Research Article: Molecular evolutionary analysis of a gender-limited MID ortholog from the homothallic species Volvox africanus with male and monoecious spheroids

Date Published: June 30, 2017

Publisher: Public Library of Science

Author(s): Kayoko Yamamoto, Hiroko Kawai-Toyooka, Takashi Hamaji, Yuki Tsuchikane, Toshiyuki Mori, Fumio Takahashi, Hiroyuki Sekimoto, Patrick J. Ferris, Hisayoshi Nozaki, James G. Umen.


Volvox is a very interesting oogamous organism that exhibits various types of sexuality and/or sexual spheroids depending upon species or strains. However, molecular bases of such sexual reproduction characteristics have not been studied in this genus. In the model species V. carteri, an ortholog of the minus mating type-determining or minus dominance gene (MID) of isogamous Chlamydomonas reinhardtii is male-specific and determines the sperm formation. Male and female genders are genetically determined (heterothallism) in V. carteri, whereas in several other species of Volvox both male and female gametes (sperm and eggs) are formed within the same clonal culture (homothallism). To resolve the molecular basis of the evolution of Volvox species with monoecious spheroids, we here describe a MID ortholog in the homothallic species V. africanus that produces both monoecious and male spheroids within a single clonal culture. Comparison of synonymous and nonsynonymous nucleotide substitutions in MID genes between V. africanus and heterothallic volvocacean species suggests that the MID gene of V. africanus evolved under the same degree of functional constraint as those of the heterothallic species. Based on semi quantitative reverse transcription polymerase chain reaction analyses using the asexual, male and monoecious spheroids isolated from a sexually induced V. africanus culture, the MID mRNA level was significantly upregulated in the male spheroids, but suppressed in the monoecious spheroids. These results suggest that the monoecious spheroid-specific down regulation of gene expression of the MID homolog correlates with the formation of both eggs and sperm in the same spheroid in V. africanus.

Partial Text

Volvox is a genus of spheroidal, multicellular green algae with a surface layer of hundreds to thousands of biflagellated somatic cells, and a much smaller number of non-flagellated germ cells (gonidia) that develop into asexual progeny. Life cycles of all Volvox species are facultatively sexual with haploid asexual phase; typically many rounds of asexual reproduction occur between rounds of sexual reproduction in which thick-walled diploid zygotes are formed and meiosis occurs during zygote germination to produce haploid progeny (Fig 1). During sexual reproduction, spheroids that contain eggs or sperm packets (bundles of male gametes or sperm) or both are produced. This genus exhibits various types of sexuality and/or sexual spheroids that have been used to define separate taxa within Volvox [1–3]. For example, whether the sexual spheroids are dioecious or monoecious is an important criterion for distinguishing species of Volvox; several monoecious species are recognized in Volvox [1–3].

Sexual differentiation in heterothallic species of the unicellular and colonial/multicellular volvocine algae is controlled by a sex-determining or mating type locus (MT) containing MID in the minus or male strain [8, 28, 29]. Comparative analyses of MT loci in volvocine algae are important to elucidate the molecular and genomic basis of evolution of sexual differentiation [8, 29]. However, there is, as yet, no genome information from homothallic species in the chromosomal region homologous to the MT locus of their heterothallic relatives, except for the MID genes that we described here in two homothallic species, V. africanus and V. ferrisii.




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