EVOLUTION OF LAND PLANTS (UNDER CONSTRUCTION)

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

Background. As little as thirty years ago our understanding of the evolution of land plants was very different from what it is now. Then it was usually thought that Psilotum represented a very ancient group, often being compared with plants from the Devonian Rhynie Chert; that horsetails were also ancient (but not immediately related), and were linked to the fossil Sphenophyllum and its relatives; that Lycopodium, Selaginella and relatives formed a group, after which came ferns, gymnosperms, and seed plants. Bryophytes, that is mosses, liverworts and hornworts, represented the earliest land plants. Relationships between the bryophytes was unclear, but they seemed to form a single group, while the aquatic Characeae (inc. Nitella) with their quite complex haploid plant bodies were thought to be the "algal" group most closely related to land plants (e.g. Graham 1993). Overall, evolution was depicted as a fairly straightforward increase in complexity, but this comforting sequence has been severely challenged over the last fifteen years or so.

Relatives of Land Plants. Land plants or Embryopsida are members of a clade embedded in a largely aquatic paraphyletic group, the green algae; the two together make up Viridiplantae. Viridiplantae can be divided into two main groups, Chlorophyta s. str. and Streptophyta, which includes the paraphyletic "Charophyta s.l.". For general 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. Lewis and McCourt (2004) emphasize that many clades of "green algae" have terrestrial representatives, of which Embryopsida are merely the most prominent. Other chlorophytes include Volvox, Caulerpa, Ulva and Acetabularia.

STREPTOPHYTES

These include land plants (= embryophytes or Embryopsida) and a subset of freshwater green algae like Mesostigma viride, Chlorokybus, Klebsormidium, Spirogyra, Coleochaete, and Chara.

Age. Stem streptophytes have been dated to 1200-725 m.y. (Yoon et al. 2004: Chaetosphaeridium vs. the rest), while Zimmer et al. (2007) give an age of (963-)725(-587) m.y. for the divergence of Chlamydomonas from the streptophytes.

A possible synapomorphy for the node that includes Mesostigma viride and the rest is the presence of the ndh and rps15 and the loss of the rps9 chloroplast genes, although Chara has the rps9 but not the rps15 genes (Martín & Sabater 2010); the presence of introns in the ndhA and ndhB genes may also be apomorphies around here. The BIP multigene family is prominent (Friedl & Rybalka 2012). Lang et al. (2010) noted that a considerable number of transcription-associated protein families evolved in the basal land plants or their immediate aquatic ancestors, many more than subsequently, but exactly where subsequent changes occur is unclear since nothing between Selaginella and angiosperms was included (interestingly, there seems to be no whole-genome duplication in Selaginella). 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; Wodniok et al. 2011 - see also next paragraph).

There are several other features common in streptophytes. The zoospores are covered with small square scales and have paired flagellae that are laterally inserted, joining a multilayered structure (Mattox & Stewart 1984; Simon et al. 2006). The photorespiratory glycolate pathway occurs in peroxisomes rather than in mitochondria (Stabenau & Winkler 2005). The duplication yielding the important GAPA/B gene pair occurred around here, and streptophytes have a particular isoform of glyceraldehyde-3-phosphate dehydogenase, GAPDH B (Peterson et al. 2006).

Phylogeny. Resolving the relationship of the polyphyletic prasinophytes, mostly Chlorophyta, has been important (e.g. Lewis & McCourt 2004; Niklas & Kutschera 2010). Mesostigma viride, the only streptophyte with an eye spot, used to be included in that group, but it 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). Its zoospores have scales but lack a cellulose cell wall (J. Petersen et al. 2006) and it links with the non-motile Chlorkybus (Simon et al. 2006).

Characeae (inc. Nitella) initially seemed to be the immediate sister group of land plants (e.g. Graham 1993: still useful and readable; Karol et al. 2001; Turmel et al. 2003; Delwiche et al. 2004; Qiu et al. 2007: quite strong support), partly because they seemed to be intermediate between simple "algal"-like morphologies and the more complex land plants - they are filamentous, growth is by an apical cell, and they are oogamous. However, Turmel et al. (2006, 2007) 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] + Embryopsida]]] (see also Chang & Graham 2011: Staurastrum not included).

Relationships suggested by Finet et al. (2010) were [Nitella [[Spirogyra, Closterium, etc.] [Coleochaete + Embryopsida]]], however, Zhong et al. (2013a, b; c.f. Springer & Gatesy 2014; Zhong et al. 2014a) found the relationships [Charales [Coleochaetales (inc. Chaetosphaeridium) [[Zygnematales + Desmidales] + Embryopsida]]] or [[Coleochaetales + Zygnematales] Embryopsida], and similar relationships were found by Simon et al. (2006) and Sayou et al. (2014). Although Springer and Gatesy (2014) found different topologies using other methods to analyse the data of Zhong et al. (2013a), Charales were never sister to embryophytes. Indeed, evidence for the sister group relationships of embryophytes and Spirogyra and its relatives is now strong (Timme et al. 2012; see also Wodniok et al. 2011; Ruhfel et al. 2014; Davis et al. 2014a: whole chloroplast genomes; Wickett et al. 2014: transcriptome analyses); the phylogenetic structure in the former is most frequently [[Chlorokybus + Mesostigma] [Klebsormidium [Nitella [[Coleochaete + Chaetosphaeridium] [[Penium + Spirogyra] + embryophytes]]]]]. The [Penium + Spirogyra] clade has a number of apomorphies, including the loss of flagellae and also the loss of morphological complexity (Wodniok et al. 2011; Timme et al. 2012). Whatever the sister-group relationships of embryophytes might be, Chara et al. are no longer likely candidates.

Although this topology questions an evolutionary scenario involving the evolution of ever more complex plant bodies, it is in line with chloroplast genome evolution, including that of the tufA gene. Both Zygnema and the desmid Staurastrum secondarily lack the chloroplast inverted repeat, present in the other streptophytes (Turmel et al. 2007). Many genera of Desmidaceae are polyphyletic (Friedl & Rybalka 2012 and references). Clarifying the relationships of Zygnematales is clearly critical.

EMBRYOPSIDA Pirani & Prado

Gametophyte dominant, independent, multicellular, thalloid, with single-celled apical meristem, showing gravitropism; flavonoids + [absorbtion of UV radiation]; chloroplasts lacking pyrenoids; protoplasm dessication tolerant [plant poikilohydric]; cuticle +; cell wall also with (1->3),(1->4)-ß-D-glucans [Mixed-Linkage Glucans], lignin +; rhizoids unicellular; several chloroplasts per cell; glycolate metabolism in leaf peroxisomes [glyoxysomes]; centrioles in vegetative cells 0, metaphase spindle anastral, predictive preprophase band of microtubules, phragmoplast + [cell wall deposition spreading from around the spindle fibres], plasmodesmata +; antheridia and archegonia jacketed, stalked; spermatogenous cells monoplastidic, centrioles develop de novo, associated with basal bodies of flagellae, multilayered structure +, proximal end of basal bodies lacking symmetry, stellate pattern associated with doublet tubules of transition zone; spermatozoids with a left-handed coil; male gametes with 2 lateral flagellae; oogamy; sporophyte dependent on gametophyte, embryo initially surrounded by haploid gametophytic tissue, plane of first division horizontal [with respect to long axis of archegonium/embryo sac], suspensor/foot +, cell walls with nacreous thickenings; sporophyte multicellular, with at least transient apical cell [?level], sporangium +, single, dehiscence longitudinal; meiosis sporic, monoplastidic, microtubule organizing centre associated with plastid, cytokinesis simultaneous, preceding nuclear division, sporocytes 4-lobed, with a quadripolar microtubule system; spores in tetrads, sporopollenin in the spore wall, wall with several trilamellar layers [white-line centred layers, i.e. walls multilamellate]; close association between the trnLUAA and trnFGAA genes on the chloroplast genome, LEAFY gene present.

Many of the bolded characters in the characterization above are apomorphies of subsets of streptophytes along the lineage leading to the embryophytes, not apomorphies of crown-group embryophytes per se. Members of Klebsormidiales, Coleochaetales, Desmidaceae and Zygnematales have pyrenoids, and so the loss of pyrenoids might be an apomorphy for embryophytes (Cook 2004a, b).

All groups below are crown groups, nearly all are extant; characters mentioned are those of the common ancestor of the group.

Age. Clarke et al. (2011: other estimates, too) suggested an age for crown Embryopsida of (815-)670(-568) m.y., Cooper et al. (2012) estimated its age at (519-)493(-469) m.y., and Magallón et al. (2013: including temporal constraints) an age of around (480.4-)475.3-474.6(-471) m.y. (see the constraint age in Heinrichs et al. 2007) and a stem age of around (962.5-)912-6-911.3(-870) m.y.; the lowest crown date is around 439 m.y. (Magallón & Hilu 2009). An age of (629.5-)529.8(-449.0) m.y. is suggested in Zhong et al. (2014b: fossil calibration); see also P. Soltis et al. (2002) for a vareiety of age depending on calibrations used.

Evolution. Divergence & Distribution. A variety of spores, including spores in permanent tetrads, were produced by "protoembryophytic" plants whose sporophyte basically consisted of these spores alone, and such plants are known from the mid-Ordovician ca 476 m.y. onwards (e.g. Gray 1993; Wellman 2004; Brown & Lemmon 2011a). Fragments of the plant bodies of the first land plants, perhaps liverworts, first appear in rocks from later in the Ordovician, in Oman (Kenrick 2000; Wellman et al. 2003).

The interpolation of mitotic cell divisions between zygote formation and meiosis would allow the production of spores (meiospores, the immediate products of meiosis) of early land plants (for which, see also Edwards et al. 2014) in larger numbers (e.g. Brown & Lemmon 2011a). Thus the evolution of land plants effectively involved 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 (e.g. Haig 2008; Gerrienne & Gonez 2011). More specifically, there may have been an initial development of a diploid spore-producing sporangium (= sporogonium), and later the elaboration of a full-blown free-living sporophyte in the polysporangiophyta (e.g. Kaplan 1997: chap. 19; Kato & Akiyama 2005; Qiu et al. 2012: extensive discussion; Ligrone et al. 2012b). However, we lack reliable knowledge of life cycles in most charophyte algae, and this greatly hampers our understanding of the events that led to the development of this alternation of generations (Haig 2010).

For a detailed study of the morphology of early land plants placed in a phylogenetic context, see Kenrick and Crane (1997), although some aspects of this are now dated, and for apomorphies of various "bryophyte" groups and the early polysporangiophytes, see Ligrone et al. (2012a). Characters supporting a relationship between Embryopsida and subsets of streptophytes include many details of cell division, occurrence of an apical cell in the gametophyte (perhaps), numbers and types of introns in the chloroplast DNA, flagellum ultrastructure, occurrence of sporopollenin (but in lower streptophytes it is associated with the wall of the zygote, not the walls of the spores), retention of the zygote on the haploid plant, and nrDNA in a single array.

The sustained work by Brown and Lemmon (e.g. 1990, 1997, 2007, 2013; Brown et al. 2010) has unravelled much of the complexity of both mitotic and meiotic cell cell division. Brown and Lemmon (1997, see also 2008) reviewed the distribution of the quadripolar microtubule system in land plants; it occurs in all three groups of the "bryophytes", in lycophytes, and in Marattiales, at least. This system is linked with monoplastidy, the microtubule organising centre being associated with the plastid. For variation in plastid number and possible correlations with patterns of microspore division, see Rudall and Bateman (2007). Mougeotia, in the clade sister to Embryopsida, lacks centrioles and has a preprophase band of microtubules, while Coleochaete (same clade, or next clade down) has monoplastidic meiosis and centrioles (e.g. Brown & Lemmon 1993, 2011b). In streptophytes as a whole basal bodies develop de novo immediately prior to the formation of motile sperm cells (Wastenays 2002). As the phylogeny becomes better understood, this will clarify how the distinctive phragmoplast with associated desmotubules (included endoplasmic reticulum), axial microtubules and associated body plan changes of land plants, 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; Stabenau & Winkler (2005: glycolate metabolism, from mitochondria to cytoplasmic; 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; Doyle 2013). Strigolactones, involved in the establishment of vesicular-arbuscular mycorrhizal associations, are known from some streptophytes (Charales) and seem initially to have been involved the control of rhizoid elongation (Delaux et al. 2012). For other possible apomorphies, see e.g. Goffinet (2000), Renzaglia et al. (2000), Schneider et al. (2002), Johnson and Renzaglia (2009) and Doyle (2013). Carothers and Duckett (1982: "bryophytes") and Renzaglia and Garbary (2001) discussed the evolution of the male gametes in land plants in some detail. See e.g. Timme et al. (2012) for apomorphies immediately below the embryophyte node.

If monophyletic bryophytes are indeed sister to polysporangiophyes/vascular plants (Cox et al. 2014), then much of the above will need reevaluation.

Ecology & Physiology. Problems of dealing with life on land centring on water loss, movement of water through the plantprotection from ultraviolet radiation, etc., have shaped the evolution of both gametophyte and sporophyte (e.g. Watkins et al. 2007; McAdam & Brodribb 2011; Willis & McElwain 2014). One of the major changes - better, complex of changes - that facilitated the spread of land plants may have been the evolution of sporopollenin-covered spores from the sporopollenin-covered zygotes of their aquatic ancestors (Gray 1993; Blackmore & Barnes 1987; Brown & Lemmon 2011a). Sporopollenin, the protective element of the zygote wall, became associated with the walls of the haploid spores by a complex process involving precocious initiation of cytokinesis (hence the often quadrilobed, quadripolar microtubule system of many bryophytes), acceleration of meiosis, delay in wall deposition, etc., a mixture of heterochrony and heterotopy (Brown & Lemmon 2011a). The composition of sporopollenin has been remarkably stable, and in lycophyte fossils ca 310 m.y.o. it is rather similar to that in extant lycophytes, indeed, it is similar to the sporopollenin around the embryos in some Charales (Fraser et al. 2012), although the sporopollenin of conifers, at least, may differ.

For photosynthesis in bryophytes and other early land plants, see Hanson and Rice (2014). Komatsu et al. (2014; see also Doi et al. 2006) discuss chloroplast movement in land plants, mediated by a single copy of the blue-light sensitive photoropin gene.

Bacterial/Fungal Associations. Associations between Embryopsida 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 involved. 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 (B. Wang et al. 2010, commentary by Bonfante & Selosse 2010).

Indeed, all the major groupings of fungi that form mycorrhizal associations with plants, Glomeromycota, ascomycetes, and basidiomycetes, are asssociated with liverworts (Read et al. 2000; Duckett et al. 2006b; Pressel et al. 2010; Bidartondo et al. 2011). Bidartondo et al. (2011; see also Pressel et al. 2010) found that Endogone-like fungi (Mucoromycotina) also formed associations with Treubia, Haplomitrium, some hornworts, etc., and surmised that this might be the original land plant-fungus association; associations between liverworts and basidiomycetes and ascomycetes are likely to be secondary (Bidartondo & Duckett 2009). However, even if Mucoromycota were the first fungal associates of liverworts, the establishment of plant-fungus relationships there may be independent of those in other plants.

In some cases the fungus may have moved to the liverwort from a tracheophyte (Ligrone et al. 2007), or, vice versa, the fungus may move from liverworts to seed plants (Pressel et al. 2010: see also Bidartondo & Duckett 2009). For the (mostly ascomycete) endophytic fungi to be found in mosses and liverworts, see Stenroos et al. (2010) and Pressel et al. (2010).

Plant-Animal Interactions. Some caterpillars of Micropterigidae, a basal, jawed, lepidopteran clade that is perhaps Jurassic in age, are detritivores, but others eat mosses (e.g. Atrichum) and especially liverworts (Imada et al. 2011; Hosts, consulted iii.2014), although they also eat angiosperms (Davis & Landry 2012 and references). For the host plants of other jawed moths, see Araucariaceae and Nothofagaceae.

Genes & Genomes. Details of gene and genome evolution in plastids are given by Jansen et al. (2007), A. M. Magee et al. (2010) and Wicke et al. (2011). The trnLUAA and trnFGAA genes are not associated in other green plants (Quandt et al. 2004). For intron distributions in mitochondrial genes, see Dombrovska and Qiu (1994), Qiu et al. (1998) and Regina et al. (2005). In general, "bryophytes" have small mitochondral genomes and little variation in gene order compared with mitochondria in vascular plants (Y. Liu et al. 2014a). RNA editing in which the organelle-targeted pentatricopeptide repeat proteins play an important role is restricted to Embryopsida (Rüdinger et al. 2008).

Sayou et al. (2014) discussed the evolution of the LEAFY gene, usually in a single copy in embryophytes (but two in gymnosperms), yet variously involved in cell division and specification of floral identity. Its binding specificity is notably variable (promiscuous) in the hornworts, and although the evolutionary scenario suggested by Sayo et al. (2014) depicts the topology [hornworts [mosses [liverworts + vascular plants]]], which otherwise seems to have little evidence supporting it (see also below), they suggest that whatever the topology, their promiscuity hypothesis is likely (see their Fig. S9).

In mosses, at least, the great majority - ca 95% - 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 and were recruited by the sporophytic generation. However, 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). It is only in angiosperms that there is a substantial proportion (ca 25%) of genes expressed in the sporophyte alone (Szövényi et al. 2010). Yue et al. (2012) suggested that numerous genes, including those involved in many embryophyte functions like cuticle and lateral root formation, had been acquired by horizontal transfer from fungi and bacteria.

Much of interest is likely to come from the study of individual pathways and their control. Thus important signaling intermediates, the G-protein complex, is known from Chara and land plants (but not the green alga Micromeris), although elements of the pathway seem to be missing in some mosses and liverworts (Hackenberg et al. 2013). Various classes of phosphoprotein phosphatases also have interesting distributions, with the ApaH phosphatases currently being known from streptophytes only, while the ALPH class is absent from land plants (Uhrig et al. 2012). See also Floyd and Bowman (2007)for numerous developmental changes possibly occurring at this node.

Chemistry, Morphology, etc. S lignin, made up of syringyl units, has been found in some liverworts and is scattered elsewhere in vascular plants; in flowering plants it is very common (Li & Chapple 2010; Espiñeira et al. 2010; see also Gómez-Ros et al. 2007). 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).

Duckett et al. (2014) discuss the evolution of rhizoids and rhizoid-like structures; the smooth rhizoids of at least some liverworts are highly endopolyploid. The sporangium develops from tiers of four cells (quadrants) which divide periclinally producing an ampithecium and endothecium; the major groups of bryophytes differ in how the capsule wall and spores develop from these cells (Ligrone et al. 2012a for a summary).

See also Kenrick (2000) and Ligrone et al. (2012a), both morphology, Bateman et al. (1998) and Hemsley and Poole (2004), physiology and ecology of early land plants, Friedman et al. (2004: evolution of plant development), Taylor et al. (2009: fossils, inc. those of fungi associated with plants), Kenrick and Strulla-Derrien (2014): roots and rhizoid-based rooting systems), Jones and Dolan (2012: rhizoids and root hairs), Blackmore and Crane (1998: spore/pollen apertures), Edwards et al. (2014: spores of cryptophytes, spores of land plants not initially as tetrads?), Brown and Lemmon (2013 and references: sporogenesis), Renzaglia and Garbary (2001: male gametes), Schneider et al. (2002), Wastenays (2002: microtubules), Tomescu et al. (2014: apical cells of sporophyte), Waters (2003: molecular adaptation), Hedges et al. (2004: timing), Hodges et al. (2012: cilia) and Doyle (2013: reproductive features). Goffinet and Shaw (2009) and Shaw et al. (2011) provide much general information about the "bryophytes" as a whole.

Phylogeny. See Kenrick and Crane (1997), Nishiyama and Kato (1999) and Shaw and Renzaglia (2004) for early literature on bryophyte relationships. Mitochondrial sequence data sometimes placed hornworts as sister to all other land plants (for references, see Stech et al. 2003); Sayou et al. (2014) found this position in their analysis of the LEAFY gene. Although Renzaglia and Garbary (2010) considered that the evidence for the hornwort basal hypothesis was compelling, Dombrovska and Qiu (1994) had earlier outlined several lines of evidence such as the content of the inverted repeat and intron distributions 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). 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 were sister to all other land plants (see also Rydin & Källersjö 2002 and Karol et al. 2010, but neither in 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 position is also favoured by an analysis of cpITS spacer sequences (Samigullin et al. 2002) and a complete plastome analysis (Karol et al. 2010); see also Magallón et al. (2013).

Other relationships have been suggested. 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. 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). Cox et al. (2014) noticed that trees based on protein coding sequences and trees based on the proteins they coded differed in their topologies, and they suggested that there may have been synonymous substitutions in the sequences; they argued strongly for the monophyly of bryophytes. Liverworts and mosses formed a clade in the recent tree of Finet et al. (2010: hornworts were not sampled), and in some analyses in Karol et al. (2010). In a few earlier studies the liverworts appeared not to be monophyletic (Bopp & Capesius 1998 and references). For possible relationships within land plants as a whole, see also Fiz-Palacios et al. (2011).

Many 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 data sets. 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]; Qiu et al. 2007; S. Li et al. 2013; Y. Liu et al. 2014b: mitochondrial nucleotide and amino acid data, support for any other relationships very weak). In an analysis of whole chloroplast genomes, the relationships [liverworts, mosses [hornworts + vascular plants]] were obtained, although a [liverwort + moss] clade was sometimes recovered (Ruhfel et al. 2014). Indeed, that clade was also recovered by Wickett et al. (2014) in transcriptome analyses, and in many analyses bryophytes (as [hornworts [mosses + liverworts]]) were monophyletic.

MARCHANTIOPHYTA / LIVERWORTS

Gametophyte thalloid, thallus simple, apical cell wedge- or lens-shaped; rhizoids unicellular, smooth, living (pegged, dead); perforate water conducting cells +; distinctive, membrane-surrounded oil bodies + (absent); cell walls with relatively little cellulose; sporophyte with apolar auxin transport, with a bulbous foot, seta evanescent, forming by cell elongation after the sporangium develops; sporangium lacking a columella, opening by four slits; endothecial cells producing archesporial tissue alone; elaters +, unicellular; mitosis with polar organizers as MTOCs; (sporogenesis multiplastidic), spore walls with more or less continuous parallel lamellae at maturity (Wellman et al. 2003).

Age. The crown group is dated to (509-)484(-452) m.y. by (Cooper et al. 2012), although dates in Newton et al. (2007) and Heinrichs et al. (2007) are rather younger, e.g. (410.5-)407.6(-404.7) m.y. in the latter.

From fossil evidence, 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); see also Heinrichs et al. (2007) for an evaluation of the identity of fossils purported to be liverworts.

1. Haplomitriopsida

Mucuromycotan symbiont; thallus apical cell tetrahedral; mucilage copious [stalked slime papillae]; (rhizoids 0 - Hapolomitrium); distinctive blepharoplast.

3/

[Marchantiopsida + Jungermanniopsida]: ?

Age. This node is dated to before the Middle Devonian (475-)442(-408) m.y.a. (Cooper et al. 2012), while Heinrichs et al. (2007) suggest an age of (382.8-)372.6(-362.4) m.y. (see also Newton et al. 2007) and Zhong et al. (2014b) an age of (569.7-)375.8(-172.5) m.y. - [Marchantia + Ptilidium].

2. Marchantiopsida

Mucuromycotan, glomeromycotan or no symbiont; thallus complex; branching truly dichotomous; sporogenesis variable, (sporocytes lacking lobing - Marchantia, etc.).

3. Jungermanniopsida

Mucuromycotan, glomeromycotan, or dikaryan fungal symbiont, (plants epiphytes; fungal association 0 - Porellales); (plant leafy, cutting faces of apical cell at 120o, leaves (2-)3-ranked).

Evolution. Divergence and Distribution. Heinrichs et al. (2007) discussed the evolution of the ca 4,500 species of leafy liverworts, suggesting possible divergence times for the clades (see also Newton et al. 2007), and Wilson et al. (2007a, b) discuss the diversification of Lejeuneaceae in particular. Much of the diversification of Porellales and Jungermanniales, both leafy liverworts epiphytic on bark and leaves of flowering plants, has occurred since the evolution of angiosperms (Ahonen et al. 2003; Forrest & Crandall-Stotler 2004). Indeed, although many liverwort families had diverged by the end of the Cretaceous, they have diversified considerably since (Cooper et al. 2012). Dates in Newton et al. (2007) and Heinrichs et al. (2007) can be quite dramatically older or younger, but their overall conclusions are similar.

For general information easily placed in a phylogenetic context, see Goffinet and Buck (2013); for characters of Haplomitriopsida, see Duckett et al. (2006a).

Ecology & Physiology. Understanding the ecophysiology of the first liverworts is a challenge, but it may be relevant that extant Marchantia, at least, is mixotrophic (Hata et al. 2000; Graham et al. 2010). Field et al. (2012, 2014 and references) discuss details of the nature of the mutualistic association betweem fungus and plant in some liverworts, including Haplomitriopsida (see also Ligrone et al. 2007).

Porellales and Jungermanniales are leafy liverworts that are bark and leaf epiphytes on flowering plants; quite a number of liverworts are dessication tolerant, although most lack internal water-conducting cells (Ligrone et al. 2000).

Reproductive Biology. The dead, pegged rhizoids to be found in marchantialean liverworts with complex thalli may help ensure the water supply to the stalked carpocephala (Duckett et al. 2014).

Plant/Animal Interactions. For a summary of herbivory and galling, including examples from the Middle Devonian where some cells of the fossils perhaps contained oil and represent defence against herbivory, see Labandeira et al. (2013). Caterpillars of the otherwise detritivore Micropterigidae, a basal, jawed, lepidopteran clade, are common on Conocephalum conicum in Japan (Imada et al. 2011).

Bacterial/Fungal Associations. The three major groupings of fungi that form mycorrhizal associations with plants, Mucoromycotina, Glomeromycota, and Dikarya (= ascomycetes + basidiomycetes), are associated with liverworts (Read et al. 2000; Duckett et al. 2006b; Pressel et al. 2010; Bidartondo et al. 2011; Field et al. 2014). Liverworts in the basal pectinations are associated with Glomeromycota (Kottke & Nebel 2005; Field et al. 2014), but this association may subsequently have been lost (Duckett et al. 2006b).

Within Jungermanniopsida, Porellales lack fungus associations, and epiphytic or epilithic liverworts are often not associated with VAM fungi (Pressel et al. 2010). Associations with ascomycetes in Jungermanniales are very old, more than 250 m.y. (Pressel et al. 2008), and the fungus may move from these liverworts to seed plants (Pressel et al. 2010: see also Bidartondo & Duckett 2009). The ascomycete Rhizoscyphus [= Hymenoscyphus] ericae is very commonly an associate of the hair roots of North Temperate Ericaceae, and it also forms mycorrhizal associations with Jungermanniales-Schistochilaceae and other leafy liverworts; colonization of the liverwort is by their rhizoids (Duckett & Read 1995; Upson et al. 2007; Pressel et al. 2008).

Cryptopthallus mirabilis is the only myco-heterotrophic liverwort, indeed, it is the only myco-heterotrophic member of the three basal clades, and it obtains its metabolites from pine or birch via the ectomycorrhizal basidiomycete, Tulasnella (Wickett & Goffinet 2008). Cryptopthallus may be nested within Aneura, also associated with basidiomycetes (Pressel et al. 2010).

Blasia fixes nitrogen by virtue of of its association with Nostoc (Rai et al. 2000).

Chemistry, Morphology, etc. For apical cell division, see Piatkowski et al. (2013).

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, 2013). Monoplastidic meiosis is known from Monoclea, Haplomitrium and Blasia (Brown & Lemmon 2011a). Endopolyploidy has not been detected in liverwort nuclei (Bainard & Newmaster 2010a, b).

For the development of the unicellular elaters, see Renzaglia et al. (1997) and Crandall-Stotler and Stotler (2000), for rhizoids, see Duckett et al. (2014).

Phylogeny. Liverworts are probably monophyletic, despite earlier suggestions that they might not be (Quandt & Stech 2003 for references). 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), Volkmar and Knoop (2010) and Cooper et al. (2012: Treubiopsida = Haplomitriopsida).

Marchantiopsida include Blasia, Sphaerocarpos, etc., although support for the inclusion of the former in this clade was still weak (but c.f. some analyses in Forrest & Crandall-Stotler 2004, esp. 2005; Qiu et al. 2007: Blasia sister to the rest; see also He-Nygrén et al. 2004). Cooper et al. (2012) also found Blasia - with Cavicularia to be sister to the rest. 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: grouped with some simple-thalloid genera; Cooper et al. 2012: extensive study). These general relationships were also recovered by Qiu et al. (2007). For relationships within the speciose Lepidoziaceae, see Cooper et al. (2011), and for those within Lejeunaceae, see Gradstein et al. (2003) and Yu et al. (2013).

Classification. See Crandall-Stotler et al. (2009) for a formal phylogeny-based classification of Marchantiophyta.

STOMATOPHYTES

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

Age. Clarke et al. (2011) suggested an age for this clade of (750-)632(-548) m.y., Magallón et al. (2013) an age of around 458.3 m.y.; other estimates are (748-)703(-658) m.y. (Heckman et al. 2001: protein sequence analysis), a little over 500 m.y. (Villarreal & Renner 2014), (580-)496(-412) m.y. (Zimmer et al. 2007), ca 450 m.y. (Theißen et al. 2001), and (550.8-)487.6(-435.6) m.y. (Zhong et al. 2014b) and ca 470 m.y.a. (Y. Liu et al. 2014a); see also Hedges et al. (2004) and P. Soltis et al. (2002).

Evolution. Divergence & Distribution. Optimization of such distinctive and important features as the presence of stomata, trilete spores, etc., is not easy. Stomata, although optimized to this node, are absent from some of the basal clades of mosses (see below; Merced & Renzaglia 2013; Haig 2013), perhaps suggesting their independent origin within mosses, while trilete spores are known from some mosses, although they are optimized to the next node above here.

When mosses were thought to be sister to vascular plants the conducting tissue in the centre of the stem in some moss gametophytes could be thought of as being homologous with 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). Ligrone et al. (2002) found no great similarity between the water conducting cells of Takakia, the hydroids of other mosses, and the conducting tissues in Haplomitrium and metzgerialean liverworts.

Recent work clarifies such interpretations. Thus Xu et al. (2014) found that similar NAC transcription factor family genes genes were expressed in the development of hydroids of mosses and xylem of vascular plants, despite the difference in generation and in morphology (no pitting or lignification in hydroids), i.a. inducing cell death in both. Such NAC genes are uncommon in liverworts. Similarly, the formation of both sporophytic root hairs in Arabidopsis and gametophytic rhizoids in Physcomitrella involves the same regulatory gene, perhaps independent recruitment and/or some kind of heterochrony/topy (Menand et al. 2007; Pires & Dolan 2010 and references; see also Szövényi et al. 2010); Jones and Dolan (2012) also discuss the evolution of root hairs and rhizoids.

Ecology & Physiology. It has been suggested that stomata are not involved in gas exchange for photosynthesis in either mosses or hornworts, rather, they may facilitate the drying out of the capsule and hence aid in spore dispersal (Pressel et al. 2011; see also Merced & Renzaglia 2013). If this was the original function of stomata (McAdam & Brodribb 2012a, b), then the central role that stomata now play in photosynthesis in vascular plants becomes a spectacular case of an exaption. Much work does suggest that stomatal behaviour of vascular plants differs from that of "bryophytes" (McAdam & Brodribb 2011, esp. Fig. 4), and abscisic acid plays a crucial role in control of stomatal opening only in seed plants, even if similar genes involved in abscisic acid metabolism are found throughout land plants (McAdam & Brodribb 2012). However, Chater et al. (2011) suggested that stomata of the moss Physcomitrella responded to at least some environmental stimuli rather like those of flowering plants, abscisic acid being involved in both (see also Beerling & Franks 2009). Another possible function for stomata is that they increase transpiration and so improve the supply of nutrients to the sporangium (e.g. Haig 2013).

Genes & Genomes. Two copies each of the plant homeobox KNOX genes, involved in meristem activity in vascular plants, and the MADS-box MIKC genes, subsequently functioning i.a. as floral identity genes, are found in mosses; subsequent duplication generated the diversity of these gene classes found in flowering plants in particular (Theißen et al. 2001). For post-transcriptional editing of the chloroplast genes, see Martín and Sabater (2010).

Chemistry, Morphology, etc. For a summary of the literature on the development and adult morphology of the stomata of extant and extinct stomatophytes, see Rudall et al. (2013). 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?). For spore morphology, see Qiu et al. (2012) and Blackmore et al. (2012) and references (correlation: monolete spores, successive sporogenesis, tetrads tetragonal/decussate).

MOSSES.

Several gametophytes developing from a single spore; gametophyte leafy, cutting faces of apical cell at 136o [most], leaves spiral, unistratose; rhizoids multicellular; perichaetium +; sporophyte with basipetal polar auxin transport, sporangium with a pointed foot, seta indurated; calyptra persistent; archesporial tissue from endothecium, columella +; microtubule organizing centres not associated with plastids, diffuse, perinuclear; archesporial cells monoplastidic; endopolyploidy widespread.

Evolution. Crown-group mosses may be (400-)379(-362) m.y.o. (Newton et al. 2009).

Age. The separation of Takakia and Sphagnum is dated to 319-129 m.y.a. (Shaw et al. 2010a).

1. Takakiopsida

Gametophyte initially ?thalloid, mycorrhizal; cutting faces of apical cell at 120o, leaves forked, ± 3-ranked; rhizoids 0; perforate water conducting cells +; plant acrocarpous; capsule dehiscence spiral; stomata 0; monoplastidic mitosis during vegetative growth as well; n = 4.

1/2. East Asia, west North America.

Age. The age of a clade [Sphagnum + The Rest] is (360-)352(-344) m.y.a. (Y. Liu et al. 2014a).

2. Sphagnopsida

Gametophyte with initial protonemal stage, thalloid structure soon developing; leaf cells dimorphic [groups of empty and hyaline cells surrounded by strands of chloroplast-containing cells]; rhizoids 0; capsule sessile, pseudopodium +, dehiscence subapical and transverse ["operculate"], explosive; stomata +, non-functional; columella massive, overarched by spores; archesporial tissue from amphithecium; spore wall multilayered.

1-4/250. World-wide.

Age. Crown-group Sphagnopsida are around 104-30 m.y.o. (Shaw et al. 2010a) orca 25 m.y.o. (Shaw & Devos 2014).

3. Andreaeopsida

Gametophyte initially thalloid; plant acrocarpous; capsule sessile, pseudopodium +; columella overarched by spores; sporangium dehisces down four (eight) vertical slits; stomata 0; spore exine initiated as globules.

2/100: Andreaea (100).

4. The Rest.

Gametophyte initially protonemal; hydroids + [cells dead, no contents], stomata +; capsule dehiscence transverse, peristome +; spores hilate.

Evolution. Divergence & Distribution. Polytrichopsida/Dicranidae/haplolepidious taxa are a diverse but species-poor group compared to the ca 12,000 species of Hypnanae/hypnalian pleurocarpous/arthrodontous mosses (Cox et al. 2010); Newton et al. (2007, 2009; see also Zhong et al. 2014b) give dates for many clades. There is strong geographical signal in the phylogeny of Polytrichopsida, clades being largely south or north temperate (Bell & Hyvönen 2010: intergeneric hybridization?). 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), although there may also have been more recent ([post-]Cretaceous) diversification as well.

Given that some combination of Andreaea, Takakia and Spagnum are at the base of the moss phylogenetic tree and all have distinctive morphologies, apomorphies for mosses as a whole are unclear.

Ecology & Physiology. Mosses are important components of tundra and boreal forests biomes (for the bryosphere, see Lindo & Gonzalez 2010) and may represent a substantial proportion of the biomass in boreal forests (Wardle et al. 2013). Hummock-forming Sphagnum is a major element of the boggy vegetation in such areas, and Sphagnum litter in particular decomposes more slowly than that of other land plants (Verhoeven & Liefveld 1997; Lang et al. 2011). The discovery of Sphagnum-like fossils in Ordovician rocks 455-460 m.y.o. suggests that the ecological equivalents of Sphagnum peatlands may have been around for a rather long time (Graham et al. 2013). However, the diversification of extant peat-forming Sphagnum probably occurred as late as the mid-Miocene (Shaw et al. 2010a; Shaw & Devos 2014).

A few species of feather mosses like Hylocomium splendens and Pleurozium schreberi, pleurocarpous Hypnales, form close associations with Nostoc, nitrogen moving from the latter into the former (Bay et al. 2013). However, details of further movement of nitrogen in the ecosystem are still unclear (Rousk et al. 2013; Lindo et al. 2013).

Bacterial/Fungal Associations. Bay et al. (2013) discuss associations between Nostoc and some pleurocarpous mosses in boreal forests; other blue-green algae are also involved (Rousk et al. 2013 for a review). Functional mycorrhizal associations, i.e. associations that are involved in the exchange of nutrients, are very rare in mosses, and most moss-fungus associations involve parasitic fungi (Read et al. 2000; Davey & Currah 2006). Other endophytic fungi may also affect moss growth and ecology (Read et al. 2000; Davey & Currah 2006).

For the microbiome of Sphagnum, integral to the functioning of the organism and its ecosystem, see Bragina et al. (2014).

Reproductive Biology. For the recurrent evolution of dioecy in mosses - at least 133 times - see McDaniel et al. (2013); this may be accompanied by sexual dimorphism of the plants. Reversal to hermaphroditism is less common, and diversification may be higher in hermaphroditic clades (McDaniel et al. 2013).

Very small arthropods are attracted to volatile compounds produced by Ceratodon purpureus and are involved in the transfer of sperm to the archegonia (Rosenstiel et al. 2012; see also Cronberg et al. 2006).

Genes & Genomes. Genomes in mosses are small, 1C values being less than 1.4 pg (Bennett & Leitch 2005); I do not know what the sizes are in liverworts, etc.. There is a very large (ca 71 kb) inversion of the chloroplast genome in Funariaceae (which includes Physcomitrella), Disceliaceae, and Encalyptaceae, all Funariidae, although Gigaspermaceae lack this inversion (Goffinet et al. 2007).

Yue et al. (2012) found a number of genes in Physcomitrella patens that had moved there by lateral transfer from fungi and bacteria; how widely they might be distributed in mosses is unknown.

Chemistry & Morphology. Gametophyte vascularization is particularly well developed in Polytrichopsida, and the leptoids apparently transport organic molecules (Ligrone et al. 2000). For spore wall morphology of Sphagnum, see Brown et al. (1982); some layers, e.g. the translucent layer, may be unique. There is widespread endopolyploidy, although not in the near-basal Sphagnum (Bainard & Newmaster 2010a, b).

For general information easily placed in a phylogenetic context, see Goffinet and Buck (2013) and for a general entry into the literature, see Goffinet et al. (2004); for sporogenesis, see Brown and Lemmon (1984: Andreaea, 2013), for apical cell division, see Piatkowski et al. (2013), for stomata, see Merced and Renzaglia (2013).

Phylogeny. Relationships between clades at the base of the moss tree remain unclear. Sphagnum, Andreaea and Takakia, initially thought to be a liverwort (see Renzaglia et al. 1997), are all in this area, Sphagnum and Takakia perhaps being sister taxa and Andreaea sister to remaining mosses (e.g. Cox et al. 2004; Qiu et al. 2006, 2007: rather strong support; Volkmar & Knoop 2010; Shaw et al. 2010b [perhaps]; S. Li et al. 2013: 9 loci). 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). Recent work suggests relationships may be [Takakia [Sphagnum [[Andreaea + Andreaeobryum] + The Rest]]] (Chang & Graham 2009, esp. 2011: a [Takakia + Sphagnum] clade was recovered in maximum parsimony reconstructions).

Within the remaining mosses, Chang and Graham (2009, esp. 2011) and S. Li et al. (2013) found Oedopodium sister to other mosses. See Cox et al. (2010) for a phylogenetic study of mosses focusing on genera and families. Wahrmund et al. (2010) used a new mitochondrial locus to investigate relationships among mosses; the position of Timmia was particularly unclear.

See Shaw et al. (2010b; also Shaw et al. 2003a for morphology, 2010a) for relationships in the Sphagum et al. clade. The very distinctive Sphagnum leucobryoides (= Ambuchanania) was described only some twenty five years ago (Yamaguchi et al. 1990), and it and a very few other species of Sphagnum (placed in genera like Flatbergia) are outside Sphagnum s. str., the bulk of the clade.

For relationships in Dicranidae (haplolepidious mosses), see Stech et al. (2012). 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. Most branch lengths in the speciose Hypnales are short (Huttunen et al. 2012), however, Huttunen et al. (2013: focus on Plagiothecaceae) optimize the evolution of a number of features in both Hypnales and Hookeriales.

Classification. For a classification of mosses based on phylogeny, see Shaw and Goffinet (2000, also Goffinet & Buck 2004), and for an (over)classification of Sphagnum s.l., see Shaw et al. (2010b)

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

Age. Clarke et al. (2011: other estimates, but all old) suggested that this clade was (596-)524(-475) m.y.o., an age of around 440 m.y. was offered by Magallón et al. (2013), an age of (501.5-)454.4(-413.6) m.y. by Zhong et al. (2014b) and of around 460 m.y.a. by Villarreal and Renner (2012); see also P. Soltis et al. 2002).

Evolution. Divergence & Distribution. Qiu et al. (2006b, 2007 and references) note a number of features of hornworts, particularly of the sporophyte, that suggest similarities with polysporangiophytes, and they may be synapomorphies of the two. For the evolution of trilete spores, see Qiu et al. (2012).

ANTHOCEROPHYTA Stotler & Crandall-Stotler / HORNWORTS

Gametophyte thalloid, (leafy), apical cell wedge-shaped, with four cutting faces; branching truly dichotomous; rhizoids unicellular; mucilage cells +; antheridia in chambers [endogenous]; spermatozoids bilaterally symmetrical, with a right-handed coil; stellate pattern in basal body of cilia absent; chloroplasts with a pyrenoid (not); close association with the N-fixing Nostoc; flavonoids 0; axial microtubule system at mitosis; monoplastidy throughout life cycle; first division of zygote often vertical; sporophyte with apolar auxin ransport, lacking apical cell, basal meristem active for an extended period, foot bulbous, (stomata 0 if sporophytes more or less enclosed); sporangium dehiscing by 2 longitudinal slits; archesporial tissue from amphithecium; elaters +, spirally thickened, multicellular.

11/300. World-wide.

Age. The age of this clade is around 290 m.y. (Villarreal & Renner 2012).

LEIOSPOROCEROTOPSIDA Stotler & Crandall-Stotler

Thallus with mucilaginous clefts only in young uninfected plants, Nostoc in branching schizogenous strands in the centre of the thallus; antheridia up to 70/chamber; spore tetrads bilateral alterno-opposite, spores "minute", monolete, smooth.

1/1: Leiosporoceros dussii.

ANTHOCEROTOPSIDA Jancz.

Neochrome +; (pyrenoids +); thallus with mucilaginous clefts, Nostoc in spherical colonies; antheridia 1-6/chamber; spores ornamented; (sometimes more than one plastid/cell - Megaceros, but still monoplastidic cell division); phototropins lack introns; elevated rate of RNA editing.

10/300.

Age. The age of this clade is (399-)306, 248(-173) m.y. (Villarreal & Renner 2012).

Evolution. Divergence and Distribution. Most diversification within Anthocerotopsida has taken place within the last 100 m.y. or so (Villarreal & Renner 2012, q.v. for dates, etc.).

Goffinet and Buck (2013) provide general information easily placed in a phylogenetic context.

Ecology & Physiology. Neochromes, a chimaeric photoreceptor in which red-sensing phytochrome and blue-sensing phototropin are fused into a single molecule, have been found in all hornworts sampled (Leiosporoceros not studied: F.-W. Li et al. 2014). Pyrenoids vary considerably in morphology and have evolved five times or more between 101 and 18 m.y.a. (and also subsequently been lost); their evolution seems to be another example of a "tendency", since they are unknown from other land plants (Villarreal & Renner 2012).

For the association of hornworts with the nitrogen-fixing Nostoc, see Rai et al. (2000), and for what is known about Nostoc and nitrogen fixation, see Santi et al. (2013).

Bacterial/Fungal Associations. Endogone-like fungi (Mucoromycotina) are associated with some hornworts (Bidartondo et al. 2011), and are quite common there, as are Glomeromycota (Pressel et al. 2010). The two may form mycorrhizal associations with the same species, but whether either or both mycorrhizal association was ancestral in the group is unclear (Desirò et al. 2013); the latter association, at least, seems rather casual (Pressel et al. 2010).

In most taxa Nostoc enters the gametophyte through mucilaginous clefts; these are probably not homologous with stomata (Adams 2002; Adams & Duggan 2008).

Genes & Genomes. The extensive RNA editing in Anthoceros and its relatives is at codon positions that are otherwise universlly conserved in all land plants (Duff et al. 2007). 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). Anthoceros has lost the chloroplast rps15 gene (Martín & Sabater 2010) and the IR has expanded somewhat (Villarreal et al. 2013), while there has been extensive loss of protein-coding genes in the mitochoindrion, i.e. ca ½, versus less than ⅓ in other land plants (Y. Liu et al. 2014b).

Chemistry, Morphology, etc. 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.

See also Ligrone et al. (2000) for general information, Villarreal et al. (2010) for a summary of our understanding of hornworts, and Brown and Lemmon (2013) for sporogenesis; for antheridia, see Duff et al. (2004) and Cargill et al. (2005).

Phylogeny. Relationships within hornworts are still unclear in part. Leiosporoceros may be sister to all other hornworts, although the extensive RNA editing in other members of the clade obscures this position in some analyses (e.g. Duff et al. 2007); it has many distinctive features (see above). See also Stech et al. (2003), Duff et al. (2004) and Villarreal and Renner (2012) for relationships. Leiosporoceros has an intron in the mitochondrial nad5 geno, as do Anthoceros and immediate relatives (Villarreal et al. 2013). 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). Villarreal and Renner (2014) discussed relationships around Nothoceros.

Classification. Several classifications or this clade have appeared recently (Frey & Stech 2005; Stotler & Crandall-Stotler 2005; Duff et al. 2007); they tend to be rather elaborate. For the limits of Nothoceros, see Villarreal and Renner (2014).

POLYSPORANGIOPHYTA†

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

Evolution. Divergence & Distribution. The exact relationship between the sporophyte of polysporangiophytes and that of "bryophytes" is unclear (Shaw et al. 2011), and the stalk of a moss capsule may not be homologous to the branching sporophyte axis of the polysporangiophytes (Kato & Akiyama 2005; Qiu et al. 2012). Sterlization of the sporangial axis or simple elaboration of a "bryophyte" sporangium leading to the evolution of a branched sporophyte are ideas that have been suggested, but perhaps prolongation of embryonic growth is more likely (Tomescu et al. 2014). Certainly some early sporophytes were very small and possibly dependent on the gametophyte (Rothwell 1995; Boyce 2008b). Some early polysporangiophyte gametophytes were quite elaborate structures, although different in morphology from the sporophytes, and they had stomata (Taylor et al. 2005; Gerrienne & Gonez 2011; Ligrone et al. 2012a). A later stage in the evolution of vascular plants may involve an ancestor in which the generations were pretty much ismorphic. Indeed, this largely isomorphic alternation of generations represented by some of the plants from the Lower Devonian Rhynie Chert of some 410 m.y.a. figures largely in attempts to understand the evolution of land plant life cycles (Niklas & Kutschera 2009, 2010), however, the Silurian cooksonioids in particular which have sporophytes that are very narrow in diameter (1 mm or substantially less) and probably dependent physiologically on the gametophyte (Boyce 2008b). The sequence may be gametophyte only free living, sporophyte unbranched, dependent on the gametophyte → gametophyte only free living, sporophyte branched, dependent on the gametophyte → generations ± isomorphic → sporophyte dominant, gametophyte free-living → sporophyte dominant, gametophyte dependent on sporophyte (see also Tomescu et al. 2014). For a comprehensive study of the early evolution of land plants, see Kenrick and Crane (1997), and for apomorphies at all levels, incorporating fossil members of the whole clade, see Doyle (2013).

For the evolution of roots, see below.

Bacterial/Fungal Associations. A variety of fungal associations have been found in fossils of early polysporangiophytes, whether in gametophyte or sporophyte, and sometimes the fungi pervade the whole plant, furthermore, because true roots had not yet evolved, they are best called paramycorrhizal associations (Kenrick & Strullu-Derrien 2014).

EXTANT TRACHEOPHYTA / VASCULAR PLANTS

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

Age. Clarke et al. (2011) suggested an age for the clade of (456-)446(-425) m.y., and there are somewhat younger ages in Magallón et al. (2013), around (434.3-)424-421.6(-416.2) m.y., and Zhong et al. (2014b), (492.9-)428.8(-400.1) m.y., largely in line with fossil-based estimates (Kenrick et al. 2012) which were used in the calibrations (a similar age in Villarreal & Renner 2014). However, P. Soltis et al. (2002: variety of estimates) suggested an older crown age for extant tracheophyes of (813-)603(-393) m.y. ago.

Evolution. Divergence & Distribution. Hilate/trilete spores that separate appear in the Early Silurian may mark the origin of vascular plants (Kenrick et al. 2012). The composition of the sporopollenin in lycophyte fossils ca 310 m.y. old in cave deposits is very similar to that of spores of extant taxa (Fraser et al. 2012).

Pryer et al. (2004b) provide a useful summary of the evolution of vascular plants, while Floyd and Bowman (2006), Boyce (2008a), and Boyce and Leslie (2012) emphasize the diversity of leaf morphologies, growth forms, etc., to be found in non-angiospermous plants in general; leaf development in extant lycophytes is very different from that in other vascular plants. 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.

Tracheophytes all have some kind of roots, although these have almost certainly evolved more than once (e.g. Raven & Edwards 2001); see also Tomescu rt al. (2014) for the evolution of roots in vascular plants. There is discussion above about the evolution of root hairs.

Ecology & Physiology. Kenrick et al. (2012) discussed the effect of vascular plants on the carbon cycle. There are broad correlations between atmospheric CO2 concentration and stomatal size that have important implications for plant productivity, transpiration, and rock weathering. When the CO2 concentration of the atmosphere is low, leaves tend to have higher densities of smaller stomata, allowing more CO2 to diffuse into the leaf, when concentrations increase, relationships are the reverse (e.g. Franks & Beerling 2009). It has also been suggested that CO2 concentration, guard cell size, and genome size can be linked, the first and last being broadly correlated over the last 400 m.y. (Haworth et al. 2011), although genome size reconstructions (Fig. 4) and some other aspects of this story (see also Franks et al. 2012) are difficult to understand. For water use efficiency throughout the Phanerozoic, see Franks and Berrling (2009a) and Assouline and Or (2013: a different interpretation for higher CO2 concentrations)

The response of photosynthesis to red light and passive stomatal control of leaf hydration are perhaps best tagged to this node (see above: McAdam & Brodribb 2011). Thus the mechanism of stomatal closure in ferns is like that of lycophytes rather than seed plants (McAdam & Brodribb 2011, 2012, 2013; see also Haworth et al. 2011, 2013); it is passive, and abscisic acid is not immediately involved. Watkins and Cardelús (2012) noted that in some respects epiphytic ferns, at least, are ecologically more like angiosperms than terrestrial ferns, using water quite efficiently (and having very low hydraulic conductivity). However, one of the ways in which ferns and lycophytes, whether gametophyte or sporophyte, can grow in drier conditions is by being dessication tolerant, even if the mechanism of stomatal control is overall similar to that in ferns growing in more mesic conditions (McAdam & Brodribb 2013).

Genes & Genomes. Three new families of transcription-associated proteins may have evolved somewhere in this general area (Lang et al. 2010: hornworts not included; see also Zhu et al. 2012, Lang et al. not cited). For genome sizes in monilophytes and lycophytes, see Nakazato et al. (2008).

Chloroplast genomes seem particularly labile in taxa ouside the angiosperms (Guisinger et al. 2011 for references). For evolution of the chloroplast genome in other than seed plants, see Wolf and Karol (2012). On the other hand, the order of genes in the mitchondrion is relatively invariable in the "bryophytes", much more variable in vascular plants (Y. Liu et al. 2014a).

Chemistry, Morphology, etc. Condensed tannins are polymerized in a chloroplast thylakoid-derived tannosome (Brillouet et al. 2013). In extant vascular plants, lignins are rich in guaiacyl units (Harris 2005), and 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; c.f. Gómez-Ros et al. 2007; Zu et al. 2009).

Stems have an apical meristem, whether of a single cell or group of cells (e.g. Kato & Akiyama 2005); 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 plasmodesmatal connections between the cells (many - meristem a single cell, few - meristem a group of cells: see Imaichi & Hiratsuka 2007). However, although it is commonplace to make this distinction between tracheophytes that have meristems of a single cell or of several cells (Imaichi 2008), this may be incorrect; Korn (2013) suggested that all seed plants have stem meristems with but a single cell. For apical cells in "bryophytes", see Tomescu et al. (2014).

Early land plants have a variety of tracheid morphologies (e.g. Strullu-Derrien et al. 2013 for literature). 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 a 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). However, 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. The developmental control of conducting tissue in moss gametophytes and vascular plant sporophytes suggests that at one level they may not be that much different (see also above). For a general comparison of tracheary cells, see Bailey and Tupper (1918).

Secondary thickening has evolved more than once and the pattern of secondary growth differs quite widely. The vascular cambium is usually unifacial, producing xylem internally only, and there are usually no anticlinal divisions of the cambial cells; Sphenophyllales alone outside the seed plant lineage may have developed bifacial vascular cambium (e.g. Rothwell et al. 2008b; Spicer & Groover 2010; Hoffman & Tomescu 2011; Strullu-Derrien et al. 2013).

Kaplan (1997; vol. 3, 2001) provides an extensive discussion and analysis of the basic morphology of lycophytes and monilophytes in particular. Sporangia are borne adaxially on the sporophylls (Schneider et al. 2002).

Phylogeny. The relationships [lycophytes [monilophytes + lignophytes]] are commonly found (although not in some analyses of chloroplast genomes in Ruhfel et al. 2014).

Classification/Previous Relationships. Lycophytes and monilophytes or ferns have traditionally been included in the pteridophytes.

LYCOPHYTA

Roots from angles of branches [?modified stems], branching dichotomous; root hairs +, modified leaves, (0); xylem lobed [actinostele], exarch [development centripetal], (secondary thickening +, unifacial [xylem alone cut off internally]); leaves small, with a single vein, phloem surrounding xylem; sporangia 1/leaf, adaxial, often heart-shaped, dorsiventrally flattened, dehiscence transverse along line of conspicuously thickened cells; mitosis and meiosis monoplastidic; embryo endoscopic, plane of first cell division variable, with quadrant/octant formation, zygote elongation occuring, embryonic axis reorients during development; (loss of three group II mitochondrial introns). - 3 families, 5 genera, ca 1300 species.

Age. Magallón et al. (2013) estimated an age of around 383.7 m.y., Zhong et al. (2014b) an age of (403-)386.3(-377.4) m.y., and Villarreal and Renner (2014) an age of only around 270 m.y. for crown-group lycophytes; see also P. Soltis et al. (2002).

Evolution. Divergence & Distribution. For the early evolution of lycophytes, see Gensel and Berry (2001) and Ambrose (2013 and references).

Bacterial/Fungal Associations. A variety of fungi, including Glomales, have been found in the echlorophyllous gametophytes that are common in Lycophyta. One, a member of Sebacinales group A from Diphasiastrum alpinum that was also found on Calluna vulgaris growing in the same habitat, allowed the movement of nutrients from the vascular plant to the echlorophyllous gametophyte (Horn et al. 2013).

Genes & Genomes. At least some lycophytes (Selaginella, but not Huperzia) have a highly reorganized chloroplast genome (Tsuji et al. 2007).

Chemistry, Morphology, etc. Roots in this group appear to be modified branches and the root hairs are modified leaves (Pigg 1992; Rothwell & Erwin 1985; Rothwell 1995; c.f. in part Tomescu et al. 2014); thus in Isoetes the "roots" are exogeneous (Rothwell & Erwin 1985). (L. and S. - adventitious roots??) The leaves of lycophytes have been called microphylls or lycophylls, and are characterized by having an intercalary meristem and being supplied by a single vein that does not leave a gap in the central stele when it departs (see Kaplan 1997, vol. 2: chap. 16, vol. 3: chap. 19, 2001 for leaf morphology). Lycopsida represent the extant members of this clade, and have vascularized leaves, stellate xylem in the stem, a close association of sporangia and leaves (hence sporophylls), etc. (Kenrick & Crane 1997). The mitochondrial organizing center is on the nuclear envelope (NE-MTOC) and meiosis is poyplastidic and anastral (Brown & Lemmon 2008 [check level]).

For general information, see also Boyce (2005a) and Ranker and Haufler (2008), for sporophytes and their placentae, see Renzaglia and Whittier (2013), for spore wall ultrastructure, especially of fossil members, see Gensel et al. (2013).

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

LYCOPODIACEAE Mirbel   Back to Lycophyta

Terrestrial or epiphytic; stem with group of apical cells; strobili +/0; (gametophyte myco-heterotrophic); n = 34 [quite often; lots of other numbers].

3-4/400+: Huperzia (300), Lycopodiella (60). ± World-wide, esp. South America

Evolution. Divergence & Distribution. Wikström and Kenrick (1997, 2001) 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 or more m.y.a. when there are fossils with the distinctive plectostele that characterises Lycopodium s. str., most of the group - which includes many epiphytes in Huperzia - are younger that 80 m.y. at most. At a still finer level, there are about 60 species of Huperzia in the Andean páramo, probably derived from epiphytic species within the last 15 m.y. (Wikström et al. 1999; Sklenár et al. 2011).

Ecology & Physiology. About two thirds of the species of Huperzia are epiphytic (Wikström et al. 1999; Zotz 2013).

Chemistry, Morphology, etc. For general information, see Ølgaard (1990).

Phylogeny. The bulbiferous Huperzia selago group is sister to the rest of the genus, which is mostly epiphytic; there are New and Old World clades (Wikström et al. 1999).

[Isoetaceae + Selaginellaceae]: leaves with adaxial ligule; plant heterosporous, megaspore wall with much silica; megagametophyte endosporous, transfer cells 0.

ISOETACEAE Dumortier   Back to Lycophyta

Terrestrial or aquatic; roots from beneath the corm/rhizome, with a central air space, vascular bundle single, excentric, xylem abaxial to phloem; stem often cormose and unbranched; ?apical cell; xylem mesarch; ?cambium; most leaves fertile, leaves with several vascular strands; sporangia trabeculate; 50-300 megaspores/sporangium; microsporogenesis successive, tetrads decussate, microspores monolete; male gametes multiflagellate [10-20 flagellae]; n = (10) 11.

1/80. More or less world-wide.

Evolution. Divergence & Distribution. For fossils that have been linked with Isoetes and the evolution of the whole group, see Grauvogel-Stamm and Lugardon (2001) and Pigg (1992, 2001).

Ecology & Physiology. Some species of Isoetes take up CO2 from the mud in which it grows via its very well developed roots, Stylites and submerged individuals of Isoetes even lacking stomata (Bristow 1975; Keeley 1998; Raven et al. 1998 and references). Photosynthesis is by the CAM pathway, which may well have a substantially more ancient origin here than in flowering plants (Edwards & Ogburn 2012).

Chemistry, Morphology, etc. Isoetes, at least, has thickened, nacreous, placental cell walls. The growth and anatomy of Isoetes is poorly understood (e.g. Gifford & Foster 1988), and it is unclear whether or not it has secondary thickening (Kaplan 1997, vol. 3: chap. 19).

For general information, see also Jermy (1990).

SELAGINELLACEAE Willkommen   Back to Lycophyta

Usu. terrestrial; syringyl lignin +; growth bipolar; stele in central cavity surrounded by trabeculate endodermal cells; (vessels +); stem with single apical cell; leaves (4-ranked), often anisophyllous; strobili +, usu. terminal, often 4-ranked; sporangia ± spherical, 4 megaspores/sporangium, microspores echinate; n = (7-)9(10, 12), genome size [1C] 0.16-0.24 pg.

1/800. World-wide.

Evolution. Ecology & Physiology. Selaginella grows in habitats varying from very humid and in considerable shade to open and xeric; plants in the latter habitats reconstitute quite nicely when water is added.

Chemistry, Morphology, etc. For the synthesis of syringyl lignin in Selaginella, see J.-K. Weng et al. (2010); details of the synthetic pathway are quite different to those in angiosperms.

[MONILOPHYTA + LIGNOPHYTA] ("Euphyllophyta" may well be a misnomer...)

Branching ± indeterminate; lateral roots +, endogenous, root apex multicellular, root cap +; tracheids with scalariform-bordered pits; leaves with apical/marginal growth, venation development basipetal, growth determinate; sporangia borne in pairs and grouped in terminal trusses, dehiscence longitudinal, a single slit; cells polyplastidic, microtubule organizing centres not associated with plastids, diffuse, perinuclear; male gametes multiflagellate, basal bodies staggered, blepharoplasts paired; chloroplast long single copy ca 30kb inversion [from psbM to ycf2]; LITTLE ZIPPER proteins [see below].

Age. The divergence of the monilophytes and lignophytes may date to 401-380 m.y.a. (Leebens-Mack et al. 2005); Theißen et al. (2001) suggested an age of ca 400 m.y., Clarke et al. (2011: other estimates) an age of (452-)434(-410) m.y. and Magallón et al. (2013) estimated an age of around (422-)411-404(-394) m.y.; (463.5-)428.9(-400.1) m.y. is the age in Zhong et al. (2014b). See also Pryer et al. (1995, 2000, 2001a, 2004), P. Soltis et al. (2002: a variety of ages, some very old), Schneider et al. (2002) and Stein et al. (2012).

Evolution. Divergence & Distribution. For possible apomorphies of crown members of this clade, see Raubeson and Jansen (1992b), Kenrick and Crane (1997), and Schneider et al. (2009).

The clade [monilophytes + lignophytes] is sometimes called the euphyllophytes. However, details of the evolution of the euphylls or megaphylls that are supposed to characterise this clade are unclear, although the developemnt of megaphylls (probably modified lateral branches) is quite different from that of microphyllls (probably tissue outgrowths: Floyd & Bowman 2006). Schneider et al. (2009: p. 461 and references) suggest that mega/euphylls did arise once, and can be characterized by apical/marginal growth, apical origin of the venation, determinate growth, etc., while Floyd and Bowman (2007) thought that megaphylls have evolved independently in the seed plant and monilophyte lineages, an estimated 3-6 times in the latter alone, and perhaps elsewhere as well (see also Kenrick & Crane 1997; Boyce & Knoll 2002; Gensel & Kenrick 2007; Tomescu 2009; Sanders et al. 2009; Galtier 2010; Corvez et al. 2012: at least two origins). Zimmermann's (1930, see 1952) telome theory that euphylls are the result of overtopping, planation and webbing of a stem/branch system, has been influential, although in detail this is not tenable (e.g. Beerling & Fleming 2007).

Indeed, there seems to be no satisfactory definition for euphylls (but see Corvez et al. 2012). In general euphylls are determinate organs, perhaps planated branch systems, with ad/abaxial identities; their vascular supply leaves a "gap" in the central stele when it departs (see e.g. Sporne 1965, but c.f. Kaplan 1997, vol. 3: chap. 19, 2001 in particular, see also Harrison et al. 2005; Boyce 2005a: summary of earlier literature, 2008; Tomescu 2008, 2009; Sanders et al. 2007, 2009; Corvez et al. 2012). However, the leaf supply in monilophytes seems to have evolved by dissection of an amphiphloic siphonostele (the vascular construction of the rhizome in some true ferns is also made up of sympodia - Karafit et al. 2005), 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 leaves with large blades 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). The growth of fern leaves is accompanied by proliferation at the apex of the blade and that of angiosperms by proliferation at the base (Nardmann & Werr 2013), while Boyce (2005b, 2008a) noted the prevalence of marginal leaf growth in non-angiospermous leaf blades and of diffuse growth in angiosperm leaf blades - these may be oversimplifications, but they suggest major differences between the two.

However, Floyd et al. (2014) are chipping away at understand the developmental background of euphylls or megaphylls of whatever they are called. They place the origin of the pst-translational negative regulators LITTLE ZIPPER proteins at this node; they are part of the C3HDZ stable of genes. The genes may be connected with the sporophyte apical meristem, etc. in land plants, and LITTLE ZIPPER is connected with shoot and leaf development in seed plants, at least (Floyd et al. 2014).

Osborne et al. (2004) provide an ecological explanation for the origin of mega/euphylls based on falling CO2 levels. However, the developmental mechanisms involved in megaphyll formation may have evolved long before euphylls appeared (Beerling 2005a, b and references).

Chemistry, Morphology, etc. For roots and their evolution, see Kenrick and Strullu-Derrien (2014), and for lamina morphology and venation development, see Boyce (2005b).

Phylogeny. Ferns and their relatives, the monilophytes or Moniliformopses, and lignophytes, the extant members of which are seed plants or spermatophytes, are both well supported clades.

MONILOPHYTA / FERNS s.l.

Roots originate from the pericycle, lateral roots from the endodermis, root apical meristem of a single cell; shoot apex with cell lineage-specific plasmodesmatal network; stem with peripheral band of fibres [stereome - hypodermal and outer-cortical]; amphiphloic siphonostele +, discontinuities in stele in t.s. caused by frond gaps; protoxylem restricted to lobes of central xylem strand [xylem development mesarch], tracheids with scalariform pits; phloem fibres rare; stem endodermis and pericycle +; leaves megaphyllous [ad/abaxial symmetry evolved first, then determinancy], development acropetal; petiole with multiple leaf traces coming from a U-shaped bundle; frond veins not anastomosing; sporangia grouped in sori, sporangium stalk 6< cells across, walls two cells thick, dehiscence by an exothecium, tapetum amoeboid, spores/sporangium 1000<, white, globose-tetrahedral, wall development centrifugal, exospore 3-layered, pseudoendospore +; antheridium wall ³5 cells thick, spermatozoids with 30-150 cilia, with numerous plastids and mitochondria; chloroplast nine-nucleotide insertion in the rps4 gene, LSC inversion from trnG-GCC to trnT-GGU; loss of one group II mitochondrial intron.

Age. Magallón et al. (2013) estimated an age of around (404-)394.3-389.9(-382) m.y. for this clade, ca 360 and ca 364 m.y. are the ages in Schuettpelz and Pryer (2007) and Y-L. Qiu et al. (2007) respectively, (390.7-)368.5(-354) m.y. in Zhong et al. (2014b) and around 330 m.y. in Villarreal and Renner (2014); see also P. Soltis et al. (2002) for suggestions.

Evolution. Divergence & Distribution. Schuettpelz and Pryer (2009, esp. Tables 2, 3 in the Supplement) provide extensive dating of divergence times in monilophytes, and for more ages of the major monilophyte clades, see Y.-L. Qiu et al. (2007) and Schneider et al. (2004a). Schuettpelz and Pryer (2009) also list a number of fossil records; for the fossil record, see also Rothwell and 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, and again in the Jurassic and the Cretaceous (Rothwell & Stockey 2008). General fern diversity decreased (along with that of the cycads) through the Cretaceous (Wing & Boucher 1998). However, 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 taken place after the diversification of the angiosperms (Lovis 1977; Rothwell & Stockey 2008; Schuettpelz & Pryer 2009; Schneider et al. 2004a). Ferns appear to have temporarily dominated at least locally after the end-Cretaceous bolide impact (Schneider et al. 2004a).

Leptosporangiate ferns make up at least 80% of fern species, and about one third of these are epiphytes. Diversification of epiphytic ferns in particular occurred during the Palaeogene, perhaps linked with the Palaeocene-Eocene thermal maximum some 10 m.y. after the bolide impact at the K/T boundary (Schneider et al. 2004a, b; Schuettpelz 2007; esp. Schuettpelz & Pryer 2009: Supplemental Tables 2, 3; Watkins et al. 2010; c.f. Dubuisson et al. 2009, in part). An exception is Trichomanes and relatives (but not Hymenophyllum and its relatives, for which, see Dubuisson et al. 2009), a group diversifying in the early Cretaceous; the former are commonly epiphytic on tree ferns, which themselves had begun diversifying in the Jurassic (Schuettpelz 2007; also Schuettpelz & Pryer 2009; Rothwell & Stockey 2008 for early radiations of leptosporangiate ferns).

On the other hand, the eusporangiate Marattia and Angiopteris, and also the leptosporangiate tree ferns, are almost living fossils, showing little molecular and even morphological evolution (P. Soltis et al. 2002).

A provisional hierarchy of characters obtained from Smith et al. (2006, 2008), Pryer et al. (1996), and Rothfels et al. (2012b) is given below. For a first stab at apomorphies for members of the polypod II clade, see Sundue and Rothfels (2013); their suggestions are largely followed here; problems with sampling, character state delimitation, and different apomorphies produced by different character reconstructions taken into account as far as possible. Only unambiguous synapomorphies (Sundue & Rothfels 2013) are flagged below. Kaplan (1997, vol. 3: chap. 19) summarized the sporangium wall morphology of monilophyta; the annulus is an apomorphy of Polypodiopsida, leptosporangiate ferns. For other possible apomorphies, see e.g. Schneider et al. (2009), however, more features may need to be added, for instance, if the megaphyllous leaf of most ferns and that of extant seed plants have evolved independently, which seems likely (see above).

Understanding the evolution of the apparently very unfern-like plant body of Psilotales and of Psilotum itself, until fairly recently considered to be perhaps the most primitive extant vascular plant - when I was taught about Psilotum, it was compared with the Palaeozoic rhyniophytes - still presents difficulties. Kaplan (1997, vol. 3: chap. 10; Siegert 1973 and references) summarized the literature, noting that these problems were because the morphology of Psilotum in particular was compared with these fossil plants, now thought to be entirely unrelated. As he noted, young leaves of Psilotum did have features of fronds (see also Kaplan 1977).

Similarly, the leaves of Equisetum may be secondarily simple. Thus its fossil relative Sphenophyllum has much larger leaves with dichotomous venation; bifacial xylem has been found in this genus (Kenrick & Crane 1997; Doyle 2013 and references).

Ecology & Physiology. 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; water transport is thus relatively efficient despite the absence of any secondary thickening and bordered pits, as in conifers (Pittermann et al. 2011).

Kawai et al. (2003) found a distinctive chimaeric red/far red light photoreceptor (phy 3, = neochrome) in which red-sensing phytochrome and blue-sensing phototropin are fused into a single molecule (F.-W. Li et al. 2014) in some polypod ferns, possibly aiding in phototropic responses in the shaded conditions in which ferns have diversified in the Tertiary; neochrome is very sensitive to white light (Wada 2008). Recent work suggests that neochrome was acquired by Polypodiales from hornworts via horizontal transport around 179 m.y.a., which, perhaps not so coincidentally, is about the age of Polypodiales (Schneider et al. 2004a), and may even have been acquired more than once (F.-W. Li et al. 2014).

In seed plants, stomata open in response to both red and blue light. Stomata of those few ferns examined, all leptosporangiates (Pteris, Adiantum, Asplenium and Nephrolepis), lack a blue light-specific opening response, although elements of the response, including the relevant phototropin, a blue right receptor protein kinase, are present (Doi et al. 2006). In the shaded environments that many ferns prefer, blue (and red) light has been preferentially absorbed by the canopy above; stomatal closure is mediated by red light. (In seed plants the effectiveness of the response is white/blue + red > blue > red > green light - Willmer & Fricker 1996.)

Ca 3,000 species of leptosporangiate ferns, about one third of the group and concentrated in Hymenophyllaceae, Polypodiaceae, Pteridaceae (e.g. Vittaria) and Dryopteridaceae (e.g. Elaphoglossum) (Schuettpelz & Pryer 2009; Kato & Tsutsumi 2013), are epiphytes. These represent some 10% of all vascular epiphytes. The gametophytes of epiphytes in particular are often strap-shaped and long-lived, and are notably resistant to dessication; as Watkins et al. (2007: p. 716) observed, "fern gametophytes are, for all intents and purposes, bryophytes" (see also Nayar & Kaur 1971: survey of gametophyte diversity; Dassler & Farrar 2001; Farrar et al. 2008; Watkins & Cardelús 2012; Rothfels & Schuettpelz 2014). Ferns show a variety of other adaptations to the epiphytic habitat, including CAM photosynthesis (Watkins & Cardelús 2012) and production of gemmae (Farrar 1974), and mycorrhizae are less frequent (e.g. Wang & Qiu 2006; Kato & Tsutsumi 2013). Testo and Sundue (2014) found that both terrestrial species and hemiepiphytes (where roots from the climbing plant establish a connection with the soil) were derived within a clade of epiphytic Polypodiaceae.

Fertilization & Spore Dispersal. The distributions of the sporophytic and gametophytic plants of the one fern species may be quite different, particularly if the gametophyte is other than heart-shaped. Strap-shaped or filamentous gametophytes can live for a very long time and/or produce gemmae, and so they can persist in sites that are hundreds of miles from the nearest sporophytes (e.g. Farrar 1967; Ebihara et al. 2013). With the advent of the ability to identify gametophytes directly by molecular sequencing, rather than waiting for them to produce sporophytes, this phenomenon is turning out to be remarkably common (Ebihara et al. 2013), and it has interesting implications for the evolution of ferns (see e.g. Ebihara et al. 2009).

For the mechanics of how the annulus functions in sporangium dehiscence, see Noblin et al. (2012).

Bacterial/Fungal Associations. For mycorrhizae in ferns, see Lehnert et al. (2010 and references). Mycorrhizal associations are not known in Equisetum (Read et al. 2000).

Genes & Genomes. For the evolution of the monilophyte chloroplast genome, see Karol et al. (2010) and Grewe et al. (2013). Within Polypodiopsida, some inversions in the chloroplast inverted repeat may be high-level synapomorphies (Gao et al. 2009). Grammitidaceae s. str. in particular (included in Polypodiaceae) have green spores and accelerated plastid genome evolution, a correlation found elsewhere in ferns, although it is not 100% (Schneider et al. 2004b), indeed, spores that less obviously contain chloroplasts are more widespread (Sundue et al. 2011). There has been an abrupt reduction in the rate of molecular evolution in the largely arborescent Cyatheales (Korall et al. 2010: Marattiopsida, Osmundales, etc., not included).

Ferns are noted for their high incidence of polyploidy, almost 1/3 (31%) of all speciation events being accompanied by polyploidy (Wood et al. 2009), and base chromosome numbers are also usually very high. For information on genome size, see Obermayer et al. (2002); large genomes may be an apomorphy for [Psilotales + Ophioglossales].

Chemistry, Morphology, etc. There is substantial variation in xyloglucan composition of the primary cell walls, that of Equisetum being particularly distinctive (Hsieh & Harris 2012). For cell wall polysaccharides, see also Silva et al. (2011),

Basic plant morphology was outlined by Kaplan (1997, vol. 2: chap. 11, 18, vol. 3: chap. 19, 2001). 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). Hernández-Hernández et al. (2012) discuss the distribution of the circumendodermal band, tannin-containing cells surrounding the petiolar leaf trace that have a common orgin with the endodermis; they also detail the distributions of a number of other vegetative/habit features. Vasco et al. (2013) summarize fern leaf morphology and development, noting a number of shoot-like features.

For details of spermatozoid morphology and movement, etc., see e.g. Renzaglia et al. (2000b, 2002) and Schneider et al. (2002). The 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 information on pteridophytes in general (these have often - and still may - include lycophytes), see also Kato (2005) and Ranker and Haufler (2008). For other general information, see Raven and Edwards (2001), for comparative anatomy, see Ogura (1972), for venation, see Wagner (1979) and Boyce (2005b), for details of stelar morphology and evolution, see Beck et al. (1982), and for young sporophytes, etc., see Johnson and Renzaglia (2009 and references).

Phylogeny. The circumscription of this clade has only recently become clear. It includes the strongly supported [Psilotum + Ophioglossum] clade (Tmesipteris is close to Psilotum) that is perhaps sister to all other ferns. The position of Equisetum reamins uncertain. It may be sister to Angiopteris, etc. (although support currently only moderate), the combined clade in turn being sister to remaining ferns (e.g. Pryer et el. 2001a, 2004a; Wikström & Pryer 2005; Qiu et al. 2007; Ebihara et al. 2011; c.f. in part Wolf et al. 1998). Alternatively, it may be sister to all other ferns, as in a rps4 analysis, and also 4- and 5-gene analyses, the latter two with strong support (Schuettpelz et al. 2006) and also in a matK phylogeny (Kuo et al. 2011). However, Schneider et al. (2009) noted potential morphological apomorphies such as simple leaf blade and stems with both radial and dorsiventral symmetries (= erect plus creeping stems...) suggesting a clade [Psilotales + Equisetales]. Interestingly, spore wall ultrastructure of Calamites, an extinct equisetaceous plant, is not so different from that of Ophioglossaceae and other ferns (Lugardon & Brousmiche-Delcambre 1994; Grauvogel-Stamm & Lugardon 2009). Equisetum has no mitochondrial atp1 intron, either a secondary (and parallel) loss or plesiomorphic absence, depending on the topology of the whole group (Wikström and Pryer 2005: see the character hierarchy below). Wickett et al. (2014) obtained a [Marattiales + Ophioglossales] clade sister to leptosporangiate ferns, but this may be a sampling issue. The inclusion of morphology alone or in combination with molecular data also affects relationships detected (Wikström & Pryer 2005 and references); see also Grand et al. (2013) for various morphological analyses. Structural changes in the chloroplast genome also suggested a [Psilotales + Equisetales] clade (Grewe et al. 2013), and these relationships are provisionally followed below (see some analyses in Karol et al. 2010; also Wolf & Karol 2012; Ruhfel et al. 2014).

This reorganisation of monilophytes has sometimes been severely criticised (Rothwell & Nixon 2006), but 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 by those authors makes their work difficult (for me, at least) to interpret. Indeed, in several morphological cladistic analyses (e.g. Bremer 1985; Stevenson & Loconte 1996; Rothwell 1999: fossils included or not) Psilotum came out as sister to all other vascular plants. However, some morphological analyses do include Psilotum with other monilophytes, even if the same analyses also place flowering plants within a paraphyletic group of extant gymnosperms (Schneider et al. 2009).

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, adjustments to this classification are being made as details of the phylogeny become better understood (Schuettpelz & Pryer 2007, 2008; Kuo et al. 2011; Rothfels et al. 2012b: reclassification of eupolypods II). Developments in classification proceed apace: The linear sequence of families and genera (Christenhusz et al. 2011a) is now dated, and for a recent classification of ferns, see Christenhusz and Chase (2014) - to be digested.

Previous Relationships. Psilotum and Equisetum were previously thought to represent independent lineages, with Psilotum and relatives considered to be the most primitive living vascular plants, and the latter do look superficially similar to some of these early fossils. Their association with ferns, now very largely accepted, was unexpected (but see Kenrick & Crane 1997). Although Bierhorst (1968, see also 1977) compared Psilotum with the extant fern Stromatopteris and found some morphological similarities, most of these have turned out to be parallelisms.


EQUISETOPSIDA / [Equisetales [Psilotales + Ophioglossales]]: plant with erect and creeping stems; embryo exoscopic, suspensor 0; chloroplast rps16 gene and rps12i346 intron lost.

Age. The clade that contains Equisetum has probably been separate from other monilophytes since the Permian, ca 250+ m.y.a. (Stanich et al. 2009); Zhong et al. (2014b) thought that this clade was (370.3-)296.2(-189.9) m.y. old.

EQUISETALES Berchtold & Presl
EQUISETACEAE

Roots ?arch; cell wall also with (1->3),(1->4)-ß-D-glucans [Mixed-Linkage Glucans], plants with Si02; stem xylem endarch [development centrifugal], stem ridged, with central canal; protoxylem lacunae developing; amphicribral leaf vascular bundles; branches whorled; stomata paracytic; leaves small, simple, 1-veined, whorled, basally connate; sporangiophores peltate, aggregated into a strobilus; sporangial cell walls with helical secondary thickenings; spores with circular aperture, abapertural obturator +, spore green, elaters 4-6, spatulate, helically-coiled; plane of first cell division of embryo variable; x = 108; mitochondrial atp1 intron 0.

1/15. ±World-wide, not the Antipodes.

Age. Extant species of Equisetum seem to have separated in the Tertiary (Des Marais et al. 2003, but c.f. Stanich et al. 2009). Fossils with some of the apomorphies of crown group Equisetum are known from Lower Cretaceous deposits some 136 m.y. or more old (Stanich et al. 2009); for still older Equisetum-like spores - but with trilete marks - and associated elaters from the Middle Triassic, see Schwendemann et al. (2010).

Evolution. Divergence & Distribution. Change in spore morphology from the Calamites type to the at first sight very different trilete spores of Equisetum is convincingly demonstrated by Grauvogel-Stamm and Lugardon (2009). Other fossils placed in this area include Sphenophyllum; they have much larger leaves, suggesting that those of Equisetum may be reduced.

Reproductive Biology. Aided by their elaters, spores of Equisetum can either jump up to 1 cm in the air as they dry, or move by short random walk-type movements along the ground (Marmottant et al. 2013).

Chemistry, Morphology, etc. For (1->3,1->4)-ß-d-glucans, see Fry et al. (2008) and Xue and Fry (2012); or aerophores, see Davies (1991), and for general ecology and Si concentration, see Husby (2012).

[Psilotales + Ophioglossales]: Root hairs 0; leaf vascular bundles collateral; gametophyte subterranean, axial, non-photosynthetic, mycorrhizal; genome size [1C] 32.7-64.8 pg.

Age. Magallón et al. (2013) estimated an age of around 275.6 m.y. for this clade, and (316-)306(-267) m.y. is the age in Y. L. Qiu et al. (2007); see also P. Soltis et al. 2002) for estimates.

Genes & Genomes. Both Psilotum and Ophioglossum have very large genomes with 1C values at least 35 pg (Bennett & Leitch 2005), very unusual for land plants.

PSILOTALES Prantl
PSILOTACEAE

Roots 0; leaves small, simple, veins 1 or 0, (laterally flattened - Tmesipteris); sporangia 2-3, forming synangium; spores kidney-shaped, monolete; gametophyte with septate rhizoids; (transfer cells in sporophyte only - Psilotum), n = 52.

2/12.

Age. Zhng et al. (2014b) estimated an age of (147.1-)72.3(-14.7) m.y. for this clade.

OPHIOGLOSSSALES Link
OPHIOGLOSSACEAE

Root with 2-5 protoxylem poles; cork mid cortical; vascular cambium +; stem stele sympodial in construction; tracheids with circular bordered pits; (axillary buds +); fronds compound to simple, venation reticulate, with internally directed veins, bases sheathing; vernation nodding; one or more sporophores associated with each tropophore; (embryo endoscopic; first cell wall of the zygote vertical); n = (44) 45 (46) ... 130. 4/80.

See Hauk et al. (2003) for a phylogeny, Mankyua not included, also Shinohara et al. (2013), Mankyua included, but position unstable - sister to rest of family (also in the joint analysis), or to Ophioglossum s. str.. Takahashi and Kato (1988) describe the development of lateral meristems in the family.

[Marattiopsida + Polypodiopsida]: amphicribral leaf vascular bundles; aerophores +; frond compound, vernation circinate; scales +; sporangia abaxial on sporophyll; gametophyte green, surficial; changed gene adjacencies at borders of clhoroplast IR; mitochondrial atp1i361 intron gain.

Age. Zhong et al. (2014b) suggested an age of (378.8-)336.7(-291.5) m.y. for this clade.

See P. Soltis et al. (2002) for a variety of suggestions for node ages in this whole clade.

MARRATTIOPSIDA

Roots with several protoxylem poles; root hairs septate [?multicellular]; stipules +, fleshy and starchy; ; embryo endoscopic.

MARATTIALES Link
Synonymy: Christenseniales Doweld

MARATTIACEAE

Dictyostele +; mucilage canals +; rhizome with scales; hydathodes [lenticels] +; fronds pulvinate, (leaflet venation reticulate, with internally directed veins - Christensenia), spores bilateral or ellipsoid, monolete; meiosis monplastidic [Angiopteris]; x = 40. 5/150: Danaea (50).

For some comments on biogeography, see Christenhusz and Chase (2013).

For a phylogeny, see Murdock (2008a), also Christenhusz et al. (2008); the fossil Psaronius seems to associate consistently with Marattia (e.g. Grand et al. 2013 and references). Both Marattia and Angiopteris are paraphyletic, but they can easily be made monophyletic (Murdock 2008b). For Danaea, see Christenhusz (2010), for meiosis, see Brown and Lemmon (2001).

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; leaf trace single; sporangium leptosporangiate [derived from periclinal division of a single epidermal cell, wall one-layered, stalk 4-6 cells across]; sporangium with exothecium forming an annulus, spores 64-800; antheridium ± exposed; gametophyte cordate [level?]; embryo prone [first cell wall of the zygote vertical, parallel to gravity], with quadrant/octant formation, suspensor 0.

Age. Magallón et al. (2013: with temporal constraints) estimated an age of around (267.8-)252.7-251.4(-246.1) m.y. for this clade (but see immediately below); (330-)323(-310) m.y. is the age in Y. L. Qiu et al. (2007),perhaps 350 m.y.a. in Schneider et al. (2004a) and around 170 m.y.a. in Villarreal and Renner (2014).

Phylogeny. The large clade made up of leptosporangiate ferns has 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). 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 relationships within leptosporangiate ferns (e.g. Pryer et al. 2004a, b and references; Schuettpelz & Pryer 2007; c.f. in part Kuo et al. 2011: positions of Gleicheniaceae, Lindsaeaceae, Nephrolepis [previously in Lomariopsidaceae] unclear). Lindsaeaceae are probably sister to the rest of the Polypodiales, but the genera Cystodium, ex Dicksoniaceae, and Lonchitis and Saccoloma, both ex Dennstaediaceae and the last as a separate family below, are also in that area (Lehtonen et al. 2012). Davalliaceae and related taxa are sister to the polygrammoid ferns, and both 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, 2011) are consistent with those suggested by sequence analyses. Cystopteris and relatives form a clade that may be sister to the eupolypod II clade (Rothfels et al. 2009, esp. 2012a, 2013 and references).

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; zygote elongation occuring; x = 22. 4/20.

The Osmunda clade originated in the late Carboniferous, ca 323 or 305 m.y.a. (Phipps et al. 1998; Schneider et al. 2004a), and is very diverse from the Permian onwards, less so more recently. Fossils some 180 m.y.o. have anatomy that is remarkably like that of the extant Osmunda claytoniana, and probably the chromosome number and genome size of the fossil plant were similar, too (Bomfleur et al. 2014a).

It has been suggested that Osmunda is paraphyletic, and Osmunda (now = Osmundastrum) cinnamomea being sister to the rest of the family (Metzgar et al. 2008). However, Bomfleur et al. (2014b) argue for the monophyly of Osmunda based on extensive data from fossils and a re-evaluation of the molecular evidence, i.a. they note that O. cinnamomea is able to hybridize with some species of Osmunda, but not with other Osmundaceae.

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

Age. (297-)286(-272) m.y. is the age for this node in Y. L. Qiu et al. (2007).


[Hymenophyllales + Gleicheniales]: ?

Age. The age for this node in Y. L. Qiu et al. (2007) was estimated at (283-)273(-259) m.y..

HYMENOPHYLLALES A. B. Frank
HYMENOPHYLLACEAE

Epiphytes common; 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; embryo not with tetrad/octant formation; x = 36. 9/600.

Crown Hymenophyllaceae are ca 206 m.y.o. (Schuettpelz & Pryer 2007); for other dates, see that article and Hennequin et al. (2008).

For the rate of molecular evolution if Hymenophyllaceae, with an apparent slow-down in Hymenophyllum, see Schuettpelz and Pryer (2007).

For epiphytism in Hymenophyllaceae, see Hennequin et al. (2008). Over half the family is epiphytic (Zotz 2013), and there are also climbing taxa (see Dubuisson et al. 2009 for growth forms in Hymenophyllum). Epiphytism in Trichomanes evolved before that in Hymenophyllum, probably on the stems of Cyantheaceae on which it is still often to be found (Hennequin et al. 2008), indeed, diversification in Trichomanes is estimated to have begun in the middle of the Jurassic and that in Hymenophyllum in the middle of the Cretaceous (Schuettpelz & Pryer 2007).

Despite the delicate fronds of Hymenophyllaceae, dessication tolerance is at least sometimes well developed - c.f. mosses (Proctor 2003). Indeed, the sporophytes of some epiphytic trichomanoid ferns have lost both cuticle and roots ("regressive evolution" - Dubuisson et al. 2011), and may be functionally similar to bryophytes; the stem stele may have just a single vascular element (Dubuisson et al. 2013; see also Dubuisson et al. 2003b).

For the phylogeny of the family, see Pryer et al. (2001b) and Dubuisson et al. (2003a, 2013), for that of Trichomanes and relatives, see Ebihara et al. (2007), for that of Hymenophyllum, with a focus on the large subgenus Mecodium, which turns out to be polyphyletic but common in a number of basal clades, see Hennequin et al. (2006), and for a possible base chromosome number in the family - previous suggestions x = 6-9, 11, 13, but here = 36 - see Hennequin et al. (2010).

GLEICHENIALES Schimper
Root steles with 3-5 protoxylem poles; rhizome with scales; frond 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; (embryo exoscopic, cell wall vertical - gametophyte subterranean); x = 22, 34, etc. 6/125.

There has been a chloroplast genome inversion in the family (Wolf & Roper 2008).


[Dipteridaceae + Matoniaceae]: ?

DIPTERIDACEAE

Frond 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, earlier in Tertiary widespread.


MATONIACEAE

Stems solenostelic, with two vascular cylinders and a central bundle; fronds or pinnae ± dichotomously branched; sporangia in ring surrounding central "receptacle", sorus indusiate; x = 25, 26. 2/4. Malesia, previously widespread.

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

Age. (281-)266(-250) m.y. is the age for this node in Y. L. Qiu et al. (2007).

SCHIZAEALES Schimper
Fronds differentiated into fertile/sterile portions; annulus sub-apical.

LYGODIACEAE

Fronds 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; fronds undivided or fan-shaped, veins dichotomizing; sporangia borne on marginal projections at blade tip; spores bilateral, monolete; gametophyte filamentous, (white, subterranean, tuberous; embryo exoscopic, cell wall vertical); x = 77, 94, 103. 2/30.

There has been a chloroplast genome inversion somewhere around here (Wolf & Roper 2008); see also the next node up.

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

SALVINIALES Bartling
Aquatics, aerenchyma +; stems dichotomizing; leaves simple; veins ± anastomosing; sterile/fertile frond 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, 2007: 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, genome size [1C] ca 0.8 pg [Azolla]. 3/75.

For the phylogeny of Marsilea and character evolution there, see Nagalingum et al. (2007).

SALVINIACEAE

Plant free-floating; fronds sessile, 2-ranked, <2.5 cm long; x = 9, 22. 2/16.

[Cyatheales + Polypodiales]: dictyostele +; hydathodes +; IR with several large inversions, ycf2 duplication.

Age. The age for this node is ca 211 m.y. in Y. L. Qiu et al. (2007) and (270.1-)228.8(-187.5) m.y. in Zhong et al. (2014b).

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.

Synonymy: Dicksoniales Deveal, Hymenophyllopsidales Reveal, Loxomatales Reveal, Metaxyales Doweld, Plagiogyriales Reveal

THYRSIDOPTERACEAE

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

Multiple leaf traces coming from a U-shaped bundle; young fronds with dense, pluricellular, mucilage-secreting hairs; indusium 0; x = ?66. 1/15.


[Cibotiaceae + Cyatheaceae + Dicksoniaceae + Metaxyaceae]: paraphyses +.

CIBOTIACEAE

Multiple leaf traces coming from a U-shaped bundle; stomata with three subsidiary cells; spores with equatorial flange, usu. parallel ridges on distal face; x = 68. 1/11.


CYATHEACEAE

Stem with polycyclic dictyostele; multiple leaf traces coming from a U-shaped bundle; scales +, large (also small); fronds large; (sori superficial; indusium 0 to completely surrounding sporangia); x = 69. 5/600.

The rate of chloroplast genome evolution has slowed down considerably here, probably because of the long generation time of tree ferns (P. Soltis et al. 200; esp. Zhong et al. 2014b).

Korall and Pryer (2014) outline major biogeographic patterns in the group; initially Gondwanan vicariance seems to be involved, although crown-goup diversification did not begin until ca 96 m.y.a. (the stem age - divergence from Dicksoniaceae - was estimated at ca 150 m.y.a.) with subsequent rather limited (for ferns) transoceanic long distance dispersal. The 100+ endemic species of Cyathea on Madagascar represent the Pliocene ([4.24-]3.07> m.y) diversification of three separate clades each of which has a fairly lengthy sojourn on the island (Janssen et al. 2008, see also Korall & Pryer 2014). Bystriakova et al. (2011) discussed niche evolution.

See Korall et al. (2006, 2007) for a phylogeny.

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
Rhizome dorsiventral [?level]; aerophores +; sporangial maturation mixed; stalk 1-3 cells thick, annulus vertical, interrupted by stalk and stomium; neochrome/phy 3 +.

Age. This clade is some (200-)176(-163) m.y.o. (Schneider et al. 2004a).

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; leaf traces two, from V-shaped bundle; 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 + The Rest]: ?

Age. Zhong et al. (2014b) suggested an age of (217-)154.3(-93.1) m.y. for this node {Denn. + Pterid.].

DENNSTAEDTIACEAE

Chimaeric red/far red light photoreceptor [phy 3, neochrome]; stele?; hairs jointed; petiole bearing buds, with gutter-shaped bundle; x = 26, 29. 11/170.


PTERIDACEAE

(Epiphytic), (xeric); scales +; indusium 0; (spores bilateral); (gametophyte ribbon-like); x = 29, 30. 50/950: Pteris (250), Adiantum (200), Vittaria (80).

The age of this clade is around 90 m.y. (Rothfels & Schuettpelz 2014).

For phylogenies, see Crane et al. (1995), Prado et al. (2007), Schuettpelz (2007) and Chao et al. (2014: Pteris, position of P. longifolia, the type, unclear); for increased rates of molecular evolution, see Rothfels and Schuettpelz (2014). Cheilanthoid ferns, some 400 or more species, can grow in very dry conditions, but generic limits are difficult there; see Grusz et al. (2014 and references) for their phylogeny.

Eupolypods: scales +; spores reniform, monolete; x = 41.

Age. This clade, which includes the bulk of the monilophytes, is around (124-)105(-91) m.y.o. (Schneider et al. 2004a).

[Dryopteridaceae [Lomariopsidaceae [Tectariaceae [Oleandraceae [Davalliaceae + Polypodiaceae]]]]] / polypod I: rhizome scales of stalk + shield, persistent, dense; leaf traces several, from V-shaped bundle; petiole with three or more vascular bundles.

This is a largely epiphytic clade; for rhizome scales, perhaps protecting the plant 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).

DRYOPTERIDACEAE

(Epiphytic); perine winged; gametophyte strap-like; x= 41. 30-35/1700.

Elaphoglossum is the major epiphytic genus in the family - ca 400 species are epiphytes (Zotz 2013). For a phylogeny, see H.-M. Liu et al. (2007) and Lóriga et al. (2014: 20-15 m.y.a. fossil from Dominican amber); Moran et al. (2010a, b) investigate relationships within the bolbitidoid ferns focussing on variation in perispore morphology, Rouhan et al. et al. (2004) on relationships within the speciose Elaphoglossum, and Li and Lu (2006a, b), L.-B. Zhang et al. (2012), Sessa et al. (2012a), and McHenry and Barington (2014: exindusiate Andean species monphyletic, sister to Mexican spp.) on those within Dryopteris itself, a genus whose limits are being clarified (e.g. Zhang & Zhang 2012) and which shows extensive hybridization at all levels (Sessa et al. 2012b). See also Labiak et al. (2014) for relationships around Lastreopsis, with movement to and fro between Australia and South America towards the middle of the Tertiary.

[Tectariaceae [Oleandraceae [Davalliaceae + Polypodiaceae]]]]: ?
frond veins free, parallel or pinnate. 4/70.

TECTARIACEAE

(Climbers); (rhizome slender), (stipe and pinnae articulated); (frond veins free, parallel or pinnate), with jointed usually stubby hairs; n = 40-42: Tectaria (200). 8-19/320. Pantropical, inc. oceanic islands.

Synonymy: Arthopteridaceae H. M. Liu, Hovenkamp & H. Schneider, Lomariopsidaceae


Although in the analysis of H.-M. Liu et al. (2013) the position of Arthropteridaceae was uncertain, F. G. Wang et al. (2014) found that they were embedded in Polypodiaceae-Tectarioideae, as were Lomariopsidaceae.

[Oleandraceae [Davalliaceae + Polypodiaceae]]: fronds abscising from rhizome.

OLEANDRACEAE

Fronds abscising just above the base [so leaving phyllopodia]; x = 41. 1/40.


[Davalliaceae + Polypodiaceae]: epiphytes predominant.

DAVALLIACEAE

x = 40. 4-5/65.

For a generic classification, see Kato and Tsutsumi (2008).

POLYPODIACEAE

(Rhizome polysmmetrical); (Petiole with one or two vascular bundles - grammitids); indusium 0; (spores green, globose-tetrahedral, trilete - grammitids); (gametophyte strap-like); x = 35-37. 56/1200: Drynaria (50).

Ca 87% of the species of Polypodiaceae are epiphytic (Zotz 2013), making them the major epiphytic clade in the monilophytes. For the phylogeny of grammitid ferns, see Sundue et al. (2014a, esp. b: Grammatis still polyphyletic).

Janssen et al. (2005) discussed the evolution of the diverse frond morphologies in Drynaria s.l.. For root anatomy, see Schneider (1996, 1997), and for petiole anatomy, see Sundue et al. (2014a, esp. b and references).

For a phylogeny of microsoroid ferns, see Kreier et al. (2008), for that of grammitid ferns, see Sundue et al. (2010, 2015 and references: generic changes). Wang et al. (2014) include a broadened Tectariaceae as a subfamily of Polypodiaceae; to be done here?

[Cystopteridaceae [[Rachidosoraceae [Diplaziopsidaceae [Hemidictyaceae + Aspleniaceae]] [Thelypteridaceae [Woodsiaceae [Athyriaceae [Blechnaceae + Onocleaceae]]]]]] / polypod II: leaf traces two, from V-shaped bundle, circumendodermal band surrounding trace; petiole with two ± crescent-shaped vascular bundles; rhachis sulcus wall confluent with the costa of pinna.


CYSTOPTERIDACEAE Shmakov

Rhizome long-creeping; veins reaching the frond margin; indusium 0 or hood-like; n = 40, etc.. 3/36: Cystopteris (27).

For phylogenetic relationships, see Rothfels et al. (2013). The genera are monpphyletic, but there has been very extensive hybridization within Cystopteris and Gymnocarpidium(Rothfels et al. 2014)

[[Rachidosoraceae [Diplaziopsidaceae [Hemidictyaceae + Aspleniaceae]] [Thelypteridaceae [Woodsiaceae [Athyriaceae [Blechnaceae + Onocleaceae]]]]]: ?
[Rachidosoraceae [Diplaziopsidaceae [Hemidictyaceae + Aspleniaceae]]: sorus on one side of the vein.

RACHIDOSORACEAE X. C. Zhang

Scales clathrate; n = 41; 1/4-7.


[Diplaziopsidaceae [Hemidictyaceae + Aspleniaceae]]: scales on mature fronds 0.

DIPLAZIOPSIDACEAE X. C. Zhang & Christenhusz

Roots pale, fleshy, proliferous [producing plantlets by asexual reproduction]; fronds soft and fleshy; vein endings raised and thickened, forming a submarginal vein; sori elongated, only on one side of vein; n = 40, 41; 3/5.


[Hemidictyaceae + Aspleniaceae]: ?

HEMIDICTYACEAE Christenhusz & H. Schneider

Frond with submarginal collecting vein and margins with broad membranous border; vein endings raised and thickened; n = 31; 1/1.


ASPLENIACEAE Newman

Epiphytes common; root pericyclic sclereids with excentric lumina; leaf trace single, circumendodermal band surrounding trace 0; petiole with back-to back C-shaped strands, these fusing and becoming X-shaped; scales clathrate; frond usu. with small clavate hairs; leaf margins decurrent and forming the lateral ridge along rhachis; sori linear; indusia lateral, linear; sporangium stalk 1 cell thick in the middle; spores with decidedly winged perine; x = 35, 36, 38, 39. 1-10/700.

Asplenium s.l. includes a large number of epiphytic species (Zotz 2013). Helical, non-lignified wall thickenings (c.f. the velamen of monocots) occur in cortical cells of some Asplenium, mostly epiphytic species (Leroux et al. 2011).

For generic limits, see Bellefroid et al. (2010 and references); Asplenium s. str. is paraphyletic.

[Thelypteridaceae [Woodsiaceae [Athyriaceae [Blechnaceae + Onocleaceae]]]]: frond once-pinnate/pinnatifid.

THELYPTERIDACEAE Pichi-Sermolli

Petiole vascular bundles uniting distally into a gutter shape; hairs acicular, whitish or hyaline, rhizome scales with hairs on surface and/or margins; first venation of frond lobe/pinnule develops on basiscopic side [catadromous]; n = 27-36. 8/950: Microsorium (600).

For a careful evaluation of generic limits, which are best drawn broadly given the extensive generic polyphyly and highly homoplasious "generic" characters, especially within Cyclosorus s.l., see He and Zhang (2012).

[Woodsiaceae [Athyriaceae [Blechnaceae + Onocleaceae]]]: ?

WOODSIACEAE Herter

Plant epipetric; rhizomes suberect; petiole bases persist; circumendodermal band surrounding leaf trace 0; indusium basal, of many scale-like or filamentous segments, receptacle raised; n = 33, 38, 39, 41. 1/35.


[Athyriaceae [Blechnaceae + Onocleaceae]]: ?

ATHYRIACEAE Alston

Mature leaf with abundant anthocyanin; leaf margins entire, petiole base swollen, (starch-containing), ± persistent [= trophopod]; corniculae/scales at adaxial junction of pinna costa with rachis; indusia opening to face away from a single vein [either two linear back to back sori, or J-shaped indusium of a single sorus wrapped around the vein]; n = 40, 41. 5/600: Diplazium (400).

Wei et al. (2013) evaluated relationships within Diplazium and found i.a. that species previously assigned to Allantodia in particular were scattered through the tree; they circumscribed Diplazium broadly and provided an infrageneric classification for it.

[Blechnaceae + Onocleaceae]]: (fertile and sterile fronds dimorphic).

BLECHNACEAE Newman

Young leaves reddish; leaf traces several, from V-shaped bundle; petiole at the base with three to many round vascular bundles arranged in a ring; (fronds monomorphic), veins forming narrow areoles near the costa; sori elongated, on costal commissural vein, indusia linear, opening towards median nerve; perine winged; n = 34 [27, 28, 31-37, 40]. 4/200.

For relationships in Blechnaceae, with Blechnum circumscribed rather broadly, see Perrie et al. (2014).


ONOCLEACEAE Pichi-Sermolli

Circumendodermal band surrounding leaf trace 0; petiole vascular bundles uniting distally into a gutter shape; trophopods +; sori enclosed by reflexed lamina margins; indusium deltate; spores chlorophyllous; n = 37, 39, 40. 4/5.