EMBRYOPSIDA Pirani & Prado

Gametophyte dominant, independent, multicellular, thalloid, with single-celled apical meristem, showing gravitropism; rhizoids +, unicellular; acquisition of phenylalanine lysase [PAL], flavonoids [absorbtion of UV radiation], phenylpropanoid metabolism [lignans], xyloglucans +; plant poikilohydrous [protoplasm dessication tolerant], ectohydrous; cuticle +; cell wall also with (1->3),(1->4)-ß-D-MLGs [Mixed-Linkage Glucans], lignin +; chloroplasts per cell, lacking pyrenoids; glycolate metabolism in leaf peroxisomes [glyoxysomes]; centrioles in vegetative cells 0, metaphase spindle anastral, predictive preprophase band of microtubules, phragmoplast + [cell wall deposition spreading from around the spindle fibres], plasmodesmata +; antheridia and archegonia jacketed, stalked; spermatogenous cells monoplastidic; blepharoplast, bicentriole pair develops de novo in spermatogenous cell, associated with basal bodies of cilia [= flagellum], multilayered structure [4 layers: L1, L4, tubules; L2, L3, short vertical lamellae] + spline [tubules from L1 encircling spermatid], basal body 200-250 nm long, associated with amorphous electron-dense material, microtubules in basal end lacking symmetry, stellate array of filaments in transition zone extended, axonemal cap 0 [microtubules disorganized at apex of cilium]; male gametes [spermatozoids] with a left-handed coil, cilia 2, lateral; oogamy; sporophyte dependent on gametophyte, embryo initially surrounded by haploid gametophytic tissue, plane of first division horizontal [with respect to long axis of archegonium/embryo sac], suspensor/foot +, cell walls with nacreous thickenings; sporophyte multicellular, with at least transient apical cell [?level], sporangium +, single, dehiscence longitudinal; meiosis sporic, monoplastidic, microtubule organizing centre associated with plastid, cytokinesis simultaneous, preceding nuclear division, sporocytes 4-lobed, with a quadripolar microtubule system; spores in tetrads, sporopollenin in the spore wall, wall with several trilamellar layers [white-line centred layers, i.e. walls multilamellate]; nuclear genome size <1.4 pg, LEAFY gene present, ethylene involved in cell elongation; chloroplast genome with close association between trnLUAA and trnFGAA genes.

Many of the bolded characters in the characterization above are apomorphies of subsets of streptophytes along the lineage leading to the embryophytes, not apomorphies of crown-group embryophytes per se.

All groups below are crown groups, nearly all are extant. Characters mentioned are those of the immediate common ancestor of the group, [] contains explanatory material, () features common in clade, exact status unclear.


Abscisic acid, ?D-methionine +; sporangium with seta, seta developing from basal meristem [between epibasal and hypobasal cells], sporangial columella + [developing from endothecial cells]; stomata +, anomocytic, cell lineage that produces them with symmetric divisions [perigenous]; underlying similarities in the development of conducting tissue and in rhizoids/root hairs; spores trilete; polar transport of auxins and class 1 KNOX genes expressed in the sporangium alone; shoot meristem patterning gene families expressed; MIKC, MI*K*C* and class 1 and 2 KNOX genes, post-transcriptional editing of chloroplast genes; gain of three group II mitochondrial introns.

[Anthocerophyta + Polysporangiophyta]: archegonia embedded/sunken in the gametophyte; sporophyte long-lived, chlorophyllous; sporophyte-gametophyte junction interdigitate, sporophyte cells showing rhizoid-like behaviour.


Sporophyte branched, branching apical, dichotomous; sporangia several, each opening independently; spore walls not multilamellate [?here].


Photosynthetic red light response; plant homoiohydrous [water content of protoplasm relatively stable]; control of leaf hydration passive; (condensed or nonhydrolyzable tannins/proanthocyanidins +); sporophyte soon independent, dominant, with basipetal polar auxin transport; vascular tissue +, sieve cells + [nucleus degenerating], tracheids +, in both protoxylem and metaxylem, plant endohydrous; endodermis +; root xylem exarch [development centripetal]; stem with an apical cell; branching dichotomous; leaves spirally arranged, blades with mean venation density 1.8 mm/mm2 [to 5 mm/mm2]; sporangia adaxial on the sporophyll, derived from periclinal divisions of several epidermal cells, wall multilayered [eusporangium]; columella 0; tapetum glandular; gametophytes exosporic, green, photosynthetic; basal body 350-550 nm long, stellate array in transition region initially joining microtubule triplets; placenta with single layer of transfer cells in both sporophytic and gametophytic generations, embryonic axis not straight [root lateral with respect to the longitudinal axis; plant homorhizic].


Sporophyte branching ± indeterminate; lateral roots +, endogenous, root apex multicellular, root cap +; (endomycorrhizal associations + [with Glomeromycota]); tracheids with scalariform-bordered pits; leaves with apical/marginal growth, venation development basipetal, growth determinate; sporangia borne in pairs and grouped in terminal trusses, dehiscence longitudinal, a single slit; cells polyplastidic, microtubule organizing centres not associated with plastids, diffuse, perinuclear; blepharoplasts +, paired, with electron-dense material, centrioles on periphery, male gametes multiciliate; chloroplast long single copy ca 30kb inversion [from psbM to ycf2]; LITTLE ZIPPER proteins.

LIGNOPHYTA†  Back to Main Tree

Sporophyte woody; lateral root origin from the pericycle; branching lateral, meristems axillary; cork cambium + [producing cork abaxially], vascular cambium bifacial [producing phloem abaxially and xylem adaxially].

SEED PLANTS†  Back to Main Tree

Plants heterosporous; megasporangium surrounded by cupule [= integument]; megaspores retained on the plant, germinating to produce the female gametophyte.

Age. The age for this node is estimated to be around (382-)374(-367) m.y.a. (Silvestro et al. 2015).

Evolution. Divergence & Distribution. Characters to be placed at this node and those at the extant seed plant node have not been clearly distinguished.

EARLY SEED PLANT EVOLUTION (very much under development)

Evolution. Divergence & Distribution. Niklas et al. (1983) note a marked increase in land plant diversity at the end of the Devonian through the Carboniferous and Permian, mainly the result of diversification of pteridophytes (ferns and lycopods), although gymnosperms were slowly diversifying through this period. Indeed, The origins of extant seed plants, the focus of this site, are to be sought in mid-Devonian lignophytes, progymnosperms like Archaeopteridales and Aneurophytales. These plants usually have complex leaves and well-developed secondary thickening with much parenchyma mixed in with tracheids (e.g. Beck 1962; Carluccio et al. 1966). In some early taxa the leaves proper 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 seed plants can be seen in taxa in which the solid central vascular tissue became ridged and dissected into vertical columns, pith developing. Ultimately the vascular system came to consist 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 1968a-c; Stewart & Rothwell 1993 for a good summary). Baucher et al. (2007) discuss the evolution of secondary thickening.

It is still unclear when the megaphylls that characterise nearly all seed plants, fossil and extant, evolved - they seem to have evolved several times (e.g. Tomescu 2009; Tomescu et al. 2014) - and what they represent. Floyd and Bowman (2010) compared gene expression patterns in shoots and leaves of seed plants, suggesting that the marginal blastozones of leaves and the shoot apical meristem may be similar in some respects, consistent with the hypothesis that seed plant megaphylls/leaves could represent a modified branch system. It remains an open question whether or not seed plant megaphylls arose in parallel with those of ferns (Boyce 2005a summarizes earlier literature, 2008a; Corvez et al. 2012), or, importantly, whether the issue should even be conceptualized in this way (Kaplan 1997, vol. 3: chap. 19, 2001); see also [Monilophyta + Lignophyta] for more on this topic.

Heterospory has evolved several times in land plants (Bateman & DiMichele 1994 for a review). Spore-bearing and photosynthetic leaves seem to be quite different in seed plants, while in other vascular plants there is no fundamental dissimilarity between the two (e.g. Kaplan 1997, vol. 3: chap. 19; Boyce 2005b). Some Upper Devonian Archaeopteridales and Aneurophytales were heterosporous; mega- and microspores were apparently mixed in a single sporangium in some Aneurophytales, while the distinct megasporangia of Archaeopteris produced several megaspores (Bateman & DiMichele 1994); megaspores are not always larger than microspores, although seeds are (see below).

Extant seed plants are distinctive because they usually have only a single megaspore per megasporangium, the megasporangia developing in ovules (see Boyce 2005b); there are a maximum of four megaspores per megasporangium, three of which abort (Kenrick & Crane 1997). The ovule is made up of the megasporangium proper, the nucellus, i.e. the megasporangium wall, the whole being more or less enclosed by one or more integuments, which may be deeply lobed. The megaspore germinates while still in the ovule and on the mother plant. The egg/ovum that develops from the megaspore is fertilized when in the ovule, and the embryo that develops receives its nutrition from the female gametophyte that is retained in the ovule, although directly or indirectly it comes from the parental sporophyte. Initial embryo development in other heterosporous land plants is entirely dependent on the gametophyte. The seed is a fertilized ovule, the beginning of the next generation sporophyte, and it is more or less surrounded by gametophytic reserve tissue and in turn by the seed coat, of parental sporophyte integumentary origin. Bateman and DiMichele (1994: esp. fig 13) carefully dissected out the separate elements involved in heterospory and ovule production.

Archaeopteridales flourished from about 377 m.y.a., but were diminishing greatly by the beginning of the Carboniferous ca 363 m.y.a. (Algeo et al. 2001). Ovules are known from the Devonian onwards (Stewart & Rothwell 1993; Kenrick & Crane 1997; Cleal et al. 2009 and references); some Archaeopteridales from ca 365 m.y.a. had a lagenostome, a tubular projection of the nucellus with a central column that was probably involved in pollen capture, and pollination/fertilization mechanisms were probably quite like those of extant gymnosperms. The ovules of Runcaria, a seed plant probably to be assigned to Aneurophytales and from the middle Devonian of some 385 m.y.a., lacked a lagenostome and Gerrienne et al. (2004) suggested that the antherozoids reached the megagametophyte by lysis of the megasporangium wall, which forms a long, terminal projection in this plant.

Pollen is produced in microsporangia. In seed ferns, pteridosperms, and their immediate relatives pollen probably germinated via the adaxial surface of the microspore and the tetrad of megaspores is linear; the integument is vascularized (Taylor et al. 2009). It is likely that some early conifers and Cordiatales had microspores whose development was endosporic (e.g. Friedman & Gifford 1997); there is likely to have been zoidogamy, fertilization by motile male gametes.

In the Carboniferous in particular there was a considerable variety of plants, including the seed ferns with their fern-like leaves and ovules - although the Carboniferous has been called the age of ferns, perhaps as accurately it could be called the age of seed ferns. Recent studies are helping to clarify their morphology, although is is difficult to assemble whole organisms from dispersed leaves, ovules, and trunks (Taylor et al. 2006 and references, also other papers in J. Torrey Bot. Soc. 133(1). 2006; Taylor et al. 2009), and how the ovule was attached to the plant can be difficult to establish (e.g. Spencer et al. 2012). Ovule morphology alone does not indicate the identity of the organism - pteridosperm or coniferophyte - bearing the ovule (Seyfullah et al. 2010).

A link between fossil gymnosperms, especially Cordiatales, and extant conifers has been suggested, the short shoot made up of bract + ovuliferous scale of most extant members being linked to more complex and obviously shoot-like structures of fossil taxa (Florin 1951). The rather conifer-like Cordaitales and Callistophytales, which had compound pollen-bearing structures and saccate pollen, are found in the lower Carboniferous. Slightly later there are the still more conifer-like ("ancestral") Voltziales that lacked saccate pollen; they have been associated with Cupressaceae (Rothwell et al. 2011 and references; Taylor et al. 2009: survey of early gymnosperms). Cheirolepidaceae, recently found in the northern hemisphere (Oregon, USA), have been associated with Araucariaceae and Podocarpaceae (Stockey & Rothwell 2013). The so-called coniferophytes are often distinguished from conifers, although what the two contain and their relationships are both unclear (Rothwell & Mapes 2001); phylogenetic studies are certainly not suggesting a simple answer (e.g. Crane 1985b; Doyle & Donoghue 1986a, 1992; Rothwell & Serbet 1994; Doyle 1996; etc.).

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, probably parallelisms.

Ecology & Physiology. For good general summaries of fossils and what they disclose about plant physiology in the past, see Boyce (2009) and Kenrick and Strullu-Derrien (2014: esp. roots). The bottom line is that seed plants in particular, and plants with secondary thickening in general, have long helped change the global environment (e.g. Beerling et al. 2001; Feild & Edwards 2012). There are a number of feedback loops, many positive, implicated in changing climates and CO2 concentration (e.g. Berner 1999; Beerling 2005a; Beerling & Berner 2005).

Integrated in this section is quite a bit of general seed plant evolution. There is also mention of extinctions, mass or otherwise, that have been popular subjects of discussion for 40 years or more, for instance, see the classic paper by Raup and Sepkoski (1984). However, not only are they not clearly defined, they are measured in various ways, the scale may be local or global, and both their cause(s) and any connection with diversification and the evolution of novelty can be difficult to establish.

A number of early land plants had some sort of secondary thickening. Thus fossils from Canada and France from up to ca 407 m.y. (Early Devonian), otherwise quite like Psilophyton, have secondary xylem with rays and tracheids (Gerrienne et al. 2011; Hoffman & Tomescu 2011, 2013: see also Donoghue 2005; Rothwell et al. 2008b for wood evolution in general). Although secondary thickening may have evolved several times, in most cases the cambium cut off only a small amount of vascular tisue, a little xylem, and only to the inside. For discussion about the evolution of growth forms and xylem in lignophytes, see Rowe and Speck (2005: cambium as a nascent innovation), Gerrienne et al. (2011), Stein et al. (2012), and Strullu-Derrien et al. (2013).

Giesen and Berry (2013) reconstructed the morphology of the middle Devonian pseudosporochnalean Calamophyton, perhaps related to monilophytes. It was a small tree, and the primary stem increased in width for up to 2 m (did the apical meristem increase in size at the same time?); there was secondary growth towards the base of the stem/trunk. The primary stem, at up to 10 cm across, was very stout; the branches themselves branched dichotomously and bore small appendages/leaves and were shed as units (cladoptosis: Giesen & Berry 2013).

The first lignophytes were small, and Gerrienne et al. (2011) suggest that it was initially the need for increased water conductance in response to decreasing CO2 concentration (the stomata would have to be open more), not the need for support, that drove the early evolution of a vascular cambium (see also Stein et al. 2012). Overall, photosynthesis and the sequestration of carbon by plants increased, and global carbon and nutrient cycling and energy flow began to be dramatically changed (Qiu et al. 2012; Kenrick et al. 2012).

Lignin also provides support, so facilitating the size increase of land plants evident from the Middle Devonian onwards (e.g. Beerling et al. 2001). By the mid-Devonian ca 385 m.y.a. forests are surprisingly complex, with the early seed plant group Aneurophytales being scramblers up much larger pseudosporochnalean trees (of uncertain affinities, see above: Stein et al. 2007, 2012). Certainly by the later Devonian there were true lignophytes about 1 m d.b.h., and up to 2 m across by the lowermost Carboniferous. (Algeo et al. 2001; Galtier & Meyer-Berthaud 2006). Although these lignophytes were not necessarily taller than the tree lycophytes of e.g. the Carboniferous, they were stouter, and they also had well developed true roots, the fine roots presumably having root hairs; in Archaeopteridales, early lignophytes, there was cladoptosis (Algeo et al. 2001). These early trees may represent an independent acquisition of the habit from that later cordiatalean plants (Galtier & Meyer-Berthaud 2006).

The evolution of megaphylls, found in most seed plants, may have been a two-stage process. Megaphylls are to be found in the Mid- to Late-Devonian progymnosperm, Archaeopteris, and also in the Late Devonian-early Mississippian pteridosperms (Osborne et al. 2004). A major problem with megaphylls is overheating. Variables here are leaf blade size, atmospheric CO2 concentration, air and leaf temperature, and stomatal density (e.g. Hetherington & Woodward 2003; Osborne et al. 2004; Franks & Beerling 2009). Indeed, understanding the evolution of stomatal morphology and functioning is one key to understanding the success of lignophytes, although it is difficult to pinpoint exactly when some of the changes took place (McAdam & Brodribb 2011, see Fig. 4, Cycadaceae not examined, 2013). As atmospheric CO2 decreased in the Devonian, stomatal density increased to allow more CO2 uptake, and transpiration also increased, but atmospheric temperature was decreasing along with the decrease in CO2 concentration, and this would tend to decrease transpirational loss (Osborne et al. 2004; Franks & Beerling 2009a). The possibility that megaphylls might overheat was reduced because of evaporative cooling caused by increased transpiration as well as lamina dissection (Beerling et al. 2001; Beerling 2005a and references). The well-developed vascular system produced by secondary thickening would permit increased transpiration, the water it transported supplying the dorsi-ventrally flattened photosynthetic leaves/megaphylls that facilitated CO2 uptake (Raven & Edwards 2001; Beerling et al. 2001; see also below).

If evidence from extant land plants is any guide, there have been changes in how stomatal opening and closure is controlled (see also Stomatophytes). Stomatal closure in ferns - in whatever habitat they grow, although many prefer moister conditions - occurs when the leaf still has a relatively high water potential when compared with angiosperms not growing in shade (Brodribb & Holbrook 2004). Furthermore, the water potential of the leaf at which irreparable damage occurs is only slightly lower than that at which stomatal closure occurs (McAdam & Brodribb 2013). Stomata of "bryophytes", ferns and lycophytes do not respond to abscisic acid (but c.f. Chater et al. 2011), and control over stomatal opening is passive (McAdam & Brodribb 2011, 2012, 2013; Haworth et al. 2013). Stomatal conductivity of seed plants other than flowering plants does not respond to elevated CO2 concentrations in the atmosphere (Brodribb et al. 2009; McAdam & Brodribb 2011) or to blue light (Doi & Shimizaku 2008).

In seed plants stomatal control is active. On drying of the leaf, the stomata close more or less immediately, but open more slowly, being sensitive to the enhanced levels of abscisic acid (Brodribb & McAdam 2010; McAdam & Brodribb 2012a). In Metasequoia, at least, initial stomatal response to water stress on drying of the leaf is passive, as in ferns and lycophytes; subsequently, abscisic acid-mediated behaviour became apparent (McAdam & Brodribb 2014). In angiosperms, the subsidiary cells lose turgor first if water loss is rapid, and this causes guard cells to open the stomatal aperture (Brodribb & McAdam 2010). This difference in control, much more flexible in angiosperms, is related to the fact that angiosperm leaves may also have a relatively higher amount of water still available after stomata close and before leaf death occurs than in ferns or lycophytes. Furthermore, when light is not saturating, the ratio of photosynthesis to water loss decreases in ferns with high photosynthetic rates, while in seed plants it remains about the same (McAdam & Brodribb 2012b). Such factors may have been involved in the success and ecological dominance of early seed plants as the late-Palaeozoic environments became drier (McAdam & Brodribb 2012b, 2013). However, other findings suggest that the difference in stomatal control between angiosperms and gymnosperms is not so clear-cut (Haworth et al. 2013).

Early seed plants, monilophytes, etc., have leaf blades with a low venation density, ca 3 mm/mm2 or less, and the venation is not hierarchical, but dendritic (open) and often dichotomizing. Seed ferns like Glossopteridales and Giganopteridales have reticulate venation (the veins in some of the latter may even have a quasi-hierarchical organization); this might be linked with the development of a drier climate (Roth-Nebelsick et al. 2001). Stomatal density and size are also important variables here (e.g. Osborne et al. 2004), and stomatal density varies inversely with size (Franks et al. 2014). Stomata of Archaeopteris, at about 62±3µm long, were large, stomata reaching ca 78µm long in a few taxa (Hetherington & Woodward 2003), but large stomata at low density would allow less evaporative cooling. Stomatal density is negatively and size is positively correlated with atmospheric CO2 concentrations (e.g. Franks & Beerling 2012: esp. Fig. 3), and venation density may also be inversely correlated with CO2 concentration, although the variation is not extensive (2-3 mm/mm2, "large fluctuations": Retallack 2005). However, there seems to have been no major changes in plant productivity despite major changes in CO2 concentration (Boyce & Zwieniecki 2012 and refs, c.f. e.g. Franks & Beerling 2009a), certainly, there is no simple positive correlation. These aspects of seed plant evolution are discussed further later.

Roots are also implicated in these early changes via a complex series of feed-back loops (e.g. Raven & Edwards 2001; Beerling & Berner 2005). Even early lignophytes are likely to have been endomycorrhizal, with vesicular-arbuscular mycorrhizae (VAM) (Quirk et al. 2012 and references). The roots of lignophytes penetrate some one metre or so into the ground, so greatly facilitating weathering by enabling carbon dioxide to penetrate to greater depths; roots and VAM also produce chelates and organic acids, some photosynate moves directly from the root tip to the soil, more moves in to the fungus (Kaiser et al. 2015), while decay of organic litter produces carbonic and other organic acids, and all these facilitate plant micronutrient uptake and rock breakdown (Berner 1997; Algeo et al. 2001; Raven & Edwards 2001; Beerling 2005a; Taylor et al. 2009; Kenrick et al. 2012). VAM cause calcium silicate dissolution from basalt, although this was reduced when atmospheric CO2 concentrations were lower (Quirk et al. 2014). This plant/fungus-aided chemical weathering of rocks entails the loss of atmospheric CO2 as it reacts with rock minerals, with rock silicates being converted into bicarbonates (HCO3-) and aluminium silicates. The former are carried to the sea where they can be precipitated out, eventually becoming limestome or dolomite, while the latter form the basis of clays (Quirk et al. 2012). Increased transpiration can lead to increased rainfall, and roots would help retain the clay-rich soil, improve its structure and so increase the retention of water and extend the period over which rock weathering can proceed (Berner 1997; Retallack 1997a; Beerling 2005a; c.f. Taylor et al. 2009 in part).

All in all, the evolution of arborescent vascular plants is likely to have led to a major increase in the rate of weathering (e.g. Berner 1997; Boyce & Lee 2011), and atmospheric carbon dioxide fell precipitously during the Devonian (Kenrick et al. 2012), all told, some 90% over the late Palaeozoic. Thus estimates of the carbon dioxide concentration in the atmosphere at the end Silurian are 4-20 times the pre-industrial concentration of 270 p.p.m.V, but only 3-13 times this by the end of the Devonian, and by the Late Carboniferous and in particular Early Permian they were close to modern values.

As lignophytes spread over the land, the increased photosynthesis they carried out led to increasing oxygen concentration in the atmosphere. 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 much CO2 is unlikely to have been released from dead plant remains in this way (Scott & Glasspool 2006; Belcher et al. 2010b). This Devonian increase in oxygen concentration in the atmosphere may have allowed the evolution of animals with larger bodies; the evolution of placoderm arthrodire fish, some of which reached ca 10 m in length, has been linked to the rise in oxygen concentration in the sea (Dahl et al. 2010). However, towards the end of the Devonian (ca 372 m.y.a., the Frasnian-Famennian boundary, other events as recently as 360 m.y.a.) there were notable extinction events, but there was no particular negative affect on vascular plants (Cascales-Miñana & Cleal 2014); Silvestro et al. (2015) noted that the extinction rate of spore-bearing, which had been high, vascular plants dropped markedly after this period and overall net diversification rates for vascular plants across this whole period were high.

DiMichele (2014) discussed the dynamics of coal-age tropical vegetation. He pointed out that even in places where vegetation indicated wetter conditions, there were periods when plants that preferred drier conditions predominated, and overall there was a trend towards drier conditions. During the Pennsylvanian (359-299 m.y.a.) arborescent lycopsids became less common and marattialean tree ferns more common (the latter at least temporarily), and Cordaitales were replaced by conifers, the latter preferring the seasonally drier conditions that became commoner (DiMichele 2014). Burnham (2009) noted the relative abundance of climbers at this time, although they became much less common, remaining so until the Cretaceous or Caenozoic. Some scrambling or climbing seed ferns like Callisophyton, Lyginopteris, and in particular Medullosa, had long and wide - from 65-237 µm across, the upper part of this range in Medullosa - tracheids and their water conductivity was probably on a par with that of some extant angiosperms with vessels (Wilson & Knoll 2010).

The largely southern hemisphere supercontinent Pangea had formed by around 320 m.y.a., and this would have increased chemical weathering and so aided in the CO2 decrease. The Permo-Carboniferous Ice Age/Late Palaeozoic Ice Age (LPIA) began in the late Carboniferous and is dated to about 320-290 m.y.a., perhaps persisting to ca 280 m.y.a. in east Australia. The oxygen concentration of the atmosphere probably reached a high of about 30% towards the end Carboniferous/beginning Permian during the LPIA (e.g. Shi & Waterhouse 2010), close to the 35% at which plants burn readily even if they are not dry. Gigantism, e.g. of dragonflies and in particular fusilinid foraminferans, has been linked to this increased oxygen concentration (Payne et al. 2012).

The decomposition of lignins, major and complex components of the secondary cell walls of the xylem in particular of vascular plants, is important here. Lycophytes had proportionally a large amount of lignin (Robinson 1990), and litter from extant ferns, lycophytes and bryophytes is slow to decompose compared to that of gymnosperms and especially angiosperms (Cornwell et al. 2008). Millipedes, diversifying by ca 410 m.y.a. (Misof et al. 2014), were early detritivores. However, they cannot destroy lignin; secondary metabolites protecting against herbivores may have evolved about this time, and they might decrease CO2 produced by respiration of organisms that would otherwise have helped decompose the plants (Retallack 1997a). Termites, whose associated bacteria can break down lignin, did not evolve until much later, perhaps in the Jurassic (Bignell et al. 2011). In any event, large amounts of carbon accumulated in the anoxic Carboniferous swamps, it was buried by the accumulating sediments produced by rock weathering (Beerling 2005a), and then converted into the massive coal deposits that characterize rocks from the later Carboniferous.

Today white-rot basidiomycete fungi are the most important decomposers of lignin. However, there do not appear to have been lignin-decomposing fungi in Carboniferous forests, and this is an important element to take into account when thinking of Carboniferous coal swamps (Floudas et al. 2012: there may have been some photodegradation of lignin, see Austin & Ballaré 2010). The capability to degrade lignin may have evolved in the ancestor of the Agaricomycetes clade (372-)290(-222) m.y.a. around the beginning of the Permian, and this is consistent with the fossil record, the earliest fossils of white-rot (lignin-decomposing) fungi being around 260 m.y.a. (Floudas et al. 2012, q.v. for other similar dates; Eastwood et al. 2011 suggest an age of around 219.6 m.y. for the [Russulales + Agaricales] clade); basal members of this clade have other life styles, too (Kohler et al. 2015). Peroxidases, which play a central role in this lignin degradation are found only in white rot fungi, and they effectively burn off the lignin, at the same time producing CO2, etc.. While brown rot fungi can access much of the cellulose in the cell wall, they do not destroy the lignin; they may have evolved from white-rot fungi (e.g. Floudas et al. 2012; Kohler et al. 2015). Some ascomycetes, soft rot fungi, can also break down lignin (Shary et al. 2007 and references).

At the end of the Carboniferous 305-295 m.y.a. there were two or more extinction events which included the ecological collapse of the Euramerican tropical swamp forests which in turn was associated with a drying climate (Sahney et al. 2010). This was perhaps the first animal extinction event accompanied by notable vascular plant extinctions (Cascales-Miñana & Cleal 2014: family the unit of analysis), although it was not picked up by Silvestro et al. (2015: genus the unit). The global climate oscillated greatly, with mean annual temperature increases at times of 8-10o C as is evident in rocks from both tropical and more temperate environments. Temperatures may even have become lethally hot at the equator, with equatorial sea surface temperatures (SST) approaching 40oC and land temperatures fluctuating even higher (the current SST is 25-30oC), and land temperatures in places may have exceeded 70oC (Zambito & Benison 2013: at the beginning of the CO2 fluctuations below), a remarkable figure (see also Tabor 2013). Under such conditions, the photosynthetic rate decreases and that of photorespiration increases, the latter predominating above 35o C (Sun et al. 2012); 45-52o C is lethal for non-succulent leaves (Beerling et al. 2001) and most animal and plant life would have had a hard time at 70oC. Linked with such changes, atmospheric CO2 concentrations fluctuated greatly at the end-Permian beginning Triassic around 275-210 m.y.a. varying from 300-500 to almost 8,000 p.p.m. (Algeo et al. 2001; Driese & Mora 2001; Montañez et al. 2007; Shi & Waterhouse 2010; Kaufman & Xiao 2012; Retallack 2013b). The last glaciations, the last for over 200 m.y., were around 260 m.y.a. (Montañez et al. 2007). There are various ideas explaining such changes. Possibly the marine bacterium Methanosarcina acquired the ability by horizontal gene transfer to break down organic compounds to methane, facilitated by nickel (needed by the enzymes) produced by eruptions that produced the vast Siberian traps (Rothman et al. 2014); these eruptions also produced large amount of CO2 and other gases.

Interestingly, reptile diversity and specialization (e.g. appearance of herbivores) increased markedly over the earlier Permian in particular (Sahney et al. 2010). In western Euramerica during this time, as the climate dried and bacame warmer, vegatation with conifers like Walchia, cycadophytes, peltasperms and plants like Cordaites replacing Carboniferous pteridosperms and tree ferns, which did persist into the early Permian at times when precipitation was higher (Montañez et al. 2007; Retallack 2013b). Cycads, otherwise Mesozoic plants, appeared at the end of the early Permian, and even conifers were not to be a major feature of the vegetation until the end-Permian (Montañez et al. 2007).

The Permo-Triassic boundary ca 251 m.y.a. is marked by an extinction that was about as severe as any in the earth's history, although with three identifiable episodes spread over 20 m.y. it was a rather protracted and complex episode (Sahney & Benton 2008). This extinction, the second to have affected both plants and animals according to (Lascales-Miñana and Cleal (2014), negatively affected sporing vascular plants, seed ferns and conifers, although their origination rates were quite high during this period (Silvestro et al. 2015); Niklas ert al. (1983) noted that this was the beginning of the period when gymnosperms dominated the flora, partly replacing pteridophytes. There was a world-wide end-Permian "coal gap", a ca 7 m.y. period when sediments with coal deposits were absent, perhaps because of the extinction of peat-forming plants (Retallack et al. 1996; Sun et al. 2012). Glossopterids, giganopterids, tree lycopsids and cordaites all became extinct (Retallack et al. 2006; Retallack 2013b). Atmospheric oxygen levels fell to somewhat below those current immediately after the end of the Permian, sometimes only 12.5% in the Triassic, but they then increased and have shown only moderate changes since (e.g. Scott & Glasspool 2006; Labandeira 2007). Throughout the southern hemisphere cool forest area there was increased weathering with rivers becoming higher-energy in an environment that had become more unstable, the soils were more infertile (oligotrophic), and deciduous (Glossopteris) forest was replaced by evergreen forest that had a lower albedo (Retallack & Krull 1999; Retallack et al. 2006 for more details). There was extensive die-off of coniferous forest, Walchiaceae going extinct (Looy et al. 1999; Grauvogel-Stamm & Ash 2005), soil erosion, and loss of peat forests.

Temperature and CO2 fluctuations continued into the Triassic, and high temperatures at higher latitudes were accompanied by increases of lycopsid spores and plants with stout stems, otherwise plants like conifers, seed ferns and ferns were common (Retallack 2013b). The heterosporous lycopsid Pleuromeia sternbergii or other lycopsids dominated for 5 million or more years early in the Triassic before being replaced by i.a. conifers like Voltzia in which fertilization was probably by siphonogamy (Looy et al. 1999); these conifers, thought to be related to late Permian conifers, include the almost herbaceous Aethophyllum (Grauvogel-Stamm & Ash 2005). Grauvogel-Stamm and Ash (2005) emphasize the length of the recovery period of the Triassic vegetation, up to 14 m.y. in total, 1-2 m.y. being the normal time for recovery to begin after such events.

Carbon dioxide concentrations then decreased and temperatures cooled somewhat, and there was an end-Triassic extinction event around 201.6 m.y. ago (McElwain et al. 2009 for references). This affected vascular plants only slightly, although the origination rate of gymnosperm clades decreased at about this time (Silvestro et al. 2015; see also Cascales-Miñana & Cleal 2014). Again there was an increase of atmospheric CO2 (about four-fold, from ca 600 to 2,100-3,000 p.p.m.) and an increase in temperature of 2.5-5o C, or locally even more, and there were extinctions/declines in standing diversity/increases in heterogeneity of community composition of both plants and animals (McElwain et al. 1999, 2007; Huynh & Poulsen 2005; Steinthorsdottir et al. 2011). The period has also been characterised more by ecological rearrangement of the vegetation, but little extinction of sporomorphs, at least (Bonis & Kürschner 2012; see akso Mander et al. 2010), similarly, in eastern Greenland the new community dominants were previously rare, while the previous dominant species tended to become rare (McElwain et al. 2007, 2009). Reproductively specialized plants like cycads, bennetitalean plants and seed ferns seem to have been particularly affected (e.g. Mander et al. 2010). This extinction can perhaps be linked to the beginning of major eruptions in the Central Atlantic Magmatic Province associated with the break-up of Pangea, perhaps because methane was released from clathrates then (McElwain et al. 2007; Bonis & Kürschner 2012); eruptions with associated spikes in atmospheric CO2 continued even when biological recovery was underway (Blackburn et al. 2013).

The high temperatures may have increased leaf temperatures near or above the limit of lethality. Thus species that persist across the Triassic-Jurassic boundary or first occur in the early Jurassic had notably more divided and/or narrower leaf blades compared to those of the late Triassic flora, and this would result in lower leaf temperatures than if the leaves were broad and undivided (McElwain et al. 1999; Beerling & Berner 2005); these more dissected (or smaller, narrower) leaves were also more flammable (Belcher et al. 2010a). As temperatures increased, so did stomatal size and transpiration, while stomatal frequency, as well as runoff and gross erosion, decreased (Steinthorsdottir et al. 2012). Fire activity in parts of the Northern Hemisphere, at least, increased, despite the low atmospheric oxygen concentration (Belcher et al. 2010a).

Gymnosperms like Cheirolepidaceae tend to be common in the drier interior of early Jurassic Pangea, where they could completely dominate the vegetation, while spore-bearing plants, among which liverworts were commoner around the more humid peirphery (Bonis & Kürschner 2012).

It is only at the end of this whole period, perhaps within the last 200 m.y., that ectomycorrhizal (ECM) relationships between plants and fungi develop. The clade including ECM truffles and relatives may have evolved as early as 185 m.y.a. (Bonito et al. 2014), while the evolution of the ECM habit in Pinaceae, the oldest extant clade of ECM plants, is around (271-)237-153(-100) m.y. - these are crown-group ages of Pinaceae, so actual ages of the ECM association may well be older. For further details, see the ecophysiology of ECM plants and their evolution.

Pollination Biology & Seed Dispersal and Plant-Animal Interactions. For details, see evolution.

Genes & Genomes. Jiao et al. (2011) provide evidence for a genome duplication in the lineage basal to all extant seed plants, and date the peak of the age curve of the duplicated genes that it caused to (352-)349, 347(-343) m.y. in the early Carboniferous (Mississippian) - the overall age spread is from ca 400 to just over 250 m. years. Lang et al. (2010; see also Zhu et al. 2012) discuss the evolution of transcription-associated proteins, perhaps associated with genome duplications; three new protein families evolved somewhere between the lycophytes and flowering plants.

Chemistry, Morphology, etc. Phloem anatomy in early seed plants is discussed by Decombeix et al. (2014).

Some early conifers and Cordiatales had microspores of a kind often called prepollen. The microspores lack a sulcus, but there are proximal trilete or monolete ridges, haptotypic marks reflecting where the spores were attached in the tetrad before it broke up. The development of the male gametophyte probably took place inside the spore, so it was endosporic, and germination occurred via these ridges (e.g. Friedman 1993; Friedman & Gifford 1997). Motile gametes are likely to have been produced (Looy et al. 1999). All extant seed plants have true pollen; here germination is distal, that is, the pollen tube grows out through the part of the pollen grain that was not adjacent to the the other members of the tetrad, and there are no haptotypic marks. Development is initially endosporic here, too. However, the relationships between fossil plants with prepollen and those with true pollen, and extant gymnosperms, also with true pollen, are not well understood, and it is not easy to understand the evolution of the sulcus in fossil gymnosperms (Doyle 2013); distinguishing between prepollen and pollen may be of little value (Poort et al. 1996 for a review; Taylor et al. 2009).


Plant evergreen; nicotinic acid metabolised to trigonelline, (cyanogenesis via tyrosine pathway); primary cell walls rich in xyloglucans and/or glucomannans, 25-30% pectin [Type I walls]; lignins derived from (some) sinapyl and particularly coniferyl alcohols [hence with p-hydroxyphenyl and guaiacyl lignin units, so no Maüle reaction]; root stele with xylem and phloem originating on alternate radii, not medullated [no pith], cork cambium deep seated; shoot apical meristem interface specific plasmodesmatal network; stem with vascular cylinder around central pith [eustele], phloem abaxial [ectophloic], endodermis 0, xylem endarch [development centrifugal]; wood homoxylous, tracheids and rays alone, tracheid/tracheid pits circular, bordered; mature sieve tube/cell lacking functioning nucleus, sieve tube plastids with starch grains; phloem fibres +; cork cambium superficial; leaves with single trace from vascular sympodium [nodes 1:1]; stomatal pore with active opening in response to leaf hydration, control by abscisic acid, metabolic regulation of water use efficiency, etc.; buds axillary (not associated with all leaves), exogenous; prophylls two, lateral; leaves with petiole and lamina, development basipetal, blade simple; plant heterosporous, sporangia borne on sporophylls, sporophylls spiral; microsporophylls aggregated in indeterminate cones/strobili; grains monosulcate, aperture in ana- position [distal], exine and intine homogeneous; ovules unitegmic, parietal tissue 2+ cells across, megaspore tetrad linear, functional megaspore single, chalazal, lacking sporopollenin, megasporangium indehiscent; pollen grains land on ovule; gametophytes dependent on sporophyte; apical cell 0, male gametophyte development initially endosporic, tube developing from distal end of grain, to ca 2 mm from receptive surface to egg; male gametes two, developing after pollination, with cell walls, starch grains 0; female gametophyte endosporic, initially syncytial, walls then surrounding individual nuclei; embryo cellular ab initio, endoscopic, plane of first cleavage of zygote transverse, suspensor +, short-minute, embryonic axis straight [shoot and root at opposite ends; plant allorhizic], cotyledons 2; plastid transmission maternal; ycf2 gene in inverted repeat, whole nuclear genome duplication [zeta duplication], two copies of LEAFY gene, PHY gene duplications [three - [BP [A/N + C/O]] - copies], nrDNA with 5.8S and 5S rDNA in separate clusters; mitochondrial nad1 intron 2 and coxIIi3 intron and trans-spliced introns present.

Age. Early estimates of the age for crown-group seed plants range from 348-285 m.y. (Becker et al. 2000; Theißen et al. 2001; Leebens-Mack et al. 2005). Some recent molecular estimates are (366-)330, 327(-296) m.y. (Smith et al. 2010: see also their table S3), around (351-)330.3-324.3(-313.1) m.y. (Magallón et al. 2013, 2015; Naumann et al. 2013 and Iles et al. 2014 are similar), (339.4-)317.5(-306.2) m.y. (Zhang et al. 2014), and about 302 m.y.a. (Z. Wu et al. 2014). Somewhat older ages of (368-)351(-330) m.y. are suggested by Clarke et al. (2011: also other estimates), and (457-)385(-313) m.y. by Zimmer et al. (2007); P. Soltis et al. (2002) offer a variety of estimates.

Note: Possible apomorphies are in bold. However, the actual level at which many of these features, particularly the more cryptic ones, should be assigned is unclear. This is partly because many characters show considerable homoplasy, in addition, basic information for all too many is very incomplete, frequently coming from taxa well embedded in the clade of interest and so making the position of any putative apomorphy uncertain. Then there is the not-so-trivial issue of how ancestral states are reconstructed (see above).

Evolution. Divergence & Distribution. For possible apomorphies throughout this group, see e.g. Doyle (1998a, b, esp. 2006, 2013); presence of scale leaves may need to be added to the apomorphies for Spermatophyta. 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 may seem to characterise angiosperms may properly also be put at the level of extant seed plants. An example may be successive microsporogenesis with the microspore walls developing by centripetal furrowing (Nadot et al. 2008).

The secondary wall of tracheary tissue in extant seed plants is more or less homogeneous, lignified and resistant, and so 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.

Chanderbali et al. (2010) found that genes involved in microsporangium, etc., production in at least some gymnosperms are also expressed in the perianth of angiosperms; only a few genes involved in ovular expression are also expressed there. S. Kim et al. (2004b) age the split that gave rise to the paleo AP3 and PI genes to around (297-)290-230(-213) m.y., while Jiao et al. (2011) suggested that there was a whole genome duplication around here, estimates of peak ages are (245-)236, 234(-225) m.y.a., the first half of the Triassic, although the overall spread of ages is 275-150 m.y., which gives the imagination pretty free rein. For other studies plotting the evolution of genes involved in floral morphology and development, see the Amborella Working Group (2013) - some 70% of the genes involved were present in the most recent common ancestor of extant seed plants, others are still older. There have been dramatic changes in the expressions of some genes during land plant evolution (e.g. Banks et al. 2011), but where on the tree these changes occurred is unknown. Thus Szövényi et al. (2010: ca 30% of the genome mapped) noted that a total of only ca 5% of the genes in Funaria hygrometrica were expressed uniquely in the sporophytic and gametophytic generations, but in Arabidopsis ca 5% of the genes were differentially expressed in the gametophyte alone and ca 25% in the sporophyte alone. Gene expression in neither bryophyte generation was like that in the Arabidopsis gametophytes, but where in the tree between Funaria and Arabidopsis this shift might have taken place is unknown. For other such studies, see Lang et al. (2010) and Zhu et al. (2012).

Ecology & Physiology. See above.

Pollination Biology & Seed Dispersal. For the integument and its possible evolution, see Andrews (1963), for ovule growth, see Leslie and Boyce (2012), and for the evolution of embryo size, see Forbis et al. (2002).

Genes & Genomes. For type II MADS-box gene diversificiation in seed plants, see Becker et al. (2000) and especially Gramzow et al. (2014), 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), for 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 (Cameron et al. 2003). For the mitochondrial nad1 intron 2, see Gugerli et al. (2001).

Chemistry, Morphology, etc. Lignins drived from p-coumaryl alcohol are uncommon in gymnosperms, so S [syringyl] lignin units are also generally uncommon and there is no Maüle reaction; for the binding of ferulic acid to the primary cell wall, see Carnachan and Harris (2000). Trapp and Croteau (2001b) noted that gymnosperm monoterpene synthase genes contained 9 introns and 10 exons while in angiosperms the numbers were 6 and 7 respectively. Strasburger/albuminous cells have many plasmodesmata on the walls that they have in common with the sieve tubes.

For general information, see Gifford and Foster (1988), Hill (2005) and Anderson et al. (2007: including fossils). For leaf anatomy, see Napp-Zinn (1966), for phloem lignification, see Esau (1969), for the shoot apex, see Johnson (1951), for the roots of lycophytes and of lignophytes, apparently quite different, see Gensel and Berry (2001) and Gensel et al. (2001), for stelar morphology and evolution, see especially Beck et al. (1982e), for nodal anatomy in extant and fossil seed plants, see e.g. Kumari (1963: Lyginopteris, Heterangium and Archaeopteris all have but a single leaf trace, although the leaves themselves may be large) and Galtier (1999), for "megaphylls", see also [Monilophyta + Lignophyta], for venation development, see e.g. Boyce (2005b), for venation density, see Boyce et al. (2008a), for stomatal morphology, see J. A. Doyle et al. (2008b), and for cuticle waxes and their composition, see Wilhelmi and Barthlott (1977).

For the major features of gymnosperm wood, see e.g. Bannan (1934) and Mauseth (2009), for the distinction between angio- and gymno-ovuly and angio- and gymnospermy, see Tomlinson (2012), for variation in life cycle and embryology, see Saxton (1913) and in particular Singh (1978) and Sakai (2013), 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), Kurmann and Zavada (1994) and Poort et al. (1996); for ovules and seed anatomy, inc. that of fossils, see Schnarf (1937), and for seed mass, with a "59-fold divergence between angiosperms (small seeded) and gymnosperms (large seeded)", see Moles et al. (2005a: p. 578).

Phylogeny. A distinction has been drawn between manoxylic and pycnoxylic taxa. In manoxylic taxa there is much parenchyma mixed in with the tracheids in the secondary xylem and the pith is broad, while in pycnoxylic taxa the secondary xylem there is much less parenchyma in the seondary xylem and the pith is narrower. The cycadophytes, which include seed ferns like Lyginopteridaceae and Medullosaceae, cycads, and the immediately unrelated cycadeoids (e.g. Bennettitales), have manoxylic wood, while the coniferophytes, which include all other extant gymnosperms and several fossil groups (Chamberlain 1935; see also Gifford & Foster 1988), have pycnoxylic wood. Xylem in the short shoots of Ginkgo is manoxylic and in the long shoots, pycnoxylic (Gifford & Foster 1988; Little et al. 2013).

The distinction between radiospermy and platyspermy is also unlikely to be particularly fundamental, especially if Bennettitales are close to Gnetales (see below). Indeed, both radiospermy and platyspermy are evident, but in different tissues, in the seeds of Stephanospermum braidwoodensis (Spencer et al. 2012) and radiospermic and platyspermic taxa are interspersed in phylogenetic analyses of ovules (Seyfullah et al. 2010). Within gymosperms as a whole, manoxylic wood, large ("megaphyllous") leaves, and radiospermic (polysymmetric) seeds seem to be associated, as do pycnoxylic wood, smaller ("microphyllous") leaves, and platyspermic (disymmetric) seeds (Sporne 1965).

Relationships Of Gnetales In Particular. In the 1980s and 90s morphological phylogenetic studies suggested that extant seed plants were probably to be placed in five groups: cycads, Ginkgo, conifers, Gnetales (Gnetum, Ephedra and Welwitschia), and angiosperms. Extant gymnosperms were thought to be paraphyletic, the botanical equivalent of reptiles. Establishing the position of Gnetales has been difficult.

It was thought that plants with a heterosporangiate strobilus, the anthophytes, included flowering plants, Gnetales, and also fossil taxa like Bennettitales, while the glossophytes, the glossopterid seed ferns, were also thought to be fairly close; conifers, cycads, etc., were more distantly related (see Friis et al. 2011 for a good summary). Thus Gnetales and a larger or smaller group of fossil gymnosperms/pteridosperms were together sister to angiosperms (e.g. Crane 1985a, b; Doyle & Donoghue 1986a, b; Nixon et al. 1994; Taylor & Hickey 1995; Doyle 1998a, b); Doyle (in Sanderson et al. 2000: p. 783) noted that this position was "well supported" in bootstrap analyses that were carried out subsequently.

Seeds clearly of Ephedraceae are similar to those of Erdmanithecales (Rydin et al. 2006: see seed plant evolution). Detailed studies of small Early Cretaceous seeds suggests that both Erdmanithecales and Bennettitales have seeds very similar to those of Gnetum and Welwitschia in particular, the latter order agreeing in details of micropylar closure, and all have paracytic stomata (Friis et al. 2007, 2009; Mendes et al. 2008; c.f. Rothwell et al. 2009). Members of this BEG group (Bennettitales, Erdtmanithecales, Gnetales) have chlamydospermous seeds in which a thin testa is surrounded by a thicker layer probably derived from (a) bract(s) (the group has been called Chlamydospermae); there is a long micropylar tube (Friis et al. 2014 and references). The ovules are radiospermic and lack a cupule,the nucellus but not the integument is vascularized, and the seeds have an outer sarcotesta, a sclerotesta, and a layer inside that (Rothwell & Stockey 2002). A further link with Ephedra is in the granular infratectum of the pollen that all share (Friis et al. 2007), although the pollen of Eucommiidites (Erdmanithecales) is psilate and has two equatorial colpi as well (Pedersen et al. 1989). Members of the BEG group were very diverse in the northern hemisphere in the Lower Cretaceous, where they co-occur with early angiosperms (Friis et al. 2014), and Gnetales, at least, are abundant in the Brazilian Crato formation of around 115-112 m.y.o. (e.g. Löwe et al. 2013 and references).

Analyses of morphological data, which generally 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 and their like. Thus they support some kind of anthophyte hypothesis (Rydin et al. 2002; Doyle 2006; Hilton & Bateman 2006; Rothwell et al. 2009; Schneider et al. 2009; Crepet & Stevenson 2009, esp. 2010; Friis et al. 2007: seed morphology, 2011: summary, 2013a; Zavialova et al. 2009: pollen, walls homogeneous or granular). However, bootstrap support for these relationships is low (Doyle 2006; Hilton & Bateman 2006). In a recent study possible relationships among seed plants even included a paraphyletic Gnetales, with angiosperms sister to [Gnetum + Welwitschia]; [Archaefructus + Ceratophyllum] were sister to all other angiosperms (S. Wang 2010: e.g. Fig. 8.10), although this seems rather unlikely. Doyle (2006) studied seed plant evolution in the context of a morphological analysis that was constrained by a (molecular) topology in which Gnetales were nested within gymnosperms; he noted that this was almost as parsimonious as if Gnetales were linked with angiosperms.

Morphological phylogenetic analyses often suggest a connection between the "flowers" of Bennettitales and those of angiosperms (Rothwell et al. 2008a, 2009; Crepet & Stevenson 2009, esp. 2010: c.f. relationships among angiosperms). In the latter analyses the topology is sensitive to change of one character state in one taxon, and in some morphological analyses Bennettitales do not group with anthophytes and are associated with cycadofilicalean plants, extant gymnosperms are not monophyletic, but Gnetales are sister to angiosperms (Crepet & Stevenson 2009, 2010). However, Rothwell et al. (2009) and Rothwell and Stockey (2013) strongly questioned the idea of a close relationship between Bennettitales and Gnetales, noting i.a. that the former had spiral, not decussate, insertion of parts, the nucellus formed a plug in the micropyle, and there was no pollen chamber.

Several characters that Gnetales and angiosperms have in common fail to meet one or more of Remane's three basic criteria of similarity ("hoomology"), those of position, special properties, and intermediates. Thus the sieve areas in the phloem cells of Gnetales are very like those of other gymnosperms and are unlike those of the sieve tubes of angiosperms (Behnke 1990a). Vessels in Gnetales develop from circular pits and those in flowering plants from scalariform pits (e.g. Rodin 1969; Carlquist 1996), although Muhammad and Sattler (1982) suggested that in Gnetum, at least, the distinction was not so clear. Interestingly, vessels have also been found in some members of the poorly-known pteridosperm group Gigantopteridales - along with oleanane, known widely in angiosperms (Moldowan et al. 1994; E. L. Taylor et al. 2006). The tunica of Gnetales has only a single layer, not two or three as is common in angiosperms (e.g. Donoghue & Doyle 2000a; Doyle 2006). Similarly, the tension (reaction) wood in Gnetum, produced as the branches maintain their orientation against gravity, consists of gelatinous extra-xylary fibres in the adaxial position on the branch; this makes it unique among seed plants and unlike the tension wood of angiosperms (Tomlinson 2001b, 2003; see also Höster & Liese 1966). Indeed, in Ephedra these fibres seems not to function as reaction wood (Montes et al. 2012). Ovule size in angiosperms does not increase between pollination and fertilization, while the ovule in Gnetum increases appreciably in size during this period, with some gametophyte development continuing after fertilization (Leslie & Boyce 2012). Other characters in common between the two such as fast pollen tube growth (Williams 2008) have been deconstructed in the same way, although whether there are comparable differences in the loss of sperm cilia and the associated development of a pollen tube growing towards the ovule and in the increased venation density of the leaves of Gnetum (Boyce et al. 2009) is unknown. Finally, details of leaf development, particularly the expression of members of the WOX (Wuschel-related homeobox) gene family, are similar in Gnetum and angiosperms; there are fewer similarities with other gymnosperms (Nardmann & Werr 2013).

Interestingly, in an experimental study on "basal" chordates, it was found that as organisms decayed later-derived characters tended to become unrecognisable before earlier-derived characters, hence fossils tended to take up a more "basal" position in the tree than they should (Sansom et al. 2010, 2011; Sansom 2015: how to interpret missing data). Even in extant plants, phylogenetic analyses using morphological data alone may face difficulties, and given our current state of knowledge, relying on a topology determined by morphological analyses of fossils seems a bit optimistic. Our understanding of fossils will need to be much improved for a phylogeny whose topology is determined by fossil morphology to be convincing. Of course, the argument, morphology with/without better/worse than molecules, is independent of the group being studied (see e.g. Springer et al. 2007 for mammals).

Sister-group relationships between Gnetales and angiosperms are strongly questioned in most analyses of molecular data, even if the monophyly of extant gymnosperms sometimes still seems problematic. Thus Gnetales may be sister to a clade including all other seed plants (e.g. Sanderson et al. 2000: two genes, third positions only; Seider et al. 2002: rbcL gene only; Rydin et al. 2002: nuclear genes only; Rai et al. 2003: large chloroplast data set; Quandt et al. 2004: trnL intron; C.-S. Wu et al. 2012b: LBA, 2013: some analyses). Extant gymnosperms would then be paraphyletic (see also Burleigh & Mathews 2004). In another wrinkle of the issue of the monophyly of extant gymnosperms, Mathews et al. (2010) suggested a [cycad + angiosperm] clade, although no support values were given, other gymnosperms formed a sister clade; morphological data optimised using this topology as a constraint tree yielded little bootstrap support and posterior probabilities from unconstrained analyses were very low (Mathews et al. 2010).

There is further discussion on the relationships of Gnetales in the context of a position in or near Pinales (q.v.).

Gymnosperms In General. Several studies suggest that Cycadales might be sister to all other extant gymnosperms (Hasebe 1997 for early literature). Variation in some morphological characters is consistent with this position, thus L. Wang et al. (2011) thought that the embryological similarities between Ginkgo and Cycadales were plesiomorphic and the other morphological similarities between Ginkgo and Pinales were apomorphies. Features supporting a [Ginkgoales + Pinales] clade include: tree branched; wood pycnoxylic; tracheid side wall pits with torus:margo construction, bordered; phloem with scattered fibres alone [Cycadales?]; axillary buds at at least some of the nodes; microsporangiophore/filament simple with terminal microsporangia; microsporangia abaxial, dehiscing by the action of the hypodermis [endothecium].

A clade [Ginkgoales + Cycadales] is increasingly frequently being recovered, perhaps especially in maximum parsimony analyses and in analyses using chloroplast data (Schmidt & Schneider-Poetsch 2002; Qiu et al. 2006a; Raubeson et al. 2006: 61 plastid genes; Wu et al. 2007: 56 cp protein-coding genes; Chumley et al. 2008; Finet et al. 2010; Soltis et al. 2011: weak support; Moore et al. 2011: weak support; Lee et al. 2011; and Ruhfel et al. 2014 and Z. Wu et al. 2014, both whole chloroplast genomes; Magallón et al. 2015; also Davis et al. 2014a: see below). In a careful series of studies by C.-S. Wu et al. (2013), the clade [Ginkgoales + Cycadales] was consistently recovered in amino acid analyses, being unaffected by taxon sampling, tree-building methods, and the like. The position of the two was much less stable in nucleotide analyses, and there the inclusion of the highly variable third position was in appreciable part to blame (C.-S. Wu et al. 2013). The clade [Ginkgoales + Cycadales] was recovered in the transcriptome analyses of Wickett et al. (2014). Xi et al. (2013b: much nuclear and plastid data, few taxa) also recovered this relationship in most analyses, and only with concatenation analyses of few (25) subsampled platid genes did Ginkgo move to become sister to all other gymnosperms. On balance, the hypothesis of a [Ginkgoales + Cycadales] clade is preferred, and the main tree has been modified accordingly (ii.2014); most of the features at the end of the preceding paragraph are thus features of all seed plants.

It has also been suggested that Gnetales are sister to all other extant gymnosperms. Thus Schmidt and Schneider-Poetsch (2002: see also Samigullin et al. 1999) looked at patterns of duplication of PHY genes, and Gnetales were sister to all the rest since they had fewer duplicated genes - assuming that they had not been lost. A whole genome duplication found only in cycads, conifers, and Ginkgo also separates Gnetales from other extant gymnosperms (Barker et al. 2010). The relationships [Gnetales [Pinales [Cycadales + Ginkgoales]]] were also found in an analysis of large amounts of nuclear gene data from 101 genera of seed plants (E. K. Lee et al. 2011: see also Cibrián-Jaramillo et al. 2010: most data from ESTs, much missing; Shanker et al. 2011: no Ginkgo; Magallón et al. 2015; and by Wickett et al. (2014) in coalescent-based transcriptome analyses.

On balance, extant gymnosperms appear to be monophyletic (e.g. Goremykin et al. 1996, Raubeson 1998; Frohlich & Parker 2000: duplication of Floricaula/LEAFY gene; Antonov et al. 2000; Winter et al. 2000; Bowe et al. 2000; Sanderson et al. 2000; Chaw et al. 2000; Pryer et al. 2001a; Aris-Brosou 2003; Magallón & Sanderson 2002; Qiu et al. 2006: support weak; Xi et al. 2013b; etc.).

Papers in this area pay much attention to methodology. Hilton and Bateman (2006) discussed sampling in morphological and molecular phylogenies (Bateman et al. 2006b, much else besides). From their point of view, molecular studies are inherently flawed because the sampling cannot be improved, while more fossils can always be included in morphological studies, and they allowed only a slight possibility that their morphology-based tree could be superseded (Hilton & Bateman 2006; see also Farjon 2007). Thus 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; Zhong et al. 2010). Long-branch attraction involving the branch leading to angiosperms (Rydin & Källersjö 2002; Stefanovic et al. 2004; Geuten et al. 2007: discussion of rather easier - although still difficult - examples) may affect the results of molecular studies, especially the position of Gnetales, but this is very hard to deal with given the relatively few extant gymnosperms. Coalescent and concatenation analyses may also produce different results, perhaps because of the signal produced by fast evolving sites in the latter (Xi et al. 2013b).


Biflavonoids +; cuticle wax tubules with nonacosan-10-ol; ferulic acid ester-linked to primary unlignified cell walls; phloem 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, Strasburger/albuminous cells associated with sieve tubes, the two not derived from the same immediate mother cell, phloem fibres +, scattered; stomatal poles raised above pore, no outer stomatal ledges or vestibule, epidermis lignified; sclereids +, ± tracheidal transfusion tissue +; buds perulate/with cataphylls; lamina development marginal; plants dioecious; microsporangium with exothecium; pollen tectate, infratectum alveolate [esp. saccate pollen], endexine lamellate at maturity, esp. intine with callose; ovule unitegmic, with pollen chamber formed by breakdown of nucellar cells, nucellus massive; ovules increasing considerably in size between pollination and fertilization, but aborting unless pollination occurs; ovule with pollination droplet; pollen germinates in two or more days, tube with wall of pectose + cellulose microfibrils, branched, growing at up to 10(-20) µm/hour, haustorial, breaks down sporophytic cells; male gametophyte of two prothallial cells, a tube cell, and an antheridial cell, the latter producing a sterile cell and 2 gametes; male gametes released by breakdown of pollen grain wall, with >1000 cilia, basal body 800-900 nm long; fertilization 7 days to 12 months or more after pollination, to ca 2 mm from receptive surface to egg; female gametophyte initially with central vacuole and peripheral nuclei plus cytoplasm, cellularization/alveolarization by centripetal formation of anticlinal walls, the inner periclinal face open, with a single nucleus connected to adjacent nuclei by spindle fibres; seeds "large" [ca 8 mm3], but not much bigger than ovule, with morphological dormancy; testa mainly of coloured sarcoexotesta, scleromesotesta, and ± degenerating endotesta; first zygotic nuclear division with chromosomes of male and female gametes lining up on separate but parallel spindles, embryogenesis initially nuclear, embryo ± chlorophyllous; gametophyte persists in seed; nuclear genome size 8-32(-76) pg [1 pg = 109 base pairs]; two copies of LEAFY gene [LEAFY, NEEDLY] and three of the PHY gene, [PHYP [PHYN + PHYO]], second intron in the mitochondrial rps3 gene [group II, rps3i2].

Age. This clade may be (382-)366(-344) m.y.o. (Won & Renner 2006), (337-)316(-306) m.y.o. (Clarke et al. 2011), ca 311.6 m.y.o. (Magallón et al. 2013), or >315 m.y. (Crisp & Cook 2011). Some estimates are as little as ca 150 m.y.a. (Z. Wu et al. 2014) or 180-140.1 m.y.a. (Naumann et al. 2013), but these are unlikely. (285.3-)224.1(-165.4) m.y. is the age in Zhang et al. (2014), and ca 271 m.y.a. in Magallón et al. (2015). From the tree in Leslie et al. (2012: Gnetum, etc., not included) one can estimate an age of ca 325 m.y.; other ages for this node are (316-)302, 301(-293) m.y. (Smith et al. 2010; see Table S3); P. Soltis et al. (2002) offer a variety of estimates.

If Pinales are sister to all other extant conifers (see above), the age of this node must be well over 200 m.y., the oldest fossils assigned to Pinales being Rissikia (Podocarpaceae: Townrow 1967) at ca 220 m.y.o. (see Eckert & Hall 2006; Rothwell et al. 2012).

Note: Possible apomorphies are in bold. However, the actual level at which many of these features, particularly the more cryptic ones, should be assigned is unclear. This is partly because many characters show considerable homoplasy, in addition, basic information for all too many is very incomplete, frequently coming from taxa well embedded in the clade of interest and so making the position of any putative apomorphy uncertain. Then there is the not-so-trivial issue of how ancestral states are reconstructed (see above).

Evolution. Divergence & Distribution. Crisp and Cook (2011; also Davis & Schaefer 2011) discuss the patterns of diversification in extant gymnosperms, emphasizing their high rates of extinction compared to those of angiosperms. Much speciation has been relatively recent, i.e. Caenozoic, despite the antiquity of some of the genera (e.g. Nagalingum et al. 2011; Leslie et al. 2012; X.-Q. Wang & Ran 2014 and references).

Much of the characterisation of extant gymnosperms may apply to that of all extant seed plants (see above). Stevenson (2013) summarized morphological variation among extant gymnosperms.

Lee et al. (2011) discussed character evolution in the context of the relationships [Gnetales [Pinales [Cycadales + Ginkgoales]]], 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 be ancestral in the gymnosperms (plesiomorphic)". That is, such a loss would be an apomorphy for [angiosperms + extant gymnosperms], and the motility of the male gametes of cycads would need to be restored by regaining cilia, etc. - Dollo would be decidedly unhappy. This aside, other aspects of character evolution interpreted in the context of this topology still need not be the same as in the Anthophyte hypothesis (c.f. Lee et al. 2011). But here, as elsewhere, simple parsimony is a rather blunt instrument to use when thinking of character evolution.

Ecology & Physiology. Extant gymnosperms are notable for showing an increase in the ratio of leaf mass per area, i.e., a decrease in SLA (Cornwell et al. 2014).

Endoplasmic reticulum associated with the phloem sieve areas may expand if damaged, so blocking flow through the sieve tube (Evert 1990; Schulz 1992 and references).

Pollination Biology & Seed Dispersal. In extant gymnosperms unfertilised ovules are relatively large compared to the seed since they keep on growing until fertilization occurs, which may be a long time after pollination; if pollination does not occur, the loss to the plant is quite substantial (Haig & Westoby 1989). Sakai (2013) suggested that this rather protracted gametophytic stage represents an evolutionarily stable strategy; at fertilization little more in the way of nutrients is needed for the development of the embryo.

For pollination in gymnosperms, see Stützel and Röwekamp (1999b).

Givnish (1980) discussed the general correlation of monoecy with dry disseminules and dioecy with fleshy disseminules.

Genes & Genomes. Most gymnosperms have large to massive nuclear genomes - and chromosomes - largely because of the number of repetitive elements, and pseudogenes are much more common than functional genes (Nystedt et al. 2013; see also Ickert-Bond et al. 2014; X.-Q. Wang & Ran 2014; c.f. in part Leitch et al. 2001, 2005). Reductions in genome size have probably occurred in Podocarpaceae and in particular in Gnetum, so increase in size in gymnosperms in general is not totally a one-way ticket (c.f. Bennetzen & Kellogg 1997). This increase in size, in Pinales, at least, seems not to be caused by whole genome duplication (Nystedt et al. 2013); endopolyploidy has not been reported here (Barow & Jovtchev 2007). For the duplication of the phytochrome gene, see Schmidt and Schneider-Poetsch (2002); although Gnetaceae appear to have only two copies, one may have been lost.

Both plastids and mitochondria are transmitted paternally in Pinales, although in a few taxa like Taxus mitochondrial transmission is both paternal and maternal or entirely maternal (X.-Q. Wang & Ran 2014). The few records in other gymnosperms all suggest that maternal plastid transmission is widespread (see Moussel 1978: Ephedra; Chesnoy 1987; Neale et al. 1991; Mogensen 1996: summary for Pinales; Cafasso et al. 2001: Encephalartos; Wilson & Owens 2006: podocarps).

Rai et al. (2003) noted that Ginkgoales and Cycadales had a reduced rate of molecular evolution in the chloroplast genome and an elevated transition:transversion ratio. Variation in the mitochondrial genomes is quite extensive but poorly understood (X.-Q. Wang & Ran 2014 and references); for the rps3 gene, see Ran et al. (2010).

Chemistry, Morphology, etc. Roots of gymnosperms tend to be thicker than those of angiosperms, although data are few (Comas et al. 2012 and references). For root nodules, see Khan and Valder (1972); they lack both root cap and apical meristem, and the end of the vascular tissue is completely surrounded by endodermis. They are found in some fossils, and their position on the tree is uncertain. Where to put pits with a margo-torus structure on the tree is unclear (Bauch et al. 1972: pit membrane variation in gymnosperms); here their origin is placed within the gymnnosperm clade, although they are also found in a few angiosperms. Microfilament-rich peripheral phloem cells may be restricted to this clade (Pesacreta 2009). The nucleus in mature phloem cells of all(?) gymnosperms is degenerated and pycnotic (c.f. 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 Sciadopitys), but which has bordered pits and functions in water transport, see Hu and Yao (1981: little information from Cycadales) and Brodribb et al. (2007). There seem to be few reports 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 grains often also being saccate, the distinction may 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). In a number of gymnosperms, including Cycadales, Taxaceae, Gnetum, etc., the ovules have a nucellar cap (Singh 1978).

The actual process of cellularisation of the gymnosperm embryo is apparently similar to that in the endosperm of flowering plants (Fineran et al. 1982 and references). Dogra (1993) compared early embryo development in Ginkgo and cycads, finding a number of differences between them (see characterizations). For an 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). Dörken (2014) noted that the embryo was chlorophyllous even in taxa with cryptocotylar germination.

For general information, see Walters and Osborne (2004), for anatomy, seee Greguss (1968), for additional information on the cellular organization of the shoot apex, see Johnson (1951), for sieve tube plastids, see Behnke (1974: starch grains often club-shaped) and Behnke and Paliwal (1973), for seed lipids, see Wolff et al. (1999), for reports of double fertilization (well attested only in Gnetales), see Friedman (1992); for pollen tube growth, see Williams (2008) and Abercrombie et al. (2011), and for the female gametophyte, see Maheshwari and Singh (1967).

Phylogeny. For discussion on the relationships of extant seed plants, see above. Given the uncertainty in our knowledge of the relationships between the major seed-plant clades - although this is decreasing - here are direct links to Cycadales, Gnetales, Ginkgoales, flowering plants, and Pinales.

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

[Ginkogoales + Cycadales]: mucilage +; cataphylls +; 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, cilia numerous; seeds with coloured sarcoexotesta, scleromesotesta, and ± degenerating endotesta; germination hypogeal, cryptocotylar.

Age. The age of this node is estimated to be around 158 m.y. (Magallón et al. 2015).

CYCADALES Dumortier  Main Tree.

Stout, unbranched treelets; roots and stems with contractile tissue; ß-methylamino-L-alanine and compounds producing azoxyglycosides +, unique biflavones, polysaccharide gums/mucilage copious, in canals, (S [syringyl] lignin units common [positive Maüle reaction] - Stangeria); successive cambia in roots; apogeotropic coralloid roots with N-fixing Nostoc or Anabaena, cork cambium in these roots, at least, superficial, root hairs 0; shoot apex massive, primary thickening meristem +; cone dome +; stem centrifugally polyxylic; cortical steles +; wood manoxylic, large amounts of secondary phloem persisting; reaction wood 0; pith cell packets; nodes of foliage leaves multilacunar, traces girdling; protoxylem poles changing from endarch in the stem to exarch in the leaf traces; (bundles with abaxial xylem in the periphery of the pith); petiole vascular bundles in inverted omega shape; leaf vascular bundles amphicribral; epidermal cells with perforations; internodes short; axillary buds 0; leaves large, pinnate; microsporangia in synangia, many/sporophyll, abaxial, exothecium +; megasporophylls with terminal sterile portion; integument free only in apical portion; pollen tube wall with abundant pectins, microgametophyte with one prothallial cell; megasporophylls in simple strobili; young embryo with cells tending to congregate at the chalazal end, at micropylar end divisions fewer and wall development slower, suspensor cells ± elongated; sarcoexotesta and inner fleshy layer both vascularized; 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.

Age. The Cycas lineage may have diverged from Zamiaceae by the Permian, at least 250 m.y.a. (Hermsen et al. 2006a; see also Bogler & Francisco-Ortega 2004). Magallón et al. (2013: with temporal constraints) suggested an age of around (181-)171.5(-167) m.y., Salas-Leiva et al. (2013) an age of (271-)223(179) m.y., while Crisp and Cook (2011) estimated the age at over 260 m.y. and Won and Renner (2006) an age of (307-)283(-271) m.y.. Alternatively, it has been suggested that Zamiaceae diverged from Cycas only ca 92 m.y.a. (see Wink 2006; Treutlein & Wink 2002; Nagalingum et al. 2009). This is another case where age estimates are hopelessly at odds.

Cycads (the term refers to the whole order) are known fossil from the Upper Palaeozoic 290-265 m.y.a. and are derived from Palaeozoic pteridosperms (Mamay 1969; Gao & Thomas 1989); cycads were particularly diverse in the Jurassic-Cretaceous period. The Permian Antarcticycas may be sister to crown-group Cycadales, while Crossozamia, from ca 270 m.y.a., may be sister to extant Cycadaceae (Hermsen et al. 2006a); for fossils, see also Pant (1987).

Note: Possible apomorphies are in bold. However, the actual level at which many of these features, particularly the more cryptic ones, should be assigned is unclear. This is partly because many characters show considerable homoplasy, in addition, basic information for all too many is very incomplete, frequently coming from taxa well embedded in the clade of interest and so making the position of any putative apomorphy uncertain. Then there is the not-so-trivial issue of how ancestral states are reconstructed (see above).

Evolution. Divergence & Distribution. Dispersal by continental drift across more or less continuous land had earlier been invoked to explain the scattered distribution of species of apparently ancient groups like Cycas with propagules that could not float (Dehgan & Yuen 1983).

And why are there so few cycads? Olsen and Gorelick (2011) find no evidence of whole genome duplication in the clade (or in Ginkgo). This might reduce the amount of speciation and also curtail various developmental changes - but the venation density of the leaves, absence of axillary branching, and a variety of other features could equally reasonably be invoked. There have been a number of Caenozoic bouts of speciation of cycads (see below); perhaps extinction has been higher in gymnosperms in general than in angiosperms (Crisp & Cook 2011).

Artabe and Stevenson (1999) suggest a number of possible apomorphies for the clade, while Hill et al. (2003) provide a useful list of characters varying within Cycadales (see also Hermsen et al. 2006a).

Pollination Biology & Seed Dispersal. The sometimes quite close association between the insects that commonly pollinate Cycadales are probably relatively recent (Downie et al. 2008). For the aerodynamics of cycad pollen, see Hall and Walter (2011); the pollen tends to clump, as is common in animal-pollinated taxa. See also Terry et al. (2012a, b) for what is known about pollination in the group - often by beetles, especially weevils - and Roemer et al. (2013) for records of thermogenesis.

Cycadales often live in rather open, fire-prone habitats, and reproductive events occur after burns (Lamont & Downes 2011). Animal dispersal of the seeds, which are large, often brightly coloured, and with a fleshy outer layer, is likely for most genera.

Plant-Animal Interactions. A few brightly-coloured caterpillars, in particular those of lycaenids like the genus Eumaeus, also beetles, eat cycads in the neotropics (Schneider at al. 2002; Prado et al. 2014 for references). They rarely eat old leaves, which are too tough, or very young leaves, which have very high azoxyglycoside concentrations; the highly toxic methyl-azoxymethanol core is released by glycosidases, and this deters generalist herbivores (Prado et al. 2014). The conspicuous eumaeid caterpillars are distasteful to potential predators, and orsodacnid beetles also sequester the azoxyglycosides (Prado et al. 2014 and references: see also below under Zamiaceae); in general, however, few insects eat Cycadales.

Cycads are noted for having some rather potent toxins that 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 is a possible neurotoxin, while MAM can cause severe digestive upsets, cancers, etc. (Brenner et al. 2003 and references).

Bacteria/Fungal Associations. The nitrogen-fixing cyanobacteria Nostoc and Anabaena are probably to be found in all cycads (Rai et al. 2000 for a review). 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). Fixation of nitrogen has been demonstrated (Vessey et al. 2004 and references); it is translocated to the host as citrulline and glutamine, or sometimes just as the latter (Costa & Lindblad 2002). Several species of Nostoc have been found in Australian species of Macrozamia and there is no host specificity (Gehringer et al. 2010). The toxic ß-methylamino-L-alanine (BMAA, see above) is probably produced by these cyanobacterial associates of cycads (Cox et al. 2005).

Genes & Genomes. There is no correlation between chromosome number and genome size in Cycadales; number changes are probably the result of chromosome fissions or fusions (Gorelick et al. 2014).

Chemistry, Morphology, etc. 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). Superficial cork may be paricularly well developed in the coralloid roots, and its presence may also be connected with the reported absence of root hairs in cycads (Vessey et al. 2004). Tomlinson et al. (2014) recorded the presence of gelatinous fibres (g-fibres) in the roots of both Cycas and Zamia that are involved in contraction in length of the root.

The shoot apex is notably wide, being 500-3,300 µm across, sometimes increasing dramatically with the age of the plant (Clowes 1961; Stevenson 1980); a primary thickening meristem is also developed which is responsible for the development of the characteristically stout cycad stems (Stevenson 1980). 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). Coulter and Chamberlain (1917) described the vascularisation of the young leaves of Ceratozamia; the cotyledons have split lateral vascular traces. The leaf traces become mesarch or are endarch near the base and exarch in the upper portions (Chamberlain 1935). There is transfusion tissue in the leaf.

Mundry and Stützel (2003) found that sporangia in Zamia developed on a lateral lobe of the microsporophyll, which were thus basically pinnate in construction. Individual sporangiophores had a radial construction, and they suggested a link to medullosan pteridosperms; this morphology is unlike that of other extant gymnosperms (Mundry & Stützel 2003). The tapetum plays no part in the formation of the sporoderm. There are up to perhaps 40,000 cilia per male gamete.

There are several excellent general references and bibliographies, including Gifford and Foster (1988), Johnson and Wilson (1990), Stevenson (1990), Norstog and Nicholls (1997: I have used this a great deal), Schneider et al. (2002: biology and evolution), Friis et al. (2011), Stevenson et al. (2012: proceedings of a symposium), and The Cycad Pages (Hill & Stevenson 2002 onwards); see also the Gymnosperm Database. For branching, see Stevenson (1988), neurotoxic compounds, Whiting (1989), anatomy, see Artabe and Stevenson (1999), embryology, see Singh (1978), and for a coleorhiza in the seedling, see Robbertse et al. (2011).

Phylogeny. Cycas is sister to other cycads.

Classification. There are good morphological characters supporting the division of the order into two families (K. D. Hill et al. 2003).

See Jones (2002) for an account of all taxa, Walters and Osborne (2004) for problems of species delimitation, etc., Christenhusz et al. (2011b) for a linear classification, and Osborne et al. (2012) for a list of included taxa.

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


Hairs transparent; outer wall of epidermis pitted; leaf bases persistent, leaflets circinate, (dichotomously divided), midrib +, secondary vasculature diffuse; megasporophylls not forming a determinate cone, margins lobed or toothed; ovules (1-)3-8/sporophyll, erect; seeds platyspermic; n = 11; tenfold increase in mitochondrial tandem repeat sequences, Bpu mobile sequences.

Age. Diversification within Cycas may have begun ca 36 m.y.a. (see Wink 2006; Treutlein & Wink 2002; Nagalingum et al. 2009).

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

Evolution. Pollination Biology & Seed Dispersal. In Cycas beetle larvae eat the male cones, and hasten the reproductive process as they do so (Marler 2010); see also Roemer et al. (2013) for thermogenesis. Wind pollination may also occur (Kono & Tobe 2007.

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).

Genes & Genomes. For the distinctive mitochondrial genome of Cycas, which may even include some self-replicating elements, see Chaw et al. (2008), and for the chloroplast genome of Cycas taitungensis, see C.-S. Wu et al. (2007).

Chemistry, Morphology, etc. For a detailed survey of leaflet anatomy, see Griffith et al. (2014).

ZAMIACEAE Horaninow Back to Cycadales


S [syringyl] lignin units common [positive Maüle reaction - syringyl:guaiacyl ratio more than 2-2.5:1]; (cone dome 0); (cortical steles 0); (stem not polyxylic); hairs coloured; (cataphylls 0); leaflets (circinate - Bowenia), lacking a midrib (midrib + Stangeria), secondary veins regular, subparallel; megasporophylls forming a determinate cone, peltate; ovules 2(-3)/sporophyll, inverted; seeds radiospermic; n = 8, 9 [Zamia variable], (13).

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

Age. Downie and Donaldson (2005) dated divergence within Zamiaceae to ca 94 m.y.a., and the estimate in Salas-Leiva et al. (2013), at (111-)91(-70) m.y., is similar, while around 185 m.y. is the age suggested by Crisp and Cook (2011).

If the assignment of fossils like Kurtziana to near Zamia are correct, a crown-group age of over 200 m.y. is likely (Wilf & Escapa 2014). Thus morphological analysis of fossil and extant Cycadales, including a new Late Cretaceous fossil from Argentina, had that fossil and many others embedded well within Zamiaceae, where [Bowenia + Stangeria] were sister to rest of the family (Martínez et al. 2012). This would also suggest an older age for crown-group diversification.

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

Diverification within many genera in Cycadaceae may have happened more or less synchronously in the late Miocene, extant species being a mere 12 m.y.o. or so at most (Nagalingum et al. 2011). Crisp and Cook (2011) also thought that diversification within all cycad genera was Caenozoic (the spread of ages for Zamia does extend into the later Cretaceous), but was not synchronous, while Salas-Leiva et al. (2013) gave stem ages of the genera of 75-33 m.y., although divergence within the genera was only late Miocene at the earliest. The relatively recent development of particular pollination associations may have contributed to diversification in Encephalartos, Macrozamia, etc., in the (late) Caenozoic (Oberprieler 2004).

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; Peñalver et al. 2012 for references to thrip pollination). Thermogenesis has been detected in the strobili of some Cycadales (Seymour 2001). Wind pollination may also occur (Suinyoy et al. 2009: Cucujoidea also involved).

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. In S.E. Africa a group of brightly coloured diptychine geometrids (loopers) with brightly-coloured caterpillars is more or less restricted to cycads (Cooper & Goode 2004).

Chemistry, Morphology, etc. Stangeria is perhaps particularly distinctive: it develops buds from its roots, it lacks cataphylls, and its leaflets have a midrib and pinnate venation; these are derived features. 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 male gametes per male gametophyte and there are several - even hundreds - of ovules on each female gametophyte.

Phylogeny. For relationships within Zamiaceae, 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). Details of relationships in the clade remain rather unclear (support for nodes along the spine mostly low) and conflict in part, at least, with those suggested by previous morphological studies; The positions of Bowenia, Stangeria and Dioon are particularly uncertain; all three are distinctive genera. Stevenson (1992; see also Brenner et al. 2003) placed Bowenia and Stangeria in Boweniaceae, however, Chaw et al. (2005, see also Rai et al. 2003; Zgurski et al. 2008) suggested the following quite well supported relationships within Zamiaceae: [Dioon [Bowenia (not always here) [the rest - including Stangeria]]]. Dioon was also found to be sister to the rest of Zamiaceae by Crisp and Cook (2011: support strong), Griffith et al. (2012: morphology and molecules) and Gorelick et al. (2014), and this position is consistent with e.g. variation in the micromorphology of the cuticular waxes (Wilhelmi & Bartlott 1997), Dioon and Cycas having a plesiomorphic micromorphology. In these studies, Stangeria never forms a clade with Dioon or Bowenia.

For relationships within Encephalartos, which may have split from Lepidozamia as recently as 5-20 m.y.a., see Treutlein et al. (2005).

Classification. Zamiaceae are circumscribed broadly - the family is not very big. Chaw et al. (2005) suggest a realignment of generic limits throughout the family.

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