Streptophyte Algae and the Origin of Embryophytes

Home , Chlorodendrales, Coleochaetophyceae, Dasycladales, Mesostigma, Mesostigmatophyceae

Annals of Botany 103: 999–1004, 2009 doi:10.1093/aob/mcp044, available online at www.aob.oxfordjournals.org BOTANICAL BRIEFING Streptophyte algae and the origin of embryophytes

Burkhard Becker* and Birger Marin* Botanisches Institut, Universita¨tzuKo¨ln, Gyrhofstr. 16, 50931 Ko¨ln, Germany

Received: 11 November 2008 Returned for revision: 15 December 2008 Accepted: 6 February 2009 Published electronically: 8 March 2009 Downloaded from https://academic.oup.com/aob/article-abstract/103/7/999/104345 by guest on 12 September 2019 † Background 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. † Recent Progress 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. † Conclusions 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.

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

INTRODUCTION molecular physiology and genome evolution as well as primary adaptations and evolutionary trends, which were The Viridiplantae (Latin for ‘green plants’) include all green important for the origin of true land plants. 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 PHYLOGENY OF THE STREPTOPHYTA biochemistry. The colonization of terrestrial habitats by des- The phylogenetic relationships within the Viridiplantae were cendents of streptophyte algae started approx. 470–450 MY summarized by Lewis and McCourt (2004). Most phyloge- ago (Ordovician period; reviewed in Sanderson et al., 2004), netic relationships proposed at that time appear to be still and was undoubtedly one of the most important steps in the valid. The Viridiplantae split early into two evolutionary evolution of life on earth (Graham, 1993; Kenrick and lineages: Chlorophyta and Streptophyta (Fig. 1A). This split Crane, 1997; Bateman et al., 1998). The evolution of the occurred about 725–1200 MY ago, according to different esti- various groups of land plants (embryophytes ¼ bryophytes, mates by molecular clock methods (Hedges et al., 2004; Yoon pteridophytes and spermatophytes) resulted in our current ter- et al., 2004; Zimmer et al., 2007). Within the streptophyte restrial ecosystems (Waters, 2003) and significantly changed algae six morphologically distinct groups were recognized: the atmospheric oxygen concentration (Berner, 1999; Scott the flagellate Mesostigmatales, sarcinoid Chlorokybales, fila- and Glasspool, 2006). In this Briefing we will first describe mentous (unbranched) Klebsormidiales, the Zygnematales recent progress in our understanding of the phylogenetic (characterized by conjugation as the method of sexual repro- relationships within the Viridiplantae with a focus on strepto- duction and total absence of flagellated cells), and the two phyte algae. We will then present new results and ideas in morphologically most complex groups, the Charales (stoneworts) and Coleochaetales, both of which are characterized * Both authors contibuted equally to this work. For correspondence, by true multicellular organization (with plasmodesmata) of e-mail [email protected] or [email protected] parenchyma-like thalli or branched filaments with apical # The Author 2009. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For Permissions, please email: [email protected] 1000 Becker & Marin — Streptophyte algae and the origin of embryophytes

A Chlorophyceae evolution of streptophyte algae and land plants in textbooks Trebouxiophyceae (e.g. Raven et al., 2005) or review articles (Lewis and Ulvophyceae Chlorophyta McCourt, 2004; McCourt et al., 2004; Qiu, 2008), the Chlorodendrales Charales (stoneworts) are shown as sister to the embryophytes. Pseudoscourfieldiales This is supported by an analysis of four genes encoded by Coccoid prasinophytes et al. Mamiellales three cellular compartments (Karol , 2001). However, in Pyramimonadales recent phylogenetic analyses, either the Charales or alterna- Mesostigmatophyceae tively the Coleochaetales or Zygnematales are found as Chlorokybophyceae sisters to the land plants, depending on the gene(s) analysed Klebsormidiophyceae and the taxon sampling, but none of these topologies has con- Zygnemophyceae vincing statistical support. Analyses of chloroplast genomes Downloaded from https://academic.oup.com/aob/article-abstract/103/7/999/104345 by guest on 12 September 2019 Coleochaetophyceae Streptophyta tend to support the Zygnematales or a clade consisting of the Charophyceae Zygnematales and the Coleochaetales as sister to the embryo- Embryophytes phytes (Turmel et al., 2007). In contrast, in both our ongoing B Ulvophyceae work using a phylogenomic approach [similar to the one used Chlorophyceae for Mesostigma (Rodriguez-Ezpeleta et al., 2007) using five Chlorophyta Trebouxiophyceae streptophyte algae including Chara and Coleochaete; Chlorodendrales S. Wodniok, M. Melkonian, H. Philippe and B. Becker, Coccoid prasinophytes University of Cologne, Germany, unpubl. res.], or using com- Nephroselmidophyceae plete rRNA operons of the nuclear and plastidic genomes Pycnococcaceae (using ten streptophyte algae; B. Marin and M. Melkonian, Coccoid prasinophytes Mamiellales University of Cologne, unpubl. res.) we observed the Pyramimonadales Charales as sister to embryophytes, albeit with low statistical Mesostigmatales support. We are currently trying to test these results by Chlorokybales improved taxon sampling (rRNA trees) and the inclusion of a Klebsormidiales larger number of genes (phylogenomics). The phylogenetic Zygnematales relationships between the streptophyte algae we both currently Coleochaetales agree on are depicted in Fig. 1B. Streptophyta Charales Embryophytes Prasinophytes GENOME EVOLUTION WITHIN Streptophyte algae STREPTOPHYTES AND THE UNIQUENESS OF EMBRYOPHYTES F IG. 1. Phylogenetic relationships among the major lineages of the Viridiplantae. Branches indicated by dotted lines are not well supported. (A) Public literature databases (e.g. Web of Science) contain many According to Lewis and McCourt (2004), and (B) based on unpublished, references to proteins/genes that are considered to be plant- ongoing work by the authors. Some of the class names used by Lewis and McCourt (2004) have never been validly described, and for this reason we specific. Unfortunately, the term ‘plant-specific’ is often mis- use order designations in (B) and throughout the text. The informal term ‘pra- leading, and merely indicates that a protein is only known sinophytes’ is commonly used for scaly green flagellates (Mesostigmatales and from land plants (embryophytes) or spermatophytes, and there- basal Chlorophyta). fore the term spermatophyte- or embryophyte-specific would be much better. Horizontal gene transfer into embryophytes growth and oogamous sexual reproduction. The genus is extremely rare (Richardson and Palmer, 2006; Huang and Spirotaenia, usually classified as member of the Gogarten, 2008; Keeling and Palmer, 2008), with the excep- Zygnematales, probably represents an independent lineage tion of mitochondrial genes transferred from one plant to separate from the Zygnematales (Gontcharov and Melkonian, another (Richardson and Palmer, 2006; Keeling and Palmer, 2004). The branching order among streptophyte algae was 2008), and an ancient horizontal or endocytic gene transfer not resolved in 2004 and has subsequently been addressed from a chlamydial-type bacterium (Huang and Gogarten, by several publications, using rRNA and/or rbcL genes 2007; Becker et al., 2008) to the ancestor of Plantae (e.g. Hall et al., 2008), complete plastid genomes (e.g. (Glaucoplantae, Rhodoplantae and Viridiplantae). Therefore, Turmel et al., 2005, 2006), or phylogenomic approaches nearly all the genes present in extant embryophytes were inher- (Rodriguez-Ezpeleta et al., 2007). However, in phylogenetic ited from the eukaryotic host or the cyanobacterial endosym- trees obtained to date the divergence of streptophyte algae is biont of the common ancestor of all Plantae (Martin et al., still poorly resolved. The only major exception refers to the 2002). Thus, we should be very careful with terms such as phylogenetic position of Mesostigma. Called an enigma in ‘plant-specific gene’ (in the sense of embryophyte- or 2004 (Lewis and McCourt, 2004), recent work has now spermatophyte-specific) until at least a single genome of a firmly established that Mesostigma forms a clade with streptophyte alga is completely sequenced. Chlorokybus (Fig. 1B), both representing the earliest diver- We are convinced that many plant ‘innovations’ will actu- gence of streptophyte algae (Lemieux et al., 2007; ally turn out to be innovations of the streptophyte algae (or Rodriguez-Ezpeleta et al., 2007). In contrast, the question as the viridiplants), once complete streptophyte genomes to which group represents the sister to the embryophytes is become available and/or comparisons include chlorophyte far from being settled. In many illustrations depicting the genomes (Ostreococcus, Chlamydomonas). Recent examples Becker & Marin — Streptophyte algae and the origin of embryophytes 1001

TABLE 1. Examples of ‘plant-speciﬁc’ proteins recently found in Freshwater adaptation allowed a slow and gradual move streptophyte and/or chlorophyte algae towards moist habitats in the proximity of water, and ulti- mately the colonization of dry land, dependent on rainwater. Protein* Reference In contrast, the ecological gradient between marine and terrestrial habitats is very sharp (mainly salinity; but also extremes Arabinogalactan-proteins Eder et al. (2008) of temperature, exposure to high irradiance, dehydration, ultra- BIP 2 Nedelcu et al. (2006) Class II homeodomain-leucin zipper Floyd et al. (2006) violet radiation; Smith and Smith, 2006), and apparently did Embryophyte type of cellulose synthase Ces A Roberts and Roberts (2004) not enable the successful colonization of terrestrial regions by Endotransglucosylase (XET; MXE) Van Sandt et al. (2007), marine algae. Interestingly, the animal groups with major Fry et al. (2008) players in terrestrial habitats (insects and vertebrates) originated

GAPDHB Petersen et al. (2006), Downloaded from https://academic.oup.com/aob/article-abstract/103/7/999/104345 by guest on 12 September 2019 Simon et al. (2006) in freshwater environments and are still completely (amphi- MIKc-type MADS-box Tanabe et al. (2005) bians and insects) or largely (reptiles, birds and mammals) absent from the oceans (Vermeij and Dudley, 2000; Glenner * BIP, binding protein; GAPDHB, glyceraldehyde 3-phosphate et al., 2006). The same holds for streptophyte algae (strict fresh- dehydrogenase isoform B; MXE, mixed-linkage-glucan: xyloglucan water preference, with only a few Charales that tolerate brackish endotransglucosylase; XET, xyloglucan endotransglucosylase. habitats), and for the Embryophyta with primary terrestrial origin and adaptation, many secondary freshwater plants (bryophytes, ferns and angiosperms), and only very few derived of proteins/genes now also found in streptophyte and/or chlor- angiosperms adapted to marine, fully saline environments ophyte algae are given in Table 1. (the monocot sea-grasses, e.g. Zostera). A nice example is the ‘plant-specific’ vacuolar sorting Streptophytes adapted to deal with freshwater conditions receptor (formerly known as BP80). One of us has recently very early during their evolution, and probably were the first shown that this protein originated in the last common viridi- eukaryotic freshwater algae (Fig. 2A). For the foundation of plant ancestor and is present in the Chlorophyta and the the first terrestrial ecosystems, streptophytes were exploiting Streptophyta (Becker and Hoef-Emden, 2009). The overall an entirely new environment, almost free of competing organ- structure of the receptor has not changed in green algae and isms, probably with the exception of cyanobacteria and fungi land plants and the overall rate in sequence evolution (Labandeira, 2005). This situation allowed the explosive radi- appears to be slower in streptophytes than in chlorophytes. ation of early land plants, beginning in the Silurian period, This seems to be a general pattern. Similar slow evolution possibly earlier in the Ordovician or even Cambrian rates have been observed for many proteins in phylogenetic (Labandeira, 2005; Taylor and Strother, 2008), adapting their trees published in recent years. Embryophyte evolution morphology, physiology, life history and reproduction to appears mainly to involve expansion of protein families fol- land life (Fig. 2B). Any algal group that later developed a ten- lowed by differential expression rather than sequence vari- dency towards terrestrial and macrophytic life styles was con- ations. This seems also to be the case for the chloroplast fronted with the opposite situation: competition with already genome. Turmel et al. (2007) concluded that ‘most of the fea- adapted land plants. It is therefore not surprising that no tures typical of land plant chloroplast genomes were inherited second lineage of land plants evolved successfully besides from their green algal ancestors’. streptophytes.

What can be speculated about the origin and advantage of the NEW HYPOTHESES ABOUT THE ORIGIN OF sporophyte generation? EMBRYOPHYTES AND THE EVOLUTION OF STREPTOPHYTE ALGAE The major difference between streptophyte algae and embryophytes is the heteromorphic life history of the latter, Why were terrestrial environments conquered by only a single i.e. development of the zygote towards an embryo and a lineage of ‘true land plants’, which evolved from streptophyte diploid sporophyte generation. All streptophyte algae are hap- green algae? lonts with the zygote being the only diploid cell, which Given the diversity in morphology, cell architecture, life his- immediately undergoes meiosis (resulting in four meiospores). tories and reproduction, and biochemistry among photoauto- In contrast to gametes (eggs, sperms), spores are enclosed by a trophic eukaryotes, it is surprising that ‘true land plants’ pigmented cell wall composed of sporopollenin, an extremely evolved uniquely within the streptophytes. Terrestrial (micro) resistant biopolymer, and are thus well protected from preda- algae are present in several other algal groups (e.g. Cyano- tors, mechanical and chemical damage, degradation and muta- bacteria, diatoms, Chlorophyceae and Trebouxiophyceae); genic UV light. Interestingly again, sporopollenin evolved however, none of these algae ever rose above their substrate. within the streptophyte algae (Delwiche et al., 1989). Spores Macroalgae (Ulvophyceae, red and brown seaweeds) became are not protected from desiccation, but tolerate dehydration, dominant players in marine habitats but never invaded terres- which might even offer an advantage for spore dispersal. trial ecosystems. Why were streptophytes so successful in the Therefore, the optimal reproduction and dispersal strategy for colonization of terrestrial habitats? We suggest that strepto- early terrestrial plants was the production of spores rather phyte algae were physiologically pre-adapted to terrestrial than gametes, ideally in very large numbers, to ensure survival existence by their primary freshwater life style, in contrast to and germination of at least some of them. We regard the pre- their marine sister lineage, i.e. Chlorophyta (Fig. 2A). sence of a multicellular sporophyte, resulting from a delay of 1002 Becker & Marin — Streptophyte algae and the origin of embryophytes

C. Paleozoic to Mesozoic Era: Carboniferous–Cretaceous Period Freshwater (approx. 360–65 MY ago) i Chloro- and Trebouxiophyceae (Chlorophyceae dominated freshwater phytoplankton communities after the Ocean Permian/Triassic mass extinction i 250 MY ago) Ulvophyceae (e.g. Ulvales i Dasycladales, Bryopsidales, Streptophyte algae (mainly Charales Cladophorales) and Zygnematales) i i ‘Prasinophytes’ (e.g. Embryophyte water plants (first aquatic Mamiellales, angiosperms: early Cretaceous Period) Downloaded from https://academic.oup.com/aob/article-abstract/103/7/999/104345 by guest on 12 September 2019 Pyramimonadales)

i Rapid adaptive radiation of Chloro- and Trebouxiophyceae i Gradual reduction in diversity and abundance of streptophyte green algae (exception: evolutionary diversification B. Paleozoic Era: and speciation of the Zygnematales Ordovician–early during the Jurassic and Cretaceous Period) Devonian Period (approx. 490–400 MY ago)

ophyceae

Four clades Adaptation of Chlor of derived and Trebouxiophyceae to Chlorophyta: freshwater habitatsEMBRYOPHYTA (bryophytes, lycophytes, ferns, spermatophytes) Charales (stoneworts - branched filaments organized as a main axis and whorls, resembling Equisetum) , soil) Coleochaetales (parenchymateous branched filaments) Ancient Chlorophyta: , soil) several clades of marine Zygnematales (conjugating green algae; Ulvophyceae(marine) unicells or unbranched filaments) ‘prasinophyte’ flagellates Chlorophyceae and/or coccoids Trebouxiophyceae (freshwater (marine) Klebsormidiales and Entransia (freshwaterChlorodendrales (unbranched filaments) Mesostigma and Chlorokybus Phycoplast (flagellate, sarcinoid) Phragmoplast CHLOROPHYTA STREPTOPHYTA A. Neoproterozoic Era: Cryogenian–Ediacaran Period Freshwater (approx. 850–540 MY ago)

Ocean

Ancient Chlorophyta: Ancient Streptophyta: marine and brackish unknown ancestors of extant streptophyte lineages – leiosphaerids and tasmanitids – freshwater flagellates, coccoids, sarcinoids and filaments ancestors of extant ‘prasinophytes’ ancestors of Mesostigma (scaly green flagellates and coccoids) and Chlorokybus (scaly freshwater flagellates)

CHLOROPHYTA STREPTOPHYTA

F IG. 2. Diversification of green plants (Viridiplantae) and colonization of terrestrial habitats by streptophyte algae. Three stages are shown: (A) early evolution of the viridiplant algae during the Neoproterozoic era; (B) colonization of terrestrial habitats by streptophyte algae during the Palaeozoic era; and (C) origin of current 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). Becker & Marin — Streptophyte algae and the origin of embryophytes 1003 meiosis, as the first adaptation to terrestrial life. The erect spor- Mesozoic dinosaur age, caused the extinction of the charalean ophyte morphology with terminal sporangia optimized the family Clavatoraceae, and an ongoing progressive reduction of long-range dispersal of spores, whereas the haploid gameto- the diversity of the surviving Charales (Martıń-Closas, 2003; phyte generation usually remained on the ground, since the Soulie´-Ma¨rsche, 2004; Martıń-Closas and Wang, 2008). ‘traditional’ oogamous fertilization (eggs and sperm cells) Except for the Charales, the fossil record of streptophyte required free water. The embryophytes of the Rhynie chert algae is unfortunately rather poor, and thus we can only specu- Lagersta¨tte (early Devonian) already showed a size difference late about the disappearance of other ancient groups of strepto- between gametophytes and sporophytes [e.g. Cooksonia phyte algae by mass extinctions. It is currently unclear whether (Gerrienne et al., 2006); Rhynia (Kerp et al., 2004); further catastrophes such as the recent ice ages have also Aglaophyton (Taylor et al., 2005)]. Initially a dependent shaped the freshwater flora. ‘spore-producing organ’, the developmental potential of the The second problem streptophyte algae were confronted Downloaded from https://academic.oup.com/aob/article-abstract/103/7/999/104345 by guest on 12 September 2019 sporophyte generation to form highly differentiated and auton- with was the invasion of freshwater habitats by other algae omous plant bodies was exploited only later by lycophytes, and/or plants, followed by harsh competition for light, space ferns and seed plants. and nutrients. At first, modern groups of Chlorophyta (primar- Interestingly, the haploid/diploid transition in ily marine green algae) appeared after a new mode of cell div- Chlamydomonas is regulated by two homeobox proteins of ision was introduced, the phycoplast, which enabled complex the KNOX/BELL protein family (Lee et al., 2008). In embry- multicellular growth (analogous to the streptophyte phragmo- ophytes BELL and KNOX homeodomain proteins are plast; Fig. 2B). Two of these derived groups, the classes involved in maintaining the shoot apical meristem (Ariel Chlorophyceae and Trebouxiophyceae, switched almost com- et al., 2007) and form part of a large protein family pletely towards freshwater habitats. Since about the Permian/ [homeodomain- (HD) containing proteins] associated with Triassic mass extinction (250 MY ago; Fig. 2B, C), these various cell differentiation events. Members of the ‘plant- groups dominated the freshwater phytoplankton (Martıń- specific’ HD-ZIP subfamily have now also been reported Closas, 2003) and apparently brought the hegemony of strep- from streptophyte algae (Floyd et al., 2006). Thus it seems tophyte algae in their original habitat to an end. It remains likely that the sporophyte originated by simple changes in unclear whether the appearance of (better-adapted?) the expression pattern of homeobox proteins of the BELL/ Chlorophyceae and Trebouxiophyceae was the main reason KNOX family followed by an expansion and diversification for the reduction of streptophyte diversity via competition, or of the HD-containing proteins to become important regulators whether they just radiated into a largely empty freshwater eco- of cell differentiation. system after the previously dominant streptophyte algae had already been reduced, like successive ‘dynasties’ of green algae. Later, the first water embryophytes, dinoflagellates Early diversification and progressive extinction: explanations of (both since the Cretaceous, approx. 100 MY ago), diatoms why an evolutionary key group such as the streptophyte algae (Palaeocene, ca. 60 MY ago) and chrysophytes (Eocene, consists of only a few extant lineages approx. 40 MY ago) appeared in freshwater environments Extant streptophyte algae display a surprisingly low diver- (Martıń-Closas, 2003), and further competed with the surviv- sity (about 13 families, 122 genera), in contrast to the ing streptophyte algae, which never again reached the diversity Chlorophyta with about 100 families containing 700 genera. and ecological dominance they once had. The series of evolutionary events that shaped the current distri- bution and diversity of green algae can be tentatively recon- CONCLUSIONS structed from molecular phylogenies and the scarce fossil record of algae and early land plants (summarized in Fig. 2). There is now agreement that embryophytes originated from After their separation from ancient marine Chlorophyta, strep- streptophyte algae. Their primary freshwater adaptation appar- tophyte algae conquered freshwater habitats worldwide, and ently played a key role in the colonization of dry land habitats. probably were the only eukaryotic freshwater algae during However, the branching order of streptophyte algae is far from the Precambrian (Fig. 2). They coexisted ‘side by side’ with settled. A complete understanding of the evolution of land their embryophyte descendents, at least before the appearance plants will require the remaining phylogenetic questions to of the first aquatic embryophytes (Cretaceous; Martıń-Closas, be solved and genome evolution within streptophytes to be 2003), and with their marine ‘sisters’ (Chlorophyta). What addressed. The latter requires genome information on strepto- caused the failure of streptophyte algae to dominate the fresh- phyte algae. While a growing number of genomes of chloro- water permanently? At first, two catastrophic events signifi- phyte algae have been sequenced, currently there is to our cantly reduced the streptophyte diversity, as is obvious from knowledge not a single genome project (except ESTs) on the fossil record of the Charales: the Permian/Triassic and any streptophyte alga. Without any genome sequence of a the Cretaceous/Tertiary mass extinctions, both probably streptophyte alga for comparison, our picture of the evolution related to volcanism and/or asteroid impact and accompanied of embryophytes remains far from complete. by climatic changes. For example, the Permian/Triassic Boundary event (250 MY ago) marked the extinction of ACKNOWLEDGEMENTS those Charales with anti-clockwise oogonia, and from then on, the enveloping cells of charalean oogonia display the This paper is dedicated to Prof. Dr M. Melkonian on the modern clockwise coiling pattern. The Cretaceous/Tertiary occasion of his 60th birthday, a pioneer in evolutionary extinction (65 MY ago), which is known as the end of the studies on green algae. 1004 Becker & Marin — Streptophyte algae and the origin of embryophytes

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