EMBRYOPSIDA Pirani & Prado
Gametophyte dominant, independent, multicellular, initially ±globular, not motile, branched; showing gravitropism; acquisition of phenylalanine lysase* [PAL], flavonoid synthesis*, microbial terpene synthase-like genes +, triterpenoids produced by CYP716 enzymes, CYP73 and phenylpropanoid metabolism [development of phenolic network], xyloglucans in primary cell wall, side chains charged; plant poikilohydrous [protoplasm dessication tolerant], ectohydrous [free water outside plant physiologically important]; thalloid, leafy, with single-celled apical meristem, tissues little differentiated, rhizoids +, unicellular; chloroplasts several per cell, pyrenoids 0; glycolate metabolism in leaf peroxisomes [glyoxysomes]; centrioles/centrosomes in vegetative cells 0, microtubules with γ-tubulin along their lengths [?here], interphase microtubules form hoop-like system; metaphase spindle anastral, predictive preprophase band + [with microtubules and F-actin; where new cell wall will form], phragmoplast + [cell wall deposition centrifugal, from around the anaphase spindle], plasmodesmata +; antheridia and archegonia +, jacketed*, surficial; mblepharoplast +, centrioles develop de novo, bicentriole pair coaxial, separate at midpoint, centrioles rotate, associated with basal bodies of cilia, multilayered structure + [4 layers: L1, L4, tubules; L2, L3, short vertical lamellae] (0), 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 +*, multicellular, growth 3-dimensional*, cuticle +*, plane of first cell division transverse [with respect to long axis of archegonium/embryo sac], sporangium and upper part of seta developing from epibasal cell [towards the archegonial neck, exoscopic], with at least transient apical cell [?level], initially surrounded by and dependent on gametophyte, placental transfer cells +, in both sporophyte and gametophyte, wall ingrowths develop early; suspensor/foot +, cells at foot tip somewhat haustorial; sporangium +, single, terminal, dehiscence longitudinal; meiosis sporic, monoplastidic, MTOC [= MicroTubule Organizing Centre] associated with plastid, sporocytes 4-lobed, cytokinesis simultaneous, preceding nuclear division, quadripolar microtubule system +; wall development both centripetal and centrifugal, 1000 spores/sporangium, sporopollenin in the spore wall* laid down in association with trilamellar layers [white-line centred lamellae; tripartite lamellae]; plastid transmission maternal; nuclear genome [1C] <1.4 pg, main telomere sequence motif TTTAGGG, KNOX1 and KNOX2 [duplication] and LEAFY genes present, ethylene involved in cell elongation; chloroplast genome with close association between trnLUAA and trnFGAA genes [precursors for starch synthesis], tufA, minD, minE genes moved to nucleus; mitochondrial trnS(gcu) and trnN(guu) genes +.
Many of the bolded characters in the characterization above are apomorphies of more or less inclusive clades 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.
Sporophyte well developed, branched, branching dichotomous, potentially indeterminate; hydroids +; stomata on stem; sporangia several, terminal; spore walls not multilamellate [?here].
II. TRACHEOPHYTA / VASCULAR PLANTS
Sporophyte long lived, cells polyplastidic, photosynthetic red light response, stomata open in response to blue light; plant homoiohydrous [water content of protoplasm relatively stable]; control of leaf hydration passive; plant endohydrous [physiologically important free water inside plant]; PIN[auxin efflux facilitators]-mediated polar auxin transport; (condensed or nonhydrolyzable tannins/proanthocyanidins +); xyloglucans with side chains uncharged [?level], in secondary walls of vascular and mechanical tissue; lignins +; roots +, often ≤1 mm across, root hairs and root cap +; stem apex multicellular [several apical initials, no tunica], with cytohistochemical zonation, plasmodesmata formation based on cell lineage; vascular development acropetal, tracheids +, in both protoxylem and metaxylem, G- and S-types; sieve cells + [nucleus degenerating]; endodermis +; stomata numerous, involved in gas exchange; leaves +, vascularized, spirally arranged, blades with mean venation density ca 1.8 mm/mm2 [to 5 mm/mm2], all epidermal cells with chloroplasts; sporangia in strobili, sporangia adaxial, columella 0; tapetum glandular; sporophyte-gametophyte junction lacking dead gametophytic cells, mucilage, ?position of transfer cells; MTOCs not associated with plastids, basal body 350-550 nm long, stellate array in transition region initially joining microtubule triplets; archegonia embedded/sunken [only neck protruding]; embryo suspensor +, shoot apex developing away from micropyle/archegonial neck [from hypobasal cell, endoscopic], root lateral with respect to the longitudinal axis of the embryo [plant homorhizic].[MONILOPHYTA + LIGNOPHYTA]
Sporophyte growth ± monopodial, branching spiral; roots endomycorrhizal [with Glomeromycota], lateral roots +, endogenous; G-type tracheids +, with scalariform-bordered pits; leaves with apical/marginal growth, venation development basipetal, growth determinate; sporangium dehiscence by a single longitudinal slit; cells polyplastidic, MTOCs diffuse, perinuclear, migratory; blepharoplasts +, paired, with electron-dense material, centrioles on periphery, male gametes multiciliate; nuclear genome [1C] 7.6-10 pg [mode]; chloroplast long single copy ca 30kb inversion [from psbM to ycf2]; mitochondrion with loss of 4 genes, absence of numerous group II introns; LITTLE ZIPPER proteins.
Sporophyte woody; stem branching lateral, meristems axillary; lateral root origin from the pericycle; cork cambium + [producing cork abaxially], vascular cambium bifacial [producing phloem abaxially and xylem adaxially].
SEED PLANTS† / SPERMATOPHYTA†
Growth of plant bipolar [plumule/stem and radicle/root independent, roots positively geotropic]; plants heterosporous; megasporangium surrounded by cupule [i.e. = unitegmic ovule, cupule = integument]; pollen lands on ovule; megaspore germination endosporic [female gametophyte initially retained on the plant].
EXTANT SEED PLANTS
Plant evergreen; nicotinic acid metabolised to trigonelline, (cyanogenesis via tyrosine pathway); microbial terpene synthase-like genes 0; primary cell walls rich in xyloglucans and/or glucomannans, 25-30% pectin [Type I walls]; lignin chains started by monolignol dimerization [resinols common], particularly with guaiacyl and p-hydroxyphenyl [G + H] units [sinapyl units uncommon, no Maüle reaction]; roots often ≥1 mm across, stele diarch to pentarch, xylem and phloem originating on alternating radii, cork cambium deep seated; stem apical meristem complex [with quiescent centre, etc.], plasmodesma density in SAM 1.6-6.2[mean]/μm2 [interface-specific plasmodesmatal network]; eustele +, protoxylem endarch, endodermis 0; 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; leaf nodes 1:1, a single trace leaving the vascular sympodium; leaf vascular bundles amphicribral; guard cells the only epidermal cells with chloroplasts, stomatal pore with active opening in response to leaf hydration, control by abscisic acid, metabolic regulation of water use efficiency, etc.; axillary buds +, exogenous; prophylls two, lateral; leaves with petiole and lamina, development basipetal, lamina simple; sporangia borne on sporophylls; spores not dormant; microsporophylls aggregated in indeterminate cones/strobili; grains monosulcate, aperture in ana- position [distal], primexine + [involved in exine pattern formation with deposition of sporopollenin from tapetum there], exine and intine homogeneous, exine alveolar/honeycomb; ovules with parietal tissue [= crassinucellate], megaspore tetrad linear, functional megaspore single, chalazal, sporopollenin 0; gametophyte ± wholly dependent on sporophyte, development initially endosporic [apical cell 0, rhizoids 0, etc.]; male gametophyte with tube developing from distal end of grain, male gametes two, developing after pollination, with cell walls; female gametophyte initially syncytial, walls then surrounding individual nuclei; embryo cellular ab initio, suspensor short-minute, embryonic axis straight [shoot and root at opposite ends], primary root/radicle produces taproot [= allorhizic], cotyledons 2; embryo ± dormant; chloroplast ycf2 gene in inverted repeat, trans splicing of five mitochondrial group II introns, rpl6 gene absent; ??whole nuclear genome duplication [ζ - zeta - duplication], 2C genome size (0.71-)1.99(-5.49) pg, two copies of LEAFY gene, PHY gene duplications [three - [BP [A/N + C/O]] - copies], 5.8S and 5S rDNA in separate clusters.
IID. ANGIOSPERMAE / MAGNOLIOPHYTA
Lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, apigenin and/or luteolin scattered, [cyanogenesis in ANA grade?], lignin also with syringyl units common [G + S lignin, positive Maüle reaction - syringyl:guaiacyl ratio more than 2-2.5:1], hemicelluloses as xyloglucans; root cap meristem closed (open); pith relatively inconspicuous, lateral roots initiated immediately to the side of [when diarch] or opposite xylem poles; epidermis probably originating from inner layer of root cap, trichoblasts [differentiated root hair-forming cells] 0, hypodermis suberised and with Casparian strip [= exodermis]; shoot apex with tunica-corpus construction, tunica 2-layered; starch grains simple; primary cell wall mostly with pectic polysaccharides, poor in mannans; tracheid:tracheid [end wall] plates with scalariform pitting, multiseriate rays +, wood parenchyma +; sieve tubes enucleate, sieve plates with pores (0.1-)0.5-10< µm across, cytoplasm with P-proteins, not occluding pores of plate, companion cell and sieve tube from same mother cell; ?phloem loading/sugar transport; nodes 1:?; dark reversal Pfr → Pr; protoplasm dessication tolerant [plant poikilohydric]; stomata randomly oriented, brachyparacytic [ends of subsidiary cells ± level with ends of guard cells], outer stomatal ledges producing vestibule, reduction in stomatal conductance with increasing CO2 concentration; lamina formed from the primordial leaf apex, margins toothed, development of venation acropetal, overall growth ± diffuse, secondary veins pinnate, fine venation hierarchical-reticulate, (1.7-)4.1(-5.7) mm/mm2, vein endings free; flowers perfect, pedicellate, ± haplomorphic, protogynous; parts free, numbers variable, development centripetal; P = T, petal-like, 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], each theca dehiscing longitudinally by a common slit, ± embedded in the filament, walls with at least outer secondary parietal cells dividing, endothecium +, cells elongated at right angles to long axis of anther; tapetal 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, intine in apertural areas thick, orbicules +, pollenkitt +; nectary 0; carpels present, superior, free, several, spiral, ascidiate [postgenital occlusion by secretion], stylulus at most short [shorter than ovary], hollow, cavity not lined by distinct epidermal layer, stigma ± decurrent, carinal, dry; suprastylar extragynoecial compitum +; 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, nucellar cap?; megasporocyte single, hypodermal, functional megaspore lacking cuticle; female gametophyte lacking chlorophyll, four-celled [one module, egg and polar nuclei sisters]; ovule not increasing in size between pollination and fertilization; pollen grains bicellular at dispersal, germinating in less than 3 hours, siphonogamy, pollen tube unbranched, growing towards the ovule, 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 gametophytes tricellular, gametes 2, lacking cell walls, ciliae 0, double fertilization +, ovules aborting unless fertilized; fruit indehiscent, P deciduous; mature seed much larger than fertilized ovule, small [<5 mm long], dry [no sarcotesta], exotestal; endosperm +, ?diploid [one polar nucleus + male gamete], cellular, development heteropolar [first division oblique, micropylar end initially with a single large cell, divisions uniseriate, chalazal cell smaller, divisions in several planes], copious, oily and/or proteinaceous, embryo short [<¼ length of seed]; plastid and mitochondrial transmission maternal; Arabidopsis-type telomeres [(TTTAGGG)n]; nuclear genome [2C] (0.57-)1.45(-3.71) [1 pg = 109 base pairs], ??whole nuclear genome duplication [ε/epsilon event]; 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, palaeo AP3 and PI genes [paralogous B-class genes] +, with "DEAER" motif, SEP3/LOFSEP and three copies of the PHY gene, [PHYB [PHYA + PHYC]]; chloroplast chlB, -L, -N, trnP-GGG genes 0.
[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]]]]: phloem loading passive, via symplast, plasmodesmata numerous; vessel elements with scalariform perforation plates in primary xylem; essential oils in specialized cells [lamina and P ± pellucid-punctate]; tension wood + [reaction wood: with gelatinous fibres, G-fibres, on adaxial side of branch/stem junction]; anther wall with outer secondary parietal cell layer dividing; tectum reticulate; 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 [?here]; pollen tube growth intra-gynoecial; extragynoecial compitum 0; carpels plicate [?here]; embryo sac monosporic [spore chalazal], 8-celled, bipolar [Polygonum type], antipodal cells persisting; endosperm triploid.
[MONOCOTS [CERATOPHYLLALES + EUDICOTS]]: (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 [or next node up]; fruit dry [very labile].
EUDICOTS: (Myricetin +), 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 ?, 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]: mitochondrial rps11 gene lost.
CORE EUDICOTS / GUNNERIDAE: (ellagic and gallic acids +); leaf margins serrate; compitum + [one position]; micropyle?; γ whole nuclear genome duplication [palaeohexaploidy, gamma triplication], x = 3 x 7 = 21, 2C genome size (0.79-)1.05(-1.41) pg, 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 = K + C, K enclosing the flower in bud, with three or more traces, C with single trace; A = 2x K/C, in two whorls, internal/adaxial to C, alternating, (numerous, but then usually fasciculate and/or centrifugal); pollen tricolporate; G [(3, 4) 5], whorled, placentation axile, style +, stigma not decurrent, compitum + [another position]; endosperm nuclear; fruit dry, dehiscent, loculicidal [when a capsule]; floral nectaries with CRABSCLAW expression.
[DILLENIALES [SAXIFRAGALES + ROSIDS]]: stipules + [usually apparently inserted on the stem].
[SAXIFRAGALES + ROSIDS] / ROSANAE Takhtajan / SUPERROSIDAE: ??
ROSIDS / ROSIDAE: anthers ± dorsifixed, transition to filament narrow, connective thin.
[ROSID I + ROSID II]: (mucilage cells with thickened inner periclinal walls and distinct cytoplasm); if nectary +, usu. receptacular; embryo long; 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 at most scanty.
[HUERTEALES [MALVALES + BRASSICALES]]: ?
[MALVALES + BRASSICALES]: ?
BRASSICALES Bromhead - Main Tree.
Glucosinolates +, from phenyalanine and/or tyrosine [aromatic] and valine/isoleucine/leucine [aliphatic; 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, 405 genera, 5,035 species.
Note: In all node characterizations, boldface denotes a possible apomorphy, (....) denotes a feature the exact status of which in the clade is uncertain, [....] includes explanatory material; other text lists features found pretty much throughout the clade. Note that the particular node to which many characters, particularly the more cryptic ones, should be assigned is unclear. This is partly because homoplasy is very common, in addition, basic information for all too many characters 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 are the not-so-trivial issues of how character states are delimited and ancestral states are reconstructed (see above).
Age. Wikström et al. (2001) dated crown Brassicales to 79-71 Ma. Other estimates are (76-)73(-70) and (63-)69(-57) Ma (two penalized likelihood dates: H. Wang et al. 2009), while Magallón and Castillo (2009) estimated ages of ca 65.9 Ma, Bell et al. (2010) ages of (94-)83, 82(-69) Ma, while (133-)92(-50) Ma is the estimate in Edger et al. (2015: note topology) and (112.6-)102.8(-94.4) Ma in Cardinal-McTeague et al. (2016).
The earliest fossil placed by some in this clade is from the Turonian, ca 89.5 Ma - Dressiantha (Gandolfo et al. 1998c), but c.f. Couvreur et al. (2010) and also below.
Evolution: Divergence & Distribution. Brassicales contain ca 2.2% eudicot diversity (Magallón et al. 1999) and show quite high diversification rates (Magallón & Sanderson 2001; Magallón & Castillo 2009), perhaps also linked to the absence of mycorrhizae (see below) and the herbaceous habit (see Maherali et al. 2016), both very common in the order.
Cardinal-McTeague et al. (2016) date nodes throughout Brassicales, and the dates below are taken from their Fig. S1 and Table S5 which are based on all four calibrations that they use. These calibrations are discussed in Table S3. Interestingly, if they exclude the fossil Dressiantha, as would seem to be reasonable (see below), they obtain somewhat older ages for the deeper nodes in particular - and ages in Fig. S1 are already older than most others proposed for the order and branches within it. Cardinal-McTeague et al. (2016) go on to discuss the biogeography of the family.
Edger et al. (2015) discuss glucosinolate evolution in the context of genome duplications in the order, linking this evolution to both brassicalean and pierine diversification; their dates for the two major genome diversifications in Brassicales are followed here, but note the difference in the topology of their tree and the one immediately below. Two clades of Pierinae, Pierina and Anthocharidini (Edger et al. 2015; Wahlberg et al. 2014 for phylogeny and classification), may have moved on to Brassicales from an original host in Fabaceae (Braby & Trueman 2006) some (90-)85(-60) Ma and within ten Ma or so of the origin of Brassicales, shifts that seem to have been accompanied by bursts in diversification; Coliadinae, sister group of Pierinae, are less diverse (Wheat et al. 2007; Fordyce 2010). However, Edger et al. (2015) suggest a rather later date of some (75-)68(-60) Ma, with pierines initially primarily moving on to Brassicales that had evolved tryptophan-derived indole glucosides, i.e. the clade [Limnanthaceae + the rest] here, or perhaps the next node up. For more on glucosinolates, see below.
Rodman et al. (1996) proposed some apomorphies for the order (and for some nodes within it), but where some are to be placed on the tree is unclear, although Tobe (2015b) makes suggestions for a number of characters. Characters like ovules in two ranks, parietal placentation, and clawed petals are notably common in this clade. Ronse de Craene and Haston (2006) examined morphological evolution in Brassicales 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 plants; 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. The ecophysiological interactions involved in the glucosinolate pathway and their evolution make a complex story, and some of the physiological interactions are summarised by Nakano et al. (2016: esp. Fig. 6).
Glucosinolates are mustard oil glycosides, and mustard oils are esters of isothiocyanic acid with a R—N=C=S group; they have a pungent smell and sharp taste. Specialised, protein-rich myrosin cells with rough endoplasmic reticulum contain enzymes like thioglucoside glucohydrolase (a ß-thioglucohydrolase, or myrosinase) that breaks down glucosinolates into glucose and aglucones when plant tissue is damaged, as by a herbivore, and enzyme and substrate are brought into contact; here the two parts of the defence system are physically quite separate before the damage (Nakano et al. 2016). The aglucones then automatically rearrange and form toxic isothiocyanates, or are converted into thiocyanates (mustard oils), nitriles (not necessarily toxic), and other compounds (e.g. Andréasson et al. 2001). This is the "Senfölbombe" or "mustard oil bomb", most details of which have been worked out in Brassicaceae (see Rask et al. 2000, Wittstock et al. 2003; Grubb & Abel 2006; Halkier & Gershenzon 2006; Agerbirk et al. 2008, 2010; Burow et al. 2009; Textor & Gershenzon 2009 and other papers in Phytochem. Review 8(1). 2009; Pentzold et al. 2014). The ß-glucosidase is similar to those that break down cyanogenic glycosides, and glucosinolate synthesis has evolved from the pathway by which cyanogenic compounds are synthesized (Halkier & Gershenzon 2006; Bak et al. 2006; Morant et al. 2008). Although protective (but see below), their metabolic cost is high (Bekaert et al. 2012).
Well over 200 glucosinolates are known (Fahey et al. 2001; Agerbirk & Olsen 2012; Leite & Castilho 2017), and they are likely to be many more; a species like Arabidopsis thaliana can synthesize over 40 different kinds (Olsen et al. 2016). 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, although some families there are poorly known (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, indeed, "atypical" (EE) myrosinases are to be found in cells with ER (endoplasmic reticulum) bodies that contain myrosinases, and here the separation of the two components of the Senfölbombe is at the intracellular level - but in fact there is no evidence that the myrosinases in the two systems have a common origin (the myrosinases in myrosin cells are "typical" QE myrosinases), or even that one evolved from the other (Nakano et al. 2016); for further details, see below. Even in Brassicaceae, which do have myrosin cells, their distribution varies with the age and species of the plant concerned (Maile 1980; Andréasson et al. 2001). 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 (Jørgensen 1995), but they 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) and Textor and Gershenzon (2009) for literature. Glucosinolates may protect against herbivory, but at the same time caterpillars of the 780-840 species of Pieridae-Pierinae (food plants of ca 360 species in 33+ genera have been 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, although 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 (Malpighiales-Putranjivaceae) and Capparaceae (Yata et al. 2010), and of course both groups contain glucosinolates. There is also a clade of Pierinae on Santalalean hosts (see Aporiina: Braby & Trueman 2006), but few details of the interactions between the two seem to be known and glucosinolates have not been recorded from Santalales.
The herbivores that have evolved to be able to handle the glucosinolate defence do so in a variety of ways, including avoiding breaking down the cells (so the different parts of the breakdown pathway do not come together), rapidly absorbing the glucosinolates (which has much the same effect), and so on (e.g. Bones & Rossiter 2006; Agerbirk et al. 2010; Winde & Wittstock 2011; Pentzold et al. 2014). The ability of pierine caterpillars to live on Brassicales is associated with the evolution of a novel glucosinolate detoxifying mechanism in which nitriles rather than toxic isothiocyanates are produced on the hydrolysis of the glucosinolates (the nitrile-specifier protein - NSP - gene: e.g. Fischer et al. 2008; Edger et al. 2015), and more basal pierine clades that lack this mechanism are less diverse (Wheat et al. 2007). These nitriles are then excreted unchanged (aliphatic nitriles) or further metabolized (aromatic nitriles), and for pierids, the evolution of NSP may have been a key innovation (Winde & Wittsock 2011) allowing them to radiate in glucosinolate-containing Brassicales. It is interesting that a single carbon atom can be removed from aromatic nitriles in the form of hydrogen cyanide, the mustard oil bomb transforming into a cyanide bomb, but the larvae of Pieris rapae, at least, detoxify the HCN in their guts (Stauber et al. 2012). Benzyl glucosinolates that are detoxified in this way are found in Tropaeolaceae, Caricaceae, etc. (see below; Stauber et al. 2012). In the [Capparaceae [Cleomaceae + Brassicaceae]] clade glucosinolates are primarily synthesized from methionine and caterpillars of about four times as many pierines are to be found here as are found on Brassicales with tryptophan-derived glucosinolates (Edger et al. 2015: check).
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), even if the isothiocyanates may deter predators of the herbivores, aphids in this case - note that aphid stylets may miss the myrosin cells (Kos et al. 2012a). 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. 2012b).
Some chrysomelid beetles also favour 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) - although sometimes the plant seems to ignore aphids, perhaps because the latter attack single cells (Textor & Gershenzon 2009). 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). Lysack (2018) discusses genome duplication, the evolution of chromosome numbers (base number - x = 9 or 14?), etc., in the family.
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. Carlquist (2016) carried out a comprehensive anatomical survey of the order; as he noted, features like stroying of the vascular tissue might be hard to see in a group with many herbs, or plants in which woodiness is not well developed. Most families have "stipules" of some sort or another, although they are often small; 1:1 nodes are common in the order, and stipule anatomy and morphology would repay further study - modified colleters? Strongly developed and fused ventral carpellary bundles may be another synapomorphy for the order (Ronse de Craene & Haston 2006).
For general information, see Mehta and Moseley (1981) and Kubitzki (2002a, b: as Capparales), for chemistry, see Leite and Castilho (2017) and Fay and Christenhusz (2010), for anatomy, see Carlquist (1985a); also Tobe and Raven (2012: aspects of seed evolution).
Phylogeny. For early phylogenetic work on Brassicales, see also Rodman (1991a, b) and Rodman et al. (1993, 1994). Relationships within Brassicales show a fair bit of structure, as Rodman et al. (1997, 1998), Carol et al. (1999), Chandler and Bayer (2000), Kubitzki (2002a), Olson (2002a), Hall et al. (2004) and Cardinal-McTeague et al. (2016) have found. However, a recent transcriptome analysis yielded a clade [[Moringaceae + Caricaceae] [Tropaeolaceae + Akaniaceae]] sister to a clade made up of the rest of the order (Edger et al. 2015: unsurprisingly, sampling only moderate). 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; Edger et al. 2018) although the position of the two was reversed in M. Sun et al. (2016). [Koeberliniaceae [Bataceae + Salvadoraceae]] is an odd little group but it commonly forms a clade, however, Sun et al. (2016) suggest that Salvadoraceae are paraphyletic, Azima tetracantha in particular being sister to Batis while Edger et al. (2018; Edger et al. 2015 is compatible with this topology, see also Lysack 2018) found the well supported relationships [... [[Bataceae + Salvadoraceae] [Koeberliniaceae ...]]].
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 was then poorly understood (but see below); they thought that it might be sister to [Bataceae + Salvadoraceae], but noted that there was little support for this position. There are further details of relationships in this area below.
Analysis of morphological data alone yielded only one clade ([Polanisia + Cleome]!) in Brassicales that had even weak support, and Bretschneidera and Akania were associated with Sapindaceae (Ronse de Craene & Haston 2006). Morphology was also combined with molecular data (four genes, some taxa lacked up to three of them); there are differences in detail of the topology of their tree and that used here (Ronse de Craene & Haston 2006).
Classification. For the history of the classification of the group, see Fay and Christenhusz (2010). The limits of families in the core Brassicales have been rather labile in the past, but it is to be hoped that they can now settle down (see A.P.G. IV 2016).
Previous Relationships. Some Brassicales, particularly 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), orders 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, Brassicaceae, Capparaceae, Caricaceae, Cleomaceae, Emblingiaceae, Gyrostemonaceae, Koeberliniaceae, Limnanthaceae, Moringaceae, Pentadiplandraceae, Resedaceae, Salvadoraceae, Setchellanthaceae, Tovariaceae, Tropaeolaceae -
Synonymy: Brassicineae Shipunov, Resedineae Engler - 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 [ca 1.5< cm across], obliquely monosymmetric [median C adaxial]; K + C forming a 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), (56-)35, 34(-18) Ma (Bell et al. 2010), (54-)36(-19) Ma (Edger et al. 2015: note topology), or (86.6-)75(-66.1) Ma (Cardinal-McTeague et al. 2016).
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), this "hypanthium" 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
Tannins?; cork subepidermal; (vessel elements with simple perforation plates); no bordered pits in imperforate tracheary elements; ?nodes; petiole bundle?; cuticle waxes 0, strong cuticular cracks; stomata ?; leaves odd-pinnate, vernation supervolute-curved; pollen tricolpate; G [3-5]; stigma small, 3-lobed; micropyle bistomal; capsule loculicidal; testa multiplicative, vascularized, exotestal cells palisade, thick-walled, mesotesta ± thick, cells thick-walled, endotesta thickened; embryo color?
2 [list]/2. Southeast Asia, E. Australia.
Age. Bell et al. (2010) suggested that the two genera diverged (12-)6(-2) Ma, the age in Wikström et al. (2001) is 31-23 Ma, and that in Cardinal-McTeague et al. (2016) is (66.3-)64.1(-62.4) Ma - note that Cardinal-McTeague et al. (2016) included fossils of both Akania (see below) and Dressiantha (also see below) among their calibration points.
Fossils attributed to Akania are known from Patagonia in deposits as old as the Palaeocene 61.7 Ma (Iglesias et al. 2007; Gandolfo et al. 2011 and references; Wilf et al. 2011).
1. Akania J. D. Hooker
Evergreen tree; stomata in clusters; leaflet margins spinulose-toothed; inflorescence branched, ?morphology; flowers polysymmetricca 10 mm across; C barely clawed; nectary 0; A 10; stigma small, 3-lobed; ovules superposed, parietal tissue 5-7 cells across; endosperm copious; n = ?
1/1: Akania bidwillii. E. Australia (map: see above, Australia's Virtual Herbarium i.2014; Conran et al. 2019 - fossils).
2. Bretschneidera Hemsley
Deciduous tree; leaflet margins entire, vernation supervolute-curved, petiolules swollen or articulated; K ± connate; nectary +; A 8; G ([4-5]), stigma small; ovules campylotropous, parietal tissue 7-8 cells across; embryo sac bisporic (the spores chalazal) and 8-celled [Allium type]; n = 9.
1/1: Bretschneidera sinensis. S.W. China, adjacent Vietnam and Thailand, Taiwan (map: see above). Photo: Collection.
Evolution: Divergence & Distribution. Fossils of Akania are known from deposits in Argentinian Patagonia as young as 18-16 Ma (Brea et al. 2017 and references) and from Miocene deposits ca 29 Ma in New Zealand (Conran et al. 2019), so its distribution in the fairly recent past was very different from that now.
Chemistry, Morphology, etc. In Bretschneidera, glucosinolates are also produced from valine/isoleucine and/or leucine.
Stapf (1912) described the pollen of Akania as being 4-porate, c.f. Conran et al. (2019). Bretschneidera has clearly strongly obliquely monosymmetric flowers, 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 the embryology of Bretschneiders, see Tobe and Peng (1990), for ovules, see Mauritzon (1936), for fruit and seed, see Doweld (1996a, b).
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. III 2009).
Previous Relationships. A relationship with Sapindales was often suggested in the past (e.g. Carlquist 1997a), and a phylogenetic analysis of morphological data also suggested this position (Ronse de Craene & Haston 2006). Bretschneidera does look rather sapindaceous, and with its eight stamens and often three carpels...
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; nodes 3:3; 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; C 2 + 3 (2 + 2), (margin ± deeply lobed/laciniate); K + C (fused adaxially only), spurred, (spur ca 1 mm or less), nectary in spur; pollen grains tricellular; median carpel adaxial, style impressed, stigma trifid, dry; ovules with endostomal micropyle, parietal tissue 0; fruit a schizocarp, mericarps drupaceous or nut-like/(samara), K deciduous; seed pachychalazal, coat undistinguished, part of mesotesta suberized; cotyledon cell walls with xyloglucans [thick, pitted - amyloid), suspensor haustorium +, penetrates micropyle and adjacent maternal tissue; n = 12-15; germination hypogeal, epicotyl +.
1 [list]/105. New World, esp. Andean (map: see Sparre & Andersson 1991). [Photos - Tropaeolum Flower, ditto.]
Evolution: Genes & Genomes. There may be a whole genome duplication preceding diversification in Tropaeolaceae (Lysak 2018 and references).
Chemistry, Morphology, etc. Carlquist and Donald (1996) report vague storying of the secondary phloem of the root. Kumar (1977) described the nodes as being trilacunar. 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 is in the K/C spur, and is outside the staminal ring (Ronse Decraene et al. 2002a). 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 embryo 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), and for those in section. Chilensia, see Hershkovitz et al. (2006: some hybridization). 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 + Resedaceae]], Tovariaceae, [Cleomaceae [Capparaceae + Brassicaceae]]]]]]]]: several [>6] ovules/carpel.
Age. The age of this clade is estimated as ca 73.3 Ma (Hohmann et al. 2015), 72-68 Ma (Wikström et al. 2001), (90.5-)72(-47.9) Ma (Couvreur et al. 2010), (90-)79, 65(-55) Ma (Bell et al. 2010), (68-)54(-38) Ma (N. Zhang et al. 2012), as little as ca 39.0 or 36.3 Ma (Xue et al. 2012) or as much as ca 92.2 Ma (Edger et al. 2018) or even (105.9-)97.6(-91.4) Ma (Cardinal-McTeague et al. 2016: Dressiantha used as calibration, but see below).
[Moringaceae + Caricaceae]: woody, stems stout [pachycaul or cauduciform]; endoplasmic reticulum-dependent vacuoles +; xylem ± 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; embryo white.
Age. The two families diverged some 61-58 (Wikström et al. 2001), (86-)67, 64(-45) (Bell et al. 2010), (93-)64(-34) (Edger et al. 2015: note topology) or (94.1-)73.2(-46.4) Ma (Cardinal-McTeague et al. 2016).
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, but there are certainly 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; (vestured pits +), 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 5, opposite C, declinate, monothecal/(bithecal), 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 +; (archesporium -3-celled); 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, (weakly multiplicative), one layer persists; endosperm 0, suspensor ?"massive"/0; 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; see Puri (1941, 1942) for embryology and floral anatomy and Muhl et al. (2016) for embryo and seed development.
Phylogeny. For relationships, see Olson (2000b); three pachycaul bottle trees, Morinda drouhardii, M. hildebrantii and M. stenopetala, the first two from Madagascar, are successively sister to the rest of the genus.
Synonymy: Hyperantheraceae Link
CARICACEAE Dumortier, nom. cons. - Back to Brassicales
Small to medium trees, (viny, but with stout tuber), usu. prickly; ?cyanogenic glycosides, cysteine proteases +, 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]; x = 9 (n = 7, 8).
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) Ma (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 Ma (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?) have a similar floral syndrome.
Myrmecochory is reported from Carica (Lengyel et al. 2010) despite (perhaps) its fleshy fruits.
Plant-Animal Interactions. Proteases in the latex of Carica, at least, are involved in defence against herbivorous insects (Konno et al. 2004) - they are not just meat tenderizers.
Genes & Genomes. The basic chromoromosome number for the family may be 9 (Murat et al. 2015b). For the evolution of the X chromosome in Carica papaya, which is dated to only ca (9.5-)7(-1.9) Ma, 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 (Spencer & Seigler 1984; c.f. Jørgenson 1995).
For the morphology and mineral composition of the stinging hairs of Horovitzia, see Mustafa et al. (2018b).
Some general information is taken from Badillo (1971), Miller (1982) and Kubitzki (2002d), and see the e-monograph by Carvalho (2013; also Carvalho et al. 2015); for latex coagulation, see references in Bauer et al. (2014),for wood anatomy, see Carlquist (1998c), for floral development, see Ronse Decraene and Smets (1998b), for pollen, see Zini et al. (2018) and for embryology, see Singh (1970).
Phylogeny. For phylogenetic relationships, see Kyndt et al. (2005), Carvalho and Renner (2012), Carvalho (2013) and M. Sun et al. (2016). The African Cylicomorpha is sister to the rest of the family, which are all American - [Cylicomorpha [[Jacaratia + Vasconcellea] [Carica papaya [Horovitzia + Jarilla]]]], 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 + Resedaceae]], Tovariaceae, [Cleomaceae [Capparaceae + Brassicaceae]]]]]]]: nodes 1:1; C clawed; (A splitting) [= chorisis], extended 3' terminus of rbcL gene.
Age. The age of this clade is around 60-54 Ma (Wikström et al. 2001), (85-)73, 71(-61) Ma (Bell et al. 2010: c.f. relationships) or (97.9-)88.8(-80.8) Ma (Cardinal-McTeague et al. 2016).
Genes & Genomes. For the extended 3' terminus of rbcL gene and changes in stop codons, etc., see Karol et al. (1999).
Chemistry, Morphology, etc. Chorisis, i.e. splitting, of the stamen primordia, of which dédoublement is a special case, is scattered in this clade (see Tobe 2015b); Tobe (2015b) noted that in such cases centrifugal development of the stamens is common.
SETCHELLANTHACEAE Iltis - Back to Brassicales
Shrub; myrosin cells 0; young stem with vascular cylinder; vestured pits +; 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 opposite K, 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 [list]/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 + Resedaceae]], Tovariaceae, [Cleomaceae [Capparaceae + Brassicaceae]]]]]]: indole glucosinolates +; endomycorrhizae 0; root hair cells in vertical files alternating with files of cells lacking hairs; At-β genome duplication [?next node down?].
Age. The age for this node is estimated to be 54-52 Ma (Wikström et al. 2001: c.f. topology), (112-)77.5(-42)/(123-)85(-46) Ma (Edger et al. 2015, 2018: note topology), (96-)87.1(-78.7) Ma (Cardinal-McTeague et al. 2016) or around 124 Ma (Kagale et al. 2014); see also below for suggested ages of the genome duplication placed at this node.
Evolution: Divergence & Distribution. For an increase in net diversification possibly associated with the At-β genome duplication, see below. Van den Bergh et al. (2016) suggest that this genome duplication is associated with the evolution of indole glucosinolates derived from tryptophan (for the duplication and indole glucosinolates, see also Edger et al. 2015, 2018).
Tropaeolaceae are the nearest family that is known to lack "striped" root hair development (Dolan & Costa 2001).
Bacterial/Fungal Associations. Loss of the ability to form endomycorrhizae (arbuscular mycorrhizae - AM) has been placed at this node by Delaux et al. (2014), and Brassicaceae in particular are noted for being non-mycorrhizal, its members often growing in habitats where soil phosphorus is abundant (Lambers 2015c). AM are at best uncommon in Brassicales as a whole, and this is linked with the loss of the RAM2 - Reduced Arbuscular Mycorrhization - locus; RAM2 is involved in the production of cutin monomers recognized by both glomeromycotes during the establishment of endomycorrhizal associations and oomycetes during the initiation of parasitism (E. Wang et al. 2012; Geurts & Vleeshouwers 2012). Roots of non-mycorrhizal Brassicales are significantly thinner than those of AM rosids (Valverde-Barrantes et al. 2017). The establishment of AM associations has a considerable effect on plant defences, upregulating some and downregulating others (e.g. Jung et al. 2012). There seems to be a trade-off here: The loss of the ability to form AM associations is linked to resistance to oomycete infestations (see also Kamel et al. 2016). However, the oomycete Albugo s. str., a white blister rust, is a common parasite in this clade, A. candida growing on members of Brasicaceae, Capparaceae and Cleomaceae, for example (Choi et al. 2009; Thines & Voglmayr 2009; Ploch et al. 2010a). The effect of Albugo on the plant is complicated, and in some cases it facilitates infection by Phytophthora infestans, another oomycete (Prince et al. 2017). For other possible connections between AM and oomycete infections, see Estrada-Navarrete et al. (2016).
Chemistry, Morphology, etc. Indolic glucosinolates may be present in the plant after experimental herbivory treatments in Carica and Tropaeolum (Textor & Gershenzon 2009). 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).
Phylogeny. Edger et al. (2015) found the relationships [Limnanthaceae [Bataceae [Koeberliniacaeae + core Brassicales]]]], but Setchellanthaceae, Salvadoraceae and Emblingiaceae were not included, and only one species in each included family was examined - but see Edger et al. (2018).
Genes & Genomes. The At-β/ARTHβ genome duplication has been dated to 124.6±2.6 Ma (Kagale et al. 2014), while other estimates are ca 50 Ma (Woodhouse et al. 2011), 69-53 Ma (Murat et al. 2015b) or ca 77 Ma (Landis et al. 2018), also clade age estimates above, see also Hohmann et al. (2015) for discussion). Either some ages of this duplication are wildly wrong, and/or it is placed at the wrong node - the next node down is perhaps a possibility (see also Lysak 2018; Bayat et al. 2018).
Thanks. To Jean-Michel Ané, for help with the literature on oomycete infection and plant/fungal signalling.
LIMNANTHACEAE R. Brown, nom. cons. - Back to Brassicales
Annual herbs; erucic acid, ellagic acid, myricetin, non-hydrolysable tannins +, fructan sugars accumulated as isokestose oligosaccharides [inulins], stomatal myrosin cells 0; complete vascular cylinder not forming; cork?; leaf pinnate, or lamina pinnately lobed, vernation conduplicate, margins with teeth, stipules 0; (flowers single, axillary); flowers 3-5-merous, bracteoles 0; K valvate, with one trace [Limnanthes], C contorted (open); nectaries on abaxial bases of antesepalous A; A 2x K, of two lengths, largest opposite sepals; tapetal cells binucleate; pollen grains elongated bun-shaped, heteropolar, zonosulcate; 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 14-20 cells across, parietal tissue 1 cell across; 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, cell walls with xyloglucans [thick, pitted - amyloid]; n = 5; germination hypogeal or epigeal, radicle soon dies [Limnanthes - ?both].
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 Ma (Wikström et al. 2001), (22-)13, 12(-5) Ma (Bell et al. 2010), or (22.1-)12.1(-4) Ma (Cardinal-McTeague et al. 2016).
Chemistry, Morphology, etc. Hofmann and Ludewig (1985) showed the stem-born roots of Limnanthes departing from the sides of the leaf gaps.
There are very different interpretations of the pollen morphology of Limnanthes, Buchner et al. (1990) are followed here. What is going on in Floerkea is unclear (Maheshwari & Johri 1956), although the pollen does appear to be heteropolar. According to van Tieghem (1898), the ovules are epitropous, but they are shown ab beingapotropous by Maheshwari and Johri (1956). Maheshwari and Johri (1956) and Johri (1970) described an endosperm pouch or haustorium on the funicular side of the micropylar region in Floerkea.
Some general information is taken from Bayer and Appel (2002); for wood anatomy, see Carlquist and Donald (1996), for floral differences in nectaries, see Link (1992a), and for embryology, see Fagerlind (1939b) and Mathur (1956).
Although Limnanthaceae are small, it is unclear if some of the bolded characters above really are apomorphies for the whole family...
Previous Relationships. Eckert (1966) compared floral morphology of Limnanthaceae with that of other families believed to be related, as did Hofmann and Ludewig (1985: they included other features; possible relatives covered the waterfront. Limnanthaceae were often included in Geraniales (e.g. Cronquist 1981), but were placed in Solananae by Takhtajan (1997).
[[Koeberliniaceae [Bataceae + Salvadoraceae]] [Emblingiaceae [[Pentadiplandraceae [Gyrostemonaceae + Resedaceae]], Tovariaceae, [Cleomaceae [Capparaceae + Brassicaceae]]]]]: 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 Ma (Wikström et al. 2001), (112-)77.5(-42) Ma (Edger et al. 2015, 2018: c.f. topology), or (88.6-)80.2(-72.5) Ma (Cardinal-McTeague et al. 2016).
The fossil Dressiantha, from some 90 Ma 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 suggests a position around here. Its use in calibration would seem ill-advised and it is best excluded from Brassicales. Interestingly, its exclusion as a calibration point in Cardinal-McTeague et al. (2016: Table S5) resulted in ages of deeper nodes in particular in Brassicales clade becoming somewhat older.
Chemistry, Morphology, etc. Amino acids like isoleucine with branched chains may have more carbons added 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 merosity 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]]: wood ± storied; idioblastic myrosin cells 0; vestured pits +; flowers 4-merous; pollen 3-colporoidate; G ; fruit indehiscent; exotestal cells well developed; x = 11.
Age. This node is estimated to be about 43-37 Ma (Wikström et al. 2001), (71-)60, 59(-48) Ma (Bell et al. 2010), or (83.4-)71(-56.3) Ma (Cardinal-McTeague et al. 2016).
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 orientation oblique, gynophore +, short, 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 chlorophyllous, endosperm type?, moderate, cotyledons incumbent.
1 [list]/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]: 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; A 5; 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, so although they both have 5 stamens, whether they are in the same position is unclear (c.f. Tobe 2015b).
BATACEAE Perleb, nom. cons. - Back to Brassicales
Fleshy shrublets; (hydroxy)proline betaines +, tannins?; cork pericyclic; perforation plate borders vestigial; leaves fleshy, blade terete, 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 ovary"], style 0, 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. Cronquist (1981) described the placentation as being parietal-basal, Tomlinson (2016) as being apical.
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; 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 K, free, basally connate, or adnate to C; pollen triporate, surface reticulate; G (gynophore +), 1-2-4-locular [see below], orientation oblique, (style short), stigma punctate to 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
Core Brassicales / [Emblingiaceae [[Pentadiplandraceae [Gyrostemonaceae + Resedaceae]], Tovariaceae, [Cleomaceae [Capparaceae + Brassicaceae]]]] : glucosinolates also from tryptophane [?here]; cisternae of endoplasmic reticulum dilated and vacuole-like; cuticle wax crystalloids 0; inflorescence terminal, bracteoles 0; floral development open; nectary outside A; endotesta crystalliferous; 3' rbcL extension.
Age. Core Brassicales have been dated to ca 66.1 Ma (Edger et al. 2018), (75.6-)68.5(-62) Ma (Hall et al. 2015) and (80.6-)72.9(-65.5) Ma (Cardinal-McTeague et al. 2016).
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 has been suggested that the At-ß genome duplication is to be placed at this node; it is absent from Carica (Barker et al. 2009: sampling); see below for recent ideas as to where this should go.
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 may be beginning to be resolved. Emblingia is often recovered as sister to other members of the clade (e.g. Cardinal-McTeague et al. 2016), although M. Sun et al. (2016) recovered a [Tovariaceae + Embligiaceae] clade, although it had little support. Of the sampled Stixideae (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 where they were to be placed was unclear; see Resedaceae-Stixideae below. 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; Cardinal-McTeague et al. 2016) or to Capparaceae et al. (Su et al. 2012), although in both cases with little support. Indeed, the relationships recovered by Cardinal-McTeague et al. (2016) are [[Tovariaceae [Pentadiplandraceae [Borthwickia [[Stixis + Tirania] [Forchhammeria + Reseda, etc.]]]]] [Capparaceae [Cleomaceae + Brassicaceae]]]. Edger et al. (2018) recovered the phylogeny below,
Classification. Small families were added in this area because some fugitives from the old Capparaceae were finding homes, but they are usefully combined in an expanded Resedaceae in A.P.G. IV (2016).
EMBLINGIACEAE Airy Shaw - Back to Brassicales
Subshrub; plant hispid; mustard oils?; cork cambium deep-seated; cambium storying?; sclereids +; leaves ± opposite, lamina ± cartlaginous, margins ± entire, stipules +; flowers axillary, monosymmetric; K connate, lobed, deeply divided abaxially, C 2, adaxial, connate by epidermis, slipper-shaped, not clawed; nectary adaxial, partly enclosed by walls from the petals [= calceolus]; androgynophore +, curved abaxially; A 5, opposite C, doubling in number [= dédoublement], fertile A 4, adaxial, filaments shorter than anthers, staminodes +, 3-6, abaxial, forming a torus/hood; pollen with short colpi with rounded ends and bulging apertures, adjacent exine thickened; G [(2-)3], odd member abaxial, placentation axile, stigma shortly lobed; ovule 1/carpel, ?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 initially largely followed Melville's interpretation (in Erdtman et al. 1969), see also Mueller (1860). Recent studies by Tobe (2015b) have clarified what is going on, in particular, how the flower is oriented. Although the flower is axillary, it reorients during deveopment so that it is presented to the pollinator as being inverted. In the characters allowing one to recognise the family (and in the family characterization pre-2015) the "pollinator's" orientation is emphasized, in the family characterization it is the "morphologist's" orientation! Tobe (2015b) also suggests that the androecium is haplostemonous and oppositipetalous; simple ndéduplication of the stamens occurs.
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 + Resedaceae]], Tovariaceae, [Cleomaceae [Capparaceae + Brassicaceae]]]: (glucosinolates chain-elongated BCAAs); "stipules" +, minute; gynophore +, short; ovules in two ranks, outer integument 2(-3) cells across; exotegmen fibrous.
Age. The age for this node is estimated to be 42-33 Ma (Wikström et al. 2001), (68-)57, 54(-45) Ma (Hall et al. 2010), (89-)61(-33) Ma (Edger et al. 2015, 2018) or (75.6-)68.5(-62)/(70.1-)61.7(-54.0) Ma (Cardinal-McTeague et al. 2016: note Tovaria is sister to this clade, resultant crown group age of whole clade, first set of numbers...).
Evolution: Ecology & Physiology. Dilated cisternae, protein–containing vacuoles derived from the endoplasmic reticulum (ER), alias protein–rich ER–dependent vacuoles, have been described from members of all families of this clade except Pentadiplandraceae (Jørgensen 1981). have a common origin
Brassicaceae, Resedaceae and Capparidaceae, at least, have a number of species that are gypsophiles, growing in soils rich in hydrous calcium sulphate, and some accumulate sulphur i.a. in organic compounds as well as in gypsum crystals (Escudero et al. 2014; C. T. Muller et al. 2017). Brassicales are often not associated with arbuscular mycorrhizal fungi (AF), and such fungi in gypsum-derived soils may be quite distinctive (Torrecillas et al. 2014). There is perhaps a parallel here with Caryophyllales, quite commonly growing in gypsum-rich soils and also often not AM plants.
Animal-Plant Interactions. The larvae of Chrysomelidae-Alticinae beetles are quite commonly to be found on members of this clade (Jolivet 1988).
Bacterial/Fungal Associations. An oomycetous white blister rust, Albugo, grows on Brassicaceae, Capparaceae, Cleomaceae, and Resedaceae, as welll as on Fabaceae (Onobrychis: Choi et al. 2011).
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 + Resedaceae]]: placentation axile, stigma lobed.
Age. This node is estimated to be (80-)55(-29.5) Ma (Edger et al. 2015, 2018) or (70.1-)61.7(-54) Ma (Cardinal-McTeague et al. 2016).
PENTADIPLANDRACEAE Hutchinson & Dalziel - Back to Brassicales
Shrubs or tuberous lianes; benzyl and 4-methoxybenzyl glucosinolates +, ellagic acid?, tannins?; ?cork; vestured pits +; nodes 3:3; mucilage cells +; lamina margin entire; inflorescence axillary, subcorymbose; flowers polygamous, 5-merous; K imbricate, C base enlarged, ± concave, limb flat, ± spreading; andogynophore +, short, nectariferous; 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 [list]/?1: Pentadiplandra brazzeana. Tropical W. Africa (map: from Hall et al. 2004; Trop. Afr. Fl. Pl. Ecol. Distr. 5. 2010).
Evolution: Divergence & Distribution. Ronse de Craene and Haston (2006) suggest that its floral morphology is close to the ancestral form of the core Brassicales.
Plant-Animal Interactions. Fruits contains the sweet-tasting (to most primates and many other monkeys) protein, brazzein - they are also described as having the flavour of a horseradish - however, this is false advertisement, since they are not a good source of energy. However, gorillas have a mutation in a taste gene, do not find the fruits sweet, and so are not deceived (Guevara et al. 2016).
Chemistry, Morphology, etc. 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.). Ronse Decraene (2002) described its floral anatomy; there are no marginal or placental strands in the ovary.
For general information, see Villers (1973) and Bayer and Appel (2002), for glucosinolates, see de Nicola et al. (2012), and for embryo colour, Martin Cheek (pers. comm.).
Embryologically - and in many other respects - Pentadiplandra is poorly known.
Previous Relationships. Cronquist (1981) included Pentadiplandra in his rather broadly circumscribed Capparaceae, Takhtajan (1997) segregated it as a family.
[Gyrostemonaceae + Resedaceae]: idioblastic myrosin cells 0; hairs unicellular; styluli +; seeds arillate.
Age. The age of this node is estimated to be (67-)46(-22.5) Ma (Edger et al. 2015, 2018) and (62.8-)53.5(-44.3) Ma (Cardinal-McTeague et al. 2016: Gyr + rest).
Evolution: Divergence & Distribution. There may have been an increase in diversification rates at this node (Edger et al. 2018).
Pollination Biology & Seed Dispersal. Posession of myrmecochorous seeds may be an apomorphy at this level.
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; nectary 0; 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-)many, borne around axis in 1 (2) whorls, connate or not, when G 2, transverse, (ovary roof +, 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, nuclear genome [1C] ca 0.65 pg.
5 [list]/18+: Gyrostemon (12). Australia, not in the north (map: see Fl. Austral. 8. 1982).
Age. Crown-group Gyrostemonaceae - [Gyrostemon + Tersonia] - are about (9.9-)5.7(-2.3) Ma (Cardinal-McTeague et al. 2016).
Evolution: Divergence & Distribution. Fossils of Gyrostemonaceae have been reported from the early Miocene ca 20 Ma from New Zealand (D. E. Lee et al. 2001).
Pollination Biology & Seed Dispersal. Gyrostemonaceae are wind-pollinated, hence the absence of a nectary; the seeds are myrmecochorous (Lengyel et al. 2010).
Genes & Genomes. A genome duplication, the GYRAα event, associated with this family has been dated to ca 31.9 Ma (Landis et al. 2018).
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).
Phylogeny. Gyrostemon is paraphyletic in the study of Cardinal-McTeague et al. (2016), although only three species were examined.
RESEDACEAE Martinov, nom. cons. - Back to Brassicales
± Woody; K valvate; A many.
8 [list]/96 - three groups below. Mostly Northern hemisphere, a few southern Africa.
Age. Crown-group Resedaceae are estimated to be (57-)47.8(-37.8) Ma (Cardinal-McTeague et al. 2016).
1. Borthwickia W. W. Smith
Small tree; ?hair type; leaves opposite, trifoliate, lamina margins entire, stipules 0; flowers 5-8-merous, ?monosymmetric; K connate; C with proximal and distal parts differentiated, not clawed; androgynophore +, short; filaments long; pollen exine perforate; gynophore quite long, G [4-6], ribbed, stigma undivided; ovules many/carpel, ?morphology; capsule ?septifragal; ?aril; n = ?
1/1: Borthwickia trifoliata. China (southwest Yunnan) and adjacent Myanmar.
Synonymy: Borthwickiaceae Su, Wang, Zhang & Chen
[Stixideae + Resedeae]: ?
Age. This clade is dated to (46.7-)38(-29.3) Ma (Cardinal-McTeague et al. 2016: Stixis + rest; see also Hall et al. 2015).
Evolution: Divergence & Distribution. Cardinal-McTeague et al. (2016) noted an increaser in species diversification at this node.
2. Stixideae Hallier
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).
Synonymy: Stixidaceae Doweld
3. Resedeae Reichenbach
Usu. herbs; 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.
3/75: Reseda (68). Warm temperate and dry subtropical, esp. Mediterranean-Middle East-North African, also Oligomeris in southern Africa, S.W. North America and S.W. China (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 Resedeae have been dated to (13.5-)12.6, 10.5(-8.7) Ma (Martin-Bravo et al. 2009).
Synonymy: Astrocarpaceae A. Kerner
Evolution: Divergence & Distribution. Martín-Bravo et al. (2007) discuss the phylogeny and biogeography of Resedeae. Oligomeris, native to both the Old and New Worlds (western), shows considerable disjunctions (Martín-Bravo et al. 2009), O. linifolia showing a recent disjunction between the Old and New Worlds (Martín-Bravo & Escudero 2012).
Pollination Biology & Seed Dispersal. The seeds of Reseda are myrmecochorous (Lengyel et al. 2010), however the seed ecology of Stixideae in particular is little known.
Chemistry, Morphology, etc. Forchhammeria contains methyl glucosinolates like those of Capparaceae and Cleomaceae (Mithen et al. 2010). The reaction wood contains gelatinous fibres, so if perhaps "normal" (Schweingruber 2006); c.f. Brassicaceae.
Resedeae are florally very variable. Thus Reseda alba seems to lacks a gynophore, Caylusea has a gynophore, Sesamoides has an androgynophore, while in R. luteola the stamens are inserted immediately below the carpels on a receptacular protrusion (Sobick 1983). The androecium of Reseda luteola may be in 3-4 whorls (for references, see Abdallah 1978), while Sobick (1983) shows the stamens as being opposite the petals and developing centrifugally, while in other taxa in Resedeae they develop from a ringwall. Ochradenus has C 0, A many, [G 3], the carpels are ultimately closed, and the fruit is berry-like - c.f. Gyrostemonaceae (Hufford 1996). Within Stixideae, Tirania has six sepals and petals, while Forchhammeria has two carpels, as well as an irregular number of sepals (again, see Gyrostemonaceae), no petals, one ovule/carpel, and only one ovule/fruit usually develops.
The seeds of Borthwickia are described as being 4-6 per capsule and the embryo as being scarcely differentiated by Zhang and Tucker (2008), but this must be incorrect. The appendages on the seeds in some Resedeae are also described as being caruncles. From illustrations in Hennig (1929) it is unclear whether the seeds are endotestal or exotegmic.
For general information on Resedeae, 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). For additional information on Stixideae, see Carlquist (1988b), 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 these genera in Capparaceae. For some information on Borthwickia, see Su et al. (2012).
Borthwickia in particular, but also most Stixideae, are poorly known.
Phylogeny. The above relationships between the three tribes were strongly supported in Z.-D. Chen et al. (2016). From the topology of the tree presented by Martín-Bravo et al. (2007), there are three main clades in Resedeae, [Caylusea [Sesamoides + Reseda]], Reseda including both Ochradenus and Oligomeris.
Classification. The expanded limits of Resedaceae are those suggested by A.P.G. IV (2016).
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 (6-)8(-9), opposite K; 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) and for floral morphology, see Fisch and Weberling (1990).
[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]; cork also cortical; (wood ± storied); vestured pits +; 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 6, 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 [Cleomaceae + Brassicaceae] has been dated to as little as some 31-24 Ma (Wikström et al. 2001), but other estimates are older, e.g. divergence at ca 41 Ma (Schranz & Mitchell-Olds 2006), around 41-34.7 Ma (Tank et al. 2015: Table S1, S2), ca 39.6 Ma (Magallón et al. 2013), at (55-)43, 41(-30) Ma (Bell et al. 2010) and at ca 58 Ma (Hall et al. 2015). Beilstein et al. (2010) suggest a still older age of (83.2-)71.3(-59.7) Ma, so clarification here, as elsewhere, is in order. The age for this node is estimated at (71.5-)49(-26.5)Ma by Edger et al. (2015, 2018), (60.8-)56.3(-52.1)Ma by Cardinal-McTeague et al. (2016), and also of (54.2-)48.0(-44.2) Ma and also substantially younger, but still Eocene (Magallón et al. 2018).
Evolution: Divergence & Distribution. Tank et al. (2015) note a pronounced increase of net diversification at this node (see also Cardinal-McTeague et al. 2016) as do Magallón et al. (2018) and Edger et al. (2018) - for ages, see above. This may be associated with the At-β genome duplication, which happened much earlier (see above).
Rodman et al. (1996) listed 11 possible apomorphies for this node; Iltis et al. (2011) also suggested apomorphies for around here.
Ecology & Physiology. PYK10 β-glucosidase, which has myrosinase activity, is to be found localized in ER bodies, rod-shaped bodies ca 10 x 1 μm derived from endoplasmic reticulum (Yamada et al. 2006; Nakano et al. 2016; Z. Wang et al. 2019). These ER bodies have been found only in core Brassicales and are especially noticeable in roots and seedlings, but can be induced elsewhere by wounding (Z. Wang et al. 2019 and references). (These ER bodies have been equated by what have been called "dilated cisternae" in the literature, - for literature on their distribution, see Nakano et al. (2016), however, Jørgensen (1981) described two kinds of dilated cisternae from Brassicales, and ER bodies may perhaps be compared with her utricular cisternae.) PYK10 β-glucosidase is a member of a group of some 16 myrosinases and it acts on indole glucosinolates; it seems to be involved in interactions with soil-dwelling microbes (Nakano et al. 2016). For further discussion, see below.
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; Edger et al. 2015, also above). For details of the interactions of butterflies and plants, see Courtney (1986) and Chew (1988 and references). Caterpillars of ditrysian moths of the Yponomeutoidea-Plutellidae are also common on this group (Sohn et al. 2013).
Bacterial/Fungal Associations. Ca 1,000 species are susceptible to pseudoflower-forming rust fungi, Puccinia spp. (Roy 1993, 2001); see especially Brassicaceae, also above.
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 and Gyrostemonaceae (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 (Resedaceae-Stixideae) 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). For additional discussion on chemistry, see Leite and Castilho (2017); they suggest that "allyl glucosinolates" are common here.
For a survey of floral morphology, see Endress (1992); Brassicaceae were compared with Cleomaceae and Capparaceae combined. 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 in Brassicaceae) and 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/soon deciduous, stems green); 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; (gynophore 0 - Dipterygium); 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 (324): 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.]
Age. The age of crown-group Capparaceae is around (57.8-)49.5(-39.2) Ma (Cardinal-McTeague et al. 2016).
Evolution: Divergence & Distribution. For other agess in the family, see Cardinal-McTeague et al. (2016).
Ecology & Physiology. Capparaceae are notably prominent in seasonally dry tropical forests (Pennington et al. 2009).
Genes & Genomes. There may be a whole genome duplication preceding diversification here, and variation is chromosome number is considerable (Lysak 2018 and references: x = 13?).
Chemistry, Morphology, etc. New World Capparaceae have several distinctive and perhaps unique glucosinolates (Mithen et al. 2010).
Capparis retusa is reported to have stipules and 3:3 nodes, as well as as axillary nectaries (di Sapio et al. 2001). 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: esp androecium and gynoecium), 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; Cardinal-McTeague et al. 2016; M. Sun et al. 2016). For relationships in Capparis, see Tamboli et al. (2017).
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 Resedaceae-Stixideae, Setchellanthus (Setchellanthaceae), Pentadiplandra (Pentadiplandraceae) and Koeberlinia (Koeberliniaceae). At least all are still members of Brassicales!
[[Cleomaceae + Brassicaceae]: annual or perennial herbs (shrubs); inflorescence ± corymbose, (bracts foliaceous); A 6; stigma not lobed; 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) Ma, while the estimate in Bell et al. (2010) is (43-)33, 31(-21) Ma old. Other estimates are 23-18 Ma old (Wikström et al. 2001), some 41 Ma old (Schranz & Mitchell-Olds 2006), (45-)19(-1) Ma (!: Franzke et al. 2009: 95% HPD), some 50 Ma (Al-Shehbaz et al. 2006), (62-)43(-23) Ma (Edger et al. 2015, 2018), ca 52.6 Ma (Kagale et al. 2014), and (60.7-)59.5, 55.5(-54.3) Ma (C.-H. Huang et al. 2015). The age of this node is (53.8-)50.8(-48.5) Ma in Cardinal-McTeague et al. (2016).
Evolution: Divergence & Distribution. The flowers of Cleomaceae are 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). 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), so where details of symmetry changes go on the tree remain to be firmly established; monosymmetric flowers are scattered throughout core Brassicales. How colours in flowers of at least some Cleomaceae and Brassicaceae change with age may be distinctive (Nozzolillo et al. 2010).
Ecology & Physiology. For a major reduction of plant height at this node, see Cornwell et al. (2014). About 1,050 species (ca 28%) of Brassicaceae are annuals (Hohmann et al. 2015), as are a number of Cleomaceae.
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 studied). Long non-coding RNAs found in the few species from this clade examined were conserved in position, often being near important genes, but they varied in their sequences - and in Arabidopsis thaliana, at least, they tended to be close to the telomeres (Mohammadin et al. 2015). 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). The gene that microRNA827 targeted had changed in the taxa in Brassicaceae and Cleomaceae examined, while microR827 itself was lost in Carica (Lin et al. 2017).
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).
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). For floral development, see Leins (2000, and references).
CLEOMACEAE Berchtold & J. Presl - Back to Brassicales
Herbs (annual) to shrubs (small trees); root hairs 0; hairs simple (plant glabrous), (multicellular glands); petiole bundle(s) arcuate to forming a ring; leaves palmately compound (simple), stipules filiform to laciniate or spinose/0; bracts foliaceous (not); (plant monoecious - Podandrogyne); flowers monosymmetric (weakly so/polysymmetric); K with one trace [?all], adaxial member envelops the bud/all ± equal, C (toothed), (nectary on C towards base); (androgynophore +); A (1-)6(-many), (staminodes +, 2-many), anthers coiled at dehiscence, linear, (filaments apophysate [± swollen towards the apex]); pollen surface variously sculpted, often spinulose; (gynophore +), (G , orthogonal), stigma capitate to punctate; inner integument 2-10 cells across, parietal tissue 2-5 cells across, (nucellar cap ca 2 cells across), (endothelium +); fruit (nut-like/winged - Dipterygium), longer than broad [= silique]; 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.
25 and counting [list]/270 (346): Sieruela (40), Tarenaya (30), Cleome (27), Podandrogyne (26), Cleomella (25). 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.]
Age. Crown-group Cleomaceae are (48.7-)43.2(-37.3) Ma (Cardinal-McTeague et al. 2016).
Evolution: Divergence & Distribution. For additional ages for nodes in the family, see Cardinal-McTeague et al. (2016). Soltis et al. (2009) suggested that diversification in Cleomaceae might be connected with the Thα genome triplication (see below); see also S. Cheng et al. (2013). The duplication may be linked with floral developmental in which the sepals are more or less equal in bud, termed the early disymmetric pathway (Patchell et al. 2011; Bayat et al. 2018), although mature flowers of the species with that pathway are frequently monosymmetric...
Biogeographic relationships in Cleomaceae are interesting. If Cleomella, a smallish North American clade, is sister to the rest of the family, 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; see also Huang et al. 2016). 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, root endodermal cells seem to have been coopted in bundle sheath development in both (Külahoglu et al. 2014), while there is a set of transcription factors expressed along with C4 photosynthesis genes in the two (Aubry et al. 2014). See also Bayat et al. (2018) for C4 photoynthesis, etc..
A number of taxa grow in quite arid environments.
Pollination Biology & Seed Dispersal. Despite their often monosymmetric flowers, there is little to report about pollination (Bayat et al. 2018).
Plant-Animal Interactions. For the evolution of the glucosinolate pathway in Tarenaya hassleriana following a genome duplication, although tandem duplications, etc., are also involved, see van den Bergh et al. (2016).
Genes & Genomes. A duplication (hexaploid), the Cs-α or Th-α event, of the genome occurred ca 13.7 or 20 Ma (Schranz & Mitchell-Olds 2006: Cleome spinosa; M. S. Barker et al. 2009: C. spinosa; S. Cheng et al. 2013: Tarenaya hassleriana, also called the Tr-α duplication; van den Bergh et al. 2014, 2016).
The genome of Cleome spinosa is about twice the size of that of Arabidopsis thaliana (Schranz & Mitchell-Olds 2006; 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) and Bayat et al. (2018), 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 s.l. itself is widely scattered on the tree (Hall 2008; Bayat et al. 2018). 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 for clades in analyses of the chloroplast markers than from ITS: A group of North American Cleomaceae (= Cleomella) were sister to the rest of the family, and the C. droserifolia group (= Rorida) 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); Cardinal-McTeague et al. (2016) also found Cleomella to be sister to the rest of the family. However, Barrett et al. (2017) found that Cleome s. str. was sister to the rest of the family, although support was weak.
For phylogenies of parts of the family, see Sánchez-Acebo (2005), Catalan et al. (2007), Inda et al. (2008b), Riser et al. (2013) and Barrett et al. 2017). 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; see also Cardinal-McTeague et al. 2016; Barrett et al. 2017).
Classification. Generic limits were for some time very unsatisfactory and needed attention (see e.g. Hall et al. 2008; Riser et al. 2013). Many of the clades did not even correspond even to sections of Cleome, however, the wholesale dismemberment of Cleome that was under way then was poorly advised; piecemeal splitting is not a course to be advocated. However, 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), and Roalson et al. (2015), and Roalson and Hall (2017) have begun a re-evaluation of generic limits in the family as a whole; in the latter, five monotypic genera rather than one variable genus were recognized in part because the species came out in four (actually three) places in the key....
Synonymy: Oxystylidaceae Hutchinson
BRASSICACEAE Burnett, nom. cons.//CRUCIFERAE Jussieu, nom. cons. et nom. alt. - Back to Brassicales
(Nortropane alkaloids +), (camalexin - indole alkaloid - +), methyl glucosinolates 0, chain elongation of 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.; tapetal cells binucleate; pollen grains tricellular, with tryphine, orbicules 0, surface often reticulate; gynophore short/0; ovary with commissural septum [= false septum], stigma commissural, dry; ovules slender, outer integument 2-4(-5) cells across, inner integument (2-)3-8(-15) cells across, endothelium +, body of ovule long, slender, parietal tissue 1 cell across (0 - Malcombia), 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; x = 8; duplication of PHYB → PHYD gene, loss of CYP73 gene duplicate [class II]; sporophytic self-incompatibility system present; At-α genome duplication, 2C genome size (0.51-)0.89(-1.55) pg.
353 [list]/4,010 - six groups below. World-wide, esp. Tajikstan, Turkey and N. Temperate and drier areas in general, few Australia southern Africa (map: from Vester 1940; Hultén 1971; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003). [Photos - Collection].
Age. Crown group diversification, i.e. separation of Aethionemeae from the rest, occurred perhaps ca 40 Ma (Al-Shehbaz et al. 2006, see also Koch 2011). Other estimates are a mere (35-)15(-1) Ma (Franzke et al. 2009), (46-)32(-17) Ma (Edger et al. 2015, 2018, see also Hohmann et al. 2015), (49.4-)37.6(-24.2) Ma (Couvreur et al. 2010: also summary), (46.6-)43.4(-40.3) Ma (Hall et al. 2015, see also Cardinal-McTeague et al. 2016), (42.7-)42, 37.1(-36.3) Ma (C.-H. Huang et al. 2015) or (58.9-)48(-37.5) Ma (Mohammadin et al. 2017). Beilstein et al. (2010) suggested an age of (64.2-)54.3(-45.2) Ma for crown group Brassicaceae. Franzke et al. (2016) discuss the various problems surrounding dating here.
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 subshrub, perennial (annual) herb, (spiny); nortropane alkaloids +; plant glabrous; leaves articulated between petiole and blade, blade ± linear (to broadly obovate), undivided, margin entire; 3 veins on petal claws; nectaries 2, lateral; (1-)2-4(-8) ovules/carpel; fruit short, relatively broad ["silicle"], surrounded by wing, angustiseptate, (also indehiscent, plant heterocarpic); testa (mucilaginous); cotyledons accumbent; n = 7, 8 (11, 12, 14...).
1/60-70. The Mediterranean and Southern Europe to Afghanistan, esp. Turkey-Iran (map: from Hedge 1976; see also Mohammadin et al. 2017). [Photo - Flowers.]
Age. Estimates for the age of crown-group Aethionemeae range from (28-)11(-1) Ma (Franzke et al. 2009), ca 11.3 Ma (Hohmann et al. 2015) to (30.9-)20.6(-10.8) Ma (Cardinal-McTeague et al. 2016), (34.6-)24(14.6) Ma (Mohammadin et al. 2017) and (54.3-)46.9(-39.4) Ma (Beilstein et al. 2010).
[Clade E [Clade D [Clade A [Clade B + C]]]] / core Brassicaceae: (methionine-derived glucosinolates 0), structural elaborations of glucosinolates; (included phloem +); (indumentum various); (flowers monosymmetric - esp. Streptanthus); (C fringed or lobed); A (2, 4, to 24 - Pringlea), (long); tapetosomes with T-oleosin; (pollen omniaperturate); (G stipitate), (commissural septum 0 - Pringlea), (style long); fruit angusti- or latiseptate, quadrangular; (seeds winged); cotyledons also variants of conduplicate-incumbent, etc.; genome duplication [At-α, Br-α].
Age. Koch (2012) suggested an age for this node of around (53.5-)49(-43) Ma, in line with the estimates of Beilstein et al. (2010); 38 Ma was the estimate in Hall et al. (2015: "core Brassicaceae"), (35.6-)35.1, 29.7(-29.1) Ma in C.-H. Huang et al. (2015), and ca 23.3 Ma that in Hohmann et al. (2015: note topology). Couvreur et al. (2010) suggested an age of ca 32.3 Ma, (28-)11(-1) Ma was suggested by Franzke et al. (2009) and ca 25.3Ma by Edger et al. (2018: Arab-Brass).
Clade E (Hesperideae, etc.)
multicellular glands (0); stigma lobes decurrent (not lobed); fruit longer than broad.
Age. The age of this clade is (17.6-)17.2(-16.8) Ma (C.-H. Huang et al. 2015).
[Clade D [Clade A [Clade B + C]]]: ?
Age. This clade is (29-)28.5(-27.8) Ma (C.-H. Huang et al. 2015).
Clade D. (Hairs stellate); (stigma lobed, lobes not decurrent); fruit relatively broad.
Alysseae de Candolle
Hairs stellate; filaments with appendages; capsule latiseptate to terete (angustiseptate); seeds "few"; n = (7) 8 (9, 11, 15).
24/280: Alyssum (105), Odontarrhena (95). Eurasia, North Africa (1 sp. northwest North America).
[Clade A [Clade B + C]]: (stigma variously lobed).
Age. The crown-group age of this clade is (28-)27.4(-26.9) Ma (C.-H. Huang et al. 2015).
(Cardenolides + - Erysimum); (hairs stellate); fruit longer than broad.
Age. The crown-group age of clade A is (24-)23.6(-23.1) Ma (C.-H. Huang et al. 2015), 21-15 Ma (Fiebig et al. 2004) or 18.9(1) Ma (Mandáková et al. 2017).
Cardamineae DumortierErysimum ([150-]225[-300]), Cardamine (200).
Descurainieae Al-Shehbaz, Beilstein & E. A. KelloggDescurainia (50),
Smelowskieae Al-Shehbaz, Beilstein & E. A. Kellogg
[Camelineae [Erysimieae + Alyssopsidae]: ?
Age. The age of this clade is ca ca 9.5(1) Ma (Mandáková et al. 2017).
Camelineae de Candolle
[Erysimieae + Alyssopsidae]: ?
Age. The crown-group age of this clade is ca 8.6(0.8) Ma (Mandáková et al. 2017).
Crucihimalayeae D. A. German & Al-Shehbaz
[Halimolobieae + Boechereae]: ?
Age. The age of this clade is ca 11.1(0.9) Ma (Mandáková et al. 2017).
Halimolobieae Al-Shehbaz, Beilstein & E. A. Kellogg
Boechereae Al-Shehbaz, Beilstein & E. A. KelloggBoechera (110).
Microlepidieae Al-Shehbaz, Warwick, Mummenhoff & M. A. Koch
Annual to perennial; n = 4, 6-8, 10 (24).
17/56: Pachycladon (11). Australia (most), New Zealand.
[Clade B + C]: ?
Age. The crown-group age of this clade is (27.1-)26.6(-26.1) Ma (C.-H. Huang et al. 2015).
Fruit (terete), relatively broad, (longer than broad, often segmented [lomentum]); seeds usu. not winged; x = 7, (Br-α WGD - Brassiceae).
Age. This clade has been dated to (24.2-)23.7(-23.3) Ma (C.-H. Huang et al. 2015).
Sisymbrieae de CandolleSisymbrium s. str. (45: only Old World).
Brassiceae de Candolle
(Plant ± glabrous); nortropane alkaloids +; nectaries 4; fruit relatively broad; n = (7, 11), 12, (13).
Age. Clade C is some (26.2-)25.7(-25.1) Ma (C.-H. Huang et al. 2015).
2/30. The western Mediterranean, maritime Western Europe, circum-Arctic (map: from Hultén & Fries 1986; Koch 2012).
2-12 ovules carpel; capsule lati- or angustiseptate.
5/70: Biscutella (55).
Draba (365), Noccaea (130), Arabis (120), Physaria (105: inc. Lesquerella: pollen 4≤ colpate), Rorippa (85), Heliophila (80), Isatis (80), Matthiola (50), Hesperis (45). World-wide, esp. N. temperate (diverse in the Irano-Turanian area, less so in E. North America), uncommon in humid lowland tropics. [Photo - Flowers, Flowers, Fruit.]
Lepidieae de Candolle
Synonymy: Arabidaceae Döll, Drabaceae Martynov, Erysimaceae Martynov, Isatidaceae Döll, Raphanaceae Horaninow, Schizopetalaceae A. Jussieu, Sisymbriaceae Martynov, Stanleyaceae Nuttall, Thlaspiaceae Martinov
Evolution: Divergence & Distribution. The very different ages suggested for Brassicaceae (see also Moazzeni et al. 2014; esp. Franzke et al. 2016 for literature) are reflected in differences in dates of diversification within tribes, of ancient hybridization events, etc.. Thlaspi primaevum, some 30.8-29.2 Ma old, is known from Oligocene deposits in Montana, and Manchester and O'Leary (2010) thought it was indeed a Thlaspi; there are even impressions of the distinctive seeds on the capsule wall (Beilstein et al. 2010). However, the attribution of this fossil to the genus, even the family, has been questioned (Franzke et al. 2011), indeed, it is older than some estimates of the family age in C.-H. Huang et al. (2015: e.g. c.f. Fig. 5). Franzke et al. (2011) noted how age estimates for the family changed when the the fossil was used in the calibration - deeper nodes are ca 5 Ma older, and many prefer a crown-group age of 38-32 Ma (Esmailbegi et al. 2018). Couvreur et al. (2010: Table 3), Hohmann et al. (2015), C.-H. Huang et al. (2015), Cardinal-McTeague et al. (2016) and Mandáková et al. (2017) give diversification times for various clades within the family, which overall has high speciation rates and a small genome, albeit a high rate of genome change, all correlated (Puttick et al. 20015).
Hardly surprisingly, there are various ideas - not all incompatible - about the diversification of Brassicaceae. Stem Brassicaceae may have been adapted to warm and humid conditions in the east Mediterranean area, later moving into more open and dry environments (Franzke et al. 2009). Alternatively, the family may have originated in a tropical environment, subsequently radiating with the onset of aridification and global cooling 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 now (Hedge 1976; Franzke et al. 2009, 2011 and references; Karl & Koch 2013). Aethionema itself seems to have diversified along the Anatolian diagonal, the area in Turkey between the N.E. Mediterranean and S.W. Black Sea (Mohammadin et al. 2017: Cleome droserifolia used in ancestral area reconstructions); note that in this reconstruction there is a fuse of ca 24Ma before diversification in the genus begins. Mohammadin et al. (2017) cite several papers suggesting that inital diversification of everything from species (Arabis alpina), genera and tribes (Arabideae) had been in this particular area or in the general Anatolian region. 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) - but did this happen around about the Eocene-Oligocene cooling or substantially later (C.-H. Huang et al. 2015)?
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); this duplication has been dated to ca 25 Ma (Woodhouse et al. 2011) or ca 47 Ma (Kagale et al. 2014), although note that 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 event - they thought it characterized the whole family - and diversification in the family. Kagale et al. (2014) and Hohmann et al. (2015) survey chromosome number and genome size across the family, linking changes in these features with increasing diversification and also linking them with climatic changes in the Neogene in particular; most diversification has taken place in the last 23 Ma.
Edger et al. (2015, 2018) noted a notable increase in diversification in core Brassicaceae and the evolution of considerable diversity in glucosinolates following the At-α duplication event, interestingly, anthocharine and pierine Pierinae independently colonized the family and diversified there. Anthocharine speciation increased ca 22 Ma and that of the [Brassiceae + Sisymbrieae] clade increased ca 21 Ma (Cardinal-McTeague et al. 2016).
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, the initial hybridization occurring probably in Australia and within the last 1.3 Ma (Mummenhoff et al. 2001, 2004; 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 (Majeský et al. 2017 and literature), the latter even occuring between genera of Boechereae (Windham et al. 2014). The speciose crown-group Arabideae are perhaps around 14 Ma, but much diversification has been within the last 5 Ma, 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 Ma (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 has northern and southern clades, with the cushion life form evolving independently in taxa growing in more extreme conditions in both the main clades that they recovered. Some distributions have been explained by vicariance. Thus the sister-group relationships between taxa of Descuraina from Macaronesia and the Mediterranean and those from North America has been attributed to vicariance events as the North Atlantic opened 120-100 Ma (Grehan 2017), which adds another if perhaps unlikely dimension to the whole discussion. For diversification in the Macaronesian Crambe section Dendrocrabe within the last ca 8.2-7.2 Ma, see S. C. Kim et al. (2008).
Aethionema, with a more or less sessile gynoecium, is sister to all other Brassicaceae. Stanleya, etc., are well embedded in Brassicaceae (as Thelypodieae - Koch et al. 2012; not included in C.-H. Huang et al. 2015), and their similarities to Cleomaceae, e.g. long gynophore and stamens, are parallelisms (Galloway et al. 1998). Characters associated with clades 1-5 below are taken from C.-H. Huang et al. (2015).
See Beilstein et al. (2006) for trichome evolution; this is put in a different phylogenetic context by C.-H. Huang et al. (2015).
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 precipitation that does fall is not very seasonal (Franzke et al. 2010; Cornwell et al. 2014). Brassicaceae also include over 60 species of cushion plants, a disproportionatey high number; such plants favour cold and dry conditions (Boucher et al. 2016b).
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; see Boyd 2007, Grennan 2009, and Anjum et al. 2012 for reviews; Australian J. Bot. 63(1-2). 2015). 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: White 2016 for a summary of the literature), but not by other species of the genus, however, a number of its immediate relatives, including Brassica napa, are also Se tolerant (Cappa et al. 2014b). Se - up to ca 1.5% dry weight, 30% elemental Se has been recorded - may protect the plant against herbivory by prairie dogs and arthropods alike (Galeas et al. 2007; Freeman et al. 2009; Cappa et al. 2014a; Schiavon & Pilon-Smits 2016); S. pinnata incorporates Se into the non-protein amino acid methylselenocysteine (with a C-Se-C motif) and so is unaffected by it. Endophytic bacteria are involved in Se uptake into the plant (Lindblom et al. 2013; Sura-deJong et al. 2015 and references). 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).
Thellungiella halophila reproduces even when the salt concentration of the water in which it is growing is that of seawater (Gong et al. 2005), while tolerance to salinity in Eutrema has been studied in detail (see articles in Ann. Bot. 115(3). 2015).
For cabbage whites (Pieris spp.) as keystone herbivores of Brassicaceae, see Poelman and Kessler (2016). Glucosinolate diversity in the family is considerable, as is variation in content between different brassicaceous species in the same community and different genera in the same tribe, although few glucosinolates seem to be unique to a particular species. Thus Arabidopsis thaliana alone can synthesize over 40 different kinds and a number of other taxa can synthesize around 20 or so, indeed, members of Brassicaceae-Cardamineae can synthesize around half the known glucosinolates (Olsen et al. 2016). There is even infraspecific variation in the type of glucosinolate produced - as well as in triterpenoid saponins - in Barbarea vulgaris (Byrne et al. 2017). Species like A. thaliana have distinct chemotypes (six in this case) which may have distinct distributions within species, overall, herbivory is affected by the particular glucosinolates a plant may have (Bidart-Bouzat & Kliebenstein 2008; Nallu et al. 2017). 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). Although glucosinolates are defences against many herbivores, specialist herbivores like Pieris brassicae prefer plants with glucosinolates over those in which glucosinolate-producing genes have been inactivated (Schweizer et al. 2013); interestingly, the butterfly responds to the glucosinolate odour only after mating (Ikeura et al. 2010). Winde and Wittstock (2011) discuss the various ways in which insects can avoid the harmful effects of glucosinolates.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. Further details of the plant-insect association are discussed below.
Glucosinolates can depress vesicular-arbuscular mycorrhizal activity in other plants, and this may help Alliaria petiolata be invasive in parts of North America (Wolfe & Klironomos 2005: see also "Bacterial-Fungal Associations" below).
There are a number of proto-Kranz species in Brassicaceae (R. Sage et al. 2014).
Arabidopsis thaliana can take up organic nitrogen as amino acids (Hirner et al. 2006), although the 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: Busch et al. 2012); 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 functional groups. Polinatots may have driven some of the variation in floral shape, but overall the connection between pollinator and floral morphology is slight (Gómez et al. 2015), although another way of looking at things is that despite a "very similar floral bauplan", there were connections between floral morphology and pollinators, especially when these latter were specialized (Gómez et al. 2016: p. 889).
The sporophytic incompatibility system common in Brassicaceae has been much studied (e.g. Dickinson et al. 1998; Tarutani et al. 2010; Nasrallah 2011; S. Cheng et al. 2013). Some of the components of the incompatibility system are contained in the distinctive tryphine covering the pollen grains, and some components are produced by the individual pollen grains, so although the incompatibility system is usually 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 pollen tube and allowed it to penetrate the Torenia embryo sac (Takeuchi & Higashiyama 2012).
Apomixis at the diploid level is known from Boechera (Hörandl et al. 2007 and references).
Explosively dehiscent capsules are known in Cardamine, probably the result of a combination of square exocarp cells that contract in length but increase in volume when the fruit dehisces, and hypodermal cells of the endocarp with a distinctive hinged U- or V-shaped pattern of lignification that cannot contract, dehiscence occurring when the fruit is turgid, not dry (Hofhuis et al. 2016; Hofhuis & Hay 2017). In taxa like Arabidopsis fruit opening is not explosive. In C. hirsuta mucilaginous pectins accumulate in the endocarpial area (Vaughan et al. 2011), while in other taxa it is the extotesta that is quite often mucilaginous (e.g. d'Arbaumont 1890; Vaughan & Whitehouse 1971), 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 (Western 2011; 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. 2006, 2011); the two parts of the fruit may separate transversely and so the one plant can have very different dispersal mechanisms. Although phylogenetic relationships in Brassiceae are uncertain, heteroarthrocarpy is likely to have evolved more than once here (Hall et al. 2011); for the evolution of heteroarthrocarpy in Raphanus, see Avino et al. (2012).
Plant-Animal Interactions. For the diversification of Pierinae butterflies on Brassicaceae, see above; caterpillars of Yponomeutoidea-Plutellidae moths are also common here (Sohn et al. 2013). The presence of particular glucosinolates may induce oviposition by cabbage white butterflies, whether or not the crucifer with those glucosinolates is edible or kills the caterpillar (Chew 1979, see also 1988). Gene expression in both host and herbivore change most as eggs are laid, less in the plant as it is being eaten or in the caterpillar, indeed, about 50% of the genes of Arabidopsis thaliana change their expression on oviposition by Pieris rapae (Nallu et al. 2017). 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). Caterpillars of cabbage white butterflies and the diamond-back moth (Plutella xylostella) are able to detoxify the isothiocyanates produced when they damage plant tissue. The hydrolysis process is normally catalyzed by myrosinase, instead, the hydrolysis process is redirected, and non-toxic substances such as nitriles are produced by the plant's nitrile-specifier protein (Wittstock et al. 2004; Ratzka et al. 2002; Nallu et al. 2017); the whole process can be very complex (Agerbirk et al. 2010).
Furthermore, parasitoids of the caterpillar are attracted to the scene, and interactions become very intricate (Fatouros et al. 2008). Thus the effect of caterpillars on the plant can be manipulated by braconid parasitoids of the caterpillars - indeed, it was found that plant responses to herbivory depended more on the identity of the parasitoid than of the pierid caterpillar, and was ultimately affected by polydnaviruses associated with and specific to the parasitoid. The effect of the parasitoid on the plant was mediated by the composition of the fluid that the caterpillar regurgitated during eating, and this effect also involved changes in the volatiles the plant produced; these volatiles gave hyperparasites, in this case ichneumonid wasps, information about whether or not their prey, the braconid larvae, were present (Poelman et al. 2011; Zhu et al. 2018; see also Tan et al. 2018). Further details of the plant-insect association are discussed above.
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). 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).
Bacterial/Fungal Associations. The association between the pseudoflower-forming Puccinia rust, a basidiomycete, and its brassicaceous host has been much studied (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 the crucifer host and the other plants in the general area, containing i.a. constitutively-released isothiocyanates, aldehydes, esters, and aromatic alcohols (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.
Any arbuscular mycorrhizal (AM) associations in the roots of Brassicaceae are at most weak and facultative (Medve 1983). Thus although AM have been reported from Thlaspi, it is doubtful if an effective symbiosis results (Regvar et al. 2003), and this is certainly true of Arabidopsis thaliana (Veiga et al. 2013). Cosme et al. (2018) develop this theme, noting that the role of AM associations in Brassicaceae was unclear, but at the same time, understanding the behaviour of those taxa that formed rudimentary arbuscular mycorrhizal (RAM) association may help understand how AM in general function. How Brassicaeae might compensate for the absence of functional AM associations is beginning to be understood. Ascomycete helotialean fungi common in the root cortex of non-mycorrhizal Arabis alpina are involved in the uptake of P in low-P soils with the consequent improved growth of the plant (Almario et al. 2017). Hiruma et al. (2016) looked at the association of another ascomycete endophyte, Colletotrichum tofieldiae, with Arabidopsis and found a similar relationship, which, they noted, was reminiscent of mycorrhizal associations.
The oomycete Albugo, the white blister rust, parasitizes a number of Brassicaceae (Ploch et al. 2010a), although it quite commonly also persists as a symptomless endophyte (Ploch & Thines 2011); in some cases it facilitates infestation by Phytophthora infestans, another oomycete (Prince et al. 2017). However, the loss of the RAM2 locus compromises the establishment both of mycorrhizal associations and of infections by a variety of oomycetes (Wang et al. 2012; Gobbato et al. 2013, see also above.
Genes & Genomes. X = 8 may be ancestral in the family (Lysak et al. 2006, 2016; Murat et al. 2015b), x = 4 being the number of the pre-At-α duplication genome (Franzke et al. 2011 and references). This duplication of the whole genome, the Ata/At-α/ARTHα palaeopolyploidization, has been dated to as much as 34-25 or 60-20/ca 25 Ma, fairly soon after the split of Brassicaceae from Capparaceae (Vision et al. 2000; Blanc & Wolfe 2004a; M. S. Barker et al. 2009; Woodhouse et al. 2011), perhaps just 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; Y. Yang et al. 2015; Edger et al. 2015; c.f. Schranz et al. 2012) or before it (Lysack 2018). Ca 14.1 Ma is the age suggested by Landis et al. (2018) for this event. Three duplication events were picked up by Vanneste et al. (2014a) and dated at (69.4-)61.2(-54.6) Ma (the ARTHβ event?), (52.3-)50.1, 48.7(-47.6) Ma, and (28.6-)26.8(-24.8) Ma, while Kagale et al. (2014) date the main duplication to 47±1 Ma - note that some of these ages predate other ages for the split of Cleomaceae and Brassicaceae. There is evidence of fractionation bias or genome dominance associated with duplications in Arabidopsiss and in particular in Brassica, suggesting alloploid events in both cases (Garsmeur et al. 2013).
Woodhouse et al. (2011) discussed gene transposition after the Ata/At-α duplication event; see also Jiang et al. (2013) and Murat et al. (2015a) for what happened to duplicated genes and to the latter in particular for the fates of the centromeres. 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), and chromosome remodelling in Brassicaceae is also discussed by Lysak et al. (2016). Lysak et al. (2016) found that numbers of genome blocks (for which, see also e.g. Parkin et al. 2005), polyploidy events, and chromosome numbers were not necessarily connected. In Arabidopsis 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). T. Zhao and Schranz (2019), looking at genome order across angiosperms, found that overall there was a low proportion of syntenic genes, however, Brassicaceae had a notably high proportion of such genes, and they also had a number of multicopy and/or lineage-specific microsynteny clusters that were specific to them (Zhao &Schranz 2019).
Subsequently there has been extensive hybridization and associated genome duplications (Vision et al. 2000; Kellogg & Bennetzen 2004; Blanc & Wolfe 2004a; Blanc et al. 2007; Lysak et al. 2007, 2016). Franzke et al. (2011) discuss genome duplication events in detail, suggesting that several more remain to be discovered. Apparently diploid species like Brassica oleracea, with n = 9, are hypothesised to be ancestral hexaploids, the hexaploidy event occurring 16-5 Ma (the Br-α event: Mitchell-Olds et al. 2005; Lysak et al. 2005; X. Wang et al. 2011; Tang et al. 2012; S. Cheng et al. 2013). Jaillon and Eury et al. (2007) suggest that Arabidopsis has had two quite recent whole genome duplications, although there is some discussion as to the exact number, however, an At-α event has been dated to ca 23 Ma (Barker et al. 2009; Hao et al. 2018 and references). Hao et al. (2018) discuss the subsequent response to natural selection of the genes that have remained duplicated, and their response reflects their pre-duplication selection regimes. The immediate origin of the Brassiceae genome can be represented by 4x X 2x → 3x → 6x, where x = 7 (Cheng et al. 2013 and references). There are of course earlier duplications, so the genome of extant Brassica represents around 288 multiples of the angiosperm ur-genome (Wendel 2015; see also Chalhoub et al. 2014), and in some Brassicaceae chromosomal reorganizations have been very extensive (Koch & Kiefer 2005). The La-α (Leavenworthia alabamica triplication event is about the same age as the Br-α event. 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 Ma (Koch et al. 2005). The Antipodean Microlepidieae are thought to be the polyploid descendents of a Crucihimalayeae (n = 8) x Smelowskieae (n = 7) → n = 13 event that occured 10.6-7 Ma in the Northern Hemisphere, with several subsequent reduction series developing, and n = 4 in some species (Mandáková et al. 2017). Thelypodieae are very diverse, and genome duplication may be involved here, too (Hawkins et al. 2017). Hohmann et al. (2015) also discuss genome evolution in detail.
Still lower level hybridization/polyploidization events are common in the family, including in Arabidopsis and Brassica (see Soltis et al. 2016b annd references). 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 hybridization within Brassica involved members of clades that have been separate for around 18 Ma (20 Ma 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). Xiaowu Wang et al. (2011) noted the extensive gene loss following genome triplication in Brassica, as in polyploidization events in general.
Genome duplications aside, details of karyotype evolution in the family are of considerable interest. Chromosome numbers in the family range from n = 4-13 on upwards - thus the diploid number of Brassica napus is 38. 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 & Lysak 2008; Franzke et al. 2011). 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 (X. Wang et al. 2011). Johnston et al. (2005) discussed the evolution in genome size in Brassicaceae; in that part on which they focussed (Caps. Lepid Cardam. Brass Draba) there tended to an increase, although the ancestral size was estimated to be a mere 1C = 0.2 pg. Overall, genome size was quite small and not that variable when compared with other families (Johnston et al. 2005), and it was not particularly linked with chromosome number (Lysak et al. 2009, 2016). The small genome of Arabidopsis is probably the result of illegitimate recombination (Devos et al. 2002).
For the loss of the CYP73 class II duplicate gene involved in the phenolic network, see Renault et al. (2017); this duplication may have occurred in the common ancestor of extant seed plants or, perhaps more probably, that of flowering plants.
T. Sun et al. (2018) discuss the evolution of a set of transposable elements that was probably in place at the Core Brassicaceae node, at least, and the subsequent movement of these genes to Brassicaceae.
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.
Economic Importance. For oils from oilseed rape, other brassicas, and even Lesquerella, see papers in Vollmann and Rajcan (2009). Caterpillars of the diamondback moth, Plutella xylostella (Yponomeutoidea-Plutellidae), are a major pest of cruciferous crops, especially cabbages et al. (Brassica oleracea: Sohn et al. 2013).
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) put morphology in general in the context of comparative developmental genetics. The reaction wood is made up of thick-walled fibres (Schweingruber 2006); c.f. Resedaceae-Resedeae. The border cells of the root cap dissociate in rows (Driouich et al. 2006); other Brassicales should be examined for this character. Nikolov et al. (2019) examined gene expression in the context of leaf morphology, simple vs complex. There are rarely more or less glandular "stipules" in the inflorescence and elsewhere (see Weberling 2006 for a summary, also Bowman 2006; Bosch et al. 2008). Ca 29 genera include species in which the inflorescence axis does not develop, so-called "rosette flowering"; here long-pedicellate flowers spring directly from the rosette, whether or not they are subtended by foliaceous bracts (Bosch et al. 2008).
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 has been a long-standing controversy about the evolutionary origin of the six stamens in Brassicaceae: Did they arise by dédoublement or by reduction (Endress 1992 and Ronse Decraene & Smets 1993b for literature)? Stamen number in Brassicaceae certainly sometimes increases, thus Megacarpaea polyandra can have 24 stamens. In Succowia the outer secondary parietal cells produces the endothecium and middle layer, the inner producing the tapetum only (Hakki 1974). Maybe a quarter of the family have omniaperturate pollen grains, that is, whatever the morphology of the grains, the pollen tubes can break through the pollen wall anywhere. However, in 8/9 apparently omniaperturate species examined, there was also normal pollen tube germination, and only in Matthiola incana was there 100% germination through the walls (Edlund et al. 2016). Another controversy concerns carpel number ansd morphology (e.g. Carlquist 1970 for references). 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 decidedly uncommon in Brassicales.
The ovule of Succowiahas a zig-zag micropyle (like Capsella) and something quite like a postament, endothelial cells may have up to 32 nuclei, and the suspensor is uniseriate and quite large (Hakki 1974). 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 Al-Shehbaz (1984), Appel and Al-Shehbaz (2002), Koch et al. (2003), Hurka et al. (2005) and Mitchell-Olds et al. (2005) for general information, Moazzeni et al. (2018: Aethonema), also Koch et al. 2012) for BrassiBase, a very useful resource - check out "Morphology Tool", for instance. See also Schweingruber (2006) for phloem and xylem anatomy, Erbar and Leins (1997a, b) and Leins and Erbar (2010) for floral development, Bernadello (2007) for nectary variation, Khalik et al. (2002) for pollen morphology, Pammel (1897), Vaughan and Whitehouse (1971: much information), Prasad (1975), Bouman (1975), and Khoul et al. (2002) for ovules and seed coat, 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), Mummenhoff et al. (2009) for fruit development, Prasad (1977) for testa, and for chromosome numbers, see Warwick and Al-Shehbaz (2006: summary) and Spaniel et al (2015: Alysseae).
Phylogeny. Over the last ten years or more, progress has been made in providing a phylogenetic framework for the family (e.g. Koch et al. 2001: Koch 2003; Beilstein et al. 2006; Warwick et al. 2010; Z.-D. Chen et al. 2016) and realigning taxa accordingly. Aethionema, a variable genus with angustiseptate fruits, is sister to the rest of the family (e.g. Zunk et al. 1996, 1999; Koch et al. 2001; Beilstein et al. 2006, 2010; Kagale et al 2014). 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; Warwick et al. 2010; Zhao et al. 2010; M. Sun et al. 2016). Three larger clades, Lineages I, II, and III, have been recognised (Beilstein et al. 2007: relationships between these clades uncertain; Franzke et al. 2009). Relationships may be [paraphyly [[Lineage I + Lineage III][ paraphyly + Lineage II]] (Beilstein et al. 2010). Kagale et al. (2014: transcriptome pyrosequencing) recovered the relationships [Lineage III [Lineage I + Lineage II]], but sampling was poor, in Beilstein et al. (2007). However, the monophyly of Lineage II in particular is uncertain, and several well-known genera like Alliaria and Thlaspi are outside the three main clades (Beilstein et al. 2007, 2010; Franzke et al. 2009).
C.-H. Huang et al. (2015) recovered five main clades in a tree based on the analysis of nuclear genes of 29/51 tribes then recognized; although neither clade C nor its sister-group relationship with clade B were particularly well supported, support for other relationships was generally strong. Clade E includes Lineage III taxa, clade D two Lineage II taxa, clade C, Lineage II and III and unassigned taxa, clade B nearly all Lineage II (plus one unasigned) taxa, and clade A nearly all Lineage I (plus one Lineage II) taxa (C.-H. Huang et al. (2015). In a more recent phylogenomic analysis including members of 50/52 tribes of the family, Nikolov et al. (2019) recovered the three lineages just mentioned and they delimited two more, fifteen genera remaining unplaced; there was a fair bit of support for the toplogy of their tree, although less along the spine of the tree in the [Lineage II + Lineage V] area and at the bases of those two lineages themselves.
Relationships elsewhere in the family remain to be established (e.g. Koch et al. 2012; Moazzeni et al. 2014). For the limits of Aethionema, see Khosravi et al. (2008). For relationships in the genus, see Mohammadin et al. (2017); [A. spinosum + A. lepidoides], spiny plants, are sister to the rest of the genus. Relationships along the spine of Lineage I are quite well supported (Salariato et al. 2014; see also Mohammadin et al. 2017), 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 Microlepidieae, somewhat expanded (Heenan et al. 2012), on Physarieae (Fuentes-Soriano & Al-Shehbaz 2013: also morphological diversification), and Erysimeae (Moazzeni et al. 2014). For relationships in Lepidieae, see Zunk et al. (2011) and for those within Lepidium itself, see Mummenhoff et al. (2001, 2004). Although Arabidopsis thaliana (Camelineae) is perhaps the most important model vascular plant in biology, the limits of Arabidopsis itself are only now being established (see Clauss & Koch 2006 for a discussion of its immediate relatives). For relationships in Cardamineae, see Olsen et al. (2016), and although these are largely unresolved along the spine of the tree, the South African Aplanodes is sister to the rest, while Cardamine itself is likely to be most horribly para- or polyphyletic (see also Carlsen et al. 2009). For work on 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 most tribes there has good support (see also Mohammadin et al. 2017). Brassiceae: Warwick and Sauder (2005) found that to make this tribe monophyletic 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). Arabideae: For relationships in this tribe, see Karl and Koch (2013), for the circumscription of Arabis itself, 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). Thlaspideae. Relationships in the tribe, which has around 42 species, are discussed by Esmailbegi et al. (2018); the sometimes invasive Alliaria petiolata, with very different fruit morphology, is to be included here. Mummenhoff et al. (1997), Koch and Mummenhoff (2001) and Meyer (2003) discuss generic limits surrounding Thlaspi, a polyphyletic genus. Sisymbrieae: Sisymbrium s. str. 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 gynoecial etc. 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), in Cochlearieae, Koch (2012), and in Chorisporeae-Dontostemoneae, see German et al. (2011). For work on Matthiola (Anchonieae), see Jaén-Molina et al. (2009). For Stenodraba, whose previous assignment was morphology-based, see Salariato et al. (2018) - wrongly assigned, and of course polyphyletic
Biscutelleae and some other tribes are unplaced. Alysseae are also outside the three main clades, and for a study of Alysseae and related tribes, see Warwick et al. (2008) and Spaniel et al. (2016). 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; see also Spaniel et al. (2015). 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). Ali et al. (2016) provide a phylogeny for Coluteocarpeae.
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 52 (as of 7.xii.2017), only 20 genera with 34 species remaining unassigned (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 to named tribes are put in new tribes, not accommodated in old tribes; the new tribal classification was begun when relationships were imperfectly known, if for the best of motives (Al-Shehbaz et al. 2006).
At the generic level the story is rather similar, as the tale of the recent nomenclatural wanderings of German Brassicaceae told by Koch (in Kadereit et al. 2016) makes clear. There has been parallel or convergent evolution of just about all the morphological features used to distinguish genera (e.g. Koch 2003; Al-Shehbaz et al. 2006; Bailey et al. 2006a, b; Beilstein et al. 2008; Franzke et al. 2011), 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), and for generic limits in Coluteocarpeae, c.f. Al-Shehbaz (2014: followed here) and Ali et al. (2016). For the genera of Alysseae, see Spaniel et al. (2016). 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.
Thanks. To I. Al-Shehbaz, for interesting discussions.