DEEP DIVISION IN THE CHLOROPHYCEAE (CHLOROPHYTA) REVEALED BY CHLOROPLAST PHYLOGENOMIC ANALYSES¹

Abstract

The Chlorophyceae (sensu Mattox and Stewart) is a morphologically diverse class of the Chlorophyta displaying biflagellate and quadriflagellate motile cells with varying configurations of the flagellar apparatus. Phylogenetic analyses of 18S rDNA data and combined 18S and 26S rDNA data from a broad range of chlorophycean taxa uncovered five major monophyletic groups (Chlamydomonadales, Sphaeropleales, Oedogoniales, Chaetophorales, and Chaetopeltidales) but could not resolve their branching order. To gain insight into the interrelationships of these groups, we analyzed multiple genes encoded by the chloroplast genomes of Chlamydomonas reinhardtii P. A. Dang. and Chlamydomonas moewusii Gerloff (Chlamydomonadales), Scenedesmus obliquus (Turpin) Kütz. (Sphaeropleales), Oedogonium cardiacum Wittr. (Oedogoniales), Stigeoclonium helveticum Vischer (Chaetophorales), and Floydiella terrestris (Groover et Hofstetter) Friedl et O'Kelly (Chaetopeltidales). The C. moewusii, Oedogonium, and Floydiella chloroplast DNAs were partly sequenced using a random strategy. Trees were reconstructed from nucleotide and amino acid data sets derived from 44 protein-coding genes of 11 chlorophytes and nine streptophytes as well as from 57 protein-coding genes of the six chlorophycean taxa. All best trees identified two robustly supported major lineages within the Chlorophyceae: a clade uniting the Chlamydomonadales and Sphaeropleales, and a clade uniting the Oedogoniales, Chaetophorales, and Chaetopeltidales (OCC clade). This dichotomy is independently supported by molecular signatures in chloroplast genes, such as insertions ⁄ deletions and the distribution of transspliced group II introns. Within the OCC clade, the sister relationship observed for the Chaetophorales and Chaetopeltidales is also strengthened by independent data. Character state reconstruction of basal body orientation allowed us to refine hypotheses regarding the evolution of the flagellar apparatus.

Phylogeny and Molecular Evolution of the Green Algae

“…Within the OCC clade, the sister relationship observed for the Chaetophorales and Chaetopeltidales has also been supported by rDNA data Müller et al, 2004;Caisová et al, 2011) and similarities in zoospore structure (O'Kelly et al, 1994) and the occurrence of two trans-spliced group II introns at identical positions . These results have strengthened the notion that the ancestor of the Chlorophyceae was likely a quadriflagellate with a DO+DO configuration of the flagellar apparatus, and that the CW configuration evolved independently in the Chlamydomonadales and the Chaetophorales Turmel et al, 2008) (but see Nozaki et al, 2003, discussed below), and further suggest that the stephanokont zoospores of the Oedogoniales arose from the DO condition .…”

“…Traditional orders and genera were found to be polyphyletic while others were moved to other classes (e.g., Chlorellales) (see Lewis & McCourt, 2004 for a taxonomic history). Molecular and ultrastructural data have identified five major clades (Booton et al, 1998a;Wolf et al, 2002;Wolf et al, 2003;Turmel et al, 2008). The Chlamydomonadales is characterized by a CW flagellar apparatus orientation in biflagellate members, but quadriflagellate representatives may display various other orientations (Nakayama et al, 1996a;Nozaki et al, 2003;Watanabe et al, 2006b).…”

“…These datasets have mainly involved concatenated sequences of proteincoding genes that are shared among green algal chloroplast genomes. To date, 26 complete green algal plastid genomes have been sequenced and assembled (Wakasugi et al, 1997;Turmel et al, 1999b;Lemieux et al, 2000;Maul et al, 2002;Turmel et al, 2002b;Pombert et al, 2005;Turmel et al, 2005;Bélanger et al, 2006;de Cambiaire et al, 2006;Pombert et al, 2006;Turmel et al, 2006a;de Cambiaire et al, 2007;Lemieux et al, 2007;Robbens et al, 2007a;Brouard et al, 2008;Turmel et al, 2008;Turmel et al, 2009a;Turmel et al, 2009b;Zuccarello et al, 2009;Brouard et al, 2010;Brouard et al, 2011), in addition to more than 30 angiosperm plastid genomes (Soltis et al, 2009). Chloroplast genomes are particularly useful for phylogenetic reconstruction because of their relatively high and condensed gene content, in comparison to nuclear genomes.…”

New phylogenetic hypotheses for the core Chlorophyta based on chloroplast sequence data

“…Five orders are recognized within the class (Oedogoniales, Chaetophorales, Chaetopeltidales, Volvocales and Sphaeropleales), and the relationships among them are fairly well understood (Booton et al, 1998;Buchheim et al, 2001;Wolf et al, 2002;Turmel et al, 2008;Tippery et al, 2012). By contrast, higher classification within Ulvophyceae and especially Trebouxiophyceae is still unresolved.…”

Affinity, life cycle, and intracellular complexity of organic-walled microfossils from the Mesoproterozoic of Shanxi, China

“…Considering the sequence of phylogenetic divergences within the lineage Chloroplastida, which also reflects ecological adaptations from marine to fresh water environments and colonization of terrestrial realm, the Charophytes and land plants are derived and later evolved lineages (Paleozoic; Graham and Gray, 2001;Wellman et al, 2003;O'Kelly, 2007;Rubinstein et al, 2010) than primary lineages of Prasinophytes and Chlorophytes (Turmel et al, 2002(Turmel et al, , 2008Raven et al, 2005;Baldauf, 2008). Prasinophytes are known to reproduce asexually and, although producing protective cysts, they lack superficial processes.…”