Distribution of the Sex-Determining Gene MID and Molecular Correspondence of Mating Types within the Isogamous Genus Gonium (Volvocales, Chlorophyta)

Takashi Hamaji,Yoshiki Nishimura,Hisayoshi Nozaki,Ichiro Nishii,Patrick J Ferris,Senjie Lin

doi:10.1371/journal.pone.0064385

Abstract

BackgroundIsogamous organisms lack obvious cytological differences in the gametes of the two complementary mating types. Consequently, it is difficult to ascertain which of the two mating types are homologous when comparing related but sexual isolated strains or species. The colonial volvocalean algal genus Gonium consists of such isogamous organisms with heterothallic mating types designated arbitrarily as plus or minus in addition to homothallic strains. Homologous molecular markers among lineages may provide an “objective” framework to assign heterothallic mating types.Methodology/Principal FindingsUsing degenerate primers designed based on previously reported MID orthologs, the “master regulator” of mating types/sexes in the colonial Volvocales, MID homologs were identified and their presence/absence was examined in nine strains of four species of Gonium. Only one of the two complementary mating types in each of the four heterothallic species has a MID homolog. In addition to heterothallic strains, a homothallic strain of G. multicoccum has MID. Molecular evolutionary analysis suggests that MID of this homothallic strain retains functional constraint comparable to that of the heterothallic strains.Conclusion/SignificanceWe coordinated mating genotypes based on presence or absence of a MID homolog, respectively, in heterothallic species. This scheme should be applicable to heterothallic species of other isogamous colonial Volvocales including Pandorina and Yamagishiella. Homothallism emerged polyphyletically in the colonial Volvocales, although its mechanism remains unknown. Our identification of a MID homolog for a homothallic strain of G. multicoccum suggests a MID-dependent mechanism is involved in the sexual developmental program of this homothallic species.

Highlights

Isogamy is a mode of sexual reproduction involving the agglutination and fusion of two gametes that are essentially identical in size and shape
The C. reinhardtii mating type determining protein, minus dominance (MID), dominantly determines mating type minus as a transcription factor with a conserved putative DNA-binding RWP-RK domain [12,13,14], which served as a candidate sequence for designing degenerate primers for identification of homologs in colonial volvocalean algae, including two Gonium species [15,16,17,18]
The other alignment is composed of amino acid sequences (47 aa, Fig. S2) of RWP-RK domains

Summary

Introduction

Isogamy is a mode of sexual reproduction involving the agglutination and fusion of two gametes that are essentially identical in size and shape. Chlamydomonas reinhardtii, an isogamous single-celled green alga, has two genetically determined, heterothallic mating types: plus and minus [4]. In the colonial Volvocales, more than one sexually isolated group or syngen is recognized in various morphological or taxonomic species (e.g. Pandorina morum [10]; Gonium viridistellatum [11]); correspondence based on crossing experiment is not definable even within a single species with bilateral mating papillae.

Results

Conclusion