EVOLUTION OF LAND PLANTS (under construction)
Most land plants are members of a clade embedded in a largely aquatic 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), and especially Lewis and McCourt (2004). 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. Other members include Volvox, Caulerpa, Ulva and Acetabularia. Streptophytes include land plants (the embryophytes), and a subset of 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 duplication yielding the important GapA/B gene pair seems to have occured in the common ancestor of the streptophytes (J. Petersen et al. 2006). Lewis and McCourt (2004) emphasize that many clades of "green algae" have terrestrial representatives, of which embryophytes are the most prominent.
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 Zygonematales 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]]]]. 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. Characters supporting a relationship between land plants and a subset of "algae" include many details of cell division, occurence of an apical cell in the gametophyte, flagellum ultrastructure, occurence of sporopollenin, 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). Clarifying the position of Zygnematales is clearly critical.
Embryophytes are plants with a diploid embryo retained by the haploid gametophyte, apical meristem a single cell, sporic meiosis, antheridia and archegonia, adaxial sporangia, sporopollenin in the spore wall, wall development being both centripetals and centrifugal, spores the dormant phase of the life cycle, etc. (for other apomorphies, see e.g. Kenrick & Crane 1997; Goffinet 2000; Schneider et al. 2002). They are land plants as we generally think of them, and are first known from the mid-Ordovician, some 476 million years before present (Kenrick 2000; Wellman et al. 2003). For their general evolution, 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) and Friedman et al. (2004: evolution of plant development). 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); Glomales are the fungi likely to have been involved initially. Interestingly, functional mycorrhizal associations, i.e. nutrient exchanging, have not been found in mosses (Read et al. 2000; Davey & Currah 2006). Other apomorphies of embryophytes include a close association between the trnLUAA and trnFGAA genes on the chloroplast genome; these genes are not associated in other green plants (Quandt et al. 2004).
Substantial progress has been made in the last decade in disentangling relationships within and between the major groups of land plants, i.e. mosses, liverworts, clubmosses, lycophytes, ferns and their allies, gymnosperms and angiosperms (e.g. cf. Bateman et al. 1998). Relationships among the evascular land plants ("bryophytes"), and between them and other embryophytes remain somewhat unclear (e.g. Quandt & Stech 2003), although studies are tending towards supporting a set of relationships [liverworts [mosses [hornworts + vascular plants]]]. Early studies had 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, but cf. root hairs and rhizoids below). Nishiyama et al. (2004) rather unexpectedly (given studies over the last decade or more) propose that the three bryophyte groups form a 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 similar sampling issue). However, a similar grouping 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). In a few earlier studies the liverworts appeared not to be monophyletic (Bopp & Capesius 1998 and references).
Mitochondrial sequence data sometimes place hornworts as sister to all other land plants (for references, see Stech et al. 2003). Goffinet (2000) and Renzaglia and Vaughn (2000) suggests synapomorphies for the clade [all land plants minus hornworts] and Goffinet (2000) and Shaw and Renzaglia (2004) summarise the literature on this whole problem. However, Dombrovska and Qiu (1994) suggested that several lines of evidence such as the content of the inverted repeat and intron distribution 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. More recently 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 suggest that liverworts are sister to all other land plants (see also Rydin & Källersjö 2002, not all analyses). An extension of the chloroplast inverted repeat placed hornworts as sister to tracheophytes alone, as does 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). Recently, Qiu et al. (2006) confirmed the set of relationships [liverworts [mosses [hornworts + vascular plants]]] 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).
Brown and Lemmon (1997) review the distribution of the quadripolar microtubule system in land plants; it occurs in bryophytes, lycophytes, and Marattiales, at least. This system is linked with monoplastidy, the microtubule organising centre being associated with the plastid. [to be worked up]
Liverworts (Marchantiophyta) are 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). 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; 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). Treubiopsida, a small group with rather simple thalli, also include Haplomitrium; 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). Cryptopthallus mirabilis is the only mycoheterotrophic liverwort, obtaining its metabolites from pine or birch via the ectomycorrhizal basidiomycete, Tulasnella (Wickett & Goffinet 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). 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.
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). All three major groupings of fungi that form mycorrhizal associations with plants, zygomycetes, ascomycetes, and basidiomycetes, are known to be asssociated with liverworts (Read et al. 2000; Duckett et al. 2006b), and although the liverworts of the first pectinations are associated with the zygomycete Glomales 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).
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). Their classification is outlined by Shaw and Goffinet (2000, see also Goffinet & Buck 2004). 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). 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, thus the genus may be sister to all other mosses (Samigullin et al. 2002); there are no stomata on the sporophyte. 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. 2003b). The position of Takakia - was it a moss or liverwort? - was initially uncertain, but its morphology is now better understood (see Renzaglia et al. 1997), while in Sphagnales the highly distinctive Sphagnum leucobryoides (= Ambuchanania) was described less than twenty years ago (Yamaguchi et al. 1990). Andraea also has a thalloid early gametophytic stage. For a classification of mosses based on recent phylogenetic studies (e.g. Newton et al. 2000; Cox et al. 2004) see Goffinet and Buck (2004); 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, with subsequent semi-stasis (Shaw et al. 2003a; Newton et al. 2006a, b), although there may also have been more recent ([post-]Cretaceous) diversification as well. Bell et al. (2007) discuss the phylogeny of the early diverging pleurocarp clades, and adjust their taxonomy accordingly, while Buck et al. (2005) discuss the phylogeny of Hookeriales. Mosses seem not to form functional mycorrhizal associations with fungi, although endophytic fungi may affect their growth and ecology (Read et al. 2000; Davey & Currah 2006). Genome size in mosses is small, 1C vales being less than 1.4 pg (Bennett & Leitch 2005); I do not know what it is in liverworts, etc.
Hornworts are probably plesiomorphically thalloid plants that live in close association with the N-fixing Nostoc; they appear to lack flavonoids, and their sporophyte has a bulbous foot, no seta, a central columella, no well-defined valves, and there are stomata (lost 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. Relationships within hornworts are in a state of flux. It is possible that Leiosporoceros is sister to the rest of the group. 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. 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.
Qiu et al. (2006b, 2007 and references) suggest a number of features particularly of the sporophyte of hornworts that suggest similarities with polysporangiophytes in particular; they may turn out to be synapomorphies of the two. These include a long-lived, chlorophyllous sporophyte that is nutritionally largely independent of the gametophyte, an interdigitate sporophyte-gametophyte junction with the sporophyte cells showing rhizoid-like behaviour, gametangia embedded in the gametophyte, etc. The cell walls of spores and 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...
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; this construction 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 polysporangiophyte and that of bryophytes is unclear (Kato & Akiyama 2005). Some early polysporangiophyte gametophytes appear to have been elaborate structures, although different in morphology from the spotophytes, and to have had stomata (Taylor et al. 2005).
Not all polysporangiophyes have vascular tissue, and they include a more restrictive group, the tracheophytes or vascular plants, all of which do have a vascular system with tracheids and sugar-transporting cells with sieve elements. 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).
Recent molecular studies (see below for references) suggest a fundamental reorganisation of relationships among extant tracheophytes, with just three main clades being recognised - [lycophytes [monilophytes + lignophytes]]. This compares dramatically with the psilotophyes, equisetophytes, lycophytes, pteridophytes s. str., and seed plants (arranged from "primitive" to "advanced"!) that I was taught. The association of Psilotum in particular, but also Equisetum, with ferns that has recently been very largely accepted was particularly unexpected. Although there was some morphological evidence suggesting this position (e.g. Bierhorst 1977), it was not seen as being absolutely solid, and in textbooks and even 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 others, as well as looking similar to some fossils. Although the reorganisation just mentioned has been severely criticised (Rothwell & Nixon 2006), it is unclear how damning this 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.
Extant vascular plants all have some kind of roots and stem and are placed in the lycophytes and the euphyllophytes; 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. Pryer et al. (2004b) provide a useful summary of the evolution of the vascular plants, 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, etc. (Kenrick & Crane 1997; Boyce 2005 and literature). Lycopsida represent the extant members of this clade, and have vascularised 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 within the last 80 my at most.
Crown euphyllophytes mostly have roots with exarch protoxylem, spirally arranged euphylls or megaphylls (but see below), sporangia borne in pairs and grouped in terminal trusses, a 30kb chloroplast inversion in the large single-copy region of the chloroplast genome, multiflagellate sperm, etc. (Raubeson & Jansen 1992b; Kenrick & Crane 1997). They appear to date from 401-380 million years ago (Leebens-Mack et al. 2005) and are in turn made up of two clades, ferns and their relatives, the monilophytes or Moniliformopses, lacking true roots, and lignophytes, made up largely of seed plants or spermatophytes. However, details of the evolution of megaphylls - indeed, a satisfactory definition for them seems to be lacking - are still somewhat unclear (see e.g. Sporne 1965, but cf. Harrison et al. 2005; Boyce 2005 summarises the literature). The leaf supply to megaphylls in monilophytes seem 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), so from this point of view megaphylls in the two groups may represent parallelisms rather than a synapomorphy and leaf gaps are not equivalent, being used in a descriptive sense only (Namboodiri & Beck 1968c; Beck et al. 1982); Floyd and Bowman (2007) suggest that megaphylls have evolved independently in the angiosperms and ferns and relatives (see also Gensel & Kenrick 2007). The situation remains unclear, thus 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). 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).
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), spore wall development that is exclusively centrifugal, details of spermatozoid morphology and movement, a nine-nucleotide insertion in the plastid rps4 gene, etc. (e.g. Renzaglia et al. 2002; Schneider et al. 2002). Their circumcumscription has only recently become clear, and as just mentioned they include 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 Equisteaceae alone sister to all other ferns; some support came from a rps4 anlysis, and also 4- and 5-gene analyses, the latter two with strong support (Schuettpelz et al. 2006). 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). The inclusion of morphology alone or in combination also affects relationships (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). 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). Smith et al. (2006) 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. However, it is likely that adjustments to this classification will be needed as details of the phylogeny become better understood (Schuettpelz & Pryer 2007). A provisional hierarchy of characters obtained from Smith et al. (2006) and also from Pryer et al. (1996), is given below. For pteridophytes in general (these often include lycophytes), see also Kato (2005).
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 fibers rare; stem endodermis and pericycle +; frond veins not anastomosing; sporangium stalk 6< cells across, walls two cells thick, lacking an annulus, spores/sporangium 1000<, white, spores globose-tetrahedral, trilete, exospore 3-layered; gametophytes exosporic, green, photosynthetic, antheridium embedded, wall 5< cells thick; first division of the zygote horizontal; nine-nucleotide insertion in the plastid rps4 gene.
General fern diversity decreased (along with that of the cycads) through the Cretaceous (Wing & Boucher 1998), and 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 occured subsequent to the diversification of the angiosperms. Indeed, ferns appear to have temporarily dominated after the end-Cretaceous bolide impact (Schneider et al. 2004a). Quite a number of the polygrammoid ferns (Polypodiaceae + Grammitidaceae) are epiphytic, and the Grammitidaceae in particular have green spores and accelerated plastid genome evolution, a correlation also found elsewhere in ferns, but not 100% (Schneider et al. 2004b). Note that 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 details of stelar morphology and evolution, see Beck et al. (1982).
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), very unusual in land plants.
Psilotales
Psilotaceae: roots 0; leaves small, veins 1 or 0; sporangia 2-3, fused, forming synangium; spores kidney-shaped, monolete. 2/12.
Ophioglossales
Ophioglossaceae: root with 2-5 protoxylem poles; stem stele sympodial in construction; circular bordered pits+; leaf bases sheathing; vernation nodding; one or more sporophores associated with each tropophore. 4/80.
See Hauk et al. (2003) for a phylogeny, Mankyua not included.
Equisetopsida [Marattiopsida + Polypodiopsida]: amphicribral leaf vascular bundles; gametophyte green, surficial.
EQUISETOPSIDA
Equisetales
Equisetaceae: roots ?arch; stem ridged, with central canal; protoxylem lacunae developing; 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 and 4-6 spatulate coiled elaters, green. 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). Mycorrhizal associations are not known in Equisetum (Read et al. 2000).
Marattiopsida + Polypodiopsida: vernation circinate; scales +; sporangia abaxial; mitochondrial atp1 intron gain.
MARATTIOPSIDA
Marattiales
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]). 4/150.
For a phylogeny, see Christenhusz et al. (2008).
POLYPODIOPSIDA
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?]; first cell wall of the zygote vertical.
Osmundales
Osmundaceae: stem with ectophloic siphonostele, with a ring of discrete bundles; annulus a lateral group of cells; spores green. 3/20.
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 (= 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.
Hymenophyllales
Hymenophyllaceae: blades one cell thick between veins, stomata 0; sporangium maturation basipetal, receptacle ± elongated; spores globose, green. 9/600.
For the phylogeny of Hymenophyllaceae, which have both climbing and epiphytic taxa, see Pryer et al. (2001b) and Dubuisson et al. (2003), and for that of Trichomanes and relatives, see Ebihara et al. (2007).
Gleicheniales
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.
Gleicheniaceae: leaves indeterminate, pseudodichotomously forked; (spores bilateral); gametophyte with clavate hairs. 6/125.
Dipteridaceae + Matoniaceae: ?
Dipteridaceae: sporangia with "long" stalks, (spores bilateral, monolete). 2/11. N.E. India to N.E. Australia, peviously widespread.
Matoniaceae: stems solenostelic, with two vascular cylinders and a central bundle; sorus indusiate. 2/4. Previously widespread.
Schizaeales + Salviniales + Cyatheales + Polypodiales: plant with hairs; endospore 2-layered; antheridium wall ca 3 cells across.
Schizaeales
Lygodiaceae: one sporangium/sorus, subtended by antrorse indusium-like flange. 1/25.
Anemiaceae + Schizaeaceae: sporangia not in sori, exindusiate.
Anemiaceae: spores tetrahedral, with parallel ridges. 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. 2/30.
Salviniales + Cyatheales + Polypodiales: sporangium stalk 1-3 cells across [?position].
Salviniales (see Nagalingum et al. 2006: sporocarp structure).
Aquatics, aerenchyma +; veins anastomosing; sterile/fertile leaf dimorphism; sporangia lacking annulus; heterosporous, megaspore single; gametophyte development endosporic.
Marsileaceae: leaflets to 4/leaf; megaspore with acrolamella over the exine aperture, perine gelatinous; female gametophyte with 1 archegonium. 3/75.
Salviniaceae: plant free-floating; leaves sessile, distichous, less than 24 mm long. 2/16.
Cyatheales + Polypodiales: dictyostele +; hydathodes +.
Cyatheales
Hairs +; sori terminal on veins, indusiate, indusium with outer and inner parts; sporangium stalk ca 5 cells across; antheridium walls 5< cells across.
Thyrsopteridaceae: indusium cup-shaped, receptacle columnar, clavate. 1/1.
Loxomataceae + Culcitaceae + Plagiogyriaceae + Cibotiaceae + Cyatheaceae + Dicksoniaceae + Metaxyaceae: ?
Loxomataceae + Culcitaceae + Plagiogyriaceae: ?
Loxomataceae: indusium urceolate, receptacle elongate, often exserted; gametophyte with scale-like hairs. 2/2.
Culcitaceae + Plagiogyriaceae: ?
Culcitaceae: outer indusium scarcely differentiated; sori with paraphyses. 1/2.
Plagiogyriaceae: young leaves with dense, pluricellular, mucilage-secreting hairs; indusium 0. 1/15.
Cibotiaceae + Cyatheaceae + Dicksoniaceae + Metaxyaceae: paraphyses +.
Cibotiaceae: stomata with three subsidiary cells; spores with equatorial flange. 1/11.
Cyatheaceae: stem with polycyclic dictyostele; scales +, large (also small); (sori superficial; indusium 0 to completely surrounding sporangia). 5/600. See Korall et al. (2007: phylogeny).
Dicksoniaceae: adaxial [outer!?] valve formed by reflexed leaf segment margin and often differently coloured from the other. 3/30.
Metaxyaceae: indusium 0. 1/2.
Polypodiales
Sporangium stalk 1-3 cells thick; sporagial maturation mixed; sporangium with vertical annulus interrupted by stalk and stomium.
Lindsaeaceae: innermost cortical layer of root usu. of 6 large cells; stele protostelic, with internal phloem; scales +; indusium opening towards margin. 8/200.
Saccolomataceae: scales?; petiole with omega-shaped bundle; spores also with distinctive ± parallel branched ridges. 1/12.
Dennstaedtiaceae + Rest: ?
Dennstaedtiaceae: stele?; hairs jointed; petiole bearing buds, with gutter-shaped bundle. 11/170.
Pteridaceae: scales +; indusium 0. 50/950. For a phylogeny, see Prado et al. (2007); Schettpelz (2007).
Eupolypods: 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. 1-10/700.
Woodsiaceae: petiole vascular bundles uniting distally into a gutter shape. 15/700.
Thelypteridaceae: petiole vascular bundles uniting distally into a gutter shape. 5-30/950.
Blechnaceae: petiole with three to many round bundles arranged in a ring; indusia linear, opening towards midrib; perine winged. ?/200.
Onocleaceae: petiole vascular bundles uniting distally into a gutter shape; fronds strongly dimorphic; sori enclosed by reflexed lamina margins. 4/5.
Drypoteridaceae to Rest: petiole with three or more vascular bundles.
Dryopteridaceae: perine winged. 40-50/1700. For a phylogeny, see Liu et al. (2007).
Lomariopsidaceae to Rest: ?
Lomariopsidaceae: veins free, parallel or pinnate. 4/70.
Tectariaceae to Rest: ?
Tectariaceae: fronds with jointed used stubby hairs. 8-15/230.
Oleandraceae + Davalliaceae + Polypodiaceae: fronds abscising.
Oleandraceae: fronds abscising just above the base [so leaving phyllopodia]. 1/40.
Davalliaceae + Polypodiaceae: ?
Davalliaceae: 4-5/65.
Polypodiaceae: (petiole with one vascular bundle - grammitids); indusium 0; (spores green, globose-tetrahedral, trilete - grammitids). 56/1200.
For root anatomy, see Schneider (1996, 1997).