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Proceedings of the Japan Academy. Series B, Physical and Biological Sciences logoLink to Proceedings of the Japan Academy. Series B, Physical and Biological Sciences
. 2024 Nov 10;100(8):465–475. doi: 10.2183/pjab.100.029

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

Hisayoshi NOZAKI *1,*2,*3,†, Kayoko YAMAMOTO *3, Kohei TAKAHASHI *1,*4
PMCID: PMC11535005  PMID: 39401900

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

1. Introduction

The genome of an organism provides the genetic information required for each individual to express all biological characteristics of that species. In the 20th century, the development whole-genome sequencing offered a valuable tool for investigating the molecular genetic bases of various biological traits; however, early studies were limited by the time and monetary costs associated with whole-genome sequencing of even a single eukaryotic species. Sanger sequencing was used to characterize the first complete whole genome of algae by using the unicellular red alga Cyanidioschyzon merolae.1),2) Later improvements in sequencing technologies, particularly next-generation sequencing (NGS), allowed researchers to sequence the whole genomes of other algal species. Eventually, the widespread use of NGS facilitated the construction of whole-genome data for non-model organisms, for which molecular genetic analyses had not previously been performed.3) Whole-genome analyses of non-model organisms have been conducted in various eukaryotic lineages, providing exciting insights that are anticipated be crucial for understanding biodiversity and evolution.4),5)

In this review, we describe recent developments in evolutionary studies of sex in the volvocine lineage of green algae, mainly on the basis of whole-genome data from both model and non-model species. Our recent studies to obtain complete genomes for non-model, but evolutionary important, volvocine species have provided critical details about sex-determining regions (SDRs) in sex chromosomes that have contributed to our understanding of the molecular genetic bases of evolution of anisogamy (sex with male and female gametes) and diversity and evolutionary transitions of mating systems.

2. Evolution of female and male sex from isogamy in the volvocine lineage

The volvocine lineage comprises green algae with a range of sexual reproduction characteristics, from the unicellular isogamous genus Chlamydomonas through genera with increasing degrees of sexual dimorphism, such as the multicellular, isogamous Gonium, the anisogamous genus Pleodorina, and the oogamous Volvox (Fig. 1).6),7) This lineage represents an ideal model for studying the evolution and diversity of sex.7),8) During the 20th century, extensive molecular genetic studies investigated the unicellular model species Chlamydomonas reinhardtii (e.g., Refs. 9 and 10) and resolved sex-specific genes and SDRs in its sex chromosomes (Fig. 2).

Fig. 1.

Fig. 1

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(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,35),36) but a recent phylotranscriptomic analysis of nuclear proteins suggested that Tetrabaena is separated from other volvocine algae shown here.32) Photographs from Yamashita et al.37) Permitted by the Creative Commons Attribution-NonCommercial 4.0 International License (CC BY-NC 4.0).

Fig. 2.

Fig. 2

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(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.,16) Ferris et al.,17) Bold and Wynne.25) (A) Asexual and sexual cycles. (B) Genomic features of sex chromosomes.

In haploid heterothallic species, the SDR is the segment of a sex chromosome where genes differ in arrangement and composition between male and female genotypes (or plus and minus mating types in isogamous species) (Fig. 2A). Thus, sex-specific or mating type-specific genes are localized in SDRs (Fig. 2B). Charlesworth11) made the theoretical prediction that SDR genes were involved in the evolution of anisogamy from isogamy. Although SDRs and mating type-specific genes were identified in C. reinhardtii during the 20th century,9),10) molecular genetic data for anisogamous/oogamous volvocine algae were not reported until 2006, when Nozaki et al.12) found a homolog of the minus dominance (MID) gene OTOKOGI13) in the anisogamous species Pleodorina starrii (Fig. 1). The MID gene determines the minus mating type in C. reinhardtii.10) Based on Sanger sequencing, the whole genomes of two model species in the volvocine lineage, C. reinhardtii14) and Volvox carteri,15) were sequenced by large numbers of researchers from 63 and 13 laboratories, respectively.16) The discovery of the OTOKOGI gene in the non-model species P. starrii12) and a genome project involving these two model species led to the determination of the SDR of V. carteri through international collaboration.17)

Before 2005, a project was initiated to sequence the whole genome of the oogamous V. carteri in the United States, using only a female strain (Eve = HK10 = UTEX 1885). At that time, it was thought to be technologically and financially impossible to determine new whole genomes of both female and male genotypes simultaneously to elucidate SDRs differing in sequence and gene composition between the male and female genomes. Therefore, the research strategy was based on searching the libraries of genome fragments linked to bacterial artificial chromosome vectors containing sex-specific genes such as OTOKOGI, which was thought to be located in the male SDR.

In 2005, Dr. Patrick Ferris relocated to Japan. He was a leading researcher on the molecular genetics of sex in Chlamydomonas species and had previously discovered MID10); at that time, he became involved in the V. carteri genome project, which required sequences from key genes such as OTOKOGI. Thus, a Japan–United States collaboration was initiated to identify the OTOKOGI sequence of V. carteri using a degenerate primer method developed in Japan.12) Based on the V. carteri OTOKOGI sequence and genomic analyses, an expanded SDR of approximately 1 Mbp was resolved in V. carteri.17) The SDR of the oogamous V. carteri was found to be 4–5-fold larger than that of the isogamous C. reinhardtii, and many novel female- and male-specific genes were identified (Fig. 3A). This study represented the first comparison of eukaryotic sex chromosomes between an isogamous organism and a closely related organism with male and female differentiation. The findings suggested that SDRs in which the genomes of both sexes are not recombined were important in the evolution from isogamous to anisogamous or oogamous sexual reproduction.

Fig. 3.

Fig. 3

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(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.17) (B) Whole genome analyses of two multicellular volvocine algae, isogamous Yamagishiella unicocca and anisogamous Eudorina sp. resolving their reduced SDR.18) For references of other SDRs, see De Hoff et al.,38) Hamaji et al.39) and Ferris et al.17) Modified based on the figure of Hamaji et al.18) Permitted by the Creative Commons Attribution 4.0 International License (CC BY 4.0).

The advent of NGS subsequently facilitated the construction of whole genomes for non-model multicellular volvocine algal species, including several that are evolutionarily important and have revealed whole SDRs in sex chromosomes. Next, four sets of de novo whole genomes for isogamous Yamagishiella (plus and minus mating types) and anisogamous Eudorina (male and female) species, which are evolutionarily intermediate between isogamous Chlamydomonas and oogamous Volvox, were constructed based on the combined assembly of PacBio long reads and Illumina short reads through NGS.18) Although SDRs were previously thought to have gradually expanded in size to include new genes during the evolution of anisogamy (Fig. 3A),19) these intermediate volvocine algae have reduced SDRs, measuring 7–268 kbp (Fig. 3B), and only one male-specific gene, OTOKOGI/MID, was conserved during their evolution of anisogamy from isogamy.18) These results suggested that SDR expansion might not have been related to the evolution of anisogamy and raised new questions about the molecular basis of this process in volvocine algae.

A transgenic study of the OTOKOGI/MID gene in V. carteri demonstrated that its presence determines the formation of sperm packets, i.e., bundles of male gametes, in reproductive cells,20) which suggested the functional evolution of this gene from determining the minus mating type to male gametogenesis, i.e., sperm packet formation. Thus, reduced SDRs appear to be sufficient to harbor OTOKOGI/MID, which may have been responsible for producing the first male gamete. However, two major problems remained. First, the origin and evolutionary history of the expanded SDR of V. carteri was unexplained. Despite the description of more than 20 phylogenetically diverse Volvox species,21) whole-genome and SDR information was available for only one species, V. carteri. The second problem was that algae in the volvocine lineages for which SDRs were identified were limited to heterothallic species with two sexes, designated either female and male or plus and minus mating types (Fig. 4). However, homothallic species that produce gametes of both sexes within the same genotype are widespread throughout the volvocine lineage.8)

Fig. 4.

Fig. 4

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(Color online) Two closely related species of Volvox with different mating systems, heterothallic V. reticuliferus and homothallic V. africanus, subjected to whole genome analyses.23) Based on Nozaki et al.21) and Yamamoto et al.24) (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).

3. Evolution of SDRs during the transition from heterothallism to homothallism in Volvox

The expansion of SDRs in V. carteri and their fate during the transition from heterothallism to homothallism were explored through comparative genome analyses of two closely related non-model Volvox species, Volvox reticuliferus and Volvox africanus, collected from Lake Biwa, Japan, and Kalasin Province, Thailand21),22) (Fig. 5). In 2021, whole genomes of three Volvox culture strains (specifically, female and male genotypes of heterothallic V. reticuliferus and a homothallic V. africanus strain from Lake Biwa) were constructed de novo through mixed assembly of long PacBio and short Illumina reads.23) The results showed an expanded SDR of approximately 1 Mbp in heterothallic V. reticuliferus, and a continuous SDR-like region (SDLR) of approximately 1 Mbp in homothallic V. africanus from Lake Biwa.23) Although the OTOKOGI/MID gene was detected in the male SDR of V. reticuliferus, as in heterothallic V. carteri,17) the homothallic strain of V. africanus had a cluster of five paralogs of OTOKOGI/MID within a short SDLR outside of the expanded SDLR. Furthermore, genes in the expanded SDLR of V. africanus were closely related to those in the SDR of female heterothallic V. reticuliferus, suggesting that the SDLR had directly originated from the female SDR of an ancestral heterothallic species. Therefore, the expanded 1-Mbp SDR may have been present in the common ancestor of V. reticuliferus and V. carteri ca. 75 million years ago, and the expanded female SDR of the ancestral heterothallic species may have been almost directly transmitted to the homothallic species V. africanus now found in Lake Biwa.23) A new whole-genome sequence was obtained in 2023 using a homothallic V. africanus strain from Thailand. Both the Lake Biwa and Thai strains are homothallic, but they differ from each other in the mode of sexual spheroid production. The Lake Biwa V. africanus strain produces both bisexual (monoicous) and male sexual spheroids, whereas the Thai strain produces separate male and female sexual spheroids in clonal cultures. Whole-genome analysis of the Thai strain demonstrated that it has a continuous, expanded SDLR of approximately 1 Mbp; however, its SDLR retains genes directly transmitted from the male SDR of the ancestral heterothallic species.24) Therefore, the expanded SDRs of females or males of the ancestral heterothallic species were inferred to have persisted during evolution to homothallic species, in which they became SDLRs (Fig. 5).

Fig. 5.

Fig. 5

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(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.23),24) and Nozaki et al.22)

4. Molecular genetic basis for the evolution of three sex phenotypes in a single haploid species, the multicellular volvocine Pleodorina starrii

In haploid organisms such as algae and fungi, only two basic mating systems were traditionally recognized: heterothallism and homothallism.25),26) However, a new mating system was recently discovered in the multicellular volvocine species P. starrii.27) Pleodorina starrii was originally described as a heterothallic species,28) and the male-specific gene OTOKOGI (PlestMID) was discovered in the male strain.12) However, two bisexual strains of a Pleodorina species were found to coexist with P. starrii in an aquatic system in Japan, and an intercrossing experiment between individuals of a bisexual Pleodorina species and a male or female P. starrii demonstrated no sexual isolation between these species,27) instead producing a haploid trioecious species that included three sex phenotypes (unisexual female, unisexual male, and bisexual) (Fig. 6A).

Fig. 6.

Fig. 6

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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.29) Permitted by the Creative Commons Attribution 4.0 International License (CC BY 4.0).

To resolve the molecular genetic basis for the evolution of a trioecious mating system in P. starrii, three sets of whole P. starrii genomes (unisexual female, unisexual male, and bisexual genotypes) were de novo generated.29) Comparative genome analyses of the three datasets resolved the SDRs of all three sex phenotypes in detail. As suggested by the ratios of the three phenotypes of progeny produced in the intercrossing experiment,27) male and bisexual phenotypes had the same male SDR type, whereas females had a female SDR type (Fig. 6B). Notably, the male SDR type harbored three paralogs of OTOKOGI/MID, two of which were pseudogenes. FUS1, which is not found in female or male SDRs of P. starrii, is a gamete recognition gene that is generally localized in the female or plus mating type SDR in volvocine lineage members.18) However, the genotypes of each sex phenotype contained FUS1 in the autosomal region. Thus, the unisexual male and bisexual phenotypes of P. starrii have both FUS1 and OTOKOGI/MID genes in a single haploid genotype. There is an inverse correlation between FUS1 and OTOKOGI/MID expression in P. starrii.29) Under sexual induction of P. starrii, FUS1 expression is upregulated in the unisexual female phenotype (lacking OTOKOGI/MID) whereas strong suppression of FUS1 is present in the unisexual male phenotype.29) It is therefore likely that FUS1 is regulated in female sex-specific gene expression, possibly in a manner analogous to the regulation of VcGSP1 by the RWP-RK family transcription factor VSR1 in the absence of OTOKOGI/MID expression in V. carteri.30) However, in the bisexual phenotype of P. starrii, FUS1 expression is upregulated even in the presence of OTOKOGI/MID expression in sexual induction, possibly due to an unknown autosomal bisexual factor.29) Therefore, the bisexual phenotype of P. starrii exhibits both female and male traits as a result of the presence of FUS1 and bisexual factor in autosomal regions and OTOKOGI/MID in the SDR (Fig. 6B). Phylogenetic analysis of FUS1 sequences demonstrated that FUS1 may have been transmitted from the female SDR to autosomal regions early in the evolution of P. starrii as a triecious species, through a drastic reorganization of SDRs (Fig. 6C). These genomic data suggest the existence of a species in which the three sexes coexist stably and are anticipated to have significant implications in the research of sex determination systems and the evolution of sexual diversity.

5. Conclusions

SDRs in sex chromosomes are generally thought to ensure genetic differences between males and females in heterothallic species. However, an expanded, continuous SDR of approximately 1 Mbp was retained in both males and females from ancestral heterothallic species, even following the transmission of the SDR to homothallic species (Fig. 5). Similar results were recently reported in liverwort, in which the male SDR of ancestral species was retained almost intact during evolution from heterothallism to homothallism.31)

In a Lake Biwa strain of V. africanus, the ancestral female SDR was transmitted to the homothallic genotype (Fig. 5), which also harbors male-specific genes such as OTOKOGI/MID, suggesting that both male and female genes of the ancestral heterothallic species are essential for establishing homothallism or bisexuality in a single haploid genotype of V. africanus. In the trioecious species P. starrii, a bisexual phenotype appears possible based on the coexistence of the male SDR and the female gene FUS1 (Fig. 6). By contrast, the Thai V. africanus strain has a male-derived SDLR but lacks female-derived genes. Thus, bisexuality could evolve in this species based on the gene compositions of the male genotypes alone. Male-specific genes such as OTOKOGI/MID are essential for sexual reproduction in Volvox. In addition, an expanded SDR (approximately 1 Mbp long) may have been conserved since the divergence of V. reticuliferus and V. carteri ca. 75 million years ago, and an expanded, continuous SDLR of approximately 1 Mbp has persisted, even after the evolution of homothallism (Fig. 5). The expanded SDR and SDLR may be important for sexual reproduction in both homothallic and heterothallic Volvox species; however, we can only speculate on their biological significance until future studies explore their evolution and functions in greater detail.

The present review focuses on the diversity and evolution of sex in the major volvocine lineage including Eudorina, Pleodorina, and Volvox excluding Volvox species with thick cytoplasmic bridges (Volvox sect. Volvox) (Figs. 1, 3B). Thus, only a single evolutionary transition of anisogamy from isogamy was discussed in the present review based on the sex-specific genes and SDRs. However, at least two additional, independent evolutionary transitions of anisogamy/oogamy with sperm packets likely occurred, in Platydorina-Colemanosphaera and Volvox sect. Volvox.32) Only OTOKOGI/MID genes were examined in Volvox sect. Volvox,33),34) and SDR-related genes have not been studied in Platydorina-Colemanosphaera. Thus, further genomic studies of these anisogamous/oogamous volvocine species will clarify the genetic basis for parallel evolution of male and female in volvocine algae.

Acknowledgments

This work was partially supported by Grants-in-Aid for the Japan Society for the Promotion of Science for Scientific Research (B) (Grant No. JP20H03299 to HN) and Scientific Research (C) (Grant No. JP24K08946) from the Ministry of Education, Culture, Sports, Science and Technology (MEXT)/JSPS KAKENHI (https://www.jsps.go.jp/english/e-grants).

Non-standard abbreviation list

MID

minus dominance gene

NGS

next-generation sequencing

SDLR

SDR-like region

SDR

sex-determining region

Profile

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Hisayoshi Nozaki graduated from Tokyo Metropolitan University in 1978. He then became a high school teacher at Keio Gijuku until 1992, serving as a teacher of biology and boxing. He received the Keio Gijuku Athletic Association Distinguished Service Award in 1992. From April 1992 to March 1995, he served as a senior researcher at the National Institute for Environmental Studies, Tsukuba, and established the diversity conservation biology of charalean algae. In April 1995, he became an Associate Professor in the Department of Biological Science, Graduate School of Science, the University of Tokyo (UTokyo). During his tenure at UTokyo, he was responsible for both teaching and research. His teaching responsibilities included giving lectures in undergraduate and graduate programs on topics such as evolutionary biology and taxonomy, especially on volvocine green algae originally established from field collection samples. In addition to publishing over 200 scientific papers, he has supervised 18 MSc and 12 PhD students in biological sciences. After retiring from UTokyo in March 2021, he started research on the cryopreservation of volvocine green algae and established more than 100 cryopreserved culture strains with the help of the staff from the Microbial Culture Collection at the National Institute for Environmental Studies.

graphic file with name pjab-100-465-g008.gif

Kohei Takahashi graduated from Tokyo University of Science in 2016. He received his master's degree in 2019 and PhD degree in 2023 from the University of Tokyo. After one year as a postdoctoral fellow at the University of Tokyo, he is working in the Max Planck Institute for Biology Tübingen in Germany as a JSPS Overseas Research Fellow from 2024. His research interest is the genetic mechanisms of haploid sex-determination systems in eukaryotes. To reveal this question, he uses Pleodorina starrii, a colonial volvocine green alga with three sex phenotypes in one biological species.

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