LIGNOPHYTA Back to Main Tree
True roots +, origin endogeneous, root cap +, apex multicellular; endodermis +; shoot apical meristem multicellular; lateral meristems +, cork cambium producing cork abaxially, vascular cambium producing phloem abaxially and xylem adaxially; lamina with mean venation density 1.8 mm/mm2 (to 5 mm/mm2).
SEED PLANT EVOLUTION (very much under development)
Age. ignophytes are sister to the monilophytes, i.e. ferns and their relatives, and the two split in the mid- to later Devonian, some 375-400 m.y.a. (Pryer et al. 1995, 2000, 2001a, 2004; Schneider et al. 2002; Stein et al. 2012).
Evolution. Divergence & Distribution. The origins of extant seed plants, the focus of this site, are to be sought in mid-Devonian lignophytes, the progymnosperm 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).
It is still unclear when the megaphylls that characterise nearly all seed plants, fossil and extant, evolved - they certainly evolved several times (Tomescu 2009) - 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 may represent a modified branch system. However, it is an open question whether or not seed plant megaphylls arose in parallel with those of ferns (Boyce 2005a summarizes earlier literature, 2008), 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. The well-developed vascular system that resulted from secondary thickening permitted increased transpiration and also allowed the evolution of large, dorsi-ventrally flattened photosynthetic leaves that facilitated CO2 uptake (Raven & Edwards 2001). The possibility that such leaves might overheat was reduced because of evaporative cooling (Beerling et al. 2001; Beerling 2005a and references).
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). Heterospory has evolved several times in land plants (Bateman & DiMichele 1994 for a review). Some Archaeopteridales and Aneurophytales were heterosporous; Archaeopteris has even been found in the same fossil beds as fossilized seeds (see e.g. Beck 1981 and references). Mega- and microspores may be mixed in a single sporangium in some Aneurophytales, and when separate, megasporangia may produce several megaspores (Bateman & DiMichele 1994); megaspores are not always larger than microspores.
Extant heterosporous plants produce microspores ("pollen") in microsporangia and a maximum of four megaspores per megasporangium (Kenrick & Crane 1997). In seed plants the megasporangium is borne in an ovule, with is made up of the megasporangium proper, the nucellus being the megasporangium wall, that is more or less enclosed by one or more integuments, which may be deepy lobed; the ovum that develops from the megaspore is pollinated and fertilized when in the ovule. Extant seed plants are distinctive because they usually have only a single megaspore/ovule and also because their aporangia are not borne on leaves, rather, they develop as separate structures (see Boyce 2005b). The embryo that develops from the fertilized egg (and so ultimately from the megaspore) receives its nutrition from a gametophyte that is retained in the ovule; it depends directly or indirectly on the parental sporophyte for nutrition; embryo development in other heterosporous land plants is dependent on the gametophyte. The seed is a fertilized ovule; seed plants are all heterosporous plants that produce seeds. Bateman and DiMichele (1994: esp. fig 13) carefully dissect 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. may have had a lagenostome and probably pollination/fertilization mechanisms more like those of seed plants. Gerrienne et al. (2004) described the ovules of Runcaria, a seed plant and probably to be assigned to Aneurophytales and from the middle Devonian of some 385 m.y.a.; it lacked a lagenostome, a columnar projection of the nucellus or sporangium wall that was probably involved in pollen capture, and Gerrienne et al. (2004) suggest that the antherozoids reached the megagametophyte by lysis of the megasporangium wall, which forms a long, terminal projection in this plant. In seed ferns and their immediate relatives pollen probably germinated via the adaxial surface, the tetrad of megasopores is linear, and 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 with fern-like leaves and ovules, these are the seed ferns or pteridosperms. Indeed, although the Carboniferous has been called the age of ferns, but more accurately it is the age of seed ferns. Recent studies are helping to clarify their morphology, although is is difficult to reassemble 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) - even 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.).
Manoxyly, with broad pith, not much secondary thickening that contains much parenchyma, etc., versus pycnoxyly, with a narrow pith and much secondary thickening, and radiospermy versus platyspermy are unlikely to represent fundamental distinctions, especially if Bennettitales are close to Gnetales (see below). Xylem in the short shoots of Ginkgo is manoxylic and in the long shoots, pycnoxylic (Gifford & Foster 1988; Little et al. 2013), while 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).
Ecology & Physiology. There is quite a diversity of early land plants with 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, and secondary thickening may have evolved several times (Gerrienne et al. 2011; Hoffman & Tomescu 2011, 2013: see also Donoghue 2005; Rothwell et al. 2008b for wood evolution in general). For a general discussion about the evolution of growth forms in lignophytes, see Rowe and Speck (2005: cambium as a nascent innovation), Gerrienne et al. (2011) and Stein et al. (2012).
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). 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. (Algeo et al. 2001). 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. 2012).
Burnham (2009) noted the relative abundance of climbers in the Carboniferous fossil record, although they became much less common, remaining so until the Cretaceous or Tertiary. 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 that probably had water conductivity on a par with that of some extant angiosperms with vessels (Wilson & Knoll 2010).
The first lignophytes were small, and Gerrienne et al. (2011) suggest that it was 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). As atmospheric CO2 decreased, stomatal density and hence transpiration increased (Franks & Beerling 2009). The well-developed vascular system that resulted from secondary thickening permitted this increased transpiration, supplying the dorsi-ventrally flattened photosynthetic leaves/megaphylls that facilitated CO2 uptake (Raven & Edwards 2001). The possibility that such leaves might overheat was reduced because of evaporative cooling (Beerling et al. 2001; Beerling 2005a and references). Overall, photosynthesis and the sequestration of carbon by plants increased, and global carbon and nutrient cycling and energy flow was dramatically changed (Qiu et al. 2012).
For a good general summary of fossils and what they disclose about plant physiology in the past, see Boyce (2009). Understanding the evolution of stomatal functioning may be a 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). However, if evidence from extant land plants is any guide, there have been changes in how stomatal opening and closure is controlled. 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). However, 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, stomata responding to abscisic acid. 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). If water loss is rapid in angiosperms, the subsidiary cells lose turgor first, 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. 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 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-cur (Haworth et al. 2013).
Roots are also implicated in these early changes via a complex series of feed-back loops (e.g. Raven & Edwards 2001; Beerling & Berner 2005). The true roots of lignophytes penetrated deeply into the ground, some one metre or so, so greatly facilitating weathering by enabling carbon dioxide to penetrate to greater depths and also producing chelates and organic acids, while decay of organic litter produces carbonic and other organic acids (Berner 1997; Algeo et al. 2001; Raven & Edwards 2001; Beerling 2005a; Taylor et al. 2009; Quirk et al. 2012); note that lignin-decomposing fungi were unlikely to have been around. This plant-aided chemical weathering of rocks entails the loss of CO2 as it reacts with rock minerals, and so atmospheric CO2 concentration becomes further reduced. Silicates are converted into bicarbonates and aluminium silicates. The former may be carried to the sea where it can be precipitated out, and the latter form the basis of clays. 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).
Nutrients in the rocks are released in the course of weathering, and the increased nutrients in water drainage could lead to algal blooms and may be connected with marine anoxic episodes; in the later Devonian there was some glaciation as well as the die-off of Palaeozoic reefs, perhaps connected with these changes (Algeo & Scheckler 1998; Algeo et al. 2001).
Carbon in plant material is likely to have been buried by the accumulating sediments produced by rock weathering (Beerling 2005a). Indeed, there is no evidence of lignin-destroying fungi in the middle Palaeozoic (Floudas et al. 2012), so much carbon fixed in photosynthesis is likely to have been sequestered in sediments (and later converted to the great Carboniferous coal deposits), although there may have been some photodegradation of lignin (for which, see Austin & Ballaré 2010). Protective secondary metabolites may have evolved about this time, and they would decrease CO2 produced by respiration of organisms that would have decomposed the plants (Retallack 1997a). Millipedes were early detritivores.
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. Through the Devonian there had been a major draw-down of carbon dioxide in the atmosphere - some 90% over the late Palaeozoic - and a great increase in oxygen (see below). Thus estimates of the carbon dioxide concentration in the atmosphere at the end Silurian are 4-20 times the pre-industrial concentration of 270 ppmV, 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; Pangea formed around 320 m.y.a., and this would have increased chemical weathering and so aided in the CO2 decrease.
The capability to degrade lignin seems to have evolved in the ancestor of the Agaricomycetes clade (372-)290(-222) m.y.a., somewhere around the beginning of the Permian, and this is consistent with the fossil record (Floudas et al. 2012). Peroxidases play a central role in lignin degradation, and by effectively burning off the lignin, fungi can access and degrade additional sources of cellulose and use it as a source of energy, at the same time producing CO2, etc.. By ca 276 m.y.a. in the early Permian CO2 concentrations had rebounded to perhaps 2000-3500 ppmv (Algeo et al. 2001; Driese & Mora 2001; Montañez et al. 2007; Shi & Waterhouse 2010; Kaufman & Xiao 2012). As CO2 concentrations increased, climates became at least locally drier in western Euramerica during the early Permian, with tree ferns (pteridosperms, peltasperms) becoming less common, conifers more common (Montañez et al. 2007).
The Permo-Triassic boundary is marked by major extinctions. The global climate had become very much warmer, with a mean annual temperature increase of 8-10o C evident in rocks from both tropical and more temperate environments; atmospheric CO2 concentrations were around 1,500 ppm (Retallack & Krull 1999; Shi & Waterhouse 2010). There was extensive die-off of coniferous forest, soil erosion, and loss of peat forests (Looy et al. 1999). The world-wide "coal gap", a period when sediments with coal deposits were absent, perhaps because of the extinction of peat-forming plants, was at the end of the Permian (Retallack et al. 1996; Sun et al. 2012). Indeed, temperatures may even have become lethally hot at the equator, with the sea surface approaching 40oC and land temperatures fluctuating even higher (the current SST is 25-30oC). Under such conditions, the photosynthetic rate would have decreased and that of photorespiration increased, the latter predominating above 35o C (Sun et al. 2012). Throughout the southern hemisphere cool forest area there was increased weathering 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 for more details). Indeed, the flora changed. Thus the heterosporous lycopsid Pleuromeia sternbergii dominated for some 5 million years before being replaced by i.a. conifers like Voltzia that lacked prepollen, i.e. fertilization was by siphonogamy (Looy et al. 1999).
Carbon dioxide concentrations then decreased and temperatures cooled somewhat, but there was another major extinction event at the end of the Triassic. Again this was accompanied by an increase of atmospheric CO2 (about four-fold, from ca 600 to 2,100-3,000 ppm) and an increase in temperature of 2.5-5o C, or even more locally, and there was a massive extinction/decline in standing diversity/increase in heterogeneity of community composition of both plants and animals (McElwain et al. 1999, 2007; Huynh & Poulsen 2005; Steinthorsdottir et al. 2011); reproductively specialized plants like cycads and seed ferns seem to have been particularly affected (e.g. Mander et al. 2010) and the overall pattern of vegetation change in sites it eastern Greenland is complex (McElwain et al. 2007). This extinction can perhaps be linked to the beginning of major eruptions in the Central Atlantic Magmatic Province and it has been dated to around 201.5 m.y.a., although more than one triggering factor may be involved (McElwain et al. 2007), interestingly, eruptions with associated spikes in atmospheric CO2 continued even when biological recovery was underway (Blackburn et al. 2013). Fire activity in parts of the Northern Hemisphere, at least, increased, despite the low atmospheric oxygen concentration (Belcher et al. 2010a). High ambient temperatures may have increased leaf temperatures above the limit of lethality (45-52o C for non-succulent leaves). 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). Interestingly, in eastern Greenland the new community dominants were previously rare, while previous dominants tended to become rare (McElwain et al. 2007).
As lignophytes spread over the land, the increased photosynthesis they supported 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). Interestingly, the 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). The oxygen concentration of the atmosphere continued to increase after the end-Devonian, probably reaching a high of about 30% towards the end Carboniferous/beginning Permian during the LPIA (e.g. Shi & Waterhouse 2010), and this is close to the 35% at which plants would have burned readily even if they were not dry. Gigantism, e.g. of dragonflies and in particular fusilinid foraminferans, has been linked to this increased oxygen concentration (Payne et al. 2012). However, atmospheric oxygen concenration crashed to somewhat below current levels immediately after the end of the Permian and has shown only moderate changes since (e.g. Scott & Glasspool 2006).
There are also suggestions that lycophytes had proportionally a large amount of lignin (Robinson 1990), while litter from extant ferns and fern allies and bryophytes is slow to decompose compared to that of gymnosperms and especially angiosperms (Cornwell et al. 2008).
Pollination Biology & Seed Dispersal. Insects first appeared in the late Devonian (Garrouste et al. 2012). Insect pollination probably occurred in at least some pre-Cretaceous gymnosperms, beetles, neuroptera, mecopterids (scorpion flies, Mecoptera, perhaps) and true flies (the evolution of bee flies may be early Jurassic - see Wiegmann et al. 2011), thrips, as well as other groups being involved (Labandeira 1998, 2010; Grimaldi 1999; Labandeira et al. 2007; Ren et al. 2009; Peñalver et al. 2012). Thrip, beetle, fly and moth pollination are all known in extant gymnosperms (Kato & Inoue 1994; Schneider et al. 2002; Oberprieler 2004; Labandeira 2005). Similarly, a number of old but not very speciose clades of weevils (Curculionoidea) and leaf beetles (Chrysomeloidea) are found on gymnosperms, including cycads, an association that has been dated to the Jurassic or earlier, and initial diversification of these insects seems to have been on those plants in the Jurassic (e.g. Labandeira et al. 1994; Farrell 1998; Mckenna et al. 2009), but this story may need to be rethought (Hunt 2007).
A number of gymnosperms, both living and extict, have saccate pollen. In general, there is a correlation between saccate pollen, erect cones, inverted or downwards-facing ovules, and the presence of a pollination droplet - although perhaps not in Cordaitales. Saccate pollen, a device to help float the pollen onto the micropyle rather than to facilitate wind dispersal of the grains, has evolved more than once (Leslie 2008, 2010b). See also Stützel and Röwekamp (1999b) for pollination of gymnosperms.
Sims (2012) suggests that during the middle Mississippian to Pennsylvanian average seed size increased to about 8 mm3, a value that held largely steady until the evolution of flowering plants; cycads (large) and pines (small) are the two ends of the size spectrum in extant gymnosperms. Seeds of Mesozoic seed plants are very diverse morphologically (e.g. Anderson & Anderson 2004). Lovisetto et al. (2012) discuss the evolution of fleshiness in disseminules of seed plants in general; similar genes are involved, even if the location of fleshiness may be very different morphologically.
Plant-Animal Interactions. Lepidopteran diversification may have begun on Jurassic gymnosperms (Labandeira et al. 1997), although this has been questioned (Grimaldi 1999).
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 duplicated genes to (352-)349, 347(-343) m.y. in the early Carboniferous (Mississippian) - the overall age spread is ca 400 to just over 250 m.y. 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. A distinction has been drawn between manoxylic and pycnoxylic taxa. In manoxylic taxa the secondary xylem has much parenchyma mixed in with the tracheids, while in pycnoxylic taxa the secondary xylem there is much less parenchyma. 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. 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. 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).
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. These ridges, haptotypic marks, mark 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, other fossils with true pollen, and extant gymnosperms, which also have true pollen, are not well understood, and it is not easy to understand the evolution of the sulcus in fossil gymnosperms (Doyle 2013); separating prepollen and pollen may be of little value (Poort et al. 1996 for a review; Taylor et al. 2009).
EXTANT SEED PLANTS / SPERMATOPHYTA
Plant woody, evergreen; nicotinic acid metabolised to trigonelline, (cyanogenesis via tyrosine pathway); primary cell walls rich in xyloglucans and/or glucomannans, 25-30% pectin [Type I walls]; lignins derived from (some) sinapyl and particularly coniferyl alcohols, thus containing p-hydroxyphenyl and guaiacyl lignin units [so no Maüle reaction]; root xylem exarch, cork cambium deep seated; arbuscular mycorrhizae +; shoot apical meristem interface specific plasmodesmatal network; stem with vascular tissue around central pith [eustele], vascular bundles with interfascicular tissue, ectophloic, endodermis 0, xylem endarch; 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 +; stem cork cambium superficial; branches exogenous; leaves with single trace from vascular sympodium ["nodes 1:1"]; vascular bundles collateral [stem: phloem external; leaf: phloem abaxial]; stomata morphology?, pore opening in response to leaf hydration active, control by abscisic acid, metabolic regulation of water use efficiency, etc.; leaves with petiole and lamina, spiral, development basipetal, blade simple; axillary buds +, not associated with all leaves; prophylls two, lateral; plant heterosporous, sporangia borne on sporophylls; microsporophylls aggregated in indeterminate cones/strobili; true pollen +, grains mono[ana]sulcate, exine and intine homogeneous; ovules unitegmic, parietal tissue 2+ cells across, megaspore tetrad tetrahedral, only one megaspore develops, megasporangium indehiscent; male gametophyte development first endo- then exosporic, tube developing from distal end of grain, to ca 2 mm from receptive surface to egg; spermatozoids two, developing after pollination, with cell walls, starch grains 0, flagellae numerous; ovules increasing considerably in size between pollination and fertilization, female gametophyte endosporic, initially syncytial, walls then surrounding individual nuclei; seeds "large" [ca 8 mm3], but not much bigger than ovule, with morphological dormancy; embryo cellular ab initio, endoscopic, plane of first cleavage of zygote transverse, suspensor +, short-minute, embryo straight, shoot and root at opposite ends [allorrhizic], white, cotyledons 2; plastid transmission maternal; ycf2 gene in inverted repeat, 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; Leebens-Mack et al. 2005). Some recent molecular estimates are rather older, ranging from (356-)327(-296) m.y. (with eudicot calibration) to (366-)330(-301) m.y. (without: Smith et al. 2010: see also their table S3), while Clarke et al. (2011: 95% credibility intervals, other estimates) suggested a still older age of (368-)351(-330) m.y. and Magallón et al. (2013: with temporal constraints) an age of around (351-)330.3-324.3(-313.1) m.y..
Evolution. Divergence & Distribution. For possible apomorphies throughout this group, see e.g. Doyle (1998a, b, esp. 2006, 2013); presence of pointed scale leaves may need to be added to the apomorphies for Spermatophyta. However, because of the probable sister group relationship between extant gymnosperms and angiosperms, many life cycle characteristics cannot be polarised. 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 also may properly be pegged as characteristic of seed plants as a whole. An example may be successive microsporogenesis with the microspore walls developing by centripetal furrowing (Nadot et al. 2008).
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.
Pollination Biology & Seed Dispersal. The seed, the next generation sporophyte more or less surrounded by gametophytic reserve tissue and in turn surrounded by the seed coat, of integumentary origin, differs from the megaspores of heterosporous pteridophytes and lycophytes in several respects. One is that the seed is much larger than the ovule, the seed precursor, which can be aborted easily if pollination does not occur (Haig & Westoby 1989), and another is that seeds themselves are very variable in size, ranging in size from 10-7 to 104 grams, i.e. smaller than megaspores to massively larger than them (Haig & Westoby 1991). For pollination in gymnosperms, see Stützel and Röwekamp (1999b).
Genes & Genomes. 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).
Chemistry, Morphology, etc. Lignins drived from p-coumaryl alcohol are uncommon, 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.
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 Beck et al. (1982: valuable), 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 [Monilophyta + Lignophyta], for venation development, see e.g. Boyce (2005b), for venation density, see Boyce et al. (2008), for stomatal morphology, see J. A. Doyle et al. (2008b), and for cuticle waxes and their composition, see Wilhelmi and Barthlott (1977).
For an analysis of the distinction between angio- and gymno-ovuly, and angio- and gymnospermy, see Tomlinson (2012); for variation in the 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); for the integument and its possible evolution, see Andrews (1963); for ovule growth, see Leslie and Boyce (2012), for the evolution of embryo size, see Forbis et al. (2002); for the mitochondrial nad1 intron 2, see Gugerli et al. (2001).
EXTANT GYMNOSPERMS / PINOPHYTA / ACROGYMNOSPERMAE Back to Main Tree
Biflavonoids +; cuticle wax tubules with nonacosan-10-ol; ferulic acid ester-linked to primary unlignified cell walls; phloem with sieve and Strasburger/albuminous cell pairs, the two not derived from the same immediate mother cell, 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, phloem fibres +, scattered; stomata subsidiary cells not produced from the same cell that gave rise to the guard cell initials [perigenous], stomatal poles raised above pore, no outer stomatal ledges or vestibule, epidermis lignified; sclereids +, ± tracheidal transfusion tissue +; buds with scale leaves/cataphylls; lamina development marginal; plants dioecious; microsporangium with exothecium; pollen tectate, infratectum alveolate [esp. saccate pollen], endexine lamellate at maturity; ovule unitegmic, with pollen chamber formed by breakdown of nucellar cells, nucellus massive; pollination droplet +, ovules aborting unless pollination occurs, fertilization 7 days to 4-6 months or more after pollination, pollen germinates in two or more days, tube with wall of pectose + cellulose microfibrils, branched, growing away from ovule 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 producing a sterile cell, gametes 2, released by breakdown of pollen grain wall, with >1000 cilia; female gametophyte with radially-elongated cells [alveoli] that grow centripetally, the nucleus of the female gamete being on the open face and connected to adjacent nuclei by spindle fibres; seed fleshy, testa mainly of coloured sarcoexotesta and scleromesotesta, ± vascularized, and ± degenerating endotesta, ± vascularized; first zygotic nuclear division with chromosomes of male and female gametes lining up on separate but parallel spindles, embryogenesis initially nuclear; gametophyte persists in seed; 2C genome size 25-32< pg [1 pg = 109 base pairs]; two copies of LEAFY gene and three of the PHY gene, [PHYP [PHYN + PHYO]], second intron in the mitochondrial rps3 gene [group II, rps3i2].
Age. This clade may be ca 311.6 m.y.o. (Magallón et al. 2013).
Evolution. Divergence & Distribution. Much of this characterisation may apply to all extant seed plants (see above). Stevenson (2013) discussed morphological variation among extant angiosperms.
Since Pinales are sister to all other extant conifers, 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). From the tree in Leslie et al. (2012: Gnetum, etc., not included) one can estimate an age of ca 325 m.y. Magallón et al. (2013: with temporal constraints) suggested an age of ca 311.7 m.y.; other ages are (316-)302, 301(-293) (Smith et al. 2010; see Table S3), while Clarke et al. (2011: 95% credibility intervals) suggested an age of (337-)316(-306) m.y..
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. Tertiary, despite the great antinquity of some of the genera (e.g. Nagalingum et al. 2011; Leslie et al. 2012).
Pollination Biology & Seed Dispersal. Sakai (2013) suggested that the rather protracted gametophytic stage in most extant gymnosperms, where the megagametophyte continues to grow, so monopolizing resources for the seed, represents an evolutionarily stable strategy; at fertilization little more is needed for the development of the embryo in particular.
Ecology and Physiology. E.R associated with the phloem sieve areas may expand if damaged, so blocking flow through the sieve tube (Evert 1990; Schulz 1992 and references).
Genes & Genomes. Gymnosperms in general have large to massive nuclear genomes (Nystedt et al. 2013; 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 in this whole clade (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.
Chemistry, Morphology, etc. 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 also found in some fossils, so their position on tree might change. 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 non-"basal" 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 Sciadpopitys), but which has bordered pits and functions in water tansport, see Hu and Yao (1981: little information from Cycadales) and Brodribb et al. (2007). I have found few records of cork cambium initiation in the gymnosperms.
Although gymnosperm pollen can be divided into grains with an alveolate and those with a granular infratectal layer, the former 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).
Pinales show paternal transmission of plastids and mitochondria, although in taxa like Taxus mitochondrial transmission is both paternal and maternal. 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).
For additional information, see the references in the preceding section; for details of 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 the male gametophyte, see Williams (2008), for the female gametophyte, see Maheshwari and Singh (1967), for the rps3 gene, see Ran et al. (2010).
Phylogeny. 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. 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. Extant gymnosperms were thus thought to be paraphyletic, the botanical equivalent of reptiles. Plants with a heterosporangiate strobilus, the anthophytes, included flowering plants, Gnetales, and also fossil taxa like Bennettitales, while the glossophytes, also fairly close cladistically to the anthophyte clade, included the glossopterid seed ferns. Conifers, cycads, etc., were more distantly related to flowering plants.
Analyses of morphological data, especially those that include fossil taxa, continue to suggest that gymnosperms are paraphyletic, the four main groups being independently derived from a pteridosperm grade, with Gnetales close to angiosperms and often associated with Bennettitales, etc. 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, 2013a; Zavialova et al. 2009: pollen, walls homogeneous or granular). However, bootstrap support for these relationships is very low (Doyle 2006; Hilton & Bateman 2006), as it was for the original anthophyte clade. In a recent study possible relationships among seed plants 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) outlined seed plant evolution in the context of a morphological analysis that was constrained by a molecular topology in which Gnetales were nested within gymnosperms, rather than carrying out an independent morphological study; he noted that this was in fact almost as parsimonious as if Gnetales were linked with angiosperms. Hilton and Bateman (2006), on the other hand, allow only a slight possibility that their morphology-based tree could be superseded (see also Farjon 2007). Interestingly, in an experimental study on "basal" chordates, it was found that as the organism 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).
Hilton and Bateman (2006) also discussed sampling in the context of morphological versus molecular phylogenies (Bateman et al. 2006b, much else besides); from this point of view, molecular studies will remain flawed because the sampling cannot be improved, while more fossils can always be included in morphological studies. However, even in extant plants, morphological studies may face difficulties, and given the current state of knowledge, relying on a topology determined by morphological studies of fossils seems a bit optimistic; relationships that are supported by morphology alone are likely to deceive. I think that our knowledge 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 group being studied (see e.g. Springer et al. 2007 for mammals).
It is taking much work to clarify ideas of relationships between the three or four major clades of extant gymnosperms, and papers in this area pay much attention to methodology. 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.
Sister-group relationships between Gnetales and angiosperms are indeed strongly questioned in most analyses of molecular data. However, the monophyly of extant gymnosperms appears to be problematic in some studies. Thus Gnetales are sometimes found to 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, this clade in turn was sister to other gymnosperms; 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). On balance, extant gymnosperms do 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; Becker et al. 2000: MADS-box gene diversity; Sanderson et al. 2000; Chaw et al. 2000; Pryer et al. 2001a; Aris-Brosou 2003; Magallón & Sanderson 2002; Qiu et al. 2006: support weak; etc.).
Within extant gymnosperms, several studies have suggested that Cycadales might be sister to all other members (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].
On the other hand, a clade [Cycadales + Ginkgoales] is increasingly frequently being recovered, perhaps especially in maximum parsimony analyses (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: see below). In a careful series of studies by C.-S. Wu et al. (2013), the clade [Ginkgoales + Cycadales] was again consistently recovered in amino acid analyses, being unaffected by taxon sampling, tree-building methods, etc. 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). 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. On balance, the hypothesis of a [Cycadales + Ginkgoales] clade is preferred here.
Establishing the position of Gnetales within extant gymnosperms still causes problems. One suggestion is that Gnetales are sister to all other 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. Indeed, 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 found in a recent 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). Lee et al. (2011) discussed character evolution in the context of this topology, suggesting that "motile male gametes would be independently and uniquely evolved (apomorphic) in cycads plus Ginkgo, and loss of motile male gametes in Gnetales would would be ancestral in the gymnosperms (plesiomorphic).". That is, such a loss would be an apomorphy for [angiosperms + gymnosperms], and the motility of the male gametes of cycads would need to be restored by regaining flagellae, 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 in character evolution.
A position of Gnetum, etc., in or near Pinales is becoming increasingly credible. A [Gnetales + Pinales] clade - the Gnetifer hypothesis - has frequently been recovered (e.g. Samigullin et al. 1999: not all analyses; Antonov et al. 2000; Sanderson et al. 2000; Chaw et al. 2000; Gugerli et al. 2001: rather strong support; de la Torre et al. 2006: much hidden support, but not from the chloroplast partition; Wu et al. 2007; Rydin & Korall 2009: Bayesian analysis; Ran et al. 2010: the mitochondrial rps3 gene; C.-S. Wu et al. 2013: some analyses; Magallón et al. 2013), and it is the preferred topology in Englund et al. (2011) and Groth et al. (2011). Gnetales may even be placed within Pinales, in particular being sister to Pinaceae, the Gnepine hypothesis (e. g. Chaw et al. 2000; Bowe et al. 2000; Gugerli et al. 2001; Hajibabaei 2003; Burleigh & Mathews 2004, 2007c: supermatrix analyses; Hajibabaei et al. 2006: genes from all three compartments, but sampling?; Qiu et al. 2007; Graham & Iles 2009; Finet et al. 2010: quite strong support; Soltis et al. 2011). This topology was also found by Zhong et al. (2011, see also 2010; also C.-S. Wu et al. 2011b) when the most variable sites in concatentated alignments were removed, so reducing the LBA/heterotachy problem.
If both quickly-evolving proteins and also proteins in which there appeared to be much parallel evolution in Cryptomeria and the branch leading to all Gnetales were removed from an amino acid matrix derived from chloroplast genomes, Gnetales - on a long branch - were sister to Cupressaceae - the Gnecup hyothesis (Zhong et al. 2010). If they were not removed, a clade [Cryptomeria + Gnetales] was obtained (Zhong et al. 2010; see also Moore et al. 2011; C.-S. Wu et al. 2013). Similarly, an analysis of variation in 83 plastid genes strongly suggested a grouping [Pinaceae [Gnetales + other Pinales]], although other relationships could not be entirely rejected (Chumley et al. 2008). Finally, Raubeson et al. (2006) found a grouping of Welwitschia with Podocarpus (this may be due to rate heterogeneity). However, Rydin et al. (2002) strongly questioned the possibility of the paraphyly of Pinales.
There are more specific points of genomic similarity between Gnetum, etc., and some or all Pinales. Some Pinaceae have lost a number of the chloroplast genes that are missing in Gnetales (Wu et al. 2009). All eleven NADH dehydrogenase genes in the chloroplast of Pinus thunbergii are absent - or are present, but as pseudogenes (Wakasugi et al. 1994); other work suggests that these genes are absent in all Gnetales and Pinales alone (Braukmann et al. 2009, also 2010; Martín & Sabater 2010; Wicke et al. 2011). The rps16 gene in Gnetales and Pinaceae is commonly lost (Wu et al. 2007, 2009). All Pinales sampled have but a single copy of the chloroplast inverted repeat (Strauss et al. 1988; Tsudzuki et al. 1992); nearly all other seed plants have two copies (Raubeson & Jansen 1992; Lackey & Raubeson 2008), and this may be marked by micromorphological changes in the genome. Interestingly, one end of the inverted repeat of Welwitschia has expanded (Welwitschia is derived within Gnetales) with duplication of trnI-CAU and partial duplication of pscbA gene region at the end of the Large Single Copy region, and these match those of the remnant inverted repeat known from Pinus and other Pinaceae, but not other members of Pinales (Margheim et al. 2006; McCoy et al. 2006, 2008: details of relationship depend on methods of analysis; see also Braukmann et al. 2009; Hirao et al. 2009).
Detailed morphological work suggests that many characters in common between Gnetales and angiosperms fail one or more of Remane's three basic criteria of homology, 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, so it is unique among seed plants, and is 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). Other characters in common between the two such as the loss of sperm flagellae and the associated development of a pollen tube growing towards the ovule, the increased venation density of the leaves of Gnetum (Boyce et al. 2009), and some of the details of the timing of events in the pollination-fertilization process (Williams 2008) have not been deconstructed in the same way. However, in angiosperms ovule size 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). 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).
Despite a number of unresolved issues, a position somewhere around Pinales seems most likely for Gnetales. There are some morphological similarities between the two, and within the former, perhaps particularly with Pinaceae. The binucleate sperm cells, basic proembryo structure, development of polyembryony, etc., of Ephedra agree with Pinales in general and perhaps Pinaceae in particular. Some Pinus species have mesogenous stomata in which the subsidiary cells are produced from the same initial that gives rise to the guard cells (Gifford & Foster 1989; see also Mundry & Stützel 2004), as in Gnetales. Strobili with both micro- and megasporangia are common as abnormalities in Pinales (Chamberlain 1935; Rudall et al. 2011a) and occur normally in Gnetum. Wherever Gnetales are placed, they will have numerous apomorphies. Although nearly all Pinales have megasporangiate strobili with spirally-arranged ovuliferous scales or modifications of them, Gnetales have decussating bracts (Magallón & Sanderson 2002); loss of the ovuliferous scale, etc., might then be apomorphies for Gnetales (Finet et al. 2010).
I have set up the synapomorphy scheme below in a way that I hope allows one to understand possible synapomorphies whatever the relationships turn out to be. Given the uncertainty in our knowledge of the relationships between the major seed-plant clades, direct links to them are provided here: Cycadales, flowering plants, and Pinales; for general discussion, see seed plant evolution.
Classification. For a linear sequence of gymnosperms, see Christenhusz et al. (2011c).
[Ginkogoales + Cycadales]: mucilage +; midrib 0; plants dioecious; pollen tube branched, growing away from the ovule, spermatogenous cells delimited by circular anticlinal wall, zooidogamy, male gametes with cell wall, released from the swollen proximal part of the tube, flagellae numerous; seeds with coloured sarcoexotesta, scleromesotesta, and ± degenerating endotesta; germination cryptcotylar.
CYCADALES Dumortier Main Tree.
Stout, unbranched treelets; roots and stems with contractile tissue; ß-methylamino-L-alanine and compounds producing methylazoxymethanol, unique biflavones, polysaccharide gums/mucilage copious, in canals; successive cambia in roots and shoots; apogeotropic coralloid roots with 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; cataphylls +; leaves large, pinnate; microsporangia in synangia, many microsporangia/sporophyll, sporangia abaxial, with an exothecium; megasporophylls with terminal sterile portion; integument free only in apical portion; pollen tube wall with abundant pectins, one prothallial cell, generative cell delimited by circular anticlinal wall; megasporophylls in simple strobili; young embryo with cells tending to congregate at the chalazal end, at micropylar end divisions fewer and wall development more tardy, suspensor cells ± elongated; seed with sarcotesta and inner fleshy layer, both vascularized; germination hypogeal, seedling cryptocotylar, coleorhiza +; mitochondrial nad1 intron 2 and coxIIi3 intron and trans-spliced introns present, one duplication in the PHYO gene group. - 2 families, 10 genera, 305 species.
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., while Crisp and Cook (2011) estimated the age at over 200 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 different estimates of ages 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).
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 characters 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...
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 might equally reasonably be invoked. Anyhow, there have a number of Tertiary bouts of speciation of cycads (see above). 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).
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). In Austalian species of Macrozamia, at least, several species of Nostoc are involved and there is no host specificity (Gehringer et al. 2010). Interestingly, the toxic ß-methylamino-L-alanine (BMAA) is probably produced by the cyanobacterial associates of cycads (Cox et al. 2005).
Pollination Biology & Seed Dispersal. The sometimes quite close association between the insects that commonly pollinate Cycadales are probably relatively recent (Downie et al. 2008). See Terry et al. (2012a, b) for what is known about pollination in the group - often by beetles - and Roemer et al. (2013) for records of thermogenesis.
Animal dispersal of the seeds - they are large, often brightly coloured, and have a fleshy outer layer - is likely for most genera.
Plant-Animal Interactions. A few brightly-coloured caterpillars, in particular those of lycaenids like the genus Eumaeus, eat cycads (Schneider at al. 2002 for references). These conspicuous larvae are distasteful to potential predators (see also below under Zamiaceae). In general, however, few insects eat Cycadales.
Genes & Genomes. For the chloroplast genome of Cycas taitungensis, see C.-S. Wu et al. (2007).
Cycads are noted for having some rather potent toxins that, it has been suggested, may have contributed to the persistence of the clade. ß-methylamino-L-alanine (BMAA) is widespread, as is methylazoxymethanol (MAM), produced by the hydrolysis of glycosides such as cycasin (a monosaccharide) and macrozamin (with a disaccharide). BMAA, probably produced by the cyanobacterial associates of cycads (Cox et al. 2005), is a possible neurotoxin, while MAM can cause severe digestive upsets, cancers, etc. (Brenner et al. 2003 and references).
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). 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, and they suggested a link to medullosan pteridosperms; this morphology is unlike that of other extant gymnosperms (Mundry & Stützel 2004b). The tapetum plays no part in the formation of the sporoderm. There are up to perhaps 40,000 flagellae per male gamete!
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), Stevenson et al. (2012: proceedings of a symposium), and The Cycad Pages (Hill & Stevenson 2002 onwards); see also the Gymnosperm Database. For embryology, see Singh (1978), branching, see Stevenson (1988), neurotoxic compounds (Whiting 1989), anatomy, see Artabe and Stevenson (1999), for fossils, see Pant (1987), 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., 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; 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 = 12; tenfold increase in mitochondrial tandem repeat sequences, Bpu mobile sequences.
Age. Diversification within Cycadaceae may have begun ca 36 m.y.a. (see Wink 2006; Treutlein & Wink 2002; Nagalingum et al. 2009).
1/100. 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).
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), (midrib + Stangeria), secondary veins regular, subparallel; megasporophylls forming a determinate cone, peltate; ovules 2(-3)/sporophyll, inverted; seeds radiospermic; n = 8, 9, 13 (Zamia variable).
9-10/200: Encephalartos (65), Zamia (55), Macrozamia (40). Scattered throughout the tropics and subtropics (map: from Jones 2002). [Photo - Encephalartos, Zamia.]
Age. Downie and Donaldson (2005) dated divergence within Zamiaceae to ca 94 m.y.a. Other estimates differ. On the other hand, it has been suggested that the divergence of many genera in Zamiaceae may have occurred more or less synchronously in the late Miocene, a mere 12 m.y. or so ago (Nagalingum et al. 2011).
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. Divergance & Distribution. Chaw et al. (2005) suggest apomorphies for Zamiaceae and some clades within it.
The splitting of many genera in Cycadaceae may have occurred more or less synchronously in the late Miocene, a mere 12 m.y. or so ago (Nagalingum et al. 2011). Crisp and Cook (2011) also thought that diversification within all cycad genera was Tertiary (the spread of ages for Zamia does extend into the later Cretaceous), but was not synchronous. The relatively recent development of particular pollination associations may have contributed to diversification in Encephalartos, Macrozamia, etc., in the (late) Tertiary (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 spermatozoids 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 are rather unclear (support for nodes mostly low) and conflict in part, at least, with those suggested by previous morphological studies; thus Stevenson (1992; see also Brenner et al. 2003) placed Bowenia and Stangeria in Boweniaceae. Indeed, the positions of Bowenia, Stangeria and Dioon are particularly uncertain; all three are distinctive genera. 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 which is never close to the first two]]]. Dioon was also found to be sister to the rest of Zamiaceae by Crisp and Cook (2011: support strong) and Griffith et al. (2012: morphology and molecules), 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.
For relationships within Encephalartos, which may have split from Lepidozamia as recently as 5-20 m.y. before present, 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 Zamiaceae.
Synonymy: Boweniaceae D. W. Stevenson, Dioaceae Doweld, Encephalartaceae Doweld, Microcycadaceae Tarbaeva, Stangeriaceae L. A. S. Johnson