Three genomes in the algal genus Volvox reveal the fate of a haploid sex-determining region after a transition to homothallism

Kayoko Yamamoto, Takashi Hamaji, Hiroko Kawai-Toyooka, Ryo Matsuzaki, Fumio Takahashi, Yoshiki Nishimura, Masanobu Kawachi, Hideki Noguchi, Yohei Minakuchi, James G. Umen, Atsushi Toyoda, Hisayoshi Nozaki

Research output: Contribution to journalArticlepeer-review

21 Scopus citations

Abstract

Transitions between separate sexes (dioecy) and other mating systems are common across eukaryotes. Here, we study a change in a haploid dioecious green algal species with male- and female-determining chromosomes (U and V). The genus Volvox is an oogamous (with large, immotile female gametes and small, motile male gametes) and includes both heterothallic species (with distinct male and female genotypes, associated with a mating-type system that prevents fusion of gametes of the same sex) and homothallic species (bisexual, with the ability to self-fertilize). We date the origin of an expanded sex-determining region (SDR) in Volvox to at least 75 Mya, suggesting that homothallism represents a breakdown of dioecy (heterothallism). We investigated the involvement of the SDR of the U and V chromosomes in this transition. Using de novo whole-genome sequences, we identified a heteromorphic SDR of ca 1 Mbp in male and female genotypes of the heterothallic species Volvox reticuliferus and a homologous region (SDLR) in the closely related homothallic species Volvox africanus, which retained several different hallmark features of an SDR. The V. africanus SDLR includes a large region resembling the female SDR of the presumptive heterothallic ancestor, whereas most genes from the male SDR are absent. However, we found a multicopy array of the male-determining gene, MID, in a different genomic location from the SDLR. Thus, in V. africanus, an ancestrally female genotype may have acquired MID and thereby gained male traits.

Original languageEnglish
Article numbere2100712118
JournalProceedings of the National Academy of Sciences of the United States of America
Volume118
Issue number21
DOIs
StatePublished - May 25 2021

Keywords

  • Evolution
  • Volvox
  • heterothallism
  • homothallism
  • sex

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