EMBRYOPSIDA Pirani & Prado (crown group)
Gametophyte dominant, independent, multicellular, thalloid, with single-celled apical meristem, showing gravitropism; cuticle +; cell walls with (1->4)-ß-D-glucans [xyloglucans], lignin +; rhizoids unicellular; several chloroplasts per cell; glycolate metabolism in leaf peroxisomes [glyoxysomes]; centrioles in vegetative cells 0, metaphase spindle anastral, predictive preprophase band of microtubules, phragmoplast + [cell wall deposition spreading from around the spindle fibres], plasmodesmata +; antheridia and archegonia jacketed, stalked; spermatogenous cells monoplastidic, centrioles develop de novo, associated with basal bodies of flagellae, multilayered structure +, proximal end of basal bodies lacking symmetry, stellate pattern associated with doublet tubules of transition zone; spermatozoids with a left-handed coil; male gametes with 2 lateral flagellae; oogamy; diploid embryo initially surrounded by haploid gametophytic tissue, plane of first division horizontal, suspensor/foot +, cell walls with nacreous thickenings; sporophyte multicellular, sporangium +, single, with polar transport of auxin, 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 multilaminate]; spores trilete [?level]; close association between the trnLUAA and trnFGAA genes on the chloroplast genome.
Note that many of the bolded characters in the characterization above are apomorphies in the streptophyte clade along the lineage leading to the embryophytes rather than being apomorphies of the embryophytes.
Abscisic acid, ?D-methionine +; sporangium with columella; stomata +, anomocytic, cell lineage that produces them with symmetric divisions [perigenous]; polar transport of auxins and class 1 KNOX genes expressed in the sporangium alone; MIKC, MI*K*C* and class 1 and 2 KNOX genes, post-transcriptional editing of chloroplast genes; gain of three group II mitochondrial introns.
[Hornworts + Polysporangiophyta]: archegonia embedded in the gametophyte; sporophyte long-lived, chlorophyllous, nutritionally largely independent of the gametophyte; sporophyte-gametophyte junction interdigitate, sporophyte cells showing rhizoid-like behaviour; spores trilete.
Sporophyte well developed, branched, free living, sporangia several; apical meristem +.
EXTANT TRACHEOPHYTA / VASCULAR PLANTS
Photosynthetic red light response, passive control of leaf hydration; (condensed or nonhydrolyzable tannins/proanthocyanidins +); vascular tissue +, sieve cells + [nucleus degenerating], tracheids +, in both protoxylem and metaxylem; endodermis +; root xylem exarch [development centripetal]; stem with an apical cell; leaves spiral, blades with mean venation density 1.8 mm/mm2 [to 5 mm/mm2]; sporangia adaxial on the sporophyll, lacking columella, eusporangiate [sporangia derived from periclinal divisions of several epidermal cells, wall multilayered]; stellate pattern split between doublet and triplet regions of transition zone; placenta with single layer of transfer cells in both sporophytic and gametophytic generations, embryo with roots arising lateral to the main axis [plant homorhizic].[MONILOPHYTA + LIGNOPHYTA]
Branching ± monopodial; lateral roots +, endogenous, root apex multicellular, root cap +; tracheids with scalariform-bordered pits; leaves spirally arranged, with apical/marginal growth, venation development basipetal, growth determinate; sporangia borne in pairs and grouped in terminal trusses, dehiscence longitudinal, a single slit; cells polyplastidic, microtubule organizing centres not associated with plastids, diffuse, perinuclear; male gametes multiflagellate, basal bodies staggered, blepharoplasts paired; chloroplast long single copy ca 30kb inversion [from psbM to ycf2].
Plant woody; lateral root origin from the pericycle; shoot apical meristem multicellular; 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 with xylem and phloem originating on alternate radii, vascular tissue not medullated, cork cambium deep seated; arbuscular mycorrhizae +; shoot apical meristem interface specific plasmodesmatal network; stem with vascular cylinder around central pith [eustele], phloem abaxial [ectophloic], endodermis 0, xylem endarch [development centrifugal]; wood homoxylous, tracheids and rays alone, tracheid/tracheid pits circular, bordered; mature sieve tube/cell lacking functioning nucleus, sieve tube plastids with starch grains; phloem fibres +; stem cork cambium superficial; branches exogenous; leaves with single trace from vascular sympodium [nodes 1:1]; stomatal pore with active opening in response to leaf hydration, control by abscisic acid, metabolic regulation of water use efficiency, etc.; leaves with petiole and lamina, development basipetal, blade simple; axillary buds +, not associated with all leaves; prophylls two, lateral; plant heterosporous, sporangia borne on sporophylls; microsporophylls aggregated in indeterminate cones/strobili; true pollen +, grains mono[ana]sulcate, exine and intine homogeneous; ovules unitegmic, parietal tissue 2+ cells across, megaspore tetrad linear, functional megaspore single, chalazal, lacking sporopollenin, megasporangium indehiscent; pollen grains landing on ovule; male gametophyte development first endo- then exosporic, tube developing from distal end of grain, gametes two, developing after pollination, with cell walls; female gametophyte endosporic, initially syncytial, walls then surrounding individual nuclei; seeds "large" [ca 8 mm3], but not much bigger than ovule, with morphological dormancy; embryo cellular ab initio, endoscopic, plane of first cleavage of zygote transverse, suspensor +, short-minute, embryo axis straight, so shoot and root at opposite ends [plant allorhizic], white, cotyledons 2; plastid transmission maternal; ycf2 gene in inverted repeat, whole nuclear genome duplication [zeta duplication], two copies of LEAFY gene, PHY gene duplications [three - [BP [A/N + C/O]] - copies], nrDNA with 5.8S and 5S rDNA in separate clusters; mitochondrial nad1 intron 2 and coxIIi3 intron and trans-spliced introns present.
Lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, apigenin and/or luteolin scattered, [cyanogenesis in ANITA grade?], S [syringyl] lignin units common [positive Maüle reaction - syringyl:guaiacyl ratio more than 2-2.5:1], and hemicelluloses as xyloglucans; root apical meristem intermediate-open; root vascular tissue oligarch [di- to pentarch], lateral roots arise opposite or immediately to the side of [when diarch] xylem poles; origin of epidermis with no clear pattern [probably from inner layer of root cap], trichoblasts [differentiated root hair-forming cells] 0, exodermis +; shoot apex with tunica-corpus construction, tunica 2-layered; reaction wood ?, associated gelatinous fibres [g-fibres] with innermost layer of secondary cell wall rich in cellulose and poor in lignin; starch grains simple; primary cell wall mostly with pectic polysaccharides, poor in mannans; tracheid:tracheid [end wall] plates with scalariform pitting, wood parenchyma +; sieve tubes enucleate, sieve plate with pores (0.1-)0.5-10< µm across, cytoplasm with P-proteins, cytoplasm not occluding pores of sieve plate, companion cell and sieve tube from same mother cell; sugar transport in phloem passive; nodes 1:?; stomata brachyparacytic [ends of subsidiary cells level with ends of pore], outer stomatal ledges producing vestibule, reduction in stomatal conductance to increasing CO2 concentration; lamina formed from the primordial leaf apex, margins toothed, development of venation acropetal, overall growth ± diffuse, venation hierarchical-reticulate, secondary veins pinnate, veins (1.7-)4.1(-5.7) mm/mm2, endings free; most/all leaves with axillary buds; flowers perfect, pedicellate, ± haplomorphic, parts spiral [esp. the A], free, numbers unstable, development in general centripetal; P +, members each with a single trace, outer members not sharply differentiated from the others, not enclosing the floral bud; A many, filament not sharply distinguished from anther, stout, broad, with a single trace, anther introrse, tetrasporangiate, sporangia in two groups of two [dithecal], ± embedded in the filament, with at least outer secondary parietal cells dividing, each theca dehiscing longitudinally, endothecium +, endothecial cells elongated at right angles to long axis of anther; tapetum glandular, cells binucleate; microspore mother cells in a block, microsporogenesis successive, walls developing by centripetal furrowing; pollen subspherical, tectum continuous or microperforate, ektexine columellate, endexine thin, compact, lamellate only in the apertural regions; nectary 0; carpels present, superior, free, several, ascidiate, with postgenital occlusion by secretion, stylulus short, hollow, cavity not lined by distinct epidermal layer, stigma ± decurrent, carinal, dry [not secretory]; ovules few [?1]/carpel, marginal, anatropous, bitegmic, micropyle endostomal, outer integument 2-3 cells across, often largely subdermal in origin, inner integument 2-3 cells across, often dermal in origin, parietal tissue 1-3 cells across [crassinucellate], nucellar cap?; megasporocyte single, hypodermal, functional megaspore lacking cuticle; female gametophyte four-celled [one module, nucleus of egg cell sister to one of the polar nuclei]; supra-stylar extra-gynoecial compitum +; ovule not increasing in size between pollination and fertilization; pollen grains landing on stigma, binucleate at dispersal, mature male gametophyte trinucleate, germinating in less than 3 hours, pollination siphonogamous, tube elongated, growing between cells, growth rate 20-20,000 µm/hour, outer wall pectic, inner wall callose, with callose plugs, penetration of ovules via micropyle [porogamous], whole process takes ca 18 hours, distance to first ovule 1.1-2.1 mm; male gametes lacking cell walls, flagellae 0, double fertilization +, ovules aborting unless fertilized; P deciduous in fruit; seed exotestal, becoming much larger than ovule at time of fertilization; endosperm diploid, cellular [micropylar and chalazal domains develop differently, first division oblique, micropylar end initially with a single large cell, divisions uniseriate, chalazal cell smaller, divisions in several planes], copious, oily and/or proteinaceous; embryogenesis cellular; dark reversal Pfr -> Pr; Arabidopsis-type telomeres [(TTTAGGG)n]; 2C genome size 1-8.2 pg [1 pg = 109 base pairs], whole nuclear genome duplication [epsilon duplication], 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.]; (vessels with simple perforation plates in primary xylem); nodes 3:3; stomata anomocytic; flowers (dimerous), cyclic; K/outer P members with three traces, ("C" +, with a single trace); A few, (polyandry widespread, initial primordia 5, 10, or ring, ± centrifugal), filaments fairly slender, anthers basifixed; microsporogenesis simultaneous, pollen tricolpate, apertures in pairs at six points of the young tetrad [Fischer's rule], cleavage centripetal, wall with endexine; G with complete postgenital fusion, stylulus/style solid [?here]; seed coat?
[PROTEALES [TROCHODENDRALES [BUXALES + CORE EUDICOTS]]]: plant woody; (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 developing internally/adaxially to the corolla whorl and successively 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.
[DILLENIALES [SAXIFRAGALES [VITALES + ROSIDS s. str.]]]: nodes 3:3; stipules + [usually apparently inserted on the stem].
[SAXIFRAGALES [VITALES + ROSIDS]] / ROSANAE Takhtajan / SUPERROSIDAE: ??
[VITALES + ROSIDS] / ROSIDAE: anthers articulated [± dorsifixed, transition to filament narrow, connective thin].
ROSIDS 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: two penalized likelihood dates) suggested an age of (114-)108, 91(-85) m.y.a.; Bayesian relaxed clock estimates were (116-)114, 113(-110) m.y.. 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) 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) about 89.1 m.y.; ages in Schneider et al. (2004) range from about 110-167 m.y., while ca 96 m.y. is the age suggested by Sytsma 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 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 also 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 of the tree has since been much clarified (Hengcheng Wang et al. 2009). The composition of the rosid I clade (= fabids) has been perhaps particularly problematical. In an analysis including the mitochondrial matR and two chloroplast genes, [Celastrales + Oxalidales + Malpighiales] (the COM clade) were sister to the N-fixing clade, with weak to moderate support; Crossosomatales were weakly supported as sister to the rosid II clade (= malvids), while Myrtales and Geraniales appeared to be 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) recovered this [Myrtales + Geraniales] clade as sister to the rosid II clade, albeit with weak support, but the combined clade had strong support (weaker using maximum parsimony) and in turn being strongly supported as sister to the rosid I clade, albeit with sketchy sampling - i.e. the same basic set of relationships found in the comprehensive analysis of Hengcheng Wang et al. (2009).
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 grouping [COM clade + rosid II] (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 rosid I was not monophyletic, while Burleigh et al. (2011) in a genome-level analysis found that Malpighiales were embedded in the rosid II clade, although no representatives of Celastrales or Oxalidales were included in their study (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) discuss the influence of mitochondrial genes on relationships around here; they found that an analysis of mitochondrial genes alone placed a weakly supported COM clade as sister to core Malvidae with quite strong support.
The [COM + rosid II] clade was also obtained (just) in an analysis of 31 (30 eudicot) complete chloroplast genomes (Fajardo et al. 2013). Endress and Matthews (2006a) suggest some morphological characters that are consistent with such relationships. Ruhfel et al. (2014) also recovered varying relationships around here, although the [COM + N-fixing] clade was was sometimes recovered, however, mentioning a study by Sun et al. that was in the works, they suugested that there might be evidence that the COM clade was the result of a very ancient hybridization between a member of the fabids and of the malvids.
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 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).
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).
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...
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
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 ca 6 cells and inner integument 4-5 cells across; fruit nut, with retrorsely barbed spines; seed 1, exotestal cells enlarged, tanniniferous, tegmen to 7 cells thick, largely disappearing; endosperm development?, 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).
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.]
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
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.
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.
(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 [Morkellioideae + Tribuloideae] [Seetzenioideae [Larreoideae + Zygophylloideae]], however, there do not seem to be good characters distinguishing the groups. For relationships between Larrea and relatives, see Lia et al. (2001). For relationships and morphology of Zygophylloideae, see Beier et al. (2003). For relationships of the southern African Zygophyllaceae, see Bellstedt et al. (2008). The distinctive Balanites is to be included in Tribuloideae for the time being, at least (Sheahan & Chase 1996, 2000)
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).