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.

CORE EUDICOTS / GUNNERIDAE    Back to Main Tree

Ellagic and gallic acids common; compitum + [one place]; micropyle?; PI-dB motif +, small deletion in the 18S ribosomal DNA common.

Evolution. Divergence & Distribution. The age of stem core eudicots has been estimated as some 120-116 million years before present with its divergence beginning 116-115 million years before present (Anderson et al. 2005), other stem group ages are 121.2 or 121.9 million years (relaxed and constrained penalized likelihood: Magallón & Castillo 2009), and crown group ages are 132-119(-89) million years in Soltis et al. (2008: a variety of estimates), 114.4 or 115.1 million years in Magallón and Castillo (2009, relaxed and constrained penalized likelihood again), (113-)110(-105) million years (Moore et al. 2010: 95% highest posterior density), and (139-)127, 119(-109) million years (Bell et al. 2010 for details).

For general information on core eudicot diversification, see Magallón et al. (1999); most of the estimates of percentage diversity of clades are taken from this work. The diversification rates of many of the clades are higher than the rates in other angiosperms (Magallón & Sanderson 2001).

Floral Biology & Seed Dispersal. Compitum presence could perhaps be pegged as a key innovation at this node, given that it is found in Gunneraceae, the rosids, and the extended asterid clade, although not Myrothamnaceae or Dilleniaceae (cf. Endress 2011).

Chemistry, Morphology, etc. The floral morphology of Gunnerales is more like that of Buxales, etc., i.e., of taxa on more basal branches in the eudicots; i.e., it is apparently plesiomorphic and is not very like that of other core eudicots (e.g. D. Soltis et al. 2003a; Doust & Stevens 2005; Kubitzki 2006a). However, note that chemically Gunnerales seem similar to core eudicots, e.g. they have ellagic acid (e.g. Soltis et al. 2005b), and general molecular data link them closely with core eudicots. Some perhaps important gene duplications may have occurred somewhat earlier (see the Trochodendrales page), and it is not known if they have the euAP3 gene, etc. (see link below). Wanntorp and Ronse De Craene (2005) and Ronse De Craene and Wanntorp (2006) note that the morphology of Gunnerales flowers cannot be directly related to that of the pentamerous core eudicots, the floral morphology of the former being shaped by the exigencies of wind pollination. Wanntorp and Ronse De Craene (2005) also note that three successive floral whorls may be opposite each other, and this is a feature e.g. of some Ranunculales like Berberidaceae, Sabiales, etc., but not of core eudicots. Indeed, the flowers cannot be considered as being readily derived from those of other core eudicots given our current knowledge of floral morphology and development, rather, they seem fundamentally similar to those scattered in other eudicot clades basal to Gunnerales. For discussion of the "typical" core eudicot flower, see the Dilleniales page.

Whether or not the rps2 and rps11 genes occur in Gunnerales is apparently unknown, but the first is absent in Buxales and Trochodendrales and the second in Buxales alone (Adams et al. 2002b); they are probably lost slightly lower down on the tree (as are benzylisoquinoline alkaloids).

Phylogeny. This clade is strongly supported, e.g. Chase et al. (1993), D. Soltis et al. (1997, 1999, 2003a), Hoot et al. (1998), Nandi et al. (1998), and Zhu et al. (2007), although indistinguishable from other core eudicots in (e.g.) P. Soltis et al. (1999). However, in some earlier studies the exact position of Gunnerales was unclear (e.g. Chase et al. 1993; Morgan & Soltis 1993), but quite strong support for a position sister to the rest of the core eudicots was provided by Senters et al. (2000: Gunneraceae alone sampled), rather weaker support by Hilu et al. (2001). A four-gene analysis also provided strong support for this position (D. Soltis et al. 2003a).

Classification. Gunnerales were excluded from the core eudicots in earlier versions of this site (pre Version 7; cf. A.P.G. I and II 1999, 2003) because of their apparently largely plesiomorphic floral morphology. However, in the interests of consistency between classification systems their limits have been adjusted to conform with those now generally used.

GUNNERALES Reveal   Main Tree, Synapomorphies.

Ellagic acid +; vascular cambium 0 [?all taxa]; vessel elements?; sieve tube plastids with protein crystalloids and starch; pith with sclerenchymatous diagrams; lamina margins with hydathodal teeth, 2ndary veins palmate; plants dioecious; inflorescences with terminal flowers; flowers small; P 0; A latrorse; stigma at most weakly secretory; seed coat?

Evolution. Divergence & Distribution. Stem group Gunnerales date from 115 to 112 million years before present, the dates for the crown group members being 90-55 million years before present (Anderson et al. 2005); Magallón and Castillo (2009) suggest a stem group age of 114.4 or 115.1 million years. Soltis et al. (2008: a variety of estimates) suggest an age of divergence of the Gunnerales from other core eudicots of 132-119(-89) million year.

Chemistry, Morphology, etc. This is a rather surprising group. Gunneraceae and Myrothamnaceae look very different; one is an often gigantic mesophytic herb, the other a resurrection shrub of arid habitats. In the former, hydathodes are well developed and mucilage or possibly resinous lacquer is secreted, in the latter, hydathodes are poorly developed (but see Drennan et al. 2009) and the plant secretes resin. They do both have flowers without much of a perianth, although the plesiomorphic condition for the order may be to have some kind of perianth, but details of pollen (e.g. cf. Zavada & Dilcher 1986; Wanntorp et al. 2004), etc., differ. González and Bello (2009) suggest possible apomorphies for the pair, including the presence of stipules, but see below for a possible interpretation of the stipules of Gunnera.

Classification. There is an option of including Myrothamnaceae in Gunneraceae in A.P.G. II (2003), both being small and monogeneric families, but they are so different in appearance that it seems best to keep them separate (see Wilkinson 2000 for a table of differences).

Includes Gunneraceae, Myrothamnaceae. 2 families, 2 genera, ca 45 species.

Synonymy: Myrothamnales Reveal - Gunnerineae Shipunov - Myrothamnanae Takhtajan

GUNNERACEAE Meisner, nom. cons.   Back to Gunnerales

Perennial (annual) herbs, rhizomatous or stoloniferous; Nostoc colonies in stem and root; cork ?; vessel elements with simple or few-barred scalariform perforation plates [stems] or scalariform, bars to ca 150 [stolons]; axis polystelic [stem] or vascular cylinder [stolons]; nodes multilacunar; stem with endodermis, also low glandular areas; petiole anatomy complex; cataphylls common; stolons with opposite scales; leaves spiral, colleters +; inflorescence usu. branched-racemose, (plant polygamous), bracteoles 0; P 2 (3), valvate; staminate flowers: (P 4, 0); A 1-2; pollen semitectate-reticulate; pistillode +; carpellate flowers: staminodes +; G [2], inferior, transverse and alternate with P, uni(bi)locular, stigmas dry; ovules 1(-2)/carpel, apical, epitropous, micropyle endostomal, outer integument ca 3 cells across, inner integument ?2/ca 4 cells across; embryo sac tetrasporic, 16-celled [Peperomia-type]; fruit drupaceous (nut); seed coat?; endosperm with some starch; n = 17.

1[list]/40-50. Circum S. Pacific, Africa and Madagascar (map: see van Balgooy 1975; Wanntorp & Wanntorp 2003; fossil records [green] from the Late Cretaceous, see Jarzen & Dettmann 1989, also Osborne & Sprent 2002). [Photo - Leaf, Inflorescence]

• Gunneraceae are sometimes huge herbs that can be recognised by their spiral leaves the blades of which are toothed and have palmate venation that is very prominent on the lower surface, their often rather stipule-like "scale leaves", and their relatively large and branched inflorescences bearing many small, inconspicuous flowers; the ovary is inferior and bicarpellate.

Evolution. Divergence & Distribution. The pollen is distinctive and is known from the Early Cretaceous onwards (Wanntorp et al. 2004b) in all four continents of the Southern Hemisphere, as well as from North America, India and deposits in the Indian and south Atlantic Oceans (the latter three localities in the Palaeogene - see Jarzen & Dettmann 1989).

Bacterial/Fungal Associations. All taxa have an association with the cyanobacterium, Nostoc (Osborne & Sprent 2002 for the ecology of the interrelationship). Glands on the stem found immediately below the leaves secrete mucilage, and Nostoc enters the plant here as motile hormogonia. Johansson and Bergman (1994, and references) and in particular Khamar et al. (2010) describe the establishment of this association; there are different sugars in the mucilage that attracts Nostoc and in the gland tissue in which Nostoc grows (Khamar et al. 2010). Nostoc infects as hormogonia, but in the plant it loses its motility and produces many heterocysts; it may not photosynthesise at all there (Bergman 2002). Söderbäck and Bergman (1993) detail the physiology of the two partners; see also Adams et al. (2006).

Chemistry, Morphology, etc. There are stipule-like structures on the stem of many species (but this is not an apomorphy for the family) that are interpreted as being cataphylls by Wanntorp et al. (2003). Since they are at least sometimes opposite they may be prophylls; they range in shape from suboblong and entire to deeply laciniate with linear lobes. The lamina varies from 7 mm to 3 m across, and the teeth have a glandular apex that broadens distally; two higher order veins are also involved. The difference in anatomy between stems and stolons is striking; the roots are triarch to polyarch (Wilkinson 2000). Although Gunnera herteri, sister to the rest of the genus, has normal stem anatomy, it is an annual and its anatomy is conceivably derived. The difference in size, etc., between the inner and outer tepals is such that they are sometimes described as sepals and petals (e.g. Wanntorp & Ronse de Craene 2005; Ronse de Craene & Wanntorp 2006; González & Bello 2009). The rather uncommon perfect flowers then have two median sepals, two lateral petals, two stamens opposite the petals, and two carpels also opposite the petals (Ronse de Craene & Wanntorp 2006; González & Bello 2009), indeed, there is considerable infraspecific variation in floral morphology (González & Bello 2009).

Much information is taken from Wilkinson (1998: anatomy); for ovules, etc., see Schnegg (1902) and Warming (1913), for pollen, Wanntorp et al. (2004a), and for floral morphology and development see Rutishauser et al. (2004), Wanntorp and Ronse De Craene (2005) and Ronse De Craene and Wanntorp (2006); Wilkinson and Wanntorp (2006) summarize what is known about the family.

Phylogeny. For a phylogeny of Gunnera, see Wanntorp et al. (2001, also Wanntorp 2006: summary); the annual G. herteri is sister to the rest of the genus.

Previous Relationships. In the past Gunneraceae have often been associated with Haloragaceae, also with an inferior ovary and reduced flowers, but in the latter the stamens are as many as the sepals, and opposite them, the gynoecium is multilocular, with one ovule/loculus, etc. - see Saxifragales. Gunneraceae were included in Saxifraganae - Rosidae by Takhtajan (1997). Recently Fuller and Hickey (2005), examining details of leaf architecture, etc., suggested that Gunneraceae were best associated with the herbaceous Saxifragaceae, but this is probably because of habit/habitat-associated parallelisms.

MYROTHAMNACEAE Niedenzu, nom. cons.   Back to Gunnerales

Aromatic-resinous shrubs, resurrection plants; essential oils, gallotannins, myricetin, dihydro/chalcones +; cork?; vessel elements with reticulate perforations; nodes split-lateral; petiole bundle arcuate; individual epidermal cells resiniferous; plant glabrous; leaves opposite, basally forming a sheath, lamina vernation plicate, 2ndary veins palmate-flabellate, stipules 2, small, persisting on the petiolar sheath; spikes bracteate, with terminal flowers; staminate flowers: A 3-4, or (3-)4(-8) and connate, anthers valvate basally, connective produced; pollen in tetrads, triporate, intectate, with clavate projections themselves papillate; pistillode 0; carpellate flowers: staminodes 0; G 3-4, only basally connate, with 5 vascular bundles and surface oil cells, the odd member abaxial, styluli short, recurved, stigma decurrent, in two crests; ovules many/carpel, micropyle bistomal; embryo sac bisporic, 8-celled [Allium-type]; fruit follicular (and septicidal); exotestal cells with somewhat thickened outer walls; endosperm development?; n = 10.

1[list]/2. Africa and Madagascar (map: from Puff 1978b). [Photos - Collection]

• Myrothamnaceae are resurrection plants; the leaves may appear to dry out, but they regain turgor, etc., when conditions improve. They are vegetatively very distinctive aromatic shrubs; the leaves are opposite and have a long, common sheath on which there are four persistent stipular points, and the blades have palmate secondary veins and toothed margins.

Evolution. Ecology & Physiology. Myrothamnaceae are resurrection plants; the leaves may appear to dry out, but they regain turgor, etc., when conditions improve. Moore et al. (2007) discussed the physiology of Myrothamnus, which shows surprising infraspecific variation.

Chemistry, Morphology, etc. The stems are narrowly winged and there is no axial parenchyma. There are four veins in the leaf sheaths - two bundles going directly to the midrib, and two commissural veins (Grundell 1933). Since carpellate flowers lack perianth or staminodes, it is not clear if the ovary is inferior. When flowers are terminal - on the main or lateral axes - there are four "Hochblätter" as well as bracts and bracteoles, and the four carpels are opposite the "Hochblätter" (Jäger-Zürn 1966) which might even be interpreted as perianth or tepals (Wanntorp and Ronse De Craene 2005); see also Puff (1978a, 1978b). The carpellate flowers have been described as being zygomorphic (Moore et al. 2007).

For information, see Kubitzki (1993b: general).

Previous relationships. Myrothamnaceae were included in Hamamelididae by Takhtajan (1997).