EMBRYOPSIDA Pirani & Prado
Gametophyte dominant, independent, multicellular, thalloid, with single-celled apical meristem, showing gravitropism; rhizoids +, unicellular; acquisition of phenylalanine lysase [PAL], flavonoids [absorbtion of UV radiation], phenylpropanoid metabolism [lignans], xyloglucans +; plant poikilohydrous [protoplasm dessication tolerant], ectohydrous; cuticle +; cell wall also with (1->3),(1->4)-ß-D-MLGs [Mixed-Linkage Glucans], lignin +; chloroplasts per cell, lacking pyrenoids; glycolate metabolism in leaf peroxisomes [glyoxysomes]; centrioles in vegetative cells 0, metaphase spindle anastral, predictive preprophase band of microtubules, phragmoplast + [cell wall deposition spreading from around the spindle fibres], plasmodesmata +; antheridia and archegonia jacketed, stalked; spermatogenous cells monoplastidic; blepharoplast, bicentriole pair develops de novo in spermatogenous cell, associated with basal bodies of cilia [= flagellum], multilayered structure [4 layers: L1, L4, tubules; L2, L3, short vertical lamellae] + spline [tubules from L1 encircling spermatid], basal body 200-250 nm long, associated with amorphous electron-dense material, microtubules in basal end lacking symmetry, stellate array of filaments in transition zone extended, axonemal cap 0 [microtubules disorganized at apex of cilium]; male gametes [spermatozoids] with a left-handed coil, cilia 2, lateral; oogamy; sporophyte dependent on gametophyte, embryo initially surrounded by haploid gametophytic tissue, plane of first division horizontal [with respect to long axis of archegonium/embryo sac], suspensor/foot +, cell walls with nacreous thickenings; sporophyte multicellular, with at least transient apical cell [?level], sporangium +, single, dehiscence longitudinal; meiosis sporic, monoplastidic, microtubule organizing centre associated with plastid, cytokinesis simultaneous, preceding nuclear division, sporocytes 4-lobed, with a quadripolar microtubule system; spores in tetrads, sporopollenin in the spore wall, wall with several trilamellar layers [white-line centred layers, i.e. walls multilamellate]; nuclear genome size <1.4 pg, LEAFY gene present, ethylene involved in cell elongation; chloroplast genome with close association between trnLUAA and trnFGAA genes.
Many of the bolded characters in the characterization above are apomorphies of subsets of streptophytes along the lineage leading to the embryophytes, not apomorphies of crown-group embryophytes per se.
All groups below are crown groups, nearly all are extant. Characters mentioned are those of the immediate common ancestor of the group,  contains explanatory material, () features common in clade, exact status unclear.
Abscisic acid, ?D-methionine +; sporangium with seta, seta developing from basal meristem [between epibasal and hypobasal cells], sporangial columella + [developing from endothecial cells]; stomata +, anomocytic, cell lineage that produces them with symmetric divisions [perigenous]; underlying similarities in the development of conducting tissue and in rhizoids/root hairs; spores trilete; polar transport of auxins and class 1 KNOX genes expressed in the sporangium alone; shoot meristem patterning gene families expressed; MIKC, MI*K*C* and class 1 and 2 KNOX genes, post-transcriptional editing of chloroplast genes; gain of three group II mitochondrial introns.
[Anthocerophyta + Polysporangiophyta]: archegonia embedded/sunken in the gametophyte; sporophyte long-lived, chlorophyllous; sporophyte-gametophyte junction interdigitate, sporophyte cells showing rhizoid-like behaviour.
Sporophyte branched, branching apical, dichotomous; sporangia several, each opening independently; spore walls not multilamellate [?here].
EXTANT TRACHEOPHYTA / VASCULAR PLANTS
Photosynthetic red light response; plant homoiohydrous [water content of protoplasm relatively stable]; control of leaf hydration passive; (condensed or nonhydrolyzable tannins/proanthocyanidins +); sporophyte soon independent, dominant, with basipetal polar auxin transport; vascular tissue +, sieve cells + [nucleus degenerating], tracheids +, in both protoxylem and metaxylem, plant endohydrous; endodermis +; root xylem exarch [development centripetal]; stem with an apical cell; branching dichotomous; leaves spirally arranged, blades with mean venation density 1.8 mm/mm2 [to 5 mm/mm2]; sporangia adaxial on the sporophyll, derived from periclinal divisions of several epidermal cells, wall multilayered [eusporangium]; columella 0; tapetum glandular; gametophytes exosporic, green, photosynthetic; basal body 350-550 nm long, stellate array in transition region initially joining microtubule triplets; placenta with single layer of transfer cells in both sporophytic and gametophytic generations, embryonic axis not straight [root lateral with respect to the longitudinal axis; plant homorhizic].[MONILOPHYTA + LIGNOPHYTA]
Sporophyte branching ± indeterminate; lateral roots +, endogenous, root apex multicellular, root cap +; (endomycorrhizal associations + [with Glomeromycota]); tracheids with scalariform-bordered pits; leaves with apical/marginal growth, venation development basipetal, growth determinate; sporangia borne in pairs and grouped in terminal trusses, dehiscence longitudinal, a single slit; cells polyplastidic, microtubule organizing centres not associated with plastids, diffuse, perinuclear; blepharoplasts +, paired, with electron-dense material, centrioles on periphery, male gametes multiciliate; chloroplast long single copy ca 30kb inversion [from psbM to ycf2]; LITTLE ZIPPER proteins.
Sporophyte woody; lateral root origin from the pericycle; branching lateral, meristems axillary; cork cambium + [producing cork abaxially], vascular cambium bifacial [producing phloem abaxially and xylem adaxially].
EXTANT SEED PLANTS / SPERMATOPHYTA
Plant evergreen; nicotinic acid metabolised to trigonelline, (cyanogenesis via tyrosine pathway); primary cell walls rich in xyloglucans and/or glucomannans, 25-30% pectin [Type I walls]; lignins derived from (some) sinapyl and particularly coniferyl alcohols [hence with p-hydroxyphenyl and guaiacyl lignin units, so no Maüle reaction]; root stele with xylem and phloem originating on alternate radii, not medullated [no pith], cork cambium deep seated; shoot apical meristem interface specific plasmodesmatal network; stem with vascular cylinder around central pith [eustele], phloem abaxial [ectophloic], endodermis 0, xylem endarch [development centrifugal]; wood homoxylous, tracheids and rays alone, tracheid/tracheid pits circular, bordered; mature sieve tube/cell lacking functioning nucleus, sieve tube plastids with starch grains; phloem fibres +; cork cambium superficial; leaves with single trace from vascular sympodium [nodes 1:1]; stomatal pore with active opening in response to leaf hydration, control by abscisic acid, metabolic regulation of water use efficiency, etc.; buds axillary (not associated with all leaves), exogenous; prophylls two, lateral; leaves with petiole and lamina, development basipetal, blade simple; plant heterosporous, sporangia borne on sporophylls, sporophylls spiral; microsporophylls aggregated in indeterminate cones/strobili; grains monosulcate, aperture in ana- position [distal], exine and intine homogeneous; ovules unitegmic, parietal tissue 2+ cells across, megaspore tetrad linear, functional megaspore single, chalazal, lacking sporopollenin, megasporangium indehiscent; pollen grains land on ovule; gametophytes dependent on sporophyte; apical cell 0, male gametophyte development initially endosporic, tube developing from distal end of grain, gametes two, developing after pollination, with cell walls; female gametophyte endosporic, initially syncytial, walls then surrounding individual nuclei; embryo cellular ab initio, endoscopic, plane of first cleavage of zygote transverse, suspensor +, short-minute, embryonic axis straight [shoot and root at opposite ends; plant allorhizic], cotyledons 2; plastid transmission maternal; ycf2 gene in inverted repeat, whole nuclear genome duplication [zeta duplication], two copies of LEAFY gene, PHY gene duplications [three - [BP [A/N + C/O]] - copies], nrDNA with 5.8S and 5S rDNA in separate clusters; mitochondrial nad1 intron 2 and coxIIi3 intron and trans-spliced introns present.
ANGIOSPERMAE / MAGNOLIOPHYTA
Lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, apigenin and/or luteolin scattered, [cyanogenesis in ANITA grade?], S [syringyl] lignin units common [positive Maüle reaction - syringyl:guaiacyl ratio more than 2-2.5:1], and hemicelluloses as xyloglucans; root apical meristem intermediate-open; root vascular tissue oligarch [di- to pentarch], lateral roots arise opposite or immediately to the side of [when diarch] xylem poles; origin of epidermis with no clear pattern [probably from inner layer of root cap], trichoblasts [differentiated root hair-forming cells] 0, exodermis +; shoot apex with tunica-corpus construction, tunica 2-layered; reaction wood ?, associated gelatinous fibres [g-fibres] with innermost layer of secondary cell wall rich in cellulose and poor in lignin; starch grains simple; primary cell wall mostly with pectic polysaccharides, poor in mannans; tracheid:tracheid [end wall] plates with scalariform pitting, wood parenchyma +; sieve tubes enucleate, sieve plate with pores (0.1-)0.5-10< µm across, cytoplasm with P-proteins, cytoplasm not occluding pores of sieve plate, companion cell and sieve tube from same mother cell; sugar transport in phloem passive; nodes 1:?; stomata brachyparacytic [ends of subsidiary cells level with ends of pore], outer stomatal ledges producing vestibule, reduction in stomatal conductance to increasing CO2 concentration; lamina formed from the primordial leaf apex, margins toothed, development of venation acropetal, overall growth ± diffuse, venation hierarchical-reticulate, secondary veins pinnate, veins (1.7-)4.1(-5.7) mm/mm2, endings free; most/all leaves with axillary buds; flowers perfect, pedicellate, ± haplomorphic; protogynous; parts spiral [esp. the A], free, numbers unstable, development in general centripetal; P +, members each with a single trace, outer members not sharply differentiated from the others, not enclosing the floral bud; A many, filament not sharply distinguished from anther, stout, broad, with a single trace, anther introrse, tetrasporangiate, sporangia in two groups of two [dithecal], sporangium pairs dehiscing longitudinally by a common slit, ± embedded in the filament, walls with at least outer secondary parietal cells dividing, endothecium +, endothecial cells elongated at right angles to long axis of anther; (tapetum glandular), cells binucleate; microspore mother cells in a block, microsporogenesis successive, walls developing by centripetal furrowing; pollen subspherical, tectum continuous or microperforate, ektexine columellate, endexine lamellate only in the apertural regions, thin, compact; nectary 0; carpels present, superior, free, several, ascidiate, with postgenital occlusion by secretion, stylulus at most short [shorter than ovary], hollow, cavity not lined by distinct epidermal layer, stigma ± decurrent, carinal, dry [not secretory]; ovules few [?1]/carpel, marginal, anatropous, bitegmic, micropyle endostomal, outer integument 2-3 cells across, often largely subdermal in origin, inner integument 2-3 cells across, often dermal in origin, parietal tissue 1-3 cells across [crassinucellate], nucellar cap?; megasporocyte single, hypodermal, functional megaspore, chalazal, lacking cuticle; female gametophyte four-celled [one module, nucleus of egg cell sister to one of the polar nuclei]; supra-stylar extra-gynoecial compitum +; ovule not increasing in size between pollination and fertilization; pollen grains land on stigma, bicellular at dispersal, mature male gametophyte tricellular, germinating in less than 3 hours, pollen tube elongated, unbranched, growing between cells, growth rate (20-)80-20,000 µm/hour, apex of pectins, wall with callose, lumen with callose plugs, penetration of ovules via micropyle [porogamous], whole process takes ca 18 hours, distance to first ovule 1.1-2.1 mm; male gametes lacking cell walls, cilia 0, siphonogamy; double fertilization +, ovules aborting unless fertilized; P deciduous in fruit; mature seed much larger than ovule when fertilized, small , dry [no sarcotesta], exotestal; endosperm diploid, cellular, heteropolar [micropylar and chalazal domains develop differently, first division oblique, micropylar end initially with a single large cell, divisions uniseriate, chalazal cell smaller, divisions in several planes], copious, oily and/or proteinaceous; dark reversal Pfr → Pr; Arabidopsis-type telomeres [(TTTAGGG)n]; nuclear genome size <1.4 pg [1 pg = 109 base pairs], whole nuclear genome duplication [epsilon duplication]; protoplasm dessication tolerant [plant poikilohydric]; ndhB gene 21 codons enlarged at the 5' end, single copy of LEAFY and RPB2 gene, knox genes extensively duplicated [A1-A4], AP1/FUL gene, paleo AP3 and PI genes [paralogous B-class genes] +, with "DEAER" motif, SEP3/LOFSEP and three copies of the PHY gene, [PHYB [PHYA + PHYC]].
[NYMPHAEALES [AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]]: wood fibres +; axial parenchyma diffuse or diffuse-in-aggregates; pollen monosulcate [anasulcate], tectum reticulate-perforate [here?]; ?genome duplication; "DEAER" motif in AP3 and PI genes lost, gaps in these genes.
[AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]: vessel elements with scalariform perforation plates in primary xylem; essential oils in specialized cells [lamina and P ± pellucid-punctate]; tension wood +; tectum reticulate; anther wall with outer secondary parietal cell layer dividing; carpels plicate; nucellar cap + [character lost where in eudicots?]; 12BP [4 amino acids] deletion in P1 gene.
[[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]] / MESANGIOSPERMAE: benzylisoquinoline alkaloids +; sesquiterpene synthase subfamily a [TPS-a] [?level], polyacetate derived anthraquinones + [?level]; outer epidermal walls of root elongation zone with cellulose fibrils oriented transverse to root axis; P more or less whorled, 3-merous [possible position]; pollen tube growth intra-gynoecial; embryo sac bipolar, 8 nucleate, antipodal cells persisting; endosperm triploid.
[MONOCOTS [CERATOPHYLLALES + EUDICOTS]]: (extra-floral nectaries +); (veins in lamina often 7-17 mm/mm2 or more [mean for eudicots 8.0]); (stamens opposite [two whorls of] P); (pollen tube growth fast).
[CERATOPHYLLALES + EUDICOTS]: ethereal oils 0.
EUDICOTS: (Myricetin, delphinidin +), asarone 0 [unknown in some groups, + in some asterids]; root epidermis derived from root cap [?Buxaceae, etc.]; (vessel elements with simple perforation plates in primary xylem); nodes 3:3; stomata anomocytic; flowers (dimerous), cyclic; protandry common; K/outer P members with three traces, ("C" +, with a single trace); A few, (polyandry widespread, initial primordia 5, 10, or ring, ± centrifugal), filaments fairly slender, anthers basifixed; microsporogenesis simultaneous, pollen tricolpate, apertures in pairs at six points of the young tetrad [Fischer's rule], cleavage centripetal, wall with endexine; G with complete postgenital fusion, stylulus/style solid [?here]; seed coat?
[PROTEALES [TROCHODENDRALES [BUXALES + CORE EUDICOTS]]]: (axial/receptacular nectary +).
[TROCHODENDRALES [BUXALES + CORE EUDICOTS]]: benzylisoquinoline alkaloids 0; euAP3 + TM6 genes [duplication of paleoAP3 gene: B class], mitochondrial rps2 gene lost.
[BUXALES + CORE EUDICOTS]: ?
CORE EUDICOTS / GUNNERIDAE: (ellagic and gallic acids +); leaf margins serrate; compitum + [one place]; micropyle?; whole nuclear genome duplication [palaeohexaploidy, gamma triplication], PI-dB motif +, small deletion in the 18S ribosomal DNA common.
[ROSIDS ET AL. + ASTERIDS ET AL.] / PENTAPETALAE: root apical meristem closed; (cyanogenesis also via [iso]leucine, valine and phenylalanine pathways); flowers rather stereotyped: 5-merous, parts whorled; P = calyx + corolla, the calyx enclosing the flower in bud, sepals with three or more traces, petals with a single trace; stamens = 2x K/C, in two whorls, internal/adaxial to the corolla whorl, alternating, (numerous, but then usually fasciculate and/or centrifugal); pollen tricolporate; G , G  also common, when [G 2], carpels superposed, compitum +, placentation axile, style +, stigma not decurrent; endosperm nuclear; fruit dry, dehiscent, loculicidal [when a capsule]; RNase-based gametophytic incompatibility system present; floral nectaries with CRABSCLAW expression; (monosymmetric flowers with adaxial/dorsal CYC expression).
[DILLENIALES [SAXIFRAGALES [VITALES + ROSIDS s. str.]]]: stipules + [usually apparently inserted on the stem].
[SAXIFRAGALES [VITALES + ROSIDS]] / ROSANAE Takhtajan / SUPERROSIDAE: ??
[VITALES + ROSIDS] / ROSIDAE: anthers articulated [± dorsifixed, transition to filament narrow, connective thin].
ROSIDS Back to Main Tree
(Mucilage cells with thickened inner periclinal walls and distinct cytoplasm); embryo long; genome duplication; chloroplast infA gene defunct, mitochondrial coxII.i3 intron 0.
Age. The age of this node was estimated at (113-)109, 104(-100) m.y. by Wikström et al. (2001). Hengcheng Wang et al. (2009) suggested an age of (114-)108, 91(-85) m.y.a.; Bayesian relaxed clock estimates were (116-)114, 113(-110) m.y. ago. Magallón and Castillo (2009) suggested ages of ca 107.9 and 108.4 m.y.. Moore et al. (2010: 95% HPD) estimated an age of (110-)106(-103) m.y., and Bell et al. (2010) ages of (121-)116, 114(-108) m.y., Clarke et al. (2011: Populus + Arabidopsis) an age of (115-)94((-83) m.y.. In a study using a small sample of nuclear genomes, Argout et al. (2010) gave an age of ca 90 m.y. while the estimate in N. Zhang et al. (2012) is (103-)99(-94) m.y. and in Xue et al. (2012) 90.4-89.1 m.y.a.; ages in Schneider et al. (2004) range from about 110-167 m.y., while ages of around 106.4 and 95.5 m.y.a. are provided by Naumann et al. (2013) and ca 96 m.y.a. is the age suggested by Sytsma et al. (2014); the oldest, at at around 150 m.y., is that of Z. Wu et al. (2014).
Poinar et al. (2007, 2008) found a possible rosid fossil from Myanmar/Burma with a floral formula of K 5, C ?, A 10, G , styles diverging. It was thought that the rocks in which it was found were 110-100 m.y. old from the Early Cretaceous, but recent estimates are somewhat younger, being Early Cenomanian and (99.4-)98.8(-98.2) m.y.o. (Shi et al. 2012).
Evolution. Divergence & Distribution. Sharkey et al. (2013) suggested that there was a single origin of isoprene emission around here, but this was followed by multiple losses; they link the origin to the high atmospheric CO2 concentrations in the later Cretaceous.
Plant-Animal Interactions. Redfern (2011) notes that Cynipinae gall wasps are common on rosids, particularly on Rosaceae and Fagaceae.
Bacterial/Fungal Associations. Brundrett (2002) suggested that ectomycorrhize were most common is rosids, rare elsewhere (e.g. Nyctaginaceae), although modified forms dominate in Ericales and Orchidales.
Chemistry, Morphology, etc. For the distribution of mucilage cells with thickened inner periclinal walls and distinct cytoplasm ("special mucilage cells"), see Matthews and Endress (2006b), for floral development, see Schönenberger and von Balthazar (2006), and for the distribution of a number of floral features, see Endress and Matthews (2006a).
Phylogeny. See the Dilleniales and Saxifragales pages for further discussion on the major patterns of relationships within Pentapetalae.
D. Soltis et al. (2003a) found 79% support for rosids s.s., i.e., lacking Vitales and Saxifragales. Within rosids s. str., relationships have been somewhat unclear (e.g. Soltis et al. 2005b; Jansen et al. 2006a; Bausher at al. 2006; Zhu et al. 2007; versions of this site up to March 2009), but the topology is being clarified (e.g. Hengcheng Wang et al. 2009). The relationships of the rosid I clade (= [fabids/N-fixing clade + [Celastrales [Oxalidales + Malpighiales]]], the latter is the COM clade) have been particularly problematical. In an analysis including the mitochondrial matR and two chloroplast genes, the COM clade were sister to the fabids/N-fixing clade, with weak to moderate support; Crossosomatales were weakly supported as sister to the rosid II clade (= malvids) (Zhu et al. 2007). Jansen et al. (2007) recovered a malvid clade with strong support (weaker using maximum parsimony), in turn strongly supported as sister to the rosid I clade, albeit with sketchy sampling. Ruhfel et al. (2014) recovered a variety of relationships around here, including a [COM + N-fixing] clade, and Z. Wu et al. (2014: chloroplast genomes) also recovered a [COM + N-fixing] clade, and with Zygophyllaceae sister to the former.
However, in some analyses of four mitochondrial genes, Qiu et al. (2010) found that the rosid I clade was not monophyletic, there being quite strong support for a [COM + malvids] clade (see also Duarte et al. 2010; Burleigh et al. 2011). Similarly, in an analysis of 154 protein-coding genes Shulaev et al. (2011) found that Populus was sister to [Carica + Arabidopsis], rather than to four taxa from the nitrogen-fixing clade, so again the rosid I clade was not monophyletic, and the same basic relationships were found by E. K. Lee et al. (2011: better sampling, but no Celstrales or Oxalidales). Burleigh et al. (2011) in a genome-level analysis found that Malpighiales were embedded in the malvids, although no representatives of Celastrales or Oxalidales were examined (see also Duarte et al. 2010); similar relationships were rejected by all tests in the combined analysis of Zhu et al. (2007), although they were found in the analysis of matR data alone.
Soltis et al. (2011) discussed the influence of mitochondrial genes on relationships in this part of the tree; mitochondrial genes alone placed a weakly supported COM clade as sister to core malvids with quite strong support. In analyses of large amounts of chloroplast data Malpighiales grouped with the N-fixing clade, while in analyses of nuclear data they grouped with the malvids (Xi et al. 2014). A [COM + malvid] clade was also obtained (just) in an analysis of 31 (30 eudicot) complete chloroplast genomes (Fajardo et al. 2013).
Thus the COM clade in general, or Malpighiales in particular, do not have stable relationships. In an important study by Sun et al. (2014) the sampling of taxa with genome data from different compartments was matched as carefully as possible. They found that a [COM + fabid/N-fixing] clade was obtained in analyses of chloroplast data, while a [COM + malvid] clade was recovered in analyses of mitochondrial and nuclear data. (The mitochondrial tree showed a number of idiosyncracies, e.g. Lonicera was sister to other campanulid taxa included, Crossosomatales and Zygophyllales formed a clade outside the [fabid [COM + malvid]] clade, Garryaceae and Aquifoliaceae switched positions, Platanus was sister to Ranunculales, etc., although overall support values were very low [Sun et al. 2014]). They suggested that the COM clade might be the result of a very ancient hybridization between a fabid and malvid, with the chloroplast genes coming from the former and much of the rest of the genome from the latter, an idea supported by the much larger number of nuclear genes that grouped with the malvids rather than the fabids (Sun et al. 2014). Slightly disconcerting was the inclusion of Caryophyllales within rosids s.l., although clades like Picramniales and in particular Dilleniaceae that were not represented in the study may affect some placements.
Endress and Matthews (2006a; also Endress et al. 2013) suggested that some morphological characters are consistent with such relationships; these include the frequency of features such as a contorted corolla and polystaminate androecium and polycarpy, while the inner integument also tends to be thicker than the outer integument in the [COM + malvid] clade.
Using mitochondrial and chloroplast genes, Zhu et al. (2007) found that Myrtales and Geraniales were successively sister to all other rosids - but with little support (Zhu et al. 2007). S.-B. Lee et al. (2006) found some support for the clade [Geraniales + Myrtales] sister to the rosid I clade, although sampling was poor. Jansen et al. (2007; see also Z. Wu et al. 2014) recovered this [Myrtales + Geraniales] clade as sister to the malvids, albeit with weak support. Xi et al. (2014) found that Eucalyptus was weakly supported as sister to all rosids in analyses using nuclear data, while in those using chloroplast data, the genus was sister to the malvids, and with strong support, however, representatives of Geraniales were not included and sampling in general was a bit sketchy (this was not the main focus of their work). There is a fair amount of variation in relationships in this area in the trees provided by Sun et al. (2014).
ROSID I / FABIDAE / [ZYGOPHYLLALES [the COM clade + the nitrogen-fixing clade]]: endosperm scanty. Back to Main Tree
Age. Argout et al. (2010) suggested a date for this clade of a mere ca 77 m.y., but this is surely an underestimate. Other ages for this node are (104-)101, 95(-92) m.y. (Wikström et al. 2001), (114-)108(-102) and (97-)91(-85) m.y. (Hengcheng Wang et al. 2009), while ages of (114-)107, 103(-99) m.y. were suggested by Bell et al. (2010) and around 100.4 m.y. by Naumann et al. (2013).
Evolution. Divergence & Distribution. Hengcheng Wang et al. (2008: penalized likelihood dates) suggested that rapid radiation within Fabidae occurred (114-)108-91(-85) m.y.a., perhaps a little before that in Malvidae.
Chemistry, Morphology, etc. Extrafloral nectaries in this clade - perhaps particularly frequent in Malpighiales - commonly are made up of palisade epidermal cells (Zimmermann 1932).
Phylogeny. The position of Zygophyllales was rather labile in the comprehensive analysis of Hengcheng Wang et al. (2009). It sometimes appeared to be linked with the malvids/rosid II (maximum parsimony), or sometimes with the fabids/rosid I (maximum likelihood), but the former position could be rejected (Wang et al. 2009). Bell et al. (2010) placed Zygophyllales in a polytomy with the COM and N-fixing clades (see also Magallón & Castillo 2009), while several recent analyses, including that by Hengcheng Wang et al. (2009) and the 17-gene analysis of Soltis et al. (2011) are placing it sister to all other Fabidae (as here), although Qiu et al. (2010: mitochondrial genes) recently suggested that Zygophyllales were embedded in Crossosomatales, but with only moderate support, the combined clade being sister to all rosids. Analyses by Ruhfel et al. (2014) also found a rather peripatetic Zygophyllales.
ZYGOPHYLLALES Link Main Tree.
Harman alkaloids, diversity of linans and neolignans +; mycorrhizae 0; cork cambium deep cortical or pericyclic (superficial); vessel elements with simple perforation plates; rays (predominantly) uniseriate; tension wood?; (stomatal orientation transverse); (pollen colpate); style +; micropyle endostomal; seeds ± exotestal; endosperm 0; chloroplast infA gene +. - 2 families, 27 genera, 305 species.
Age. Ages for crown group Zygophyllales are (88-)79(-70) or (64-)55(-46) m.y. (two penalized likelihood dates), but some Bayesian relaxed clock ages were up to 102 m.y. (Hengcheng Wang et al. 2009). Wikström et al. (2001) suggested an age for the separation of the two families of some (74-)70, 64(-60) m.y.a., and this age was estimated at (88-)70, 65(-45) m.y. by Bell et al. (2010) and (93.4-)61.9(-29.3) m.y. by Naumann et al. (2013).
Note: Possible apomorphies are in bold. However, the actual level at which many of these features, particularly the more cryptic ones, should be assigned is unclear. This is partly because many characters show considerable homoplasy, in addition, basic information for all too many is very incomplete, frequently coming from taxa well embedded in the clade of interest and so making the position of any putative apomorphy uncertain. Then there is the not-so-trivial issue of how ancestral states are reconstructed (see above).
Evolution. Bacterial/Fungal Associations. Mycorrhizae are usually absent from this clade, perhaps not unexpected, given their preference for arid/saline habitats. However, arbuscular mycorrhizae have been reported from roots of Larrea tridentat in the Mojave Desert (Apple et al. 2005); c.f. also Amaranthaceae.
Chemistry, Morphology, etc. For harman alkaloids, see Kubitzki (2006a); for lignans and neolignans, see Simpson (2006) and Sheahan (2006). Carlquist (2005b) lists several features of wood anatomy that may be synapomorphies for the group.
Phylogeny Zygophyllaceae have often been found to be sister to Krameriaceae, as in Soltis et al. (1998) and Savolainen et al. (2000a). However, relationships of Zygophyllales have been unclear. In analyses of Hilu et al. (2003), Larrea (Zygophyllaceae) were weakly associated with Fabaceae, the only member of Fabales included in their rbcL study; they noted that the possession of anthroquinones was a possible synapomorphy between Zygophyllaceae and the N-fixing clade (see also Sheahan & Chase 2000). However, a position of Zygophyllales as sister to the rest of the whole rosid I/fabid clade was recovered, and with reasonable support, by Wang et al. (2009).
Classification. The inclusion of Krameriaceae in Zygophyllaceae was initially optional, although the two do not have much in common; see A.P.G. II (2003); the narrower circumscription of the families was adopted by A.P.G. III (2009).
Includes Krameriaceae, Zygophyllaceae.
Synonymy: Balanitales C. Y. Wu, Krameriales Martius - Zygophyllanae Doweld
KRAMERIACEAE Dumortier, nom. cons. Back to Zygophyllales
Hemiparasitic, shrubs to herbs; wood fluorescence?; nodes 1:1; petiole bundle (deeply) arcuate; hairs unicellular, thin-walled; stomata usu. paracytic; cuticle waxes ± ribbon-like platelets; leaves spiral, (trifoliolate), lamina margins entire, stipules 0; inflorescence racemose, or flowers solitary, pedicels articulated; flower monosymmetric, K (4) 5, petal-like internally, median member abaxial, larger than the others, C with (2) 3 adaxial C clawed, ± connate, 2 abaxial smaller, not clawed, elaiophores on abaxial petals; A 4, (3), (adnate to adaxial C), anthers dehiscing by pores, endothecial cells with thickening parallel to long axis of cells, filaments often stout; nectary 0; G , adaxial member much reduced, style long, stigma small, recessed; ovules 2/carpel, apical, collateral, outer integument 3-6 cells and inner integument 3-5 cells across, suprachalazal zone massive; fruit nut, with retrorsely barbed spines; seed 1, testa and tegmen ?weakly multiplicative, exotestal cells enlarged, tanniniferous, tegmen to 7 cells thick, largely disappearing; endosperm 0, cotyledons large, cordate/auriculate; n = 6, chromosomes 10-24.6 µm long; seedlings without root hairs.
1[list]/18. S.W. U.S.A. to Chile, the West Indies (map: from Simpson et al. 2004). [Photo - Flower © Jim Manhart, Fruit © Dan Nickrent.]
Age. The age of crown group Krameria has been estimated at (34-)12(-5) m.y. (Renner & Schaefer 2010).
Evolution. Pollination Biology. Bees (Centris) collect oil from the rather papilionoid-looking flowers on their legs from the paired, modified, abaxial petals; the latter have epithelial elaiophores (Vogel 1974; Simpson et al. 1977).
Genes & Genomes. The rate of genome evolution here is rather slower than that of other parasitic taxa (Bormham et al. 2013).
Chemistry, Morphology, etc. The roots have a red phlobaphene pigment. There are no vessels in the leaves.
Simpson (1982, 2006) discussed the long controversy over the orientation of the flower, however, the flowers do appear to be inverted (see also Milby 1971, see Fig. 73 in Simpson 2006). The traces to the sepals, petals and stamens in the flower are all separate; the abaxial petals (elaiophores) are densely vascularized (Milby 1971).
For further details, see Leinfellner (1971: ovary), Verkeke (1985: ovule and seed), Simpson (1989) and Carlquist (2005b: wood anatomy); Leinfellner (1971) and especially Bello et al. (2012) for floral morphology, and Simpson (2006), The Parasitic Plant Collection, and Heide-Jørgensen (2008) give much general information.
Phylogeny. Simpson et al. (2004) provide a phylogeny of the family.
Previous Relationships. Krameriaceae have often been considered to be close to Polygalaceae (Fabales), as by Cronquist (1981).
ZYGOPHYLLACEAE R. Brown, nom. cons. Back to Zygophyllales
Trees to herbs (thorny); mycorrhizae absent; (C4 photosynthesis), anthroquinones +, guaiacs +, ellagic acid 0, tannins 0 [Zygophyllum]; wood often fluorescing; storying +; pits vestured; nodes often swollen or jointed, 1:1 + split laterals; cortical strands of fibres and sclereids +; petiole bundle annular, with wing bundles; stomata anomocytic; leaves opposite (spiral), (odd-) even-pinnate (2, 3-foliolate), lamina vernation flat or, (secondary veins ± palmate), margins toothed, stipules (spinescent) cauline, or 1, interpetiolar (0); A obdiplostemonous, or equal and opposite to the petals; pollen variable; nectary as basal scales adaxial to A, or annular; G [(2-)5], opposite petals, style short to long, stigma punctate, or as commissural ridges down style, dry or wet; ovules 1-10/carpel, outer integument 2-6 cells across, inner integument 2-4 cells across, endothelium +, (weak nucellar cap +), parietal tissue 1-2(-4) cells across, hypostase +, obturator +; (megaspore mother cells several), embryo sac long; fruit a loculicidal or septicidal capsule, (dry, indehiscent; schizocarp; drupe; berry); (seed arillate), exotesta often palisade (not thickened - Seetzenia), endotesta crystalliferous, U-lignified or not, endotegmic cells periclinally elongated, lignified; (endosperm +), embryo green.
22[list]/285 - 5 groups below. Dry and warm temperate, also tropical (map: from Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; Beier et al. 2004; Brummitt 2007.)[Photo - Flower, Fruit.]
[Morkillioideae + Tribuloideae]: ?
1. Morkillioideae Rose & J. H. Painter
3/4. Mexico, Baja California.
2. Tribuloideae D. H. Porter
(Pollen polyporate); (outer integument 4-8 cells across, inner integument 3-6 cells across - Balanites).
6/63: Tribulus (25), Kallstroemia (17). World-wide.
Synonymy: Agialidaceae Wettstein, nom. illeg., Balanitaceae M. Roemer nom. cons., Tribulaceae Trautvetter
[Seetzenioideae [Larreoideae + Zygophylloideae]]: ?
3. Seetzenioideae Sheahan & Chase
Prostrate herbs; C 0; A 5, opposite?; styles 5; ovule 1/carpel, epitropous, micropyle bostomal; outer integument 6-7 cells across, endothelium 0; fruit septicidal, with pyrenes; endosperm +.
1/1: Seetzenia lanata. S. Africa, and N. Africa to Afghanistan.
[Larreoideae + Zygophylloideae]]: ?
4. Larreoideae Sheahan & Chase
(Sieve tube plastids with protein and starch - Larrea); stamens often with scales, ovary stipitate or not; fruit capsular, winged or not, 1 seed/loculus; endosperm +.
7/30: Bulnesia (8). S.W. U.S.A. and Mexico to South America.
5. Zygophylloideae Arnott
(Outer integument ca 2 cells across, inner integument ca 2 cells across - Zygophyllum).
4/137: Zygophyllum (100). Mostly drier areas of the Old World, also S.W. U. S. A. and Chile.
Evolution. Ecology & Physiology. Members of Zygophyllaceae are notable components of halophytic vegetation in the Irano-Turanian area and in seasonally dry tropical forests, especially in Central America (Pennington et al. 2009). Larrea tridentata, the creosote bush, is an important shrub of the deserts of S.W. North America; its is very drought tolerant indeed, being the only shrub in those deserts.
For C4 photosynthesis, see Muhaidat et al. (2007); Christin et al. (2011b) suggest dates for when this pathway may have been acquired.
Plant-Animal Interactions. Caterpillars of Lycaeninae are quite commonly found on plants of this family (Fielder 1995). Fourteen species of a clade of the cecidomyiid gall former, Asphondylia, the creosote gall midge, have diversified on different parts of the plant of the one species of Larrea.
Pollination and Seed Dispersal. In studies of the pollination of creosote bush, Larrea tridentata, widespread in drier regions in the American southwest, 22 species of medium-sized to small oligolectic bees were found to use Larrea for pollen and nectar, while another 22 species of polylectic bees also regularly visited the plant (Hurd & Linsley 1975).
A number of species, including those of Zygophyllum, have myrmecochorous seeds (Lengyel et al. 2010).
Genes & Genomes. In at least some species of Larrea chloroplasts are inherited paternally (Yang et al. 2000).
Economic Importance. Guaiacum has very hard, self-lubricating wood that was used in the past to make bearings.
Chemistry, Morphology, etc. For guaiacs, perhaps similar to guaiacol/methoxy phenol/C6H4(OH)(OCH3), see Lambert et al. (2013).
Howard (1970) found no stipules in Balanites, but there are structures in the stipular position there, if minute. A number of taxa with opposite leaves have split lateral nodes (e.g. Howard 1970), and this may even been the plesiomorphic condition for the family, however, Viscainoa has simple, spiral leaves with trilacunar nodes - and two epitropous ovules/carpel. There is considerable variation in ovule type in the family. The style of Zygophyllum is more or less gynobasic.
For ovule morphology, see Mauritzon (1934b, d), Masand (1963) and Narayana and Rao (1963), for floral orientation, see Eckert (1966), for chemistry, see Hegnauer (1973, 1990), for foliar anatomy, see Sheahan and Cutler (1993), for a general account of the family, see Sheahan (2006), and for character evolution, etc., in the southern African representatives, see Bellstedt et al. (2008).
Phylogeny. Phylogenetic relationships within the family are fairly well resolved; Sheahan and Chase (1996, also 2000), and can be summarized as [Morkillioideae + Tribuloideae] [Seetzenioideae [Larreoideae + Zygophylloideae]], however, there do not seem to be good characters distinguishing the groups. The distinctive Balanites is to be included in Tribuloideae for the time being, at least (Sheahan & Chase 1996, 2000).
For relationships between Larrea and its relatives, see Lia et al. (2001). For relationships and morphology within Zygophylloideae, see Beier et al. (2003). For relationships of the southern African Zygophyllaceae, see Bellstedt et al. (2008).
Classification. The subfamilial classification above follows that of Sheahan and Chase (2000), although there is not much in the way of characters distinguishing the clades recognized. Beier et al. (2003) provide a reclassification of Zygophylloideae; Sands (2001) monographed the distinctive Balanites.
Previous Relationships. Some genera that used to be included in Zygophyllaceae are now in Nitrariaceae (Sapindales, rosid II).