LIGNOPHYTA

True roots +; lateral meristems: cork cambium producing cork abaxially, vascular cambium producing phloem abaxially and xylem adaxially.

EXTANT SEED PLANTS/SPERMATOPHYTA

Plant woody, 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, thus containing p-hydroxyphenyl and guaiacyl lignin units, (lignins derived from p-coumaryl alcohol, i.e. S [syringyl] lignin units); true roots present, apex multicellular, xylem exarch, and branching endogenous; arbuscular mycorrhizae +; shoot apical meristem multicellular, interface specific plasmodesmatal network; stem with ectophloic eustele, endodermis 0, xylem endarch, branching exogenous; vascular tissue in t.s. discontinuous by interfascicular regions; vascular cambium + [xylem ("wood") differentiating internally, phloem externally]; wood homoxylous, tracheids and rays alone, tracheid/tracheid pits circular, bordered; mature sieve tube/cell lacking functioning nucleus, plastids with starch grains; phloem fibres +; stem cork cambium superficial, root cork cambium deep seated; leaves with single trace from sympodium ["nodes 1:1"]; stomata ?; leaf vascular bundles collateral; leaves megaphyllous [determinancy evolved first, then ad/abaxial symmetry], spiral, simple, lamina with vein density up to 5 mm/mm² [mean for all non-angiosperms 1.8]; axillary buds associated with at most some leaves; prophylls [including bracteoles] two, lateral; plant heterosporous, sporangia eusporangiate, on sporophylls, sporophylls aggregated in indeterminate cones/strobili; true pollen [microspores, i.e. no distal pore for release of gametes] +, grains mono[ana]sulcate, exine and intine homogeneous; ovules unitegmic, crassinucellate, megaspore tetrad tetrahedral, only one megaspore develops, megasporangium indehiscent; male gametophyte development first endo- then exosporic, tube developing from distal end of grain, to ca 2 mm from receptive surface to egg, gametes two, developing after pollination, with cell walls, with many flagellae; female gametophyte endosporic, initially syncytial, walls then surrounding individual nuclei; seeds "large", first cell wall of zygote transverse, embryo straight, endoscopic [suspensor +], short-minute, with morphological dormancy, white, cotyledons 2; plastid transmission maternal; 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.

MAGNOLIOPHYTA

Lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, non-hydrolysable tannins, quercetin and/or kaempferol +, 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; shoot apex with tunica-corpus construction, tunica 2-layered; reaction wood ?, with gelatinous fibres; 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 cells from same mother cell that gave rise to the sieve tube; sugar transport in phloem passive; nodes unilacunar [1:?]; stomata with ends of guard cells level with pore, paracytic, outer stomatal ledges producing vestibule; leaves petiolate, lamina [formed from the primordial leaf apex], development of venation acropetal, 2ndary veins pinnate, fine venation reticulate, veins (1.7-)4.1(-5.7) mm/mm², endings free; most/all leaves with axillary buds; flowers perfect, pedicellate, polysymmetric, parts spiral [esp. the A], free, numbers unstable, development in general centripetal; P not sharply differentiated, with a single trace, outer members not enclosing the rest of the bud, often smaller than inner members; 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 by action of hypodermal endothecium, endothecial cells elongated at right angles to long axis of anther; tapetum glandular, binucleate; microspore mother cells in a block, microsporogenesis successive, walls developing by centripetal furrowing; pollen subspherical, tectum continuous or microperforate, ektexine columellar, endexine thin, compact, lamellate only in the apertural regions; nectary 0; G free, several, ascidiate, with postgenital occlusion by secretion, stylulus short, hollow, cavity not lined by distinct epidermal layer, stigma ± decurrent, 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, megaspore tetrad linear, functional megaspore chalazal, lacking sporopollenin and cuticle; female gametophyte four-celled [one module, nucleus of egg cell sister to one of the polar nuclei]; P deciduous in fruit; seed exotestal; pollen binucleate at dispersal, trinucleate eventually, germinating in less than 3 hours, pollination siphonogamous, tube elongated, growing at 80-600 µm/hour, with pectic outer wall, callose inner wall and callose plugs, growing between cells, penetration of ovules via micropyle [porogamous] within ca 18 hours, distance to first ovule 1.1.-2.1 mm, tube moves between nucellar cells; double fertilisation +, endosperm diploid, cellular [micropylar and chalazal domains develop diffently, 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 cellular ab initio, minute; germination hypogeal, seedlings/young plants sympodial; Arabidopsis-type telomeres [(TTTAGGG)_n]; whole genome 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]].

Evolution. Possible apomorphies for flowering plants are in bold. Note that the actual level to which many of these features, particularly the more cryptic ones, should be assigned is unclear. This is because some taxa basal to the [magnoliid + monocot + eudicot] group have been surprisingly little studied, there is considerable homoplasy as well as variation within and between families of the ANITA grade in particular for several of these characters, and also because details of relationships among gymnosperms will affect the level at which some of these characters are pegged. For example, if reticulate-perforate pollen is optimized to the next node on the tree (see Friis et al. 2009 for a discussion), it effectively makes the pollen morphology of the common ancestor of all angiosperms ambiguous... For other features such as details of sugar transport in the phloem, their placement on the tree is frankly speculative. Finally, for features such as parietal tissue/a nucellus only one (Nymphaeales) to three cells thick above the embryo sac and a stylar canal lacking an epidermal layer, although plesiomorphous for basal grade angiosperms (Williams 2009), I am unsure where on the tree a thicker nucellus and a stylar epidermal layer are acquired.

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

ROSIDS ET AL. = DILLENIALES [SAXIFRAGALES [VITALES + ROSIDS]]: 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.

Evolution. Divergence & Distribution. Wang et al. (2009: two penalized likelihood dates, Dilleniales not included) suggested that radiation in crown group rosids began (114-)108, 91(-85) million years ago, the stem group age being (116-)110, 93(-87) million years; Bayesian relaxed clock estimates were slightly older, to 116 and 119 million years respectively. Wikström et al. (2001) suggested an age of (98-)95(-92) million years, while Magallón and Castillo (2009) estimated ages of ca 107.9 and 108.4 million years for relaxed and constrained penalized likelihood datings respectively for crown rosids and 112.6 and 113.9 (relaxed and constrained again) for the divergence of stem rosids. Moore et al. (2010: 95% highest posterior density) estimate an age of (110-)106(-103) million years for this crown group, and ages of (121-)116, 114(-108, and details of basal branching in rosids different from the main tree here) million years are suggested by Bell et al. (2010 for details: Dilleniaceae in superasterids...). Davies et al. (2011: 95% credibility intervals, Dilleniaceae not included) suggested an age for the crown group of (115-)94((-83) million years. On the other hand, in a study using a small sample of nuclear genomes, Argout et al. (2010) give a date for this clade of only ca 90 million years.

Plant-Animal Interactions. Redfern (2011) notes that Cynipinae gall wasps are common on rosids, particularly on Rosaceae and Fagaceae.

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 the rosids.

ROSID I / FABIDAE  Back to Main Tree

Endosperm scanty.

Evolution. Divergence & Distribution. Argout et al. (2010) give a date for this clade of a mere ca 77 million years, however, Wang et al. (2008: penalized likelihood dates) suggested that rapid radiation within Fabidae occurred (114-)108-91(-85) million years ago, perhaps a little before than in Malvidae.

Phylogeny. The position of Zygophyllales was rather labile in the comprehensive analysis of Wang et al. (2009). It sometimes appeared to be linked with the malvids (maximum parsimony), or sometimes with the fabids (maximum likelihood), but the former position could be rejected (Wang et al. 2009). However, several recent analyses, including the 17-gene analysis of Soltis et al. (2011) are placing it sister to the N-fixing clade (Fabidae), 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.

ZYGOPHYLLALES Link   Main Tree, Synapomorphies.

Harman alkaloids, diversity of linans and neolignans +; 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.

Evolution. Divergence & Distribution. The age of crown group Zygophyllales was estimated as (88-)79(-70) or (64-)55(-46) million years (two penalized likelihood dates), the stem group age being (114-)108(-102) and (97-)91(-85) million years; Bayesian relaxed clock estimates were slightly older, to 102 and 115 million years respectively (Wang et al. 2009). Wikström et al. (2001) suggested an age for stem Zygophyllales of some (98-)95(-92) million years, and separation of the two families some (68-)64(-60) million years before present, while Magallón and Castillo (2009) estimated ages of ca 95 and 95.3 million years for relaxed and constrained penalized likelihood datings for the divergence of stem Zygophyllales.

Bacterial/Fungal Associations. Mycorrhizae are usually absent from the whole 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; hairs unicellular, thin-walled; wood fluorescence?; nodes 1:1; petiole bundle (deeply) arcuate; 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, petaloid internally, median member abaxial, larger than the others, (2) 3 adaxial C clawed, ± connate, 2 abaxial smaller, not clawed, glandular [often secreting lipid]; A (3) 4, (adnate to adaxial C), filaments often stout, anthers dehiscing by pores, endothecial cells with thickening parallel to long axis of cells; G [2], adaxial member much reduced, placentation apical, style long, stigma small, recessed; ovules 2/carpel, collateral, outer integument ca 6 cells and inner integument 4-5 cells across; fruit nut-like, 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]

• Krameriaceae may be recognised by their small, spiral, often elliptic, entire leaves and their distinctive, rather pea-like flowers. These are inverted, with the odd petal adaxial, and have four or five large elliptic sepals that are petaloid internally; the three strongly clawed adaxial petals are more or less connate by their bases and the usually four fertile stamens are also adaxial. The one-seeded fruits have retrorsely-barbed spines.

Evolution. Divergence & Distribution. It has been estimated that crown group Krameria started diverging (34-)12(-5) million years ago (Renner & Schaefer 2010).

Floral 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. There are no vessels in the leaves, and the traces to the sepals, petals and stamens in the flower are all separate. The roots have a red phlobaphene pigment. Simpson (1982, 2006) discussed the long controversy over the orientation of the flower, however, the flowers do appear to be inverted (cf. also Milby 1971, see Fig. 73 in Simpson 2006).

For further details, see Leinfellner (1971: ovary), Verkeke (1985: ovule and seed), Simpson (1989) and Carlquist (2005b: wood anatomy); Simpson et al. (2004) provide a phylogeny of the family and Simpson (2006), and The Parasitic Plant Collection and also Heide-Jørgensen (2008) give much general information.

Previous Relationships. Krameriaceae have often been considered to be close to Pollygalaceae (Fabales), as by

ZYGOPHYLLACEAE R. Brown, nom. cons.   Back to Zygophyllales

Trees to herbs (thorny); mycorrhizae absent; (C₄ photosynthesis), anthroquinones +, 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, (2ndary 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 Beier et al. 2004, esp. 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.

5. Zygophylloideae

(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.

• Zygophyllaceae are a variable group growing in more or less arid and saline conditions almost worldwide. They are herbs to trees often with compound usually stipulate and opposite leaves that lack a terminal leaflet; the nodes tend to be swollen. The flowers have all parts free apart from the carpels; there are usually ten stamens that often have scales at the base. Some aspects of floral morphology, e.g. obdiplostemony, gross stigma morphology, are reminiscent of Geraniales.

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 the deserts there.

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.

Seed Dispersal. A number of species, including those of Zygophyllum, have myrmecochorous seeds (Lengyel et al. 2010).

Economic Importance. Guaiacum has very hard, self-lubricating wood that was used in the past to make bearings.

Chemistry, Morphology, etc. A number of taxa with opposite leaves have split laterals (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. In at least some species of Larrea chloroplasts are inherited paternally (Yang et al. 2000).

• Balanites is very different from other Zygophyllaceae in both floral and vegetative features. It is a thorny shrub or tree with bitter bark, the petiole anatomy is complex, and the stomata on the stem are transverse to the long axis. The leaves are spiral and 2-foliolate. The C envelops the flower when young; There is 1 pendulous ovule per carpel with a bistomal, zig-zag micropyle. The fruit is a drupe with a single seed and no endosperm (Sheahan & Cutler 1993; see also Parameswaran & Conrad 1982). Balanites also differs from other Zygophyllaceae in seed anatomy, i.a. having a multiplicative and vascularized outer integument (Boesewinkel 1994). However, it is to be included in Tribuloideae for the time being, at least (Sheahan & Chase 1996, 2000). Howard (1970) found no stipules in Balanites, but there are structures in the stipular position, if minute.

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).

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).