Whole-genome sequencing analysis of volvocine green algae reveals the molecular genetic basis for the diversity and evolution of sex

Abstract

This review describes the development of evolutionary studies of sex based on the volvocine lineage of green algae, which was facilitated by whole-genome analyses of both model and non-model species. Volvocine algae, which include Chlamydomonas and Volvox species, have long been considered a model group for experimental studies investigating the evolution of sex. Thus, whole-genomic information on the sex-determining regions of volvocine algal sex chromosomes has been sought to elucidate the molecular genetic basis of sex evolution. By 2010, whole genomes were published for two model species in this group, Chlamydomonas reinhardtii and Volvox carteri. Recent improvements in sequencing technology, particularly next-generation sequencing, allowed our studies to obtain complete genomes for non-model, but evolutionary important, volvocine algal species. These genomes have provided critical details about sex-determining regions that will contribute to our understanding of the diversity and evolution of sex.

Keywords: evolution of sex; non-model organism; sex-determining region; sex-specific gene; volvocine green algae; whole genome sequence.

Fig. 1

(Color online) Schematic representation of the morphology, sexual reproduction, and phylogeny of a major group of the volvocine green algae. Phylogeny is based on chloroplast multigene phylogeny,^, but a recent phylotranscriptomic analysis of nuclear proteins suggested that Tetrabaena is separated from other volvocine algae shown here. Photographs from Yamashita et al. Permitted by the Creative Commons Attribution-NonCommercial 4.0 International License (CC BY-NC 4.0).

Fig. 2

(Color online) Diagrams of heterothallic life cycle, mating types, and chromosomes in a model species of the volvocine lineage, Chlamydomonas reinhardtii. Based on Craig et al., Ferris et al., Bold and Wynne. (A) Asexual and sexual cycles. (B) Genomic features of sex chromosomes.

Fig. 3

(Color online) Diagrammatic representation of sex-determining regions (SDRs) in sex chromosomes of the volvocine algae. (A) Comparison of SDRs between two model species of the volvocine green lineage. Based on Ferris et al. (B) Whole genome analyses of two multicellular volvocine algae, isogamous Yamagishiella unicocca and anisogamous Eudorina sp. resolving their reduced SDR. For references of other SDRs, see De Hoff et al., Hamaji et al. and Ferris et al. Modified based on the figure of Hamaji et al. Permitted by the Creative Commons Attribution 4.0 International License (CC BY 4.0).

Fig. 4

(Color online) Two closely related species of Volvox with different mating systems, heterothallic V. reticuliferus and homothallic V. africanus, subjected to whole genome analyses. Based on Nozaki et al. and Yamamoto et al. (A–C) Heterothallic V. reticuliferus from Lake Biwa. (A) Asexual spheroid producing two daughter spheroids with gonidia (g) (reproductive cells). (B) Male spheroid with sperm packets (sp) (bundles of male gametes). (C) Female spheroid with eggs (e). (D–G) Homothallic V. africanus from Lake Biwa. This alga produces both sexual male and monoicous (bisexual) spheroids in a single clonal culture. (D) Asexual spheroid showing two daughter spheroids with gonidia (g). (E) A parental spheroid with both male and monoicous spheroids. (F) Male spheroid with sperm packets (sp). (G) Monoicous spheroid with both eggs (e) and sperm packets (sp).

Fig. 5

(Color online) Schematic representation of the phylogeny and evolution of sex-related, morphological and genomic characteristics of three species of Volvox. Based on Yamamoto et al.^, and Nozaki et al.

Fig. 6

The trioecious volvocine species Pleodorina starrii with three sex phenotypes. (A) Diagrammatic representation of three sex phenotypes. sp: sperm packet (bundle of male gametes), mg: male gamete, fg: female gamete. All scale bars ＝ 50 μm. (B) Comparison of sex-determining region (SDR) in sex chromosomes and FUS1 gene in autosome between three sex phenotypes. Light blue and orange regions represent male and female SDRs, respectively. Genes with dark blue and red backgrounds represent male- and female-specific genes, respectively. Yellow regions represent pseudo-autosomal regions. Gray shading indicates a syntenic bloc. Note that autosomal regions harbor FUS1 homologs of three sex phenotypes. (C) Diagrams of an evolutionary hypothesis of three sex phenotypes in the trioecious volvocine species Pleodorina starrii. Based on Takahashi et al. Permitted by the Creative Commons Attribution 4.0 International License (CC BY 4.0).