EMBRYOPSIDA Pirani & Prado

Gametophyte dominant, independent, multicellular, thalloid, with single-celled apical meristem, showing gravitropism; rhizoids +, unicellular; flavonoids + [absorbtion of UV radiation]; chloroplasts lacking pyrenoids; protoplasm dessication tolerant [plant poikilohydric]; cuticle +; cell walls with (1->4)-ß-D-glucans [xyloglucans], lignin +; several chloroplasts per cell; glycolate metabolism in leaf peroxisomes [glyoxysomes]; centrioles in vegetative cells 0, metaphase spindle anastral, predictive preprophase band of microtubules, phragmoplast + [cell wall deposition spreading from around the spindle fibres], plasmodesmata +; antheridia and archegonia jacketed, stalked; spermatogenous cells monoplastidic, centrioles develop de novo, associated with basal bodies of flagellae, multilayered structure +, proximal end of basal bodies lacking symmetry, stellate pattern associated with doublet tubules of transition zone; spermatozoids with a left-handed coil; male gametes with 2 lateral flagellae; oogamy; sporophyte dependent on gametophyte, embryo initially surrounded by haploid gametophytic tissue, plane of first division horizontal [with respect to long axis of archegonium/embryo sac], suspensor/foot +, cell walls with nacreous thickenings; sporophyte multicellular, with at least transient apical cell [?level], sporangium +, single, dehiscence longitudinal; meiosis sporic, monoplastidic, microtubule organizing centre associated with plastid, cytokinesis simultaneous, preceding nuclear division, sporocytes 4-lobed, with a quadripolar microtubule system; spores in tetrads, sporopollenin in the spore wall, wall with several trilamellar layers [white-line centred layers, i.e. walls multilamellate]; close association between the trnLUAA and trnFGAA genes on the chloroplast genome.

Many of the bolded characters in the characterization above are apomorphies of subsets of streptophytes along the lineage leading to the embryophytes, not apomorphies of crown-group embryophytes per se.

All groups below are crown groups, nearly all are extant; characters mentioned are those of the common ancestor of the group.

STOMATOPHYTES

Abscisic acid, ?D-methionine +; sporangium with seta, seta developing from basal meristem [between epibasal and hypobasal cells], sporangial columella + [developing from endothecial cells]; stomata +, anomocytic, cell lineage that produces them with symmetric divisions [perigenous]; underlying similarities in the development of conducting tissue and in rhizoids/root hairs; spores trilete; polar transport of auxins and class 1 KNOX genes expressed in the sporangium alone; MIKC, MI*K*C* and class 1 and 2 KNOX genes, post-transcriptional editing of chloroplast genes; gain of three group II mitochondrial introns.

[Anthocerophyta + Polysporangiophyta]: archegonia embedded/sunken in the gametophyte; sporophyte long-lived, chlorophyllous; sporophyte-gametophyte junction interdigitate, sporophyte cells showing rhizoid-like behaviour.

POLYSPORANGIOPHYTA†

Sporophyte branched, branching apical, dichotomous; sporangia several; spore walls not multilamellate [?here].

EXTANT TRACHEOPHYTA / VASCULAR PLANTS

Photosynthetic red light response; water content of protoplasm relatively stable [plant homoiohydric]; control of leaf hydration passive; (condensed or nonhydrolyzable tannins/proanthocyanidins +); sporophyte soon independent, dominant, with basipetal polar auxin transport; vascular tissue +, sieve cells + [nucleus degenerating], tracheids +, in both protoxylem and metaxylem; endodermis +; root xylem exarch [development centripetal]; stem with an apical cell; branching dichotomous; leaves spirally arranged, blades with mean venation density 1.8 mm/mm2 [to 5 mm/mm2]; sporangia adaxial on the sporophyll, derived from periclinal divisions of several epidermal cells, wall multilayered [eusporangium]; columella 0; tapetum glandular; gametophytes exosporic, green, photosynthetic; stellate pattern split between doublet and triplet regions of transition zone; placenta with single layer of transfer cells in both sporophytic and gametophytic generations, embryonic axis not straight [root lateral with respect to the longitudinal axis; plant homorhizic].

[MONILOPHYTA + LIGNOPHYTA]

Branching ± indeterminate; lateral roots +, endogenous, root apex multicellular, root cap +; tracheids with scalariform-bordered pits; leaves with apical/marginal growth, venation development basipetal, growth determinate; sporangia borne in pairs and grouped in terminal trusses, dehiscence longitudinal, a single slit; cells polyplastidic, microtubule organizing centres not associated with plastids, diffuse, perinuclear; male gametes multiflagellate, basal bodies staggered, blepharoplasts paired; chloroplast long single copy ca 30kb inversion [from psbM to ycf2].

LIGNOPHYTA†

Plant woody; lateral root origin from the pericycle; branching lateral, meristems axillary; cork cambium + [producing cork abaxially], vascular cambium bifacial [producing phloem abaxially and xylem adaxially].

EXTANT SEED PLANTS / SPERMATOPHYTA

Plant evergreen; nicotinic acid metabolised to trigonelline, (cyanogenesis via tyrosine pathway); primary cell walls rich in xyloglucans and/or glucomannans, 25-30% pectin [Type I walls]; lignins derived from (some) sinapyl and particularly coniferyl alcohols [hence with p-hydroxyphenyl and guaiacyl lignin units, so no Maüle reaction]; root stele with xylem and phloem originating on alternate radii, not medullated [no pith], cork cambium deep seated; arbuscular mycorrhizae +; shoot apical meristem interface specific plasmodesmatal network; stem with vascular cylinder around central pith [eustele], phloem abaxial [ectophloic], endodermis 0, xylem endarch [development centrifugal]; wood homoxylous, tracheids and rays alone, tracheid/tracheid pits circular, bordered; mature sieve tube/cell lacking functioning nucleus, sieve tube plastids with starch grains; phloem fibres +; stem cork cambium superficial; leaves with single trace from vascular sympodium [nodes 1:1]; stomatal pore with active opening in response to leaf hydration, control by abscisic acid, metabolic regulation of water use efficiency, etc.; leaves with petiole and lamina, development basipetal, blade simple; branches axillary (buds not associated with all leaves), exogenous; prophylls two, lateral; plant heterosporous, sporangia borne on sporophylls; microsporophylls aggregated in indeterminate cones/strobili; true pollen +, grains mono[ana]sulcate, exine and intine homogeneous; ovules unitegmic, parietal tissue 2+ cells across, megaspore tetrad linear, functional megaspore single, chalazal, lacking sporopollenin, megasporangium indehiscent; pollen grains landing on ovule; gametophytes dependent on sporophyte; male gametophyte development initially endosporic, tube developing from distal end of grain, gametes two, developing after pollination, with cell walls; female gametophyte endosporic, initially syncytial, walls then surrounding individual nuclei; seeds "large" [ca 8 mm3], but not much bigger than ovule, with morphological dormancy; embryo cellular ab initio, endoscopic, plane of first cleavage of zygote transverse, suspensor +, short-minute, embryonic axis straight [shoot and root at opposite ends; plant allorhizic], white, cotyledons 2; plastid transmission maternal; ycf2 gene in inverted repeat, whole nuclear genome duplication [zeta duplication], two copies of LEAFY gene, PHY gene duplications [three - [BP [A/N + C/O]] - copies], nrDNA with 5.8S and 5S rDNA in separate clusters; mitochondrial nad1 intron 2 and coxIIi3 intron and trans-spliced introns present.

ANGIOSPERMAE / MAGNOLIOPHYTA

Lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, apigenin and/or luteolin scattered, [cyanogenesis in ANITA grade?], S [syringyl] lignin units common [positive Maüle reaction - syringyl:guaiacyl ratio more than 2-2.5:1], and hemicelluloses as xyloglucans; root apical meristem intermediate-open; root vascular tissue oligarch [di- to pentarch], lateral roots arise opposite or immediately to the side of [when diarch] xylem poles; origin of epidermis with no clear pattern [probably from inner layer of root cap], trichoblasts [differentiated root hair-forming cells] 0, exodermis +; shoot apex with tunica-corpus construction, tunica 2-layered; reaction wood ?, associated gelatinous fibres [g-fibres] with innermost layer of secondary cell wall rich in cellulose and poor in lignin; starch grains simple; primary cell wall mostly with pectic polysaccharides, poor in mannans; tracheid:tracheid [end wall] plates with scalariform pitting, wood parenchyma +; sieve tubes enucleate, sieve plate with pores (0.1-)0.5-10< µm across, cytoplasm with P-proteins, cytoplasm not occluding pores of sieve plate, companion cell and sieve tube from same mother cell; sugar transport in phloem passive; nodes 1:?; stomata brachyparacytic [ends of subsidiary cells level with ends of pore], outer stomatal ledges producing vestibule, reduction in stomatal conductance to increasing CO2 concentration; lamina formed from the primordial leaf apex, margins toothed, development of venation acropetal, overall growth ± diffuse, venation hierarchical-reticulate, secondary veins pinnate, veins (1.7-)4.1(-5.7) mm/mm2, endings free; most/all leaves with axillary buds; flowers perfect, pedicellate, ± haplomorphic, parts spiral [esp. the A], free, numbers unstable, development in general centripetal; P +, members each with a single trace, outer members not sharply differentiated from the others, not enclosing the floral bud; A many, filament not sharply distinguished from anther, stout, broad, with a single trace, anther introrse, tetrasporangiate, sporangia in two groups of two [dithecal], ± embedded in the filament, with at least outer secondary parietal cells dividing, each theca dehiscing longitudinally, endothecium +, endothecial cells elongated at right angles to long axis of anther; (tapetum glandular), cells binucleate; microspore mother cells in a block, microsporogenesis successive, walls developing by centripetal furrowing; pollen subspherical, tectum continuous or microperforate, ektexine columellate, endexine +, thin, compact, lamellate only in the apertural regions; nectary 0; carpels present, superior, free, several, ascidiate, with postgenital occlusion by secretion, stylulus short, hollow, cavity not lined by distinct epidermal layer, stigma ± decurrent, carinal, dry [not secretory]; ovules few [?1]/carpel, marginal, anatropous, bitegmic, micropyle endostomal, outer integument 2-3 cells across, often largely subdermal in origin, inner integument 2-3 cells across, often dermal in origin, parietal tissue 1-3 cells across [crassinucellate], nucellar cap?; megasporocyte single, hypodermal, functional megaspore, chalazal, lacking cuticle; female gametophyte four-celled [one module, nucleus of egg cell sister to one of the polar nuclei]; supra-stylar extra-gynoecial compitum +; ovule not increasing in size between pollination and fertilization; pollen grains landing on stigma, bicellular at dispersal, mature male gametophyte tricellular, germinating in less than 3 hours, pollination siphonogamous, tube elongated, growing between cells, growth rate (20-)80-20,000 µm/hour, apex of pectins, wall with callose, lumen with callose plugs, penetration of ovules via micropyle [porogamous], whole process takes ca 18 hours, distance to first ovule 1.1-2.1 mm; male gametes lacking cell walls, flagellae 0, double fertilization +, ovules aborting unless fertilized; P deciduous in fruit; seed exotestal, much larger than ovule at time of fertilization; endosperm diploid, cellular, heteropolar [micropylar and chalazal domains develop differently, first division oblique, micropylar end initially with a single large cell, divisions uniseriate, chalazal cell smaller, divisions in several planes], copious, oily and/or proteinaceous; dark reversal Pfr → Pr; Arabidopsis-type telomeres [(TTTAGGG)n]; 2C genome size 1-8.2 pg [1 pg = 109 base pairs], whole nuclear genome duplication [epsilon duplication]; protoplasm dessication tolerant [plant poikilohydric]; ndhB gene 21 codons enlarged at the 5' end, single copy of LEAFY and RPB2 gene, knox genes extensively duplicated [A1-A4], AP1/FUL gene, paleo AP3 and PI genes [paralogous B-class genes] +, with "DEAER" motif, SEP3/LOFSEP and three copies of the PHY gene, [PHYB [PHYA + PHYC]].

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

[AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]: 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 +; sesquiterpene synthase subfamily a [TPS-a] [?level], polyacetate derived anthraquinones + [?level]; outer epidermal walls of root elongation zone with cellulose fibrils oriented transverse to root axis; P more or less whorled, 3-merous [possible position]; pollen tube growth intra-gynoecial; embryo sac bipolar, 8 nucleate, antipodal cells persisting; endosperm triploid.

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

[CERATOPHYLLALES + EUDICOTS]: ethereal oils 0.

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

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

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

[BUXALES + CORE EUDICOTS]: ?

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

[ROSIDS ET AL. + ASTERIDS ET AL.] / PENTAPETALAE: root apical meristem closed; (cyanogenesis also via [iso]leucine, valine and phenylalanine pathways); flowers rather stereotyped: 5-merous, parts whorled; P = calyx + corolla, the calyx enclosing the flower in bud, sepals with three or more traces, petals with a single trace; stamens = 2x K/C, in two whorls, internal/adaxial to the corolla whorl, alternating, (numerous, but then usually fasciculate and/or centrifugal); pollen tricolporate; G [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; (monosymmetric flowers with adaxial/dorsal CYC expression).

[DILLENIALES [SAXIFRAGALES [VITALES + ROSIDS s. str.]]]: 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.

Age. Suggestions for the age of this node are (88-)71(-63) m.y. (N. Zhang et al. 2012; see also Xue et al. 2012), (102-)96(-90) and (80-)76(-72) m.y. (Hengchang Wang et al. 2009), ca 98.25 m.y. (Magallón & Castillo 2009) and around 93.6-89.9 m.y. (Naumann et al. 2013).

Evolution. 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.

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

Phylogeny. Relationships between the malvid clades are somewhat uncertain. The clade [Malvales + Sapindales] may be sister group to Brassicales (Soltis et al. 2000; Peng et al 2003: both weak support; Bell et al. 2010), and Endress and Matthews (2006) note that there are some features perhaps more common in these first two families than elsewhere in this affinity. Other studies suggest that [Malvales + Sapindales] may be sister to [Brassicales + Tapisciales] (Soltis et al. 2007a: support weak for the latter pair; Bell et al. 2010). Although Bausher et al. (2006) in an analysis of whole chloroplast genomes found strong support for the clade [Brassicales + Malvales], only one species from the three larger orders and no Huerteales were included (see also S.-B. Lee et al. 2006: sampling even more exiguous; 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), when describing his Gerrardinaceae, found that Huerteales (Perrottetia not included), Brassicales and Malvales formed a polytomy, the combined group being rather poorly supported as sister to Sapindales, while Worberg et al. (2007b, 2009) recovered the relationships [Sapindales [Huerteales [Brassicales + Malvales]]], with strong support, and they found that each of the four orders was monophyletic. In studies including the mitochondrial matR gene, although the malvid clade was recovered, relationships within it were unclear (Zhu et al. 2007). I follow Worberg et al. (2009).

SAPINDALES Berchtold & J. Presl  Main Tree.

Interesting secondary compounds, ethereal oils, myricetin +; (secretory cells/tissue +); 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); (pollen 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, 6095 species.

Age. The age of crown-group Sapindales was variously estimated as 117.4, 104.9, and 90.5 m.y. (Muellner et al. 2007: c.f. topology).

Note: Possible apomorphies are in bold. However, the actual level at which many of these features, particularly the more cryptic ones, should be assigned is unclear. This is partly because many characters show considerable homoplasy, in addition, basic information for all too many is very incomplete, frequently coming from taxa well embedded in the clade of interest and so making the position of any putative apomorphy uncertain. Then there is the not-so-trivial issue of how ancestral states are reconstructed (see above).

Evolution. Divergence & Distribution. 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. A notable diversity of monoterpene synthase genes have been found in Sapindales studied, and the products of these genes may be involved either directly in plant defence, or indirectly by signalling to parasitoids of herbivores, but studies of these genes are currently only preliminary (Zapata & Fine 2013 and references). 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) note some floral developmental features found widely in this clade. Inconspicuous oblique monosymmetry may be common in the order, although many Sapindaceae, for example, are more strongly monosymmetric. The flowers are often imperfect, but since staminate and carpellate flowers have well-developed pistillodes and staminodes respectively, they can be difficult to distinguish. The rather uncommon feature of floral tubes that are formed by connate or closely adpressed and flattened filaments occur throughout Meliaceae, in a number of Rutaceae, and in Boswellia dioscorides (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.

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, albeit poorly supported, suggest the 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 early placed Biebersteinia, ex Geraniaceae, in Sapindales, albeit with a long branch (Bakker et al. 1998). Its herbaceous habit is rather unusual for Sapindales, but its ethereal oils (no oxygenated sequiterpenes, high proportion of aliphatic hydrocarbons - Bate Smith 1973; Greenham et al. 2001), single ovule/carpel, etc., are all congruent with a position here.

Previous Relationships. In the past Bretschneideraceae and Akaniaceae (= Akaniaceae, see Brassicales here) have been associated with Sapindales, Bretschneidera in particular looking very like a member of Sapindaceae; at the time, 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 - Burseranae Doweld, Rutanae Takhtajan, Sapindanae Doweld - Aceropsida Endlicher, Aesculopsida Brongniart, Rutopsida Meisner - Rutidae Doweld

BIEBERSTEINIACEAE Schnitzlein   Back to Sapindales

Biebersteiniaceae

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.]

Age. The age of crown-group Biebersteiniaceae is estimated as 63.3-54.8 m.y. (Muellner et al. 2007).

Chemistry, Morphology, etc. At least some species of Biebersteinia are foul-smelling.

The ante-petalous stamens are longest. Takhtajan (1997) described the ovules as being unitegmic. The exotegmen of Biebersteinia is rather like that of Vivianaceae (both Geraniales), especially when young, since both exotesta and endotegmen are tanniniferous (Boesewinkel 1988, 1997).

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

Biebersteinia is little known.

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

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

Age. The age of this node was estimated to be around (66-)63(-60) or (73-)71(-69) m.y., two penalized likelihood dates (Hengchang Wang et al. 2009: c.f. topology).

NITRARIACEAE Lindley   Back to Sapindales

Nitrariaceae

Annual to perennial herbs to shrubs; mycorrhizae absent [Peganum]; -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 15, with antepetalous staminal pairs, filament bases broad, flattened, [Nitraria, Peganum), or flower (3-)4-merous; A 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 loculicidal capsule, or 1-seeded drupe, 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; Fl. Austral. vol. 26. 2013). [Photo - Flowers.]

Age. The age of crown-group Nitrariaceae is around 96.5, 86.1, or 57.7 m.y. (Muellner et al. 2007).

Evolution. Divergence & Distribution. Given the phylogeny of the family, the distinctive flowers of Tetradiclis may be derived.

Chemistry, Morphology, etc. The variation in this group is rather puzzling. However, Bachelier et al. (2011) discuss floral morphology in detail, attempting to clarify features like androecial morphology that had been interpreted in various ways in earlier literature.

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 placed in an expanded Zygophyllaceae (Cronquist 1981), while Takhtajan (1997) included the genera in Nitrariaceae as three separate families in his Zygophyllales. Zygophyllales-Zygophyllaceae here are not remotely close to Nitrariaceae.

Synonymy: Peganaceae Takhtajan, Tetradiclidaceae Takhtajan

[[Kirkiaceae [Anacardiaceae + Burseraceae]] [Sapindaceae [Simaroubaceae [Rutaceae + Meliaceae]]]]: wood silicified or with SiO2 grains in all major families [esp. Anacardiaceae and Burseraceae]; tension wood +; persistent floral apex in the center of the gynoecium [?this level]; ovules 2/carpel, superposed, micropyle endostomal, inner integument elongated, S- or Z-shaped, nucellar cap +.

Age. Wikström et al. (2001) dated this node to (66-)62-57(-53) m.y. and Bell et al. (2010) suggested an age of around (75-)71(-70) m.y.; about 61.75 m.y. is the age in Naumann et al. (2013).

[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.

Age. The age of this node is somewhere around 93.6, 83.6 or 74.1 m.y. (Muellner et al. 2007), or (127-)116(-105) m.y. (Weeks et al. 2014).

Evolution. Ecology & Physiology. All families in this clade (bar Kirkiaceae) are common tress at least 10 cm across in Amazonian forests and have at least one of the 227 species that make up half the stems in Amazonian forests (for a total of 24 species; ter Steege et al. 2013).

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

Kirkiaceae

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).

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 inflorescence branches have carpellate 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 (Cronquist 1983, but with some doubt) or near Simaroubaceae (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.

Age. Bell et al. (2010) suggested that the two families diverged (73-)64(-56) or (51-)50(-49) m.y.a., while Wikström et al. (2001) gave ages of (56-)51, 47(-42) m.y. and Weeks et al. (2014) ages of (121-)108(-95) m.y.; a mere 37.7 m.y. is the age in Naumann et al. (2013).

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

Evolution. Divergence & Distribution. Weeks et al. (2014) compared the path of evolution in Burseraceae and Anacardiaceae, clades of the same age and about the same size, noting the comparatively greater diversity of fruit morphologies and expanded climatic tolerances in the latter (see also Donoghue & Edwards 2014 for biome shifts).

Chemistry, Morphology, etc. Anacardiaceae like Pachycormus have thin, brown, flaking bark that looks quite like that of 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 Anacardioideae, as by Pell (2004: Campnosperma 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

Anacardiaceae

Trees or shrubs; 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; (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), 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.

80[list]/873. Tropical, also temperate (map: from Heywood 1976; modified by Barkley 1937; Fl. Austral. vol. 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, but this will almost certainly have to change. [Photo - Flower, Fleshy fruit, Dry fruits.]

Age. Estimates of ages of crown-group Anacardiaceae are 72.7, 65.2, and 54.8 m.y. (Muellner et al. 2007), or (128-)97(-83) m.y. (Weeks et al. 2014).

1. Spondioideae Takhtajan

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

20/138: Lannea (40). Tropical.

Synonymy: Spondiadaceae Martynov

2. Anacardioideae Takhtajan

(Vines; perennial herbs); exudate gums and resins, 5-deoxyflavonoids, also alkylcathechols and alkylresorcinols [phenols with unsaturated side chains - allergenic] +; leaves (opposite), (simple); (flowers monosymmetric); K and/or C (0), K and C single trace [Toxicodendron]; A (1 [+ staminodes]), 5 [opposite sepals], 10 (many), (basally connate); tapetal cells bi- or polynucleate; G 1 [pseudomonomerous?], [3(-6)], (inferior), (highly) asymmetric, one carpel fertile (2 - Campnosperma), symplicate zone?, style also 1, (stigma punctate); ovule apical to basal, (unitegmic, nucellus apex exposed - Pistacia), nucellus 6-11 cells across, funicle massive, with outgrowths - Pistacia, Toxicodendron, etc.); (chalazogamy + - Pistacia, Toxicodendron, etc.); drupe often asymmetric, ± flattened, (K much accrescent, fruit a samara), (hypocarp developed); exocarp thin, epidermis lignified, endocarp with up to three layers of palisade lignified sclereids, internal to these a crystalliferous layer [= stratified], (not), (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

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).

Weeks et al. (2014) emphasized the diversity of fruit dispersal types in the family, the amount of dispersal, and they also noted that the ability to live in cooler (i.e. with some freezing) conditions has evolved here.

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), the sometimes massive, spherical galls producing terpenes that dissuade goats, at least, from eating them (Rostás et al. 2013), and aphid galls form on other Anacardiaceae (Wool 2004). 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 here. Branching in Anacardium may occur on the current flush.

Hardly surprisingly, 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). In Pistacia, at least, the fruit develops well before the seed, so for some time it appears almost empty (Copeland 1955).

For general information, see Ding Hou (1978), Pell et al. (2011) and Michell et al. (2006); Pell (2004) covered the morphology of the whole family in a phylogenetic context. For general chemistry, see Young (1976), for chemistry of Julianaceae, see Hegnauer (1966, 1989), for exudates, see Lambert et al. (2013), for wood anatomy, see Gupta and Agarwal (2008), for floral morphology, Wannan and Quinn (1991), for some embryology, see Grimm (1912), Copeland and Doyel (1940) and Copeland (1955), for fruit anatomy, Wannan and Quinn (1990), for ovules, fruit and seed, see von Teichman and van Wyk (1988 and references), and for seed anatomy, see von Teichman (1991, 1994, and references).

Phylogeny. Spondiadoideae-Spondiadeae and some Rhoeeae, including Pegia, Tapirira and Cyrtocarpa (see Aguilar-Ortigosa & Sosa 2004; Pell 2004) have been recovered as sister to the rest of the family. However, the situation is now rather complicated. Buchanania in some analyses is quite well supported as sister to other Anacardioideae (Aguilar-Ortigosa & Sosa 2004; Wannan 2006), consistent both with its chemistry, endocarp anatomy (it lacks a stratified endocarp), carpel number of 4-6, and different position of the fertile carpel, but its phylogenetic position is not fixed in other analyses (Pell & Mitchell 2007, c.f. abstract). Campnosperma, initially 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; it was not sequenced by Pell (2004). Pell et al. (2011) suggest that Spondiadoideae may be polyphyletic. Indeed, Weeks et al. (2014) found that Spondiadoideae were paraphyletic, Campnosperma being between the two parts, Buchanania ending up sister to one of those parts, and Pentaspadon was sister to the whole family - however, support was not strong.

In the remainder of the family, there are four main clades, with [Dobinaea + Campylopetalum] sister to the whole lot, support for the scaffolding is quite good (Weeks et al. 2014). In the old Anacardioideae (Pell & Urbatsch 2000, 2001) wind-dispersed taxa do not form a single group (Pell & Mitchell 2007, c.f. Pell & Urbatsch 2001).

Classification. See Mitchell et al. (2006) for a list of genera; Pell et al. (2011) included 21 genera in their polyphyletic Spondiadoideae. Buchanania and Campnosperma are included in Anacardioideae above, and this robs the subfamily of much in the way of apomorphies, but obviously the current classification is decidedly temporary. For the limits of Rhus, which seem best narrowly drawn (i.e., restricted to ca 35 species), see Yi et al. (2006 and references).

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 +; pith cells heterogeneous; nodes usu. 5:5; sclereids in stem; 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, with columella, stone with valves, K deciduous; (exotesta with shortly radially elongate but unthickened cells), endotesta lignified, ± tracheidal; embryo reserves hemicellulosic.

19[list]/755: four groups below. Tropical. [Photos - Leaf, Flower, Fruit.]

Age. De-Nova et al. (2012) dated crown-group Burseraceae to the early Palaeocene (69.7-)64.9(-60.3) m.y.a.; the estimate in Weeks et al. (2005: n.b. in text as the divergence between Anacardiaceae and Burseraceae) is (61.9-)60(-58.1) m.y.a. and in Weeks et al. (2014) the age is (106-)91(-78) m.y.a.; an age of 120 m.y. plus can be estimated from the discussion in Becerra (2005).

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

1. Beiselieae Thulin, Beier & Razafimandimbison

Plant deciduous; (vessel elements with scalariform perforation plates); 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).

Bursereae

[Garugeae [Bursereae + Protieae]]: (plant deciduous); oleoresins with mono- and bicyclic monoterpenes, triterpenes with ursane and oleanane components; (pith cells not heterogeneous); petiole bundle with medullary strands, (not); snail glands + [curled ± uniseriate glandular hairs]; (K with single trace); A (apparently in a single whorl), tapetal cells binucleate; (pollen psilate); 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 cells across (?0); pyrenes usu. with pericarpial pseudo-aril, mesocarp quite frequently splits down loculicidal radius, or fruit indehiscent, seeds embedded in ± fleshy pericarp; drupe often angled; vascular bundle in outer integument; cotyledons straight to variously folded, entire to palmately lobed.

18/754. 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.).

Age. The crown-group age of this clade can be dated to (60.2-)58(-55.8) m.y. (Weeks et al. 2005) or (66.5-)63.4, 54.2(-48.8) m.y. (Fine et al. 2014), but some (116-)98, 92.7(-74.8) m.y. (Becerra et al. 2012: rather older in Becerra 2003, 2005).

2. Garugeae Marchand

(Cork cambium deeper - Santiria); (leaves deciduous), (leaflets not pulvinate), ("stipules" petiolar or cauline, laciniate to entire); dioecious, or flowers perfect; flowers often 3-merous, (hypanthium +); (C connate); (A connate - Canarium); (pollen striate); fruit often not dehiscent, (pyrenes winged); if germination hypogeal, often phanerocotylar; n = 13, 22-24.

11/275: Canarium (120), Dacryodes (70). Tropical, esp. Old World.

[Bursereae + Protieae]: ?

Age. The age of this node can be dated to (66.8-)63.2, 48.6(-46) m.y. (Fine et al. 2014).

3. Bursereae de Candolle

(Petiole bundle arcuate - Commiphora); (plant thorny - Commiphora); leaves usu deciduous; plant (polygamo-)dioecious; pollen colpi short; (pyrenes winged), (pseudaril +); n = 12, 13.

3/286: Commiphora (185), Bursera (110). Pantropical, not tropical Southeast Asia-Malesia, 150 species Commiphora from Africa.

4. Protieae Marchand

C induplicate-valvate, (connate); (stamens = and opposite sepals); n = 11.

3/140: Protium (130). Mostly neotropical, also a few Madagascar and Malesia

Age. Crown-group Protieae can be dated to (43.2-)32.6, 25.7(-18) m.y.a. (Fine et al. 2014).

Synonymy: Balsameaceae Dumortier [?where]

Evolution. Divergence & Distribution. Dates for the split between Bursera and Commiphora vary from ca 120 to ca 60 m.y.a. - c.f. Becerra (2005) and Becerra et al. (2012); with the earlier age, distributions could be affected by continental drift. 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.o., although they thought that diversification within the genus did not really get going until (23-)20 m.y. ago. Becerra et al. (2009) had suggested that Bursera, speciose in the seasonally-dry, tropical forests of Mexico, had diversified most within about the last 25 m.y., while De-Nova et al. (2012) estimated the age of most species of Bursera there at ca 7.5 m.y. - more or less as predicted for species in such forests (Pennington et al. 2009; Dick & Pennington 2011).

Weeks et al. (2005), Weeks and Simpson (2007: much detail) and Weeks et al. (2014) discuss the complex biogeographic relationships within Burseraceae, the latter emphasizing the paucity of biome shifts in the family and the importance of Miocene radiations in both Protieae and Bursereae.

Ecology & Physiology. Burseraceae are a notable component of the Amazonian forests, and include a disproportionally large number of the common tree species with stems at least 10 cm across (ter Steege et al. 2013).

Fine et al. (2014 and references) have studied the diversification of the Protieae, an important element of neotropical forests, in some detail; this began well before the uplift of the Andes. 35 species of Burseraceae, mostly Protium, in the western Amazon largely separated out ecologically, preferring either fertile clay, white sand, or terrace soils (Fine et al. 2005); differentiation of secondary metabolites may also be involved - see also below. In Mexico, Becerra et al. (2009) noted that some 85% of the some 100 species of Bursera, often quite narrowly distributed, were to be found in seasonally-dry tropical forests. De-Nova et al. (2012) suggested that there had been nine shifts to xerophytic scrublands, seven to oak forests, and one to tropical forests, but overall they discussed the habitat preferences of the genus in terms of niche conservatism.

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., although other estimates for the age of the family (see above) suggest that this figure is very much an over-estimate. Toxic material in Species that have a squirt defence have toxic material under pressure in their tissues, and when these are perforated it is ejected to a diastance of up to 2 m; such species 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).

Zapata and Fine (2013) found there were 3-5 copies of monoterpene synthase genes in Protium, one copy being very old, the other copies representing duplication events that occurred 50-70 m.y.a., before the diversification of Protieae (Fine et al. 2014). The evidence suggested that the products of these genes might have functions other than direct defence against herbivores, rather, they might attract predators and parasitoids of these herbivores (Zapata & Fine 2013).

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 stipule-like structures; 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 often very deeply seated in the ovule, with up to 85 cell layers between it and the nucellar 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) and Lambert et al. (2013: exudates), for pollen morphology, see Harley and Daly (1995: Protieae) and Harley et al. (2005: considerable variation), for embryology, Narayana (1960 and references), and for pseudaril anatomy, see Ramos-Ordoñez et al. (2013).

Phylogeny. The quite recently-described Beiselia is sister to the rest of the family (Clarkson 2002; Weeks et al. 2005; Thulin et al. 2008). This has considerable implications for character evolution; Beiselia also has several probably autapomorphic features.

In some studies Commiphora was embedded in Bursera, but with weak support (Weeks et al. 2005). Becerra et al. (2012) and De-Nova et al. (2012, but c.f. some analyses in the latter) also found that a monophyletic Bursera was sister to Commiphora; what about B. tonkinensis? Protieae, Bursereae, and Garugeae (the latter including Canarium, etc.) all had strong support individually, but relationships between them were unclear (Thulin et al. 2008); thus although Becerra et al. (2012) suggested the relationships [Canarieae [Protieae + Bursereae]], 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.

Age. Wikström et al. (2001) dated this node to (61-)57, 55(-51) m.y.a., Magallón and Castillo (2009) suggested an age of around 70.7 m.y., and Bell et al. (2010) an age of (70-)64(-57) or (54-)51(-49) m.y..

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

Sapindaceae

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. vol. 25. 1985). [Photo - Flower, Fruit, Fruit.]

Age. Wikström et al. (2001) date crown-group Sapindaceae to (43-)39, 36(-32) m.y., Bell et al. (2010) suggested an age (53-)42, 41(-30) m.y. - alternatively, it is mid Cretaceous and (very approximately) 116-98 m.y.o. (Buerki et al. 2010c). Crown and stem ages of 36 and 55 m.y.a. respectively were suggested by Quirk et al. (2012).

Fossils ascribable to Sapindaceae are known from the later Cretaceous (Coetzee & Muller 1984).

1. Xanthoceroideae Thorne & Reveal

Phloem stratified; stomata anomocytic; buds perulate; 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.

Age. Wikström et al. (2001) dated this node to (36-)33, 29(-26) m.y., Bell et al. (2010) suggested that it was (46-)37, 35(-26) m.y.o. - alternatively, its age is mid Cretaceous between (very approximately) 116 and 98 m.y. (Buerki et al. 2010c), or somewhere in between, variously around 75.5, 65.8, or 58.8 m.y. (Muellner et al. 2007).

2. Hippocastanoideae Dumortier

Cyanogenic glucosides 0; (pericyclic sheath 0); cuticle wax crystalloids quite common [Acer]; stomata actinocytic (anomocytic); buds perulate (0); leaves opposite, palmate or simple, with palmate venation (odd pinnate), 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.

Age. Wikström et al. (2001) dated crown-group Hippocastanoideae to (29-)26, 20(-17) m.y.o., Bell et al. (2010) to (37-)25(-14) m.y.o. - or they may be 83±20.5 m.y. old (Buerki et al. 2013b).

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).

Age. The age of this node may be mid Cretaceous between (very approximately) 116-98 m.y.a. (Buerki et al. 2010c).

3. Dodonaeoideae Burnett

Cork pericyclic [Dodonaea]; stomata cyclocytic [Dodonaea]; C (0), petal 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.

Age. Crown-group Dodonaeoideae are 80.5±12.75 m.y. old (Buerki et al. 2013b).

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

Evolution. Divergence & Distribution. Cupaniopsis-type pollen is widespread in the fossil record, including from several sites in Africa, although Sapindaceae with such pollen are no longer to be 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).

For the biogeography of the family, in which much dispersal is involved, see Buerki et al. (2010c, 2013b). The subfamilies of Sapindaceae spread in the mid Cretaceous 116-98 m.y., initially from Laurasia, with South East Asia remaining an important area in the evolution of the family (Buerki et al. 2010c, 2013b).

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). The split between Acer and Dipteronia has been dated to (98-)78(-63.5) m.y.a. (Renner et al. 2007b).

Ecology. The largely neotropical Paullinieae (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 large 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), while Ronse de Craene (2010) depicts gynoecial orientation as varying within an inflorescence.

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 can look like a follicle when only one carpel develops; dehiscence is, however, down the abaxial side and rudiments of other carpels are sometimes visible. 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 general accounts, see Radlkofer (1890, 1933 to 1934, etc.) 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), that of Handeliodendron, Cao et al. (2008), of Acer, etc., Leins and Erbar (2010), and for that of Xanthoceras, Zhou and Liu (2012), for nectaries, which may have three vascular traces, see Solis and Ferucci (2009) and Zini et al. (2014), 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), and for genome size, Coulleri et al. (2014: not much correlation with anything).

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, see Buerki et al. (2009, 2010b: 81 and 104 genera respectively); Delevaya and Koelreuteria are successively sister to the rest of Sapindoideae (Buerki et al. 2013b). 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, their seeds may be arillate, etc., but they are not closely related.

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

Age. Wikström et al. (2001) dated this node to (51-)47, 45(-41) m.y.a..

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).

[Simaroubaceae + Rutaceae]: ?

Age. The age for this node is estimated at ca 52 m.y.a. (Pfeil & Crisp 2008) (101.4-)88.4(-75.9) m.y. (Clayton et al. 2009).

Hartl (1958) suggested that there were similarities between 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) and carboline alkaloids and canthinones (Waterman & Grundon 1983).

[Simaroubaceae + Meliaceae]: ?

Age. An age for this node is suggested as (48-)44, 40(-36) m.y.a. (Wikström et al. 2001).

SIMAROUBACEAE Candolle, nom. cons.   Back to Sapindales

Simaroubaceae

Trees or shrubs; bark very bitter, 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); leaflets not articulated, vernation also supervolute-curved, margins coarsely toothed to entire, (stipules 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); 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 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, nucellar cap 2-7 cells across; carpels ± separate in fruit; seed (pachychalazal), with undistinguished testa or scattered lignified cells, endotesta often slightly lignified, tegmen crushed, (mesotegmen with reticulate thickenings); (endosperm with 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, Fruit.]

Age. Crown-group Simaroubaceae are dated to around the Cretaceous-Maastrichtian, a little more than 65 m.y. ago (Clayton et al. 2009).

1. Picrasmateae Engler

(Plant all thorny; leaves scales); (stipules cauline); plant mon- or dioecious; fruits drupaceous mericarps.

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

Synonymy: Castelaceae J. Agardh, Holacanthaceae Jadin, nom. inval.

2. The Rest: (leaves with flat surface glands), (stipules +, cauline - some Soulamea); (K 0, C 0; A 1-4 - Leitneria); A 10<; fruits 1-seeded drupelets or samaras; (endosperm with starch [Leitneria]).

Age. The age of this clade is variously suggested to be around 61.1. 52, or 47.5 m.y. (Muellner et al. 2007: inc. Soulamea).

Synonymy: Ailanthaceae J. Agardh, Leitneriaceae Bentham & J. D. Hooker, Soulameaceae Pfeiffer

Within "The Rest" is the clade

[Quassieae Baillon [Samadera + Simaroubeae Dumortier]]: (filaments with with lateral or basal-adaxial scales); (style long, with separate canals); (tissue below embryo sac massive, with central elongated cells - Samadera).

Synonymy: Quassiaceae Bertolini, Simabaceae Horaninow

Evolution. Divergence & Distribution. Most diversification of Simaroubaceae has been in the Caenozoic (Clayton et al. 2009). Despite (or because of?) the fairly good fossil history of the family in the northern hemisphere, the biogeographic hisory of Simaroubaceae is of considerable complexity with much dispersal (and some extinction) needed to explain the current distribution of taxa (Clayton et al. 2009, see also 2007b).

Indeed, in the map above it is obvious that distributions of some genera in the past and the present are very different. 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 been found in eastern Siberia (Ozerov 2012).

I have put in some phylogenetic structure above because of its effect on our understanding of character evolution; the [Quassia [Samadera + Simarouba etc.]] clade has some distinctive features, but it is well embedded in the family, so these features are not family-level apomorphies.

Chemistry, Morphology, etc. The quassinoids, probably tetracyclic triterpenes, that are charactistic of and restricted to Simaroubaceae replace other limonoids (Waterman 1993; Vieira & Braz-Felho 2006).

The adult plant of Holacantha is basically a giant, intricately-branched branched thorn; the leaves are reduced to scales.

Although the carpels may seem more or less 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 fertilization in the family (c.f. Anacardioideae: Rao 1970).

For additional information, see Clayton (2011: general), for chemistry, see Hegnauer (1973, 1990, also 1966, 1989, as Leitneriaceae), and for other information, see Jadin (1901) and Boas (1913), both vegetative anatomy, Webster (1936: wood anatomy), Wiger (1935: embryology), Abbe (1974) and Tobe (2011a, 2013), inflorescence, floral morphology/anatomy and embryology of Leitneria, Endress et al. (1983: carpel morphology), and Fernando and Quinn (1992: pericarp anatomy).

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 that for some 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 in the family (Clayton et al. 2007b) and has embryological similarities with Brucea, in the same clade (Soulamea, etc.).

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, too).

Classification. Note the demise of Leitneriaceae, the only family previously thought to be restricted to the continental U. S. A. - alack! For the dismemberment of Quassia, see Clayton et al. (2007b).

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

[Rutaceae + Meliaceae]: tetranortriterpenes, flavones +; style-head discoid or capitate, lobed.

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), 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.

Age. Bell et al. (2010) suggested that this node was (51-)40(-29) m.y.o.; however, other dates are (87-)82(-74) m.y.a. (Appelhans et al. 2012a), around 93.3, 82.1, or 72.9 m.y. (Muellner et al. 2007, see also 2006), (72.7-)62.7(-53.3) m.y.a. (Pfeil & Crisp 2008), or (43-)39, 37(-33) m.y.a. (Wikström et al. 2001), so there is quite a range with which to work.

1. Cneoroideae Webb

Cneoroideae

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; Fl. Austral. vol. 26. 2013).

Age. Crown Cneoroideae have been dated to (78-)74(-58) m.y.a. (Appelhans et al. 2012a).

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

Rutoideae

[Amyridoideae [Rutoideae + Aurantioideae]]: dihydrocinnamic acid derivates, carboline alkaloids and canthinones [with tryptophane nucleus; ?level]; (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).

Age. The age of this node may be (56.8-47.6(-36.4) m.y.a. (Pfeil & Crisp 2008), (73-)70(-62) m.y.a. (Appelhans et al. 2012a) or (90-)74(-58) m.y.a. (Salvo et al. 2010: q.v. for more dates).

2. Amyridoideae Arnott

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), (sarcoexotesta [spongy], lignified endotesta - Melicope, etc.), (mesotesta fibrous - Phellodendron), 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

[Rutoideae + Aurantioideae]: Methylcarbazole alkaloids, distinctive flavonoids by polymethoxylation; (thorns +); (leaf rhachis winged), (leaflets alternate); C imbricate (valvate), clawed; G postgenitally united; outer integument (3-)4(-6) cells across, inner integument (2-)3(-4) cells across; seed with multiplicative testa, exotestal, (cells palisade), (mucilaginous), (endotesta thicekend), (tegmen multiplicative), (exotegmen thickened).

3. Rutoideae Arnott

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.

4. Aurantioideae Eaton

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, (testa sclereidal-fibrous - Atalanta), (exo, meso- and) endotesta with crystal-containing cells, exotegmen fibrous; endosperm 0, (nucellar polyembryony +), cotyledons thick, not folded (not Micromelum); n/x = 9.

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

Age. The age for this node is estimated at (28.2-)19.8(-12.1) m.y.a. (Pfeil & Crisp 2008) or ca 30 m.y.a. (Muellner et al. 2007.

Synonymy: Amyridaceae Kunth, Aurantiaceae Jussieu, Citraceae Roussel

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.

For other 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). About 1/4 (400< spp.) of the species in the family are to be found in Australia (see Bayly et al. 2013b for a phylogeny), where most have narrow distributions; movement seems to have been from rainforest habitats to more sclerophyllous/xerophytic vegetation, but there were only four or five of these shifts (Bayly et al. 2013b). There is a major radiation of Melicope on Hawaii of 50+ species, and from Hawaii there seems to have been dispersal to the Marquesas Islands; the source area is likely to be in the general Australia-New Guinean region (Harbaugh et al. 2009b; Appelhans et al. 2014a). Appelhans et al. (2014b) suggested that the black shiny seeds common in the Acronychia-Melicope clade were a key innovation; the exotesta is edible (birds), and this clade has about 17x as many species as Tetracomia and the Euodia clade, successively its sisters.

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. See also Bayly et al. (2013b) for morphology in Australasian members of the family.

Seed Dispersal. For black, shiny, fleshy seeds in the Acronychia-Melicope clade, see Bayley et al. (2013) and Appelhans et al. (2014b). Diosmeae (South African) and Boronia and relatives (Australian) both have seeds with elaiosomes that are endocarpial in origin and are dispersed by ants (Kubitzki et al. 2011; Bayley et al. 2013).

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), a distribution that has exercised phytochemists' imaginations in the past (Kubitzki et al. 2011).

Caterpillars of Papilionidae-Papilionini butterflies are notably common on Rutaceae, and about ca 1/3 of the records are from this family, and 80% of the ca 550 species of Papilio will eat Rutaceae (Zakharov et al. 2004). Like the magnoliids, e.g. Aristolochiaceae, on which other Papilionidae are 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; Simonsen et al. 2011; Condamine 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. 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. 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). Wei et al. (2011) thought that the plesiomorphic condition for Rutaceae was to have 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 (e.g. 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) and Endress et al. (1983), 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); for seed anatomy in Rutoideae, see Gallet (1913). 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), although the position of Harrisonia - sequences from only one gene - was 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 while Waterman (1993) noted that the genus contained no quassinoids, unique to Simaroubaceae. 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] were 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.

Within core Rutaceae, [Aurantioideae [Chloroxylon, Boenninghausenia, Ruta, Chloroxylon, etc. (Ruteae plus!, = Rutoideae)]] 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; Bayly et al. 2013b; Morton & Telmer 2014:). For relationships within the group, see Pfeil and Crisp (2008) and Bayer et al. (2009), and for relationships in the Irano-Turanian Haplophyllum (Rutoideae), which colonized the Mediterranean area more than once, see Salvo et al. (2011) and Manafzadeh et al. (2011). Clauseneae may not be monophyletic (Morton 2009); Glycosmis and/or Micromelum may be sister to other Aurantioideae (Groppo et al. 2012), and both have (1-)2 ovules/carpel and similar chromosome numbers (Mou & Zhang 2012). For relationships in Aurantieae/-oideae, see Morton (2009), and for relationships around Citrus, see Scott et al. (2000), Samuel et al. (2001), Araújo et al. (2003), and Bayer et al. (2009).

Other genera in the family form a single clade, and the classical subfamilies other than Aurantioideae are variously mixed up in it. Hartley (e.g. 1981, 1997, 2001a, b) had early suggested some generic realignments in Malesian-Pacific Rutaceae that largely ignored the then-conventional subfamilies; this work has held up fairly well in molecular studies. Neither the large genus Melicope nor the related Acronychia and Melicope are monophyletic (Appelhans et al. 2014b). 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 (see also Morton & Telmer 2014). Rutaceae not included in the previous three subfamilies formed a clade [Dictamnus et al. [[Pilocarpus + Ravenia] The Rest]]] (see Poon et al. 2007; Groppo et al. 2008, 2012; Salvo et al. 2010; Morton & Telmer 2014) or were part of a polytomy including them (Bayly et al. 2013b). One large clade is mostly Old World-Oceanian in distribution, although it includes the Chilean Pitavia (Groppo et al. 2012). Flindersia and relatives 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 another moderately to well supported clade (Salvo et al. 2010; Groppo et al. 2012) perhaps sister to a clade including most of the Australian taxa that were included in the old Boronieae (Bayly et al. 2013b), and the [Zanthoxylum + Toddalia] clade (Groppo et al. 2012: support poor), in turn sister to the Flindersia group (Bayly et al. 2013b). A final clade (see e.g. Bayley et al. 2013b) includes the North American Ptelea, a largely African Diosmeae (for relationships, see Trinder-Smith et al. 2007), and a largely Central and South American Galipeinae (for relationships, see Kallunki & Groppo 2007). However, support for some of these groups, and of relationships between and within them, is still rather weak (Groppo et al. 2012; Bayly et al. 2013b; Morton & Telmer 2014).

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

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 and subfamilial 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). For the rest, I tentatively follow the subbfamilial framework suggested by Morton and Telmer (2014), although the sampling is rather slight (34 species, even if they do represent all subfamilies and tribes), bolstered by that in Groppo et al. (2012), etc..

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), Diosmeae (Trinder-Smith et al. 2007) and around Melicope (Appelhans et al. 2014b); the necessary nomenclatural changes are gradually being made.

Previous Relationships. Cronquist (1981) placed Cneoraceae in his Sapindales which included Rutales more or less as above 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. Thorne (1992) included Harrisonia (ex Simaroubaceae), although no reasons were given.

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

MELIACEAE Jussieu, nom. cons.   Back to Sapindales

Meliaceae

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 not enclosing C [?level], 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, 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]/640 - 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; Fl. Austral. vol. 26. 2013).

Age. Bell et al. (2010) suggested that the two subfamilies diverged (48-)39, 38(-27) m.y.a.; Muellner et al. (2007, see also 2006) thought that diversification within the family had begun considerably earlier, (98.6-)96.1, 73.6(-61.4) m.y.a., while Wikström et al. (2001) suggested another later date of (40-)36, 30(-26) m.y.a..

For fossil Meliaceae, see Mabberley (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.

36/585. Aglaia (120), Dysoxylum (80), Guarea (75), Trichilia (70), Turraea (60), Chisocheton (50). Pantropical, but largely Old World.

Age. Diversification within Melioideae began (91.2-)78.2, 70.0(-58.3) m.y.a. (Muellner et al. 2006, 2007 - the latter a little bit older).

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

2. Cedreloideae Arnott

Buds perulate (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.]

Age. Diversification within Cedreloideae began (86.2-)75.1, 67.5(-58.0) m.y.a. (Muellner et al. (2006, 2007).

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

Evolution. Divergence & Distribution. Muellner et al. (2006) discussed the biogeography of the family, suggesting its origin in Africa and subsequent dispersal. For the biogeography of Aglaia, see Muellner et al. (2008b) and Grudinski et al. (2014a), the latter suggesting Oligocene-Miocene rather than Eocene diversification; movement was from West Malesia eastwards.

Ecology & Physiology. Although only a small family, Meliaceae make up 17% of all trees >10 cm d.b.h. 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 can 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. Although it was thought that the two subfamilies could be separated by their limonoid types, work on Quivisianthe (Melioideae) suggests that the distinction may not be that simple (Mulholland et al. 2000). Sieve tube plastids with protein crystalloids and starch occur in Melia and Azederach. Walsura often has leaflets with ± pulvinate petiolules and prominent reticulate venation.

Gouvêa et al. (2008b) drew the flowers of Swietenia as being inverted; carpellate flowers are the first to be produced in the cymose inflorescences. The filaments of Vavaea are largely free, as are those of Cedrela and Toona (Cedreloideae-Cedreleae). Indeed, Cedreleae are rather different florally from other Meliaceae, but features found there such as more or less free stamens may be derived, not plesiomorphous as one might think (c.f. Gouvêa et al. 2008a). In Walsura the stamens are also more or less free, and the fruit is often 1-seeded. There is considerable variation in seed morphology and 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). 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) and Grudinski et al. (2014a, b), 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). The connection between species limits in the latter genus and phylogenetic relationships as they are currently understood is somewhat unclear (Grudinski et al. 2014b).

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