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Phylogeny and Classification of Zygnematophyceae (Streptophyta): Current State of Affairs

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Phylogeny and Classification of Zygnematophyceae (Streptophyta): Current State of Affairs Fottea 8(2): 87–104, 2008 87 REVIEW Phylogeny and classification of Zygnematophyceae (Streptophyta): current state of affairs Andrey A. GONTCHAROV Institute of Biology and Soil Science, 690022, Vladivostok-22, Russia, e-mail: [email protected] Abstract: Conjugates (Zygnematophyceae) represent the most species-rich (ca. 4000 spp) algal lineage within the Streptophyta. Studies using various molecular markers have placed the class as one of the crown groups in Streptophyta and even suggested a close relationship between the zygnematophycean algae and land plants. Phenotypic diversity complicates systematics of the class and the relationships between its taxa remain poorly understood. Molecular phylogenetic analyses have established a number of clades in the class and revealed a disagreement between the traditional taxonomic structure of Zygnematophyceae and the pattern of phylogenetic relationships between the class members. In this paper, an overview of recent advances in our understanding of the phylogeny and classification of conjugating green algae is presented, with emphasis on the major clades established in the class, the clades’ structure and polyphyly of some genera. We describe the areas of conflict and agreement between molecular phylogeny and traditional morphology-based taxonomy and stress that phenotypic characters provide little evidence for inferring relationships between taxa even at low taxonomic levels. Key words: conjugates, phylogenetic relationship, polyphyly, Streptophyta, Zygnematophyceae Introduction Ultrastructural and molecular phylogenetic data suggested clear affinities of the conjugating green Green conjugating algae comprise coccoid, algae with a paraphyletic assemblage of algae filamentous and colonial forms that are distinct in previously known as the Charophyceae (sensu a unique type of sexual reproduction (conjugation, MATTOX & STEWART 1984) and the embryophyte land first recognized by AUCHERV 1803), the complete plants (PICKETT -HEA P S 1975, MATTOX & STEWART absence of flagellate reproductive stages, and 1984, recent reviews by LEWIS & MCCOURT , 2004, centriolar centrosomes through the life cycle. MCCOURT et al. 2004). In a cladistic framework The conjugates have fascinated professional and (BRE M ER 1985, BRE M ER et al. 1987, KENRICK & amateur microscopists for over 200 years because CRANE 1997) the conjugating green algae lineage of their morphological diversity and complex is designated as the class Zygnematophyceae cell symmetry, which make them organisms within the division Streptophyta [Streptobionta of great natural beauty. This attraction resulted (KENRICK & CRANE 1997)], which, together with the in the description of more than 4000 species Chlorophyta, form the green plants [Viridiplantae that are classified in ca. 60 genera (HOSHAW & or Chlorobionta (CAVALIER -SM ITH 1981, KENRICK MCCOURT 1988, GERRATH 1993, Appendix). It is & CRANE 1997)]. It appears that the name of the not really known whether this number reflects class, Zygnematophyceae ROUND (1971), is an natural diversity in the group or not because illegitimate substitute for the Conjugatophyceae other estimates range from 1500 to 12000 spp EN G LER (1892) because Conjugata (Spirogyra) is (CRANWELL et al. 1990, HOSHAW et al. 1990). not a synonym for Zygnema (see SILVA 1980). Also, the class was described without a Latin diagnosis The distinctness of the conjugates and their and therefore it is not a validly described taxon. alliance with the green algae has never been in doubt (BROOK 1981). However, the relationships Classification schemes of the Zygnematophyceae between the families, genera and species of the have generally been based on morphology, conjugates as well as the genus concepts in the emphasizing cell wall ultrastructure, cellular group have remained controversial and elusive. organization (unicells, filaments), and chloroplast 88 GONTCHAROV : Phylogeny and classification of Zygnematophyceae structure (MIX 1972, PRESCOTT et al. 1972, 1975, was obtained as early as in 1985 (HORI et al. 1985), HOSHAW & MCCOURT 1988, GERRATH 1993). phylogenetic relationships in the group are far Two orders based on cell wall ultrastructure from being well established. Here my attempt is to are recognized within the Zygnematophyceae, summarize recent studies that have addressed the namely, the Zygnematales and the Desmidiales evolution and taxonomy of the Zygnematophyceae (Mi x 1972, Rů ž i č k a 1977). The Zygnematales from a molecular phylogenetic perspective. This are characterized by smooth cell walls consisting paper briefly discusses the class closest relatives, of a single piece lacking pores and other or- the types of molecular data used to analyse namentations. Zygnematalean taxa forming relationships within the Zygnematophyceae, the filaments are distinguished as the family major clades established in the class and point Zygnemataceae from the unicellular algae out discordance between the class phylogeny and classified as the Mesotaeniaceae, formerly known taxonomy, arguing that considerable work remains as ‘‘saccoderm desmids’’ (TRANSEAU 1951, to be done before a convincing picture emerges. PRESCOTT 1972, GERRATH 1993, KADLU B OWSKA 1984). The Desmidiales (‘‘placoderm desmids’’) Phylogylogenetic position within Streptophyta have cell walls consisting of two or more pieces Conjugating green algae have been always having ornamentations and pores (Mix 1972). considered as members of the green plant Based on cellular organization and cell wall lineage because of their pigments and starch as features the Desmidiales are subdivided into a reserve product (BROOK 1981), althought in three or four families (MIX 1972, KOUWETS & some classification schemes conjugates have been COESEL 1984, BROOK 1981, GERRATH 1993), regarded as a class distinct from the other green the Peniaceae, Gonatozygaceae, Closteriaceae, algae (FOTT 1971, ROUND 1971, BOLD & WY NNE and Desmidiaceae. Genera and species of 1985). Even when classified within Chlorophyta, the Zygnematophyceae are based mostly on the conjugates have been seen as a group with rather differences in cell organization (filaments/ unclear relationships due to the uniqueness of their unicells), cell symmetry, size and shape, cell wall defining characters. Ultrastructural studies in the projections and ornamentations, and chloroplast conjugates revealed cytokinesis by a phragmoplast structure. In most taxa neither the stability of the allying them with the Charales, Coleochaete, a few taxonomic characters nor their evolutionary status other algal taxa and embryophyte plants (FOWKE (plesiomorphic or apomorphic) has been studied & PICKETT -HEA P S 1969a, b, PICKETT -HEA P S 1975, in any detail. MATTOX & STEWART 1984, GROLI G 1992). Further biochemical and molecular data has shown an Generally, evolution of morphological traits advanced position of the class Zygnematophyceae in the class is not well understood. There was among streptophyte algae but were not conclusive a number of hypotheses regarding origin and regarding its exact placement there because evolution of certain phenotypical character but their results were affected by insufficient taxon these were largely logical constructions that often sampling, weak resolving power of the markers contradicted each other in very basic assumptions. used or long-branch attraction artefact (KRANZ Particularly this refers to the ancestral growth habit & HUSS 1996, BHATTACHAR Y A & MEDLIN 1998, (filamentous or unicellular), chloroplast type and CHA pm AN et al. 1998, QIU & PAL M ER 1999, degree of the cell radiation (WEST & WEST 1904, MCCOURT et al. 2000). WEST & FRITSCH 1927, PRESCOTT 1948, TEILIN G 1950, 1952, RANDHAWA 1959, YA M A G ISHI 1963, A phylogeny based on four genes from three PRESCOTT et al. 1977, HOSHAW & MCCOURT 1988). genomes (the nuclear 18S rRNA, the chloroplast atpB and rbcL and the mitochondrial nad5) In the last two decades molecular phylogenetic suggested that the conjugates diverged after analyses have advanced our understanding of the Mesostigma, Chlorokybus and Klebsormidium relationships between plants at different levels, but before Coleochaete and Chara. The latter was have challenged many long-standing hypotheses resolved as a sister to the land plants with high on plants evolution and significantly affected their support (KAROL et al. 2001, MCCOURT et al. 2004). systematics. The conjugates are not an exception Generally this sistership is in agreement with in this respect, however, apart from the fact that the hypotheses on evolution of morphological, the first zygnematophycean nucleotide sequence ultrastructural and biochemical characters that Fottea 8(2): 87–104, 2008 89 accompanied the emergence of streptophyte algae many other groups of organisms where introns from an aquatic habitat and the colonization of generally have patchy distribution (DUJON 1989, the land (GRAHA M 1993, 1996, LEWIS & MCCOURT BHATTACHAR Y A et al. 1996). Analyses of the intron 2004, MCCOURT et al. 2004, Fig. 1). However, the secondary structure and self-splicing capacity in following analyses of chloroplast small and large the class revealed that it has undergone significant subunit rRNA contended the sister relationship changes after the enter event dated ca. 350-400 between Charales and embryophytes (TUR M EL Mya (BHATTACHAR Y A et al. 1994, 1996, BESENDAHL et al. 2002). As a further development in this & BHATTACHAR Y A 1999). controversial issue, analysis of 76 cpDNA- encoded genes resolved the conjugates as sister to A growing
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