SEED PLANT EVOLUTION (still being developed)

LIGNOPHYTES  Back to Main Tree

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

Evolution. Divergence & Distribution. Sister to the monilophytes, ferns and their relatives, are the lignophytes, which have secondary thickening, and the split between the two is old, occurring in the mid- to later Devonian, some 375-400 million years before present (Pryer et al. 1995, 2000, 2001a, 2004; Schneider et al. 2002). However, fossils from Canada and France of up to ca 407 million years old (Early Devonian), otherwise quite like Psilophyton, have secondary xylem with rays and tracheids (Gerrienne et al. 2011).

Bennettitales (perhaps close to Gnetales), Corystospermales (pteridosperms; these seem to have survived the end-Cretaceous mass extinction in Tasmania - see McLoughlin et al. 2008), and conifers were all radiating in the Triassic. Although extant seed plants can be assigned to five ancient clades, as is dicussed under individual groups extant diversity is mostly post-Cretaceous in age, although of course angiosperms diversification began in the Early Cretaceous or perhaps earlier.

Ecology & Physiology. Early lignophytes were small, and Gerrienne et al. (2011) suggest that the need for increased water conductance in response to decreasing CO₂ concentration (the stomata would have to be open more), not need for support, early drove the evolution of a vascular cambium.

Lignophytes soon became quite large plants, larger than earlier land plants but not necessarily larger than the tree lycophytes of e.g. the Carboniferous; they also had well developed true roots, the fine roots presumably having root hairs. They are implicated in climate change in the Silurian-Devonian via a complex series of feed-back loops (e.g. Beerling & Berner 2005). There was a draw-down of carbon dioxide - some 90% over the late Paleozoic - and an increase in oxygen in the atmosphere, and concomitant with this carbon dioxide decrease, stomatal density and hence transpiration increased. Hence the advantage of a well-developed vascular system produced by secondary thickening. This increased transpiration also allowed the the evolution of megaphylls whose temperature would stay within bounds because of evaporative cooling (Berling et al. 2001; Beerling 2005a and references). Photosynthesis and the sequestration of carbon increased, and carbon in plant material is likely to have been buried by the accumulating sediments produced by rock weathering (Beerling 2005a). Furthermore, the roots of early lignophytes may have increased this weathering, not so much by direct action, but by improving soil structure and so increasing drainage (Retallack 1997; Beerling 2005a; cf. Taylor et al. 2009 in part); the increased nutrients in water drainage could lead to algal blooms and may be connected with marine anoxic episodes (Algeo & Scheckler 1998). Of course, this whole weathering process also entails the loss of CO₂ and a reduction in its atmospheric concentration (e.g. Beerling 2005a; Taylor et al. 2009).

Protective secondary metabolites may have evolved about this time, so decreasing CO₂ produced by respiration of organisms that would have decomposed the plants (Retallack 1997a). However, there is no evidence of lignin-destroying fungi in the Paleozoic (), so overall carbon fixed in photosynthesis is likely to have been sequestered in sediments or used up by the increased rock weathering, thus decreasing atmospheric CO₂ concentration.

As lignophyte vegetation extended over the land, the increased photosynthesis they supported led to increasing oxygen concentration in the atmosphere. Indeed, fires were only moderately common in the Silurian, and oxygen seems to have reached ca 16%, the lower limit at which the burning of organic materials becomes possible, only towards the end of the Devonian, so CO₂ is unlikely to have been released from dead plant remains in this way (Scott " Glasspool 2006; Belcher et al. 2010). Interestingly, the increase in oxygen concentration in the atmosphere may have allowed the evolution of animals with larger bodies; it has been suggested that evolution of arthrodire fish, some of which reached ca 10 m in length, is linked to the rise in oxygen concentration in the sea (Dahl et al. 2010). Oxygen concentration of the atmosphere contuinued to increase gradually after the end-Devonian, probably reaching a high of about 30% towards the end of the Permian, close to the 35% at which plants would have burned readily even if they were not dry. However, it crashed to somewhat below current levels immediately after the end of the Permian and has shown only moderate changes since (Scott & Glasspool 2006).

There is interesting variation in stomatal control in extant land plants. Stomatal closure in ferns - whatever their habitat - seems to occur when the leaf still has a relatively high water potential when compared with angiosperms not growing in shade (Brodribb & Holbrook 2004). If water is rapidly lost in angiosperms, subsidiary cells lose turgor first, and this causes guard cells to open the stomatal aperture (Brodribb & McAdam 2010). Recently it has been shown that stomata of ferns and lycophytes do not respond to abscisic acid, whereas those of conifers and angiosperms do (they close more or less immediately - Brodribb & McAdam 2010), similarly, ferns do not respond to elevated CO₂ concentrations in the atmosphere (Brodribb et al. 2009) or to blue light (Doi & Shimizaku 2008) - control over stomatal opening is active rather than passive. [Para needs work.]

There are also suggestions that lycophytes had proportionally a large amount of lignin (Robinson 1990), while litter from extant ferns and fern allies and bryophytes is slow to decompose compared to that of gymnosperms and especially angiosperms (Cornwell et al. 2008).

On Vegetative Morphology. Lignophytes have distinctive secondary thickening. Their stems have a vascular cambium which is bifacial, producing secondary phoem externally and secondary xylem internally (e.g. see Donoghue 2005; Rothwell et al. 2008b for wood evolution in general); thus lignophytes often have stems with large amounts of wood (see Robinson 1990 for the decrease in bark:wood ratios from the lycopods). There is also external bark produced by the separate cork cambium. The origins of seed plants, the focus of this site, are to be sought in the mid-Devonian progymnosperms, often homosporous plants with compound leaves and well-developed, manoxylic secondary thickening the tracheids of which have circular bordered pits on the radial walls. The leaves themselves may have been small, although the branch systems as a whole may have been flattened; there are no obvious leaf traces. The origin of a stele more like that of extant spermatophytes can be seen in taxa in which the solid central vascular tissue (the xylem was exarch or mesarch) became ridged and dissected into vertical columns, pith developing. The vascular system consisted of sympodia terminating in leaves (the ultimate portion being the leaf trace), the other part of the sympodia continuing on up the stem as reparatory strands (e.g. Beck 1962; Kumari 1963; Namboodiri & Beck 1968; Stewart & Rothwell 1993 for a good summary).

Pollination Biology & Seed Dispersal. Plants with similar vegetative morphologies may have been heterosporous, and may be found in the same fossil beds as fossilised seeds (see e.g. Beck 1962, 1981; Carluccio et al. 1966; Namboodiri and Beck 1968). The progymnosperm Archaeopteridales and Aneurophytales are fossil orders of plants of this kind; they both have mesarch xylem like the monilophytes. Flowering plants are but a single clade of seed plants, and seed plants or spermatophytes in general are characterised by heterospory, a single megaspore per sporangium, and the presence of an integument (Kenrick & Crane 1997; Cleal et al. 2009 and references). They have a relatively very rich fossil record, and these fossils may have morphologies very unlike those of any living plant, whether angiosperm or gymnosperm. Ovules are known from the Devonian (Stewart & Rothwell 1993), and recently Gerienne et al. (2004) described the ovules of Runcaria, a seed plant from the middle Devonian of some 385 million years before present. Detailed studies on pteridosperms are helping to clarify their morphology (Taylor et al. 2006 and references, also other papers in J. Torrey Bot. Soc. 133(1). 2006; see also Taylor et al. 2009 for a summary), and this will help us to understand the phylogeny of this whole area.

Runcaria, from the Middle Devonian, is probably to be assigned to Aneurophytales, and lacks a lagenostome, and Gerienne et al. (2004) suggest that the antherozoids reached the megagametophyte by lysis of the megasporangium wall, which forms a long, terminal projection in this plant. In seed ferns and their immediate relatives pollen probably germinated on the adaxial surface, the tetrad of megasopores is linear, amd the integument is vascularized (Taylor et al. 2009). Some Archaeopteridales, from ca 365 million years before present, have a lagenostome and probably pollination/fertilisation mechanisms more like those of other seed plants. It is likely that some early conifers and Cordiatales had microspores whose development was probably endosporic (e.g. Friedman & Gifford 1997); zoidogamy, fertilization by motile male gametes, likely occurred, and pollination by insects is possible (Labadeira et al. 2007; Labandeira 2010).

A number of gymnosperms, both living and extict, have saccate pollen. Indeed, by the lower Carboniferous there were to be found the rather conifer-like Cordaitales and Callistophytales, which had compound pollen-bearing structures and saccate pollen, and slightly later, the still more conifer-like ("ancestral") Voltziales that lacked saccate pollen and which can perhaps be linked with Cupressaceae (Rothwell et al. 2011 and references; see Taylor et al. 2009 for an excellent survey of the early gymnosperms). In general, there is a correlation between saccate pollen, erect cones, inverted or downwards-facing ovules, and the presence of a pollination droplet - although perhaps not in Cordaitales; saccate pollen, a device to help float the pollen onto the micropyle, has clearly evolved more than once (Leslie 2008, 2010b).

Seeds of Mesozoic seed plants are very diverse in their morphology (e.g. Anderson & Anderson 2004). Seed size was often large [ref], and Lovisetto et al. (2012) discuss the evolution of fleshiness in disseminules of seed plants in general; similar genes are involved, even if the location of fleshiness may be very differeent morphologically.

It is likely that some early conifers and Cordiatales had microspores that lacked a sulcus, but had proximal sutures (they were trilete or monolete), and whose development was probably endosporic (e.g. Friedman & Gifford 1997). The pollen in Mesozoic seed plants is often called prepollen, having proximal (rather than distal) germination via a preformed suture and haptotypic marks showing where the pollen grains were originally attached. All extant seed plants have true pollen in which germination is distal and there are no haptotypic marks. However, the relationships between fossil plants with prepollen, other fossils with true pollen, and extant gymnosperms, which also have true pollen, even if Cycadales and Ginkgoales also show zoidogamy, are not well understood, and the distinction between prepollen and pollen may be of little value (see Poort et al. 1996 for a review; Taylor et al. 2009).

Phylogeny. Note that a major distinction has been drawn between manoxylic and pycnoxylic groups, the former, the cycadophytes, include seed ferns, cycads, and the immediately unrelated cycadeoids (e.g. Bennettitales), the latter include the coniferophytes, i.e. all other extant gymnosperms and several fossil groups (Chamberlain 1935; see also Gifford & Foster 1988). Thus within gymosperms, manoxylic wood, megaphyllous leaves, and radiospermic (polysymmetric) seeds seem to be associated, as do pycnoxylic wood, microphyllous leaves, and platyspermic (disymmetrical) seeds (Sporne 1965). However, whether or not these represent completely independent lines of evolution is unlikely, especially if Bennettitales are close to angiosperms or Gnetales (the latter seems more likely, see below). Thus Ryberg et al. (2007) emphasise the large amounts of secondary phloem that persist in a cycad stem, presumably because the cork cambium is not very active; some larger cycads have fibres in tangential bands in this phloem. Both characters are common in the Bennettitales, which with the Cycadales make up the cycadophytes. This will either be a parallelism or, just conceivably, a plesiomorophy that is lost, but establishing details of relationships will be critical. Palaeozoic seed fern groups like Lyginopteridaceae and Medullosaceae are described as being manoxylic, while the short shoots of Ginkgo are manoxylic and the long shoots pycnoxylic (Gifford & Foster 1988). Another major distinction has been drawn between radiospermic and platyspermic seeds, but this, too, may also not be as fundamental as some have suggested. Finally, a distinction is sometimes drawn between coniferophytes and conifers, although what the two contain and their relationships are unclear (Rothwell & Mapes 2001); phylogenetic studies are certainly not suggesting a single answer (e.g. Crane 1985b; Doyle & Donoghue 1986a, 1992; Loconte & Stevenson 1990; Nixon et al. 1994; Rothwell & Serbet 1994; Doyle 1996; etc.).

In the 1980s and 90s morphological phylogenetic studies suggested that extant seed plants were probably to be placed in five groups: Ginkgo, cycads, conifers, angiosperms, and Gnetales (Gnetum and its relatives Ephedra and Welwitschia). It was often suggested that these were related in a largely pectinate fashion, with Gnetales and a larger or smaller group of fossil gymnosperms/pteridosperms being together sister to angiosperms (e.g. Crane 1985a, b; Doyle & Donoghue 1986a, b; Nixon et al. 1994; Doyle 1996, 1998a, b - Doyle [in Sanderson et al. 2000] notes that this position is well-supported in bootstrap analyses); "gymnosperms" were thus highly paraphyletic, the botanical equivalent of "reptiles". Plants with a heterosporangiate strobilus, the anthophytes, included flowering plants, Gnetales, and also fossil taxa like Bennettitales, while the glossophytes also included the glossopterids. Conifers, cycads, etc., did not seem to be immediately related to flowering plants.

These relationships are now strongly questioned in most analyses of molecular data, and extant gymnnosperms appear to be monophyletic (e.g. Goremykin et al. 1996, Raubeson 1998; Winter et al. 2000; Bowe et al. 2000; Becker et al. 2000, MADS-box gene diversity; Sanderson et al. 2000; Chaw et al. 2000; Pryer et al. 2001a; Magallón & Sanderson 2002, including a summary of the literature; Qiu et al. 2006: support weak; etc.). Many studies suggest that Cycadales may be sister to all other gymnosperms (see Hasebe 1997 for a summary of the early literature). On the other hand, an association of Cycadales and Ginkgoales has also been recovered (Qiu et al. 2006: relationships between Gnetales and Pinales unclear; Raubeson et al. 2006: 61 plastid genes; Wu et al. 2007: 56 cp protein-coding genes; Schmidt & Schneider-Poetsch 2002: Cycadales and Ginkgoales associated, but not sister to all other gymnosperms; Finet et al. 2010; Soltis et al. 2011: weak support; Moore et al. 2011: weak support; Lee et al. 2011: see below). Rai et al. (2003) noted that the two had a reduced rate of molecular evolution in the chloroplast genome and an elevated transition:transversion ratio. It has also been suggested that Gnetales are sister to a clade including all other seed plants (e.g. Sanderson et al. 2000, two genes, but third positions only; Seider et al. 2002, rbcL gene only; Rydin et al. 2002, analysis of nuclear genes only; Rai et al. 2003, large chloroplast data set; Quandt et al. 2004, the trnL intron), gymnosperms being paraphyletic, although this is unlikely (Burleigh & Mathews 2004).

Gnetales are most probably part of a monophyletic gymnosperm group (e.g. Frohlich & Parker 2000, duplication of Floricaula/LEAFY gene; Antonov et al. 2000, cp rDNA ITS; Aris-Brosou 2003), although the distribution of a whole genome duplication (only in cyacds, conifers, and Ginkgo), if confirmed, might suggest that Gnetales are apart from other extant gymnosperms (Barker et al. 2010). Some phylogenies suggest that Gnetales are sister to Pinales (e.g. Samigullin et al. 1999, one gene, not all analyses; Antonov et al. 2000; Sanderson et al. 2000, two genes, first and second positions; Chaw et al. 2000; Gugerli et al. 2001, rather strong support; de la Torre et al. 2006, including ESTs, much hidden support, but not from the chloroplast partition; Wu et al. 2007; on balance, the evidence suggested by Soltis et al. 2002b), or are even to be placed within Pinales, perhaps being associated with Pinaceae in particular (e. g. Chaw et al. 2000; Bowe et al. 2000; Hajibabaei 2003; Burleigh & Mathews 2004; Hajibabaei et al. 2006 [genes from all three compartments, sampling within Pinales not very dense]; Burleigh & Mathews 2007c [supermatrix analyses]; Graham & Iles 2009; Finet et al. 2010, quite strong support; Soltis et al. 2011). Hajibabaei et al. (2006) also found a [Pinaceae + Gnetales] grouping in a variety of analyses where substitution levels were not too high. Qiu et al. (2007) also found a weakly-supported [Gnetaceae, etc. + Pinaceae] grouping. All ndh genes in the chloroplast of Pinus thunbergii are absent - or are present, but as pseudogenes (Wakasugi et al. 1994); recent work suggests that these genes are absent in all Gnetales and Pinales alone in the gymnosperms - again support for the gnepine hypothesis (Braukmann et al. 2009, also 2010; Martín & Sabater 2010). Interestingly, the 5' end of the inverted repeat of Welwitschia has expanded, and its end matches that of the remnant inverted repeat known from Pinus (Margheim et al. 2006; McCoy et al. 2006, 2008). All conifers sampled have but a single complete copy of the chloroplast inverted repeat (Tsudzuki et al. 1992; Strauss et al. 1988), however, not only Gnetales but other seed plants have two copies (Raubeson & Jansen 1992). If Gnetales and Pinales are sister taxa, the evolution of the inverted repeat would involve its expansion in the common ancestor of the two and its subsequent loss in Pinaceae, but there may be problems in such analyses. Burleigh and Mathews (2007a) showed that different topologies were obtained from analyses using single genes or the same number of sites chosen from twelve separate loci, and maximum likelihood and maximum parsimony were susceptible to systematic error in an analysis of a twelve locus data set (Burleigh & Mathews 2007b; see also Chumley et al. 2008; Rydin & Korall 2009). Rydin and Korall (2009 and references) found Gnetales to be sister to all Pinales in a Bayesian analysis, as did Ran et al. (2010) in their study of the evolution of the mitochondrial rps3 gene.... An analysis of variation in 83 plastid genes strongly suggested a set of relationships [Pinaceae [Gnetales + other Pinales]], although other relationships cannot be entirely rejected (Chumley et al. 2008). Zhong et al. (2010: chloroplast protein-encoding genes) recovered a clade [Gnetales + Pinaceae], but only after the fastest-evolving proteins and genes in which there were a number of parallel amino acid substitutions in Cryptomeria and the branch leading to all Gnetales were removed, otherwise, a clade [Cryptomeria + Gnetales] was obtained (for this clade, see also Moore et al. 2011).

Although nearly all Pinales have spirally-arranged ovuliferous scales or modifications of this, Gnetales are distinctive in having strobili with decussating bracts (Magallón & Sanderson 2002); loss of the ovuliferous scale, etc., would then be apomorphies (Finet et al. 2010). Nevertheless, there are some morphological similarities between the Pinales and Gnetales, and within the former, perhaps particularly with Pinaceae (see also Mundry & Stützel 2004). Rydin and Friis (2005) suggested that shedding of the exine during the germination of the microgametophyte might be a synapomorphy for the extended group, although there would be a number of reversals. However, the possibility of the paraphyly of the Pinales as delimited here has also been strongly questioned (Rydin et al. 2002), while Raubeson et al. (2006) found a grouping of Welwitschia with Podocarpus (this may be due to rate heterogeneity).

All this being said, based on the patterns of duplication of PHY genes - and the assumption that they are not lost - Schmidt and Schneider-Poetsch (2002) had suggested that within the gymnosperms Gnetales were sister to the rest since they had fewer duplicated genes (but see above); an early maximum parsimony analysis of Samigullin et al. (1999) had found a similar position. Indeed, a recent analysis of a large amounts of nuclear gene data from 101 genera of seed plants also suggests that Gnetales are sister to all other gymnosperms, and that Ginkgo and Cycadales are also sister groups (Lee et al. 2011: see also Cibrián-Jaramillo et al. 2010: most data from ESTs, much missing). Lee et al. (2011) discuss character evolution in the context of the distinctive topology they found, suggesting that "motile male gametes would be independently and uniquely evolved (apomorphic) in cycads plus Ginkgo, and loss of motile male gametes in Gnetales would would be ancestral in the gymnosperms (plesiomorphic)." (ibid., p. 2). From this point of view, and disregarding fossils, such a loss would be an apomorphy for [angiosperms + gymnosperms], and there would need to be a mechanism that would allow the restoration of motility to male gametes of cycads, e.g. regaining flagellae, etc. At the same time other character evolution interpreted in the context of this tree still need not be the same as in the Anthophyte hypothesis (cf. Lee et al. 2011). Even if this topology holds up, simple parsimony may be a rather blunt instrument to use when thinking of character evolution.

However, on balance, the evidence points to a [Pinaceae + Gnetales] clade - and that will entail the demise of Gnetales. Wherever Gnetales are to be placed, they will be a very derived group; here they are kept on a separate page, although movement into Pinales is likely soon. And for the implications of all this for angiosperm evolution, see

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.

Because of the probable sister group relationship between extant gymnosperms and angiosperms, many life cycle characteristics cannot be polarised. However, it is very likely that many of the features of gametophyte and young sporophyte that characterize gymnosperms are likely to be features of the extant seed plants as a whole. Some features that characterise angiosperms also may properly be pegged as characteristic of seed plants as a whole; an example may be successive microsporogenesis with the microspore walls developing by centripetal furrowing (Nadot et al. 2008).

Evolution. Divergence & Distribution. Early estimates of the age for crown-group seed plants range from 348-285 million years before present (Becker et al. 2000; Leebens-Mack et al. 2005). Recent molecular estimates of the age of extant seed plants/Spermatophyta are somewhat older, ranging from (356-)327(-296) million years (with eudicot calibration) to (366-)330(-301) million years (without: Smith et al. 2010, see also divergence-time estimates in their table S3), while Davies et al. (2011: 95% credibility intervals) suggested a somewhat older age of (368-)351(-330) million years.

Pollination Biology & Seed Dispersal. The seed, the next generation sporophyte more or less surrounded by reserve tissue and in turn surrounded by the seed coat, which is of integumentary origin, differs from the megaspores of heterosporous pteridophytes and lycophytes in several respects. One is that the seed is much larger than the ovule, the seed precursor, which can be aborted easily if pollination does not occur (Haig & Westoby 1989), and another is that seeds themselves are very variable in size, ranging in size from 10^-7 to 10⁴ grams, i.e. smaller than megaspores to massively larger than them (Haig & Westoby 1991).

Chemistry, Morphology, etc. For general information see Gifford and Foster (1988), Hill (2005) and Anderson et al. (2007: including fossils), for ovules and seed anatomy, inc. that of fossils, see Shnarf (1937), leaf anatomy, see Napp-Zinn (1966), for the shoot apex, see Johnson (1951), for the binding of ferulic acid to the primary cell wall, see Carnachan and Harris (2000), for the relationship between the roots of lycophytes and those of of lignophytes (apparently quite different), see Gensel and Berry (2001) and Gensel et al. (2001), for stelar morphology and evolution, see Beck et al. (1982: the characterisation of the stele and other details of stem anatomy above are taken from there), for nodal anatomy in extant and fossil seed plants, see Kumari (1963: Lyginopteris, Heterangium and Archaeopteris all have but a single leaf trace coming from the central stele, even although the leaves themselves may be large) and Galtier (1999), for a discussion on the evolution of megaphylls, see Sporne (1965), Schneider et al. (2009), Tomescu (2009), Galtier (2010), etc., for venation density, see Boyce et al. (2008), for sieve element plastids, see Behnke (1974) and Behnke and Paliwal (1973), for stomatal morphology, see J. A. Doyle et al. (2008b), and for cuticle waxes and their composition, see Wilhelmi and Barthlott (1977). For pollen, including the lamellate endexine, see van Campo (1971), van Campo and Lugardon (1973), Thomas and Spicer (1986), Xi and Wang (1989), Faegri and Iversen (1989), Page (1990), Osborn and Taylor (1994) and Kurmann and Zavada (1994); for variation in the life cycle and embryology, see Saxton (1913), and in particular Singh (1978); for the integument and its possible evolution, see Andrews (1963); for reports of double fertilisation (really well attested only in Gnetales), see Friedman (1992); for plastid transmission, understood fairly well in only two taxa (Encephalartos and Ephedra, Ginkgo being uncertain) outside Pinales, see Moussel (1978 - Ephedra), Chesnoy (1987), Neale et al. (1991), and Wilson and Owens (2006: these last three Pinales), Mogensen (1996 - summary), Cafasso et al. (2001 - Encephalartos); for male gametophyte development, see Williams (2008), for the female gametophyte, see Maheshwari and Singh (1967); for the evolution of embryo size, see Forbis et al. (2002); for the mitochondrial nad1 intron 2, see Gugerli et al. (2001); for LEAFY gene duplication, see Frohlich and Parker (2000), for the phytochrome gene (PHY) duplication, see Mathews and Sharrock (1997), Donoghue and Matthews (1998), Mathews et al. (2003), Schmidt et al. (2002), and Matthews (2010), for the PEBP gene family duplication, see Karlgren et al. (2011), and for the nuclear ribosomal DNA, see Wicke et al. (2011); for the mitochondrial genome, see Chaw et al. (2008 - Y. L. Qiu suggested that how mitochondrial introns are spliced [cis or trans] might be of systematic significance, see Cameron et al. 2003), and for pollination, see Stützel and Röwekamp (1999b). For general information about possible morphological apomorphies, see Doyle (1998a, and especially 2006).

EXTANT GYMNOSPERMS / PINOPHYTA / ACROGYMNOSPERMAE  Back to Main Tree

Biflavonoids +; cuticle wax tubules with nonacosan-10-ol; ferulic acid ester-linked to primary unlignified cell walls; side wall pits in tracheids circular, bordered, with tori; phloem with sieve and Strasburger cells, the sieve area with small pores generally less than 0.8 µm across that have cytoplasm and E.R., joining to form a median cavity in the region of the middle lamella; stomata perigenous, stomatal poles raised above pore, no outer stomatal ledges or vestibule; ± tracheidal transfusion tissue +; plants dioecious; microsporophylls and megasporophylls forming determinate strobili/cones; pollen tectate, infratectum alveolate [esp. saccate pollen], endexine lamellate at maturity; ovule unitegmic, with pollen chamber [developing by breakdown of nucellar cells], apex of nucellus massively thick; pollination droplet +, fertilisation 7 days to 4-6 months or more after pollination, pollen germinates in two or more days, tube, branched, haustorial, growing away from ovule at 1³-10(-20) µm/hour, breaks down sporophytic cells, wall of cellulose microfibrils, male gametophyte of two prothallial cells, a tube cell, and an antheridial cell producing a sterile cell and two multiflagellate gametes, zooidogamy, male gametes released by the breakdown of the pollen grain wall; female gametophyte monosporic, with radially-elongated cells [alveoli] that grow centripetally, the nucleus being on the open face and connected to adjacent nuclei by spindle fibres; seed fleshy, testa mainly of coloured sarcoexotesta and scleromesotesta, ± vascularized, and ± degenerating endotesta, ± vascularized; chromosomes of male and female gametes line up on separate but parallel spindles in first zygotic nuclear division, proembryo with many free-nuclear divisions; gametophyte persists in seed; genome size [1C value] intermediate, 3.5-14 pg; two copies of LEAFY gene and three of the PHY gene, [PHYP [PHYN + PHYO]], second intron in the mitochondrial rps3 gene.

Much of this characterisation may apply to all extant seed plants (see above), with more detail to be added if extant gymnosperms are paraphyletic, although this now seems increasingly unlikely.

Evolution. Divergence & Distribution. Recent molecular estimates of the crown age of this clade range from (313-)301(-293) million years old (with eudicot calibration) to (316-)302(-294) million years (without: Smith et al. 2010, see also Table S3), while Davies et al. (2011: 95% credibility intervals) suggested a somewhat older age of (337-)316(-306) million years.

Chemistry, Morphology, etc. It is possible that the secondary wall of tracheary tissue in extant seed plants, more or less homogeneous, lignified and resistant, differs from that in monilophytes and lycophytes where there is a core of degradation-prone material (Cook & Friedman 1998; Friedman & Cook 2000); this distinctive feature of seed plant cell walls is a possible apomorphy for them. Where to put pits with a margo-torus structure on the tree is unclear (see Bauch et al. 1972 for pit membrane variation in gymnosperms); here their origin is placed within the gymnnosperm clade (they are also found in a few angiosperms). Microfilament-rich peripheral phloem cells may be restricted to this clade (Pesacreta 2009). It has been suggested that E.R associated with phloem sieve areas may expand if damaged, so blocking flow through the sieve tube (Evert 1990; Schulz 1992 and references). The nucleus in mature phloem cells of all(?) gymnosperms is degenerated and its pycnotic (cf. angiosperms where the nucleus is usually chromolytic: e.g. Behnke 1986). For transfusion tissue, which may look very sclereidal (it even consists of astrosclereids in Sciadpopitys), but which has bordered pits and functions in water tansport, see Hu and Yao (1981: little information from Cycadales) and Brodribb et al. (2007). I have found few records of cork cambium initiation in the gymnosperms.

Although gymnosperm pollen can be divided into grains with an alveolate and those with a granular infratectal layer, the former often also being saccate grains, the distinction may perhaps not be that sharp; some Pinaceae seem to have some basal granules in their otherwise alveolate infratectum (Kurmann 1992). For a standardized terminology of the cells formed during male gametophyte development, see Fernando et al. (2010). Features like heterospory have clearly evolved several times in land plants; in seed plants, the dividing megaspore receives its nutrition from the parental sporophyte, whereas in other heterosporous land plants megaspore development is independent of the parent. In a number of gymnosperms, including Cycadales, Taxaceae, Gnetum, etc., the ovules have a nucellar cap (Singh 1978).

The process of cellularisation of the gymnosperm embryo is apparently similar to that in the endosperm of flowering plants (Fineran et al. 1982 and references). For the interpretation of embryo development, in particular, whether the young embryo is tiered or not, and how the secondary suspensor develops, see Doyle (2006). "Cap cells" at the apical/internal end of the proembryo seem widespread in gymnosperms; these do not persist (Owen et al. 1995c).

Extant gymnosperms have genomes of intermediate sizes compared to those of other seed plants, C values being ca 3.5-14 picograms (Leitch et al. 2001, 2005), although those of a few Pinales are somewhat larger (to 35 pg). For the duplication of the phytochrome gene, see Schmidt and Schneider-Poetsch (2002): although Gnetaceae appear to have only two copies, it is possible that one has been lost. Endopolyploidy has not been reported in this clade (Barow & Jovtchev 2007).

For additional information, see the references in the preceding section, also for ovules and seeds, see Schnarf (1937), for details of the cellular organization of the shoot apex, see Johnson (1951), for seed lipids, see Wolff et al. (1999), and for the rps3 gene, see Ran et al. (2010).

Phylogeny. There are some suggestions from analyses of molecular data of a sister taxon relationship between Ginkgoales and Cycadales (see above). If this is confirmed, the following are features that the two have in common:

Ginkogoales + Cycadales: plants dioecious; pollen tube branched, growing away from the ovule, spermatogenous cells delimited by circular anticlinal wall, zooidogamy, male gametes with cell wall, released from the swollen proximal part of the tube, flagellae numerous; seeds with coloured sarcoexotesta, scleromesotesta, and ± degenerating endotesta; germination cryptcotylar.

Classification. For a linear sequence of gymnosperms, see Christenhusz et al. (2011c).

CYCADALES Dumortier  Main Tree, Synapomorphies.

Roots and stems with contractile tissue; ß-methylamino-L-alanine and compounds producing methylazoxymethanol +, polysaccharide gums/mucilage copious, in canals; association with Nostoc or Anabaena in apogeotropic coralloid roots [cork cambium in these roots, at least, superficial], root hairs 0; primary thickening meristem +; wood manoxylic, large amounts of secondary phloem persisting; reaction wood 0; tranfusion tissue +; nodes [of foliage leaves] multilacunar, traces girdling; protoxylem poles changing from endarch in the stem to exarch in the leaf traces; (inversely oriented bundles in the periphery of the pith); petiole vascular bundles inverted omega shape; leaf vascular bundles amphicribral; epidermal cells with perforations; axillary buds 0; leaves large, pinnate; cataphylls +; sporangia abaxial; microsporangia in synangia, many abaxial microsporangia/sporophyll, dehiscing by the action of the epidermis [exothecium]; megasporophylls with terminal sterile portion; ovule with free integument only in apical portion; pollen tube wall with abundant pectins, one prothallial cell, generative cell delimited by circular anticlinal wall; seed with sarcotesta and inner fleshy layer, both vascularized; germination hypogeal, seedling cryptocotylar, coleorhiza +; mitochondrial nad1 intron 2 and coxIIi3 intron and trans-spliced introns present, one duplication in the PHYO gene group. - 2 families, 10 genera, 305 species.

Evolution. Divergence & Distribution. Cycads are known as fossils in the Upper Palaeozoic 290-265 million years before present, probably being derived from Palaeozoic pteridosperms (Mamay 1969; Gao & Thomas 1989), and they were particularly diverse in the Jurassic-Cretaceous period. The Cycas lineage may already have diverged from Zamiaceae by the Permian at least 250 million years before present (Hermsen et al. 2006a; see also Bogler & Francisco-Ortega 2004) - alternatively, it has been suggested that Cycas may have diverged from Zamiaceae only ca 92 million years before present, with diversification within the clade occurring ca 36 million years before present (see Wink 2006; Treutlein & Wink 2002; Nagalingum et al. 2009). Indeed, diversification of clades in the whole order may have occured more or less synchronously in the late Miocene, a mere 12 million years or so ago (Nagalingum et al. 2011; see also Crisp & Cook 2011), although dispersal across more or less continuous land had been invoked to explain the scattered distribution of species of Cycas with propagules that could not float (Dehgan & Yuen 1983).

And why are there so few cycads? Olsen and Gorelick (2011) suggest that there is no evidence of whole genome duplication in the clade (or in Ginkgo), and this might reduce the amount of speciation and also curtail various developmental changes, but it seems that the venation density of the leaves, absence of axillary branching, and a variety of other features might equally reasonably be invoked... And anyhow, there have been much more recent bouts of speciation (Nagalingum et al. 2011); perhaps extinction has been higher in gymnosperms in general than in angiosperms (Crisp & Cook 2011).

Bacteria/Fungal Associations. The nitrogen-fixing cyanobacteria Nostoc and Anabaena are probably to be found in all cycads. They grow either inter- or intracellularly in the apogeotropic coralloid roots that are found the surface of the soil (e.g. Lindblad et al. 1985); actual fixation of nitrogen has been demonstrated (Vessey et al. 2004 and references), and it is translocated to the host as citrulline and glutamine, or sometimes just as the latter (Costa & Lindblad 2002). In Austalian species of Macrozamia, at least, several species of Nostoc are involved and there is no host specificity (Gehringer et al. 2010). Interestingly, the toxic ß-methylamino-L-alanine (BMAA) is probably produced by the cyanobacterial associates of cycads (Cox et al. 2005).

Pollination Biology & Seed Dispersal. There are widespread, close and specific associations between Zamiaceae and their beetle (often weevil) and thrip pollinators (e.g. Stevenson et al. 1998b; Schneider et al. 2002; Terry et al. 2007). In Cycas the beetle larvae eat the male cones, and hasten the reproductive process as they do so (Marler 2010). It seems likely that in their present form these associations are relatively recent (Downie et al. 2008); wind pollination may also occur (Kono & Tobe 2007; Suinyoy et al. 2009: Cucujoidea also involved). Indeed, the development of such pollination associations may even have contributed to the relatively recent diversification of some of the cycad clades like Encephalartos, Macrozamia etc., in the (late) Tertiary (Oberprieler 2004; see also Downie & Donaldson 2005: divergence within Zamiaceae is dated to ca 94 million years before present; Wink 2006; esp. Nagalingum et al. 2011). Thermogenesis has been detected in the strobili of some Cycadales (Seymour 2001).

Animal dispersal of the seeds - they are large, often brightly coloured, and have a fleshy outer layer - is likely for most genera.

Plant-Animal Interactions.A few lepidopteran larvae eat cycads, in particular the lycaenid Eumaeus (Schneider at al. 2002 for references), although in S.E. Africa a group of brightly-coloured diptychine geometrids (loopers) is more or less restricted to cycads (Cooper & Goode 2004); it would be interesting to know if they are distasteful to potential predators.

Cycads are noted for having some rather potent toxins that, it has been suggested, may have contributed to the persistence of the clade. ß-methylamino-L-alanine (BMAA) is widespread, as is methylazoxymethanol (MAM), produced by the hydrolysis of glycosides such as cycasin (a monosaccharide) and macrozamin (with a disaccharide). BMAA, probably produced by the cyanobacterial associates of cycads (Cox et al. 2005), is a possible neurotoxin, and MAM can cause severe digestive upsets, cancers, etc. (Brenner et al. 2003 and references).

Chemistry, Morphology, etc. Note that much of the literature on "cycads" includes information on members of both families. Hermsen et al. (2006a) suggest a number of additional synapomorphies for Cycadales, including the presence of pith cell packets and three unique biflavones. The roots lack pith, the vascular tissue is (2-)4(-8)-arch and the xylem is exarch. Roots may have both superficial and deep-seated cork cambium (Pant 1973); the former may be paricularly well developed in the coralloid roots and may be connected with the reported absence of root hairs in cycads (Vessey et al. 2004). Perhaps associated with the development of a primary thickening meristem, the shoot apex is notably wide, being 500-3,300 µm across (Clowes 1961). Ryberg et al. (2007) emphasise the large amounts of secondary phloem that persist in a cycad stem, presumably because the cork cambium is not very active; some larger cycads have fibres in tangential bands in this phloem. The traces to cataphylls and sporophylls take a direct course through the cortex, and some traces may also proceed directly to the expanded leaves; nodal anatomy appears to be complex (Pant 1973). The leaf traces become mesarch or are endarch near the base and exarch in the upper portions (Chamberlain 1935). Coulter and Chamberlain (1917) described the vascularisation of the young leaves of Ceratozamia; the cotyledons have split lateral vascular traces. There is transfusion tissue in the leaf.

In their study of microspangiophore development in Zamia, Mundry and Stützel (2003) found that the sporangia developed on a lateral lobe of the microsporophyll, consistent with the individual units of the pollen cones being basically pinnate in construction, and they suggested a link to medullosan pteridosperms; this morphology is unlike that of other extant gymnosperms (Mundry & Stützel 2004b). The tapetum plays no part in the formation of the sporoderm. There are up to perhaps 40,000 flagellae per male gamete!

For embryology, see Singh (1978), branching, see Stevenson (1988), for fossils, see Pant (1987), and for a coleorhiza in the seedling, see Robbertse et al. (2011). There are several excellent general references, including Gifford and Foster (1988), Johnson and Wilson (1990), Stevenson (1990), Norstog and Nicholls (1997: I have used this a great deal), and Schneider et al. (2002: the biology and evolution of the group); Artabe and Stevenson (1999) suggest a number of possible apomorphies, and also discuss variation in a number of anatomical features within the order. See the Gymnosperm Database for general information.

Phylogeny. Given the uncertainty in our knowledge of the relationships between the five major seed-plant clades, direct links are provided to the four others from here: Cycadales, Gnetales, flowering plants or Magnoliophyta , and Pinales; general discussion under seed plant evolution.

For relationships within cycads, see e.g. Treutlein and Wink (2002: rbcL), Rai et al. (2003, 2008b), K. D. Hill et al. (2003, 2004), Bogler and Francisco-Ortega (2004) and Wink (2006). Cycas is sister to other cycads, although other details of relationships in the clade are rather unclear (support mostly low) and conflict in part, at least, with those suggested by previous morphological studies; the positions of Bowenia, Stangeria (the two have sometimes been associated, as by Stevenson 1992 in a morphological analysis [and placed in Stangeriaceae], see also Brenner et al. 2003), and Dioon are particularly uncertain; all three are distinctive genera. Such relationships are consistent with variation in the micromorphology of the cuticular waxes (Wilhelmi & Bartlott 1997), Dioon and Cycas having a plesiomorphic micromorphology.

Hill et al. (2003) provide a useful list of characters varying within Cycadades (see also Hermsen et al. 2006a).

Classification. There are good morphological characters supporting the basal division of the order into two families (K. D. Hill et al. 2003), while relationships within the larger clade (Zamiales) are still somewhat unclear, even if families have been proposed in the past based on relationships that now seem to be unlikely. Thus a conservative (broad) approach to family limits has been taken here - the whole order is not very big. Jones (2002) gives an account of all taxa while Walters and Osborne (2004) focuses on problems of species delimitation, etc. Hill et al. (2004) gives a list of taxa included here. There is a useful website with information on Cyadales, The Cycad Pages (Hill && Stevenson 2002 onwards).

Includes: Cycadaceae, Zamiaceae.

Synonymy: Cycadineae D. W. Stevenson, Zamiineae D. W. Stevenson, Dioales Doweld, Stangeriales Reveal, Zamiales Burnett - Cycadidae Gorozh., Zamiidae Doweld - Cycadopsida Brongniart, Zamiopsida Endlicher - Cycadophytina Reveal - Cycadophyta Bessey - Cycadophytanae Doweld

CYCADACEAE Persoon Back to Cycadales

Lignins lacking syringaldehyde [Mäule reaction negative]; hairs transparent; stem polyxylic; leaflets circinate, bases persistent, midrib +, secondary vasculature diffuse; megasporophylls not forming a determinate cone, margins lobed or toothed; ovules (1-)3-8/sporophyll, erect; seeds platyspermic; n = 12; tenfold increase in mitochondrial tandem repeat sequences, Bpu mobile sequences.

1/100. E. Africa and Madagascar, South East Asia to New Caledonia and Tonga (map: from Jones 2002). [Photo - Cycas megasporophyll.]

Seed Dispersal. Most species of Cycas probably have animal-dispersed seeds, and species distribution ranges are narrow; a few species like C. circinalis have larger seeds with spongy tissue and that can float; such species often have broader distributions (Dehgan & Yuen 1983).

Chemistry, Morphology, etc. For the distinctive mitochondrial genome of Cycas, which may even include some self-replicating elements, see Chaw et al. 2008).

ZAMIACEAE Horaninow Back to Cycadales

Lignins with syringaldehyde [Mäule reaction positive]; (stem polyxylic); hairs coloured; leaflets flat (circinate - Bowenia), no midrib (Stangeria +), secondary veins regular, subparallel; megasporophylls forming a determinate cone, peltate; ovules 2(-3)/sporophyll, inverted; seeds radiospermic; n = 8, 9, 13 (Zamia variable).

9-10/200: Encephalartos (65), Zamia (55), Macrozamia (40). Scattered throughout the tropics and subtropics (map: from Jones 2002). [Photo - Encephalartos, Zamia.]

Evolution. Chaw et al. (2005) also suggest apomorphies for Zamiaceae and some clades within it.

Chemistry, Morphology, etc. Stangeria is perhaps particularly distinctive: it develops buds from its roots, it lacks cataphylls, and its leaflets have dichotomously-branching pinnate venation. Stomata are to be found at the apex of the nucellus in Zamia, perhaps reflecting a time when the nucellus - really the wall of the megasporangium - was exposed. Microcycas produces multiple spermatozoids per male gametophyte and there are several - even hundreds - of ovules on each female gametophyte.

Phylogeny. A recent study (Chaw et al. 2005, see also Rai et al. 2003; Zgurski et al. 2008) suggests the following quite well supported relationships within Zamiaceae: [Dioon [Bowenia (not always here) [the rest - including Stangeria which is never close to the first two]]]. For relationships within Encephalartos, which may have split from Lepidozamia as recently as 5-20 million years before present, see Treutlein et al. (2005).

Classification. Chaw et al. (2005) suggest a realignment of generic limits throughout Zamiaceae.

Synonymy: Boweniaceae D. W. Stevenson, Dioaceae Doweld, Encephalartaceae Doweld, Microcycadaceae Tarbaeva, Stangeriaceae L. A. S. Johnson