BOTANICAL BRIEFING

Streptophyte algae and the origin of embryophytes

Burkhard Becker* and Birger Marin*

Botanisches Institut, Universitat zu Koln, Gyrhofstr. 16, 50931 Koln, Germany

Received: 11 November 2008 Returned for revision: 15 December 2008 Accepted: 6 February 2009 Published electronically: 8 March 2009

† Background Land plants (embryophytes) evolved from streptophyte green algae, a small group of freshwateralgae ranging from scaly, unicellular flagellates (Mesostigma) to complex, filamentous thalli with branching,cell differentiation and apical growth (Charales). Streptophyte algae and embryophytes form the divisionStreptophyta, whereas the remaining green algae are classified as Chlorophyta. The Charales (stoneworts) areoften considered to be sister to land plants, suggesting progressive evolution towards cellular complexitywithin 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.† Recent Progress Phylogenetic studies have demonstrated that Mesostigma (flagellate) and Chlorokybus (sarci-noid) form the earliest divergence within streptophytes, as sister to all other Streptophyta including embryo-phytes. 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 familiesand 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 fossilrecord allow a detailed reconstruction of the early evolutionary events that led to the origin of true landplants, and shaped the current diversity and ecology of streptophyte green algae and their embryophytedescendants.† Conclusions The Streptophyta/Chlorophyta divergence correlates with a remarkably conservative preference forfreshwater/marine habitats, and the early freshwater adaptation of streptophyte algae was a major advantage forthe earliest land plants, even before the origin of the embryo and the sporophyte generation. The completegenomes of a few key streptophyte algae taxa will be required for a better understanding of the colonizationof terrestrial habitats by streptophytes.

Key words: Chlorophyta, Streptophyta, Embryophyta, Charales, Coleochaetales, Zygnematales, viridiplantphylogeny, land plants, genome evolution, freshwater adaptation, sporophyte origin, diversification, extinction.

INTRODUCTION

The Viridiplantae (Latin for ‘green plants’) include all greenalgae (Chlorophyta and streptophyte algae) and embryophyteplants. They represent a monophyletic group of organisms,which display a surprising diversity with respect to their mor-phology, cell architecture, life histories and reproduction, andbiochemistry. The colonization of terrestrial habitats by des-cendents of streptophyte algae started approx. 470–450 MYago (Ordovician period; reviewed in Sanderson et al., 2004),and was undoubtedly one of the most important steps in theevolution of life on earth (Graham, 1993; Kenrick andCrane, 1997; Bateman et al., 1998). The evolution of thevarious groups of land plants (embryophytes ¼ bryophytes,pteridophytes and spermatophytes) resulted in our current ter-restrial ecosystems (Waters, 2003) and significantly changedthe atmospheric oxygen concentration (Berner, 1999; Scottand Glasspool, 2006). In this Briefing we will first describerecent progress in our understanding of the phylogeneticrelationships within the Viridiplantae with a focus on strepto-phyte algae. We will then present new results and ideas in

molecular physiology and genome evolution as well asprimary adaptations and evolutionary trends, which wereimportant for the origin of true land plants.

PHYLOGENY OF THE STREPTOPHYTA

The phylogenetic relationships within the Viridiplantae weresummarized by Lewis and McCourt (2004). Most phyloge-netic relationships proposed at that time appear to be stillvalid. The Viridiplantae split early into two evolutionarylineages: Chlorophyta and Streptophyta (Fig. 1A). This splitoccurred about 725–1200 MY ago, according to different esti-mates by molecular clock methods (Hedges et al., 2004; Yoonet al., 2004; Zimmer et al., 2007). Within the streptophytealgae six morphologically distinct groups were recognized:the flagellate Mesostigmatales, sarcinoid Chlorokybales, fila-mentous (unbranched) Klebsormidiales, the Zygnematales(characterized by conjugation as the method of sexual repro-duction and total absence of flagellated cells), and the twomorphologically most complex groups, the Charales (stone-worts) and Coleochaetales, both of which are characterizedby true multicellular organization (with plasmodesmata) ofparenchyma-like thalli or branched filaments with apical

* Both authors contibuted equally to this work. For correspondence,e-mail b.becker@uni-koeln.de or birger.marin@uni-koeln.de

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growth and oogamous sexual reproduction. The genusSpirotaenia, usually classified as member of theZygnematales, probably represents an independent lineageseparate from the Zygnematales (Gontcharov and Melkonian,2004). The branching order among streptophyte algae wasnot resolved in 2004 and has subsequently been addressedby 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 phylogenetictrees obtained to date the divergence of streptophyte algae isstill poorly resolved. The only major exception refers to thephylogenetic position of Mesostigma. Called an enigma in2004 (Lewis and McCourt, 2004), recent work has nowfirmly established that Mesostigma forms a clade withChlorokybus (Fig. 1B), both representing the earliest diver-gence of streptophyte algae (Lemieux et al., 2007;Rodriguez-Ezpeleta et al., 2007). In contrast, the question asto which group represents the sister to the embryophytes isfar 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 andMcCourt, 2004; McCourt et al., 2004; Qiu, 2008), theCharales (stoneworts) are shown as sister to the embryophytes.This is supported by an analysis of four genes encoded bythree cellular compartments (Karol et al., 2001). However, inrecent phylogenetic analyses, either the Charales or alterna-tively the Coleochaetales or Zygnematales are found assisters to the land plants, depending on the gene(s) analysedand the taxon sampling, but none of these topologies has con-vincing statistical support. Analyses of chloroplast genomestend to support the Zygnematales or a clade consisting of theZygnematales and the Coleochaetales as sister to the embryo-phytes (Turmel et al., 2007). In contrast, in both our ongoingwork using a phylogenomic approach [similar to the one usedfor Mesostigma (Rodriguez-Ezpeleta et al., 2007) using fivestreptophyte algae including Chara and Coleochaete;S. Wodniok, M. Melkonian, H. Philippe and B. Becker,University of Cologne, Germany, unpubl. res.], or using com-plete rRNA operons of the nuclear and plastidic genomes(using ten streptophyte algae; B. Marin and M. Melkonian,University of Cologne, unpubl. res.) we observed theCharales as sister to embryophytes, albeit with low statisticalsupport. We are currently trying to test these results byimproved taxon sampling (rRNA trees) and the inclusion of alarger number of genes (phylogenomics). The phylogeneticrelationships between the streptophyte algae we both currentlyagree on are depicted in Fig. 1B.

GENOME EVOLUTION WITHINSTREPTOPHYTES AND THE UNIQUENESS

OF EMBRYOPHYTES

Public literature databases (e.g. Web of Science) contain manyreferences to proteins/genes that are considered to be plant-specific. Unfortunately, the term ‘plant-specific’ is often mis-leading, and merely indicates that a protein is only knownfrom land plants (embryophytes) or spermatophytes, and there-fore the term spermatophyte- or embryophyte-specific wouldbe much better. Horizontal gene transfer into embryophytesis extremely rare (Richardson and Palmer, 2006; Huang andGogarten, 2008; Keeling and Palmer, 2008), with the excep-tion of mitochondrial genes transferred from one plant toanother (Richardson and Palmer, 2006; Keeling and Palmer,2008), and an ancient horizontal or endocytic gene transferfrom 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 inher-ited from the eukaryotic host or the cyanobacterial endosym-biont 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- orspermatophyte-specific) until at least a single genome of astreptophyte alga is completely sequenced.

We are convinced that many plant ‘innovations’ will actu-ally turn out to be innovations of the streptophyte algae (orthe viridiplants), once complete streptophyte genomesbecome available and/or comparisons include chlorophytegenomes (Ostreococcus, Chlamydomonas). Recent examples

Chlorophyceae

TrebouxiophyceaeUlvophyceae

Chlorodendrales

Chlorodendrales

PseudoscourfieldialesCoccoid prasinophytes

Coccoid prasinophytes

Coccoid prasinophytes

MamiellalesPyramimonadales

Pyramimonadales

Mesostigmatophyceae

Mesostigmatales

Chlorokybophyceae

Chlorokybales

Chlorophyta

Chlorophyta

KlebsormidiophyceaeZygnemophyceaeColeochaetophyceae

Coleochaetales

Nephroselmidophyceae

Pycnococcaceae

Mamiellales

KlebsormidialesZygnematales

CharalesEmbryophytes

PrasinophytesStreptophyte algae

Streptophyta

StreptophytaCharophyceae

Embryophytes

Ulvophyceae

ChlorophyceaeTrebouxiophyceae

A

B

FI G. 1. Phylogenetic relationships among the major lineages of theViridiplantae. Branches indicated by dotted lines are not well supported. (A)According to Lewis and McCourt (2004), and (B) based on unpublished,ongoing work by the authors. Some of the class names used by Lewis andMcCourt (2004) have never been validly described, and for this reason weuse order designations in (B) and throughout the text. The informal term ‘pra-sinophytes’ is commonly used for scaly green flagellates (Mesostigmatales and

basal Chlorophyta).

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of proteins/genes now also found in streptophyte and/or chlor-ophyte algae are given in Table 1.

A nice example is the ‘plant-specific’ vacuolar sortingreceptor (formerly known as BP80). One of us has recentlyshown that this protein originated in the last common viridi-plant ancestor and is present in the Chlorophyta and theStreptophyta (Becker and Hoef-Emden, 2009). The overallstructure of the receptor has not changed in green algae andland plants and the overall rate in sequence evolutionappears to be slower in streptophytes than in chlorophytes.This seems to be a general pattern. Similar slow evolutionrates have been observed for many proteins in phylogenetictrees published in recent years. Embryophyte evolutionappears mainly to involve expansion of protein families fol-lowed by differential expression rather than sequence vari-ations. This seems also to be the case for the chloroplastgenome. Turmel et al. (2007) concluded that ‘most of the fea-tures typical of land plant chloroplast genomes were inheritedfrom their green algal ancestors’.

NEW HYPOTHESES ABOUT THE ORIGIN OFEMBRYOPHYTES AND THE EVOLUTION

OF STREPTOPHYTE ALGAE

Why were terrestrial environments conquered by only a singlelineage of ‘true land plants’, which evolved from streptophytegreen algae?

Given the diversity in morphology, cell architecture, life his-tories and reproduction, and biochemistry among photoauto-trophic 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. Cyano-bacteria, diatoms, Chlorophyceae and Trebouxiophyceae);however, none of these algae ever rose above their substrate.Macroalgae (Ulvophyceae, red and brown seaweeds) becamedominant players in marine habitats but never invaded terres-trial ecosystems. Why were streptophytes so successful in thecolonization of terrestrial habitats? We suggest that strepto-phyte algae were physiologically pre-adapted to terrestrialexistence by their primary freshwater life style, in contrast totheir marine sister lineage, i.e. Chlorophyta (Fig. 2A).

Freshwater adaptation allowed a slow and gradual movetowards moist habitats in the proximity of water, and ulti-mately the colonization of dry land, dependent on rainwater.In contrast, the ecological gradient between marine and terres-trial habitats is very sharp (mainly salinity; but also extremesof temperature, exposure to high irradiance, dehydration, ultra-violet radiation; Smith and Smith, 2006), and apparently didnot enable the successful colonization of terrestrial regions bymarine algae. Interestingly, the animal groups with majorplayers in terrestrial habitats (insects and vertebrates) originatedin freshwater environments and are still completely (amphi-bians and insects) or largely (reptiles, birds and mammals)absent from the oceans (Vermeij and Dudley, 2000; Glenneret al., 2006). The same holds for streptophyte algae (strict fresh-water preference, with only a few Charales that tolerate brackishhabitats), and for the Embryophyta with primary terrestrialorigin and adaptation, many secondary freshwater plants (bryo-phytes, ferns and angiosperms), and only very few derivedangiosperms adapted to marine, fully saline environments(the monocot sea-grasses, e.g. Zostera).

Streptophytes adapted to deal with freshwater conditionsvery early during their evolution, and probably were the firsteukaryotic freshwater algae (Fig. 2A). For the foundation ofthe first terrestrial ecosystems, streptophytes were exploitingan entirely new environment, almost free of competing organ-isms, probably with the exception of cyanobacteria and fungi(Labandeira, 2005). This situation allowed the explosive radi-ation of early land plants, beginning in the Silurian period,possibly earlier in the Ordovician or even Cambrian(Labandeira, 2005; Taylor and Strother, 2008), adapting theirmorphology, physiology, life history and reproduction toland life (Fig. 2B). Any algal group that later developed a ten-dency towards terrestrial and macrophytic life styles was con-fronted with the opposite situation: competition with alreadyadapted land plants. It is therefore not surprising that nosecond lineage of land plants evolved successfully besidesstreptophytes.

What can be speculated about the origin and advantage of thesporophyte generation?

The major difference between streptophyte algae andembryophytes is the heteromorphic life history of the latter,i.e. development of the zygote towards an embryo and adiploid sporophyte generation. All streptophyte algae are hap-lonts with the zygote being the only diploid cell, whichimmediately undergoes meiosis (resulting in four meiospores).In contrast to gametes (eggs, sperms), spores are enclosed by apigmented cell wall composed of sporopollenin, an extremelyresistant biopolymer, and are thus well protected from preda-tors, mechanical and chemical damage, degradation and muta-genic UV light. Interestingly again, sporopollenin evolvedwithin the streptophyte algae (Delwiche et al., 1989). Sporesare not protected from desiccation, but tolerate dehydration,which might even offer an advantage for spore dispersal.Therefore, the optimal reproduction and dispersal strategy forearly terrestrial plants was the production of spores ratherthan gametes, ideally in very large numbers, to ensure survivaland germination of at least some of them. We regard the pre-sence of a multicellular sporophyte, resulting from a delay of

TABLE 1. Examples of ‘plant-specific’ proteins recently found instreptophyte and/or chlorophyte algae

Protein* Reference

Arabinogalactan-proteins Eder et al. (2008)BIP 2 Nedelcu et al. (2006)Class II homeodomain-leucin zipper Floyd et al. (2006)Embryophyte type of cellulose synthase Ces A Roberts and Roberts (2004)Endotransglucosylase (XET; MXE) Van Sandt et al. (2007),

Fry et al. (2008)GAPDHB Petersen et al. (2006),

Simon et al. (2006)MIKc-type MADS-box Tanabe et al. (2005)

* BIP, binding protein; GAPDHB, glyceraldehyde 3-phosphatedehydrogenase isoform B; MXE, mixed-linkage-glucan: xyloglucanendotransglucosylase; XET, xyloglucan endotransglucosylase.

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Oceani Ulvophyceae (e.g. Ulvales Dasycladales, Bryopsidales, Cladophorales)i ‘Prasinophytes’ (e.g. Mamiellales, Pyramimonadales)

B. Paleozoic Era: Ordovician–early Devonian Period (approx. 490–400 MY ago)

Ancient Chlorophyta:several clades of marine‘prasinophyte’ flagellatesand/or coccoids

Four cladesof derived

Chlorophyta:

Adapta

tion o

f Chlo

rophyc

eae

and Tr

ebouxio

phycea

e to

fresh

water

hab

itats

Ulvophy

ceae

(mar

ine)

Chloro

dendra

les

(mar

ine)

Chloro

phyce

ae

(fr

eshw

ater

, soil

)

Treb

ouxiophy

ceae

(fr

eshw

ater

, soil

)

CHLOROPHYTA

Phycoplast

Ancient Chlorophyta:marine and brackish

leiosphaerids and tasmanitids –ancestors of extant ‘prasinophytes’

(scaly green flagellates and coccoids)

Ancient Streptophyta:unknown ancestors of extant streptophyte lineages –freshwater flagellates, coccoids,sarcinoids and filaments ancestors of Mesostigma

and Chlorokybus (scaly freshwater flagellates)

Phragmoplast

STREPTOPHYTA

EMBRYOPHYTA (bryophytes, lycophytes, ferns, spermatophytes)

Charales (stoneworts - branched filaments organized as a main axis and whorls, resembling Equisetum)

Coleochaetales (parenchymateous branched filaments)

Zygnematales (conjugating green algae; unicells or unbranched filaments)

Klebsormidiales and Entransia (unbranched filaments)

Mesostigma and Chlorokybus (flagellate, sarcinoid)

CHLOROPHYTA STREPTOPHYTA

Freshwater

C. Paleozoic to Mesozoic Era: Carboniferous–Cretaceous Period (approx. 360–65 MY ago)

A. Neoproterozoic Era: Cryogenian–Ediacaran Period (approx. 850–540 MY ago)

Ocean

Freshwateri Chloro- and Trebouxiophyceae (Chlorophyceae dominated freshwater phytoplankton communities after the Permian/Triassic mass extinction 250 MY ago)i Streptophyte algae (mainly Charales and Zygnematales)i Embryophyte water plants (first aquatic angiosperms: early Cretaceous Period)

i Rapid adaptive radiation of Chloro- and Trebouxiophyceae

i Gradual reduction in diversity and abundance of streptophyte green algae (exception: evolutionary diversification and speciation of the Zygnematales during the Jurassic and Cretaceous Period)

FI G. 2. Diversification of green plants (Viridiplantae) and colonization of terrestrial habitats by streptophyte algae. Three stages are shown: (A) early evolutionof the viridiplant algae during the Neoproterozoic era; (B) colonization of terrestrial habitats by streptophyte algae during the Palaeozoic era; and (C) origin ofcurrent freshwater ecosystems during the Palaeozoic to Mesozoic era. The smaller freshwater body illustrates an acidic bog-pool with zygnematalean algae. Green

algae and embryophytes are illustrated in different tones of green: dark (Streptophyta) vs. bright green (Chlorophyta).

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meiosis, as the first adaptation to terrestrial life. The erect spor-ophyte morphology with terminal sporangia optimized thelong-range dispersal of spores, whereas the haploid gameto-phyte generation usually remained on the ground, since the‘traditional’ oogamous fertilization (eggs and sperm cells)required free water. The embryophytes of the Rhynie chertLagerstatte (early Devonian) already showed a size differencebetween 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 thesporophyte generation to form highly differentiated and auton-omous plant bodies was exploited only later by lycophytes,ferns and seed plants.

Interestingly, the haploid/diploid transition inChlamydomonas is regulated by two homeobox proteins ofthe KNOX/BELL protein family (Lee et al., 2008). In embry-ophytes BELL and KNOX homeodomain proteins areinvolved in maintaining the shoot apical meristem (Arielet al., 2007) and form part of a large protein family[homeodomain- (HD) containing proteins] associated withvarious cell differentiation events. Members of the ‘plant-specific’ HD-ZIP subfamily have now also been reportedfrom streptophyte algae (Floyd et al., 2006). Thus it seemslikely that the sporophyte originated by simple changes inthe expression pattern of homeobox proteins of the BELL/KNOX family followed by an expansion and diversificationof the HD-containing proteins to become important regulatorsof cell differentiation.

Early diversification and progressive extinction: explanations ofwhy an evolutionary key group such as the streptophyte algaeconsists of only a few extant lineages

Extant streptophyte algae display a surprisingly low diver-sity (about 13 families, 122 genera), in contrast to theChlorophyta with about 100 families containing 700 genera.The series of evolutionary events that shaped the current distri-bution and diversity of green algae can be tentatively recon-structed from molecular phylogenies and the scarce fossilrecord of algae and early land plants (summarized in Fig. 2).After their separation from ancient marine Chlorophyta, strep-tophyte algae conquered freshwater habitats worldwide, andprobably were the only eukaryotic freshwater algae duringthe Precambrian (Fig. 2). They coexisted ‘side by side’ withtheir embryophyte descendents, at least before the appearanceof the first aquatic embryophytes (Cretaceous; Martın-Closas,2003), and with their marine ‘sisters’ (Chlorophyta). Whatcaused the failure of streptophyte algae to dominate the fresh-water permanently? At first, two catastrophic events signifi-cantly reduced the streptophyte diversity, as is obvious fromthe fossil record of the Charales: the Permian/Triassic andthe Cretaceous/Tertiary mass extinctions, both probablyrelated to volcanism and/or asteroid impact and accompaniedby climatic changes. For example, the Permian/TriassicBoundary event (250 MY ago) marked the extinction ofthose Charales with anti-clockwise oogonia, and from thenon, the enveloping cells of charalean oogonia display themodern clockwise coiling pattern. The Cretaceous/Tertiaryextinction (65 MY ago), which is known as the end of the

Mesozoic dinosaur age, caused the extinction of the charaleanfamily Clavatoraceae, and an ongoing progressive reduction ofthe diversity of the surviving Charales (Martın-Closas, 2003;Soulie-Marsche, 2004; Martın-Closas and Wang, 2008).Except for the Charales, the fossil record of streptophytealgae is unfortunately rather poor, and thus we can only specu-late about the disappearance of other ancient groups of strepto-phyte algae by mass extinctions. It is currently unclear whetherfurther catastrophes such as the recent ice ages have alsoshaped the freshwater flora.

The second problem streptophyte algae were confrontedwith was the invasion of freshwater habitats by other algaeand/or plants, followed by harsh competition for light, spaceand nutrients. At first, modern groups of Chlorophyta (primar-ily marine green algae) appeared after a new mode of cell div-ision was introduced, the phycoplast, which enabled complexmulticellular growth (analogous to the streptophyte phragmo-plast; Fig. 2B). Two of these derived groups, the classesChlorophyceae and Trebouxiophyceae, switched almost com-pletely towards freshwater habitats. Since about the Permian/Triassic mass extinction (250 MY ago; Fig. 2B, C), thesegroups dominated the freshwater phytoplankton (Martın-Closas, 2003) and apparently brought the hegemony of strep-tophyte algae in their original habitat to an end. It remainsunclear whether the appearance of (better-adapted?)Chlorophyceae and Trebouxiophyceae was the main reasonfor the reduction of streptophyte diversity via competition, orwhether they just radiated into a largely empty freshwater eco-system after the previously dominant streptophyte algae hadalready been reduced, like successive ‘dynasties’ of greenalgae. 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(Martın-Closas, 2003), and further competed with the surviv-ing streptophyte algae, which never again reached the diversityand ecological dominance they once had.

CONCLUSIONS

There is now agreement that embryophytes originated fromstreptophyte algae. Their primary freshwater adaptation appar-ently played a key role in the colonization of dry land habitats.However, the branching order of streptophyte algae is far fromsettled. A complete understanding of the evolution of landplants will require the remaining phylogenetic questions tobe solved and genome evolution within streptophytes to beaddressed. The latter requires genome information on strepto-phyte algae. While a growing number of genomes of chloro-phyte algae have been sequenced, currently there is to ourknowledge not a single genome project (except ESTs) onany streptophyte alga. Without any genome sequence of astreptophyte alga for comparison, our picture of the evolutionof embryophytes remains far from complete.

ACKNOWLEDGEMENTS

This paper is dedicated to Prof. Dr M. Melkonian on theoccasion of his 60th birthday, a pioneer in evolutionarystudies on green algae.

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