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Genome biology and evolution
09 01, 2018;10 (9): 2248-2254.

Exploring the Limits and Causes of Plastid Genome Expansion in Volvocine Green Algae.

Hager Gaouda, Takashi Hamaji, Kayoko Yamamoto, Hiroko Kawai-Toyooka, Masahiro Suzuki, Hideki Noguchi, Yohei Minakuchi, Atsushi Toyoda, Asao Fujiyama, Hisayoshi Nozaki, David Roy Smith
Author Information
  1. Hager Gaouda: Department of Biology, University of Western Ontario, London, Ontario, Canada.
  2. Takashi Hamaji: Department of Biological Sciences, Graduate School of Science, University of Tokyo, Japan.
  3. Kayoko Yamamoto: Department of Biological Sciences, Graduate School of Science, University of Tokyo, Japan.
  4. Hiroko Kawai-Toyooka: Department of Biological Sciences, Graduate School of Science, University of Tokyo, Japan.
  5. Masahiro Suzuki: Kobe University Research Center for Inland Seas, Awaji, Hyogo, Japan.
  6. Hideki Noguchi: Center for Genome Informatics, Joint Support-Center for Data Science Research, Research Organization of Information and Systems, Mishima, Shizuoka, Japan.
  7. Yohei Minakuchi: Center for Information Biology, National Institute of Genetics, Mishima, Shizuoka, Japan.
  8. Atsushi Toyoda: Advanced Genomics Center, National Institute of Genetics, Mishima, Shizuoka, Japan.
  9. Asao Fujiyama: Advanced Genomics Center, National Institute of Genetics, Mishima, Shizuoka, Japan.
  10. Hisayoshi Nozaki: Department of Biological Sciences, Graduate School of Science, University of Tokyo, Japan.
  11. David Roy Smith: Department of Biology, University of Western Ontario, London, Ontario, Canada.
PMID: 30102347 DOI: 10.1093/gbe/evy175

Abstract

Plastid genomes are not normally celebrated for being large. But researchers are steadily uncovering algal lineages with big and, in rare cases, enormous plastid DNAs (ptDNAs), such as volvocine green algae. Plastome sequencing of five different volvocine species has revealed some of the largest, most repeat-dense plastomes on record, including that of Volvox carteri (∼525 kb). Volvocine algae have also been used as models for testing leading hypotheses on organelle genome evolution (e.g., the mutational hazard hypothesis), and it has been suggested that ptDNA inflation within this group might be a consequence of low mutation rates and/or the transition from a unicellular to multicellular existence. Here, we further our understanding of plastome size variation in the volvocine line by examining the ptDNA sequences of the colonial species Yamagishiella unicocca and Eudorina sp. NIES-3984 and the multicellular Volvox africanus, which are phylogenetically situated between species with known ptDNA sizes. Although V. africanus is closely related and similar in multicellular organization to V. carteri, its ptDNA was much less inflated than that of V. carteri. Synonymous- and noncoding-site nucleotide substitution rate analyses of these two Volvox ptDNAs suggest that there are drastically different plastid mutation rates operating in the coding versus intergenic regions, supporting the idea that error-prone DNA repair in repeat-rich intergenic spacers is contributing to genome expansion. Our results reinforce the idea that the volvocine line harbors extremes in plastome size but ultimately shed doubt on some of the previously proposed hypotheses for ptDNA inflation within the lineage.

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MeSH Term

Chlorophyta
DNA, Algal
Evolution, Molecular
Genome, Plastid
Plastids
Sequence Analysis, DNA
Volvox

Chemicals

DNA, Algal
Journal Article Research Support, Non-U.S. Gov't

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