Plant evolution and terrestrialization during Palaeozoic times—The phylogenetic context

Review of Palaeobotany and Palynology 227 (2016) 4–18 Contents lists available at ScienceDirect Review of Palaeobotany and Palynology journal homepage: www.elsevier.com/locate/revpalbo Plant evolution and terrestrialization during Palaeozoic times—The phylogenetic context Philippe Gerrienne a,⁎, Thomas Servais b, Marco Vecoli c a b c PPP, Département de Géologie, Université de Liège, Allée du 6 Août, B18 Sart Tilman, B4000, Liège, Belgium Evo-Eco-Paléo, UMR 8198 CNRS, Université de Lille, Avenue Paul Langevin, Bâtiment SN5, 59655 Villeneuve d'Ascq, France Biostratigraphy Group, Exploration Technical Services Department, Saudi Aramco, Dhahran, Saudi Arabia a r t i c l e i n f o Article history: Received 12 May 2015 Received in revised form 18 January 2016 Accepted 18 January 2016 Available online 4 February 2016 Keywords: Cryptospores Embryophytes Palaeozoic Phylogeny Streptophytes Terrestrialization a b s t r a c t Terrestrialization probably began more than one billion years ago and irreversibly altered biogeochemical processes at planetary scale. In this paper, we focus on the terrestrialization process of the Streptophyta, the division that includes charophytes and land plants (embryophytes) and whose members are today ecologically dominant in all terrestrial environments. The timing and the phylogenetic context of the early evolution of land plants are reviewed. The available information on the relationships within embryophytes and related organisms is compiled in two informal consensus trees based either on morphological/anatomical or on molecular data. We also consider the algal/embryophyte transition through the analysis of the evidence provided by microfossils (cryptospores and spores). The ongoing debate about the definition of the term cryptospores, but more importantly about the biological affinities of these microfossils that are possibly derived from early land plants, is discussed. All important clades of embryophytes, with a focus on their Palaeozoic representatives, are described; the significance of several embryophyte key characters is evaluated. The terrestrialization of land plants evolved in different steps. The new term “proembryophytic phase” is introduced to define the very long period of time during which the green algae ancestor of land plants acquired all the evolutionary characters that ultimately allowed their terrestrialization since the late Precambrian. An “eoembryophytic phase”, spanning the MiddleUpper Ordovician, is defined based on the occurrence of the earliest evidence of liverwort-like plants. The inception of the trilete spores in Late Ordovician times is then taken to define the start of the eo/eutracheophytic phase, which lasts until the first occurrence of vascular plant macrofossils in the Silurian. © 2016 Elsevier B.V. All rights reserved. 1. Introduction The colonization process of terrestrial habitats by living organisms belonging to various lineages, first of prokaryotes and later of eukaryotes, consists of an extremely complex body of phenomena and its study clearly involves collaboration across a wide range of disciplines (Vecoli et al., 2010). This colonization was made possible by a range of evolutionary novelties and associated palaeoenvironmental changes generally grouped under the heading “terrestrialization”. Terrestrialization probably began more than one billion years ago (Strother et al., 2011; Graham et al., 2014), and irreversibly altered biogeochemical processes at planetary scale. In the green lineage (= Viridiplantae Cavalier-Smith or Chloroplastida Adl et al.), all the organisms that evolved characters linked to the terrestrialization belong to the Streptophyta (sensu Leliaert et al., 2012; Wickett et al., 2014; not sensu Adl et al., 2012; Fig. 1). Within that lineage, there have probably been several independent transitions to land (Jobson and Qiu, 2011), one of which eventually led to the ecological dominance of ⁎ Corresponding author. Tel.: +32 4 366 53 63; fax: +32 4 366 53 38. E-mail address: [email protected] (P. Gerrienne). http://dx.doi.org/10.1016/j.revpalbo.2016.01.004 0034-6667/© 2016 Elsevier B.V. All rights reserved. embryophytes (land plants) in most terrestrial environments. A comprehensive survey dedicated to the algal/embryophyte transition was recently proposed by Graham et al. (2014). The evolutionary relationships within the green lineage members are still controversial (Fig. 1), but for most authors (e.g. Leliaert et al., 2012), Streptophyta includes Charophyta and Embryophyta. Charophyta is generally resolved as paraphyletic with respect to Embryophyta, the latter sharing a common ancestor with one class/ order of charophytes (Karol et al., 2001; Lewis and McCourt, 2004; Finet et al., 2010; Leliaert et al., 2012; Wickett et al., 2014; Fig. 1; see below for further comments). The transition from gametophyte-dominant haplobiontic life cycles in green algal ancestors of plants to diplobiontic life cycles, i.e. alternation of gametophytic and sporophytic generations in embryophytes (the so-called Antithetic Theory; Bower, 1890; Haig, 2008, 2015) has most probably played a pivotal role in the terrestrialization process (Kenrick and Crane, 1997a; Niklas and Kutschera, 2010; Qiu et al., 2012). The sporophyte generation releases a large number of spores, which improve reproduction efficiency. Moreover, the diploidy of the sporophyte cells helps minimizing the impact of mutagenic factors (Qiu et al., 2006). Accordingly, the shift from heteromorphic, P. Gerrienne et al. / Review of Palaeobotany and Palynology 227 (2016) 4–18 5 Fig. 1. Possible evolutionary relationships between the green lineage members. A—Karol et al. (2001); analysis based upon DNA sequence data from four genes representing three plant genomes: (plastid, mitochondrial and nuclear); B—Finet et al. (2010); analysis based upon a multilocus data set of 77 nuclear genes from 77 taxa; C—Leliaert et al. (2012); consensus reconstruction of green algal relationships, based on various molecular data; D—Wickett et al. (2014); analysis based upon concatenated alignments of first and second codon positions for 674 genes of chlorophytes and streptophytes. gametophyte-dominant generations, as present in bryophytes, to heteromorphic, sporophyte-dominant generations in vascular plants was presumably decisive in the evolutionary success of the latter (Qiu et al., 2006; Gerrienne and Gonez, 2011). In recent years, a number of works have addressed the terrestrialization and evolution of embryophytes, based on micro-, meso- and/or macrofossil evidence (e.g. Gensel, 2008; Kenrick et al., 2012; Steemans et al., 2012; Hao and Xue, 2013; Strullu-Derrien et al., 2013; Edwards et al., 2014; Edwards and Kenrick, 2015). The evolution of roots (Kenrick and Strullu-Derrien, 2014) and of the symbiosis with mycorrhizal fungi (Bidartondo et al., 2011; Kenrick and Strullu-Derrien, 2014; Strullu-Derrien et al., 2014; Selosse et al., 2015) as well as molecular and biochemical aspects (Versteegh and Riboulleau, 2010; Romero-Sarmiento et al., 2011; Delaux et al., 2012) have also been considered. The analysis of the diversity dynamics of lineages involved in the terrestrialization process (see for example Cascales-Miñana and Meyer-Berthaud, 2014; Silvestro et al., 2015) is a promising field; the major impact of the palaeogeographical pattern in the diversification of terrestrial organisms and more precisely in shaping plant palaeodiversity has recently been demonstrated for Zosterophyllopsida (early lycophytes; Cascales-Miñana and MeyerBerthaud, 2015). The co-evolution of rivers and riparian vegetation has also been addressed in several works (Corenblit et al., 2015; Gibling and Davies, 2012; Gibling et al., 2013). In this paper, we compile the available information on the relationships within embryophytes and related organisms in two informal consensus trees based either on morphological/anatomical or on molecular data, in order to set up a plausible phylogenetic framework of the various steps of the terrestrialization of the representatives of the Embryophyta. We also discuss the algal/embryophyte transition through the analysis of the evidence provided by microfossils (cryptospores and spores). Finally, all important clades of embryophytes, with a focus on their Palaeozoic representatives, are briefly described; in the same section, we evaluate the weight/significance of several embryophyte characters and of some recently described land plant taxa. 2. The evolutionary context of plant terrestrialization The phylogenetic relationships of all the organisms among the Embryophyta involved in the terrestrialization process have most generally been evaluated by the molecular systematics through the analysis of chloroplast, mitochondrial and/or nuclear genes of extant organisms. These analyses give various incongruent topologies in the basal part of the tree, and, to date, there is no consensus about the identity of the closest living relative to land plants. Three candidates have each in turn received support: the Charophyceae (or Charales—Karol et al., 2001; Lewis and McCourt, 2004; McCourt et al., 2004; Qiu et al., 2006; Qiu, 2008 and references therein; Fig. 1A), the Coleochaetophyceae (or Coleochaetales—Finet et al., 2010; Fig. 1B, C), and the Zygnematophyceae (or Zygnematales—Turmel et al., 2006; Wodniok et al., 2011; Wickett et al., 2014; Fig. 1C, D). The monophyly or paraphyly of the plant at bryophytic level of organization (non-vascular embryophytes, i.e. the Marchantiophyta, Anthocerotophyta and Bryophyta) with respect to the tracheophytes, is equally vigorously debated (Mishler and Churchill, 1984; Nishiyama et al., 2004; Zhong et al., 2013; Cox et al., 2014; Wickett et al., 2014). When the bryophytes are resolved as paraphyletic, the identity of the sister-group of the tracheophytes, either the Bryophyta (mosses) (Mishler and Churchill, 1984), or the Anthocerotophyta (hornworts) (Clarke et al., 2011; Ruhfel et al., 2014) is also discussed. However, most studies resolve (i) Marchantiophyta (liverworts) as a sister group to the remaining land plants (Qiu, 2008; Clarke et al., 2011; Bowman, 2013) and (ii) Anthocerotophyta as a sister group to 6 P. Gerrienne et al. / Review of Palaeobotany and Palynology 227 (2016) 4–18 tracheophytes (Qiu et al., 2006; Qiu, 2008; Karol et al., 2010; Ruhfel et al., 2014). All this information, uncertainties included, is compiled in Fig. 2. A few studies of land plant relationships have combined morphological data of both fossil and living taxa (Crane, 1985; Rothwell and Serbet, 1994; Rothwell, 1994, 1996, 1999; Kenrick and Crane, 1997a,b; Crane et al., 2004; Hilton and Bateman, 2006; Rothwell and Nixon, 2006; Hao and Xue, 2013). With the exception of the work of Hao and Xue (2013), which includes a large number of Early Devonian endemics from China, all those studies are compiled in Fig. 2. They gave conflicting results, and the consensus tree presented at Fig. 2 therefore includes several polytomies. 3. Microfossil evidence: the algal/plant transition 3.1. Precambrian and Early Palaeozoic terrestrial microfossils Numerous palynological investigations in the Precambrian and earliest Palaeozoic revealed the presence of organic-walled microfossils. These palynomorphs are recovered generally from marine environments, although a few terrestrial settings also provided microfossils (e.g. Strother et al., 2011; Strother and Wellman, 2016). The biological affinities of most of these microfossils are generally debated, and for this reason, most of them are attributed to the informal group of the acritarchs. Evitt (1963) defined the acritarchs as a utilitarian category, to classify all organic-walled microfossils of unknown biological affinity. Servais (1996) and Servais et al. (1997) pointed out that the definition of the acritarchs by Evitt (1963) clearly excludes a biological interpretation, and that the organisms that produced the acritarchs are of diverse origins, marine and non-marine, planktonic and non-planktonic. It is therefore possible that some of the more problematic Palaeozoic organic-walled microfossils represent organisms of freshwater and terrestrial organisms, including spores of the earliest land plants. Spherical microfossils without a prominent ornamentation, like naked sphaeromorph acritarchs, may have various biological origins (e.g., Prasinophyceae, Chlorophyceae), and some of them can be of terrestrial origin. Unornamented spores (such as “naked monad” cryptospores), without a clearly visible trilete mark, could be, for example, easily identified or classified as sphaeromorph acritarchs. Some of the Precambrian and Lower Palaeozoic organic-walled, spherical and featureless microfossils attributed to the acritarchs may therefore well derive from earliest land plants, or indicate fossil evidence of the algal-plant transition. Colonial forms of unidentified biological affinity, that have been in some cases attributed to the acritarchs, may be of algal origin (for example, some forms have been compared to colonial chlorophyceaen or hydrodyctyacean algae, others have been attributed to Gloeocapsomorpha prisca, see Colbath and Grenfell, 1995) or may also indicate the transition from algae toward the plants (e.g., possible spore masses produced in a sporangium). Numerous such colonial forms have Fig. 2. Compilation of available data on evolutionary relationships between Coleochaetales, Charales, Zygnematales and Palaeozoic Embryophytes. Consensus trees are based either on morphological/anatomical data (left part of the figure) or on molecular data (right part). Numerical ages of Period boundaries are from the International Chronostratigraphic Chart (Cohen et al., 2013). Ages in italics are calibration points from Zhong et al. (2014). Alternating shaded and white areas represent Epochs. Stratigraphic range of Charales from Feist et al. (2005) and Conkin and Conkin (1992); stratigraphic range of Zygnematales from Baschnagel (1966). Cam = Cambrian; Car = Carboniferous; Dev = Devonian; L = Lower; M = Middle; Mi = Mississippian; Ord = Ordovician; Pe = Pennsylvanian; Per = Permian; Sil = Silurian; U = Upper. See text for references and further explanation. P. Gerrienne et al. / Review of Palaeobotany and Palynology 227 (2016) 4–18 been described in the Precambrian and Early Palaeozoic, but the biological affinity of these palynomorphs mostly remains uncertain. Palynologists working in the Middle and Upper Palaeozoic easily distinguish the marine fraction (“acritarchs”) from the terrestrial part, identified as pollen grains and miospores on purely morphological grounds. However, numerous forms in the Lower Palaeozoic cannot easily be attributed to the miospores, nor to typical morphologies produced by phytoplanktonic organisms. Different terminologies have been created to name and classify such microfossils, of which the biological affinity is still debated. Among these terminologies, the term “cryptospores” has been commonly used, but different definitions and interpretations exist today, and the precise description or definition of the term are currently controversial. 3.2. Spores: Cryptospores–miospores–megaspores: definition versus interpretation The term “spore” is widely used in biology. A spore is a dormant, reproductive cell, formed by a great variety of organisms. It is usually very resistant to survive unfavourable conditions. Different spores are commonly found in the fossil record, such as fungal spores, spores of several algal groups (e.g. zygnematacean spores) and spores of higher plants. Bacteria also may produce spores that can be very resistant, surviving pasteurization and sterilization. In botany, meiospores are the cells that are one of the products of meiosis in plants, produced by sporophyte plants (whereas gametophytes produce gametes). Spores are usually produced and stored in a sporangium (plural: sporangia) that can also be fossilized in the context of exceptional preservation. In palaeobotany, different terminologies are commonly used. The term ‘miospore’ is used to include all spores and pollen grains less than 200 μm in diameter. Some fossil plants are homosporous, producing one type of spore. Other are heteroporous producing a male ‘microspore’ and a much larger female ‘megaspore.’ By analogy with the morphology of the spores of extant plants it can be assumed that these ‘miospores’ derive from higher land plants. However, some spore-like microfossils that do not display the characteristic features of plant microspores were named ‘cryptospores’ by several authors. This term has no official nomenclatural rank and is rather loosely defined, although it is of current use today. Richardson et al. (1984) first proposed the “new spore Anteturma, namely Cryptosporites.” Richardson et al. (1984) used the term for non-marine (non-pollen grains) that did not display the typical visible haptotypic features such as trilete marks or furrows which characterize tracheophyte spores or pollen grains. Based on material of the Scottish “Old Red Sandstone” Richardson et al. (1984) described among the cryptospores single grains or monads, “permanent” dyads and tetrads and sporomorphs separated from polyads which may or may not preserve contact areas. Subsequently, Richardson (1988) described some much older cryptospores from the Late Ordovician and Early Silurian of Libya. Strother (1991) described the cryptospores as “a class of sporomorphs which is distinct from trilete and monolete spores, pollen grains and acritarchs”. Strother (1991) noted that the spore-like palynomorphs are similar in many respects to spores of embryophytes, but that their classification is based on an artificial system because the biological affinity for the species of cryptospores is unknown. Strother (1991) noted that current cryptospore classification does not represent a phylogenetic classification because it does not group species on the basis of ancestor–descendant relationships. Richardson (1996) further noted that cryptospores are often enclosed within a thin envelope that is difficult to equate with similar structures in extant plants. The cryptospores are clearly a group of microfossils defined by exclusion (as are the acritarchs when compared with the dinoflagellates, by definition a non-group): the cryptospores are those spores that cannot be clearly associated with land plants, but that are also 7 “non-marine”, to distinguish them from the palynomorphs, that are usually interpreted as the cysts of marine algae. Alete spores which are known to be derived from vascular plants are also excluded. The term “permanent” is meant to reflect the tendency for these spores to remain attached to each other, forming various forms of polyads. Most interestingly, the plants that produce the cryptospores have been named cryptophytes by Edwards et al. (1995b, 2014), in analogy with the sporophytes that produce plant spores. With the creation of the term cryptophytes Edwards et al. (1995b, 2014) implied that the cryptospores are produced by “simple terrestrial organisms of short stature (i.e. millimetres high).” Similarly to the acritarchs, the precise biological affinity of the cryptospores is unknown, as clearly indicated by Strother (1991). They are generally interpreted as representing “spores” that probably derive from primitive plants, representing a dormant, reproductive cell. Some cryptospores are found in sporangia-like structures (e.g. Wellman et al., 2003; Edwards et al., 2014), strengthening their relation to land plants. However, it remains unclear by which class of land plants they have been produced. Steemans (2000) changed the “definition” of the term cryptospore to include only spores thought to be produced by embryophytes and to exclude all enigmatic palynomorphs. With this restrictive definition, all spore-like microfossils that cannot be related to the embryophytes fall outside a terminology, although they could be classified within the acritarchs, that are, by definition, a group of organic-walled microfossils without biological affinity. Steemans (2000) also declared that the cryptospores are included in the miospore group, and thus inferring a biological affinity to the cryptospores, as being produced by land plants. A consequence of the ambiguous definition of cryptospores is that certain kinds of enigmatic palynomorphs have been attributed by different authors to either the cryptospores or the acritarchs. A notable example is represented by the genera Virgatasporites Combaz, 1967 and Attritasporites Combaz, 1967, first described from the Tremadocian of the Algerian Sahara; these were considered as true terrestrial spores by Combaz (1967) who even reported Attritasporites as bearing a small trilete mark. However, this interpretation has not been generally accepted by subsequent authors, who have generally considered the two genera as representing acritarchs typical of restricted, nearshore palaeoenvironments (e.g., Vecoli, 2000). These taxa do not resemble any group of microphytoplankton, and the biological affinity is clearly not understood yet. Today, Middle Ordovician and younger cryptospores are widely considered as deriving from land plants. Wellman (2010) summarized the evidence for land plant affinities of the cryptospores as follows: (1) Middle Ordovician and younger cryptospores are morphologically similar to land plant spores in terms of size and possession of a thick, resistant wall, although they occur as monads, dyads and tetrads, rather than strictly as monads formed from the dissociation of a meiotic tetrad; (2) cryptospores have been found in terrestrial deposits; (3) phylogenetic analyses suggested that liverworts are the most basal extant land plants and certain cryptospores resemble the spores of certain extant liverworts (see also below); (4) some cryptospore dyads have spore wall ultrastructure only known among extant liverworts (Taylor, 1995); (5) remarkably preserved Lower Devonian plants contain in situ cryptospores and these plants have certain bryophytic characters (Edwards et al., 1999); (6) complete sporangia, including covering, with in situ cryptospores were recovered from the Upper Ordovician (Katian) of Oman (Wellman et al., 2003); and (7) recent geochemical analysis has demonstrated that the spore wall in cryptospores from the Silurian of Gotland, Sweden, is chemically similar to that of known land plant spores (Steemans et al., 2010a). There is an ongoing debate about the understanding of the term cryptospores, especially concerning the use of this term for assemblages older than Middle Ordovician times; i.e. between the concepts of Strother (1991) and Steemans (2000). The misunderstanding mainly 8 P. Gerrienne et al. / Review of Palaeobotany and Palynology 227 (2016) 4–18 lies in the distinction of the definition and the interpretation of the term. We advocate the use of the definition of the term “cryptospore” in its original sense by Richardson et al. (1984) and Strother (1991), as a group of spore-like microfossils of unknown biological affinity. Similarly to the acritarchs, this definition does not imply a biological affinity. In this sense, it is evident that cryptospores are present in the Cambrian, and possibly before. This, however, does not imply that these microfossils are produced by embryophytes and that embryophyte-related spores are already present in the Cambrian. 3.3. Cryptospores: fossil record and possible biological affinities It is today well accepted that first macroscopic land-plants are clearly present since the Silurian and that indisputable megafossil vascular plants appeared not until the Late Silurian (e.g. Edwards and Richardson, 2004). However, land-plant derived spores are already present with certainty in the Ordovician, and possible since the Cambrian (Fig. 3). Wellman et al. (2013) summarized the fossil record of the early land plants and indicated that plant megafossils are only recorded from 23 localities in the Early Palaeozoic (Ordovician and Silurian), whereas the fossil record of dispersed spores is much more abundant and extends back at least to the Middle Cambrian (Strother et al., 2004). The first 35 million years of land plant evolution are thus essentially documented on microscopic remains only. Hoffmeister (1959) first described trilete spores from the lower Silurian of Libya, a discovery that predated the earliest land plant megafossils by several million years. As the trilete spores are similar to the isospores of homosporous plants (such as many modern lycopsids and ferns), the finding of the first trilete spores by Hoffmeister (1959) was a major discovery. Older fossils of this type were only made some 40 years later, with the discovery of trilete spores in the Upper Ordovician of Saudi Arabia by Steemans et al. (2009). However, non-trilete spores appear much earlier in the fossil record. After a first description of such spore-like structures in the early Silurian by Gray and Boucot (1971), Gray et al. (1982) documented the by then oldest well-dated spore tetrads and cuticle-like sheets of cells from the “Caradoc” (Upper Ordovician) of western Libya. Gray et al. (1982) were among the first to conclude that land plants, including vascular plants, probably had a long pre-Silurian record, extending at least into the Upper Ordovician. Gray (1985) subsequently noted that the earliest land plants may have been similar to liverworts and were “bryophytelike” or “liverwort-like” because liverworts were the most basal extant land plants (Gray, 1985). Vavrdová (1984) described some plant microfossils of possible terrestrial origin from the Middle Ordovician of central Bohemia, followed by Strother et al. (1996) who published the by then oldest cryptospores from the Llanvirn of Saudi Arabia. These latter levels are now attributed to the Global Stage of the Darriwilian, the upper part of the Middle Ordovician (Bergström et al., 2009). The Saudi Arabian assemblages from the Hanadir Shale Member have recently been reinvestigated in more detail by Strother et al. (2015). The assemblages include a variety of cryptospore tetrads, dyads and monads. Strother et al. (2015) noted that the palynoflora is very similar to younger assemblages of latest Ordovician and earliest Silurian age, and indicated that these cryptospores were produced by early embryophytes, i.e., true land plants. Strother et al. (2015) furthermore considered that the plants that produced these cryptospores were at a “bryophyte grade of evolution.” Similar cryptospore assemblages have been recorded from other upper Middle and Upper Ordovician of other parts of the world (see below), which led Wellman and Gray (2000) and Steemans (2000) to conclude that after the Middle Ordovician the evolution of cryptospore assemblages was very slow up to the early Llandovery, with similar assemblages present on different palaeocontinents during this time interval. Strother et al. (2004) reported Cambrian cryptospores from different localities, but the land-plant origin of these microfossils was questioned by several colleagues, partly due to the problem of the definition of the cryptospores versus their interpretation (see discussion above). Subsequent microstructural work with the Transmitting Electron Microscope (TEM) of the complex resistant cell walls of Cambrian palynomorphs by Taylor and Strother (2008) indicated that some walls bear a strong resemblance to those of certain Lower Devonian hilate cryptospore monads from the Welsh Borderlands. Taylor and Strother (2008) argued that no extant algae produce spores with walls as thick or as complex, suggesting that these Cambrian palynomorphs were the “desiccationresistant spores of cryptogams belonging to the charophyte– Fig. 3. Major evolutionary advances in the cryptospore/trilete spore/plant macrofossil record during pre-Carboniferous times. Palynological data from Strother et al. (1996), Rubinstein et al. (2010), Steemans et al. (2009), Strother et al. (2004, 2011, 2015). Palaeobotanical data from Edwards and Feehan (1980), Edwards et al. (1983), Edwards and Richardson (2004), Gerrienne et al. (2004), Stein et al. (2007, 2012), Prestianni and Gerrienne (2010), Gerrienne et al. (2011). The microbial, bryophytic, tracheophytic and lignophytic landscapes have been described by Strother et al. (2010). The Eoembryophytic, Eo- and Eutracheophytic have been defined by Gray (1993) and Kenrick and Crane (1997b). The Proembryophytic is a new term applying to the very long period of time during which the green algae ancestor of land plants acquired all the evolutionary characters that ultimately allowed their terrestrialization. Rhyniophytic, Eophytic and Palaeophytic Floras have been defined by Cleal and Cascales-Miñana (2014). PAL = pCO2 Preindustrial Atmospheric level; pCO2 values from Berner and Kothavala (2001). P. Gerrienne et al. / Review of Palaeobotany and Palynology 227 (2016) 4–18 embryophyte lineage.” The question if these cryptospores are of landplant origin is currently debated. It is evident, that these assemblages are very important for the understanding of the algal–land plant interaction. Steemans et al. (2009) dated back the oldest occurrence of trilete spores in the Late Ordovician and concluded that the colonization of the land by plants most likely started with bryophyte-like plants that appeared by the Middle Ordovician, who became quickly cosmopolitan and dominated the planet, relatively unchanged, for some 30 million years. Trilete spores appeared in the Late Ordovician and became abundant in the Silurian when they underwent a rapid diversification. Steemans et al. (2009) considered that the appearance of trilete spores in the Late Ordovician coincides with the diversification of vascular plants, with a first occurrence in Gondwana. This interpretation is however discussed, because trilete monads are also produced by some living bryophytes (Edwards et al., 2014; Brown et al., 2015). This presence of trilete spores in the Late Ordovician has recently been documented in some more detail by Wellman et al. (2015). Cryptospores that were considered to be very similar to the typical Middle Ordovician morphotypes (of which the oldest records were so far those of the Darriwilian of the Czech Republic and Saudi Arabia) were found in slightly older sediments of Dapingian (early Middle Ordovician) age from Argentina (Rubinstein et al., 2010). These Argentinean cryptospores would predate the other cryptospore occurrences by ca. 8–12 million years, and are thus currently considered as the earliest evidence of plants on land by most authors. However, Strother et al. (2015) questioned the affinity of the relatively undiversified and morphologically simple Dapingian Argentinian cryptospores assemblages with the typical highly diversified bryophytic cryptospores from the Middle Ordovician of Saudi Arabia. A recent summary of the evolution and geographical distribution of the earliest plants is provided by Wellman et al. (2013) who produce a complete database with almost 800 data points of all reported Ordovician-Silurian land plant megafossil and dispersed spore assemblages. The reader is referred to this study for a complete revision of published literature. Several authors now agree that the origin of the land plants was probably on the supercontinent of Gondwana and that land plants subsequently spread to Avalonia and Baltica (e.g. Steemans et al., 2010b; Wellman et al., 2013; Wellman, 2014). After the first records of cryptospores on Gondwana from Libya (e.g. Gray et al., 1982; Gray, 1985, 1988; Richardson, 1988) and Saudi Arabia (e.g. Strother et al., 1996, 2015; Wellman et al., 2015), cryptospores have also been described from other parts of this supercontinent including Argentina (e.g. Rubinstein and Vaccari, 2004; Rubinstein, 2005; Rubinstein et al., 2010) and Algeria (e.g. Spina, 2014), as well as from microcontinents in the periphery of Gondwana, including Avalonia (e.g. Wellman, 1996; Steemans, 2001), Armorica sensu lato (e.g. Vavrdová, 1984, 1988, 1989) and Turkey (e.g. Steemans et al., 1996). Ordovician cryptospores were also found in localities from the palaeocontinent Laurentia (e.g. Gray and Boucot, 1971; Gray, 1991; Vecoli et al., 2015), from the northernmost part of Gondwana in Australia, located in the northern hemisphere (e.g. Foster and Williams, 1991), as well as from China (e.g. Wang et al., 1997; Yin and He, 2000). The first discoveries of cryptospores from Baltica are more recent. Vecoli et al. (2011) reported cryptospores of the Upper Ordovician of Estonia, followed by a report of a few, slightly older specimens from Sweden by Badawy et al. (2014). The first report of an Upper Ordovician cryptospore assemblage from the palaeocontinent Siberia is that of Raevskaya et al. (2016). However, as also indicated by Wellman et al. (2013), the global picture is far from being complete. It is evident that data are almost completely lacking for certain areas, and there is currently a concentration of data from Europe, North America, North Africa and the Middle East (Wellman et al., 2013). To sum up, the microfossil record indicates that between the early Middle Ordovician (Dapingian) and the Late Ordovician, cryptospore 9 assemblages, including monads, dyads and tetrads, appear over a broad geographic area and provide the first evidence of land plants. This period was named by Gray (1993) and Kenrick and Crane (1997b) the “eoembryophytic” phase (Fig. 3), characterized by the earliest evidence of liverwort-like plants. Subsequently, with the arrival of isolated spores, including trilete spores, an “eotracheophytic” phase started, with the probable presence of several basal land plant groups such as mosses, hornworts, and early vascular plants. The “eutracheophytic” phase (Fig. 3) is characterized by substantial increase in vascular plant diversity (Kenrick and Crane, 1997b). Strother et al. (2010) proposed an evolutionary scenario for early terrestrialization subdivided in four major phases, each one representing a relative increase in standing global carbon biomass, and marked by the appearance, in the fossil record, of major innovations (Fig. 3). The first was named the “microbial mat landscape”, which was possibly established as early as − 2.2 Ga, even if there is no or little evidence for terrestrial organisms before − 1 Ga. The second step in the evolution of the vegetative landscape is the “thalloid bryophyte landscape,” characterized in the microfossil land plant record by the dominance of cryptospores; the beginning of this phase was controversially placed in Middle Cambrian times by Strother et al. (2010), based on their interpretation of Middle Cambrian cryptospores as representing early bryophytes. The third step of the terrestrialization process involved the evolution of a “tracheophyte landscape” which could possibly start as early as Katian times if the trilete spore assemblage from Saudi Arabia of Steemans et al. (2009) is taken as to track the evolution of tracheophytes. Finally, the terrestrialization of land plants was completed by the rise of the “lignophyte landscape”, marked by the rise of a forested landscape, likely to have taken place by end of Givetian. Recently, Cleal and Cascales-Miñana (2014) described the Rhyniophytic, the Eophytic and the Palaeophytic Floras (Fig. 3), based on the evolution of embryophytes only. It is essential to document in much more detail the cryptospore record of the Cambrian (and possibly Precambrian), to integrate recent discoveries (e.g. Yin et al., 2013) in the evolutionary scenarios of the earliest plants, and to better understand the transition from the algae (e.g. charophytes) to the land plants. In this paper, we propose the term “Proembryophytic” (Fig. 3) to name this very long period of time characterized by the transition from green algae to liverworts. In-depth studies of exquisitely preserved mesofossils from the Silurian–Early Devonian of the Welsh Borderland by, among others, Edwards et al. (1995a, 1996, 1999, 2014, and references therein), Wellman et al. (1998a,b), Wellman (1999), have recently greatly improved our knowledge of the source plants of many of the dispersed spores of that age. It is equally important to establish clear relationships between the Cambrian-Ordovician dispersed spores (cryptospores and miospores) and their mother organisms, in particular with the study of in situ preserved spores in the sporangia of well-preserved algae/ plants, e.g. from Fossillagerstätten. 4. Land plant phylogeny: a Palaeozoic perspective As indicated above, the first period of land plant evolution can only be traced back by the presence of dispersed spores, as macrofossils of land plants only arrived much later in the fossil record. On the other hand, molecular clock data indicate even much earlier origins of the different clades of land plants, at least in the Cambrian, and possible even in the Precambrian. Kenrick et al. (2012) have addressed this discrepancy and showed that it can be partly explained by the variable nature of sedimentary environments during the early Palaeozoic (marine versus terrestrial sedimentation). Kenrick et al. (2012) also suggested that, with respect to calibration of molecular timetrees, accurate placement of fossil constraints and the method used are key issues. In the following section, all embryophyte lineages identified in Fig. 2 are reviewed; their main morphological or anatomical synapomorphies are described and discussed if necessary. The first fossil evidence of each 10 P. Gerrienne et al. / Review of Palaeobotany and Palynology 227 (2016) 4–18 group is identified, and, for extant lineages, the molecular clock ages of crown groups taken from various sources are listed. In this paper dedicated to the terrestrialization process, only the Palaeozoic lineages are considered. Plantae Haeckel, 1866 (= Embryophytes Engler, 1886 or Embryophyceae Lewis and McCourt, 2004 or Embryopsida Pirani and Prado, 2012) Main morphological/anatomical synapomorphies: multicellular gametophyte and sporophyte; multicellular sexual organs (archegonium and antheridium) and sporangium; embryo (early stages of the sporophyte generation surrounded by gametophytic tissue); plant body protected by a cuticle; sporopollenin in the spore wall (Mishler and Churchill, 1984; Kenrick and Crane, 1997a,b; Stevens, 2001; Pirani and Prado, 2012). Demonstrated stratigraphic range: Dapingian (early Middle Ordovivian)–present. The earliest evidence for Embryophytes comes from dispersed palynomorphs (cryptospores). It is still controversial, depending on the definition of cryptospores and on the interpretation of the fossil record (see previous chapter). The earliest unequivocal embryophyte macrofossils is Homerian (late Wenlock, mid-Silurian) specimens of Cooksonia (Edwards and Feehan, 1980; Edwards et al., 1983). Molecular clock age of crown group: – – – – 449–1042 Ma (Clarke et al., 2011). 492.7 (468.6–518.7) Ma (Cooper et al., 2012). 475.34 (471.35–480.35) Ma (Magallón et al., 2013). 529.8 (449.0–629.5) Ma (Zhong et al., 2014). Stomatophytes Kenrick and Crane, 1991 (Anthocerotophytes and Hemitracheophytes) Main morphological/anatomical synapomorphy: stomata (see Stevens, 2001 for an exhaustive list of synapomorphies of extant Stomatophytes). Demonstrated stratigraphic range: Late Silurian–present. The Late Silurian record of Stomatophytes consists of cuticles with stomata (Kenrick et al., 2012). Other evidence is indirect. Katian (Late Ordovician) trilete spores have been taken as proxies for tracheophytes (Steemans et al., 2009). This interpretation is discussed because trilete spores are also produced by some living bryophytes (Edwards et al., 2014; Brown et al., 2015). The Homerian (late Wenlock, mid-Silurian) specimens of Cooksonia (Edwards and Feehan, 1980; Edwards et al., 1983) are the earliest macrofossil evidence of presumable Tracheophytes (but no anatomical data are preserved). Another possible indirect evidence consists of Late Silurian representatives of the spore genus Emphanisporites, with suggested affinities with Anthocerotophytes (Taylor et al., 2011). Molecular clock age of crown group: – – – – 420,4–1024 Ma (Clarke et al., 2011). 484 (452–509) Ma (Cooper et al., 2012). 458,29 (?–?) Ma (Magallón et al., 2013). 487.6 (435.6–550.8) Ma (Zhong et al., 2014). Hemitracheophytes Meeuse 1966 (= Bryopsida and Polysporangiomorpha in Kenrick and Crane, 1997a) Main morphological/anatomical synapomorphies: axial gametophytes with terminal gametangia (basal members); perine layer on spores; persistent and internally differentiated sporophytes; conducting cells in gametophyte and/or sporophyte (Kenrick and Crane, 1997a; Lecointre and Le Guyader, 2006). Demonstrated stratigraphic range: uppermost Ludlow (Late Silurian)– present. The earliest evidence for Tracheophytes (and hence for Polysporangiomorpha and Hemitracheophytes) is the occurrence of in situ tracheids recovered from an unbranched axis of uppermost Ludlow age (Edwards and Davies, 1976; Edwards, 2003). Other evidence is indirect. Katian (Late Ordovician) trilete spores have been taken as proxies for tracheophytes (Steemans et al., 2009). This interpretation is discussed because trilete spores are also produced by some living bryophytes (Edwards et al., 2014; Brown et al., 2015). The Homerian (late Wenlock, mid-Silurian) specimens of Cooksonia (Edwards and Feehan, 1980; Edwards et al., 1983) are the earliest macrofossil evidence of presumable Tracheophytes (but no anatomical data are preserved). Molecular clock age of crown group: – 420,4–1024 Ma (Clarke et al., 2011). – 458,29 (? -?) Ma (Magallón et al., 2013). – 487.6 (435.6–550.8) Ma (Zhong et al., 2014). Polysporangiophytes Kenrick and Crane, 1991 Main morphological/anatomical synapomorphies: multiple sporangia (branched sporophyte); independent gametophytes and sporophytes (Kenrick and Crane, 1997a). Demonstrated stratigraphic range: Homerian–present. The Homerian (late Wenlock, mid-Silurian) specimens of Cooksonia (Edwards and Feehan, 1980; Edwards et al., 1983) are the earliest macrofossil evidence of Polysporangiophytes. Molecular clock age of crown group: – 416–454 Ma (Clarke et al., 2011). – 423.95 (416.28–434.34) Ma (Magallón et al., 2013). – 454.4 (413.6–501.5) Ma (Zhong et al., 2014). Grade: Protracheophytes Kenrick and Crane, 1991 (= non-tracheophyte Polysporangiophytes) Characters: multiple sporangia (branched sporophyte); hydroid- and leptoid-type conducting cells. Demonstrated stratigraphic range: early Pragian/earliest Emsian (Early Devonian), based on the occurrence of Aglaophyton and Horneophyton in the Rhynie chert (Kenrick and Crane, 1997a; Wellman, 2006; Parry et al., 2011, 2013; Mark et al., 2013). Molecular clock age of crown group: fossil group. Tracheophytes sensu Kenrick and Crane, 1991 Main morphological/anatomical synapomorphies: annular-helical thickenings in conducting cells and possibly lignin deposition in the inner wall of conducting cell. Demonstrated stratigraphic range: Late Ludlow (Late Silurian)–present. The earliest evidence for Tracheophytes is the occurrence of in situ tracheids recovered from an unbranched axis of uppermost Ludlow age (Edwards and Davies, 1976; Edwards, 2003). Other evidence is indirect. Katian (Late Ordovician) trilete spores have been taken as proxies for tracheophytes (Steemans et al., 2009). This interpretation is discussed because trilete spores are also produced by some living bryophytes (Edwards et al., 2014; Brown et al., 2015). The Homerian (late Wenlock, mid-Silurian) specimens of Cooksonia (Edwards and Feehan, 1980; Edwards et al., 1983) are the earliest macrofossil evidence of presumable Tracheophytes (but no anatomical data are preserved). Molecular clock age of crown group: – 416–454 Ma (Clarke et al., 2011). – 423.95 (416.28–434.34) Ma (Magallón et al., 2013). – 428.9 (400.1–463.5) Ma (Zhong et al., 2014). Comments: Tracheophytes includes Eutracheophytes, a very large clade comprising all extant vascular plants and many extinct lineages, as well as P. Gerrienne et al. / Review of Palaeobotany and Palynology 227 (2016) 4–18 the very small clade called Paratracheophytes Gerrienne et al., 2006; see below for additional information). The main synapomorphy of the clade is the possession of thickened water conducting cells called tracheids. Tracheids can be of very different structure (Friedman and Cook, 2000), and have been named according to the composition of the internal thickenings. Among the earliest vascular plants, S-type conducting cells are characteristic of Paratracheophytes; C-, G- and P-types are found in basal Eutracheophytes (Kenrick and Crane, 1997a,b; Friedman and Cook, 2000; Edwards, 2003; Edwards et al., 2003). The monophyly of Tracheophytes is most generally accepted (Kenrick and Crane, 1997a; Sperry, 2003), but it has sometimes be questioned (Kenrick and Crane, 1991; Friedman and Cook, 2000; Gerrienne et al., 2006). Paratracheophytes Gerrienne et al., 2006 (= Rhyniaceae sensu Kenrick and Crane, 1991 or Rhyniopsida sensu Kenrick and Crane, 1997a). Main morphological/anatomical synapomorphies: S-type tracheids (conducting cells with helical thickenings and cell wall including a very thin degradation resistant inner layer with micropores and a spongy outer layer); distinctive adventitious branching (Rhynia-type); sporangia attached to a “pad” of tissue (Kenrick and Crane, 1991, 1997a; Kenrick et al., 1991; Friedman and Cook, 2000; Gerrienne et al., 2006). Demonstrated stratigraphic range: early Pragian/earliest Emsian (Early Devonian), based on the occurrence of Rhynia in the Rhynie chert (Kenrick and Crane, 1997a; Wellman, 2006; Parry et al., 2011, 2013; Mark et al., 2013) to Middle Devonian, or possibly earliest Late Devonian, based on the occurrence of cf. Stockmansella langii and “possible rhyniopsids” from Colombian and Venezuelan localities respectively (Berry et al., 2000). Molecular clock age of crown group: fossil group. Comments: This extinct lineage has been successively called Rhyniaceae (Kenrick and Crane, 1991) and Rhyniopsida (Kenrick and Crane, 1997a). It includes the following taxa: Rhynia, Stockmansella and Huvenia (sporophytes), Remyophyton and Sciadophyton (gametophytes), and the morphotypes Sennicaulis hippocrepiformis and Taeniocrada dubia (Gerrienne et al., 2006). Eutracheophytes Kenrick and Crane, 1991 Main morphological/anatomical synapomorphies: thick, lignified inner layer in tracheid wall; pitlets between thickening or within pits in tracheids; sterome (Kenrick and Crane, 1991, 1997a). See Stevens (2001) for a more exhaustive list of synapomorphies of extant Eutracheophytes (= extant Tracheophytes). Demonstrated stratigraphic range: Lochkovian (Early Devonian)–present. The earliest evidence for Eutracheophytes is the occurrence of in situ tracheids recovered from Cooksonia pertoni (Edwards et al., 1992). A further earlier evidence comes from the Homerian (late Wenlock, mid-Silurian) specimens of Cooksonia (Edwards and Feehan, 1980; Edwards et al., 1983), but the specimens were preserved as coalified compressions, and no anatomical data were preserved. Molecular clock age of crown group: – 416–454 Ma (Clarke et al., 2011). – 423.95 (416.28–434.34) Ma (Magallón et al., 2013). – 428.9 (400.1–463.5) Ma (Zhong et al., 2014). Lycophytina sensu Kenrick and Crane, 1997a Main morphological/anatomical synapomorphies: reniform or rounded bivalved sporangium borne on stalk; marked sporangium dorsiventrality; isovalvate dehiscence; exarch xylem differentiation (Kenrick and 11 Crane, 1997a). See Stevens (2001) for a more exhaustive list of synapomorphies of extant Lycophytes. Demonstrated stratigraphic range: late Ludlow (Late Silurian)– present. The earliest evidence of Lycophytina include the late Ludlow representatives of Baragwanathia from Australia (Garratt, 1978, 1981; Garratt et al., 1984; Rickards, 2000) and specimens of Zosterophyllum from Bathurst Island, Arctic Canada (Kotyk et al., 2002). Molecular clock age of crown group: – 416–454 Ma (Clarke et al., 2011). – 423.95 (416.28–434.34) Ma (Magallón et al., 2013). – 428.9 (400.1–463.5) Ma (Zhong et al., 2014). Comments: Lycophytina (Lycophytes) include two lineages (Fig. 2): Zosterophyllopsida are characterized by circinate growth and tworowed sporangial disposition; Lycopsida are characterized, among other features, by microphyll (leaf with a single vein), stellate xylem strand, and a close association between sporangium and microphyll (Kenrick and Crane, 1997a). According to Kenrick and Crane (1997b), the species Cooksonia pertoni Lang, 1937 is a sister group of the lycophytes. Gonez and Gerrienne (2010a) identified the species C. pertoni and C. paranensis (Fig. 4A) as the sister group of the Lycophytina and related taxa such as Uskiella Shute and Edwards (1989), Aberlemnia caledonica (Edwards 1970) Gonez and Gerrienne (2010b; Fig. 4B) and Renalia Gensel (1976; Fig. 4C). The latter is also considered basal to the Lycophytina by Gensel (1992, Fig. 12). Euphyllophytina Kenrick and Crane, 1997a Main morphological/anatomical synapomorphies: pseudomonopodial or monopodial branching pattern; helical arrangement of lateral branching systems (see below) bearing small, pinnule-like vegetative ultimate appendages (non-planate and non-laminate in basal taxa); tracheids with scalariform bordered pits; sporangia borne in pairs grouped into terminal trusses on lateral branching systems; sporangium dehiscence through a single slit along one side (adapted from Kenrick and Crane, 1997a and references therein). See also Stevens (2001) for a more exhaustive list of synapomorphies of extant Euphyllophytes. Demonstrated stratigraphic range: mid-Pragian (Early Devonian)– present. The earliest evidence of Euphyllophytina are specimens of Dawsonites arcuatus Halle (= dispersed fertile lateral branching systems of Psilophyton) from the Brecon Beacons Quarry, Wales (Wellman et al., 1998c). Molecular clock age of crown group: – 388.2–454 Ma (Clarke et al., 2011). – 410.92 (401–422.15) Ma (Magallón et al., 2013). – 404.8 (388.2–429.2) Ma (Zhong et al., 2014). Incertae sedis Euphyllophytina Euphyllophytina (euphyllophytes) include all extant vascular plants, Lycophytina excepted. One of the main synapomorphies of euphyllophytes is the possession of lateral branching systems with ultimate appendages, the whole structure being considered a precursor unit in transformational series ultimately leading to laminated multiveined leaves called megaphylls (Galtier, 2010). Megaphylls are leaves of generally large size, with complex venation and a lamina (Gifford and Foster, 1989; Tomescu, 2009; Galtier, 2010; Corvez et al., 2012). There are several problems with regards to the “megaphyll” character: (i) the identification of leaf key characters in fossils is often hampered by bad preservation or lack of anatomical data; (ii) the earliest euphyllophytes were leafless (Vasco et al., 2013); (iii) the definition of the megaphyll is not consensual (Corvez et al., 2012). It has recently been recognized that megaphylls have evolved independently in several euphyllophyte clades (Galtier, 2010; Corvez et al., 2012), in as many 12 P. Gerrienne et al. / Review of Palaeobotany and Palynology 227 (2016) 4–18 Fig. 4. Interpretative reconstruction of incertae sedis early land plants related to the Lycophytina illustrating their morphological variety. A (modified from Gerrienne et al., 2001) = Cooksonia paranensis; B (modified from Gonez and Gerrienne, 2010b) = Aberlemnia caledonica; C (modified from Gensel, 1976) = Renalia hueberi. Scale bar = 1 cm. as nine different lineages according to Tomescu (2009), and consequently, there might be as many as nine different types of megaphylls. Tomescu (2009) suggested that the term “megaphyll” should be abandoned. Recently, a first step was taken by Corvez et al. (2012), who proposed to use “megaphyll” for lignophyte leaves (adaxial face associated with a lateral meristem; cellular differentiation and tissue maturation basipetal) and “megafrond” for monilophyte leaves (development generally circinate; cellular differentiation and tissue maturation acropetal (Tomescu, 2009; Corvez et al., 2012). Corvez et al. (2012) also noted that the « leaf gap » character, often presented as inherent to the Fig. 5. Interpretative reconstruction of incertae sedis basal euphyllophytes illustrating their morphological variety. Because of the fragmentary nature of these plants, identifying LBS (lateral branching systems) and UA (ultimate appendages) is often difficult. A (modified from Wang et al., 2007) = Wutubulaka multidichotoma Wang et al. (2007) from a late Přidoli (Late Silurian) locality of Xinjiang province (China); B (modified from Hao et al., 2001) = Polythecophyton demissum Hao et al. (2001), from an Early Devonian (Pragian) locality of Yunnan Province (China); C (modified from Gerrienne, 1992) = Foozia minuta Gerrienne (1992), from an Early Emsian (Lower Devonian) locality of Belgium; D (modified from Xiong et al., 2012) = Kunia venusta Xiong et al. (2012), from a late Middle Devonian (Givetian) locality of Yunnan Province (China); E (modified from Wang and Berry, 2001) = Tsaia denticulata Wang and Berry (2001), from a Middle Devonian (Givetian) locality of Yunnan Province (China); F (modified from Wang, 2007) = Tenuisa frasniana Wang (2007), from a Late Devonian (Frasnian) locality of Hunan Province (China). Scale bar = 1 cm. P. Gerrienne et al. / Review of Palaeobotany and Palynology 227 (2016) 4–18 definition of megaphylls, occurs only in ferns whose stelar architecture is more complex than a protostele, leaf gaps being absent in all lignophytes. Most Devonian euphyllophytes possess lateral branching systems (LBS) bearing generally small dichotomous structures called ultimate appendages (UA). The earliest record of LBS might date back to the Late Silurian Period in plants such as Wutubulaka (Wang et al., 2007; Fig. 5A), where presumably unequal divisions of the apical meristem resulted in anisotomous divisions of the main stem of the plant (the socalled pseudomonopodial habit), resulting in the individualization of LBS. Within Devonian representatives of the euphyllophytes, laminated multiveined leaves are only recorded (i) in the basalmost euphyllophyte Eophyllopyton (Hao, 1988; Hao and Beck, 1993; Hao et al., 2003, and (ii) in a few lineages of basal lignophytes including Archaeopteridales (Galtier, 2010) and early seed plants (the leaf of Elkinsia is described as frond bearing laminated pinnules; Serbet and Rothwell, 1992), and maybe in Sphenophyllales (Rotafolia; Wang et al., 2005). The earliest best known euphyllophyte genus is Psilophyton Dawson, which includes at least 12 valid species (Gerrienne, 1995, 1997). The range of morphologies displayed by the various species suggests that the concept of the genus should be clarified (Wang and Berry, 2001). Psilophyton has long been included in the subdivision Trimerophytina (Banks, 1968, 1975), but the latter has been shown by Crane (1990) and Kenrick and Crane (1997a) to be paraphyletic and should not be used anymore. Most other earliest euphyllophytes have, up to now, never been taken into consideration in any phylogenetic analysis. They are left in open nomenclature and called “basal euphyllophyte” or “incertae sedis euphyllophyte”. However, they show a wide range of morphological variations and their inclusion in phylogenetic studies would probably deeply change the topology of the euphyllophyte tree. This informal “basal euphyllophyte” group may include plants that are ancestral either to the lignophytes, or to the monilophytes. It might also include representatives of still unrecognized, extinct clades of euphyllophytes. In order to illustrate their various morphologies, several incertae sedis Late Silurian/Devonian plants of euphyllophytic affinities are presented at Fig. 5. All possess LBS and/or UA, the distinction between these two structural units being sometimes controversial because of the fragmentary nature of these plants, and/or because of different interpretations. The various LBS displayed by all the plants at Fig. 5 are possibly not homologous to each other. Monilophytes Pryer et al. (2004) (= Moniliformopses Kenrick and Crane, 1997a) Main morphological/anatomical synapomorphies: in basal members, mesarch protoxylem strands confined to lobes of xylem strand (Kenrick and Crane, 1997a). Demonstrated stratigraphic range: Givetian (late Middle Devonian)– present. The earliest evidence of the Monilophytes crown group comes from specimens of Ibyka (Iridopteridales—see below) from New York State (Skog and Banks, 1973). Molecular clock age of crown group: – 388.2–454 Ma (Clarke et al., 2011). – 392.31 (384.77–400.57) Ma (Magallón et al., 2013). – 368.5 (354.0–390.7) Ma (Zhong et al., 2014). Comments: Extant monilophytes (ferns sensu lato) includes five major lineages: ophioglossoid ferns (Ophioglossales), whisk ferns (Psilotales), marattioid ferns (Marattiales), leptosporangiate ferns (Polypodiales) and horsetails (Equisetopsida) (Pryer et al., 2001). Devonian monilophytes are represented by the extinct Cladoxylopsida, the Equisetopsida, the 13 Iridopteridales, the Rhacophytales and the genus Gillespiea Erwin and Rothwell, 1989 (Stauropteridales). Cladoxylopsida are characterized by a complex vascular system dissected in numerous vascular strands; they lack laminated leaves (Meyer-Berthaud and Decombeix, 2007, 2009). Pseudosporochnalean cladoxylopsids extend from the Middle Devonian (Eifelian) to the Frasnian (Meyer-Berthaud et al., 2007); this informal group includes the earliest arborescent plants of Earth history, namely Pseudosporochnus (Berry and Fairon-Demaret, 2002), Eospermatopteris/Wattieza (Stein et al., 2007, 2012) and Calamophyton/Duisbergia (Giesen and Berry, 2013). Nonpseudosporochnalean cladoxylopsids range from the Middle Devonian to the Mississippian (Meyer-Berthaud et al., 2007). They are distinguished from pseudosporochnalean cladoxylopsids by a range of characters including the presence of bilateral first-order branches and several anatomical features (see detailed account in Meyer-Berthaud et al., 2007). The affinities of Cladoxylopsida are still discussed, but they are generally considered basal ferns s.l. (Meyer-Berthaud and Decombeix, 2007, 2009). Iridopteridales range from the Middle to the Late Devonian, and maybe to the Mississippian (Meyer-Berthaud et al., 2007). The main characteristics of the lineage, sometimes considered possible basal Equisetopsida (Berry and Stein, 2000) include (i) a deeply ribbed stele including peripheral permanent protoxylem strands; (ii) an iterative branching pattern with a whorled arrangement of the laterals (Berry and Stein, 2000; Cordi and Stein, 2005; Meyer-Berthaud et al., 2007). The taxonomic position of the Rhacophytales and the Stauropteridales is still unclear. Both orders are generally considered as being early fernlike plants. They are characterized by biseriate/quadriseriate lateral branching systems, which bear non-laminated ultimate appendages (Taylor et al., 2009; Corvez et al., 2012). The monilophyte clade was identified by Kenrick and Crane (1997a) on the basis of a limited number of fossil taxa. Subsequently, various studies have repeatedly identified extant monilophytes as a monophyletic lineage sister to seed plants (Nickrent et al., 2000; Renzaglia et al., 2000, 2002; Pryer et al., 2001, 2004). However, Rothwell (1999) and Rothwell and Nixon (2006) have demonstrated that the inclusion of a large number of fossil taxa alter the tree topology; in these studies, monilophytes were resolved as a polyphyletic assemblage. Lignophytes Crane, 1985 Main morphological/anatomical synapomorphies: in early members, bifacial vascular cambium producing secondary xylem inwards and secondary phloem outwards (Crane, 1985). The character is lost in many members of the angiosperm lineage. Demonstrated stratigraphic range: Givetian (late Middle Devonian)– present. The earliest evidence of lignophytes comes from permineralized specimens of Rellimia from New York State (Dannenhoffer and Bonamo, 1989). Molecular clock age of crown group: – 306.2–366.8 Ma (Clarke et al., 2011). – 330.33 (313.74–351.04) Ma (Magallón et al., 2013). – 315.8 (306.2–333.2) Ma or 317.5 (306.2–339.4) Ma (Zhong et al., 2014). Comments: Vascular cambium evolved in several lineages: in Lycopsida (Givetian, late Middle Devonian; Cai and Li, 1996), basal euphyllophytes (Pragian–Emsian, Early Devonian; Gerrienne et al., 2011; Hoffman and Tomescu, 2013), in Cladoxylopsida (Frasnian, early Late Devonian; Meyer-Berthaud et al., 2004), in basal ferns (Famennian, late Late Devonian; Leclercq, 1951) and in Equisetopsida (uppermost Devonian/ lowermost Pennsylvanian; Mamay and Bateman, 1991). In all these lineages, the vascular cambium is unifacial, producing only secondary 14 P. Gerrienne et al. / Review of Palaeobotany and Palynology 227 (2016) 4–18 xylem. Bifacial vascular cambium evolved only once, in lignophytes (with the notable exception of its presence in the monilophyte genus Sphenophyllum; Eggert and Gaunt, 1973; Cichan and Taylor, 1982). Lignophytes include the free-sporing progymnospermes, the Stenokoleales (an extinct lineage known from permineralizations only; Momont et al., 2016–in this issue) and the seed plants (Spermatophytes; see below). Progymnosperms (see Taylor et al., 2009 for a detailed account) include several orders among which the isosporous, protostelic Aneurophytales and the heterosporous, eustelic Archaeopteridales. Spermatophytes (= Spermatophytata sensu Kenrick and Crane, 1997a) Main morphological/anatomical synapomorphies: single megaspore per megasporangium; integumented megasporangium. Demonstrated stratigraphic range: Famennian (late Late Devonian)– present. The earliest unequivocal evidence of seed plants is represented by specimens of Moresnetia from Belgium (Stockmans, 1948; Fairon-Demaret and Scheckler, 1987). Molecular clock age of crown group: – 306.2–366.8 Ma (Clarke et al., 2011). – 330.33 (313.74–351.04) Ma (Magallón et al., 2013). – 315.8 (306.2–333.2) Ma or 317.5 (306.2–339.4) Ma (Zhong et al., 2014). Comments: The Middle Devonian proto-ovule Runcaria heinzelinii Stockmans emend. Gerrienne and Meyer-Berthaud, 2007 has been described as a precursor of seed plants (Gerrienne et al., 2004). 5. Conclusions and perspectives In the present paper, we attempt to provide a stratigraphical frame and the phylogenetic context of the evolution of early land plants, and the timing of the terrestrialization of the land plants during the Early and Middle Palaeozoic. It appears today that there have been several independent transitions to land, one of which led to the embryophytes. However, the precise transition from algae to embryophytic plants is not yet fully understood. First definite macrofossil evidence of land plants is present in the Late Ordovician, but the dispersed spores, often also named cryptospores, indicate the presence of land plants already during mid-Ordovician times. Embryophyte-related cryptospores are indeed known since the Middle Ordovician, but there are possibly also older occurrences, such as in the Cambrian, with microfossils that cannot definitely be related to land plants, however. The literature review shows that there is an ongoing debate about the definition of the term cryptospores, but most importantly about the biological affinities of these microfossils that possibly or probably derived from early land plants. Recent studies have already revealed the source plants of a wide range of dispersed Silurian–Early Devonian spores, including cryptospores (Edwards et al., 2014, and references therein), but the affinities of these mother organisms remain sometimes unclear. Future research should therefore aim at elucidating the phylogenetic interrelationships of the basal streptophytes/embryophytes and at establishing links between the Cambrian-Ordovician dispersed spores and their source organisms. This can be realized with the investigation of in situ preserved sporangia in exceptionally preserved fossils, e.g. from Fossillagerstätten. Although the first macrofossil evidence of definite land plants is in the Silurian and that of definite land plant derived spores in the Ordovician, molecular clock data indicate that the different clades of Palaeozoic land plants evolved and diversified probably much earlier, mostly during the Cambrian and Ordovician, but possibly also earlier. There is today a general consensus that land plants had already a global distribution by the end of the Ordovician, and that the oldest land plant derived spores probably are those from Gondwana. It would thus be important to look out for the first macrofossils of land plants in the Middle or Upper Ordovician of Gondwana. The plant macrofossil record clearly indicates that embryophytes experienced a major adaptive radiation event during the Late Silurian and the first half of the Devonian: at the end of the Middle Devonian, all major clades of living plants are already represented. Since the pioneering studies of Banks (1968, 1975), and, more recently of Kenrick and Crane (1997a) and Hilton and Bateman (2006), no comprehensive studies have been undertaken in order to evaluate the phylogenetic relationship of Devonian plants on a global scale. A notable exception is the work of Hao and Xue (2013), but the latter was centred on Early Devonian floras from South China. The phylogenies that have been reconstructed so far show that the evolutionary relationships between all those clades are however still highly controversial, especially when fossil taxa are included in the analyses. Moreover, a large number of fossil taxa have never been included in any phylogenetic treatment because they are insufficiently known. As a result, the affinities of a large proportion of Devonian plant taxa are still unresolved. In the coming years, the elaboration of comprehensive, collaborative databases, at a worldwide scale, might be essential in order to elucidate the Silurian/ Devonian diversification of embryophytes. Acknowledgments This paper is the result of numerous discussions among the authors in the frame of the ANR TERRES project. We acknowledge the financial help through this project (ANR-10-BLAN-0607) and the valuable comments of the project leader, Brigitte Meyer-Berthaud (Montpellier) and of an anonymous reviewer, but also those of numerous colleagues, including Cyrille Prestianni (Bruxelles), Borja Cascales-Miñana (Liège), Paul Strother (Boston), and Charles Wellman (Sheffield). MV thanks Saudi Aramco for permission to publish. PG is a F.R.S.-FNRS Senior Research Associate. References Adl, S.M., Simpson, A.G.B., Lane, C.E., Lukeš, J., Bass, D., Bowser, S.S., Brown, M.W., Burki, F., Dunthorn, M., Hampl, V., Heiss, A., Hoppenrath, M., Lara, E., le Gall, L., Lynn, D.H., McManus, H., Mitchell, E.A.D., Mozley-Stanridge, S.E., Parfrey, L.W., Pawlowski, J., Rueckert, S., Shadwick, L., Schoch, C.L., Smirnov, A., Spiegel, F.W., 2012. The revised classification of eukaryotes. J. Eukaryot. Microbiol. 59, 429–514. Badawy, A.S., Mehlqvist, K., Vajda, V., Ahlberg, P., Calner, M., 2014. Late Ordovician (Katian) spores in Sweden: oldest land plant remains from Baltica. GFF 136 (1), 16–21. Banks, H.P., 1968. The Early History of Land Plants. In: Drake, E. (Ed.), Evolution and Environment: A Symposium Presented on the One Hundredth Anniversary of the Foundation of Peabody Museum of Natural History at Yale University. Yale University Press, New Haven, CT, pp. 73–107. Banks, H.P., 1975. Reclassification of Psilophyta. Taxon 24 (4), 401–413. Baschnagel, R.A., 1966. New fossil algae from the Middle Devonian of New York. Trans. Am. Microsc. Soc. 85, 297–302. Bergström, S.M., Chen, Xu, Gutiérrez-Marco, J.C., Dronov, A., 2009. The new chronostratigraphic classification of the Ordovician system and its relations to major series and stages and to δ13C chemostratigraphy. Lethaia 42, 97–107. Berner, R.A., Kothavala, Z., 2001. GEOCARB III: a revised model of atmospheric CO2 over Phanerozoic time. Am. J. Sci. 301, 182–204. Berry, C.M., Fairon-Demaret, M., 2002. The architecture of Pseudosporochnus nodosus Leclercq et Banks: a Middle Devonian cladoxylopsid from Belgium. Int. J. Plant Sci. 163 (5), 699–713. Berry, C.M., Stein, W.E., 2000. A new iridopteridalean from the Devonian of Venezuela. Int. J. Plant Sci. 161 (5), 807–827. Berry, C.M., Morel, E., Mojica, J., Villarroel, C., 2000. Devonian plants from Colombia, with discussion of their geological and palaeogeographical context. Geol. Mag. 137 (03), 257–268. Bidartondo, M.I., Read, D.J., Trappe, J.M., Merckx, V., Ligrone, R., Duckett, J.G., 2011. The dawn of symbiosis between plants and fungi. Biol. Lett. 7 (4), 574–577. Bower, F.O., 1890. On antithetic as distinct from homologous alternation of generations in plants. Ann. Bot. 4, 347–370. Bowman, J.L., 2013. Walkabout on the long branches of plant evolution. Curr. Opin. Plant Biol. 16 (1), 70–77. Brown, R.C., Lemmon, B.E., Shimamura, M., Villarreal, J.C., Renzaglia, K.S., 2015. Spores of relictual bryophytes: diverse adaptations to life on land. Rev. Palaeobot. Palynol. 216, 1–17. P. Gerrienne et al. / Review of Palaeobotany and Palynology 227 (2016) 4–18 Cai, C.Y., Li, C.S., 1996. On a Chinese Givetian lycopod, Longostachys latisporophyllus Zhu, Hu and Feng, emend.: its morphology, anatomy and reconstruction. Palaeontographica B238, 1–43. Cascales-Miñana, B., Meyer-Berthaud, B., 2014. Diversity dynamics of Zosterophyllopsida. Lethaia 47 (2), 205–215. Cascales-Miñana, B., Meyer-Berthaud, B., 2015. Diversity patterns of the vascular plant group Zosterophyllopsida in relation to Devonian paleogeography. Palaeogeogr. Palaeoclimatol. Palaeoecol. 423, 53–61. Cichan, M.A., Taylor, T.N., 1982. Vascular cambium development in Sphenophyllum: a Carboniferous arthrophyte. IAWA Bull. 3, 155–160. Clarke, J.T., Warnock, R., Donoghue, P.C., 2011. Establishing a time-scale for plant evolution. New Phytol. 192 (1), 266–301. Cleal, C.J., Cascales-Miñana, B., 2014. Composition and dynamics of the great Phanerozoic evolutionary floras. Lethaia 47 (4), 469–484. Cohen, K.M., Finney, S.C., Gibbard, P.L., Fan, J.X., 2013. The ICS international chronostratigraphic chart. Episodes 36 (3), 199–204 (Updated). Colbath, K., Grenfell, H.R., 1995. Review of biological affinities of Paleozoic acid resistant organic-walled eukaryotic algal micro-fossils (including “acritarchs”). Rev. Palaeobot. Palynol. 86, 287–314. Combaz, A., 1967. Sur un microbios d'âge Trémadocien à Hassi-Messaoud. Actes de la Société Linéenne de Bordeaux, vol. sp. Congrès AFAS, pp. 115–119. Conkin, J.E., Conkin, B.M., 1992. Late Silurian (Ludlovian) charophyte Moellerina laufeldi n.sp., from the Hamra beds of the Isle of Gotland, Sweden. Notes in Paleontology and Stratigraphy J. University of Louisville, pp. 1–15. Cooper, E.D., Henwood, M.J., Brown, E.A., 2012. Are the liverworts really that old? Cretaceous origins and Cenozoic diversifications in Lepidoziaceae reflect a recurrent theme in liverwort evolution. Biol. J. Linn. Soc. 107 (2), 425–441. Cordi, J., Stein, W.E., 2005. The anatomy of Rotoxylon dawsonii comb. nov. (Cladoxylon dawsonii) from the Upper Devonian of New York State. Int. J. Plant Sci. 166 (6), 1029–1045. Corenblit, D., Davies, N.S., Steiger, J., Gibling, M.R., Bornette, G., 2015. Considering river structure and stability in the light of evolution: feedbacks between riparian vegetation and hydrogeomorphology. Earth Surf. Process. Landf. 40, 189–207. Corvez, A., Barriel, V., Dubuisson, J.Y., 2012. Diversity and evolution of the megaphyll in Euphyllophytes: phylogenetic hypotheses and the problem of foliar organ definition. C. R. Palevol 11 (6), 403–418. Cox, C.J., Li, B., Foster, P.G., Embley, T.M., Civáň, P., 2014. Conflicting phylogenies for early land plants are caused by composition biases among synonymous substitutions. Syst. Biol. 63 (2), 272–279. Crane, P.R., 1985. Phylogenetic analysis of seed plants and the origin of angiosperms. Ann. Mo. Bot. Gard. 72, 716–793. Crane, P.R., 1990. The phylogenetic context of microsporogenesis. In: Blackmore, S., Knox, R.B. (Eds.), Microspores: Evolution and Ontogeny. Academic Press, London, pp. 11–41. Crane, P.R., Herendeen, P., Friis, E.M., 2004. Fossils and plant phylogeny. Am. J. Bot. 91 (10), 1683–1699. Dannenhoffer, J.M., Bonamo, P.M., 1989. Rellimia thomsonii from the Givetian of New York: secondary growth in three orders of branching. Am. J. Bot. 76, 1312–1325. Delaux, P.M., Nanda, A.K., Mathé, C., Sejalon-Delmas, N., Dunand, C., 2012. Molecular and biochemical aspects of plant terrestrialization. Perspect. Plant Ecol. Evol. Syst. 14 (1), 49–59. Edwards, D., 2003. Xylem in early tracheophytes. Plant Cell Environ. 26 (1), 57–72. Edwards, D., Davies, E.C.W., 1976. Oldest recorded in situ tracheids. Nature 263, 494–495. Edwards, D., Feehan, J., 1980. Records of Cooksonia-type sporangia from late Wenlock strata in Ireland. Nature 287, 41–42. Edwards, D., Kenrick, P., 2015. The early evolution of land plants, from fossils to genomics: a commentary on Lang (1937) ‘On the plant-remains from the Downtonian of England and Wales'. Philos. Trans. R. Soc. Lond. B Biol. Sci. 370 (1666), 20140343. Edwards, D., Richardson, J.B., 2004. Silurian and Lower Devonian plant assemblages from the Anglo-Welsh Basin: a palaeobotanical and palynological synthesis. Geol. J. 39 (3– 4), 375–402. Edwards, D., Feehan, J., Smith, D.G., 1983. A late Wenlock flora from Co. Tipperary, Ireland. Bot. J. Linn. Soc. 86, 19–36. Edwards, D., Davies, K.L., Axe, L., 1992. A vascular conducting strand in the early land plant Cooksonia. Nature 357, 683–685. Edwards, D., Davies, K.L., Richardson, J.B., Axe, L., 1995a. The ultrastructure of spores of Cooksonia pertoni. Palaeontology 38, 153–168. Edwards, D., Duckett, J.G., Richardson, J.B., 1995b. Hepatic characters in the earliest land plants. Nature 374, 635–636. Edwards, D., Davies, K.L., Richardson, J.B., Wellman, C.H., Axe, L., 1996. Ultrastructure of Synorisporites downtonensis and Retusotriletes cf. coronadus in spore masses from the Pridoli of the Welsh Borderland. Palaeontology 39, 783–800. Edwards, D., Wellman, C.H., Axe, L., 1999. Tetrads in sporangia and spore masses from the Upper Silurian and Lower Devonian of the Welsh Borderland. Bot. J. Linn. Soc. 130, 111–156. Edwards, D., Axe, L., Duckett, J.G., 2003. Diversity in conducting cells in early land plants and comparisons with extant bryophytes. Bot. J. Linn. Soc. 141 (3), 297–347. Edwards, D., Morris, J.L., Richardson, J.B., Kenrick, P., 2014. Cryptospores and cryptophytes reveal hidden diversity in early land floras. New Phytol. 202, 50–78. Eggert, D.A., Gaunt, D.D., 1973. Phloem of Sphenophyllum. Am. J. Bot. 60, 755–770. Engler, A., 1886. Fuhrer Durch Den Koniglichen Botanischen Garten Der Universitat Zu Breslau, Breslau. Erwin, D.H., Rothwell, G.W., 1989. Gillespiea randolphensis gen. et sp. nov.(Stauropteridales), from the Upper Devonian of West Virginia. Rev. Can. J. Bot. 67, 3063–3077. Evitt, W.R., 1963. A discussion and proposals concerning fossil dinoflagellates, hystrichospheres and acritarchs, II. Proc. Natl. Acad. Sci. 49, 298–302. 15 Fairon-Demaret, M., Scheckler, S.E., 1987. Typification and redescription of Moresnetia zalesskyi Stockmans, 1948, an early seed plant from the Upper Famennian of Belgium. Bull. Inst. R. Sci. Nat. Belg. Sci. Terre 57, 183–199. Feist, M., Liu, J., Tafforeau, P., 2005. New insights into Paleozoic charophyte morphology and phylogeny. Am. J. Bot. 92 (7), 1152–1160. Finet, C., Timme, R.E., Delwiche, C.F., Marlétaz, F., 2010. Multigene phylogeny of the green lineage reveals the origin and diversification of land plants. Curr. Biol. 20 (24), 2217–2222. Foster, C.B., Williams, G.E., 1991. Late Ordovician–Early Silurian age for the Mallowa Salt of the Carribuddy Group, Canning Basin, Western Australia, based on occurrences of Tetrahedraletes medinensis Strother and Traverse 1979. Aust. J. Earth Sci. 38, 223–228. Friedman, W.E., Cook, M.E., 2000. The origin and early evolution of tracheids in vascular plants: integration of palaeobotanical and neobotanical data. Philos. Trans. R. Soc. Lond. B Biol. Sci. 355 (1398), 857–868. Galtier, J., 2010. The origins and early evolution of the megaphyllous leaf. Int. J. Plant Sci. 171 (6), 641–661. Garratt, M.J., 1978. New evidence for a Silurian (Ludlow) age for the earliest Baragwanathia flora. Alcheringa 2 (3), 217–224. Garratt, M.J., 1981. The earliest vascular land plants: comment on the age of the oldest Baragwanathia flora. Lethaia 14 (1), 8. Garratt, M.J., Tims, J.D., Rickards, R.B., Chambers, T.C., Douglas, J.G., 1984. The appearance of Baragwanathia (Lycophytina) in the Silurian. Bot. J. Linn. Soc. 89 (4), 355–358. Gensel, P.G., 1976. Renalia hueberi, a new plant from the Lower Devonian of Gaspé. Rev. Palaeobot. Palynol. 22 (1), 19–37. Gensel, P.G., 1992. Phylogenetic relationships of the zosterophylls and lycopsids: evidence from morphology, paleoecology, and cladistic methods of inference. Ann. Mo. Bot. Gard. 79, 450–473. Gensel, P.G., 2008. The earliest land plants. Annu. Rev. Ecol. Evol. Syst. 39, 459–477. Gerrienne, P., 1992. The Emsian plants from Fooz-Wépion (Belgium). III. Foozia minuta gen. et spec. nov., a new taxon with probable cladoxylalean affinities. Rev. Palaeobot. Palynol. 74 (1), 139–157. Gerrienne, P., 1995. Les fossiles végétaux du Dévonien inférieur de Marchin (bord nord du Synclinorium de Dinant, Belgique). III. Psilophyton parvulum nov. sp. Geobios 28 (2), 131–144. Gerrienne, P., 1997. The fossil plants from the Lower Devonian of Marchin (northern margin of Dinant Synclinorium, Belgium). V. Psilophyton genseliae sp. nov., with hypotheses on the origin of Trimerophytina. Rev. Palaeobot. Palynol. 98 (3), 303–324. Gerrienne, P., Gonez, P., 2011. Early evolution of life cycles in embryophytes: a focus on the fossil evidence of gametophyte/sporophyte size and morphological complexity. J. Syst. Evol. 49 (1), 1–16. Gerrienne, P., Meyer-Berthaud, B., 2007. The proto-ovule Runcaria heinzelinii Stockmans 1968 emend. Gerrienne et al., 2004 (mid-Givetian, Belgium): concept and epitypification. Rev. Palaeobot. Palynol. 145 (3), 321–323. Gerrienne, P., Bergamaschi, S., Pereira, E., Rodrigues, M.A.C., Steemans, P., 2001. An Early Devonian flora, including Cooksonia, from the Paraná Basin (Brazil). Rev. Palaeobot. Palynol. 116 (1), 19–38. Gerrienne, P., Meyer-Berthaud, B., Fairon-Demaret, M., Streel, M., Steemans, P., 2004. Runcaria, a Middle Devonian seed plant precursor. Science 306 (5697), 856–858. Gerrienne, P., Dilcher, D.L., Bergamaschi, S., Milagres, I., Pereira, E., Rodrigues, M.A.C., 2006. An exceptional specimen of the early land plant Cooksonia paranensis, and a hypothesis on the life cycle of the earliest eutracheophytes. Rev. Palaeobot. Palynol. 142 (3), 123–130. Gerrienne, P., Gensel, P.G., Strullu-Derrien, C., Lardeux, H., Steemans, P., Prestianni, C., 2011. A simple type of wood in two Early Devonian plants. Science 333 (6044), 837. Gibling, M.R., Davies, N.S., 2012. Palaeozoic landscapes shaped by plant evolution. Nat. Geosci. 5, 99–105. Gibling, M.R., Davies, N.S., Falcon-Lang, H.J., Bashforth, A.R., DiMichele, W.A., Rygel, M.C., Ielpi, A., 2013. Palaeozoic co-evolution of rivers and vegetation: a synthesis of current knowledge. Proc. Geol. Assoc. 12, 524–553. Giesen, P., Berry, C.M., 2013. Reconstruction and growth of the early tree Calamophyton (Pseudosporochnales, Cladoxylopsida) based on exceptionally complete specimens from Lindlar, Germany (mid-Devonian): organic connection of Calamophyton branches and Duisbergia trunks. Int. J. Plant Sci. 174 (4), 665–686. Gifford, E.M., Foster, A.S., 1989. Morphology and Evolution of Vascular Plants. third ed. Freeman, New York. Gonez, P., Gerrienne, P., 2010a. A new definition and a lectotypification of the genus Cooksonia Lang 1937. Int. J. Plant Sci. 171 (2), 199–215. Gonez, P., Gerrienne, P., 2010b. Aberlemnia caledonica gen. et comb. nov., a new name for Cooksonia caledonica Edwards 1970. Rev. Palaeobot. Palynol. 163 (1), 64–72. Graham, L., Lewis, L.A., Taylor, W., Wellman, C., Cook, M., 2014. Early terrestrialization: transition from algal to bryophyte grade. In: Hanson, D.T., Rice, S.K. (Eds.), Photosynthesis in Bryophytes and Early Land PlantsAdvances in Photosynthesis and Respiration 37. Springer, Netherlands, Dordrecht, pp. 9–28. Gray, J., 1985. The microfossil record of early land plants: advances in understanding of early terrestrialization. 1970–1984. In: Chaloner, W.G., Lawson, J.D. (Eds.), Evolution and Environment in the Late Silurian and Early Devonian. Philosophical Transactions of the Royal Society, London, pp. 167–195. Gray, J., 1988. Land plants spores and the Ordovician–Silurian boundary. Bull. Br. Mus. Nat. Hist. Geol. 43, 351–358. Gray, J., 1991. Tetrahedraletes, Nodospora and the ‘cross’ tetrad: an accretion of myth. In: Blackmore, S., Barnes, S. (Eds.), Pollen and Spores: Patterns of DiversificationThe Systematics Association Special Volume. Clarendon Press, Oxford, pp. 49–87. Gray, J., 1993. Major Paleozoic land plant evolutionary bio-events. Palaeogeogr. Palaeoclimatol. Palaeoecol. 104 (1), 153–169. 16 P. Gerrienne et al. / Review of Palaeobotany and Palynology 227 (2016) 4–18 Gray, J., Boucot, A.J., 1971. Early Silurian spore tetrads from New York: earliest New World evidence for vascular plants. Science 173, 918–921. Gray, J., Massa, D., Boucot, A.J., 1982. Caradocian land plants microfossils from Libya. Geology 10, 197–201. Haig, D., 2008. Homologous versus antithetic alternation of generations and the origin of sporophytes. Bot. Rev. 74 (3), 395–418. Haig, D., 2015. Coleochaete and the origin of sporophytes. Am. J. Bot. 102 (3), 417–422. Hao, S.G., 1988. A new Lower Devonian genus from Yunnan, with notes on the origin of the leaf. Acta Botanica Sinica 30, 441–448 (in Chinese). Hao, S.G., Beck, C.B., 1993. Further observations on Eophyllophyton bellum from the lower Devonian (Siegenian) of Yunnan, China. Palaeontographica B230 (1–6), 27–41. Hao, S.G., Xue, J., 2013. The Early Devonian Posongchong Flora of Yunnan: a Contribution to an Understanding of the Evolution and Early Diversification of Vascular Plants. Science Press, Beijing. Hao, S.G., Gensel, P.G., Wang, D.M., 2001. Polythecophyton demissum, gen. et sp. nov., a new plant from the Lower Devonian (Pragian) of Yunnan, China and its phytogeographic significance. Rev. Palaeobot. Palynol. 116 (1), 55–71. Hao, S.G., Beck, C.B., Wang, D.M., 2003. Structure of the earliest leaves: adaptations to high concentrations of atmospheric CO2. Int. J. Plant Sci. 164, 71–75. Hilton, J., Bateman, R.M., 2006. Pteridosperms are the backbone of seed–plant phylogeny. J. Torrey Bot. Soc. 133 (1), 119–168. Hoffman, L.A., Tomescu, A.M., 2013. An early origin of secondary growth: Franhueberia gerriennei gen. et sp. nov. from the Lower Devonian of Gaspé (Quebec, Canada). Am. J. Bot. 100 (4), 754–763. Hoffmeister, W.S., 1959. Lower Silurian plant spores from Libya. Micropaleontology 5, 331–334. Jobson, R.W., Qiu, Y.L., 2011. Amino acid compositional shifts during streptophyte transitions to terrestrial habitats. J. Mol. Evol. 72 (2), 204–214. Karol, K.G., McCourt, R.M., Cimino, M.T., Delwiche, C.F., 2001. The closest living relatives of land plants. Science 294 (5550), 2351–2353. Karol, K.G., Arumuganathan, K., Boore, J.L., Duffy, A.M., Everett, K.D.E., Hall, J.D., Hansen, S.K., Kuehl, J.V., Mandoli, D.F., Mishler, B.D., Olmstead, R.G., Renzaglia, K.S., Wolf, P.G., 2010. Complete plastome sequences of Equisetum arvense and Isoetes flaccida: implications for phylogeny and plastid genome evolution of early land plant lineages. BMC Evol. Biol. 10 (1), 321. Kenrick, P., Crane, P.R., 1991. Water-conducting cells in early fossil land plants: implications for the early evolution of tracheophytes. Bot. Gaz. 152 (3), 335–356. Kenrick, P., Crane, P.R., 1997a. The Origin and Early Diversification of Land Plants. A Cladistic Study vol. 560. Smithsonian Institute Press, Washington DC. Kenrick, P., Crane, P.R., 1997b. The origin and early evolution of plants on land. Nature 389 (6646), 33–39. Kenrick, P., Strullu-Derrien, C., 2014. The origin and early evolution of roots. Plant Physiol. 166 (2), 570–580. Kenrick, P., Remy, W., Crane, P.R., 1991. The structure of water conducting cells in the enigmatic early land plants Stockmansella langii Fairon-Demaret, Huvenia kleui Hass et Remy and Sciadophyton sp. Remy et al. 1980. Argum. Palaeobot. 8, 179–191. Kenrick, P., Wellman, C.H., Schneider, H., Edgecombe, G.D., 2012. A timeline for terrestrialization: consequences for the carbon cycle in the Palaeozoic. Philos. Trans. R. Soc. Lond. B Biol. Sci. 367 (1588), 519–536. Kotyk, M.E., Basinger, J.F., Gensel, P.G., de Freitas, T.A., 2002. Morphologically complex plant macrofossils from the Late Silurian of Arctic Canada. Am. J. Bot. 89 (6), 1004–1013. Lang, W.H., 1937. On the plant-remains from the Downtonian of England and Wales. Philos. Trans. R. Soc. Lond. B Biol. Sci. 227 (544), 245–291. Leclercq, S., 1951. Étude morphologique et anatomique d'une fougère du Dévonien supérieur, le Rhacophyton zygopteroides nov. sp. Annales de la Société géologique de Belgique, Mém. in 4° IX, pp. 5–62. Lecointre, G., Le Guyader, H., 2006. The Tree of Life: a Phylogenetic Classification. The Belknap Press of Harvard University Press, Cambridge, MA. Leliaert, F., Smith, D.R., Moreau, H., Herron, M.D., Verbruggen, H., Delwiche, C.F., De Clerck, O., 2012. Phylogeny and molecular evolution of the green algae. Crit. Rev. Plant Sci. 31 (1), 1–46. Lewis, L.A., McCourt, R.M., 2004. Green algae and the origin of land plants. Am. J. Bot. 91 (10), 1535–1556. Magallón, S., Hilu, K.W., Quandt, D., 2013. Land plant evolutionary timeline: gene effects are secondary to fossil constraints in relaxed clock estimation of age and substitution rates. Am. J. Bot. 100 (3), 556–573. Mamay, S., Bateman, R., 1991. Archaeocalamites lazarii, sp. nov.: the range of Archaeocalamitaceae extended from the lowermost Pennsylvanian to the midlower Permian. Am. J. Bot. 78 (4), 489–496. Mark, D.F., Rice, C.M., Trewin, N.H., 2013. Discussion on ‘A high-precision U–Pb age constraint on the Rhynie Chert Konservat-Lagerstätte: time scale and other implications’ journal, vol. 168, 863–872. J. Geol. Soc. 170, 701–703. McCourt, R.M., Delwiche, C.F., Karol, K.G., 2004. Charophyte algae and land plant origins. Trends Ecol. Evol. 19 (12), 661–666. Meeuse, A.D.J., 1966. The early evolution of the Archegoniatae: a re-appraisal. Acta Bot. Neerl. 15 (1), 162–177. Meyer-Berthaud, B., Decombeix, A.L., 2007. A tree without leaves. Nature 446, 861–862. Meyer-Berthaud, B., Decombeix, A.L., 2009. Evolution of Earliest Trees: The Devonian Strategies. C. R. Palevol 8, 155–165. Meyer-Berthaud, B., Ruechlin, M., Soria, A., Belka, Z., Lardeux, H., 2004. Frasnian plants from the Dra Valley, Southern Anti-Atlas, Morocco. Geol. Mag. 141 (06), 675–686. Meyer-Berthaud, B., Soria, A., Young, G.C., 2007. Reconsidering differences between Cladoxylopsida and Iridopteridales: evidence from Polyxylon australe (Upper Devonian, New South Wales, Australia). Int. J. Plant Sci. 168, 1085–1097. Mishler, B.D., Churchill, S.P., 1984. A cladistic approach to the phylogeny of the “bryophytes”. Brittonia 36 (4), 406–424. Momont, N., Gerrienne, P., Prestianni, C., 2016. Brabantophyton, A New Genus with Stenokolealean Affinities from a Middle to Earliest Upper Devonian Locality from Belgium. Rev. Palaeobot. Palynol. 227, 77–96 (in this issue). Nickrent, D.L., Parkinson, C.L., Palmer, J.D., Duff, R.J., 2000. Multigene phylogeny of land plants with special reference to bryophytes and the earliest land plants. Mol. Biol. Evol. 17 (12), 1885–1895. Niklas, K.J., Kutschera, U., 2010. The evolution of the land plant life cycle. New Phytol. 185 (1), 27–41. Nishiyama, T., Wolf, P.G., Kugita, M., Sinclair, R.B., Sugita, M., Sugiura, C., Wakasugi, T., Yamada, K., Yoshinaga, K., Yamaguchi, K., Ueda, K., Hasebe, M., 2004. Chloroplast phylogeny indicates that bryophytes are monophyletic. Mol. Biol. Evol. 21 (10), 1813–1819. Parry, S.F., Noble, S.R., Crowley, Q.G., Wellman, C.H., 2011. A high-precision U–Pb age constraint on the Rhynie Chert Konservat-Lagerstätte: time scale and other implications. J. Geol. Soc. 168, 863–872. Parry, S.F., Noble, S.R., Crowley, Q.G., Wellman, C.H., 2013. Reply to Discussion on ‘A highprecision U–Pb age constraint on the Rhynie Chert Konservat-Lagerstätte: time scale and other implications’ Journal, 168, 863–872. J. Geol. Soc. 170, 703–706. Pirani, J.R., Prado, J., 2012. Embryopsida, a new name for the class of land plants. Taxon 61 (5), 1096–1098. Prestianni, C., Gerrienne, P., 2010. Early seed plant radiation: an ecological hypothesis. In: Vecoli, M., Clément, G., Meyer-Berthaud, B. (Eds.), The Terrestrialization Process: Modelling Complex Interactions at the Biosphere-Geosphere Interface. Geological Society, London, Special Publications 339, pp. 71–80. Pryer, K.M., Schneider, H., Smith, A.R., Cranfill, R., Wolf, P.G., Hunt, J.S., Sipes, S.D., 2001. Horsetails and ferns are a monophyletic group and the closest living relatives to seed plants. Nature 409 (6820), 618–622. Pryer, K.M., Schuettpelz, E., Wolf, P.G., Schneider, H., Smith, A.R., Cranfill, R., 2004. Phylogeny and evolution of ferns (monilophytes) with a focus on the early leptosporangiate divergences. Am. J. Bot. 91 (10), 1582–1598. Qiu, Y.L., 2008. Phylogeny and evolution of charophytic algae and land plants. J. Syst. Evol. 46 (3), 287–306. Qiu, Y.L., Li, L., Wang, B., Chen, Z., Knoop, V., Groth-Malonek, M., Dombrovska, O., Lee, J., Kent, L., Rest, J., Estabrook, G.F., Hendry, T.A., Taylor, D.W., Testa, C.M., Ambros, M., Crandall-Stotler, B., Duff, R.J., Stech, M., Frey, W., Quandt, D., Davis, C.C., 2006. The deepest divergences in land plants inferred from phylogenomic evidence. Proc. Natl. Acad. Sci. 103 (42), 15511–15516. Qiu, Y.L., Taylor, A.B., McManus, H.A., 2012. Evolution of the life cycle in land plants. J. Syst. Evol. 50 (3), 171–194. Raevskaya, E., Dronov, A., Servais, T., Wellman, C., 2016. Cryptospores from the Katian (Upper Ordovician) of the Tungus basin: the first evidence for early land plants from the Siberian palaeocontinents. Rev. Palaeobot. Palynol. 224 (Part 1), 4–13. Renzaglia, K.S., Duff, R.J., Nickrent, D.L., Garbary, D.J., 2000. Vegetative and reproductive innovations of early land plants: implications for a unified phylogeny. Philos. Trans. R. Soc. B Biol. Sci. 355 (1398), 769–793. Renzaglia, K.S., Dengate, S.B., Schmitt, S.J., Duckett, J.G., 2002. Novel features of Equisetum arvense spermatozoids: insights into pteridophyte evolution. New Phytol. 154 (1), 159–174. Richardson, J.B., 1988. Late Ordovician and Early Silurian cryptospores and miospores from Northeast Libya. In: El-Arnauti, A., Owens, B., Thusu, B. (Eds.), Subsurface Palynostratigraphy of Northeast Libya. Garyounis University Press, Benghazi, pp. 89–109. Richardson, J.B., 1996. Chapter 18A. Lower and Middle Palaeozoic records of terrestrial palynomorphs. In: Jansonius, J., McGregor, D.C. (Eds.), Palynology: Principles and Applications. American Association of Stratigraphic Palynologists Foundation, Houston, pp. 555–574. Richardson, J.B., Ford, J.H., Parker, F., 1984. Miospores, correlation and age of some Scottish Lower Old Red Sandstone sediments from the Strathmore region (Fife and Angus). J. Micropalaeontol. 3, 109–124. Rickards, R.B., 2000. The age of the earliest club mosses: the Silurian Baragwanathia flora in Victoria, Australia. Geol. Mag. 137 (02), 207–209. Romero-Sarmiento, M.F., Riboulleau, A., Vecoli, M., Versteegh, G.J.M., 2011. Aliphatic and aromatic biomarkers from Gondwanan sediments of Late Ordovician to Early Devonian age: an early terrestrialization approach. Org. Geochem. 42 (6), 605–617. Rothwell, G.W., 1994. Phylogenetic relationships among ferns and gymnosperms; an overview. J. Plant Res. 107 (4), 411–416. Rothwell, G.W., 1996. Phylogenetic relationships of ferns: a palaeobotanical perspective. Pteridology in Perspective 395, p. 404. Rothwell, G.W., 1999. Fossils and ferns in the resolution of land plant phylogeny. Bot. Rev. 65 (3), 188–218. Rothwell, G.W., Nixon, K.C., 2006. How does the inclusion of fossil data change our conclusions about the phylogenetic history of euphyllophytes? Int. J. Plant Sci. 167 (3), 737–749. Rothwell, G.W., Serbet, R., 1994. Lignophyte phylogeny and the evolution of spermatophytes: a numerical cladistic analysis. Syst. Bot. 19, 443–482. Rubinstein, C.V., 2005. Ordovician to Lower Silurian palynomorphs from the Sierras subandinas (Subandean ranges), northwestern Argentina: a preliminary report. In: Steemans, P., Javaux, E. (Eds.), Pre-Cambrian to Palaeozoic Palaeopalynology and Palaeobotany. Carnets de Géologie/Notebooks on Geology, Brest, Memoir 2005/02 (Abstract 09 (CG2005_M02/09)). Rubinstein, C.V., Vaccari, N.E., 2004. Cryptospores assemblages from the Ordovician/ Silurian boundary in the Puna Region, NW Argentina. Palaeontology 47, 1037–1061. P. Gerrienne et al. / Review of Palaeobotany and Palynology 227 (2016) 4–18 Rubinstein, C.V., Gerrienne, P., De la Puente, G.S., Astini, R.A., Steemans, P., 2010. Early Middle Ordovician evidence for land plants in Argentina (Eastern Gondwana). New Phytol. 188, 365–369. Ruhfel, B.R., Gitzendanner, M.A., Soltis, P.S., Soltis, D.E., Burleigh, J.G., 2014. From algae to angiosperms-inferring the phylogeny of green plants (Viridiplantae) from 360 plastid genomes. BMC Evol. Biol. 14 (1), 23. Selosse, M.A., Strullu-Derrien, C., Martin, F.M., Kamoun, S., Kenrick, P., 2015. Plants, fungi and oomycetes: a 400-million year affair that shapes the biosphere. New Phytol. 206 (2), 501–506. Serbet, R., Rothwell, G.W., 1992. Characterizing the most primitive seed ferns. I. A reconstruction of Elkinsia polymorpha. Int. J. Plant Sci. 153, 602–621. Servais, T., 1996. Some considerations on acritarch classification. Rev. Palaeobot. Palynol. 93, 9–22. Servais, T., Brocke, R., Fatka, O., LeHérissé, A., Molyneux, S.G., 1997. Value and meaning of the term Acritarch. Acta Univ. Carol. Geol. 40, 631–643. Shute, C.H., Edwards, D., 1989. A new rhyniopsid with novel sporangium organization from the Lower Devonian of South Wales. Bot. J. Linn. Soc. 100 (2), 111–137. Silvestro, D., Cascales-Miñana, B., Bacon, C.D., Antonelli, A., 2015. Revisiting the origin and diversification of vascular plants through a comprehensive Bayesian analysis of the fossil record. New Phytol. http://dx.doi.org/10.1111/nph.13247. Skog, J.E., Banks, H.P., 1973. Ibyka amphikoma, gen. et sp. n., a new protoarticulate precursor from the late Middle Devonian of New York State. Am. J. Bot. 60, 366–380. Sperry, J.S., 2003. Evolution of water transport and xylem structure. Int. J. Plant Sci. 164 (S3), S115–S127. Spina, A., 2014. Latest Ordovician (Hirnantian) miospores from the Nl-2 well, Algeria, North Africa, and their evolutionary significance. Palynology http://dx.doi.org/10. 1080/01916122.2014.944626. Steemans, P., 2000. Miospore evolution from the Ordovician to Silurian. Rev. Palaeobot. Palynol. 113, 189–196. Steemans, P., 2001. Ordovician cryptospores from the Oostduinkerke borehole, Brabant Massif, Belgium. Geobios 34, 3–12. Steemans, P., Le Hérisse, A., Bozdogan, N., 1996. Ordovician and Silurian cryptospores and miospores from southeatern Turkey. Rev. Palaeobot. Palynol. 93, 35–76. Steemans, P., Le Hérissé, A., Melvin, J., Miller, M.A., Paris, F., Verniers, J., Wellman, C.H., 2009. Origin and radiation of the earliest vascular land plants. Science 324 (5925), 353. Steemans, P., Lepot, K., Marshall, C.P., Javaux, E.J., 2010a. FTIR characterisation of the chemical composition of Silurian cryptospores from Gotland, Sweden. Rev. Palaeobot. Palynol. 162 (4), 577–590. Steemans, P., Wellman, C.H., Gerrienne, P., 2010b. Paleogeographic and paleoclimatic considerations based on Ordovician to Lochkovian vegetation. Geol. Soc. Lond., Spec. Publ. 339, 49–58. Steemans, P., Petus, E., Breuer, P., Mauller-Mendlowicz, P., Gerrienne, P., 2012. Palaeozoic innovations in the micro-and megafossil plant record: from the earliest plant spores to the earliest seeds. In: Talent, J. (Ed.), Extinction Intervals and Biogeographic Perturbations through Time. Springer, Berlin, New York, pp. 437–477. Stein, W.E., Mannolini, F., Hernick, L.V., Landing, E., Berry, C.M., 2007. Giant cladoxylopsid trees resolve the enigma of the Earth's earliest forest stumps at Gilboa. Nature 446 (7138), 904–907. Stein, W.E., Berry, C.M., Hernick, L.V., Mannolini, F., 2012. Surprisingly complex community discovered in the mid-Devonian fossil forest at Gilboa. Nature 483 (7387), 78–81. Stevens, P.F., 2001. Angiosperm Phylogeny Website. Version 12, July 2012 Evolution of Land plants. Last updated 04/28/2015 00:21:29. (Last visited on May 6, 2015) http://www.mobot.org/MOBOT/research/APweb/ (onwards). Stockmans, F., 1948. Végétaux du Dévonien supérieur de la Belgique. Mém. Mus. R. His. Nat. Belg. 110, 1–85. Strother, P.K., 1991. A classification scheme for the cryptospores. Palynology 15, 219–236. Strother, P.K., Wellman, C.H., 2016. Palaeoecology of a billion-year-old non-marine cyanobacterium from the Torridon Group and Nonesuch Formation. Palaeontology 59, 89–108. Strother, P.K., Al-Hajri, S., Traverse, A., 1996. New evidence for land plants from the lower Middle Ordovician of Saudi Arabia. Geology 24, 55–58. Strother, P.K., Wood, G.D., Taylor, W.A., Beck, J.H., 2004. Middle Cambrian cryptospores and the origin of land plants. In: Laurie, J.R., Foster, C.B. (Eds.), Palynological and Micropalaeontological Studies in Honour of Geoffrey Playford, pp. 99–113. Strother, P.K., Servais, T., Vecoli, M., 2010. The effects of terrestrialization on marine ecosystems: the effects of the fall of CO2. Geol. Soc. Lond., Spec. Publ. 339, 37–48. Strother, P.K., Battison, L., Brasier, M.D., Wellman, C.H., 2011. Earth's earliest non-marine eukaryotes. Nature 473, 505–509. Strother, P.K., Traverse, A., Vecoli, M., 2015. Cryptospores from the Hanadir Shale Member of the Qasim Formation, Ordovician (Darriwilian) of Saudi Arabia: taxonomy and systematics. Rev. Palaeobot. Palynol. 212, 97–110. Strullu-Derrien, C., Kenrick, P., Badel, E., Cochard, H., Tafforeau, P., 2013. An overview of the hydraulic systems in early land plants. IAWA J. 34 (4), 333–351. Strullu-Derrien, C., Kenrick, P., Pressel, S., Duckett, J.G., Rioult, J.P., Strullu, D.G., 2014. Fungal associations in Horneophyton ligneri from the Rhynie Chert (c. 407 million year old) closely resemble those in extant lower land plants: novel insights into ancestral plant-fungus symbioses. New Phytol. 203 (3), 964–979. Taylor, W.A., 1995. Spores in earliest land plants. Nature 373, 391–392. Taylor, W.A., Strother, P.K., 2008. Ultrastructure of some Cambrian palynomorphs from the Bright Angel Shale, Arizona, USA. Rev. Palaeobot. Palynol. 151, 41–50. Taylor, E.L., Taylor, T.N., Krings, M., 2009. Paleobotany: The Biology and Evolution of Fossil Plants. Academic Press, New York. Taylor, W.A., Gensel, P.G., Wellman, C.H., 2011. Wall ultrastructure in three species of the dispersed spore Emphanisporites from the Early Devonian. Rev. Palaeobot. Palynol. 163 (3), 264–280. 17 Tomescu, A.M., 2009. Megaphylls, microphylls and the evolution of leaf development. Trends Plant Sci. 14 (1), 5–12. Turmel, M., Otis, C., Lemieux, C., 2006. The chloroplast genome sequence of Chara vulgaris sheds new light into the closest green algal relatives of land plants. Mol. Biol. Evol. 23 (6), 1324–1338. Vasco, A., Moran, R.C., Ambrose, B.A., 2013. The evolution, morphology, and development of fern leaves. Front. Plant Sci. 4, 345. Vavrdová, M., 1984. Some plant microfossils of the possible terrestrial origin from the Ordovician of Central Bohemia. Vest. Ceskeho Geol. Ustavu 59, 165–170. Vavrdová, M., 1988. Further acritarchs and terrestrial plant remains from the Late Ordovician at Hlasna Treban (Czechoslovakia). Casopis Min. Geol. 33, 1–10. Vavrdová, M., 1989. New acritarchs and miospores from the Late Ordovician of Hlasna Treban, Czechoslovakia. Casopis Min. Geol. 34, 403–420. Vecoli, M., 2000. Palaeoenvironmental interpretation of microphytoplankton diversity trends in the Cambrian–Ordovician of the Northern Sahara Platform. Palaeogeogr. Palaeoclimatol. Palaeoecol. 160, 329–346. Vecoli, M., Meyer-Berthaud, B., Clément, G. (Eds.), 2010. The Terrestrialization Process: Modelling Complex Interactions at the Biosphere–Geosphere Interface. Geological Society of London Special Publications vol. 339 (179 pp.). Vecoli, M., Delabroye, A., Spina, A., Hints, O., 2011. Cryptospore assemblage from Upper Ordovician (Katian-Hirnantian) strata of Anticosti Island, Québec, Canada, and Estonia: palaeophytogeographic and palaeoclimatic implications. Rev. Palaeobot. Palynol. 166, 76–93. Vecoli, M., Beck, J., Strother, P.K., 2015. Palynology of the Ordovician Kanosh Shale at Fossil Mountain, Utah. J. Paleontol. 89, 411–423. Versteegh, G.J., Riboulleau, A., 2010. An organic geochemical perspective on terrestrialization. Geol. Soc. Lond., Spec. Publ. 339 (1), 11–36. Wang, D.M., 2007. Tenuisa frasniana gen. et sp. nov., a plant of euphyllophyte affinity from the Late Devonian of China. Int. J. Plant Sci. 168 (9), 1341–1349. Wang, Y., Berry, C.M., 2001. A new plant from the Xichong Formation (Middle Devonian), South China. Rev. Palaeobot. Palynol. 116 (1), 73–85. Wang, Y., Li, J., Wang, R., 1997. Latest Ordovician cryptospores from Southern Xinjiang, China. Rev. Palaeobot. Palynol. 99, 61–74. Wang, D.M., Hao, S.G., Wang, Q., 2005. Rotafolia songziensis gen. et comb. nov., a sphenopsid from the Late Devonian of Hubei, China. Bot. J. Linn. Soc. 148 (1), 21–37. Wang, Y., Fu, Q., Xu, H.H., Hao, S.G., 2007. A new plant with complex branching from Late Silurian in Xinjiang, China. Alcheringa 31, 111–120. Wellman, C.H., 1996. Cryptospores from the type area of the Caradoc Series in southern Britain. In: Cleal, C.J. (Ed.), Studies on Early Land Plant Spores from Britain. Special Papers in Palaeontology 55, pp. 103–136. Wellman, C.H., 1999. Sporangia containing Scylaspora from the lower Devonian of the Welsh Borderland. Palaeontology 42, 67–81. Wellman, C.H., 2006. Spore assemblages from the Lower Devonian ‘Lower Old Red Sandstone’ deposits of the Rhynie outlier, Scotland. Trans. R. Soc. Edinb. Earth Sci. 97, 167–211. Wellman, C.H., 2010. The invasion of the land by plants: when and where? New Phytol. 188, 1–3. Wellman, C.H., 2014. The nature and evolutionary relationships of the earliest land plants. New Phytol. 202, 1–3. Wellman, C.H., Gray, J., 2000. The microfossil record of early land plants. Philos. Trans. R. Soc. Lond. B 355, 717–732. Wellman, C.H., Thomas, R.G., Edwards, D., Kenrick, P., 1998a. The Cosheston Group (Lower Old Red Sandstone) in Southwest Wales: age, correlation and palaeobotanical significance. Geol. Mag. 135 (03), 397–412. Wellman, C.H., Edwards, D., Axe, L., 1998b. Permanent dyads in sporangia and spore masses from the Lower Devonian of the Welsh Borderland. Bot. J. Linn. Soc. 127, 117–147. Wellman, C.H., Edwards, D., Axe, L., 1998c. Ultrastructure of laevigate hilate spores in sporangia and spore masses from the Upper Silurian and Lower Devonian of the welsh borderland. Philos. Trans. R. Soc. B Biol. Sci. 353, 1983–2004. Wellman, C.H., Osterloff, P.L., Mohiuddin, U., 2003. Fragments of the earliest land plants. Nature 425, 282–285. Wellman, C.H., Steemans, P., Vecoli, M., 2013. Palaeophytogeography of Ordovician–Silurian land plants. In: Harper, D.A.T., Servais, T. (Eds.), Early Palaeozoic Biogeography and Palaeogeography. Geological Society Of London Memoirs 38, pp. 461–476. Wellman, C.H., Steemans, P., Miller, M.A., 2015. Spore assemblages from Upper Ordovician and lowermost Silurian sediments recovered from the Qusaiba-1 shallow core hole, Qasim region, central Saudi Arabia. Rev. Palaeobot. Palynol. 212, 111–126. Wickett, N.J., Mirarab, S., Nguyen, N., Warnow, T., Carpenter, E., Matasci, N., Ayyampalayam, S., Barker, M.S., Burleigh, J.G., Gitzendanner, M.A., Ruhfel, B.R., Wafula, E., Der, J.P., Graham, S.W., Mathews, S., Melkonian, M., Soltis, D.E., Soltis, P.S., Miles, N.W., Rothfels, C.J., Pokorny, L., Shaw, A.J., DeGironimo, L., Stevenson, D.W., Surek, B., Villarreal, J.C., Roure, B., Philippe, H., dePamphilis, C.W., Chen, T., Deyholos, M.K., Baucom, R.S., Kutchan, T.M., Augustin, M.M., Wang, J., Zhang, Y., Tian, Z., Yan, Z., Wu, X., Sun, X., Wong, G.K.-S., Leebens-Mack, J., 2014. Phylotranscriptomic analysis of the origin and early diversification of land plants. Proc. Natl. Acad. Sci. 111 (45), E4859–E4868. Wodniok, S., Brinkmann, H., Glöckner, G., Heidel, A.J., Philippe, H., Melkonian, M., Becker, B., 2011. Origin of land plants: do conjugating green algae hold the key? BMC Evol. Biol. 11 (1), 104. Xiong, C.H., Wang, D.M., Wang, Q., Meng, M.C., 2012. A new euphyllophyte Kunia venusta gen. et sp. nov. from the Middle Devonian of Yunnan, South China. J. Syst. Evol. 50 (6), 540–549. Yin, L., He, S., 2000. Palynomorphs from the transitional sequences between Ordovician and Silurian of northwestern Zhejiang, South China. In: Song, Z. (Ed.), Palynofloras 18 P. Gerrienne et al. / Review of Palaeobotany and Palynology 227 (2016) 4–18 and Palynomorphs of China. Press of University of Science and Technology of China, Hefei, pp. 186–202. Yin, L.M., Zhao, Y.L., Bian, L.Z., Peng, J., 2013. Comparison between cryptospores from the Cambrian Log Cabin Member, Pioche Shale, Nevada, USA and similar specimens from the Cambrian Kaili Formation, Guizhou, China. Sci. China Earth Sci. 56, 703–709. Zhong, B., Liu, L., Yan, Z., Penny, D., 2013. Origin of land plants using the multispecies coalescent model. Trends Plant Sci. 18 (9), 492–495. Zhong, B., Fong, R., Collins, L.J., McLenachan, P.A., Penny, D., 2014. Two new fern chloroplasts and decelerated evolution linked to the long generation time in tree ferns. Genome Biol. Evol. 6 (5), 1166–1173.