EVOLUTION OF LAND PLANTS (under construction)

Most land plants are members of a clade embedded in a largely aquatic paraphyletic group, the green algae; the two together make up the Viridiplantae, or green plants. This whole group is divided into two main clades, the Chlorophyta s. str. and the Streptophyta or Charophyta s.l. For information on the evolution of Chlorophyta and the streptophytes, see e.g. Lemieux et al. (2000), Turmel et al. (2002), Sanders et al. (2003), Waters (2003), Delwiche et al. (2004), Lewis and McCourt (2004) and Becker et al. (2009). Within Chlorophyta s. str. there are several algae that are involved in lichen formation (Trebouxia and its relatives) as well as several ecologically very important marine algae; similarly, Lewis and McCourt (2004) emphasize that many clades of "green algae" have terrestrial representatives, of which embryophytes are merely the most prominent. Other members include Volvox, Caulerpa, Ulva and Acetabularia. Streptophytes include land plants (the embryophytes), and a subset of freshwater green algae like Mesostigma viride, Chlorokybus, Klebsormidium, Spirogyra, Coleochaete, and Chara. Mesostigma viride is perhaps sister to the other streptophytes, as is indicated by nuclear and some, but by no means all, organellar genes (Kim et al. 2006: isoprenoid synthesis pathways and glycolate oxidizing enzymes agree), it has scales but lacks a cellulose cell wall (J. Petersen et al. 2006). The node that includes Mesostigma viride and the rest, we find that a ?synapomorphy is the occurrence of the ndh and rps 15 and the loss of the rps 9 chloroplast genes (Martín & Sabater 2010); the presence of introns in the ndhA and ndhB genes may also be apomorphies around here. The duplication yielding the important GapA/B gene pair seems to have occurred in the common ancestor of the streptophytes, although exactly where is unclear (J. Petersen et al. 2006). Lang et al. (2010) note that a considerable number of transcription-associated protein families evolved in the basal land plants or their immediate aquatic ancestors, many more than subsequently (exactly where subsequent changes might occur is compromised by the sampling - nothing between Selaginella and angiosperms). Indeed, what appear to be land plant innovations may in fact first appear more basally in the streptophyte clade (e.g. Becker & Marin 2009; Popper & Tuohy 2010 - see also next paragraph).

Characeae (inc. Nitella) may be the immediate sister group of land plants (e.g. Graham 1993, still very useful and readable; Karol et al. 2001; Turmel et al. 2003; Delwiche et al. 2004; Qiu et al. 2007, quite strong support). However, Turmel et al. (2006, 2007) recently found Zygnematales to occupy this position in a number of analyses based on complete chloroplast genome sequences - a commonly-found set of relationships was [Chara [Chaetosphaeridium [[Zygnema + Staurastrum] + embryophytes]]] (see also Chang & Graham 2011 - Staurastrum not included). Although this topology might seem to question an evolutionary scenario involving the evolution of ever more complex plant bodies in the streptophyte clade culminating in the land plants or embryophytes, it is in line with general chloroplast genome evolution, including that of the tufA gene, although Zygnema and Staurastrum both secondarily lack the chloroplast inverted repeat, which is present in the other streptophytes (Turmel et al. 2007). Clarifying the position of Zygnematales is clearly critical, as is resolving the relationship of prasinophytes (Niklas & Kutschera 2010); a recent set of relationships suggested is [Nitella [[Spirogyra, Closterium, etc.] [Coleochaete + embryophytes]]] (Finet et al. 2010). Chara itself has acquired the rps 19 and lost the rps 15 genes (Martín & Sabater 2010).

Additional characters supporting a relationship between embryophytes and a subset of "algae" include many details of cell division, occurrence of an apical cell in the gametophyte, number and type of intron in the chloroplast DNA, flagellum ultrastructure, occurrence of sporopollenin, retention of the zygote on the haploid plant, nrDNA in a single array, etc. Details of the distributions of such characters clarify how the distinctive phragmoplast with associated desmotubules (included endoplasmic reticulum), axial microtubules and associated body plan changes of land plants, and the loss of a centriole, etc., may have evolved (see Mishler & Churchill 1984, 1985, important early morphological phylogenetic analyses; Graham 1993, general; Graham et al. 2000, body plan; Becker & Marin 2009, Domozych et al. 2010, Popper & Tuohy 2010, Sørensen et al. 2010, distinctive cell wall polysaccharide polymers evolved in charophyceans or before; Pires & Dolan 2010, class of basic helix-loop-helix domains in transcription factors that diversified very early; Volokita et al. 2010, GDSL-lipase gene family; Finet et al. 2010, general; Wicke et al. 2011, nuclear ribosomal DNA organization).

Embryophytes. Embryophytes are plants with a diploid embryo retained by the haploid gametophyte, apical meristem of a single cell, sporic meiosis, antheridia and archegonia, adaxial sporangia, sporopollenin in the spore wall, wall development being both centripetal and centrifugal, spores the dormant phase of the life cycle, monoplastidic meiosis, etc. (for other apomorphies, see e.g. Kenrick & Crane 1997; Goffinet 2000; Schneider et al. 2002; for variation in plastid number within this clade and possible correlations with patterns of microspore division, see Rudall & Bateman 2007). RNA editing in which the organelle-targeted pentatricopeptide repeat proteins play an important role is restricted to embryophytes (Rüdinger et al. 2008). Brown and Lemmon (1997, see also 2008) review the distribution of the quadripolar microtubule system in land plants; it occurs in all three groups of bryophytes, lycophytes, and Marattiales, at least. This system is linked with monoplastidy, the microtubule organising centre being associated with the plastid. Other apomorphies of embryophytes include a close association between the trnL_UAA and trnF_GAA genes on the chloroplast genome; these genes are not associated in other green plants (Quandt et al. 2004). Much of the pathway by which lignin is synthesized in vascular plants is found already in mosses (Gómez-Ros et al. 2007; Xu et al. 2009, see also Guo et al. 2010).

One can think of the evolution of land plants as involving the interpolation of the sporophytic generation into a life cycle that was haploid/gametophytic, rather than divergence of intially morphologically similar diploid sporophytic and haploid gametophytic generations (Haig 2008; Gerrienne & Gonez 2011 on alternation of generations, see also below). However, we lack much reliable knowledge of life cycles in charophyte algae, and this greatly hampers understanding of the events that led to the development of alternation of generations (Haig 2010). The first land plants as we generally think of them are known from the mid-Ordovician, some 476 million years before present (Kenrick 2000; Wellman et al. 2003), and in these plants the spores may have been produced directly from diploid zygotes, the protective element of the zygote wall becoming associated with the walls of the haploid spores by a complex process involving heterochrony (Brown & Lemmon 2011). However, Clarke et al. (2011) reject post-Cambrian ages for the origin of crown embryophytes, their estimates for the age of this clade being 815-516 million years.

As little as thirty years ago our understanding of the evolution of land plants was very different from what it is now. It was usually suggested that Psilotum represented a very ancient group, often being compared with plants from the Devonian Rhynie Chert, horsetails were also ancient (but not immediately related), and were linked to the fossil Sphenophyllum and its relatives, and then there were Lycopodium and Selaginella and relatives forming a group, ferns, gymnosperms, and vascular plants. "Bryophytes" represented the earliest land plants (see Goffinet & Shaw 2009 and Shaw et al. 2011 for much general information about the "bryophytes" as we now think of them - see below). Relationships within the evascular land plants, the "bryophytes", and between them and the vascular plants were for some time somewhat unclear (e.g. Quandt & Stech 2003), but substantial progress has been made in the last decade in disentangling relationships within and between the major groups of embryophytic land plants, i.e. the bryophytes (mosses, liverworts, and hornworts) and the rest (Bateman et al. 1998).

Early studies suggested that mosses were sister to vascular plants, thus the conducting tissue in the centre of the stem in some moss gametophytes could be thought of "homologous" to the vascular tissue in the sporophytes of vascular plants (e.g. Mishler & Churchill 1984, 1985; Mishler et al. 1994). However, this was in part due to the way in which characters describing conductive tissue were conceptualized; there may be little reason to consider the conductive tissues of mosses and those of polysporangiophytes as having much similarity other than that due to their similar functions (e.g. Ligrone et al. 2000, 2002, but cf. root hairs and rhizoids below). Thus Ligrone et al. (2002) suggest there are no immediate similarities between the water conducting cells of Takakia, the hydroids of other mosses, and conducting tissues in Haplomitrium and metzgerialean liverworts. In fact, in bryophytes the great majority of genes are expressed in both generations (Szövényi et al. 2010), in line with the proposal by Banks et al. (2011) that some of the genes involved in the patterning and differentiation of vascular tissue were present in the ancestral (gametophye dominant) land plant. Note that there do seem to be substantial differences between the two generations in expression of genes controlling apical meristem growth and auxin polarity (Fujita et al. 2008; Sakakibara et al. 2008).

Mitochondrial sequence data sometimes placed hornworts as sister to all other land plants (for references, see Stech et al. 2003). Goffinet (2000) and Renzaglia and Vaughn (2000) suggested synapomorphies for the clade [all land plants minus hornworts] and Goffinet (2000) and Shaw and Renzaglia (2004) summarized the literature on this whole problem. However, Dombrovska and Qiu (1994) had earlier outlined several lines of evidence such as the content of the inverted repeat and intron distribution that were consistent with the idea that liverworts might be sister to all other land plants (see also Qiu et al. 1998b for mitochondrial introns; Antonov et al. 2000, cp rDNA ITS); Takakia is a member of the moss clade, while the third main bryophyte group includes the hornworts. Kelch et al. (2004), using structural characters of the plastome, and Groth-Malonek et al. (2004, not all analyses), looking at trans-splicing mitochondrial introns, again suggested that liverworts are sister to all other land plants (see also Rydin & Källersjö 2002, not all analyses). The distribution of an extension of the chloroplast inverted repeat placed hornworts as sister to tracheophytes alone, as did the distribution of cell wall xylans (Carafa et al. 2005) and the mitochondrial introns just mentioned (Groth-Malonek et al. 2004; Knoop 2005). This latter position is also favoured by an analysis of cpITS spacer sequences (Samigullin et al. 2002).

Now most studies support the set of relationships [liverworts [mosses [hornworts + vascular plants]]] (e.g. Goffinet & Shaw 2009; Shaw et al. 2011 for literature). Qiu et al. (2006) confirmed these relationships using three different sets of data; this seems the best hypothesis of relationships at present (see also Lewis et al. 1997; Kelch et al. 2004; Wolf et al. 2006 [many analyses, whole chloroplast genomes], and references; Qiu et al. 2007). This set of relationships is followed here.

There are some studies suggesting other relationships. Thus Nishiyama et al. (2004) proposed that the three bryophyte groups form a single clade; although 51 genes from the entire chloroplast sequence were studied, taxon sampling was poor (e.g., no lycophytes were included - see also the discussion on the position of Amborellaceae within flowering plants for a comparable sampling issue). A similar grouping also resulted from an analysis of variation within the trnL intron (Quandt et al. 2004) and another study that looked at many genes but with very skimpy sampling, that of Goremykin and Hellwig (2005). Liverworts and mosses formed a clade in the recent tree of Finet et al. (2010), but hornworts were not sampled. In a few earlier studies the liverworts appeared not to be monophyletic (Bopp & Capesius 1998 and references).

Clade including all Extant Land Plants. Polar transport of auxin in sporophyte.

Evolution. Davies et al. (2011: 95% credibility intervals) suggested an age for this clade (extant embryophytes) of (815-)670(-568) million years - see other estimates they make.

For the general evolution of land plants, see Dombrovska and Qiu (1994), Kenrick and Crane (1997: general morphology and anatomy), Bateman et al. (1998: esp. physiology and ecology of early land plants), Qiu et al. (1998b), Nishiyama and Kato (1999), Renzaglia et al. (2000), Kenrick (2000: morphology), Schneider et al. (2002), Waters (2003), Hedges et al. (2004: timing of early events), Friedman et al. (2004: evolution of plant development), Hemsley and Poole (2004: evolutionary physiology of early land plants), and Taylor et al. (2009: comprehensive survey of fossils, including of those of fungi associated with plants).

Liverworts. Liverworts (Marchantiophyta) are probably monophyletic, despite earlier suggestions that they might not be (Quandt & Stech 2003 for references). They have a plesiomorphically thalloid plant body, and the cells of most species have distinctive, membrane-surrounded oil bodies; the cell walls have relatively little cellulose. The embryo develops surrounded by gametophyte tissue. The sporophyte has a bulbous foot, there is an evanescent seta forming after the sporangium develops, there is no columella in the sporangium, and there nearly always are unicellular elaters (Renzaglia et al. 1997; Crandall-Stotler & Stotler 2000); the spore walls have more or less continuous parallel lamellae at maturity (Wellman et al. 2003). Endopolyploidy has not been detected (Bainard & Newmaster 2010a, b). Quite a number are dessication tolerant, most lacking internal water-conducting cells (Ligrone et al. 2000). Interestingly, S lignin, made up of syringyl units, has also been found in some liverworts and is scattered in vascular plants other than flowering plants, where it is of course very common (Li & Chapple 2010; Espiñeira et al. 2010; see also Gómez-Ros et al. 2007).

Within the liverworts, morphological studies indicated that Sphaerocarpos might be sister to all other liverworts (Crandall-Stotler & Stotler 2000). However, molecular data suggest rather different relationships (see also Forrest & Crandall-Stotler 2004, 2005; He-Nygrén et al. 2004; Qiu et al. 2006), although the long branches associated with Haplomitrium and Treubia sometimes caused their position in the tree to be somewhat migratory. He-Nygrén et al. (2006: 3 chloroplast and 1 nuclear genes, morphology) outline the phylogeny and classification of liverworts, finding a basic structure [Treubiopsida [Marchantiopsida + Jungermanniopsida]]. This basic topology is confirmed by Forrest et al. (2006: five genes, all three compartments, good sampling, esp. of thalloid liverworts) and Volkmar and Knoop (2010). Treubiopsida, a small group with rather simple thalli, is made up of Treubia and Haplomitrium (e.g. Forrest & Crandall-Stotler 2004, 2005); the thallus exudes copious mucilage via stalked slime papillae, there is a tetrahedral apical cell, a distinctive association with a glomeromycotan symbiont, also a distinctive blepharoplast, etc. (Duckett et al. 2006a). Marchantiopsida, the complex-thallus group, include Blasia, Sphaerocarpos, etc., although support for the inclusion of the former in this clade is still weak (but cf. some analyses in Forrest & Crandall-Stotler 2004, and especially 2005; Qiu et al. 2007, Blasia sister to the rest; He-Nygrén et al. 2004 should also be consulted); Marchantiopsida - including Blasia - have lost to ability to carry out RNA editing (Rüdinger et al. 2008). Within Jungermanniopsida, simple-thallus groups are paraphyletic with respect to the speciose and monophyletic leafy liverworts, within which Pleurozia is sister to the rest (in e.g. He-Nygrén et al. 2004; Davis 2004 it came out with some simple thalloid genera). These general relationships were also recovered by Qiu et al. (2007). For relationships within the speciose Lepidoziaceae, see Cooper et al. (2011). Crandall-Sotler et al. (2009) have recently proposed a formal phylogeny-based classification of Marchantiophyta.

Liverworts or liverwort-like plants were present by the Ordovician, and liverworts may have been common through the Silurian and Devonian (Graham et al. 2011). Understanding the ecoophysiology of these early plants is a challenge, but it may be relevant that extant Marchantia, at least, is mixotrophic (Hata et al. 2000; Graham et al. 2010). Heinrichs et al. (2007) discuss the evolution of the ca 4,500 species of leafy liverworts, suggesting possible divergence times for the clades, and Wilson et al. (2007) discuss the diversification of Lejeunaceae in particular. Details of meiosis, whether there is one or more chloroplasts, etc., vary considerably in liverworts, and some derived taxa have a pattern like that common in vascular plants (Brown & Lemmon 2008). Porellales and Jungermanniales, both leafy liverworts epiphytic on bark and leaves of flowering plants, may have diversified since the evolution of angiosperms (Ahonen et al. 2003; Forrest & Crandall-Stotler 2004).

STOMATOPHYTES

Sporophyte with stomata; post-transcriptional editing of the chloroplast.

Evolution. Davies et al. (2011: 95% credibility intervals) suggested an age for this clade of (750-)632(-548) million years.

Chemistry, Morphology, etc. For post-transcriptional editing of the chloroplast, see Martín and Sabater (2010).

Mosses. Mosses have distinctive leafy gametophytes and sporophyte with a pointed foot, indurated seta and capsule developing after the seta has elongated; the capsule has a central columella and a persistent calyptra (Renzaglia et al. 1997). There is widespread endopolyploidy, although not in the near basal Sphagnum (Bainard & Newmaster 2010a, b).

Evolution. Polytrichopsida/Dicranidae/haplolepidious taxa are a diverse but species-poor group compared to the ca 12,000 species of Hypnanae/hypnalian pleurocarps/arthrodontous mosses (Cox et al. 2010). There is strong geographical signal in the phylogeny of Polytrichopsida, with largely south and north temperate clades (Bell & Hyvönen 2010: could there be intergeneric hybridization?); gametophytic vascularization is particularly well developed in Polytrichopsida, and this includes the development of leptoids, which apparently transport organic molecules (Ligrone et al. 2000).

Phylogeny. Relationships between clades at the base of the moss tree remain unclear. Sphagnum, Andraea (in both the capsule has a pseudopodium) and Takakia (the capsule opens by a single, spiral slit) are all in this area, Sphagnum and Takakia perhaps being sister taxa and Andraea sister to remaining mosses (e.g. Cox et al. 2004; Qiu et al. 2006, 2007: rather strong support; Volkmar & Knoop 2010; Shaw et al. 2010 [perhaps]). However, Takakia has a region in the cpITS3 sequence that is very like that of all other land plants but is deleted in other mosses, from this evidence alone, Takakia might be sister to all other mosses (Samigullin et al. 2002); note that there are no stomata on the sporophyte, and monoplastidic mitosis occurs during vegetative growth as well. In Sphagnum the protonemal stage is short, being replaced by a thalloid structure; leaf cells are dimorphic, groups of cells being empty and hyaline and surrounded by strands of chloroplast-containing cells; the capsule is sessile, there is a massive columella derived from the endothecium, etc. (Shaw et al. 2003a). Andraea also has a thalloid early gametophytic stage. Recent work suggests relationships may be [Takakia [Sphagnum [[Andreaea + Andreaeobryum] [Oedipodium + the rest]]]] (Chang & Graham 2009, esp. 2011, note that a [Takakia + Sphagnum] clade was recovered in maximum parsimony reconstructions). Interestingly, the position of Takakia was initially very uncertain - was it a moss or liverwort? - but its morphology is now better understood, and it is clearly a moss (see Renzaglia et al. 1997). In Sphagnales (Sphagnopsida) the highly distinctive Sphagnum leucobryoides (= Ambuchanania) was described only some twenty years ago (Yamaguchi et al. 1990); Shaw et al. (2010) provide a classification of the whole clade, and suggest diversification within it may have occurred within about the last 50 million years.

Wahrmund et al. (2010) used a new mitochondrial locus to investigate relationships among mosses, and the position of Timmia is particularly unclear. Bell et al. (2007) discuss the phylogeny of the early diverging pleurocarp clades (for general information on pleurocarp mosses, see Newton & Tangney 2007), and adjust their taxonomy accordingly, while Buck et al. (2005) discuss the phylogeny of Hookeriales. Cox et al. (2010) present a major phylogenetic study of mosses focusing on genera and families.

Classification. For a classification of mosses based on recent phylogenetic studies (e.g. Newton et al. 2000; Cox et al. 2004) see Shaw and Goffinet (2000, see also Goffinet & Buck 2004), and for a general entry into the literature, see Goffinet et al. (2004).

Within the speciose pleurocarpous mosses - about 40% of all mosses - diversification seems to have been early and rapid, clades diverging in the early Cretaceous, but since then there has been semi-stasis (Kürschner & Parolly 1999; Shaw et al. 2003b; Newton et al. 2006, 2007); there may also have been more recent ([post-]Cretaceous) diversification as well. Genome size in mosses is small, 1C vales being less than 1.4 pg (Bennett & Leitch 2005); I do not know what sizes are in liverworts, etc.

Hornworts + Tracheophyta: Sporophyte long-lived, chlorophyllous, nutritionally largely independent of the gametophyte; sporophyte-gametophyte junction interdigitate, sporophyte cells showing rhizoid-like behaviour; gametangia embedded in the gametophyte.

Evolution. Davies et al. (2011: 95% credibility intervals) suggested an age for this clade (including Gnetales) of (286-)252(-212) million years.

Hornworts. Thalloid (leafy) plants; close association with the N-fixing Nostoc; flavonoids 0; sporophyte with bulbous foot, no seta, central columella, no well-defined valves, (stomata 0 in some taxa with more or less enclosed sporophytes). The sporophyte grows from the base for an extended period and there are distinctively-thickened elaters mixed in with the spores that have more than a single cell. Hornwort chloroplasts have a pyrenoid (lost in some taxa). There can be many antheridia (up to 40 or so) in each chamber. Anthoceros has lost the chloroplast rps 15 gene (Martín & Sabater 2010)

Qiu et al. (2006b, 2007 and references) note a number of features of hornworts, particularly of the sporophyte, that suggest similarities with polysporangiophytes in particular; they may turn out to be synapomorphies of the two (for some, see above). Note that the vegetative anatomy of hornworts is poorly known (Ligrone et al. 2000). The cell walls of spores and their elaters contain xylans, an important polysaccharide in secondary cells walls of vascular plants, but unknown in other bryophytes (Carafa et al. 2005); although the comparison here is within the sporophyte, the structures involved are rather different... It has been suggested that the stomata on the sporophyte are not involved in gas exchange, rather, they faciltated the drying out of the capsule and hence spore dispersal; if this is confirmed, and this was the original function of stomata (Pressel et al. 2011 - see also mosses!), then the central role of stomata in photosynthesis in vascular plants would be a spectacular case of an exaption. Finally, there seems to have been between 1-6 duplications in each of the three groups of GDSL lipases somewhere around here (Volokita et al. 2010).

Relationships within hornworts are in a state of flux. Leiosporoceros may be sister to all other hornworts. It has many distinctive features, including the way in which Nostoc forms branching strands in the centre of its thallus which lacks mucilaginous clefts (see Stech et al. 2003 and Duff et al. 2004 for a phylogeny). In all other taxa Nostoc forms spherical colonies and the gametophytes have mucilaginous clefts (probably not homologous with stomata) through which Nostoc enters (Adams 2002; Adams & Duggan 2008). Anthoceros and its possible segregate Folioceros are sister to remaining hornworts, and they have black or dark spores, etc. (in this they are like Leiosporoceros). All other hornworts have only 1-6 antheridia/chamber (Duff et al. 2004, see also Cargill et al. 2005). Frey and Stech (2005) provide a classification of the group and Villareal et al. (2010) a summary of our understanding of hornworts.

Fungi and Bryophytes. It is likely that associations between embryophytes and fungi, initially with the gametophytes of the former, were established very early in the Silurian/Devonian (Selosse & Tacon 1998; Redecker et al. 2000b; Nebel et al. 2004; Köttke & Nebel 2005); Glomeromycota may be the fungi likely to have been involved initially. There appear to be at least three genes involved in the establishment of mycorrhizae that were found in the common ancestor of land plants, although the DM13 gene in particular seems to have other functions in many mosses (Wang et al. 2010, commentary by Bonfante & Selosse 2010). All three major groupings of fungi that form mycorrhizal associations with plants, Glomeromycota, ascomycetes, and basidiomycetes, are known to be asssociated with liverworts (Read et al. 2000; Duckett et al. 2006b; Pressel et al. 2010), and although the liverworts of the first pectinations are associated with Glomeromycota in particular (Kottke & Nebel 2005), this association may subsequently have been lost (Duckett et al. 2006b), and in some cases the fungus involved may have moved to the liverwort from a tracheophyte (Ligrone et al. 2007). Within Jungermanniopsida, Porellales lack fungus associations, but within Jungermanniales associations with ascomycetes are very old, more than 250 million years (Pressel et al. 2008), and the ascomycetes involved may have moved from liverworts to seed plants (Pressel et al. 2010). Cryptopthallus mirabilis is the only mycoheterotrophic liverwort, indeed, it is the only mycoheterotrophic member of these three basal clades, and it obtains its metabolites from pine or birch via the ectomycorrhizal basidiomycete, Tulasnella (Wickett & Goffinet 2008); it may be nested within Aneura, also associated with basidiomycetes (Pressel et al. 2010). For the (mostly ascomycete) symbiotic fungi to be found in mosses and liverworts, see Stenroos et al. (2010) and Pressel et al. (2010).

Interestingly, functional mycorrhizal associations, i.e. involved in the exchange of nutrients, have not been found in mosses (Read et al. 2000; Davey & Currah 2006). However, endophytic fungi may affect their growth and ecology (Read et al. 2000; Davey & Currah 2006). Pressel et al. (2010) noted that fungi "more ancient" than Glomeromycota form associations with Trubia and Haplomitrium. Glomeromycota are known to be associated with at least some hornworts (Pressel et al. 2010).

POLYSPORANGIOPHYTA

All other land plants are polysporangiophytes, the crown group of which is at least 425 million years old. In polysporangiophytes the sporophyte is well developed and branched (hence "poly-" = many + "sporangia" + "phyte" = plant). There is an apical meristem, whether of a single cell or group of cells; details of the construction of this meristem varies within lycophytes (see below) but is constant in the other main groups, and correlates with the richness of plasodesmatal connections between the cells (many - a single cell, few - a group of cells: see Imaitchi & Hiratsuka 2007). Note that the exact evolutionary relationship between the sporophyte of polysporangiophytes and that of bryophytes is unclear (Shaw et al. 2011), for example, the stalk of a moss capsule way not be homologous to the branching sporophyte axis of the polysporangiopyte (Kato & Akiyama 2005). Some early polysporangiophyte gametophytes appear to have been elaborate structures, although different in morphology from the sporophytes, and to have had stomata (Taylor et al. 2005), so at this level evolution of land plants is from an ancestor in which the generations were pretty much ismorphic. Indeed, the largely isomorphic alternation of generation represented by plants from the Lower Devonian Rhynie Chert of some 410 million years ago figures largely in attempts to understand the evolution of land plant life cycles (Niklas & Kutschera 2009, 2010 - there the sequence is gametophyte only -> isomorphic -> gametophyte dominated -> sporophyte dominated?). In these earliest polysporangiophytes the sporophyte was larger, if not much more complex, than the gametophyte (Gerrienne & Gonez 2011), and in fact in bryophytes ca 95% of genes are expressed in both generations (Szövényi et al. 2010). For a comprehensive study of the early evolution of land plants, see Kenrick and Crane (1997).

Not all polysporangiophyes have vascular tissue, and those that do make up a more restricted group, the tracheophytes or vascular plants, all of which have a vascular system with tracheids and sugar-transporting cells made up of sieve elements. They all have some kind of roots (but which may be of independent origin) and stem growth is by the activity of an apical cell (e.g. Kato & Akiyama 2005). Their sporangia are borne adaxially on the sporophylls (Schneider et al. 2002).

A similarity at the regulatory gene level has recently been demonstrated in the development of rhizoids of the moss Physcomitrella and root hairs of Arabidopsis (Menand et al. 2007), suggesting that at least some sporophytic genes were recruited from the gametophytic generation (see also Szövényi et al. 2010; it is only in angiosoperms that there is a substantial proportion [ca 25%] of genes expressed only in the sporophyte). Edwards (2003) and Edwards et al. (2003) examined conducting cells of early tracheophytes and compared the morphologies of the cells involved with those of the "bryophytes". For general discussion on the evolution of water-conducting cells, with particular attention to wall sculpturing and its nature, see especially Kenrick and Crane (1991, 1997), Cook and Friedman (1997), Friedman and Cook (2000), and Edwards et al. (2006), although understanding the fossil record is difficult in part because our knowledge of the development and nature of the wall thickening even of extant vascular plants is surprisingly poor. In extant vascular plants, the lignins are rich in guaiacyl units (Harris 2005), while the evolution of the cinnamyl/sinapyl alcoholase gene family involved in the synthesis of the hydroxycinnamyl alcohol monomer units (p-coumaryl, guaiacyl, syringyl) that ultimately constitute lignin can perhaps be pegged to this node (Guo et al. 2010; cf. Gómez-Ros et al. 2007; Zu et al. 2009).

TRACHEOPHYTA

Sporophyte generation dominant, polar transport of auxins and class 1 KNOX genes expressed in the sporophyte alone; vascular system with tracheids and sieve cells; sporagia numerous; first division of the zygote horizontal.

Evolution. Davies et al. (2011: 95% credibility intervals) suggested an age for the clade of (456-)446(-425) million years.

Pryer et al. (2004b) provide a useful summary of the evolution of the vascular plants, Sakakibara et al. (2008) and Fujita et al. (2008) discuss sporophyte growth and polar auxin transport respectively in land plants, although sampling needs to be improved (what about liverworts?). Three new families of transcription-associated proteins may have evolved somewhere in this general area (Lang et al. 2010: hornworts not included). Johnson and Renzaglia (2009) discuss details of the evolution of the embryo, while Arens et al. (1998: Virtual paleobotany laboratory) is a valuable web resource.

Lycophytes have roots probably derived from stems and dichotomously branching, a protostele, exarch xylem in the stem, endarch xylem in the roots, often heart-shaped sporangia, embryo endoscopic (first division vertical - Isoetes), etc. (Kenrick & Crane 1997; Boyce 2005 and literature). The leaves of lycophytes (microphylls) have also been called lycophylls, and are characterized by having an intercalary meristem and a single vein that does not leave a gap in the central stele. Lycopsida represent the extant members of this clade, and have vascularized microphylls, stellate xylem in the stem, a close association of sporangia and leaves (hence sporophylls), etc. (Kenrick & Crane 1997). For the early evolution of lycophytes, see Gensel and Berry (2001), and more particularly for the evolution of plants associated with Isoetes, see Grauvogel-Stamm and Lugardon (2001) and Pigg (2001). Wikström and Kenrick (1997) and Wikström (2001) discuss diversification and phylogeny of extant Lycopodium s.l. and relatives. Although diversification in Lycopodium s.l. may have begun some 200 million years before present or more ago when there are fossils with the distinctive plectostele that characterises Lycopodium s. str., most of the diversity in the group is the result of events that have occurred within the last 80 million years at most. The mitochondrial organizing center is on the nuclear envelope (NE-MTOC) and meiosis is poyplastidic and anastral (Brown & Lemmon 2008 [check level]).

Chemistry, Morphology, etc. For general information, see Ranker and Haufler (2008).

Phylogeny. Extant vascular plants are now placed in the lycophytes and the euphyllophytes (but see below for the evolution of leaves). This is very largely the result of recent molecular studies (see below for references) that have suggested a fundamental reorganisation of relationships among extant tracheophytes, with just three main clades being recognised - [lycophytes [monilophytes + lignophytes = euphyllophytes]]. The association of Psilotum in particular, but also Equisetum, with ferns that is now very largely accepted was particularly unexpected (but see Kenrick & Crane 1997). Although there was some morphological evidence suggesting this position (e.g. Bierhorst 1968 [comparison with Stromatopteris, so most similarities are parallelisms], 1977), it was not seen as being absolutely solid, and in textbooks and even several morphological cladistic analyses (e.g. Bremer 1985; Stevenson & Loconte 1996; Rothwell 1999, whether or not fossils were included) Psilotum came out as the most "primitive" extant vascular plant, i.e. it was sister to all other vascular plants. Indeed, it looks similar - superficially at least - to some fossils. Some morphological analyses do include Psilotum with other monilophytes - even if the same analyses also place flowering plants in a paraphyletic gymnosperm group (Schneider et al. 2009). Although this reorganisation of monilophytes has been sometimes been severely criticised (Rothwell & Nixon 2006), it is unclear how damning such criticism is; since the evaluation of "support" values for particular topologies is integral to the approach adopted in these pages, the decision to exclude such values in Rothwell and Nixon (2006) makes their work difficult (for me, at least) to interpret.

Classification. For families and genera, see Christenhusz et al. (2011).

Previous Relationships. Our ideas of relationships in vascular plants compare dramatically with the psilotophyes, equisetophytes, lycophytes, pteridophytes s. str., and seed plants (arranged from "primitive" to "advanced") that I was taught.

Roots with exarch protoxylem, lateral roots endogenous; leaf traces leaving a gap in the central stele; euphylls or megaphylls spirally arranged, with apical/marginal growth, venation development basipetal, growth determinate; sporangia borne in pairs and grouped in terminal trusses, meiosis polyplastidic; sperm multiflagellate, monoplastidic, basal bodies staggered, centrosomes bicentriolar; 30kb chloroplast inversion in the large single-copy region of the chloroplast genome.

Evolution. Crown euphyllophytes appear to date from 401-380 million years ago (Leebens-Mack et al. 2005), while Davies et al. (2011: 95% credibility intervals) suggested rather older ages of (452-)434(-410) million years.

For information on possible apomorphies for crown euphyllophytes, see Raubeson and Jansen (1992b), Kenrick and Crane (1997), Imaichi et al. (2008: position of some characters difficult to ascertain), and Schneider et al. (2009).

Note that details of the evolution of megaphylls - indeed, a satisfactory definition for them seems to be lacking, although in general they are determinate organs with ad/abaxial identities with a vascular supply that leaves a "gap" in the central stele when it departs - are unclear (see e.g. Sporne 1965, but cf. Harrison et al. 2005; Boyce 2005 summarizes earlier literature; Tomescu 2008, 2009; Sanders et al. 2007, 2009; Galtier 2010). The leaf supply to megaphylls in monilophytes seems to have evolved by dissection of an amphiphloic siphonostele, while leaf gaps in seed plants are associated with a stele that consists of a series of sympodia of collateral vascular strands (see also below). From this point of view the megaphylls in the two groups may represent parallelisms rather than a synapomorphy and leaf gaps are not equivalent; the term "megaphyll" can thus be used in a descriptive sense only (Namboodiri & Beck 1968c; Beck et al. 1982). However, it has been found that the vascular construction of the rhizome in some true ferns is also made up of sympodia (Karafit et al. 2005); note that Schneider et al. (2009: p. 461 and references) suggest that euphylls did arise once, and can be characterized by apical/marginal growth, apical origin of the venation, determinate growth, etc. Floyd and Bowman (2007) suggest that megaphylls have evolved independently in the angiosperms and ferns and relatives (see also Boyce & Knoll 2002; Gensel & Kenrick 2007; Tomescu 2009; Sanders et al. 2009; Galtier 2010; etc.) Osborne et al. (2004) provide an ecological explanation for the origin of megaphylls based on falling CO₂ levels, even if the developmental mechanisms involved had evolved long before then (Beerling 2005 and references). 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 leaves represent a modified branch system.

Phylogeny. Extant euphylophytes are made up of two clades, ferns and their relatives, the monilophytes or Moniliformopses (these lack true roots), and lignophytes, made up today of seed plants or spermatophytes.

FERNS s.l. / MONILOPHYTA

Shoot apical meristem of a single cell, plasmodesmatal network cell-lineage specific; stem with peripheral band of fibres + [stereome - hypodermal and outer-cortical]; amphiphloic siphonostele + [discontinuities in stele in t.s. +, caused by leaf gaps]; protoxylem restricted to lobes of central xylem strand [xylem development mesarch], primary xylem with circular bordered pits; phloem fibres rare; stem endodermis and pericycle +; leaves megaphyllous [ad/abaxial symmetry evolved first, then determinancy], frond veins not anastomosing; sporangia in sori, sporangium stalk 6< cells across, walls two cells thick, lacking an annulus, spores/sporangium 1000<, white, spores globose-tetrahedral, trilete, tapetum plasmodial, spore wall development centrifugal, exospore 3-layered, pseudoendospore +; gametophytes exosporic, green, photosynthetic, antheridium embedded, wall ³5 cells thick; embryonic axis reorients during development; nine-nucleotide insertion in the plastid rps4 gene.

Evolution. Some possible apomorphies (see e.g. Schneider et al. 2009) are underlined. However, other features may need to be added. For instance, the megaphyllous leaf of ferns and that of extant seed plants may have evolved independently.

Schuettpelz and Pryer (2009, esp. Tables 2, 3 in the Supplement) provide extensive dating of divergence times in monilophytes, and also list a number of fossil records of the group (for the fossil record, see also Rothwell & Stockey 2008).

There have been several radiations of homosporous leptosporangiate ferns, the first in the Palaeozoic, giving rise to lineages that have since become extinct, in the Jurassic and again in the Cretaceous (Rothwell & Stockey 2008). General fern diversity decreased (along with that of the cycads) through the Cretaceous (Wing & Boucher 1998). The diversification that gave rise to most living ferns, especially to the polypod ferns, which make up some 80% of living fern species, may have occurred subsequent to the diversification of the angiosperms (Lovis 1977; Rothwell & Stockey 2008; Schuettpelz & Pryer 2009). Indeed, ferns appear to have temporarily dominated at least locally after the end-Cretaceous bolide impact (Schneider et al. 2004a). Quite a number of the polygrammoid ferns ([Polypodiaceae + Grammitidaceae] clade, Polypodiaceae below) are epiphytic, and they make up at least 80% of the living fern species. They may have evolved subsequent to the initial diversification of the angiosperms in the Late Cretaceous. Diversification of epiphytic ferns in particular occurred during the early Tertiary and was perhaps linked with the Palaeocene-Eocene thermal maximum, which occurred some 10 million years after the bolide impact (Schneider et al. 2004a, b; Schuettpelz 2007; esp. Schuettpelz & Pryer 2009: Supplemental Tables 2, 3; Watkins et al. 2010). An exception in ferns is Trichomanes and relatives (but not Hymenophyllum and its relatives) which were diversifying in the early Cretaceous - but then Trichomanes and relatives are commonly epiphytic on tree ferns, which themselves had begun diversifying in the Jurassic (Schuettpelz 2007; see also Schuettpelz & Pryer 2009; Rothwell & Stockey 2008 for early radiations of leptosporangiate ferns).

The evolutionary physiology of ferns is repaying examination. The tracheids tend to be long and wide, and the scalariform perforation plates may extend the length of the cell, and so are relatively efficient in water transport despite the absence of any secondary thickening and bordered pits, as in conifers (Pittermann et al. 2011). The little that is known about stomatal responses to different wave lengths of light in ferns is interesting. In seed plants, stomata open in response to both red and blue light. Those few ferns examined, all leptosporangiates (Pteris, Adiantum, Asplenium and Nephrolepis), do not show this blue light reponse, although the relevant phototropin, a blue right receptor protein kinase, etc., seem to be present (Doi et al. 2006).

Grammitidaceae s. str. in particular (inc. in Polypodiaceae) have green spores and accelerated plastid genome evolution, a correlation also found elsewhere in ferns, but not 100% (Schneider et al. 2004b; note that fern spores that less obviously contain chloroplasts are more widespread - see Sundue et al. 2011). On the other hand there has been an abrupt reduction in the rate of molecular evolution in the largely arborescent Cyatheales (Korall et al. 2010: Marattiales, Osmundales, etc., not included). Indeed, the eusporangiate Marrattia and Angiopteris, and also the leptosporangiate tree ferns, may be something of living fossils showing little molecular and even morphological evolution (P. Soltis et al. 2002).

For mycorrhizae in ferns, see Lehnert et al. (2010 and references.

Ferns are noted for the high incidence of polyploidy within the group, and it is estimated that almost 1/3 (31%) of all speciation events there are accompanied by polyploidy (Wood et al. 2009).

Chemistry, Morpholgy, etc. Monilophytes or ferns s.l. are characterised by having a siphonostele, the protoxylem being restricted to lobes of the central xylem strand, hence bringing to mind a necklace (development of the xylem is mesarch, although notably variable in the Ophioglossum/Psilotum clade). For details of spermatozoid morphology and movement, etc., see e.g. Renzaglia et al. (2002) and Schneider et al. (2002). Information on horizontal cell walls in early embryo development in ferns given by Philipson (1990) seems to be incorrect - the examples should be vertical?

For general comparative anatomy, see Ogura (1972), for details of stelar morphology and evolution, see Beck et al. (1982), for megaphylls, see Tomescu (2009), for cell wall polysaccharides, see Silva et al. (2011). For information an pteridophytes in general (these often include lycophytes), see also Kato (2005) and Ranker and Haufler (2008).

Phylogeny. The circumscription of this clade has only recently become clear. It includes Psilotum (Tmesipteris is close) sister to Ophioglossum (support strong) in a clade sister to all other ferns. Equisetum, perhaps sister to Angiopteris, etc. (although support currently only moderate), may be in turn sister to remaining ferns (e.g. Pryer et el. 2001a, 2004a; Wikström & Pryer 2005; Qiu et al. 2007; cf. in part Wolf et al. 1998). However, recent work places Equisetaceae alone sister to all other ferns; some support came from a rps4 analysis, and also 4- and 5-gene analyses, the latter two with strong support (Schuettpelz et al. 2006) and from a matK phylogeny (Kuo et al. 2011). Wikström and Pryer (2005) note that Equisteum has no mitochondrial atp1 intron, and this is either a secondary (and parallel) loss or plesiomorphic absence, depending on the topology of the whole group (see the character hierarchy below). Spore wall ultrastructure of Calamites, an extinct member of Equisetaceae, is not so different from that of Ophioglossaceae and other ferns (Lugardon & Brousmiche-Delcambre 1994; Grauvogel-Stamm & Lugardon 2009). The inclusion of morphology alone or in combination with molecular data also affects relationships detected (Wikström & Pryer 2005 and references).

Within the remaining ferns is a large clade made up of leptosporangiate ferns (with very strong support - see also Hasebe et al. 1994, 1995, Pryer et al. 1995; Wolf et al. 1998; Quandt et al. 2004; Schuettpelz et al. 2006) that originated perhaps 350 million years before present (e.g. Schneider et al. 2004a). Within this leptosporangiate clade, Osmunda and relatives, the sporangia of which have some eusporangiate features, are strongly supported as being sister to the rest. There is further substantial resolution of relationhips within leptosporangiate ferns (e.g. Pryer et al. 2004a, b and references; cf. in part Kuo et al. 2011, e.g. positions of Gleicheniaceae, Lindsaeaceae, Nephrolepis [previously in Lomariopsidaceae] unclear). Davalliaceae and related taxa are sister to the polygrammoid ferns, and they, too, include a number of epiphytes (for their evolution, see Tsutsumi & Kato 2006). Relationships suggested by structural changes in the chloroplast genome (Wolf & Roper 2008; Wolf et al. 2010) are consistent with those suggested by sequence analyses.

Classification. Smith et al. (2006, 2008) propose a phylogeny-based reclassification of the ferns, and they also include literature, ordinal and familial synonymy, and a list of accepted genera and some major synonyms; Prelli (2010) gives a nice account of European ferns. However, it is likely that adjustments to this classification will be needed as details of the phylogeny become better understood (Schuettpelz & Pryer 2007, 2008; Kuo et al. 2011). A provisional hierarchy of characters obtained from Smith et al. (2006, 2008) and also from Pryer et al. (1996), is given below; for a linear sequence of families and genera, see Christenhusz et al. (2011b).

Previous Relationships. Psilotum and relatives used to be considered the most primitive living vascular plants.

EQUISETOPSIDA

Equisetales Berchtold & Presl
Equisetaceae
Roots ?arch; (1->3,1->4)-ß-d-glucans +; stem ridged, with central canal; protoxylem lacunae developing; amphicribral leaf vascular bundles; branches whorled; leaves small, 1-veined, whorled, basally connate; sporangia borne on peltate sporangiophores, aggregated into a strobilus; sporangial cell walls with helical secondary thickenings; spores with circular aperture, green, elaters 4-6, spatulate, helically-coiled; gametophyte green, surficial; embryo exoscopic; x = 108. 1/15.
Extant species of Equisetum seem to have separated in the Tertiary, although the clade to which they belong has probably been separate from other monilophytes since the Permian, ca 250+ million years before present (Des Marais et al. 2003). Change in spore morphology over time from the Calamites type to the at first sight very different spores of Equisetum is convincingly demonstrated by Grauvogel-Stamm and Lugardon (2009). Mycorrhizal associations are not known in Equisetum (Read et al. 2000). For fossils with some of the features of crown group Equisetum, but at least 136 million years old, see Stanich et al. (2009), for still older Equisetum-like spores and elaters from the Middle Triassic - but with trilete marks on the spores, see Schwendemann et al. (2010), and for (1->3,1->4)-ß-d-glucans, see Fry et al. (2008).

Psilotales + Ophioglossales: Root hairs 0; collateral leaf vascular bundles; gametophyte subterranean, axial, non-photosynthetic, mycorrhizal; 1C genome values at least 35 pg.

Both Psilotum and Ophioglossum have very large genomes, with 1C values at least 35 pg (Bennett & Leitch 2005), that are very unusual in land plants. Note that Schneider et al. (2009) find several vegetative apomorphies such as simple leaf blade and stems with both radial and dorsiventral symmetries (= erect plus creeping stems...) suggesting a clade [Psilotales + Equisetopsida].

Ophioglossales Link
Ophioglossaceae
Root with 2-5 protoxylem poles; cork mid cortical; vascular cambium +; stem stele sympodial in construction; circular bordered pits +; (axillary buds +); leaf bases sheathing; vernation nodding; one or more sporophores associated with each tropophore; embryo development?; x = 45 (46). 4/80.
See Hauk et al. (2003) for a phylogeny, Mankyua not included. Takahashi and Kato (1988) describe the development of lateral meristems in the family.

Marattiopsida + Polypodiopsida: amphicribral leaf vascular bundles; leaf vernation circinate; scales +; sporangia abaxial; gametophyte green, surficial; mitochondrial atp1 intron gain.

MARATTIOPSIDA

Marattiales Link
Synonymy: Christenseniales Doweld
Marattiaceae
Roots with several protoxylem poles; dictyostele +; mucilage canals +; rhizome with scales; hydathodes [lenticels] +; fronds pulvinate, with fleshy and starchy stipules; root hairs septate [?multicellular]; spores bilateral or ellipsoid, monolete; embryo endoscopic [suspensor 0]; x = 40. 5/150: Danaea (50).
For a phylogeny, see Murdock (2008a), also Christenhusz et al. (2008); both Marattia and Angiopteris are paraphyletic - but can easily be made monophyletic (Murdock 2008b). For Danaea, see Christenhusz (2010).

POLYPODIOPSIDA, i.e. leptosporangiate ferns.

Primary cell walls poor in mannans and rich in tannins; roots with 2 protoxylem poles; primary xylem with scalariform bordered pits; sporangium stalk 4-6 cells across, wall one cell thick; sporangium with annulus; spores 64-800; antheridium ± exposed; gametophyte cordate [level?]; embryo prone, first cell wall of the zygote vertical, (exoscopic, cell wall vertical - gametophyte subterranean).

Osmundales Link
Osmundaceae
Stem with ectophloic siphonostele, with a ring of conduplicate/twice conduplicate discrete bundles; fertile and sterile portions of fronds separate (fertile and sterile fronds separarte); annulus a lateral group of cells; spores green; x =22. 4/20.
The Osmunda clade originated in the late Carboniferous, ca 323 million years before present, or perhaps ca 305 million years before present (Phipps et al. 1998; Schneider et al. 2004a) and are very diverse from the Permian onwards, less so more recently. Osmunda is paraphyletic, with Osmunda (now = Osmundastrum) cinnamomea being sister to the rest of the family (Metzgar et al. 2008).

[Hymenophyllales + Gleicheniales] [Schizaeales [Salviniales [Cyatheales + Polypodiales]]]: protostele +; sporangia in sori, annulus ± oblique, continuous; loss of chloroplast trnK gene and its intron.

Hymenophyllales A. B. Frank
Hymenophyllaceae
Axillary buds +; frond blades one cell thick between veins, stomata 0; sporangia on ± elongated receptacle, maturation basipetal; spores globose, green; gametophyte filamentous or ribbon-like; x = 36. 9/600.
For the phylogeny of Hymenophyllaceae, which have both climbing and epiphytic taxa, see Pryer et al. (2001b) and Dubuisson et al. (2003), for that of Trichomanes and relatives, see Ebihara et al. (2007), for epiphytism in Hymenophyllaceae, see Hennequin et al. (2008), and for a possible base chromosome number in the family - previous suggestions of x = 6-9, 11, 13, but here suggested as being 36, see Hennequin et al. (2010).

Gleicheniales Schimper
Root steles with 3-5 protoxylem poles; rhizome with scales; veins anastomosing; sporangium maturation simultaneous; antheridia with 6-12 narrow curved or twisted cells in walls.
Synonymy: Dipteridales Doweld, Matoniales Reveal, Stromatoperidales Reveal
Gleicheniaceae
Leaves indeterminate, pseudodichotomously forked; spores (bilateral), monoulcerate; gametophyte with clavate hairs; x = 22, 34, etc. 6/125.
Dipteridaceae + Matoniaceae: ?
Dipteridaceae
Veins reticulate, areoles with included veins, veins 4.4-5.6 mm/mm²; sporangia with "long" stalks, (spores bilateral, monolete); x = 33. 2/11. N.E. India to N.E. Australia, previously widespread.
Matoniaceae
Stems solenostelic, with two vascular cylinders and a central bundle; fronds or pinnae ± dichotomously branched; sorus indusiate; x = 25, 26. 2/4. Previously widespread.

Schizaeales [Salviniales [Cyatheales + Polypodiales]]: plant with hairs; endospore 2-layered; antheridium wall ca 3 cells across; two overlapping inversions in chloroplast genome.

Schizaeales Schimper
Fronds differentiated into fertile/sterile portions; annulus sub-apical.
Lygodiaceae
OLeaves indeterminate, climbing, pseudodichotomously branched, with a bud in angle of branch; one sporangium/sorus, subtended by antrorse indusium-like flange; x = 29, 30. 1/25.
Anemiaceae + Schizaeaceae: sporangia not in sori, exindusiate.
Anemiaceae
Spores tetrahedral, with parallel ridges; x = 38. 1/100.
Schizaeaceae
Inner pericyclic cells 6, 8, thickened; leaves simple or fan-shaped; sporangia borne on marginal projections at blade tip; spores bilateral, monolete; gametophyte filamentous or white, subterranean, tuberous; x = 77, 94, 103[!]. 2/30.

Salviniales [Cyatheales + Polypodiales]: sporangium stalk 1-3 cells across [?position]; two [more!] overlapping inversions in chloroplast genome.

Salviniales Bartling
Aquatics, aerenchyma +; stems dichotomizing; veins ± anastomosing; sterile/fertile leaf dimorphism; sporangia lacking annulus; heterosporous, megaspore single; gametophyte development endosporic; nrDNA with 5.8S and 5S rDNA in separate clusters.
See Nagalingum et al. 2006 (sporocarp structure) and Nagalingum et al. 2008 (phylogeny).
Synonymy: Marsileales von Martius, Pilulariales Berchtold & Presl
Marsileaceae
Leaflets to 4/frond; sori in stalked bean-shaped sporocarps; megaspore with acrolamella over the exine aperture, perine gelatinous; female gametophyte with 1 archegonium; x = 10. 3/75.
Salviniaceae
Plant free-floating; fronds sessile, distichous, less than 24 mm long; x = 9, 22. 2/16.

Cyatheales + Polypodiales: dictyostele +; hydathodes +.

Cyatheales A. B. Frank
Hairs +; sori terminal on veins, indusiate, indusium with outer and inner parts; sporangium stalk ca 5 cells across; antheridium walls ³5 cells across.
For modelling of niche evolution, see Bystriakova et al. (2011).
Synonymy: Dicksoniales Deveal, Hymenophyllopsidales Reveal, Loxomatales Reveal, Metaxyales Doweld, Plagiogyriales Reveal
Thyrsopteridaceae
Indusium cup-shaped, receptacle columnar, clavate; x = ca 78. 1/1.
[Loxomataceae + Culcitaceae + Plagiogyriaceae] [Cibotiaceae + Cyatheaceae + Dicksoniaceae + Metaxyaceae]: ?
Loxomataceae + Culcitaceae + Plagiogyriaceae: ?
Loxomataceae
Indusium urceolate, receptacle elongate, often exserted; gametophyte with scale-like hairs; x = 46, 50 2/2.
Culcitaceae + Plagiogyriaceae: ?
Culcitaceae
Outer indusium scarcely differentiated; sori with paraphyses; x = 66. 1/2.
Plagiogyriaceae
Young fronds with dense, pluricellular, mucilage-secreting hairs; indusium 0; x = ?66. 1/15.
Cibotiaceae + Cyatheaceae + Dicksoniaceae + Metaxyaceae: paraphyses +.
Cibotiaceae
Stomata with three subsidiary cells; spores with equatorial flange, usu. parallel ridges on distal face; x = 68. 1/11.
Cyatheaceae
Stem with polycyclic dictyostele; scales +, large (also small); fronds large; (sori superficial; indusium 0 to completely surrounding sporangia); x = 69. 5/600.
See Korall et al. (2007) for a phylogeny, Bystriakova et al. (2011) for niche evolution.
Dicksoniaceae
Adaxial [outer!?] valve of sorus formed by reflexed frond segment margin and often differently coloured from the other; x = 56, 65. 3/30.
Metaxyaceae
Indusium 0; x = 95, 96. 1/2.

Polypodiales Link
Sporangium stalk 1-3 cells thick; sporagial maturation mixed; sporangium with vertical annulus interrupted by stalk and stomium.
Synonymy: Aspleniales Reveal, Athyriales Schmakov, Blechnales Reveal, Dennstaedtiales Doweld, Dryopteridales Schmakov, Lindseales Doweld, Negripteridales Reveal, Parkeriales A. B. Frank, Platyzomatales Reveal, Pteridales Doweld, Thelypteridales Doweld
Lindsaeaceae
Innermost cortical layer of root usu. of 6 large cells; stele protostelic, with internal phloem; scales +; indusium opening towards margin; x = 34, 38, etc. 6/200. Pantropical (subtropical).
See Lehtonen et al. (2010) for a phylogeny and generic classification.
Saccolomataceae
Scales?; petiole with omega-shaped bundle; spores also with distinctive ± parallel branched ridges; x = ca 63. 1/12.
Dennstaedtiaceae + Rest: ?
Dennstaedtiaceae
Stele?; hairs jointed; petiole bearing buds, with gutter-shaped bundle; x = 26, 29. 11/170.
Pteridaceae
Scales +; indusium 0; x = 29, 30. 50/950.
For a phylogeny, see Prado et al. (2007) and Schuettpelz (2007).
Eupolypods/POLYPODIALES: scales +; spores reniform, monolete. Aspleniaceae + Woodsiaceae + Thelypteridaceae + Blechnaceae + Onocleaceae: petiole with two ± crescent-shaped vascular bundles.
Aspleniaceae
Root pericyclic sclereids with excentric lumina; scales clathrate; petiole with back-to back C-shaped strands, these fusing and becoming X-shaped; frond usu. with small clavate hairs; sori linear; indusia lateral, linear; sporangium stalks 1 cell thick; spores with decidedly winged perine; x = 35, 36, 38, 39. 1-10/700.
For generic limits, see Bellefroid et al. (2010 and references); Asplenium s. str. is paraphyletic. Helical, non-lignified wall thickenings (cf. the velamen of monocots) occur in cortical cells of some Asplenium, mostly epiphytic species (Leroux et al. 2011).
Woodsiaceae
Petiole vascular bundles uniting distally into a gutter shape; x = usu. 40, 41. 15/700.
Thelypteridaceae
Petiole vascular bundles uniting distally into a gutter shape; hairs acicular; x = 27-36. 5-30/950.
Blechnaceae
Petiole with three to many round vascular bundles arranged in a ring; sori elongated, parallel to median nerve, indusia linear, opening towards median nerve; perine winged; x = 27, 28, etc. ?9/200.
Onocleaceae
Petiole vascular bundles uniting distally into a gutter shape; fronds strongly dimorphic; sori enclosed by reflexed lamina margins; spores chlorophyllous; x = 37, 39, 40. 4/5.
Dryopteridaceae to Rest: rhizome scales of stalk + shield, persistent, dense; petiole with three or more vascular bundles.
A largely epiphytic clade; for rhizome scales, perhaps protecting against dessication and aiding in the absorbtion of water and nutrients, see Tsutsumi and Kato (2008); if they are not at this position on the tree, they should be placed at the next node up (with parallel evolution within Dryopteridaceae). Cystopteris may be sister to the eupolypod II clade (Rothfels et al. 2009).
Dryopteridaceae
Perine winged; x= 41. 30-35/1700.
For a phylogeny, see Liu et al. (2007); Moran et al. (2010a, b) investigate relationships within the bolbitidoid ferns focussing on variation in perispore morphology, Rouhan et al. et al. (2004) those within the speciose Elaphoglossum.
Lomariopsidaceae to Rest: ?
Lomariopsidaceae
Pinnae often articulated; veins free, parallel or pinnate; x = 41. 4/70.
Tectariaceae to Rest: ?
Tectariaceae
Fronds with jointed usually stubby hairs; x = 40. 8-15/230.
Oleandraceae [Davalliaceae + Polypodiaceae]: fronds abscising from rhizome.
Oleandraceae
Fronds abscising just above the base [so leaving phyllopodia]; x = 41. 1/40.
Davalliaceae + Polypodiaceae: epiphytic habitat predominant.
Davalliaceae
x = 40. 4-5/65.
For a generic classification, see Kato and Tsutsumi (2008).
Polypodiaceae
(Petiole with one vascular bundle - grammitids); indusium 0; (spores green, globose-tetrahedral, trilete - grammitids); x = 35-37. 56/1200.
For root anatomy, see Schneider (1996, 1997), for a phylogeny of microsoroid ferns, eee Kreier et al. (2008), for that of grammitid ferns, see Sundue et al. (2010 and references: generic changes).