SEED PLANT EVOLUTION (still being developed)

Sister to the monilophytes, ferns and their relatives, are the lignophytes, and the split between the two is old, occuring mid- to later Devonian, some 375-400 million years before present (Pryer et al. 1995, 2000, 2001a, 2004; Schneider et al. 2002). Lignophytes have distinctive secondary thickening, a vascular cambium which is bifacial, producing secondary phoem externally and secondary xylem internally (e.g. see Donoghue 2005). Thus lignophytes often have stems with large amounts of wood, and there is also 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).

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, but seed plants or spermatophytes in general are characterised by heterospory, a single megaspore per sporangium, and the presence of an integument (Kenrick & Crane 1997). 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. It 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. Some Archaeopteridales, from ca 365 million years before present, have a lagenostome and probably pollination/fertilisation mechanisms more like those of other seed plants.

Seeds of Mesozoic seed plants are very diverse in their morphology (e.g. Anderson & Anderson 2004), and Bennettitales (apparently close to Gnetales, see that page), 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. Indeed, by the lower Carboniferous there were to be found the rather conifer-like Cordiatales, which had compound pollen-bearing structures and saccate pollen, and slightly later, the still more conifer-like ("ancestral") Voltziales.

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, the coniferophytes, include 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 (see below). 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.

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 such cases is often called prepollen, having proximal rather than distal germination and haptotypic marks (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, are not well understood. A distinction is sometimes made 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.

However, these relationships are now strongly questioned in most analyses of molecular data, and the 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). 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). 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. Based on the patterns of duplication of PHY genes - and the assumption that they are not lost - Schmidt and Schneider-Poetsch (2002) suggested that within the gymnosperms Gnetales were sister to the rest since they had fewer duplicated genes (but see below; maximum parsimony analysis of Samigullin et al. 1999 gave a similar position). 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 perhaps unlikely (Burleigh & Mathews 2004).

Gnetales are most probably part of a monophyletic gymnosperm group (e.g. Frohlich & Parker 2000, duplication of Floricaula/LEAFY; Antonov et al. 2000, cp rDNA ITS; Aris-Brosou 2003). Some phylogenies suggest that they 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, in particular being associated with Pinaceae (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]). This last study 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. Interestingly, the 5' end of the inverted repeat of Welwitschia has expanded, and its position matches that of the remnant inverted repeat known from Pinus (Margheim et al. 2006; McCoy et al. 2006). All conifers sampled have but a single copy of the chloroplast inverted repeat (Strauss et al. 1988), but 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. However, 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). It has also been suggested that conifers + Gnetales are immediate relatives, and perhaps sister to flowering plants (e.g. Friedman & Floyd 2001; Gerrath et al. 2002 [distribution of phi thickenings in the root cortex]).

Although nearly all Pinales have an ovuliferous scale or modifications of this, Gnetales are distinctive in having strobili with decussating bracts (Magallón & Sanderson 2002). Nevertheless, there are some morphological similarities between the Pinales and Gnetales, and within the former, perhaps particularly with Pinaceae (see also Mundry & Stützel 2004). However, the possibility of the paraphyly of the Coniferales 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). Indeed, angiosperm characters apparently found also in Gnetum and its relatives (see above) are for the most part morphologically different and are clearly parallelisms. Thus the sieve areas in the phloem cells are very like those of other gymnosperms and unlike those of angiosperms (Behnke 1990a), the vessels in the two develop differently (e.g. Carlquist 1996), the tunica has only a single layer, etc. (e.g. Donoghue & Doyle 2000; Doyle 2006). Similarly, the reaction wood in Gnetum consists of gelatinous extra-xylary (reaction) fibers in the adaxial position - i.e., it is unique among seed plants (Tomlinson 2001b, 2003; see also Höster & Liese 1966), and is unlike the tension wood of angiosperms. Wherever Gnetales are to be placed, they seem to be a very derived group; here they are kept on a separate page.

Despite the strong suggestion from analyses of molecular data that Gnetales have no immediate or even particularly close relationships with flowering plants, the issue is not yet entirely closed (Rydin et al. 2002: Friis et al. 2007). In particular, analyses of morphological data that include fossil taxa continue to suggest that gymnosperms are paraphyletic, the four main groups being independently derived from a pteridosperm grade, with Gnetales close to angiosperms and often associated with Bennettitales (see also detailed studies of seeds: Friis et al. 2007), etc. However, bootstrap support for these relationships is very low (Doyle 2006; Hilton & Bateman 2006), as it was for the original anthophyte clade. Interestingly, rather than carrying out an independent morphological study, Doyle (2006) himself proceeded to think of seed plant evolution in the context of a morphological analysis that is constrained by a molecular topology in which Gnetales are nested within gymnosperms (he noted that this is in fact almost as parsimonious as if Gnetales were linked with angiosperms). Hilton and Bateman (2006), on the other hand, allow only a slight possibility that their morphology-based tree could be superseded (see also Farjon 2007). This argument, morphology with/without better/worse than molecules, is independant of group being studied (see e.g. Springer et al. 2007 for mammals).

Very recently it has been found that the triterpenoid oleanane is found pretty much throughout angiosperms, although not in all, and in Bennetitales, in the Permian Giganopteridales (remember, vessels here, too!), but not in any extant gymnosperms, consistent with a divergence of the angiosperm stem group from other seed plants by the late Paleozoic (Taylor et al. 2006). 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), and this will help us to understand the phylogeny of this whole area (see also evolution of angiosperms).

Although long-branch attraction involving the branch leading to angiosperms (Rydin & Källersjö 2002; Stefanovic et al. 2004) may affect the results of these molecular studies, especially the position of Gnetales, it is very hard to deal with given the paucity of extant gymnosperm taxa (see also Hilton & Bateman 2006 for sampling in the context of morphological versus molecular phylogenies; Bateman et al. 2006b for much else besides). It is unclear which extant taxon might break up the branch, and knowledge of fossils will need to be much improved for a phylogeny whose topology is determined by fossils to be convincing (e.g. see above).

Hence ideas of relationships between seed plants remain somewhat in limbo. In particular, it is unclear which seed plant fossils are stem-group angiosperms. These plants will, of course, be largely gymnospermous in their morphologies, some kind of seed fern, regardless of whether extant gymnosperms are monophyletic or paraphyletic. The most promising candidates for relatives of angiosperms include Corystospermales (Pteruchus, Ktalenia, etc. - see the mostly male theory of flower evolution, see Frohlich & Parker 2000), Bennettitales (close to Gnetales), and Caytoniales. I have set up the synapomorphy scheme below in a way that I hope allows one to understand possible synapomorphies whatever the real relationships are, however, I think it unlikely that Gnetales have anything immediately to do with flowering plants. If extant gymnosperms are monophyletic, as is seeming more likely, then loss of sperm flagellae and the associated development of a pollen tube, etc., will represent parallelisms between extant gymnosperms and the clade ancestral to angiosperms...

EXTANT SEED PLANTS

Plant woody, evergreen; nicotinic acid metabolised to trigonelline; primary cell walls rich in xyloglucans and/or glucomannans, 25-30% pectin [Type I walls]; lignins rich in guaiacyl units; true roots present, xylem exarch; shoot apical meristem complex; arbuscular mycorrhizae +; stem with ectophloic eustele, endodermis 0, xylem endarch; vascular tissue in t.s. discontinuous by interfascicular regions; vascular cambium + [xylem ("wood") differentiating internally, phloem externally]; wood homoxylous, tracheids +; tracheid/tracheid pits circular, bordered; sieve tube/cell plastids with starch grains; phloem fibers +; stem cork cambium superficial, root cork cambium deep seated; nodes ?; leaf vascular bundles collateral; leaves spiral, simple, axillary buds?, prophylls [including bracteoles] two, lateral; plant heterosporous, sporangia eusporangiate, on sporophylls, sporophylls aggregated in indeterminate cones/strobili; true pollen [microspores] +, mono[ana]sulcate, pollen exine and intine homogeneous, ovules unitegmic, crassinucellate, megaspore tetrad tetrahedral, only one megaspore develops, megasporangium indehiscent; male gametophyte development endo/exosporic, gametes two, with cell walls; 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 duplication, mitochondrial nad1 intron 2 and coxIIi3 intron present.

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).

I have found few records of cork cambium initiation in the gymnosperms. 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). 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. 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). A number of gymnosperms have a nucellar cap; these include Cycadales, Taxaceae, Gnetum, etc. (Singh 1978). 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 a few Pinales are somewhat larger (to 35 pg).

For general information see Gifford and Foster (1988) and Hill (2005), for 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 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 at coming from the central stele, even although the leaves themselves may be large), 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 sieve element plastids, see Behnke (1974) and Behnke and Paliwal (1973), and for cuticle waxes and their composition, see Wilhelmi and Barthlott (1977). For pollen, especially the alveolate infratectal layer of the ectexine and 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 the evolution of embryo size, see Forbis et al. (2002); for the mitochondrial nad1 intron 2, see Gugerli et al. (2001); for LEAFY duplication, see Frohlich and Parker (2000); for the phytochrome gene (PHY) duplication, see Donoghue and Matthews (1998) and Schmidt et al. (2002); and for pollination, see Stützel and Röwekamp (1999b). For general information about possible morphological apomorphies in particular, see Doyle (1998a, and especially 2006).

EXTANT GYMNOSPERMS/PINOPHYTA  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 pores joining to form median cavity in the region of the middle lamella; stomata haplocheilic; transfusion tissue +; microsporophylls and megasporophylls forming determinate strobili/cones; pollen tecate, infratectum alveolate [esp. saccate pollen], endexine lamellate at maturity; ovule unitegmic, with pollen chamber [developing by breakdown of nucellar cells]; pollination droplet +, fertilisation 4-6 months or more after pollination, pollen tube breaks down sporophytic cells and grows away from ovule, male gametophyte of two prothallial cells, tube cell, stalk/sterile cell, and two multiflagellate gametes, zooidogamy, male gametes released from the swollen proximal part of the tube; female gametophyte monosporic, with radially-elongated cells [alveoli]; testa mainly of coloured sarcoexotesta and scleromesotesta, ± vascularised, 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.

Note that much of this characterisation may apply to all extant seed plants (see above), with more detail to be added if extant gymnosperms are paraphyletic.

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.

There are some suggestions from analyses of molecular data of a sister taxon relationship between Gnetales 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.

CYCADALES Dumortier  Main Tree, Synapomorphies.

Roots and stems with contractile tissue; ß-methylamino-L-alanine and compounds producing methylazoxymethanol +, 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 +; plants dioecious; sporangia abaxial; microsporangia in synangia, many abaxial microsporangia/sporophyll, dehiscing by the action of the epidermis [exothecium], ektexine alveolate; megasporophylls with terminal sterile portion; pollen tube usually branched, growing away from the ovule, one prothallial cell, spermatogenous cells delimited by circular anticlinal wall; seed with sarcotesta and inner fleshy layer, both vascularized; germination cryptocotylar, coleorhiza +; mitochondrial nad1 intron 2 and coxIIi3 intron present, one duplication in the PHYO gene group. - 2 families, 10 genera, 305 species.

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

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 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). (On the other hand, it has been suggested that Cycas may have diverged from Zamiaceae ca 92 million years before present, with diversification within the clade occuring ca 36 million years before present - see Wink 2006; Treutlein & Wink 2002). There are widespread, close and specific associations between Zamiaceae and their beetle (weevil) and thrip pollinators (e.g. Stevenson et al. 1998b; Schneider et al. 2002), although it seems likely that in their present form these are relatively recent (Downie et al. 2007); the development of such 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: divergence within Zamiaceae is dated to ca 94 million years before present - Wink 2006). Cycadaceae may be wind pollinated, but pollination by beetles may also occur (Kono & Tobe 2007). 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 idf they are distasteful to potential predators. Thermogenesis has been detected in the strobili of some Cycadales (Seymour 2001).

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, interestingly, is also probably produced by the cyanobacterial associates of cycads (Cox et al. 2005). It is a possible neurotoxin, and MAM can cause severe digestive upsets, cancers, etc. (Brenner et al. 2003 and references).

In their study of microspangiophore development in Zamia, Mundry and Stützel (2003) found that the sporangia developed on a lateral lobe or the microsporophyll, consistent with the individual units of the pollen cones being basically pinnate in construction, and they suggested a link to medullosan pteridosperms.

Hermsen et al. (2006a) suggest a number of additional synapomorphies, 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. Perhaps associated with the development of a primary thickening meristem, the shoot apex is notably wide, being 500-3,300 µm across (Clowes 1961). 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. The tapetum plays no part in the formation of the sporoderm. There are up to perhaps 40,000 flagellae per male gamete!

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 fibers in tangential bands in this phloem. Both characters are common in the Bennettitales, which with the Cycadales make up the cycadophytes.

For relationships within cycads, see e.g. Treutlein and Wink (2002: rbcL), Rai et al. (2003), 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. There are, however, good morphological characters supporting the basal division (K. D. Hill et al. 2003), so a conservative (broad) approach to family limits has been taken here - the whole order is not very big. A very recent study (Chaw et al. 2005, see also Rai et al. 2003) suggests the following quite well supported relationships within Zamiaceae: [Dioon [Bowenia [the rest - Stangeria not close to the first two]]]; this is consistent with variation in the micromorphology of the cuticular waxes (Wilhelmi & Bartlott 1997), Dioon and Cycas having plesiomorphic morphology. Chaw et al. (2005) also suggest apomorphies for Zamiaceae and some clades within it, as well as a realignment of generic limits throughout the order.

For embryology, see Singh (1978), branching, see Stevenson (1988), and for fossils, see Pant (1987). 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); Jones (2002) gives an account of all taxa while Walters and Osborne (2004) focuses on problems of species delimitation, etc. Artabe and Stevenson (1999) suggest a number of possible apomorphies, and also discuss variation in a number of anatomical features within the order; Hill et al. (2003) provide a phylogeny and a useful list of characters varying within Cycadades (see also Hermsen et al. 2006a), Hill et al. (2004) a list of all taxa, while there is a good website with information on Cyadales, The Cycad Pages (Hill & Stevenson 2002-).

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, (1-)3-8 erect ovules/sporophyll; seeds platyspermic; n = 12.

1/105. E. Africa and Madagascar, South East Asia to New Caledonia and Tonga (Map: from Jones 2002). [Photo - Cycas megasporophyll]

For general information, see the Gymnosperm Database.

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, 2(-3) inverted ovules/sporophyll; 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.]

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.

For relationships within Encephalartos (which perhaps split from Lepidozamia 5-20 million years before present) see Treutlein et al. (2005).

For branching, see Stevenson (1988), for fossils, see Pant (1987), for general information, see Norstog and Nicholls (1997), Jones (2002: account of all taxa), Hill et al. (2003: further details of characters of individual clades, 2004: list of taxa), and Walters and Osborne (2004: general, especially species) and the Gymnosperm Database (general).

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