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The Basal Position of Scaly Green Flagellates Among the Green Algae (Chlorophyta) Is Revealed by Analyses of Nuclear-Encoded SSU Rrna Sequences

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The Basal Position of Scaly Green Flagellates Among the Green Algae (Chlorophyta) Is Revealed by Analyses of Nuclear-Encoded SSU Rrna Sequences Protist. Vol. 149,367-380, December 1998 © Gustav Fischer Verlag Protist ORIGINAL PAPER The Basal Position of Scaly Green Flagellates among the Green Algae (Chlorophyta) is Revealed by Analyses of Nuclear-Encoded SSU rRNA Sequences a b c b c Takeshi Nakayama , Birger Marin , Harald D. Kranz ,1, Barbara Surek , Volker A. R. Huss , a b Isao Inouye , and Michael Melkonian ,2 alnstitute of Biological Sciences, University of Tsukuba, Tsukuba, Ibaraki 305, Japan bBotanisches Institut, Lehrstuhll, Universitat zu Koln, Gyrhofstr. 15, D-50931 Koln, Germany clnstitut fOr Botanik und Pharmazeutische Biologie, Universitat Erlangen, Staudtstr. 5, D-91 058 Erlangen, Germany Submitted August 11, 1998; Accepted September 30, 1998 Monitoring Editor: Robert A. Andersen The prasinophytes comprise a morphologically heterogeneous assembly of mostly marine flagellates and coccoid taxa, which represent an important component of the nano- and picoplankton, and have previously figured prominently in discussions about the origin and phylogeny of the green plants. To evaluate their putative basal position in the Viridiplantae and to resolve the phylogenetic relation­ ships among the prasinophyte taxa, we determined complete nuclear-encoded SSU rRNA sequences from 13 prasinophyte taxa representing the genera Cymbomonas, Halosphaera, Mamiella, Manto­ niella, Micromonas, Pterosperma, Pycnococcus, and Pyramimonas. Phylogenetic analyses of SSU rRNA sequences using distance, parsimony and likelihood methods revealed four independent prasinophyte lineages (clades) which constitute the earliest divergences among the Chlorophyta. In order of their divergence these clades are represented by the genera Cymbomonas, Halosphaera, Pterosperma, Pyramimonas (clade I), Mamiella, Mantoniella, Micromonas (clade II), Pseudoscourfie/­ dia (strain CCMP 717), Nephroselmis (clade III), and Tetraselmis, Scherffelia (clade IV). The coccoid Pycnococcus provasolii diverged after clade II, but before clade III. Since no other coccoid prasino­ phyte taxa were analyzed in this study, the phylogenetic status of this taxon is presently unresolved. Our analyses provide further evidence for the basal phylogenetic position of the scaly green flagel­ lates among the Chlorophyta and raise important questions concerning the class-level classification of the Chlorophyta. Introduction 1Current address: Abteilung Biochemie, Max-Planck-Institut fOr Green plants, the Viridiplantae sensu Cavalier-Smith ZOchtungsforschung, Carl-v.-Linne-Weg 10, D- 50829 Ktiln, (1981; see also Sluiman 1985), represent a mono­ Germany 2Corresponding author; phyletic lineage of eukaryotic organisms which fax 49-2214705181 comprises the green algae and the embryophyte e-mail [email protected] land plants. The unique type of plastid (Le. the 368 T. Nakayama et al. chloroplast; for classification of plastid types see phytes (for a review of different classification Melkonian 1996) with chlorophylls a and b, two en­ schemes of prasinophytes see Sym and Pienaar velope membranes, stacked thylakoids and in­ 1993) have remained largely unexplored. As to be traplastidial starch, and the equally unique type of expected from a basal lineage, a previous analysis flagellar transitional region (the 'stellate structure'; of SSU rRNA sequence comparisons involving four Melkonian 1984) provide synapomorphic characters genera of prasinophytes (Steink6tter et al. 1994) for the group. Ultrastructural and molecular analy­ demonstrated that the prasinophytes are not mono­ ses have resulted in the recognition of two major lin­ phyletic but at most paraphyletic within the Chloro­ eages within the Viridiplantae now generally recog­ phyta, since two independent basal lineages were nized as the Streptophyta and the Chlorophyta (Bre­ identified corresponding to the previously recog­ mer 1985; Sluiman 1985; recent reviews: Friedl nized orders Pseudoscourfieldiales and Chloroden­ 1997; Huss and Kranz 1997; McCourt 1995; Melko­ drales (Melkonian 1990a). Addition of three more nian and Surek 1995). Whereas the Streptophyta prasinophyte taxa (Le. Pterosperma, Mantoniella, comprise an assemblage of green algal lineages and Mesostigma) to a phylogenetic analysis of 67 previously classified as the Charophyceae sensu taxa of Viridiplantae led to the tentative recognition Mattox and Stewart (1984) and additionally the em­ of two additional independent lineages of prasino­ bryophyte land plants (bryophytes, ferns and sper­ phytes, one of which (Le. Mesostigma) occupied a matophytes), the Chlorophyta contain all green position within the Streptophyta (Melkonian et al. algae except for the charophyte lineages. It is widely 1995). It became apparent that in order to resolve held that scaly green flagellates (their cell surface is phylogenetic relationships among prasinophytes, a covered by non-mineralized organic scales, Manton more comprehensive analysis was required. Here, and Parke 1960; for a more recent review of the we present a detailed phylogenetic analysis of the prasinophytes: Sym and Pienaar 1993) were pre­ phylogenetic position of prasinophytes among the sumably ancestral to both the Streptophyta and the Chlorophyta based on sequence comparisons of Chlorophyta. The main rationale for this assumption complete nuclear-encoded SSU rRNA from a total has been the fact that flagellate reproductive cells of 12 genera (16 taxa) of prasinophytes. We identify (zoospores, gametes) of some taxa in both phyla are at least four independent basal lineages of prasino­ covered by a layer of square-shaped scales (40-50 phytes, their order of divergence, and discuss puta­ nm in diameter), which also occur as an underlayer tive trends in the early evolution of the Chlorophyta. in many prasinophytes but nowhere outside the Viridiplantae. Previous phylogenetic analyses in­ volving comparisons of complete nuclear-encoded Results SSU rRNA sequences of selected prasinophyte taxa with other green algae have supported this notion, To position the prasinophyte taxa within the SSU as the scaly green flagellates have invariably occu­ rRNA phylogeny of the Viridiplantae we first per­ pied basal positions in the phylogenetic trees (Friedl formed a global analysis of nuclear-encoded SSU 1997; Huss and Kranz 1997; Melkonian and Surek rRNA sequences of 66 taxa of Viridiplantae (includ­ 1995; Melkonian et al. 1995; Steink6tter et al. 1994). ing both Streptophyta and Chlorophyta) using three However, until now only 7 out of the 17 recognized glaucocystophyte sequences as outgroups (Fig. 1). genera of prasinophytes have been incorporated Results of distance and maximum parsimony analy­ within a single molecular phylogenetic analysis ses revealed that all prasinophyte taxa studied were (Melkonian et al. 1995) and thus the relationships positioned with the Chlorophyta which formed a among the various genera and lineages of prasino- monophyletic lineage (supported by bootstrap val- Figure 1. Phylogeny of the Viridiplantae based on nuclear-encoded SSU rRNA sequence comparisons inferred with the neighbor joining and maximum parsimony method using a total of 1655 aligned positions. The phyloge­ netic tree shown is that of the neighbor joining (Kimura 1980; Saitou and Nei 1987) method (the distance that corre­ sponds to 3% sequence divergence is indicated by the scale). The phylogeny is rooted with the glaucocystophyte taxa Cyanophora paradoxa, Glaucocystis nostochinearum, and Cyanoptyche gloeocystis. Bootstrap values of dis­ tance (neighbor joining; number of above the nodes; 100 replications) and weighted maximum parsimony (number below the nodes; 100 replications) analyses using the identical dataset are indicated (only values >50% were recorded). * the topology in the weighted parsimony analysis is different [the Mamiellales (clade II) diverged with a 81 % bootstrap value directly after clade I; as in Fig. 2]. The prasinophyte taxa are printed in bold type. For further details see Results. Prasinophyte Ancestry of the Chlorophyta 369 .--------Sphagnumpalustre Mnium hornum Hylocomium splendens Funaria hygrometrica L- Marchantia polymorpha Fossombronia pusilla 71 Pellia epiphylla 95 L- Anthoceros agrestis L I*OO~_--lC===G~in~g~ko biloba 100 Pinusluchuensis __-jI~OO~_--i__....:Lychnothamnus barbatus L-__~I~__--1r 100 Chara foetida Streptophyta 100 L-----Nitellaflexilis ...---Mesotaenium caldariorum Mougeotia scalaris r----------Genicularia spirotaenia Staurastrum sp. M752 Cosmarium botrytis Coleochaete scutata Coleochaete orbicularis L- Klebsormidium flaccidum L- Chlorokybus atmophyticus ~--- Mamiella gilva 100 100 Mantoniella antarctica 100 100 95 Mantoniella squamata 100 Micromonas pusilla * .-----Cymbomonas sp. L..-----Halosphaera sp• .----Pyramimonas disomata Pyramimonas propulsa IUlL--- Pyramimonas olivacea L..----Pyramimonasparkeae L- Pterosperma cristatum 100 Dunaliella salina 100 L- Asteromonas gracilis L- Chlamydopodium starrii 100 Chlamydomonas reinhardtii 100 Volvox carteri Hydrodictyon reticulatum 80 Pediastrum duplex 83 Scenedesmus abundans Scenedesmus obliquus ...---- Neochloris aquatica L- Characium hindakii 92 L..- Ankistrodesmus stipitatus Chlorophyta 98 ...------Prototheca wickerhamii riiVi1,,----- Nanochlorum eucaryotum Chlorella vulgaris 1.- Oltmannsiellopsis viridis 61 Trebouxia impressa Trebouxia asymmetrica Myrmecia biatorellae Myrmecia israelensis L- Trebouxia magna Microthamnion kuetzingianum Fusochloris perforatum 1.- Leptosira terrestris 100 Acrosiphonia sp. 100 100 Ulothrix zonata 100 Pseudendoclonium basiliense 72 91'L--- Gloeotilopsis
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