EMBRYOPSIDA Pirani & Prado
Gametophyte dominant, independent, multicellular, thalloid, with single-celled apical meristem, showing gravitropism; rhizoids +, unicellular; acquisition of phenylalanine lysase [PAL], flavonoids [absorbtion of UV radiation], phenylpropanoid metabolism [lignans], xyloglucans +; plant poikilohydrous [protoplasm dessication tolerant], ectohydrous; cuticle +; cell wall also with (1->3),(1->4)-ß-D-MLGs [Mixed-Linkage Glucans], lignin +; chloroplasts per cell, lacking pyrenoids; 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; blepharoplast, bicentriole pair develops de novo in spermatogenous cell, associated with basal bodies of cilia [= flagellum], multilayered structure [4 layers: L1, L4, tubules; L2, L3, short vertical lamellae] + spline [tubules from L1 encircling spermatid], basal body 200-250 nm long, associated with amorphous electron-dense material, microtubules in basal end lacking symmetry, stellate array of filaments in transition zone extended, axonemal cap 0 [microtubules disorganized at apex of cilium]; male gametes [spermatozoids] with a left-handed coil, cilia 2, lateral; 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]; nuclear genome size <1.4 pg, LEAFY gene present, ethylene involved in cell elongation; chloroplast genome with close association between trnLUAA and trnFGAA genes.
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 immediate common ancestor of the group,  contains explanatory material, () features common in clade, exact status unclear.
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; shoot meristem patterning gene families expressed; 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.
Sporophyte branched, branching apical, dichotomous; sporangia several, each opening independently; spore walls not multilamellate [?here].
EXTANT TRACHEOPHYTA / VASCULAR PLANTS
Photosynthetic red light response; plant homoiohydrous [water content of protoplasm relatively stable]; 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, plant endohydrous; 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; basal body 350-550 nm long, stellate array in transition region initially joining microtubule triplets; 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]
Sporophyte branching ± indeterminate; lateral roots +, endogenous, root apex multicellular, root cap +; (endomycorrhizal associations + [with Glomeromycota]); 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; blepharoplasts +, paired, with electron-dense material, centrioles on periphery, male gametes multiciliate; chloroplast long single copy ca 30kb inversion [from psbM to ycf2]; LITTLE ZIPPER proteins.
Sporophyte 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; 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 +; 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.; buds axillary (not associated with all leaves), exogenous; prophylls two, lateral; leaves with petiole and lamina, development basipetal, blade simple; plant heterosporous, sporangia borne on sporophylls, sporophylls spiral; microsporophylls aggregated in indeterminate cones/strobili; grains monosulcate, aperture in ana- position [distal], exine and intine homogeneous; ovules unitegmic, parietal tissue 2+ cells across, megaspore tetrad linear, functional megaspore single, chalazal, lacking sporopollenin, megasporangium indehiscent; pollen grains land on ovule; gametophytes dependent on sporophyte; apical cell 0, 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; 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], 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; protogynous; 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], sporangium pairs dehiscing longitudinally by a common slit, ± embedded in the filament, walls with at least outer secondary parietal cells dividing, 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 lamellate only in the apertural regions, thin, compact; nectary 0; carpels present, superior, free, several, ascidiate, with postgenital occlusion by secretion, stylulus at most short [shorter than ovary], 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 land on stigma, bicellular at dispersal, mature male gametophyte tricellular, germinating in less than 3 hours, pollen tube elongated, unbranched, 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, cilia 0, siphonogamy; double fertilization +, ovules aborting unless fertilized; P deciduous in fruit; mature seed much larger than ovule when fertilized, small , dry [no sarcotesta], exotestal; 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]; nuclear genome size <1.4 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]]]]: vessel elements with scalariform perforation plates in primary xylem; essential oils in specialized cells [lamina and P ± pellucid-punctate]; tension wood +; tectum reticulate; anther wall with outer secondary parietal cell layer dividing; carpels plicate; nucellar cap + [character lost where in eudicots?]; 12BP [4 amino acids] deletion in P1 gene.
[[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]] / MESANGIOSPERMAE: benzylisoquinoline alkaloids +; 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; protandry common; 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 , G  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.
[HUERTEALES [MALVALES + BRASSICALES]]: ?
[MALVALES + BRASSICALES]: ?
BRASSICALES Bromhead Main Tree.
Glucosinolates +, from phenyalanine and/or tyrosine [aromatic] and valine/isoleucine/leucine [Branched Chain Amino Acids], idioblastic and stomatal myrosin cells +, little oxalate accumulation; endoplasmic reticulum with dilated cisternae; myricetin, other methylated flavonols, tannins 0; vasicentric axial parenchyma +; tension wood?; mucilage cells in leaf 0; leaves spiral, stipules small; inflorescence racemose; (petals clawed); G , ovules in one or two rows; seed coat?; embryo often green. - 18 families, 398 genera, 4765 species.
Age. Wikström et al. (2001) dated crown Brassicales to 79-71 m.y.a.. Other estimates are (76-)73(-70) and (63-)69(-57) m.y. (two penalized likelihood dates: Hengchang Wang et al. 2009), while Magallón and Castillo (2009) estimated ages of ca 65.9 m.y. and Bell et al. (2010) ages of (94-)83, 82(-69) m.y. ago.
The earliest fossil placed by some in this clade is from the Turonian, ca 89.5 m.y.a. - Dressiantha (see Gandolfo et al. 1998c), but c.f. Couvreur et al. (2010), also below.
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. Brassicales contain ca 2.2% eudicot diversity (Magallón et al. 1999) and show quite high diversification rates (Magallón & Catillo 2009).
Rodman et al. (1996) suggest a number of apomorphies for the order (and for some nodes within it), but where some characters are to be placed on the tree is currently unclear. Characters like ovules in two ranks, parietal placentation, and clawed petals seem notably common in this clade. Ronse de Craene and Haston (2006) examined morphological evolution in the clade in the context of a combined molecular and morphological analysis.
Ecology & Physiology. Nearly all the glucosinolate-producing families of flowering plants are in this clade (c.f. Kjær 1974; Dahlgren 1975). Putranjivaceae (Malpighiales) are the only confirmed unrelated glucosinolate-containing family; families like Phytolaccaceae (Caryophyllales) and Pittosporaceae (Apiales) are unlikely to contain them (Fahey et al. 2001 for a summary). Oceanopapaver, a genus once of uncertain affinities but now firmly placed in Malvaceae (= Corchorus: Whitlock et al. 2003), was also once thought to have myrosin cells.
Glucosinolates are mustard oil glycosides, and mustard oils are esters of isothiocyanic acid with a RóN=C=S group; they have a pungent smell and sharp taste. Specialised, protein-rich myrosin cells contain enzymes like thioglucoside glucohydrolase (a ß-thioglucohydrolase, or myrosinase), that breaks down glucosinolates into glucose and aglucones when plant tissue is damaged by a herbivore and enzyme and substrate are brought into contact. The aglucones then automatically rearrange and form toxic isothiocyanates, or are converted into thiocyanates (mustard oils), nitriles (not necessarily toxic) and other compounds. This is the "Senfölbombe" or "mustard oil bomb" (see Rask et al. 2000, Wittstock et al. 2003; Grubb & Abel 2006; Halkier & Gershenzon 2006; Agerbirk et al. 2008; Burow et al. 2009 for details, most of which have been worked out in Brassicaceae; Bones & Rossiter 2006 particularly for glucosinolate degradation; Pentzold et al. 2014). The ß-glucosidase involved is similar to those that break down cyanogenic glycosides, and there is an evolutionary link between the synthesis of glucosinolates and that of cyanogenic compounds (Halkier & Gershenzon 2006; Morant et al. 2008). Although protective (but see below), their metabolic cost is high (Bekaert et al. 2012).
Some 132 glucosimolates are known (Fahey et al. 2001; Agerbirk & Olsen 2012). They are synthesised from valine/isoleucine and/or leucine (BCAA - Branched Chain Amino Acids) in several families of Brassicales, i.e. they are aliphatic glucosinolates, but there is much more diversity in families in core Brassicales, Emblingiaceae onwards (Rodman 1991a; esp. Mithen et al. 2010 for data), interspecific variability in the genes involved being notably high (Kliebenstein 2006). The activity of glucosinolates depends on the structure of the side chain (Hopkins et al. 2009; Sønderby et al. 2010). Note that not all taxa producing mustard oils have myrosin cells, and even in Brassicaceae, which do, such cells may be absent in the young plant (Maile 1980). Myrosin cells may occur in general leaf tissue; guard cells may also be myrosin cells. In many Brassicales with stomatal myrosin cells, myrosinases occur in large quantities in the guard cells (Jørgensen 1995), and also occur in large amounts (thioglucoside glucohydrolase 1 - TGG1) in the guard cells of Arabidopsis thaliana, at least, even although Brassicaceae lack stomatal myrosin cells. Here myrosinases may have become involved in the signaling mechanisms of stomatal opening and closure, or the products of hydrolysed glucosinolates may evaporate through the stomatal pores, deterring herbivores and/or attracting their parasites (Zhao et al. 2008). Attempts are being made to engineer glucosinolates into non-glucosinolate-containing plants such as tobacco (Geu-Flores et al. 2009); this has now succeeded in Nicotiana benthamiana (Sønderby et al. 2010), so anybody for cabbage-tasting tobacco?
Plant-Animal Interactions. Glucosinolate-plant-herbivore interactions have been much studied, e.g. see Schoonhoven et al. (2005) for more literature. Caterpillars of the 780-840 species of Pieridae-Pierinae (food plants of ca 360 species in 33+ genera recorded) are commonly found on brassicalean plants (Fraenkel 1959; Tempère 1969; Ehrlich & Raven 1964; Braby & Trueman 2006; Braby et al. 2006; Beilstein et al. 2010), including Bretschneidera; however, they are abundant only in the [Capparaceae [Cleomaceae + Brassicaceae]] clade. Caterpillars of the butterfly Appias subgenus Catophaga (albatrosses) are found more or less indiscriminately on Drypetes (Putranjivaceae) and Capparaceae (Yata et al. 2010), and of course both groups contain glucosinolates.
Pierinae may have moved to Brassicales from an original host in Fabaceae (Braby & Trueman 2006) some (90-)85(-60) m.y.a. and within ten m.y. or so of the origin of Brassicales (Wheat et al. 2007), a shift that seems to have been accompanied by a burst in pierine diversification (Fordyce 2010). The ability of pierine caterpillars to live on Brassicales is associated with the evolution of a novel glucosinolate detoxifying mechanism, and more basal pierine clades that lack this mechanism are less diverse (Wheat et al. 2007; see also Winde & Wittstock 2011 and Pentzold et al. 2014 for how insects can get around the glucosinolate defences). After a gene duplication, one of the orthologs produced an enzyme that detoxifies glucosinolates by producing nitriles rather than toxic isothiocyanates on their hydrolysis (Fischer et al. 2008).
Relationships between herbivores and plants - again, nearly all information comes from Brassicaceae - are complex. Both specialised herbivores and their hymenopteran parasites may be attracted by isothiocyanates (Hopkins et al. 2009 and references), and while the growth rate even of specialized herbivores may be reduced by glucosinolates (but that of generalized herbivores more), that of parasitoids may be increased as the growth rate of their host caterpillar decreases (Kos et al. 2012).
Some chrysomelid beetles favor Brassicales, for example, the 180 species of the flea beetle Phyllotreta (Alticinae - see Jolivet & Hawkeswood 1995). Phyllotreta striolata produces its own myrosinase to break down the glucosinolates it acquired from the plant - aliphatic glucosinolates suit the insect best (Beran et al. 2014). A number of other insects can also sequester glucosinolates intact, and at least some aphids also have their own myrosinases (Beran et al. 2014 for references). The dipteran leaf miner Liriomyza brassicae is found on Resedaceae, Cleomaceae, Tropaeolaceae and Brassicaceae (Spencer 1990).
Genes & Genomes. For ca 800 genes (including those lost in Brassicaceae) unique to Brassicales - or at least [Caricaceae + The Rest], see Bhide et al. (2014).
Chemistry, Morphology, etc. A report of ellagic acid in "Capparidaceae" (Bate-Smith 1962) needs to be confirmed. Zindler-Frank (1976) lists seven families scattered throughout the order as having little oxalate accumulation.
Many taxa seem to have diarch roots, although not some Cleomaceae; sampling in the basal pectinations is poor. Most families have "stipules" of some sort or another, although they are small; 1:1 nodes are common in the order, and stipule anatomy and morphology would repay further study. Strongly developed and fused ventral carpellary bundles may be another synapomorphy for the order (Ronse de Craene & Haston 2006).
For general information, see Villers (1973), Mehta and Moseley (1981), Jørgensen (1981, 1995), Carlquist (1985a), Tobe and Peng (1990), Fisch and Weberling (1990), Rodman (1991a, b), Link (1992a), Rodman et al. (1993, 1994), Tobe and Takahashi (1995), Hufford (1996), Doweld (1996a, b), Ronse Decraene and Smets (1997a), Kubitzki (2002a, b: as Capparales), and Fay and Christenhusz (2010), also Tobe and Raven (2012: aspects of seed evolution).
Phylogeny. Relationships within Brassicales show a fair bit of structure (see tree), as Rodman et al. (1997, 1998), Carol et al. (1999), Chandler and Bayer (2000), Kubitzki (2002a), Olson (2002a) and Hall et al. (2004) have found. Setchellanthus came out just basal to Limnanthaceae in molecular phylogenies (Karol et al. 1999: support weak, see also Rodman et al. 1997; Chandler & Bayer 2000; Karol et al. 1999: strong support). Ronse de Craene and Haston (2006) examined morphological evolution in the context of a combined molecular (four genes, some taxa lacked up to three of them) and morphological study; there are differences in detail of the topology of their tree and that used here. Analysis of morphological data alone yielded only one clade ([Polanisia + Cleome]!) in Brassicales with even weak support, and Bretschneidera and Akania were associated with Sapindaceae (Ronse de Craene & Haston 2006).
Phylogenetic relationships in core Brassicales have been partly resolved in a three-gene study by Hall et al. (2004) and a four-gene analysis by Su et al. (2012), although further studies are needed. Ronse de Craene and Haston (2006) found that Emblingiaceae moved outside this group in a combined morphological-molecular study, but many data were missing for Emblingia in particular and its floral morphology is odd and poorly understood (see below); they thought that it might be sister to [Bataceae + Salvadoraceae], but noted that there was little support for this position.
Classification. For the history of the classification of the group, see Fay and Christenhusz (2010). For the limits of families around Resedaceae, currently narrowly drawn for convenience, see below.
Previous Relationships. Some Brassicales, Brassicaceae and immediately related families, have always been placed together based on morphological similarity and chemistry (smell!), but until quite recently the others have been widely separated. Many brassicalean families are included in Violanae (Dilleniidae) by Takhtajan (1997), but Gyrostemonales are in Gyrostemonanae (Caryophyllidae) and Limnanthales in Solananae (Lamiidae). Cronquist (1981) placed families here included in Brassicales in his Violales (Caricaceae), Capparales (several families), Batales (Gyrostemonaceae, Bataceae), families scattered through Dilleniidae, as well as in his Geraniales (Limnanthaceae) and Sapindales (Akaniaceae), both in his Rosidae, etc. Rolf Dahlgren began the process of pulling the order together by emphasizing the distinctive chemistry (e.g. R. Dahlgren 1975a; G. Dahlgren 1989, and references; summary in Jørgensen 1995).
Includes Akaniaceae, Bataceae, Borthwickiaceae, Brassicaceae, Capparaceae, Caricaceae, Cleomaceae, Emblingiaceae, Gyrostemonaceae, Koeberliniaceae, Limnanthaceae, Moringaceae, Pentadiplandraceae, Resedaceae, Salvadoraceae, Setchellanthaceae, Stixaceae (to be recognized?), Tovariaceae, Tropaeolaceae -
Synonymy: Brassicineae Shipunov - Akaniales Doweld, Batales Engler, Capparales Berchtold & J. Presl, Caricales L. D. Benson, Gyrostemonales Takhtajan, Limnanthales Martius, Moringales Martius, Resedales Link, Salvadorales Reveal, Tovariales Nakai, Tropaeolales Martius - Capparanae Reveal, Gyrostemonanae Takhtajan,
[Akaniaceae + Tropaeolaceae]: young stem with separate bundles; vessel elements with scalariform perforation plates; axial parenchyma sparse, adjacent to vessels; bracteoles 0; flowers quite large, obliquely monosymmetric; K/C tube +, C clawed; A 8; pollen colpate; placentation apical-axile, style long; ovules 1-2/carpel, epitropous; K deciduous; testa vascularized, multiplicative.
Age. The crown age of this clade is estimated at 61-54 (Wikström et al. 2001) or (56-)35, 34(-18) m.y. (Bell et al. 2010).
Chemistry, Morphology, etc. Carlquist and Donald (1996) give additional characters of wood anatomy that may unite these two families. Tropaeolaceae may have basically pinnate leaves (Endress 2003c), but this can perhaps be cleared up by developmental studies - another synapomorphy for the clade?
Although both families have a nectary, it is extrastaminal in Tropaeolaceae and intrastaminal in Akaniaceae. Furthermore, exactly which stamens are reduced and details of the plane of asymmetry of the flowers differ between Tropaeolum and Bretschneidera; the former is obliquely asymmetric only in bud (Ronse Decraene et al. 2002a; Ronse Decraene & Smets 2001a). A "hypanthium" was described as "lifting sepal lobes and petals high above the stamen insertion" by Ronse Decraene et al. (2002a: p. 44), i.e., it is a calyx/corolla tube in the strict sense; there is also a true hypanthium in Bretschneidera, but not elsewhere (Stapf 1912; Ronse Decraene & Smets 2001a).
AKANIACEAE Stapf, nom. cons. Back to Brassicales
Deciduous or evergreen trees; tannins?; cork subepidermal; (vessel elements with simple perforation plates); no bordered pits in imperforate tracheary elements; petiole bundle?; cuticle waxes 0, strong cuticular cracks; stomata ?; leaves odd-pinnate, leaflet margins spinulose-toothed or entire, vernation supervolute-curved, petiolules swollen or articulated; inflorescence branched or not, bracteoles 0; (hypanthium +); K ± connate, C contorted or not, barely clawed [Akania]; A 8, or 3 (4) abaxial in the whorl opposite petals [Akania], with short connective prolongations; nectary + or 0; stigma small, 3-lobed; ovules (superposed - Akania), (campylotropous - Bretschneidera), micropyle bistomal, outer integument ca 5 cells across, inner integument 2-3 cells across, parietal tissue 4-8 cells across; (embryo sac bisporic (the spores chalazal) and 8-celled [Allium type] - Bretschneidera); capsule loculicidal; exotestal cells palisade, thick-walled, mesotesta ± thick, cells thick-walled, endotesta thickened; endosperm development?, copious or not, embryo color?, cotyledons large; n = 9 [Bretschneidera].
2[list]/2. S.W. China, adjacent Vietnam, Formosa (Bretschneidera sinensis), E. Australia (Akania bidwillii) (map: Australia's Virtual Herbarium i.2014 - Akania). [Photo - Collection]
Age. Bell et al. (2010) suggested that the two genera diverged (12-)6(-2) m.y.a., the age in Wikström et al. (2001) is 31-23 m.y.a., and fossils identified as Akania are about 52 m.y.o. (Gandolfo et al. 2011), so something is wrong here.
Evolution. Divergence & Distribution. Fossils attributed to Akania are known from Patagonia in Eocene deposits of about 51.9 m.y. of age, so its distribution in the past was very different from that now (Gandolfo et al. 2011 and references; Wilf et al. 2011).
Chemistry, Morphology, etc. Stapf (1912) described the pollen of Akania as being 4-porate. In Bretschneidera, glucosinolates are also produced from valine/isoleucine and/or leucine, the leaflets are entire, the flowers are clearly strongly obliquely monosymmetric, the stamens are curved and held under one petal, there is a disc. The seeds of Akania have endosperm and the plant may lack myrosin cells, but wood of the two genera is almost identical. Seedlings of Akania initially produce at least five simple leaves with pinnate venation.
For general information, see Bayer and Appel (2002); for ovules, see Mauritzon (1936).
Classification. Separating Bretschneideraceae from Akaniaceae was considered optional in A.P.G. II (2003), however, there is nothing lost in combining them (see A.P.G. 2009).
Previous Relationships. A relationship with Sapindales has often been suggested (e.g. Carlquist 1997a); a phylogenetic analysis of morphological data also suggested this position (Ronse de Craene & Haston 2006). Bretschneideraceae do look rather sapindaceous.
Synonymy: Bretschneideraceae Engler & Gilg, nom. cons.
TROPAEOLACEAE Candolle, nom. cons. Back to Brassicales
Fleshy vines with twining petioles, (caespitose herbs), often with tuberous roots; glucosinolates also from valine/isoleucine and/or leucine, benzyl- and 4-methoxybenzyl types, stomatal myrosin cells 0, erucic acid [fatty acid] +; cork cambium deep seated? to more superficial; petiole bundles annular; pericyclic fibres 0; cuticle waxes tubular; leaves flat in bud, lamina peltate, entire to palmately lobed or compound, margins toothed to entire, stipules small, in seedling only, to fringed, subfoliaceous and throughout the plant; flowers often axillary, (bracteoles +); ± strongly monosymmetric; 3 adaxial K connate, spurred, (spur ca 1 mm or less), C 2 + 3 (2 + 2), (margin ± deeply lobed/laciniate); nectary in spur outside A; pollen grains tricellular; median carpel adaxial, style impressed, stigma trifid, dry; ovules with endostomal micropyle, parietal tissue 0; fruit a schizocarp (samara), mericarps drupaceous or nutlike, K deciduous; seed pachychalazal, coat undistinguished, part of mesotesta suberized; amyloid [xyloglucans] in cotyledons, suspensor haustorium +, penetrates micropyle and adjacent maternal tissue; n = 12-15.
1/105. New World, esp. Andean (map: see Sparre & Andersson 1991). [Photos - Tropaeolum Flower, ditto.]
Chemistry, Morphology, etc. Carlquist and Donald (1996) report vague storying of the secondary phloem of the root. For the development of the peltate leaf of Tropaeolum majus in which the petiole lacks even a basal bifacial zone, see Gleissberg et al. (2005).
For an interpretation of the axillary flowers common in Tropaeolum, see Bayer and Appel (2002). The nectary is described as being hypanthial (Troll 1957), but it ends up in the spur outside the stamens (Ronse Decraene et al. 2002). The median carpel is actually slightly off the median (Eichler 1878; Ronse Decraene & Smets 2001a); two antepetalous stamens are suppressed (Ronse Decraene et al. 2002). There are initially two ovules per carpel, but one does not develop very much. The developing seed has an elaborate suspensor haustorial system (Walker 1947; Yeung & Meinke 1993 and references).
For an account of the southerly and temperate Tropaeolum section Chilensia, see Watson and Flores (2010a, b).
Phylogeny. For phylogenetic relationships in the family, see Andersson and Andersson (2000). Distinctive reproductive morphologies - Magallana, with its winged fruits, and Trophaeastrum, which lacks a nectary spur - are derived from within the general Tropaeolum morphology of spurred flowers and simple schizocarpic fruits.
Classification. Only Tropaeolum can be recognized since maintaining Magallana and Trophaeastrum would make it paraphyletic (Andersson & Andersson 2000).
[[Moringaceae + Caricaceae] [Limnanthaceae [Setchellanthaceae [[Koeberliniaceae [Bataceae + Salvadoraceae]] [Emblingiaceae [[Pentadiplandraceae [Gyrostemonaceae [Borthwickiaceae + Stixaceae + Resedaceae]]], Tovariaceae, [Cleomaceae [Capparaceae + Brassicaceae]]]]]]]]: several [>6] ovules/carpel.
Age. The age of this clade is estimated as 72-68 m.y.a. (Wikström et al. 2001), (90.5-)72-(-47.9) m.y. (Couvreur et al. 2010), (90-)79, 65(-55) m.y. (Bell et al. 2010), (68-)54(-38) m.y. (N. Zhang et al. 2012), or as little as ca 39.0 or 36.3 m.y. (Xue et al. 2012).
[Moringaceae + Caricaceae]: woody, stems stout [pachycaul or cauduciform]; endoplasmic reticulum-dependent vacuoles +; cambium storied; nodes multilacunar; cuticle wax platelets as rosettes; lamina venation palmate, colleters on petiole/lamina, stipules as glands; inflorescences thyrses; flowers whitish; G opposite sepals, ovary longitudinally sulcate, placentation parietal, placental strands opposite the ventral bundles, style hollow; ovules many/carpel, micropyle bistomal, outer integument 4-6 cells across; testa multiplicative, mesotesta ± lignified.
Age. The two families diverged some 61-58 (Wikström et al. 2001) or (86-)67, 64(-45) m.y.a. (Bell et al. 2010).
Chemistry, Morphology, etc. Ronse de Craene and Haston (2006) suggested that nodes were unilacunar in this clade; they are tri- or multilacunar.
The sulci in the ovary are in the interplacental position. Whether or not the thickened mesotesta of the two families is comparable needs to be confirmed, certainly there are substantial anatomical differences in the seed coat (Olson 2002a).
MORINGACEAE Martynov, nom. cons. Back to Brassicales
Deciduous trees or shrubs (stem succulents); glucosinolates also from valine/isoleucine and/or leucine; hairs unicellular; schizogenous gum canals +; leaves odd-pinnate, 1- or 3-compound, leaflet margins entire; flowers monosymmetric, oblique; hypanthium +, short (long), lined with nectary, K petal-like, median [abaxial] C usu. larger than others; stamens = and opposite petals, declinate, monothecal, staminodes +, opposite sepals; gynophore +; G ([2-4]), style slender, stigma truncate-porate; micropyle zig-zag, outer integument vascularized, inner integument ca 3 cells across, parietal tissue ca 3 cells across, endothelium +; fruit 3-angled, explosively-dehiscent, loculicidal; seeds 3-angled, winged (not); mesotesta thick, outer and inner parts with helical thickenings, middle part massive, tegmen thin, (multiplicative); n = 11, 14.
1[list]/12. India to Africa, Madagascar, Moringa oleifera is quite widely cultivated (map: from Olson 2001). [Photo - Flower, Collection]
Evolution. Vegetative Variation. Olson and Rosell (2006) suggest that heterochrony is involved in the evolution of the various life forms in the family; the bottle-tree growth form is probably plesiomorphic, the tuberous shrub growth form is probably derived (see also Olson 2006 for wood anatomy). All species have rather fleshy roots/rootstock and usually grow in more or less arid habitats.
Chemistry, Morphology, etc. For wood anatomy, see Olson and Carlquist (2001); there are reports of vestured pits from the family (Jansen et al. 2001b).
Flowers of all species are slightly monosymmetric early in development (Olson 2002b), but at anthesis they range from polysymmetric to strongly monosymmetric. When flowers are monosymmetric, they are borne with the median petal adaxial, and when they are polysymmetric the median petal is in the normal abaxial position (Olson 2003). Carpel orientation is in the plane of symmetry of the flower (Ronse Decraene et al. 1998a). Corner (1976) suggests that the micropyle is exostomal. Seeds are borne along the middle of the valves which means that dehiscence is effectively loculical given that the placentation is parietal. The seedlings have either palmately compound leaves or simple leaves with palmate venation (M. Olson, pers. comm.).
Some general information is taken from Ernst (1963), who described the ovules as being apotropous. Kubitzki (2002d) and the Moringa website (Olson 1999) summarize information on the family.
Phylogeny. For relationships, see Olson (2000b).
Synonymy: Hyperantheraceae Link
CARICACEAE Dumortier, nom. cons. Back to Brassicales
Small to medium trees, (viny, but with stout tuber), usu. prickly; benzylglucosinolates +, idioblastic myrosin cells 0; laticifers +, articulated, anastomosing; lamina palmately lobed or compound, vernation flat-curved to involute, margins entire or serrate, glands on adaxial surface at base; plants di(mon)oecious; inflorescences axillary, cymose; staminate flower: K connate, small, C connate, contorted or valvate; stamens adnate to corolla, 10, of two lengths, whorled, the longer opposite the sepals, or = and opposite sepals, connective often developed; nectary on pistillode; carpellate flowers: as above, but C often free; A 0; nectary 0; G , (placentation axile), style branches ± separate, stigmas flabellate or almost petal-like (capitate), dry; inner integument 4-6 cells across; fruit a berry; sarcotesta +, mucilaginous, mesotesta with lignified ribs, tanniniferous, endotesta crystalliferous (lignified), exotegmen fibrous [?sclereidal?]; embryo white; n = 9.
4(-6)[list]/34: Vasconcellea 21. Mostly tropical (Andean) America (three genera in Mexico); Africa (Cylicomorpha only) (map: from Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; Carvalho 2013). [Photo - Plant, Flower, Fruit.]
Floral formula: * [♂] [♀]; K ; C 5; A 10; N 0; G 0< - [♂]. K 5; C 5; A 0; N 0; G  - [♀].
Age. Crown-group Caricaceae have been dated to (52.6-)43.1-35.5(-28.1) m.y. (Carvalho & Renner 2012).
Evolution. Divergence & Distribution. Caricaceae seem to have originated in Africa, moving to the New World (Central America) by long distance dispersal ca 35 m.y.a. (Carvalho & Renner 2012, q.v. for various dates within the family).
Pollination Biology & Seed Dispersal. Jacaratia has carpellate flowers with white, spreading stigmas perhaps mimicking the androecium of staminate flowers; nectar is produced only in the staminate flowers (Bawa 1980). Carica (and Vasconcellea?) has a similar floral syndrome.
Myrmecochory is reported from Carica (Lengyel et al. 2010) despite (perhaps) its fleshy fruits.
Genes & Genomes. For the evolution of the X chromosome in Carica papaya, which is dated to only ca (9.5-)7(-1.9) m.y.a., see Gschwend et al. (2012) and J. Wang et al. (2012); there are inversions, etc., in the hermaphrodite-specific region of the Y chromosome.
Chemistry, Morphology, etc. Reports of cyclopentenoid cyanogenic glycosides in the family have been questioned (Jørgenson 1995).
Some general information is taken from Badillo (1971), Miller (1982) and Kubitzki (2002d), and see especially the e-monograph by Carvalho (2013); for wood anatomy, see Carlquist (1998c), for floral development, see Ronse Decraene and Smets (1998b), and for embryology, see Singh (1970).
Phylogeny. For phylogenetic relationships, see Kyndt et al. (2005) and Carvalho and Renner (2012) and Carvalho (2013). The African Cylicomorpha is sister to the rest of the family, which are all American - [Cylicomorpha [[Jacaratia + Vasoncellea] [Carica papaya [Horovitzia + Jarillo]]]], generally good support.
Previous Relationships. Cronquist (1981) included Caricaceae in his Violales sandwiched between Achariaceae in the restricted sense (more or less herbaceous, South African) and the North American Fouquieraceae; Takhtajan (1997) placed his monofamilial Caricales in a generally similar position, i.e. along with other families that have parietal placentation.
[Setchellanthaceae [Limnanthaceae [[Koeberliniaceae [Bataceae + Salvadoraceae]] [Emblingiaceae [[Pentadiplandraceae [Gyrostemonaceae [Borthwickiaceae + Stixaceae + Resedaceae]]], Tovariaceae, [Cleomaceae [Capparaceae + Brassicaceae]]]]]]]: nodes 1:1; C clawed; extended 3' terminus of rbcL gene.
Age. The age of this clade is around 60-54 m.y. (Wikström et al. 2001) or (85-)73, 71(-61) m.y. (Bell et al. 2010: c.f. relationships in it).
Chemistry, Morphology, etc. For the extended 3' terminus of rbcL gene and changes in stop codons, etc., see Karol et al. (1999).
SETCHELLANTHACEAE Iltis Back to Brassicales
Shrub; myrosin cells 0; young stem with vascular cylinder; fibres 0; rays uniseriate, one cell high; hairs T-shaped, unicellular, on multicellular podium; blade amphistomatal; lamina secondary veins subbasal, margins entire, stipules 0; flowers axillary, large [ca 4 cm across], 6-merous (5, 7); K connate, splitting irregularly; androgynophore +; A many, centrifugal, in 5-7 groups on elongated axis; pollen tricolpate, surface striate-rugulate; nectary 0; gynophore +, short; placentation axile, style short, branches short, stigmas subcapitate; ovules 10-14/carpel, in two ranks; fruit a septifragal capsule, central column persistent; testa soft, multiplicative; endosperm development?, scanty; n = ?; seedling epigeal, phanerocotylar, cotyledons cordate.
1/1: Setchellanthus caeruleus. Mexico (map: see Iltis 1999). [Photos - Flower, Flower, Fruit]
Chemistry, Morphology, etc. The fusion of the marginal ventral carpellary bundles is commissural.
Some information is taken from Carlquist and Miller (1999: anatomy), Iltis (1999: general), Tobe et al. (1999: flowers), Tomb (1999: pollen), and Kubitzki (2002d: general).
Previous Relationships. Setchellanthus used to be included in Capparaceae.
[Limnanthaceae [[Koeberliniaceae [Bataceae + Salvadoraceae]] [Emblingiaceae [[Pentadiplandraceae [Gyrostemonaceae [Borthwickiaceae + Stixaceae + Resedaceae]]], Tovariaceae, [Cleomaceae [Capparaceae + Brassicaceae]]]]]]: (indole glucosinolates present in appreciable amounts); root hairs in vertical files.
Age. The age for this node is estimated to be 54-52 m.y. (Wikström et al. 2001: c.f. topology).
Chemistry, Morphology, etc. The distinctive vertical files of root hairs are known from Limnanthaceae and some members of core Brassicales; they have not been found in Tropaeolaceae, but other Brassicales basal to Limnanthaceae have not been studied (Dolan & Costa 2001).
LIMNANTHACEAE R. Brown, nom. cons. Back to Brassicales
Herbs; erucic acid, ellagic acid, myricetin, non-hydrolysable tannins +, isokestose oligosaccharides as storage, stomatal myrosin cells 0; cork?; leaf pinnate, or lamina pinnately lobed, vernation conduplicate, margins with teeth, stipules 0; (flowers single, axillary, bracteoles 0); flowers 3-5-merous; K valvate, C contorted (open); nectaries on abaxial bases of antesepalous A; A 2x K, of two lengths, largest opposite sepals; pollen with encircling colpus; G [2-5], opposite sepals, when 3 median member abaxial, no vascular bundles in carpel wall, placentation basal-parietal, style gynobasic, hollow, branches ± well developed, stigma punctate to minutely capitate, dry; ovule 1/carpel, apotropous, unitegmic, integument 14-16 cells across, parietal tissue 0; megaspore mother cells several, embryo sac tetrasporic, 6-7-nucleate; fruit a schizocarp, mericarps muriculate, K persistent, green; seed coat pachychalazal, thick, testa with vascular bundles, otherwise undistinguished; (endosperm haustorium + - Floerkea), embryo color?, cotyledons with backwardly-directed lobes, with amyloid [xyloglucans]; n = 5.
1(2)[list]/8. Temperate North America (map: from Culham 2007). [Photo - Flower] [Photo - Flower (close-up)]
Age. The two genera in Limnanthaceae separated ca 17-9 m.y.a. (Wikström et al. 2001) or (22-)13, 12(-5) m.y.a. (Bell et al. 2010).
Chemistry, Morphology, etc. Eckert 1966) compared floral morphology of Limnanthaceae with that of other families believed to be related. Details of the development of the embryo sac are unclear. According to van Tieghem (1898), the ovules are epitropous. Maheshwari and Johri (1956) and Johri (1970) described an endosperm pouch or haustorium on the funicular side of the micropyle region in Floerkea.
Some general information is taken from Bayer and Appel (2002); for wood anatomy, see Carlquist and Donald (1996), for floral differences for nectaries, see Link (1992a), and for embryology, see Fagerlind (1939b) and Mathur (1956).
Previous Relationships. Limnanthaceae were often included in Geraniales (e.g. Cronquist 1981); Limnanthaceae were placed in Solananae by Takhtajan (1997).
[[Koeberliniaceae [Bataceae + Salvadoraceae]] [Emblingiaceae [[Pentadiplandraceae [Gyrostemonaceae [Borthwickiaceae + Stixaceae + Resedaceae]]], Tovariaceae, [Cleomaceae [Capparaceae + Brassicaceae]]]]]: glucosinolates from chain-elongated branched-chain amino acids; style short to absent; ovules campylotropous; seeds exotegmic, exotegmen fibrous; embryo strongly curved.
Age. The age of this node is estimated at around 72-68 m.y.a. (Wikström et al. 2001).
The fossil Dressiantha, from some 90 m.y.a. in the Cretaceous-Turonian of East North America, may be assignable to a node somewhere around here. Gandolfo et al. (1998c) in a morphological analysis placed it in a clade that included Koeberliniaceae, Bataceae, Brassicaceae, etc., although excluding Gyrostemonaceae. However, with a floral formula of K4, C5, A5 + 5 staminodes, G , calyx decussate (not always evident in the images presented), androecium obdiplostemonous* (diplostemonous in the text), stamens epipetalous*, antepetalous*, staminodes +; ?nectariferous disc internal to the androecium*, anthers monothecate* and with prolonged connectives*, gynoecium stipitate, carpels ?obliquely-oriented*. Asterisks denote some distinctive characters not included in the phenetic analysis. The relationships of this remarkable fossil are unclear to me, and nothing really suggests a position around here. Its use in calibration would seem ill-advised.
Chemistry, Morphology, etc. Amino acids like isoleucine with branched chains may have additional carbons along the chain; the occurrence of such chain-elongated branched-chain amino acids is to be pegged here on the tree (J. E. Rodman, pers. comm.). There is extensive variation of floral merism in the Emblingiaceae-Brassicaceae group in particular, but 4-merous flowers could be another apomorphy at this level - but with plenty of reversals. A fibrous, if unlignified, exotegmen has been reported from Koeberliniaceae, Salvadoraceae, Resedaceae, Cleomaceae, etc. As Tobe and Raven (2008) suggest, optimisation of this and other embryological features on the tree is unclear; if ovule and seed characters are placed at this node, they reverse in the [Bataceae + Salvadoraceae] clade.
[Koeberliniaceae [Bataceae + Salvadoraceae]]: idioblastic myrosin cells 0; pits vestured; flowers 4-merous; pollen 3-colporoidate; G ; fruit indehiscent; exotestal cells well developed; x = 11.
Age. The age of this node is estimated at about 43-37 m.y.a. (Wikström et al. 2001) or (71-)60, 59(-48) m.y. (Bell et al. 2010).
Chemistry, Morphology, etc. For variation in and possible synapomorophies of this group, see Ronse Decraene and Wanntorp (2009).
KOEBERLINIACEAE Engler, nom. cons. Back to Brassicales
Woody, thorny; ellagic acid?, tannins?; glucosinolates absent; cork pericyclic; perforation plates bordered; intercellular canals +; druses 0; leaves minute, fugacious, stipules 0; inflorescences axillary; (flowers 5-merous); A (10); tapetal cells multinucleate; nectaries at the base of A; G with gynophore, orientation oblique, placentation axile, style +, stigma ± minutely expanded; ovules ca 10/carpel, apotropous and epitropous, micropyle zig-zag, outer integument 2 cells across, non-multiplicative, parietal tissue 0, nucellar epidermal cells radially enlarged; fruit a berry; seed ?arillate; exotesta with massive cuticle, then tanniniferous cells, exotegmen fibrous, walls very thick, lignified, cells moderately elongated; embryo green, endosperm type?, moderate, cotyledons incumbent.
1/2. Central and S.W. North America, Bolivia (map: from Holmes et al. 2009). [Photo - Habit] [Photo - Flower]
Chemistry, Morphology, etc. Nodal anatomy is taken from that of the bracts (Mehta & Moseley 1981). The ovules look as if they may be campylotropous (see also Tobe & Raven 2008).
For general information, see Kubitzki (2002d), for vegetative anatomy, see Gibson (1979), for floral anatomy, see Mehta and Moseley (1981), and for embryology, see Tobe and Raven (2008): von Schrenk, Aug. 8, Texas - seed anatomy.
Classification. See Holmes et al. (2009) for a monograph.
Previous Relationships. Koeberlinia itself has been included in Capparaceae (Cronquist 1981). Canotia, sometimes associated with Koeberlinia (e.g. Hutchinson 1973), is included in Celastraceae. Both are thorny shrubs, but that is the main extent of their similarity.
[Bataceae + Salvadoraceae]: wood ± storied; perforation plates not bordered; rays wide, multiseriate; nodes 1:2; stomata paracytic; leaves opposite, lamina with secondary veins ± palmate, ascending from at or near base; bracts with colleters on their tips; ovules 2/carpel, basal; exotegmen not fibrous; endosperm 0, embryo ± straight, color?
Evolution. Divergence & Distribution. The two families are really quite similar in details of morphology (Rodman et al. 1996) and anatomy (Carlquist 2002a), although quite unlike at first sight. Ronse de Craene and Haston (2006) and Ronse de Craene and Wanntorp (2009) list a number of other features the two share, including flowers that are slightly disymmetric and horizontally oriented relative to the inflorescence axis, a sepal tube, etc. The flowers of neither family are easy to interpret.
BATACEAE Perleb, nom. cons. Back to Brassicales
Fleshy shrublets; (hydroxy)proline betaines +, tannins?; cork pericyclic; perforation plate borders vestigial; leaves fleshy, blade amphistomatal, stipules intrapetiolar or cauline, unvascularized; plant monoecious or dioecious, inflorescences densely spicate, usually axillary; flowers small, bracteoles 0, nectary 0; staminate flowers: K median, enveloping flower, or K 4, connate; P clawed; A = and alternate with P; pollen surface smooth, ektexine spongy, undifferentiated; pistillode 0; carpellate flowers: P 0; staminodes 0; G with carpels divided [4-locular], stigmas capitate-penicillate; ovules collateral, epitropous, micropyle ± zig-zag, nucellar cap +; fruit multiple, or a drupe with four pyrenes; seed coat membranous; ?cotyledons.
1[list]/2. N. Australia and S. New Guinea, tropical America, and the Galapagos (map: from van Steenis & van Balgooy 1966; Heywood 1978; Fl. Austral. 8. 1982; introduced into the Hawaiian Is.). [Photo - Flowers]
Chemistry, Morphology, etc. For the nodal anatomy of Batis maritima, with what is presumably the foliar trace disappearing as it approaches the node, the leaf being supplied by two bundles from the angles of the stem, see van Tieghem (1893), but c.f. Johnson (1935) and R. A. Howard (pers. comm.). The stipules need study: van Tieghem (1893) did not see them, Johnson (1935) thought that they were between the broad leaf base and the stem, Rogers (1982b) that they were cauline, while Ronse De Craene (2005) in a floral study describes the fairly massive structures in this position in the flowers as being colleters - these descriptions are not all mutually exclusive.
The morphological nature of the structure enveloping the staminate flowers is most obvious in B. argillicola, but there is controversy over the nature of this structure, too. Ronse De Craene (2005) described it as being derived from four sepals in Batis maritima, although he noted that it had only a single vascular trace; some of the lobing of the tubular structure may be caused by pressure from other parts of the developing flower rather than reflecting an inherently four-merous tube.
Batygina et al. (1985) provide information on the ovules, for pollen, see Tobe and Takahashi (1995), and for general information, see Bayer and Appel (2002).
SALVADORACEAE Lindley, nom. cons. Back to Brassicales
Woody; tannins 0; cisternae of endoplasmic reticulum dilated; myrosin cells 0; cork superficial; wood storied; (vestured pits + - Salvadora); interxylary phloem +; druses 0; cuticle waxes with platelets; lamina vernation flat-curved [Salvadora]; plant dioecious or polygamous, or flowers bisexual; (bracteoles 0); floral orientation oblique; K 2-4(-5), (one-trace), contorted, basally connate, C (5), contorted or imbricate, (connate); (C/A tube +, short [Salvadora]); nectar glands alternating with or abaxial to A, unvascularized, or 0; A = and opposite sepals, free, basally connate, or adnate to C; pollen triporate, surface reticulate; G (with gynophore), 1-2-4-locular [see below], orientation oblique, (style short), stigma at most slightly lobed; ovules (1/carpel), apotropous, micropyle exo-, endo- or bistomal, outer integument 10-15 cells across, (with a vascular bundle - Azima), inner integument 3-5 cells across, parietal tissue ?ca 3 cells across, (obturator +); fruit a berry or drupe; testa multiplicative, exotestal cells palisade, slightly thickened, inner walls mucilaginous, crystalliferous, tegmen becoming crushed, exotegmic cells fibrous, not lignified; cotyledons thick, accumbent; n also = 12.
3[list]/11: Salvadora (5). Africa (inc. Madagascar) to South East Asia and West Malesia, often in drier regions (map: from Aubréville 1974; Frankenberg & Klaus 1980; Trop. Afr. Fl. Pl. Ecol. Distr. 5. 2010; Malesian distribution rather optimistic, perhaps only in Java). [Photo - Habit, Fruits]
Chemistry, Morphology, etc. The stipules of Salvadora persica are described as being colleter-tipped (Ronse de Craene & Wanntorp 2009). Azima has two trace-one gap nodes to the bracts and bracteoles, Salvadora has bracts with 1:1 nodes (Kshetrapal 1970). R. A. Howard (pers. comm.) reported 1:2 nodes from both genera.
The flowers may be slightly monosymmetric and with a poorly developed petal-stamen cup. The gynoecium is probably originally bicarpellate and has parietal placentation, and if there appear to be two loculi it is because of the development of a structure perhaps comparable to the false septum of Batis (Ronse de Craene & Wanntorp 2009). Gynoecial morphology needs more study.
For general information, see Kubitzki (2002d), for wood anatomy, see Carlquist (2002a) and Saxena and Gupta (2011), for floral vascularization, see Kshetrapal (1970), for pollen, see Lobreau-Callen (1977) and Perveen and Qaiser (1996), for some embryology, see Maheswari Devi (1972), and for seed morphology, see Tobe and Raven (2012).
Synonymy: Azimaceae Wight & Gardner
[Emblingiaceae [[Pentadiplandraceae [Gyrostemonaceae [Borthwickiaceae + Stixaceae + Resedaceae]]], Tovariaceae, [Cleomaceae [Capparaceae + Brassicaceae]]] / core Brassicales: Glucosinolates also from tryptophane [= indole glucosinolates]; cisternae of endoplasmic reticulum dilated and vacuole-like; cuticle wax crystalloids 0; inflorescence terminal, bracteoles 0; floral development open; nectary outside A; ovules in two rows; endotesta crystalliferous; 3' rbcL extension.
Evolution. Divergence & Distribution. Ronse de Craene and Haston (2006) suggest a number of other characters that may be synapomorphies for this clade, including floral symmetry and embryo development. Nectary morphology and absence/presence/position are very variable in Brassicales outside this core group.
Genes & Genomes. It is possible that the At-ß genome duplication is to be placed at this node; it is absent from Carica (Barker et al. 2009: sampling). This duplication is dated to ca 50 m.y. (Woodhouse et al. 2011).
Chemistry, Morphology, etc. Whether or not Emblingiaceae have indole glucosinolates is unknown; only small quantities have been reported from Pentadiplandra (references in de Nicola et al. 2012). For quaternary ammonium compounds, see McLean et al. (1996).
Phylogeny. Relationships within this clade are finally beginning to be resolved. Of the sampled Stixeae (ex Capparaceae), the Asian Tirania was close to Gyrostemonaceae and the New World Forchhammeria perhaps closer to Resedaceae (Hall & Sytsma 2000, 2002; Hall et al. 2002), or both may be associated with Resedaceae (Hall et al. 2004: relationships depend on the gene sequenced). Stixis, Borthwickia, and Neothorelia are the other genera involved. All had been excluded from Capparaceae (Kers 2002), but whether they needed to be placed in a separate family was unclear. Su et al. (2012) not only found some (60% bootstrap, 0.99 p.p.) support for Pentadiplandraceae as sister to the [Gyrostemonaceae + Resedaceae] clade, but there was strong support for [Borthwickia [Gyrostemonaceae + Resedaceae], the Resedaceae area including a well-supported [Tirania + Stixis] clade and Forchammeria; Neothorelia was not sampled. However, the position of Tovariaceae is unclear, being either sister to Pentadiplandraceae, etc (Marín-Bravo et al. 2009) or to Capparaceae et al. (Su et al. 2012), although in both cases with little support.
Classification. Small families are being added in this area because some fugitives from the old Capparaceae are finding homes here. These families are simply convenient spots for aggregating information.
EMBLINGIACEAE Airy Shaw Back to Brassicales
Subshrub; plant hispid; mustard oils?; cork cambium deep-seated; cambium storying?; sclereids +; leaves ± opposite, lamina margins ± entire; flowers axillary, monosymmetric, median K abaxial, K connate, lobed, deeply divided adaxially, C 2, abaxial, connate by epidermis, slipper-shaped, ?not clawed; nectary abaxial, androgynophore +, curved abaxially; A 4, abaxial, staminodes 4, adaxial, forming a torus, median members of both whorls absent; pollen with short colpi with rounded ends and bulging apertures, adjacent exine thickened; G [2-3], placentation axile, stigma shortly lobed; ovule 1/carpel, basal, ?morphology; fruit indehiscent, pericarp thin; seed arillate, testa thick; endosperm ?type, scanty, embryo color?, hypocotyl short; n = ?
1[list]/1: Emblingia calceoliflora. W. Australia (map: from FloraBase 2004).
Chemistry, Morphology, etc. The plant dries yellowish. There has been considerable disagreement over the floral structure. Is the flower resupinate or not? Is the hood petal-like or not? Are there one or three carpels? I largely follow Melville's interpretation (in Erdtman et al. 1969), see also Mueller (1860). Detailed studies of all aspects of this plant are needed, nevertheless, its embryo is curved, its flowers monosymmetric, and its nectary is between the petals and stamens, all features appropriate for a position around here.
For general information, see Kubitzki (2002d) and Ronse de Craene and Wanntorp (2009: stipules present, reduced).
Previous Relationships. Emblingia was included in Polygalaceae by Cronquist (1981) and Polygalales by Takhtajan (1997) based on apparent floral similarities. Savolainen et al. (2000b) placed Emblingiaceae in Gentianales in a molecular study.
[[Pentadiplandraceae [Gyrostemonaceae [Borthwickiaceae + Stixaceae + Resedaceae]]], Tovariaceae, [Cleomaceae [Capparaceae + Brassicaceae]]]: (glucosinolates chain-elongated BCAAs); stipules +, minute; gynophore +, short; ovules in two ranks [?level], outer integument 2(-3) cells across; exotegmen fibrous.
Age. The age for this node is estimated to be 42-33 m.y. (Wikström et al. 2001) or (68-)57, 54(-45) m.y. (Hall et al. 2010).
Animal-Plant Interactions. The larvae of Chrysomelidae-Alticinae beetles are quite commonly to be found on members of this clade (Jolivet 1988).
Chemistry, Morphology, etc. For details on glucosinolate variation - quite extensive - within this clade, see Mithen et al. (2010). The wood anatomy of Brassicaceae and Resedaceae is rather similar (Schweingruber 2006). For stipules, see Weberling (2006).
In Pentadiplandraceae, Brassicaceae and Tovariaceae the lateral sepals are initiated before the median sepal (Ronse Decraene 2002). Nucellar tracheids have been reported in Capparaceae and Resedaceae, at least (Werker 1997).
For ovule type and the different mechanisms by which the ovule becomes campylotropous, see Boesewinkel (1990) and Bouman and Boesewinkel (1991), for bracteoles, see Ronse Decraene (1992).
[Pentadiplandraceae [Gyrostemonaceae [Borthwickiaceae + Stixaceae + Resedaceae]]]: K valvate; gynophore short, placentation axile, stigma lobed.
PENTADIPLANDRACEAE Hutchinson & Dalziel Back to Brassicales
Shrubs or lianes; benzyl- and 4-methoxybenzyl glucosinolates +, ellagic acid?, tannins?; ?cork; ?wood; nodes 3:3; mucilage cells +; lamina margin; inflorescence axillary, subcorymbose; flowers polygamous, 5-merous; K imbricate, C base enlarged, concave, connivent, limb flat; short andogynophore/nectary; staminate flowers: A 9-13, connective shortly produced; pistillode +; carpellate flowers: staminodes +; G [3-5], opposite sepals, style long; ovules 3-10/carpel, type?; fruit a berry; 1 seed/loculus, coat with layer of white, wooly, elongated cells towards outside ["seed pubescent"], exotegmen not fibrous; embryo white; n = ?
1/?1: Pentadiplandra brazzeana. Tropical W. Africa (map: from Hall et al. 2004; Trop. Afr. Fl. Pl. Ecol. Distr. 5. 2010).
Chemistry, Morphology, etc. The fruit contains the sweet-tasting protein, brazzein (also described as having the flavour of a horseradish...). The plant does not dry dark.
Are there supernumerary buds? There are bordered pits in wood fibres and mucilage cells in the leaf epidermis (Boodle, K, ms.). Embryologically - and in many other respects - Pentadiplandra is poorly known, although Ronse Decraene (2002) described its floral anatomy; Ronse de Craene and Haston (2006) suggest that its floral morphology is close to the ancestral form of the core Brassicales. There are no marginal or placental strands in the ovary.
For general information, see Bayer and Appel (2002), for glucosinolates, see de Nicola et al. (2012), and for embryo colour, Martin Cheek (pers. comm.).
Previous Relationships. Cronquist (1981) included Pentadiplandra in his rather broadly circumscribed Capparaceae, Takhtajan (1997) segregated it as a family.
[Gyrostemonaceae [Borthwickiaceae + Stixaceae + Resedaceae]]: idioblastic myrosin cells 0; hairs unicellular; K valvate; styluli +; seeds arillate.
Evolution. Pollination Biology & Seed Dispersal. Posession of myrmecochorous seeds may be an apomorphy at this level. However, Borthwickia is largely unstudied and seed ecology of Stixaceae is little known.
Classification. If the number of small families around here gets out of control, this whole clade could reasonably be included in a single family.
GYROSTEMONACEAE A. Jussieu, nom. cons. Back to Brassicales
Trees to shrubs; stomatal myrosin cells 0, tannins?; cork subepidermal; wood storied; multiseriate rays +; petiole bundle arcuate; leaf vernation flat, (blade amphistomatal), (stipules 0); plants usu. dioecious, inflorescence various; flowers small; P +, uniseriate, connate, 4-8-lobed or not; axis flattened, disc-like; staminate flowers: A 6-many, in 1 or more whorls around axis, centripetal, anthers ± sessile; pollen tricolpate, ektexine spongy, undifferentiated; pistillode 0; carpellate flowers: staminodes 0; gynophore 0, G (1 [2-)many], borne around axis in 1 (2) whorls, connate or not, when G 2, transverse, (styluli marginal), stigmas decurrent, large and spreading or not; ovule 1/carpel, apical, apotropous; fruit a dry or succulent schizocarp (achene; syncarp), calyx persistent; endosperm copious, embryo color?; n = 14.
5[list]/18+: Gyrostemon (12). Australia, not in the north (map: see Fl. Austral. 8. 1982).
Evolution. Divergence & Distribution. Fossils of Gyrostemonaceae have been reported from the early Miocene ca 20 m.y.a. from New Zealand (D. E. Lee et al. 2001).
Pollination Biology & Seed Dispersal. Gyrostemonaceae are wind-pollinated; the seeds are myrmecochorous (Lengyel et al. 2010).
Chemistry, Morphology, etc. The perianth is uniseriate.
For general information, see Goldblatt et al. (1976) and George (2002d); for gynoecial orientation, see Friedrich (1956), for floral development, see Hufford (1996), for pollen, see Tobe and Takahashi(1995).
[Borthwickiaceae + Stixaceae + Resedaceae]: A many; style/styuli at most short..
BORTHWICKIACEAE Su, Wang, Zhang & Chen Back to Brassicales
Small tree; ?anatomy; ?hair type; leaves opposite, trifoliate, lamina margins entire, stipules 0; flowers 5-8-merous; K connate; C not clawed, but proximal and distal parts differentiated; androgynophore +, short; filaments long; pollen exine perforate; G [4-6], ribbed, stigma undivided; ovules many/carpel, ?morphology; capsule ?septifragal; ?aril; n = ?
1/1 [list]: Borthwickia trifoliata. China (southwest Yunnan) and adjacent Myanmar.
Chemistry, Morphology, etc. The seeds are described as being 4-6/capsule and the embryo as scarcely differentiated by Zhang and Tucker (2008), but this must be incorrect.
For general information, see Su et al. (2012).
STIXACEAE Doweld Back to Brassicales
Shrubs or climbers; successive cambia +; vestured pits +; tracheids +; multiseriate rays +; conjunctive tissue with sclereids containing crystals; cortical sclereids +; leaves simple (trifolioliate), secondary veins ascending, (spines in the stipular position); (flowers axillary - Neothorelia); K 4-8, C 0, 6; pollen exine reticulate; G [2-4], placentation axile, (style short), stigma lobed; ovules (1) 2-several/carpel; fruits fleshy, ?drupes; ?aril; ?seed coat; cotyledons incumbent, (strongly anisocotylous); (germination hypogeal); n = ?
4/20: Forchhammeria (10), Stixis (7). Southeast Asia, Central America. (map: from Jacobs 1960, Forchhammeria green, from Hansen 1977)
Chemistry, Morphology, etc. Forchhammeria contains methyl glucosinolates like those of Capparaceae and Cleomaceae (Mithen et al. 2010).
Tirania has six sepals and petals; Forchhammeria has two carpels, as well as an irregular number of sepals (see Gyrostemonaceae), no petals, one ovule/carpel, and only one ovule/fruit usually develops.
For additional information, see Carlquist (1988), Hansen (1977: Forchhammeria), and Carlquist et al. (2014: much anatomical detail), also Su et al. (2012: table comparing the genera), and also Kers (2002: general, he was clearly not happy having the genera in Capparaceae.
Neothorelia and Tirania are particularly poorly known.
RESEDACEAE Martinov, nom. cons. Back to Brassicales
Herbs (shrubby); stomatal myrosin cells 0, BCAA glucosinolates 0, tannins 0; cork?; multiseriate rays +; no bordered pits in imperforate tracheary elements; lamina margins entire to pinnatifid, (stipules 0); flowers monosymmetric, hypanthium short or 0; K (4-)6(-8), C valvate, (0, 2, 4-)6(-8), unequal, the adaxial largest, ligule at junction of claw and limb, limb ± fringed or not; nectary esp. pronounced adaxially, (bipartite), disciform to almost petal-like; A 3-many, from ring primordium and centrifugal, basally connate or not; exine reticulate; (gynophore 0), G [(2-)3-6(-8)] (± free), opposite sepals or when 3, median member often adaxial, often open apical-adaxially, placentation often parietal, styluli often ± marginal, at most short; ovules (1-)several/carpel, to 3-seriate, (bistomal), inner integument 3-4 cells across, (parietal tissue none), hypostase +; fruit with apical opening within the styles, (follicle; berry), calyx persistent; (aril 0), endotestal cells cuboid, ± thickened, unlignified, with crystals, exotegmic cells elongated, lignified [palisade in t.s.], (thickening U-shaped; overgrown), endotegmen (with thick cellulose walls), crystaliferous; n = 5-15.
3[list]/75: Reseda (68). Warm temperate and dry subtropical, esp. Mediterranean-Middle East-North African, also southern Africa, S.W. North America and S.W. China (all Oligomeris) (map: see Meusel et al. 1965; Frankenberg & Klaus 1980; Hultén & Fries 1986; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; Martín-Bravo et al. 2009). [Photo - Flower.]
Age. Crown-group Resedaceae have been dated to (13.5-)12.6, 10.5(-8.7) m.y.a. (Martin-Bravo et al. 2009).
Evolution. Divergence & Distribution. Martín-Bravo et al. (2007) discuss the phylogeny and biogeography of the family. Oligomeris, native to both the Old and New Worlds (western), shows a considerable disjunction (Martín-Bravo et al. 2009).
Pollination Biology & Seed Dispersal.The seeds of Reseda are myrmecochorous (Lengyel et al. 2010).
Chemistry, Morphology, etc. Ochradenus has C 0, A many, [G 3], the carpels are ultimately closed, and the fruit is berry-like - c.f. Gyrostemonaceae (Hufford 1996). The androecium of Reseda luteola may be in 3-4 whorls (for references, see Abdallah 1978), c.f. Gyrostemonaceae again. The appendages on the seeds are also described as being caruncles.
For general information, see Abdallah (1967), Abdallah and de Wit (1979) and Kubitzki (2002d), for wood anatomy, see Carlquist (1998a) and Schweingruber (2006), for stipules, see Weberling (1968), for floral development of Reseda lutea, see Leins and Sobick (1977), and for some seed/ovule anatomy, see Guignard (1893) and Singh and Gupta (1967: comparison with Violaceae).
Phylogeny. From the topology of the tree presented by Martín-Bravo et al. (2007), there are three main clades - [Caylusea [Sesamoides + Reseda]], Reseda including both Ochradenus and Oligomeris.
Classification. It makes sense to recognise the three clades as separate genera.
Synonymy: Astrocarpaceae A. Kerner
TOVARIACEAE Pax, nom. cons. Back to Brassicales
Herbs to shrubs; glucosinolates not from phenylanaline or tyrosine, tannins?; cork?; no bordered pits in imperforate tracheary elements; leaves trifoliolate, margins entire, stipules cauline or on leaf base; flowers (6-)8(-9)-merous; stamens = and opposite sepals; G [(5-)6(-8)], alternating with K, placentation ± axile, style short, stigmas lobed, spreading; ovules many/carpel, in several ranks, micropyle zig-zag, inner integument ca 3 cells across, parietal tissue ca 2 cells across, funicle long; fruit a berry; exotestal cells ± enlarged, tanniniferous, walls thickened, endotestal cells small, exotegmic cells fibrous, walls reticulately thickened; endosperm thin, embryo color?; n = 14.
1[list]/2. Tropical America (map: see Hall et al. 2004). [Photo - Flower, Fruit]
Chemistry, Morphology, etc. The ovules are ± anatropous, but become campylotropous by the post-fertilization development of the exotegmen, and nucellar tissue to the side of the embryo sac is less than in Capparaceae, etc. (Mauritzon 1934g; Boesewinkel 1990).
For general information, see Appel and Bayer (2002).
[Capparaceae [Cleomaceae + Brassicaceae]]: sinapine [alkaloidal amine], methyl glucosinolates (also from methionine - aliphatic glucosinolates), erucic acid [fatty acid] +; stomatal myrosin cells 0, cisternae of endoplasmic reticulum as vacuoles and utricles [organelle-like]; roots lacking mycorrhizae; cork also cortical; pits vestured; nodes also 3<:3< [as in Brassica!]; eglandular hairs simple, unicellular [?level]; leaves simple to palmately compound, blades usu. conduplicate, margins pinnately lobed to entire; flowers 4-merous, (monosymmetric); K 4, C 4; A from 4 primordia, centrifugal, longer than the petals, filaments articulated; gynophore long, carpels 2 (more), placentation parietal, placental strands well developed, stigma lobed or subcapitate; ovules many/carpel, micropyle zig-zag (bi-, endostomal), (parietal tissue 0[?]); K deciduous; testa 2-layered, exotesta palisade or not, tanniniferous, endotesta with inner walls ± thickened, tegmen multiplicative, endotegmen tanniniferous, lignified (or not); endosperm ³2 cells across, cotyledons accumbent or incumbent, radicle in pocket formed by testa.
Age. The divergence between Capparaceae and the [Cleomaceae + Brassicaceae] clade has been dated to around 31-24 m.y. (Wikström et al. 2001), while other estimates are older, e.g. divergence at ca 41 m.y. (Schranz & Mitchell-Olds 2006), at ca 39.6 m.y. (Magallón et al. 2013), and at (55-)43, 41(-30) m.y. (Bell et al. 2010). Beilstein et al. (2010) suggest a still older age of (83.2-)71.3(-59.7) m.y.a., so clarification here, as elsewhere, is in order.
Evolution. Divergence & Distribution. Rodman et al. (1996) listed 11 possible apomorphies for this node; Iltis et al. (2011) also suggested apomorphies around here.
Plant-Animal Interactions. Pierid caterpillars (Pieridae-Pierinae - the whites - there are ca 840 species) are notably common on members of this clade (see also Beilstein et al. 2010, also above). For details of the interactions of butterflies and plants, see Courtney (1986) and Chew (1988 and references).
Ca 1,000 species are susceptible to pseudoflower-forming rust fungi, Puccinia spp. (Roy 1993, 2001); see especially Brassicaceae. The oomycete Albugo s. str., a white blister rust, parasitizes members of this clade (and also Convolvulaceae - Albugo s.l.), Albugo candida occuring on members of all three families (Choi et al. 2009; Thines & Voglmayr 2009; Ploch et al. 2010a).
Chemistry, Morphology, etc. The distributions of root hairs and of methyl glucosinolates, and variation patterns in seed coat anatomy are a little odd. Both Brassicaceae and Resedaceae have glucosinolates derived from elongated amino acid chains, as do Tovariaceae, Gyrostemonaceae, and Resedaceae (Kjær 1973; esp. Fahey et al. 2001; Mithen et al. 2010). Wasabia japonica in Brassicaceae has a glucosinolate similar to those in Cleomaceae and Capparaceae, and an aromatic glucosinolate of Cleomaceae and Capparaceae is also found in Resedaceae. Quaternary ammonium compounds, including betaines, are common in both Capparaceae and Cleomaceae, while Forchhammeria (Stixaceae) has methyl glucosinolates with a similar distribution; quaternary ammonium compounds have not been detected in Pentadiplandra or Emblingia - or Buhsia (Capparaceae: McLean et al. 1996).
True blue or red flowers are very rare in the whole group. Campylotropy is by the inpushing of the chalazal bundle. The ventral carpellary bundles are fused and weakly developed (Ronse de Craene & Haston 2006). Guignard (1893) provides details of ovule and especially seed anatomy.
Phylogeny. Relationships are [Capparaceae [Cleomaceae + Brassicaceae]], for further details, see Hall and Sytsma (2000) and Hall et al. (2002). Vaughan and Whitehouse (1971) suggested that Brassicaceae differ from Capparaceae (inc. Cleomaceae) in that the latter have a testa that is only two (not three) cell layers thick, a persistent tegmen (rare) and an endosperm more than one cell layer thick. Judd et al. (1994) provide a morphological phylogeny for Brassicaceae and Capparaceae sensu latissimo.
Classification. Cruciferae/Brassicaceae s. str., cabbage and mustard, have always been considered as one of the most natural plant families, however, their recognition makes Capparaceae s.l. (= Capparaceae s. str. + Cleomaceae) paraphyletic. So the alternatives are to have one family (Brassicaceae s.l.); three families; or two families, a Brassicaceae including Cleomoideae and a Capparaceae. The second option is followed here (see also A.P.G. 2009; Iltis et al. 2011).
CAPPARACEAE Jussieu, nom. cons. Back to Brassicales
Trees and shrubs (herbs; twining lianes); root hairs 0; pyrrolidine alkaloids +; (successive cambia +); petiole bundle annular or arcuate; sclereids +; (inflorescence fasciculate); flowers often monosymmetric; (K + C tube +), (K connate), C (0); (nectary elongated - Cadaba); A (1-)4-8(-many and centrifugal); pollen surface variously sculpted; G [2-12], (when 2, superposed-oblique), (placentation axile), (secondary septae +), (style +); inner integument 3-6 cells across, parietal tissue ca 4 cells across; fruit a berry (transversely schizocarpic; septicidal); seeds 5-30 mm long; (endotesta with crystals), tegmen to 6 layers thick, exotegmen radially enlarged, sclerified, endotegmen with lignified bands on anticlinal walls, or most tegmic cells lignified; radicle-hypocotyl short, cotyledon texture and folding variable; n = (7-)10(-15+); 6 bp insertion in ndhF gene.
16 [list]/480: Capparis (250), Maerua (100), Boscia (37), Cadaba (30). Largely tropical (map: from Jacobs 1960; Frankenberg & Klaus 1980; Wickens 1976; Fl. Austral. 8. 1982; Jalas & Suominen 1991; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; Culham 2007 [New World]). [Photo - Flower, Fruit.]
Evolution. Ecology & Physiology. Capparaceae are notably prominent in seasonally dry tropical forest (Pennington et al. 2009).
Chemistry, Morphology, etc. Crateva has glands (?colleters) at the base of the lamina. Some Capparaceae have supernumerary buds and dry yellowish.
For general information, see Kers (2002), for some information on floral development, see Leins and Metzenauer (1979) and Ronse Decraene and Smets (1997a, b), and for embryology, see Mauritzon (1934g) and Narayana (1962b).
Phylogeny. A paraphyletic Crateva is strongly supported as being sister to the rest of the subfamily; Capparis is probably diphyletic (Hall et al. 2002; Hall 2008). New World Capparaceae have several distinctive and perhaps unique glucosinolates (Mithen et al. 2010).
Classification. Hall (2008) discusses generic limits in Capparaceae, which are in need of substantial work; for example, New World Capparis will need a new name.
Previous Relationships. This used to be a rather heterogeneous family, including Stixeae (see Stixaceae), Setchellanthus (Setchellanthaceae), Pentadiplandra (Pentadiplandraceae), and Koeberlinia (Koeberliniaceae). At least all are members of Brassicales!
[[Cleomaceae + Brassicaceae]: herbaceous annuals (shrubs); inflorescence ± corymbose, (bracts foliaceous); A 6; fruit septicidal, persistent placental strands + [replum] (0); seeds 0.5-4 mm long.
Age. Beilstein et al. (2010) suggest that this node is (76.5-)64.5(-54.4) m.y. old, while the estimate in Bell et al. (2010) is (43-)33, 31(-21) m.y. old. Other estimates are 23-18 m.y. old (Wikström et al. 2001), some 41 m.y. old (Schranz & Mitchell-Olds 2006), (45-)19(-1) m.y. (Franzke et al. 2009: 95% HPD), and some 50 m.y. (Al-Shehbaz et al. 2006).
Evolution. Divergence & Distribution. The inflorescence of Cleomaceae may be a corymb and there are usually 6 stamens (e.g. Podandrogyne - also with orange flowers and 3-foliolate leaves), just like Brassicaceae, however, the stamens are rarely tetradynamous (but see Cleome africana). The flowers are also sometimes initially disymmetric, as in Brassicaceae, but the basal condition for Cleomaceae may be monosymmetry even early in development, with the abaxial sepal much enlarged and more or less covering the rest of the developing flower - almost cochleate aestivation (Patchell et al. 2010, esp. 2011). However, there are a variety of floral morphologies in Brassicaceae (what about Aethionema?) and although the phylogenetic structure at the base of Cleomaceae is being teased apart (Patchell et al. 2014), where details of symmetry changes go on the tree remain to be established; monosymmetric flowers are scattered throughout core Brassicales.
Nozzolillo et al. (2010) thought that there were distinctive similarities in how colours in flowers of at least some Cleomaceae and Brassicaceae changed with age; a focus of comparative work in this clade is to understand floral development in Arabidopsis and other Brassicaceae better (Bhide et al. 2014).
Ecology & Physiology. For a major reduction of plant height at this node, see Cornwell et al. 2014).
Genes & Genomes. Bhide et al. (2014) studied gene and genome evolution, finding over 2,000 new genes in this clade (compared with Carica, including genes lost in one of the two members of Brassicaceae included). The rate of molecular evolution of two herbaceous groups of this clade studied is notably higher than that of woody rosids (Barker et al. 2009).
Chemistry, Morphology, etc. Some Cleomaceae and Brassicaceae have similar acylated anthocyanins (Jordheim et al. 2009). For foliaceous bracts, see Eichler (1878) and Prenner et al. (2009). For floral development, see Leins (2000, and references).
CLEOMACEAE Berchtold & J. Presl Back to Brassicales
Root hairs 0; petiole bundle(s) arcuate to forming a ring; leaves palmately compound (simple), (stipules 0); bracts foliaceous (not); (plant monoecious - Podandrogyne s. str.); flowers monosymmetric (weakly so), (androgynophore +); (C toothed); (A 5 + 1 staminode; 1 + 4 staminodes; several), anthers coiled at dehiscence, linear; pollen surface variously sculpted, often spinulose; (G , orthogonal), (gynophore 0); inner integument 2-10 cells across, parietal tissue 2-5 cells across, (nucellar cap ca 2 cells across), (endothelium +); (fruit indehiscent); seeds (arillate); exotegmen cells radially enlarged, sclerified, endotegmen cells with lignified bands on periclinal walls; (suspensor massive, haustorial), radicle-hypocotyl long, cotyledons incumbent; Tr-α genome triplication; n = ³9.
10 [list]/300: Cleome (275: including Podandrogyne). Tropical and warm temperate, esp. America (map: see Wickens 1976; Fl. Austral. 8. 1982; Jalas & Suominen 1991; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; some from Culham 2007). [Photo - Inflorescence, Flower.]
Evolution. Divergence & Distribution. Soltis et al. (2009) suggested that diversification in Cleomaceae might be connected with the α genome triplication (see below); see also S. Cheng et al. (2013).
Biogeographic relationships in Cleomaceae are interesting. A smallish North American clade is sister to the rest of the family, but it is surrounded by Old World clades both inside and outside (Brassicaceae-Aethionemeae) the family (see Patchell et al. 2014 in part).
Ecology & Physiology. There are a few species of Cleome with C4 photosynthesis, e.g. C. gynandra. Photosynthesis with carbon dioxide-concentrating mechanisms may have evolved four times in the genus, at least three of which are C4 types, and there are also C2 intermediates (Feodorova et al. 2010; see also Voznesenskaya et el. 2007 for details of the photosynthetic characterizations; Christin et al. 2011b for some dates; Patchell et al. 2014); proto-Kranz species are also known here (R. Sage et al. 2014). Koteyeva et al. (2011a, c) describe the C4 morphologies involved, which include radiating chlorenchyma surrounding both individual vascular bundles and groups of vascular bundles (see also Koteyeva et al. 2014 and references). Increased venation density in the C4 plants may be connected with a delay in differentiation of the mesophyll cells (Külahoglu et al. 2014). Brown et al. (2011: p. 1438) noted that "functionally equivalent mechanisms that control the accumulation of proteins important for C4 photosynthesis" had evolved in parallel in Cleome gynandra and in maize, and root endodermal cells seem to have been coopted in bundle sheath development in both (Külahoglu et al. 2014).
Genes & Genomes. A duplication (hexaploid), the Cs-α or Th-α duplication, of the genome occurred ca 13.7 or 20 m.y.a. (Schranz & Mitchell-Olds 2006; Barker et al. 2009; van der Bergh et al. 2015). Genome size is about twice that of Arabidopsis thaliana, which seems reasonable (c.f. Bhide et al. 2014).
Chemistry, Morphology, etc. Ronse Decraene and Smets (1993b) suggested that the four petals of this clade were equivalent to four outer diagonally-inserted stamens.
For general information, see Kers (2002: in Capparaceae), for anther dehiscence, see Mitchell-Olds et al. (2005), for pollen and seed, see Sánchez-Acebo (2005 and references), and for embryology, see Mauritzon (1934g: Polanisia trachysperma has a huge suspensor cell) and Sachar (1956b).
Phylogeny. Relationships within Cleomaceae have had rather little support, but Cleome itself appears to be widely scattered on the tree (Hall 2008). An ITS study with quite broad sampling recovered a highly paraphyletic Cleome; rooting was somewhat of a problem and there was little support for the backbone but guite good support for much of the finer detail (Feodorova et al. 2010). A 5-marker 3-genome analysis, the most comprehensive yet, found stronger support from the chloroplast markers than from ITS: A group of North American Cleomaceae were sister to the rest of the family and the C. droserifolia group and Cleome s. str. (c.f. Feodorova et al. 2010) were successively sister to the remainder (Patchell et al. 2014: q.v. for further details).
For phylogenies of parts of the family, see Sánchez-Acebo (2005), Catalan et al. (2007), Inda et al. (2008b) and Riser et al. (2013).
The small-flowered Dipterygium, placed in Capparaceae in a subfamily by itself by Kers (2002), is to be included here; it is well embedded in the family in a clade with some other Old World taxa (clade 6 of Patchell et al. 2014). It has six stamens that are all equal in length, a filiform style, a winged, 1-seeded nut, and incumbent cotyledons; methylglucosinolates are recorded from the plant (Hedge et al. 1980).
Classification. Generic limits are very unsatisfactory and need attention (see e.g. Hall et al. 2008; Riser et al. 2013). Many of the clades do not even correspond to earlier sections of Cleome, however, the wholesale dismemberment of Cleome that is under way seems poorlyl advised; piecemeal splitting is not a course that I would have taken. Patchell et al. (2014) provide a careful outline and analysis of what has been done and what may still need to be done (see also Feodorova et al. 2010). Basically, things are currently in a mess.
Synonymy: Oxystylidaceae Hutchinson
BRASSICACEAE Burnett, nom. cons.//CRUCIFERAE Jussieu, nom. cons. et nom. alt. Back to Brassicales
(Nortropane alkaloids +), methyl glucosinolates 0, methionine-derived glucosinolates +; cork ?always deep-seated; stomata anisocytic; (leaves deeply pinnately lobed), stipules 0; floral development closed, flowers disymmetric; stamens about as long as petals, the two outer shorter than the four inner [tetradynamous]; lateral nectary lobes outside inner A, etc.; pollen grains tricellular, with tryphine, surface often reticulate; gynophore short; ovary with commissural septum [= false septum, replum], stigma commissural; ovules slender, outer integument 2-4(-5) cells across, inner integument (2-)3-8(-15) cells across, endothelium +, parietal tissue ca 1 cell across, hypostase +; (megaspore mother cells several); commissural septum persistent in fruit; testa 3-layered, exotestal cells reticulately thickened on radial walls, often mucilaginous, endotesta lignified, thickenings U-shaped or on anticlinal walls alone, (unthickened), without crystals, (tegmen not multiplicative), not persistent; chalazal endosperm cyst +, endosperm 1-layered, embryo folded, (spiral), radicle-hypocotyl short to long, radicle not in testal pocket; n = (4-)8(-13); duplication of PHYB → PHYD gene; sporophytic self-incompatibility system present.
338[list]/3710 - three groups below. World-wide, esp. N. temperate and drier areas. [Photos - Collection].
Age. Crown group diversification, separation of Aethionemeae from the rest, occurred perhaps ca 40 m.y.a. (Al-Shehbaz et al. 2006, see also Koch 2011). Other estimates are (35-)15(-1) m.y. (Franzke et al. 2009: 95% HPD) or (49.4-)37.6(-24.2) m.y. (Couvreur et al. 2010: also summary). Beilstein et al. (2010) suggested an age of (64.2-)54.3(-45.2) m.y. for crown group Brassicaceae. These very different ages are reflected in differences in dates of diversification within tribes, ancient hybridization events, etc. (see below).
Couvreur et al. (2010) reasonably thought that the fossil Dressiantha might not belong to core Brassicales, or even to Brassicales at all (see above).
1. Aethionemeae Al-Shehbaz, Beilstein & E. A. Kellogg
Plant glabrous; nortropane alkaloids +; 3 veins on petal claws, nectaries 2, lateral, (1-)2-4(-8) ovules/carpel; (plant heterocarpic), fruit angustiseptate; (testa mucilaginous); n = 7, 8, 11, 12, 14...
1-2/70. The Mediterranean and Southern Europe to Afghanistan (map: from Hedge 1976). [Photo - Flowers.]
Age. Estimates for the age of crown-group Aethionemeae range from (28-)11(-1) m.y. old (Franzke et al. 2009: 95% HPD) to (54.3-)46.9(-39.4) m.y. (Beilstein et al. 2010).
[Cochlearieae + The Rest]: genome duplication [At-α, Br-α]; (interxylary phloem +).
Age. Koch (2012) suggested an age for this node of around (53.5-)49(-43) m.y., in line with the estimates of Beilstein et al. (2010).
2. Cochlearieae Buchenau
Plant ± glabrous; nortropane alkaloids +; nectaries 4; fruit angustiseptate; n = (7, 11), 12, (13).
2/30. The West Mediterranean, maritime Western Europe, circum-Arctic (map: from Hultén & Fries 1986; Koch 2012).
Age. Koch (2012) suggested crown group ages of (22.3-)13.8, 10.3(-3.3) m.y., depending on the gene used.
(Cardenolides - Erysimum); (methionine-derived glucosinolates 0); (included phloem +); (eglandular hairs branched, stellate, T-shaped); (flowers monosymmetric); (C fringed or lobed); A (2, 4, to 24), (long); tapetosomes with T-oleosin; (G stipitate), (commissural septum 0 - Pringlea), (style long); fruit angusti- or latiseptate; cotyledons also variants of conduplicate-incumbent, etc.
338/3710: Draba (365), Cardamine (200), Erysimum ([150-]225[-300]), Lepidium (230), Alyssum (195), Arabis (120), Boechera (110), Physaria (105: inc. Lesquerella), Rorippa (85), Heliophila (80), Isatis (80), Noccaea (80), Thlaspi (55), Biscutella (55), Matthiola (50), Descurainia (50), Hesperis (45), Sisymbrium s. str. (45: only Old World). World-wide, esp. N. temperate (diverse in the Irano-Turanian area, less so in E. North America), uncommon in humid lowland tropics (map: from Vester 1940; Hultén 1971; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003). [Photo - Flowers, Flowers, Fruit.]
Age. An age for this node (but see sampling) is 21-15 m.y. (Fiebig et al. 2004).
Synonymy: Arabidaceae Döll, Drabaceae Martynov, Erysimaceae Martynov, Isatidaceae Döll, Raphanaceae Horaninow, Schizopetalaceae A. Jussieu, Sisymbriaceae Martynov, Stanleyaceae Nuttall, Thlaspiaceae Martinov
Evolution. Divergence & Distribution. Couvreur et al. (2010: Table 3) give times of diversification of various clades within the family. Thlaspi primaevum, some 30.8-29.2 m.y. old, is known from Oligocene deposits in Montana (Manchester & O'Leary 2010); there are even impressions of the distinctive seeds on the capsule wall (Beilstein et al. 2010). However, the attribution of this fossil to the family, let alone the genus, has been questioned (Franzke et al. 2011). There are strongly conflicting ages for the same nodes (see Moazzeni et al. 2014 for literature).
Stem Brassicaceae may have been adapted to warm and humid conditions in the east Mediterranean area, then moving into more open and dry environments (Franzke et al. 2009). Alternatively, they may have originated in a tropical environment, subsequently radiating with the onset of aridification and global cooling in in the mid-Caenozoic (Couvreur et al. 2010). Most authors suggest that initial diversification was in the Old World, perhaps in the Irano-Turanian region from Turkey to Lake Balkhash where the family is very diverse (Hedge 1976; Franzke et al. 2009, 2011 and references; Karl & Koch 2013). Radiation of the lineages that encompass most of the extant diversity of the family seems to have been rather rapid, in line with the poor support along the backbone of the phylogeny (Beilstein et al. 2006; Al-Shehbaz et al. 2006; Bailey et al. 2006a, b; Couvreur et al. 2010).
Biogeographical histories within the family can be complex; see Koch and Kiefer (2006) for a summary of earlier work. Chloroplast and nuclear genomes of Californian and African ancestry are variously combined in Antipodean Lepidium (Dierschke et al. 2009). Kiefer et al. (2009) discuss the phylogeographic structure of the speciose largely North American Boechera (ex Arabis); divergence seems to be a Pleistocene phenomenon with considerable apomixis and hybridization, the latter even occuring between genera of Boechereae (Windham et al. 2014). The speciose crown-group Arabideae are perhaps around 14 m.y.o., but much diversification has been within the last 5 m.y., perhaps associated with the evolution of the perennial life style, associated movement into high-altitude habitats, and extensive polyploidization (Karl & Koch 2013: perennial → annual → perennial). Draba is a young polyploid complex in which there is considerable geographical structure in the distribution of diploids and polyploids, species with high ploidy levels being common in the Arctic and also at high altitudes, as in Arabis (Jordon-Thaden & Koch 2008; see also Jordon-Thaden et al. 2010). Relationships within the speciose Erysimum clades also show considerable geographic structure if little morphological support, diversification beginning around 3.5 m.y.a. (Moazzeni et al. 2014). There have been a number of very long distance dispersal events in Cardamine (Carlsen et al. (2009); although immediate ballistic dispersal is effective only over short distances, many taxa have mucilaginous seed coats which will aid longer distance transport (see below). For dates and place (N.E. Africa?) of diversification with Brassiceae, see Arias et al. (2014a). Salariato et al. (2014) discuss evolution in the South American Eudemeae, which divides into a northern and southern clade, with the cushion life form evolving independently in taxa growing in more extreme conditions in both clades.
Soltis et al. (2009) and Franzke et al. (2011) suggest that diversification in Brassicaceae may be connected with the At-α palaeopolyploidization (see also below); Couvreur et al. (2010) thought that the genome duplication occurred after the divergence of Aethionemeae. Schranz et al. (2012) suggested that there was a lag time between the At-α duplication event - they thought it characterized the whole family - and diversification in the family. Genome evolution is very rapid, especially in Brassica rapa, when compared with that in Carica, and this may be connected with differences in life histories, annual versus perennial (Xiaowu Wang et al. 2011).
Since Aethionema, with a more or less sessile gynoecium, is sister to all other Brassicaceae, similarities of Stanleya, etc., to Cleomaceae (e.g. long gynophore and stamens) are parallelisms (Galloway et al. 1998); these latter genera are well embedded in Brassicaceae (as Thelypodieae - Koch et al. 2012).
Ecology & Physiology. There is a notable decrease in seed mass and increase in leaf mass per area (SLA) in Brassicaceae. Members of the family quite often live in temperate, disturbed areas that are rather dry yet the preciptation that does fall is not very seasonal (Franzke et al. 2010; Cornwell et al. 2014).
Brassicaceae are noted hyperaccumulators of several unusual elements (Brooks 1998; Krämer 2010; Cappa & Pilon-Smits 2014), indeed, most angiosperms that are nickel and zinc hyperaccumulators are members of the family (see also Cappa et al. 2014b: hardly fair to compare Brassicaceae with Malpighiales or Asteraceae!). Brassicaceae are common on magnesium-rich dolomites and serpentines (Cecchi et al. 2010), indeed, Stanleya pinnata (see below) is phylogenetically close to a number of serpentine endemics and serpentine-tolerant species of Streptanthus and relatives, although not Streptanthus s. str. (Cacho et al. 2014). Overall, more than 100 species are involved in unusual/heavy metal tolerance, and there have been well over a dozen origins of the ability to accumulate such elements here (Cecchi et al. 2010; Krämer 2010). These and other metals they can accumulate may act as e.g. a feeding deterrent by themselves, or they may interact with other elements of the plant's defence system (Baker & Brooks 1989; Boyd 2007, Grennan 2009, and Anjum et al. 2012 for reviews). Some species actively forage for metals, root density increasing in areas of the soil where there is more metal (Qiu et al. 2012).
Selenium (Se), normally a sulphur antagonist, is accumulated by Stanleya pinnata and S. binnata (?species limits), but not other species of the genus, however, many of its immediate relatives, including Brassica napa, are selenium tolerant (Cappa et al. 2014b). Se may protect the plant against herbivory by prairie dogs and arthropods alike (Galeas et al. 2007; Freeman et al. 2009; Cappa et al. 2014a); S. pinnata incorporates Se into the non-protein amino acid methylselenocysteine (with a C-Se-C motif) and so is unaffected by it. There are also complex interactions with non-Se-accumulating plants in the same habitat, these sometimes growing better if associated with Se-accumulating plants, perhaps because of reduced herbivory, or growing worse, perhaps because of Se allelopathy (El Mehdawi et al. 2012 and refs).
Glucosinolate diversity in the family is considerable, as is variation in content between different brassicaceous species in the same community. The cost of glucosinolate production is considerable, being estimated at ca 15% of the total energy needed to synthesise the contents of a leaf cell (Bekaert et al. 2012). The level of polymorphism of defence gene alleles of Arabidopsis thaliana is related to the intensity of attack by specialist aphids (Züst et al. 2012). Both myrosin cells and glucosinolates are often localized along the veins in Brassicaceae, perhaps as a defence against herbivores damaging the vascular tissue, and glucosinolates may also be common towards the edges of the lamina and may help deter herbivores that eat from the edge inwards, as is quite common (Shroff et al. 2008; Shirakawa et al. 2014).
The presence of particular glucosinolates may induce oviposition by cabbage white (Pieris spp.) butterflies, whether or not the crucifer with those glucosinolates is edible or kills the caterpillar (Chew 1979, see also 1988); interestingly, the butterfly responds to the glucosinolate odour only after mating (Ikeura et al. 2010). Pieris brassicae prefers plants with glucosinolates over those in which glucosinolate-producing genes have been inactivated (Schweizer et al. 2013); caterpillars of cabbage white butterflies and the diamond-back moth (Plutella xylostella) are able to detoxify the glucosinolates produced when they damage plant tissue, converting them into non-toxic substances such as nitriles (Wittstock et al. 2004; Ratzka et al. 2002); Winde and Wittstock (2011) discuss these and other ways in which insects can avoid the harmful effects of glucosinolates. Parasitoids of the munching caterpillar are also attracted to the scene, and the interactions become very complex (Fatouros et al. 2008). Other insects such as the cabbage aphid, Brevicoryne brassicae, sequester glucosinolates, the aphid even producing its own myrosinases that break the glucosinolates down, so helping to deter potential predators (Kazana et al. 2007).
Any mycorrhizal associations in the roots of Brassicaceae are at best weak and facultative (Medve 1983). Thus although arbuscular mycorrhizae have been reported from Thlaspi, it is doubtful if an effective symbiosis results (Regvar et al. 2003). Indeed, glucosinolates can depress vesicular-arbuscular mycorrhizal activity, and this may help Alliaria petiolata be invasive in parts of North America (Wolfe & Klironomos 2005). See Windsor et al. (2005), Schranz et al. (2011) and Grubb and Abel (2006) for the diversity of glucosinolates and their metabolism, and for more on glucosinolates, see above.
There are a number of proto-Kranz species in Brassicaceae (R. Sage et al. 2014).
Arabidopsis thaliana can take up nitrogen in an organic form as amino acids (Hirner et al. 2006), although the general significance of this is unclear.
Pollination Biology & Seed Dispersal. Floral variation in the family is quite extensive, despite the rather stereotypical floral formula - K4, C4, A6, [G 2] - that we are all taught. The flowers of Iberis amara are monosymmetric, although the whole corymbose inflorescence is functionally more like a single polysymmetric flower with radiating petals - the two large petals of the outermost flowers (Busch & Zachgo 2007); selection on monosymmetric flowers will thus be at the functional level of the inflorescence. Genera like Streptanthus have strongly monosymmetric flowers borne on a more elongated axis. Ornithocarpus and Schizopetalum, for example, have more or less fimbriate petals, while those of Draba are bilobed. Flowers quite commonly change colour as they age (Weiss 1995). In general, flowers are visited by quite a variety of insects, an example being Hormathophylla spinosa, plants of which which were visited by 70 or more species of insects in 19 families and 5 orders over the over four-year study period (Goméz & Zamora 1999). Goméz et al. (2014) describe variation in polinators in 40 (35 in the figures) species of Erysimum in detail. 746 species of insects in 99 families and eight orders, assigned to 19 functional groups, were visitors; most species were visited by more than nine of these functional groups.
The sporophytic incompatibility system common in Brassicaceae has been much studied (e.g. Dickinson et al. 1998; Tarutani et al. 2010; Nasrallah 2011). Some of the components of the incompatibility system are in the distinctive tryphine covering the pollen grains, and this is produced by the individual pollen grains, so although the incompatibility system is described as being sporophytic, it is at least in part gametophytic in its genetics (Doughty et al. 1998; Dickinson et al. 2000). The incompatibility of Arabidopsis grains placed on a Brassica stigma can be removed by the action of Brassica tryphine (Dickinson et al. 2000). Indeed, brassicaceous pollen tubes seem singularly easily (mis)led; expression of a single Arabidopsis peptide involved in pollen tube guidance in a Torenia (Lamiales-Linderniaceae!) synergid directed the the pollen tube and allowed it to penetrate the Torenia embryo sac (Takeuchi & Higashiyama 2012).
More or less explosively dehiscent capsules are common in Brassicaceae, but the extotesta is often mucilaginous (e.g. d'Arbaumont 1890), helping either in the establishment of the dispersed seed when it rains, or the further dispersal of the seed if it becomes attached to animals (see Yang et al. 2012 for a review, many of the examples mentioned are from Brassicaceae). Several Brassiceae have heteroarthrocarpic fruits. These consist of an apical, indehiscent portion that does not differentiate into valve tissue, and a basal portion with typical valve-type tissue that may or may not be dehiscent (Hall et al. 2011); the two parts of the fruit may separate transversely and so the one plant can have very different dispersal mechanisms. Phylogenetic relationships in Brassiceae are uncertain, but heteroarthrocarpy is likely to have evolved more than once there (Hall et al. 2011); for the evolution of heteroarthrocarpy in Raphanus, see Avino et al. (2012).
Bacterial/Fungal Associations. The association between the pseudoflower-forming Puccinia rust and host has been much studied in Brassicaceae (Roy 1993 [particularly fine photograph], 2001; Ngugi & Scherm 2006). Insects come to the pseudoflowers, attracted both by the colouration of the leaves and floral fragrances. These latter differ from those of both of the crucifer host and the other plants in the general area, containing i.a. constitutively-released isothiocyanates (Raguso & Roy 1998). The insects pick up the rich fructose nectar secreted by the fungus along with the fungal spermatia, fly to another "flower", deposit the spermatia and pick up more. On combination of spermatia of the appropriate mating types, diploid aecia are produced, the "flower" stops producing nectar, and the "petals", i.e. the leaves, become green. Ruxton and Schaefer (2011) discuss the evolution of such associations.
The oomycete Albugo, the white blister rust, parasitizes a number of species of Brassicaceae (Ploch et al. 2010a), although it quite commonly also persists as a symptomless endophyte (Ploch & Thines 2011).
Genes & Genomes. Duplication of the whole genome, the Ata/At-α palaeopolyploidization, has been dated to 34-25 or 60-20/ca 25 m.y.a., fairly soon after the split of Brassicaceae from Capparaceae (Vision et al. 2000; Blanc & Wolfe 2004a; Barker et al. 2009; Woodhouse et al. 2011), and perhaps after the divergence of Aethionemeae (Blanc et al. 2003; de Bodt et al. 2005; Schranz & Mitchell-Olds 2006; Franzke et al. 2009; Galloway et al. 1998: pattern of duplication of the ADC [arginine decarboxylase] gene; c.f. Schranz et al. 2012). Getting the timing of the various genome duplications in Brassicaceae and also Capparaceae straight is important (S. Chang et al. 2013 and references).
X = 8 may be ancestral in the family (Lysack et al. 2006), x = 4 being the pre-Ata duplication genome (Franzke et al. 2010 and references). After this initial duplication, there has been extensive hybridization and further genome duplications (Vision et al. 2000; Kellogg & Bennetzen 2004; Blanc & Wolfe 2004a; Blanc et al. 2007; Lysack et al. 2007). Franzke et al. (2010) discuss genome duplication events in detail, suggesting that several remain to be discovered. The result of all the duplications is that apparently diploid species like Brassica oleracea, with n = 9, are hypothesised to be ancestral hexaploids, the hexaploidy event occurring between 10 and 5 m.y.a. (Mitchell-Olds et al. 2005; Lysack et al. 2005; Xiaowu Wang et al. 2011; Cheng et al. 2013). This is in addition to earlier duplications. The origin of the Brassiceae genome can thus be represented by 4x X 2x → 3x → 6x, where x = 7 (Cheng et al. 2013 and references). Jaillon and Eury et al. (2007) suggest that Arabidopsis has had two whole genome duplications, although there is some discussion as to exactly how many bouts of duplication have occurred. The origin of a trnF pseudogene has been associated with a duplication in the common ancestor of the Halimolobus + Boechera + Cardamine clade, some 21-16 m.y.a. (Koch et al. 2005).
Woodhouse et al. (2011) discussed gene transposition after the duplication event. There has been extensive transposition of genes in the Arabidopsis genome - between 1/4 and 3/4 of the genes may have moved some time after the origin of Brassicales as a whole (comparison with Carica: Freeling et al. 2008; see also Schranz et al. 2007). Lysack et al. (2009) found that genome size was not particularly linked to chromosome number, Xiaowu Wang et al. (2011) noting the extensive gene loss following genome triplication in Brassica, as in polyploidization events in general. The result of sequential duplications over the course of angiosperm history is that the genome of plants like Brassica napus is estimated to be 72x (Chalhoub et al. 2014), although its diploid chromosome number is 38. In Arabdopsis the extra copy of signal transduction and protein encoding genes tended to be kept and that of DNA repair and plant defence genes lost (Blanc & Wolfe 2004).
Genome duplications aside, details of karyotype evolution in the family are of considerable interest. Thus one major clade (lineage I) has x = 8, as does lineage II, while another clade that includes lineage II has x = 7, but with subsequent increase (Mandáková & Lysack 2008; Franzke et al. 2010).
Although "intergeneric" hybridisation is quite common in Brassicaceae (Warwick et al. 2006 for a summary), this is of uncertain significance given the problems with generic circumscriptions discussed below. However, Arias et al. (2014a) noted that hybdridization within Brassica involved members of clades that have been separate for around 18 m.y. (20 m.y. in the text), and intergeneric hybridization is also reported from Boechereae (Windham et al. 2014). There is extensive polyploidy and hybridization within Cardamine (Lihová & Marhold 2006).
The mitochondrial orf164 gene is derived from part of the nuclear ARF17 gene, and unusually for such transpositions, it is expressed in the mitochondrion (Qiu et al. 2015). It has so far been found only in Lineage I members - e.g. in Arabidopsis, but not in Brassica.
Chemistry, Morphology, etc. For tocopherols in Brassicaceae, see Goffman et al. (1999), see Brock et al. (2006) for nortropane alkaloids, Badami and Patil (1981) for seed fatty acids, Harborne (1999, but sampling) for distinctive sulphur-containing phytoalexins.
Bowman (2006) discussed morphology in general in the context of comparative developmental genetics. The border cells of the root cap dissociate in rows (Driouich et al. 2006); other Brassicales should be examined for this character. There are rarely glandular stipules in the inflorescence and elsewhere (see Weberling 2006 for a summary, also Bowman 2006).
C. Y. Huang et al. (2013) discuss the evolution of a cluster of tandem oleosin genes known from several Brassicaceae but that are unknown from Cleomaceae. These genes produce lipids that end up on the pollen surface; the pollen tolerates dehydration quite well. Exactly where this character should go on the tree awaits better sampling. Brassicaceae have tryphine covering the pollen grains, not pollenkitt, as in other angiosperms; in tryphine some constituents of the disorganised tapetal cells are still visible (Pacini & Hesse 2005). Details of the distribution of this feature are also unclear.
There is a long-standing controversy about the evolutionary origin of the six stamens in Brassicaceae: Did they arise by dédoublement or by reduction (Ronse Decraene & Smets 1993b for literature)? Stamen number in Brassicaceae may certainly sometimes increase, thus Megacarpaea polyandra can have 24 stamens. Another controversy concerns carpel number. The commissural stigmas of Brassicaceae have been supposed to be an indication that the gynoecium is basically 4-carpellate, but such stigmas are notably common in groups with parietal placentation. Similarly, normally-oriented bundles outside the inverted placental ventral carpellary bundle in Crataeva religiosa has been thought to indicate an original 4-carpellate condition with axile placentation (Dickison 2000, but c.f. Brückner 2000). However, flowers with four carpels are uncommon in Brassicales.
The chalazal endosperm cyst may be involved in the movement of metabolites into the developing seed, there being transfer cells around it (Brown et al. 2004). Guignard (1893) suggested that the seed coat of Lunaria was endotegmic; there was no lignification in the testa at all.
See Pammel (1897), Vaughan and Whitehouse (1971), Prasad (1975), Bouman (1975), and Khoul et al. (2002) for ovules and seed coat, and Erbar and Leins (1997a, b) and Leins and Erbar (2010) for floral development. See also Khalik et al. (2002) for pollen morphology, Abraham (1885) and Moïse et al. (2005) for seed coat structure and development, Brown et al. (2004) for endosperm cysts (Aethionema not sampled, cysts probably not in in Cleome, at least). Warwick and Al-Shehbaz (2006) summarize chromosome numbers. See Beilstein et al. (2006) for trichome evolution; Bernadello (2007) for nectary variation, and Schweingruber (2006) for phloem and xylem anatomy. Al-Shehbaz (1984), Appel and Al-Shehbaz (2002), Koch et al. (2003), Hurka et al. (2005) and Mitchell-Olds et al. (2005) contain general information.
Phylogeny. Over the last ten years or more, substantial progress has been made in providing a phylogenetic framework for the family (e.g. Koch et al. 2001: Koch 2003; Beilstein et al. 2006) and realigning taxa accordingly. Aethionema, a variable but poorly known genus with angustiseptate fruits, is usually sister to the rest of the family (e.g. Zunk et al. 1996, 1999; Koch et al. 2001; Beilstein et al. 2006); for its limits, see Khosravi et al. (2008). The relationships between many of the other tribes - and even the circumscription of some - are still in part unclear (Beilstein et al. 2006; Al-Shehbaz et al. 2006; Bailey et al. 2006a, b; Franzke et al. 2009; Mummenhoff et al. 2010; Zhao et al. 2010), but two main clades seem accomodate around 47 tribes. For a study of Alysseae and related tribes, see Warwick et al. (2008). Biscutelleae and some other tribes are unplaced, Alysseae may also be outside these two clades (Resetnik et al. 2013), Resetnik et al. (2013) looked at Alysseae in detail finding four four major clades, although support along the backbone was not strong and genera were often not monophyletic.
Relationships in the heart of the family remain to be established (e.g. Koch et al. 2012; Moazzeni et al. 2014). Relationships along the spine of Lineage I are quite well supported (Salariato et al. 2014), although groups like Erysimeae are not yet placed; Malcomia is wildly polyphyletic (Moazzeni et al. 2014) and has been dismembered (Al-Shehbaz et al. 2014). There are studies on Microlepideae, somewhat expanded (Heenan et al. 2012), on Physarieae (Fuentes-Soriano & Al-Shehbaz 2013: also morphological diversification), and Erysimeae (Moazzeni et al. 2014). Although Arabidopsis thaliana (Camelineae) is perhaps the most important model vascular plant in biology, the limits of the genus Arabidopsis itself are only now being established (see Clauss & Koch 2006 for a discussion of its immediate relatives). See also studies on Cardamine, Cardamineae, see Carlsen et al. (2009), and on Boechera and relatives, Boechereae, see Kiefer et al. (2009a, b) and Alexander et al. (2013)
Relationships between tribes and groups of tribes in Lineage II, itself often not well supported, are unsatisfactory, although the monophyly of the tribes themselves usually has good support. Warwick and Sauder (2005) found that to make a monophyletic Brassiceae little adjustment from its classical delimitation was needed, but "well-known" genera such as Brassica, Diplotaxis, Raphanus and Erucastrum were polyphyletic; as they noted, this should affect how breeders went about their business. Relationships in Brassiceae are still somewhat unclear (Hall et al. 2011), although there are eight well-supported clades (Arias & Pires 2012); ITS and cpDNA analyses give different topologies (Zipfer-Berger et al. 2015 and references). For the circumscription of Arabis (Arabideae), see Koch et al. (2010), and for a phylogeny of Draba , with three major clades, mostly perennial and a number Arctic-alpine, see Jordon-Thaden et al. (2010). Mummenhoff et al. (1997), Koch and Mummenhoff (2001) and Meyer (2003) discuss generic limits surrounding Thlaspi, a polyphyletic genus; the sometimes invasive Alliaria petiolata, with very different fruit morphology, is to be placed around here. Sisymbrium s. str. (Sisymbrieae) is restricted to the Old World, the New World taxa being unrelated and mixed in with Thelypodieae (Warwick et al. 2002, 2006a).
Studies on other Lineage II tribes include that on Schizopetaleae and Thelypodieae by Warwick et al. (2009). Thelypodieae were in the past thought to be close to Capparaceae because of their apparently plesiomorphic morphology, but they are now placed well within Brassicaceae near Brassiceae (Koch et al. 2012). Streptanthus and relatives (Thelypodieae) include several serpentine endemics as well as the selenium-tolerant Stanleya pinnata, but current genera do not reflect relationships there (Ivalú Cacho et al. 2014). For relationships in Isatideae, see Moazzeni et al. (2010), on Cochlearieae, Koch (2012), and on Chorisporeae-Dontostemoneae, see German et al. (2011). For work on Matthiola (Anchonieae), see Jaén-Molina et al. (2009).
See also Price et al. (1994), Galloway et al. (1998), Yang et al. (1999), and Warwick et al. (2007) for other phylogenetic studies. For work on some Asian taxa, see German et al. (2009: ITS), on Iranian Brassicaceae, see Khosravi et al. (2009), and on some Chinese Brassicaceae, see Liu et al. (2011).
Classification. Earlier classifications of the family have largely turned out to be something of a disaster. Both generic and tribal limits were often based on single characters like fruit "types" and embryo curvature and have proven to be very unsatisfactory (e.g. Mummenhoff et al. 1997; Al-Shehbaz et al. 2006; Moazzeni et al. 2010). Thus the combination of flattened fruits and accumbent cotyledons that characterized Lepidieae sensu Schultes has arisen perhaps 54 times in the family, and his Lepidieae are now placed in ca 13 tribes (I. Al-Shehbaz, pers. comm.), while the variation in such characters within quite small clades is impressive (e.g. Salariato et al. 2014).
The tribal reclassification began when Al-Shehbaz et al. (2006) recognised 25 monophyletic tribes based on well-supported clades; these tribes included somewhat over three quarters (260 of the 338) genera of the family then recognised (see also Beilstein et al. 2008; German & Al-Shehbaz 2008). The number of tribes has been creeping up since then, and is now 49, only 20 genera with 34 species remaining unassigned, 318 genera being placed in tribes (Al-Shehbaz 2012, see also Koch et al. 2012, BrassiBase). Things are getting a bit splitty because previously unplaced genera that end up as sister taxa to named tribes are put in new tribes, not accommodated in old tribes; the new tribal classification was begun when relationships were imperfectly known.
At the generic level the story is rather similar. There has been parallel or convergent evolution of just about all the morphological features used to distinguish genera (Koch 2003; Al-Shehbaz et al. 2006; Bailey et al. 2006a, b; Beilstein et al. 2008; Franzke et al. 2010), hence the major disagreements when comparing new and past generic limits. Some genera such Draba and Lepidium are indeed monophyletic or largely so on both morphological and molecular grounds, but most, including Brassica, are not (e.g. Mitchell-Olds et al. 2005 and references). For Isatideae, see Moazzeni et al. (2010). For the suggested placement of some of the more temperate annual species of Draba in separate genera, see Jordon-Thaden et al. (2010), for genera around Boechera, see Alexander et al. (2013). Again, things tend to be a bit splitty.
Warwick et al. (2006b) provide a species checklist, while BrassiBase (see Koch et al. 2012; Kiefer et al. 2014) is a developing resource for the family.