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Land plants (embryophytes) evolved from streptophyte green algae, a small group of freshwater algae ranging from scaly, unicellular flagellates (Mesostigma) to complex, filamentous thalli with branching, cell differentiation and apical growth (Charales). Streptophyte algae and embryophytes form the division Streptophyta, whereas the remaining green algae are classified as Chlorophyta. The Charales (stoneworts) are often considered to be sister to land plants, suggesting progressive evolution towards cellular complexity within streptophyte green algae. Many cellular (e.g. phragmoplast, plasmodesmata, hexameric cellulose synthase, structure of flagellated cells, oogamous sexual reproduction with zygote retention) and physiological characters (e.g. type of photorespiration, phytochrome system) originated within streptophyte algae.
Phylogenetic studies have demonstrated that Mesostigma (flagellate) and Chlorokybus (sarcinoid) form the earliest divergence within streptophytes, as sister to all other Streptophyta including embryophytes. The question whether Charales, Coleochaetales or Zygnematales are the sister to embryophytes is still (or, again) hotly debated. Projects to study genome evolution within streptophytes including protein families and polyadenylation signals have been initiated. In agreement with morphological and physiological features, many molecular traits believed to be specific for embryophytes have been shown to predate the Chlorophyta/Streptophyta split, or to have originated within streptophyte algae. Molecular phylogenies and the fossil record allow a detailed reconstruction of the early evolutionary events that led to the origin of true land plants, and shaped the current diversity and ecology of streptophyte green algae and their embryophyte descendants.
The Streptophyta/Chlorophyta divergence correlates with a remarkably conservative preference for freshwater/marine habitats, and the early freshwater adaptation of streptophyte algae was a major advantage for the earliest land plants, even before the origin of the embryo and the sporophyte generation. The complete genomes of a few key streptophyte algae taxa will be required for a better understanding of the colonization of terrestrial habitats by streptophytes.
The Viridiplantae (Latin for ‘green plants’) include all green algae (Chlorophyta and streptophyte algae) and embryophyte plants. They represent a monophyletic group of organisms, which display a surprising diversity with respect to their morphology, cell architecture, life histories and reproduction, and biochemistry. The colonization of terrestrial habitats by descendents of streptophyte algae started approx. 470–450 MY ago (Ordovician period; reviewed in Sanderson et al., 2004), and was undoubtedly one of the most important steps in the evolution of life on earth (Graham, 1993; Kenrick and Crane, 1997; Bateman et al., 1998). The evolution of the various groups of land plants (embryophytes = bryophytes, pteridophytes and spermatophytes) resulted in our current terrestrial ecosystems (Waters, 2003) and significantly changed the atmospheric oxygen concentration (Berner, 1999; Scott and Glasspool, 2006). In this Briefing we will first describe recent progress in our understanding of the phylogenetic relationships within the Viridiplantae with a focus on streptophyte algae. We will then present new results and ideas in molecular physiology and genome evolution as well as primary adaptations and evolutionary trends, which were important for the origin of true land plants.
The phylogenetic relationships within the Viridiplantae were summarized by Lewis and McCourt (2004). Most phylogenetic relationships proposed at that time appear to be still valid. The Viridiplantae split early into two evolutionary lineages: Chlorophyta and Streptophyta (Fig. 1A). This split occurred about 725–1200 MY ago, according to different estimates by molecular clock methods (Hedges et al., 2004; Yoon et al., 2004; Zimmer et al., 2007). Within the streptophyte algae six morphologically distinct groups were recognized: the flagellate Mesostigmatales, sarcinoid Chlorokybales, filamentous (unbranched) Klebsormidiales, the Zygnematales (characterized by conjugation as the method of sexual reproduction and total absence of flagellated cells), and the two morphologically most complex groups, the Charales (stoneworts) and Coleochaetales, both of which are characterized by true multicellular organization (with plasmodesmata) of parenchyma-like thalli or branched filaments with apical growth and oogamous sexual reproduction. The genus Spirotaenia, usually classified as member of the Zygnematales, probably represents an independent lineage separate from the Zygnematales (Gontcharov and Melkonian, 2004). The branching order among streptophyte algae was not resolved in 2004 and has subsequently been addressed by several publications, using rRNA and/or rbcL genes (e.g. Hall et al., 2008), complete plastid genomes (e.g. Turmel et al., 2005, 2006), or phylogenomic approaches (Rodriguez-Ezpeleta et al., 2007). However, in phylogenetic trees obtained to date the divergence of streptophyte algae is still poorly resolved. The only major exception refers to the phylogenetic position of Mesostigma. Called an enigma in 2004 (Lewis and McCourt, 2004), recent work has now firmly established that Mesostigma forms a clade with Chlorokybus (Fig. 1B), both representing the earliest divergence of streptophyte algae (Lemieux et al., 2007; Rodriguez-Ezpeleta et al., 2007). In contrast, the question as to which group represents the sister to the embryophytes is far from being settled. In many illustrations depicting the evolution of streptophyte algae and land plants in textbooks (e.g. Raven et al., 2005) or review articles (Lewis and McCourt, 2004; McCourt et al., 2004; Qiu, 2008), the Charales (stoneworts) are shown as sister to the embryophytes. This is supported by an analysis of four genes encoded by three cellular compartments (Karol et al., 2001). However, in recent phylogenetic analyses, either the Charales or alternatively the Coleochaetales or Zygnematales are found as sisters to the land plants, depending on the gene(s) analysed and the taxon sampling, but none of these topologies has convincing statistical support. Analyses of chloroplast genomes tend to support the Zygnematales or a clade consisting of the Zygnematales and the Coleochaetales as sister to the embryophytes (Turmel et al., 2007). In contrast, in both our ongoing work using a phylogenomic approach [similar to the one used for Mesostigma (Rodriguez-Ezpeleta et al., 2007) using five streptophyte algae including Chara and Coleochaete; S. Wodniok, M. Melkonian, H. Philippe and B. Becker, University of Cologne, Germany, unpubl. res.], or using complete rRNA operons of the nuclear and plastidic genomes (using ten streptophyte algae; B. Marin and M. Melkonian, University of Cologne, unpubl. res.) we observed the Charales as sister to embryophytes, albeit with low statistical support. We are currently trying to test these results by improved taxon sampling (rRNA trees) and the inclusion of a larger number of genes (phylogenomics). The phylogenetic relationships between the streptophyte algae we both currently agree on are depicted in Fig. 1B.
Public literature databases (e.g. Web of Science) contain many references to proteins/genes that are considered to be plant-specific. Unfortunately, the term ‘plant-specific’ is often misleading, and merely indicates that a protein is only known from land plants (embryophytes) or spermatophytes, and therefore the term spermatophyte- or embryophyte-specific would be much better. Horizontal gene transfer into embryophytes is extremely rare (Richardson and Palmer, 2006; Huang and Gogarten, 2008; Keeling and Palmer, 2008), with the exception of mitochondrial genes transferred from one plant to another (Richardson and Palmer, 2006; Keeling and Palmer, 2008), and an ancient horizontal or endocytic gene transfer from a chlamydial-type bacterium (Huang and Gogarten, 2007; Becker et al., 2008) to the ancestor of Plantae (Glaucoplantae, Rhodoplantae and Viridiplantae). Therefore, nearly all the genes present in extant embryophytes were inherited from the eukaryotic host or the cyanobacterial endosymbiont of the common ancestor of all Plantae (Martin et al., 2002). Thus, we should be very careful with terms such as ‘plant-specific gene’ (in the sense of embryophyte- or spermatophyte-specific) until at least a single genome of a streptophyte alga is completely sequenced.
We are convinced that many plant ‘innovations’ will actually turn out to be innovations of the streptophyte algae (or the viridiplants), once complete streptophyte genomes become available and/or comparisons include chlorophyte genomes (Ostreococcus, Chlamydomonas). Recent examples of proteins/genes now also found in streptophyte and/or chlorophyte algae are given in Table 1.
A nice example is the ‘plant-specific’ vacuolar sorting receptor (formerly known as BP80). One of us has recently shown that this protein originated in the last common viridiplant ancestor and is present in the Chlorophyta and the Streptophyta (Becker and Hoef-Emden, 2009). The overall structure of the receptor has not changed in green algae and land plants and the overall rate in sequence evolution appears to be slower in streptophytes than in chlorophytes. This seems to be a general pattern. Similar slow evolution rates have been observed for many proteins in phylogenetic trees published in recent years. Embryophyte evolution appears mainly to involve expansion of protein families followed by differential expression rather than sequence variations. This seems also to be the case for the chloroplast genome. Turmel et al. (2007) concluded that ‘most of the features typical of land plant chloroplast genomes were inherited from their green algal ancestors’.
Given the diversity in morphology, cell architecture, life histories and reproduction, and biochemistry among photoautotrophic eukaryotes, it is surprising that ‘true land plants’ evolved uniquely within the streptophytes. Terrestrial (micro) algae are present in several other algal groups (e.g. Cyanobacteria, diatoms, Chlorophyceae and Trebouxiophyceae); however, none of these algae ever rose above their substrate. Macroalgae (Ulvophyceae, red and brown seaweeds) became dominant players in marine habitats but never invaded terrestrial ecosystems. Why were streptophytes so successful in the colonization of terrestrial habitats? We suggest that streptophyte algae were physiologically pre-adapted to terrestrial existence by their primary freshwater life style, in contrast to their marine sister lineage, i.e. Chlorophyta (Fig. 2A). Freshwater adaptation allowed a slow and gradual move towards moist habitats in the proximity of water, and ultimately the colonization of dry land, dependent on rainwater. In contrast, the ecological gradient between marine and terrestrial habitats is very sharp (mainly salinity; but also extremes of temperature, exposure to high irradiance, dehydration, ultra-violet radiation; Smith and Smith, 2006), and apparently did not enable the successful colonization of terrestrial regions by marine algae. Interestingly, the animal groups with major players in terrestrial habitats (insects and vertebrates) originated in freshwater environments and are still completely (amphibians and insects) or largely (reptiles, birds and mammals) absent from the oceans (Vermeij and Dudley, 2000; Glenner et al., 2006). The same holds for streptophyte algae (strict freshwater preference, with only a few Charales that tolerate brackish habitats), and for the Embryophyta with primary terrestrial origin and adaptation, many secondary freshwater plants (bryophytes, ferns and angiosperms), and only very few derived angiosperms adapted to marine, fully saline environments (the monocot sea-grasses, e.g. Zostera).
Streptophytes adapted to deal with freshwater conditions very early during their evolution, and probably were the first eukaryotic freshwater algae (Fig. 2A). For the foundation of the first terrestrial ecosystems, streptophytes were exploiting an entirely new environment, almost free of competing organisms, probably with the exception of cyanobacteria and fungi (Labandeira, 2005). This situation allowed the explosive radiation of early land plants, beginning in the Silurian period, possibly earlier in the Ordovician or even Cambrian (Labandeira, 2005; Taylor and Strother, 2008), adapting their morphology, physiology, life history and reproduction to land life (Fig. 2B). Any algal group that later developed a tendency towards terrestrial and macrophytic life styles was confronted with the opposite situation: competition with already adapted land plants. It is therefore not surprising that no second lineage of land plants evolved successfully besides streptophytes.
The major difference between streptophyte algae and embryophytes is the heteromorphic life history of the latter, i.e. development of the zygote towards an embryo and a diploid sporophyte generation. All streptophyte algae are haplonts with the zygote being the only diploid cell, which immediately undergoes meiosis (resulting in four meiospores). In contrast to gametes (eggs, sperms), spores are enclosed by a pigmented cell wall composed of sporopollenin, an extremely resistant biopolymer, and are thus well protected from predators, mechanical and chemical damage, degradation and mutagenic UV light. Interestingly again, sporopollenin evolved within the streptophyte algae (Delwiche et al., 1989). Spores are not protected from desiccation, but tolerate dehydration, which might even offer an advantage for spore dispersal. Therefore, the optimal reproduction and dispersal strategy for early terrestrial plants was the production of spores rather than gametes, ideally in very large numbers, to ensure survival and germination of at least some of them. We regard the presence of a multicellular sporophyte, resulting from a delay of meiosis, as the first adaptation to terrestrial life. The erect sporophyte morphology with terminal sporangia optimized the long-range dispersal of spores, whereas the haploid gametophyte generation usually remained on the ground, since the ‘traditional’ oogamous fertilization (eggs and sperm cells) required free water. The embryophytes of the Rhynie chert Lagerstätte (early Devonian) already showed a size difference between gametophytes and sporophytes [e.g. Cooksonia (Gerrienne et al., 2006); Rhynia (Kerp et al., 2004); Aglaophyton (Taylor et al., 2005)]. Initially a dependent ‘spore-producing organ’, the developmental potential of the sporophyte generation to form highly differentiated and autonomous plant bodies was exploited only later by lycophytes, ferns and seed plants.
Interestingly, the haploid/diploid transition in Chlamydomonas is regulated by two homeobox proteins of the KNOX/BELL protein family (Lee et al., 2008). In embryophytes BELL and KNOX homeodomain proteins are involved in maintaining the shoot apical meristem (Ariel et al., 2007) and form part of a large protein family [homeodomain- (HD) containing proteins] associated with various cell differentiation events. Members of the ‘plant-specific’ HD-ZIP subfamily have now also been reported from streptophyte algae (Floyd et al., 2006). Thus it seems likely that the sporophyte originated by simple changes in the expression pattern of homeobox proteins of the BELL/KNOX family followed by an expansion and diversification of the HD-containing proteins to become important regulators of cell differentiation.
Extant streptophyte algae display a surprisingly low diversity (about 13 families, 122 genera), in contrast to the Chlorophyta with about 100 families containing 700 genera. The series of evolutionary events that shaped the current distribution and diversity of green algae can be tentatively reconstructed from molecular phylogenies and the scarce fossil record of algae and early land plants (summarized in Fig. 2). After their separation from ancient marine Chlorophyta, streptophyte algae conquered freshwater habitats worldwide, and probably were the only eukaryotic freshwater algae during the Precambrian (Fig. 2). They coexisted ‘side by side’ with their embryophyte descendents, at least before the appearance of the first aquatic embryophytes (Cretaceous; Martín-Closas, 2003), and with their marine ‘sisters’ (Chlorophyta). What caused the failure of streptophyte algae to dominate the freshwater permanently? At first, two catastrophic events significantly reduced the streptophyte diversity, as is obvious from the fossil record of the Charales: the Permian/Triassic and the Cretaceous/Tertiary mass extinctions, both probably related to volcanism and/or asteroid impact and accompanied by climatic changes. For example, the Permian/Triassic Boundary event (250 MY ago) marked the extinction of those Charales with anti-clockwise oogonia, and from then on, the enveloping cells of charalean oogonia display the modern clockwise coiling pattern. The Cretaceous/Tertiary extinction (65 MY ago), which is known as the end of the Mesozoic dinosaur age, caused the extinction of the charalean family Clavatoraceae, and an ongoing progressive reduction of the diversity of the surviving Charales (Martín-Closas, 2003; Soulié-Märsche, 2004; Martín-Closas and Wang, 2008). Except for the Charales, the fossil record of streptophyte algae is unfortunately rather poor, and thus we can only speculate about the disappearance of other ancient groups of streptophyte algae by mass extinctions. It is currently unclear whether further catastrophes such as the recent ice ages have also shaped the freshwater flora.
The second problem streptophyte algae were confronted with was the invasion of freshwater habitats by other algae and/or plants, followed by harsh competition for light, space and nutrients. At first, modern groups of Chlorophyta (primarily marine green algae) appeared after a new mode of cell division was introduced, the phycoplast, which enabled complex multicellular growth (analogous to the streptophyte phragmoplast; Fig. 2B). Two of these derived groups, the classes Chlorophyceae and Trebouxiophyceae, switched almost completely towards freshwater habitats. Since about the Permian/Triassic mass extinction (250 MY ago; Fig. 2B, C), these groups dominated the freshwater phytoplankton (Martín-Closas, 2003) and apparently brought the hegemony of streptophyte algae in their original habitat to an end. It remains unclear whether the appearance of (better-adapted?) Chlorophyceae and Trebouxiophyceae was the main reason for the reduction of streptophyte diversity via competition, or whether they just radiated into a largely empty freshwater ecosystem after the previously dominant streptophyte algae had already been reduced, like successive ‘dynasties’ of green algae. Later, the first water embryophytes, dinoflagellates (both since the Cretaceous, approx. 100 MY ago), diatoms (Palaeocene, ca. 60 MY ago) and chrysophytes (Eocene, approx. 40 MY ago) appeared in freshwater environments (Martín-Closas, 2003), and further competed with the surviving streptophyte algae, which never again reached the diversity and ecological dominance they once had.
There is now agreement that embryophytes originated from streptophyte algae. Their primary freshwater adaptation apparently played a key role in the colonization of dry land habitats. However, the branching order of streptophyte algae is far from settled. A complete understanding of the evolution of land plants will require the remaining phylogenetic questions to be solved and genome evolution within streptophytes to be addressed. The latter requires genome information on streptophyte algae. While a growing number of genomes of chlorophyte algae have been sequenced, currently there is to our knowledge not a single genome project (except ESTs) on any streptophyte alga. Without any genome sequence of a streptophyte alga for comparison, our picture of the evolution of embryophytes remains far from complete.
This paper is dedicated to Prof. Dr M. Melkonian on the occasion of his 60th birthday, a pioneer in evolutionary studies on green algae.