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Molecular Phylogeny and Revision of the Genus Netrium (Zygnematophyceae, Streptophyta): Nucleotaenium Gen

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Molecular Phylogeny and Revision of the Genus Netrium (Zygnematophyceae, Streptophyta): Nucleotaenium Gen J. Phycol. 46, 346–362 (2010) Ó 2010 Phycological Society of America DOI: 10.1111/j.1529-8817.2010.00814.x MOLECULAR PHYLOGENY AND REVISION OF THE GENUS NETRIUM (ZYGNEMATOPHYCEAE, STREPTOPHYTA): NUCLEOTAENIUM GEN. NOV.1 Andrey A. Gontcharov2,3 and Michael Melkonian Botanisches Institut, Lehrstuhl I, Universita¨tzuKo¨ln, Gyrhofstr. 15, D-50931 Ko¨ln, Germany Nuclear-encoded SSU rDNA, chloroplast LSU Molecular phylogenetic studies have significantly rDNA, and rbcL genes were sequenced from 53 changed our perception of the relationships among strains of conjugating green algae (Zygnematophy- algal taxa and challenged the importance of many ceae, Streptophyta) and used to analyze phyloge- phenotypic characters traditionally used in algal sys- netic relationships in the traditional order tematics. As a result, the composition and taxo- Zygnematales. Analyses of a concatenated data set nomic structure of many algal taxa are uncertain, (5,220 nt) established 12 well-supported clades in requiring revision based on new monographic work. the order; seven of these constituted a superclade, Species richness and morphological diversity often termed ‘‘Zygnemataceae.’’ Together with genera complicate taxonomic studies, but morphologically (Zygnema, Mougeotia) traditionally placed in the fam- simple taxa revealing only few distinguishing charac- ily Zygnemataceae, the ‘‘Zygnemataceae’’ also ters often provide equal challenges for taxonomic included representatives of the genera Cylindrocystis revision. Both situations apply to the systematics of and Mesotaenium, traditionally placed in the family the conjugating green algae (Zygnematophyceae, Mesotaeniaceae. A synapomorphic amino acid Streptophyta), which comprise >4,000 species of uni- replacement (codon 192, cysteine replaced by cellular, filamentous, or colonial algae currently valine) in the LSU of RUBISCO characterized this classified into 55 genera, six families, and two superclade. The traditional genera Netrium, Cylindro- orders (Mix 1972, 1975, Ru˚ˇzicˇka 1977, Brook and cystis, and Mesotaenium were shown to be para- or Johnson 2002, Gerrath 2003). The large number of polyphyletic, highlighting the inadequacy of pheno- species described sets this class apart from the other typic traits used to define these genera. Species of relatively species-poor lineages of streptophyte green the traditional genus Netrium were resolved as three algae. Members of the Zygnematophyceae are fur- well-supported clades each distinct in the number of ther distinctive in their peculiar mode of sexual chloroplasts per cell, their surface morphology reproduction (i.e., conjugation) and in the absence (structure and arrangement of lamellae) and the of flagellate reproductive stages throughout their position of the nucleus or nuclear behavior during life history. cell division. Based on molecular phylogenetic analy- The orders and families of the Zygnematophy- ses and synapomorphic phenotypic traits, the genus ceae were established on the basis of cell wall ultra- Netrium has been revised, and a new genus, Nucleo- structure and cellular organization (i.e., filamentous taenium gen. nov., was established. The genus Plano- or unicellular), whereas most of the genera have taenium, also formerly a part of Netrium, was been defined by characters of cell morphology, such identified as the sister group of the derived as cell and semicell shape, ornamentation of the cell Roya ⁄ Desmidiales clade and thus occupies a key wall, degree of cell constriction, and, more rarely, position in the evolutionary radiation leading to the chloroplast shape. Most of these morphological most species-rich group of streptophyte green algae. characters are apparently late innovations that occur only in the derived order Desmidiales, which is Key index words: cp LSU rDNA; Netrium; Nucleotae- characterized by ornamented and porous cell walls nium;nuSSUrDNA;phylogeny;Planotaenium; composed of two or more parts (McCourt et al. rbcL; Zygnematales; Zygnematophyceae 2000, Gontcharov et al. 2003, 2004, Hall et al. Abbreviations: BI, Bayesian inference; BP, boot- 2008). The morphological diversity of the Desmidi- strap percentages; ML, maximum likelihood; MP, ales has led to the description of >3,000 species dis- maximum parsimony; NJ, neighbor joining; PP, tributed over 35 genera. Most of these genera, posterior probabilities; rbcL, LSU of RUBISCO however, have previously been regarded as artificial. gene Recent molecular phylogenetic studies that specifi- cally addressed the phylogeny of the Desmidiales and its most species-rich family, Desmidiaceae, fully supported this notion (Denboh et al. 2001, Nam 1Received 3 March 2009. Accepted 17 September 2009. 2Permanent address: Institute of Biology and Soil Science, RUS- and Lee 2001, Gontcharov et al. 2003, Moon and 690022, Vladivostok-22, Russia. Lee 2003, Gontcharov and Melkonian 2008, Hall 3Author for correspondence: e-mail [email protected]. et al. 2008). 346 MOLECULAR PHYLOGENY AND REVISION OF NETRIUM 347 In contrast, the order Zygnematales, comprising pected because Netrium, a genus with only 10 850 species classified in 17 genera that are split described species (Ohtani 1990, Gerrath 1993), is between two families, has received comparatively lit- morphologically relatively uniform, and its identity tle attention. Zygnematalean taxa are indistinct in has never been seriously questioned (West and West their cell wall ultrastructure (the simple cell wall is 1904, Kossinskaja 1952, Prescott et al. 1972, Brook nonfragmented without ornamentation or pores). and Johnson 2002, Gerrath 2003). The taxonomic The two families (Mesotaeniaceae, Zygnemataceae) history of the genus Netrium is briefly summarized were distinguished based on cellular organization: here: originally, Netrium taxa were included in the unicellular forms comprising the family Mesotaenia- genus Penium (Ralfs 1848). Subsequently, they were ceae (five genera and 65 species); and filamentous transferred to the genus Closterium as subgenus Netri- forms, the Zygnemataceae (12 genera with 800 um (Na¨geli 1849) and finally raised to genus level species). Chloroplast shape (stellate, laminate, or by Itzigsohn and Rothe (1856). However, Ralfs’s ribbon-like) was used as the major criterion to dis- classification was often favored (Bre´bisson 1856, de tinguish genera in both families (West and West Bary 1858, Archer 1861, Turner 1892) until 1904, Czurda 1932, Kolkwitz and Krieger 1941, Kos- Lu¨tkemu¨ller (1902) showed that Netrium differs sinskaja 1952, Kadlubowska 1984, Brook and John- from Penium by its smooth, one-piece cell wall lack- son 2002, Gerrath 2003). An apparent similarity in ing pores and the different mode of cell division, chloroplast shapes between filamentous and unicel- observations later confirmed by EM and life-history lular forms was recognized early, but relationships studies (Biebel 1964, Mix 1972). between the corresponding taxa remained specula- Each of the Netrium lineages established through tive. It was assumed that each chloroplast shape had sequence comparisons was distinct in the number of evolved only once, and unicellular (or filamentous, chloroplasts per cell (one, two, and four, respec- depending on the presumed ancestral state) forms tively), a feature affecting the position and behavior arose independently in each lineage characterized of the nucleus during cell division (Pickett-Heaps by a specific chloroplast shape, thus rendering 1975, Jarman and Pickett-Heaps 1990). These find- either the Mesotaeniaceae or the Zygnemataceae ings suggested that the traditional genus Netrium polyphyletic (Randhawa 1959, Yamagishi 1963, Ho- comprises several only distantly related and pheno- shaw and McCourt 1988). Alternatively, others typically distinct lineages (Gontcharov et al. 2004). favored a monophyletic origin of the unicellular or Here, we reinvestigated the molecular phylogeny filamentous taxa in the Zygnematales (West and and taxonomic status of Netrium using an extended West 1904, Prescott et al. 1972), implying extensive taxon sampling of unicellular Zygnematales (Netrium homoplasy in chloroplast shapes. s. l., Cylindrocystis, and Mesotaenium), mostly by isolat- Molecular phylogenetic analyses demonstrated ing new strains from natural populations. To the paraphyletic nature of the order Zygnematales improve phylogenetic resolution, we also extended and rejected the traditional concept of its two fami- the data set by including the chloroplast-encoded lies, Zygnemataceae and Mesotaeniaceae, neither of (cp) LSU rRNA genes in addition to the previously which is monophyletic as their taxa intermixed in a used nuclear-encoded SSU rDNA and rbcL in a con- basal clade of the Zygnematophyceae (McCourt catenated data matrix. Using this new data set et al. 2000, Gontcharov et al. 2003). It was also (5,220 positions), we confirmed that members of revealed that the genera Roya and Netrium, tradi- the traditional genus Netrium formed three robust tional members of Mesotaeniaceae, were only dis- clades in the phylogenetic tree of the Zygnemato- tantly related to other Zygnematales and instead phyceae and fully resolved the relationships among showed affinity to the derived order Desmidiales these clades. A detailed analysis of morphological (McCourt et al. 2000, Gontcharov et al. 2003). Due traits by conventional and confocal LM identified to their plastid morphology (axial, laminate chlo- morphological synapomorphies that characterize roplasts as in many Desmidiales), Roya and Netrium each clade. In consequence, we recognize one novel
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