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18S Ribosomal RNA Gene Phylogeny of a Colonial Volvocalean Lineage (Tetrabaenaceae-Goniaceae-Volvocaceae, Volvocales, Chlorophyceae) and Its Close Relatives

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18S Ribosomal RNA Gene Phylogeny of a Colonial Volvocalean Lineage (Tetrabaenaceae-Goniaceae-Volvocaceae, Volvocales, Chlorophyceae) and Its Close Relatives J. Jpn. Bot. 91 Suppl.: 345–354 (2016) 18S Ribosomal RNA Gene Phylogeny of a Colonial Volvocalean Lineage (Tetrabaenaceae-Goniaceae-Volvocaceae, Volvocales, Chlorophyceae) and Its Close Relatives a,b, a,b a,b Takashi NAKADA *, Takuro ITO and Masaru TOMITA aInstitute for Advanced Biosciences, Keio University, Kakuganji, Tsuruoka, Yamagata, 997-0052 JAPAN; bSystems Biology Program, Graduate School of Media and Governance, Keio University, Fujisawa, Kanagawa, 252-0882 JAPAN; *Corresponding author: [email protected] (Accepted on January 19, 2016) The lineage of colonial green algae consisting of Tetrabaenaceae, Goniaceae, and Volvocaceae (TGV-clade) belongs to the clade Reinhardtinia within Volvocales (Chlorophyceae). Reinhardtinia is closely related to some species in the unicellular genera Chlamydomonas and Vitreochlamys. Although 18S rRNA gene sequences are preferred phylogenetic markers for many volvocalean species, phylogenetic relationships among the TGV-clade and its relatives have been examined mainly based on chloroplast genes and ITS2 sequences. To determine the candidate unicellular sister, 18S rRNA gene sequences of 41 species of the TGV-clade and its relatives were newly determined, and single and 6-gene phylogenetic analyses performed. No unicellular sister was determined by 18S rRNA gene analyses, but 6 unicellular clades and 11 ribospecies were recognized as candidates. Five of the candidate lineages and 27 taxa of the TGV-clade were examined by 6-gene phylogeny, revealing one clade including Chlamydomonas reinhardtii, Chlamydomonas debaryana, and Vitreochlamys ordinata to be more closely related than that containing Vitreochlamys aulata and Vitreochlamys pinguis. Key words: 18S rRNA, colonial, green algae, molecular phylogeny, unicellular, Volvocales. Tetrabaenaceae, Goniaceae, and cells) 8- to 50,000-celled genera (Pandorina, Volvocaceae constitute a colonial green Volvulina, Platydorina, Colemanosphaera, algal clade (TGV-clade) within Volvocales Yamagishiella, Eudorina, Pleodorina, and (Chlorophyceae), and include simple to Volvox). Only colonies of Volvocaceae have a complex colonial forms (e.g., Nozaki 2003a, shared colonial envelope. Nozaki et al. 2014, Nakada and Nozaki 2015). Within Volvocales, the TGV-clade belongs Tetrabaenaceae includes undifferentiated to the clade Reinhardtinia (Nakada et al. 2008, 4-celled genera (Tetrabaena, Basichlamys), 2010a). To understand the evolutionary origin Goniaceae undifferentiated 8- to 128-celled of coloniality of the TGV-clade, determination genera (Gonium, Astrephomene), and of its unicellular sister is first required. Previous Volvocaceae both undifferentiated and phylogenetic analyses showed that the TGV- differentiated (with somatic and reproductive clade is more closely related to some species —345— 346 The Journal of Japanese Botany Vol. 91 Centennial Memorial Issue of Chlamydomonas and Vitreochlamys To determine the candidate(s) unicellular (Vitreochlamys aulata (Pascher) Batko, sister of the TGV-clade, 18S rRNA gene Vitreochlamys pinguis Nakazawa, Vitreochlamys sequences of 36 strains of core-Reinhardtinia ordinata (Skuja) Nakazawa, and Vitreochlamys (15 unicellular and 21 colonial) and five species gloeocystiformis (O. Dill) Nakazawa) than to a closely related to Paulschulzia pseudovolvox clade consisting of Paulschulzia pseudovolvox were newly determined, and single gene 18S (P. Schulz) Skuja, Lobomonas rostrata Hazen, rRNA and 6-gene combined 18S rRNA-atpB- and two Vitreochlamys species (Vitreochlamys rbcL-psaA-psaB-psbC phylogenetic analyses fluviatilis (F. Stein) Batko and Vitreochlamys performed. nekrassovii (Korshikov) Nakazawa) (e.g., Nozaki et al. 1999, Nakazawa et al. 2001, Materials and Methods Pröschold et al. 2001, Nozaki et al. 2003, The methods of DNA extraction, PCR, Pröschold et al. 2005, Herron et al. 2009, Nakada and sequencing were as described previously et al. 2008, 2010a, 2010b; the most inclusive (Nakada et al. 2007, 2010c). The primers for clade containing Volvox carteri F. Stein, but not PCR and sequencing were 18S-FA, RB, FC, Paulschulzia pseudovolvox, is termed here as RD, FE, RF, FA2, and RB2 (Nakazawa and “core-Reinhardtinia”). However, phylogenetic Nozaki 2004, Nakada et al. 2007, 2010b). relationships among unicellular and colonial The 18S rRNA gene sequences obtained species/strains of core-Reinhardtinia have yet in this study (LC086332–LC086372) and to be resolved, partly because of inconsistencies several recently published sequences were in the phylogenetic marker genes used for unambiguously aligned with sequences of the unicellular and colonial species. clade Reinhardtinia (Nakada et al. 2008, 2010a, The phylogenetic relationships within the 2010b). For 18S rRNA single gene analyses, TGV-clade have been resolved mainly based the root of the clade Reinhardtinia was placed on chloroplast genes such as atpB, rbcL, psaA, on the branch leading to Heterochlamydomonas psaB, and psbC (e.g., Nozaki et al. 1995, 1997, according to Nakada et al. (2008). 1999, 2000, Nozaki 2003b, Nozaki et al. 2003, For 18S rRNA-atpB-rbcL-psaA-psaB-psbC 2014), while the phylogeny of Chlamydomonas 6-gene analyses, operational taxonomic units species tend to have been analyzed using 18S for which these five chloroplast gene sequences rRNA genes (e.g., Buchheim et al. 1990, 1996, were unavailable were excluded. The chloroplast 1997a, 1997b, Pröschold et al. 2001, Hoham 5-gene alignment was unambiguously et al. 2002, Nakada et al. 2008, Yumoto et al. constructed according to Nozaki et al. (2000) 2013). Additionally, Nakazawa et al. (2001) and combined with the 18S rRNA alignment analyzed phylogenetic relationships among (Table 1). For Bayesian phylogenetic analyses, Vitreochlamys species using rbcL genes, the alignment was divided into four partitions: showing the polyphyletic nature of the genus. 18S rRNA gene (18S), and first, second, and Pröschold et al. (2005) also showed the poorly third codon positions of the protein coding resolved ITS2 phylogeny of core-Reinhardtinia; chloroplast genes (cp1–cp3). however, only four colonial strains were The homogeneity of base frequencies was included in the analyses. Herron et al. (2009) tested for 18S rRNA and each codon position of provided the combined 6-gene phylogeny of the protein coding genes using the chi-squared core-Reinhardtinia using 18S rRNA and five test with PAUP* 4.0b10 (Swofford 2002). chloroplast genes, but 18S rRNA gene data Because homogeneity was rejected only for were missing or only partially included in the the cp3 partition (p < 0.05) when third codon analyses. positions of the atpB, psaA, or psaB genes December 2016 Nakada et al.: Unicellular relatives of colonial volvocaleans 347 Table 1. Species, genes and strains used in the 6-gene phylogenetic analyses. Sequences obtained in this study are shown in boldface Species Accession numberb (Strain designationa) 18S rRNA atpB rbcL psaA psaB psbC Core-Reinhardtinia: Unicellular Chlamydomonas debaryana AB542922 AB014034 D86838 AB044417–8 AB044469 AB044527 (SAG 15.72c = UTEX 1344d) Chlamydomonas reinhardtii M32703 M13704 J01399 AB044419 AB044470 AB044528 (UTEX 1061c, 137Cd) Vitreochlamys aulata LC086342 AB076122 AB050492 AB076144 AB076159 AB076180 (SAG 69.72c, d) Vitreochlamys ordinata LC086344 AB014036 AB014041 AB044420 AB044471 AB044529 (NIES-882c = Nozaki S-4d) Vitreochlamys pinguis LC086345 AB076120 AB050491 AB076142 AB076157 AB076174 (NIES-883c = Spha-12/1998-7-16d) Core-Reinhardtinia: Colonial Astrephomene gubernaculifera LC086347 AB014022–3 D63428 AB044234 AB044458 AB044513–4 (NIES-418c, d) Astrephomene perforata LC086348 AB014024 D63429 AB044238 AB044460 AB044518–9 (NIES-564c, d) Basichlamys sacculifera LC086349 AB014015 D63430 AB044416 AB044467–8 AB044526 (NIES-566c, d) Colemanosphaera charkoviensis LC086350 AB905589 AB905591 AB905593 AB905595 AB905597 (NIES-3388c, Isa 7-1d = NIES-3383) Eudorina elegans var. elegans LC086352 AB014009 D63432 AB044199 AB044435 AB044485 (NIES-456c, d) Eudorina elegans var. carteri LC086351 AB014012 D88806 AB044203 AB044438 AB044487–8 (NIES-721c = UTEX 1212d) Eudorina illinoisensis LC086353 AB014013 D63433 AB044198 AB044434 AB044484 (NIES-460c, d) Eudorina peripheralis LC086354 AB014007 D63434 AB044209 AB044440 AB044491–2 (NIES-725c = UTEX 1215d) Eudorina unicocca AB511841 AB014008 D86829 AB044206 AB044439 AB044489–90 (TKI-C-2c = NIES-1858, UTEX 737d) Gonium multicoccum LC086355 AB014020 D63435 AB044240 AB044461 AB044481 (NIES-737c = UTEX 2580d) Gonium pectorale LC066324 AB014016–7 D63437 AB044242 AB044463 AB044521 (NIES-569c, d) Gonium viridistellatum LC086356 AB014021 D86831 AB044244 AB044465 AB044524 (NIES-654c = UTEX 2519d) Pandorina morum LC066325 AB044179 AB044166 AB044230 AB044455 AB044509 (NIES-887c = UTEX 880d) Platydorina caudata LC086357 AB014032 D86828 AB044212 AB044442 AB044494 (NIES-728c = UTEX 1658d) Pleodorina californica LC086358 AB014004 D63439 AB044192 AB044430 AB044480 (NIES-735c = UTEX 809d) Pleodorina japonica AB688627 AB014005 D63440 AB044194 AB044431 AB044482 (NIES-577c = UTEX 2523d) aAbbreviations of the culture collections are as following: NIES. Microbial Culture Collection at the National Institute for Environmental Studies (http://mcc.nies.go.jp/top.jsp). SAG. Sammlung von Algenkulturen at the University of Göttingen (http://www.epsag.uni-goettingen.de/). UTEX. Culture Collection of Algae at the University of Texas at Austin (https:// utex.org). bAccession numbers of the genes from the International Nucleotide Sequence Database Collaboration (http://www.insdc. org).
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