespread in the Eocene ca 52 m.y.a.; it has not been recorded from the Palaeocene (Corbett & Manchester 2004; see also Clayton et al. 2009: the fossil history of Leitneria and Chaneya, the latter not certainly Simaroubaceae). Fruits identified as Leitneria, a genus now endemic to the U.S.A., have recently been found in eastern Siberia (Ozerov 2012).

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 dispersal (and some extinction) needed to explain the current distribution of taxa (Clayton et al. 2009).

Chemistry, Morphology, etc. The quassinoids charactistic of Simaroubaceae replace other limonoids (Waterman 1993). The adult plant of Holacantha is basically a giant branched thorn system; the leaves are reduced to scales. Although the carpels may be ± free, there is often only a single style. The gynoecium of Leitneria is described as having a single carpel with two ovules, of which only one is fertile (Tobe 2011a). Even in taxa with unitegmic ovules, the axis of the embryo and that of the micropyle are offset at a sharp angle, hence the latter can be thought of as being zig-zag. There are reports of other than porogamous fertilisation in the family (c.f. Anacardioideae: Rao 1970).

For chemistry, see Hegnauer (1973, 1990, also 1966, 1989, as Leitneriaceae), and for other information, see Wiger (1935: embryology), Abbe (1974) and Tobe (2011a, 2013), inflorescence, floral morphology/anatomy and embryology of Leitneria, Fernando and Quinn (1992: pericarp anatomy), Jadin (1901) and Boas (1913), both vegetative anatomy, Webster (1936: wood anatomy), and Clayton (2011: general).

Phylogeny. The overall relationships, [Picrasma etc. [Ailanthus [Soulamea, etc. [Nothospondias* [Picrolemma [Quassia* [Samadera* + Simarouba etc.]]]]]]] are are mostly quite well supported, although support for the first clade is not that strong and for a couple of nodes along the backbone (the genera that might move have an asterisk) could be improved (Clayton et al. 2007a, esp. b; 2009). Leitneria is well embedded (Clayton et al. 2007b) and has embryological similarities with Brucea, in the same clade (Soulamea, etc.). Hence the demise of the only family previously thought to be restricted to the continental U. S. A. - alack! I have put in some phylogenetic structure above because of its effect on our understanding of character evolution.

The very poorly-known Gumillea (ex Cunoniaceae) might be in Simaroubaceae, although the stamens do not appear to have scales and there are many ovules per carpel - the latter feature in particular is rather odd for any putative sapindalean plant. It has stamens alternate with the petals, so making membership in Picramniales unlikely (and ovule number also militates against this).

• Leitneria: bark not bitter; leaves simple; wind pollinated; plant is more or less dioecious, flowers are much reduced and in short catkins, in staminate plants, at least, the units being cymules: C 0?; pollen reticulate; G 1, stigma decurrent; inner integument long, folded; testa multiplicative, mesotegmen with reticulate thickenings, only entotegmen persists; endosperm starchy.

Previous Relationships. Simaroubaceae have been very difficult to delimit, and molecular data suggest the excision of Suriana and its relatives (see Surianaceae: Fabales), Harrisonia (Rutaceae), and Picramnia and Alvaradoa (Picramniaceae: Picramniales) (e.g. Fernando et al. 1995).

Synonymy: Ailanthaceae J. Agardh, Castelaceae J. Agardh, Holacanthaceae Jadin, nom. inval., Leitneriaceae Bentham & J. D. Hooker, Quassiaceae Bertolini, Simabaceae Horaninow, Soulameaceae Pfeiffer

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

RUTACEAE Jussieu, nom. cons.   Back to Sapindales

Furanocoumarins, distinctive limonoids +; (vessel elements with scalariform perforation plates); libriform fibres +; wood often fluorescing; (nodes 1:1; cuticle waxes platelets, rodlets, etc.); stomata various; schizogenous cavities +; (leaves simple), leaflets usu. prominently punctate, (subopposite), usu. articulated, vernation also flat, margins entire to crenate (serrate); flowers often perfect; (3-)5-merous; K (2-4), connate or free, C (0-4), often valvate?, (connate); A (2-many in a single whorl), obdiplostemonous, filaments ± flattened; tapetal cells 2-4-nucleate, polyploid; (gynophore +); G (1 [2-)5(-many)], variously connate to almost free, style impressed to ± gynobasic, (stylar canals as many as carpels), (apex postgenitally connate), stigma (lobed), dry or wet; ovules 1-2/carpel, (apical), micropyle also bistomal, zig-zag; chalazal embryo sac haustoria +; seed with chalazal aperture in the sclerotesta at base or raphe [?Aurantioideae]; exotegmen tracheidal + (0); (endosperm +), (embryo curved); n = (7-)9(-11+).

161[list]/2070 - three groups below. Largely tropical.

1. Cneoroideae Webb

Woody; pyranochromones, (diterpenoid cneorubin; quassinoids; alkaloids [Dictyoloma]) +; schizogenous cavities 0 (+, e.g. Spathelia), oil cells commonly solitary; petiole bundle more or less cylindrical, of two opposed plates (arcuate - Bottegoa); stomata anomocytic to cyclocytic; solitary oil cells + (0), (schizogenous cavities 0); (leaves bicompound), (stipules and stipular thorns +); C valvate; A 4-5, (8-10 - Harrisonia), filaments ± flattened, with basal appendages; pollen reticulate; G (1-)3(-5), style with canals [Harrisonia]; ovules (-5/carpel), apotropous or epitropous, campylotropous, micropyle endostomal, outer integument ca 2 cells across, inner integument ca 3 cells across, parietal tissue 4-5 cells across, nucellar cap ca 2 cells across, hypostase +; fruit a loculicidal capsule, or the carpels opening adaxially and separating laterally and from columella, a winged drupe, or follicle; (testa multiplicative, exotestal cells large, outer walls thickened - Harrisonia); n = ?

7/35: Spathelia (20). The tropics, also N. Australia and the Mediterranean (Map: from Appelhans et al. 2012a; Australia's Virtual Herbarium xii.2012).

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

[Rutoideae + The Rest]: dihydrocinnamic acid derivates; (exine striate); outer integument 3-6 cells across, inner integument 2-5(-6) cells across, parietal tissue 5-12 cells across, nucellar cap several layered; (exotesta mucilaginous) (map: from Meusel et al. 1978; Brummitt 2007; Groppo et al. 2012).

2. Rutoideae Arnott

Herbs to trees; methylcarbazole alkaloids, distinctive flavonoids by polymethoxylation; (thorns +); (leaf rhachis winged), (leaflets alternate); C imbricate (valvate), clawed; G postgenitally united.

33/295: Northern Hemisphere to the Pacific, also Africa.

2A. Ruteae Dumortieae

Perennial herbs to shrubs (trees); C (fringed - Ruta); (G 1) postgenitally united, (gynophore +); fruit loculicidal-ventricidal (septicidal, with mericarps); (seeds reniform), (winged); n = 9, 10.

7/87: Haplophyllum (66). North (warm) temperate to tropical, some southern Africa, not the Antipodes or South America.

2B. Aurantieae Reichenbach

Shrubs to trees; methylcarbazole alkaloids, distinctive flavonoids by polymethoxylation; (thorns +); (leaf rhachis winged), (leaflets alternate); (A many); G postgenitally united; (ovules -many/carpel), (unitegmic - Glycosmis); fruit a ± dry berry with mucilaginous pulp directly from endocarp or multicellular hairs; exotesta mucilaginous, inner walls lignified, often fibrous, exo- and endotesta with crystal-containing cells; (nucellar polyembryony +), cotyledons thick, not folded (not Micromelum); n = 9.

26/206: Glycosmis (50), Amyris (40), Citrus (30). Indo-Malesia and the Pacific, also Africa.

Synonymy: Amyridaceae Kunth, Aurantiaceae Jussieu, Citraceae Roussel

The Rest

Woody; quinolone and acridone [derived from anthranilic acid] or furo-pyranoquinoline and -pyranoquinoline alkaloids, (limonoids 0); (distinctive tracheal veinlet endings); oil cells also commonly solitary; (leaves opposite), (stipules intrapetiolar/petiolar sheath - Metrodorea); flowers (vertically or obliquely monosymmetric); A (connate), (2, with basal anther appendages, + 3 staminodes - Angostura alliance), (obdiplostemonous); ([andro]gynophore +); (G 2+), (opposite sepals - Zanthoxylum), (styluli [marginal] +), (connate only at apex); carpels separating in fruit, (seeds winged; or forcibly expelled with endocarp); exotesta often mucilaginous, irregularly palisade, lignified or not, or fibrous and lignified, (mesotesta sclerotic), (sarcotesta +, lignified endotesta), meso-/endotesta thickened [Zanthoxylum], exotegmen with crossed lignification bars, or not [Skimmia], (meso- and endo- tegmen tracheidal); n = (7-)8-9(-11).

113/1740: Melicope (235), Zanthoxylum (225), Agathosma (150 +), Boronia (150), Vepris (80), Zieria (60), Acronychia (48), Conchocarpus (45). Pantropical, some (warm) Temperate. [Photo - Flower, Flower, Fruit.]

Synonymy: Boroniaceae J. Agardh, Dictamnaceae Vest, Diosmaceae Bartling, Diplolaenaceae J. Agardh, Flindersiaceae Airy Shaw, Fraxinellaceae Nees & Martius, Jamboliferaceae Martynov, Pilocarpaceae J. Agardh, Pteleaceae Kunth, Zanthoxylaceae Martinov

• 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. Divergence & Distribution. For the early Tertiary fossil history of what are now East Asian endemic Rutaceae, see Manchester et al. (2009); Gregor (1989) discussed Tertiary fossil seeds.

Crown Rutaceae have been dated to (87-)82(-74) m.y.a., crown Cneoroideae to (78-)74(-58) m.y.a., and crown [Rutoideae + The Rest] to (73-)70(-62) m.y.a. (Appelhans et al. 2012a). Another estimate for crown [Rutoideae + The Rest] is in the late Cretaceous ca (90-)74(-58) m.y.a. (Salvo et al. 2010: q.v. for more dates). For dates of diversification within Rutaceae, especially Aurantieae, see Pfeil and Crisp (2008; c.f. in part Muellner et al. 2007); the family is relatively young, and distributions are unlikely to be much affected by continental drift (but c.f. Kubitzki et al. 2011; Hartley 2001a, 2001b; Ladiges & Cantrill 2007).

Ca 250 species of Diosmeae are restricted to South Africa, largely to the Cape Floristic Region (Trinder-Smith et al. 2007). Melicope has a major radiation on Hawaii of 50+ species; the source area is likely to be in the general Australia-New Guinean region, and from Hawaii there seems to have been dispersal to the Marquesas Islands (Harbaugh et al. 2009b).

Appelhans et al. (2011: many original observations!) plotted a number of morphological characters on the tree, focussing on Cneoroideae; the clade is morphologically quite heterogeneous - like the rest of the family.

Plant-Animal Interactions. Rutaceae have exceptionally diverse secondary metabolites, some of which (essential oils, coumarins, etc.) are similar to those in Apiaceae, Asteraceae, Papaveraceae, etc. (Hegnauer 1971; Kubitzki et al. 2011), while their alkaloids are like those found in some magnoliids - and are produced via nine or more different biosynthetic pathways. Thus 1-benzyltetrahydroisoquinoline alkaloids are found in a small group of related Rutoideae, and also in Papaveraceae (and a couple of other families), which exercised phytochemists' imaginations in the past (Kubitzki et al. 2011).

Caterpillars of Papilionidae-Papilionini 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 will eat this family (Zakharov et al. 2004). Like the magnoliids, e.g. Aristolochiaceae, on which closely related Papilioninae are also found, it is the alkaloids that attract the butterflies. Rutaceae may have been the original food plants for Papilio, since even those species which now eat Magnoliales will eat Rutaceae if they have to (Zakharov et al. 2004, but c.f. Fordyce 2010; see also Berenbaum & Feeney 2008).

Seed Dispersal. The South African Diosmeae, as well as Boronia and relatives, (Australian), have seeds with elaiosomes that are endocarpial in origin and are dispersed by ants (Kubitzki et al. 2011).

Chemistry, Morphology, etc. Rutaceae as circumscribed here are a variable group. For their diverse secondary metabolites, see Hegnauer (1971) and Kubitzki et al. (2011). Da Silva et al. (1988) surveyed the secondary metabolites, suggesting that an overhaul of the infrafamilial classification was in order. Adsersen et al. (2007) noted the value of prenylated acetophenones as a marker for Xanthoxyleae (inc. Melicope, etc.), and Braga et al. (2012) the distinctive dihydrocinnamic acid derivates common in Rutoideae.

Prickles of Zanthoxylum can be in the stipular position.

Rutaceae are particularly variable in flower and fruit. Monosymmetry is scattered in the family, occurring in Dictamnus (relationships uncertain) 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 held in nature is unclear since the inflorescence can be pendulous and up to 1.5 m long. The flowers of Galipeinae (the Angostura alliance of Kubitzki et al. 2011), to which Erythrochiton (but not the tube-forming Correa) belongs, may have only two stamens plus staminodes, a connate corolla, filaments connate and forming a tube, or a tube formed by the serial adnation of filaments and petals; variation in gynoecial development is also considerable (Pirani & Menezes 2007; el Ottra et al. 2011, esp. 2013). 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. Wei et al. (2011) sugest that Rutaceae may plesiomorphically have five stamens.

Triphasia has G [3], the odd member being adaxial, and the same is true of Cneorum tricoccon, which has 3-merous flowers (see Caris et al. 2006 for floral development). 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 quite widespread. The endocarp divides periclinally during development (Hartl 1957), resulting in a pronounced layering of the mature capsule, especially in Rutoideae. 

For general information, see van der Ham et al. (1995), White and Styles (1966), and especially Kubitzki et al. (2011). For chemistry, see also Hegnauer (1973, 1990, also 1964, 1989 as Cneoraceae), Waterman and Grundon (1983), Mulholland et al. (2000, esp. Ptaeroxylaceae), and Yan et al. (2011: Harrisonia in particular), and for alkaloid chemistry, Waterman (1975, 1999). For wood anatomy of Cneoroideae, see Appelhans et al. (2012b: phylogenetic signal within the subfamily), for floral development, see Caris et al. (2006b: Cneorum), Zhou et al. (2002) and Wei et al. (2011), for floral orientation, see Eichler (1878), for gynoecial morphology, see Gut (1966), for ovules of Harrisonia, see Wiger (1935), and for fruit anatomy, see Brückner (1991). For the chalazal opening (?vascular bundle) in the seed, see Wilson (1998) and Hartley (2003). See also Dahlgren and van Wyk (1988), van der Ham et al. (1995) and White and Styles (1966) for information about Cneoroideae.

Phylogeny. In a two-gene analysis, the [[Spathelia + Dictyoloma] [[Cneorum + Ptaeroxylum] Harrisonia]] clade was sister to all other Rutaceae (Chase et al. 1999: the position of Harrisonia - sequences from only one gene - somewhat unclear; see also Groppo et al. 2008, 2012). 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 which it was then placed) 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 to Rutaceae was justified on both molecular and morphological grounds. Razafimandimbison et al. (2010) also found a weakly/moderately supported clade that included the old Ptaeroxylaceae and in which [Spathelia + Dictyoloma] are sister to the rest. Appelhans et al. (2011: denser sampling, five chloroplast genes, 2012a) again found this basic topology; support for the groups was strong, and within the two major clades in Cneoroideae, both strongly geographically circumscribed, Sohnreyia was sister to other neotropical taxa and Harrisonia sister to other palaeotropical taxa (Appelhans et al. 2012a). For this clade, see Cneoroideae above.

Hartley (e.g. 1981, 1997, 2001a, b) had suggested some generic realignments in Malesian-Pacific Rutaceae that largely ignored then then-conventional subfamilies; this work has since largely been confirmed by molecular data. Within core Rutaceae, [Aurantieae (distinctive fruit with fleshy hairs in the loculi; fibrous exotegmen; endosperm 0; x = 9) [Chloroxylon, Boenninghausenia, Ruta, Chloroxylon, etc. (Ruteae plus!)]] form a poorly to well-supported clade (e.g. Morton et al. 2003; Groppo et al. 2008, 2012; Salvo et al. 2010; Appelhans et al. 2012a). For relationships within the group, see Pfeil and Crisp (2008) and Bayer et al. (2009). Clauseneae may not be monophyletic (Morton 2009); Glycosmis and/or Micromelum may be sister to other Aurantieae (Groppo et al. 2012), and both have (1-)2 ovules/carpel. For subtribal relationships, see Morton (2009), for relationships around Citrus, see Scott et al. (2000), Samuel et al. (2001), Araújo et al. (2003), and Bayer et al. (2009), and for relationships in the Irano-Turanian Haplophyllum (Ruteae), which colonized the Mediterranean area more than once, see Salvo et al. (2011) and Manafzadeh et al. (2011).

Salvo et al. (2008, also 2010; Groppo et al. 2008, 2012) found that Dictamnus was widely separate from the other members that had been included in Ruteae, rather it linked with Casimoroa and Skimmia; the remaining Rutaceae form a clade sister to Dictamnus et al. (see Poon et al. 2007; Groppo et al. 2008, 2012; Salvo et al. 2010). Subfamilies other than Aurantioideae are variously mixed up in this group. One large clade is mostly Old World-Oceanian in distribution, although it includes the Chilean Pitavia (Groppo et al. 2012). It includes Flindersia and relatives, which have secretory cells in the stem only and septifragal capsules that are 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 to well supported clade perhaps forming a clade with the Flindersia group (Salvo et al. 2010; Groppo et al. 2012), and even with the [Zanthoxylum + Toddalia] clade (Groppo et al. 2012: support poor). Then there is another clade, includinbg the North American Ptelea, an African clade (for relationships in Diosmeae, see Trinder-Smith et al. (2007), and a largely Central and South American clade (for relationships in Galipeinae, see Kallunki & Groppo 2007), however, support for these groups, and of relationships between them, is again mostly rather weak (Groppo et al. 2012).

Classification. Although Cneoroideae (also called Spathelioideae in recent literature) form a fairly distinct group, inclusion within Rutaceae s.l. is reasonable (Groppo et al. 2008, 2012; Appelhans et al. 2011). Some of the fruit characters previously used to distinguish subfamilies in other Rutaceae are proving unreliable in delimiting major clades (e.g. see Hartley 1981; But et al. 2009), and tribal limits for the most part need overhauling (e.g. Salvo et al. 2008; Poon et al. 2008). For a tribal classification of Cneoroideae, see Appelhans et al. (2011), and for the beginnings of a classification of the rest of the family, see Groppo et al. (2012), but relationships are a little too uncertain as yet to know exactly what to do.

Kubitzki et al. (2011) noted that a quarter of the genera in the family are monotypic. Beyond this, generic limits are difficult, 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); the necessary nomenclatural changes are gradually being made.

Previous Relationships. Cronquist (1981) placed Cneoraceae in his Sapindales which included Rutrales here and then some; 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), although no reasons were given, Waterman (1993) noted that the genus contained no quassinoids.

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).

Botanical Trivia. Ehrlich and Raven (1964) predicted that Pteroxylon would be found to have alkaloids, based on the caterpillars that ate it - it has (e.g. Muscarella et al. 2008).

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 (articulated), (margins toothed); plants often dioecious, but flowers apparently perfect, (3-)5(-8)-merous; K often connate, (vascular trace single), A connate, 2 X C (5-30 in a single whorl); tapetal cells 2-4(-10)-nucleate; G (1) [2-6(-many)], postgenitally united, opposite C, style-head discoid or capitate (± lobed), hairy, stigma wet; ovules ?anatropous, (micropyle exo/bistomal), outer integument 2-5 cells across, inner integument 2-4 cells across, parietal tissue 3-9(-18) cells across, nucellar cap 3-5(-9) cells across, placental obturator common; megaspore mother cells often many; seeds often pachychalazal, coat vascularized, testa and/or tegmen multiplicative (not), testa undistinguished but thick, endotesta crystalliferous, (exotegmen fibrous [Trichilia, Swietenia]); embryo white; x ?= 6, 7.

50[list]/615 - 2 groups below. Pantropical, but largely Old World; plants of the lowlands (map: see Wickens 1976; Pennington 1981; FloraBase 2006; Flora of China 11. 2008; GBIF x.2009; Trop. Afr. Fl. Pl. Ecol. Distr. 6. 2011).

1. Melioideae Arnott

(Suckering shrublets); buds naked; (nodes 3:3); (leaves two-ranked - Turraea), (simple; bipinnate); C (-14; connate); (style hollow); ovules 1-3(-many)/carpel; fruit a loculicidal capsule, (berry, drupe, nut); seeds usu. with aril [funicular in Naregamia] or sarcotesta, (dry, winged - Quivisianthe); (embryo green - Trichilia), (endosperm +); n = 8, 11, 12, 14, 15, 18 ... 140.

36/558. Aglaia (120), Dysoxylum (80), Trichilia (70), Turraea (60), Chisocheton (50), Guarea (50). Pantropical, but largely Old World.

Synonymy: Aitoniaceae R. A. Dyer, nom. illeg.

2. Cedreloideae Arnott

Buds with scales (naked - Capuronianthus); (leaves opposite); (C connate); (A at least partly free); (nectary 0); ovules (2 [Capuronianthus]) 3-many/carpel, collateral; fruit a septifragal capsule, valves falling off, columella persisting, (columella slight); seeds winged, (not winged, with massive woody or corky testa); n = 13, 18, 23, 25, 26, 28.

14/56: Cedrela (14). Pantropical, but largely Old World. [Photo - Flower, Fruit.]

Synonymy: Cedrelaceae R. Brown, Swieteniaceae E. D. M. Kirchner

• 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 the mouth of which is blocked by the large stigma. The fruits and seeds are usually quite large. [Photo - Flower, Fruit.]

Evolution. Divergence & Distribution. Muellner et al. (2006) discussed the biogeography of the family, suggesting its origin in Africa and subsequent dispersal; the family is ca 85-76 m.y. old, diversification within it beginning ca 75-67.5 m.y.a.. For fossil Meliaceae, see Mabberley (2011). For the biogeography of Aglaia, see Muellner et al. (2008b).

Although only a small family, Meliaceae make up 17% of all trees ³10 cm bole diameter in Sumatra (Mabberley 2011).

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

Animal dispersal is common in Meliodeae; for detailed studies of the dispersal of arillate-type seeds of Malesian Aglaia, see Pannell and Koziol (1987). Wind dispersal is common in Cedreloideae.

Vegetative Variation. Munronia is ± herbaceous. 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). The leaves of Chisocheton can be rooted (Fisher & Rutishauser 1990), and then they continue to grow for a long time, although I do not know that a tree has ever been produced from a leaf. Species of Chisocheton such as C. pohlianus have an epiphyllous inflorescence, flowers appearing between the leaflets; specimens have been misidentified as Rubiaceae! Capuronianthus (Swietenioideae) has opposite, compound leaves, while the simple-leaved Vavaea and Turraea (both Melioideae) look rather unmeliaceous except when in flower; the leaves of the latter genus may even be two-ranked and lack articulations.

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. Sieve tube plastids with protein crystalloids and starch occur in Melia and Azederach. Gouvêa et al. (2008b) draw the flowers of Swietenia as being inverted; carpellate flowers are the first to be produced in the cymose inflorescences. There is considerable variation in seed development (e.g. Wiger 1935; Corner 1976), even within the subfamilies, and this will have to be integrated with the phylogeny as it develops.

For chemistry, see Hegnauer (1969, 1990) and Mulholland et al. (2000), for embryology, etc., see Wiger (1935), Paetow (1931), and N. C. Nair (1962, 1970 and references), and for general information, see Mabberley et al. (1995: esp. Malesia) and Mabberley (2011).

Phylogeny. Cedreloideae (Swietenioideae) and Melioideae are clearly monophyletic (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 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 Capuronianthus, are embedded in Melioideae and Cedreloideae 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), in Chisocheton, see Fukuda et al. (2003), and in Neotropical Cedreleae, see Muellner et al. (2009).

Classification. Cedreloideae used to be called Swietenioideae. 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).

Thanks. I am grateful to David Kenfack for useful information.