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Three Genomes in the Algal Genus Volvox Reveal the Fate of a Haploid Sex-Determining Region After a Transition to Homothallism

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Three Genomes in the Algal Genus Volvox Reveal the Fate of a Haploid Sex-Determining Region After a Transition to Homothallism Three genomes in the algal genus Volvox reveal the fate of a haploid sex-determining region after a transition to homothallism Kayoko Yamamotoa, Takashi Hamaji (浜地貴志)b,1, Hiroko Kawai-Toyookaa,2, Ryo Matsuzakic,d, Fumio Takahashie, Yoshiki Nishimurab, Masanobu Kawachic, Hideki Noguchif, Yohei Minakuchig, James G. Umenh, Atsushi Toyodag, and Hisayoshi Nozakia,3 aDepartment of Biological Sciences, Graduate School of Science, The University of Tokyo, Tokyo 113-0033, Japan; bDepartment of Biological Sciences, Graduate School of Science, Kyoto University, Kyoto 606-8502, Japan; cCenter for Environmental Biology and Ecosystem Studies, National Institute for Environmental Studies, Tsukuba 305-8506, Japan; dFaculty of Life and Environmental Sciences, University of Tsukuba, Tsukuba 305-8572, Japan; eCollege of Life Sciences, Ritsumeikan University, Shiga 525-8577, Japan; fResearch Organization of Information and Systems, Mishima 411-8540, Japan; gCenter for Information Biology, National Institute of Genetics, Mishima 411-8540, Japan; and hDonald Danforth Plant Science Center, St. Louis, MO 63132 Edited by Brian Charlesworth, University of Edinburgh, Edinburgh, United Kingdom, and approved April 15, 2021 (received for review January 18, 2021) Transitions between separate sexes (dioecy) and other mating functions of both sexes and mating-types in the homothallic spe- systems are common across eukaryotes. Here, we study a change cies is poorly understood outside of fungi (8). in a haploid dioecious green algal species with male- and female- Organisms with a heterothallic haploid generation such as algae determining chromosomes (U and V). The genus Volvox is an oogamous and early diverging land plants like mosses and liverworts have (with large, immotile female gametes and small, motile male gametes) sex-determining regions (SDRs) that are differentiated between and includes both heterothallic species (with distinct male and female the two sexes and located on male and female determining (U and V) genotypes, associated with a mating-type system that prevents chromosomes (9). SDRs exhibit suppressed recombination and fusion of gametes of the same sex) and homothallic species (bisexual, harbor fully sex-linked genes including sex-specific genes (found in with the ability to self-fertilize). We date the origin of an expanded sex-determining region (SDR) in Volvox to at least 75 Mya, suggest- only one of the two sexes) and gametologs (genes with alleles in ing that homothallism represents a breakdown of dioecy (hetero- both haplotypes of the SDR) (9). A recent study has characterized EVOLUTION thallism). We investigated the involvement of the SDR of the U and genes involved in a change from sexual reproduction to parthe- V chromosomes in this transition. Using de novo whole-genome nogenesis in a heterothallic brown alga with UV chromosome sequences, we identified a heteromorphic SDR of ca 1 Mbp in male (16). However, genomics of transitions between heterothallism and female genotypes of the heterothallic species Volvox reticulife- and homothallism have not been previously studied in the context rus and a homologous region (SDLR) in the closely related homo- of haploid SDRs, and the fates of sex-determining and sex-related thallic species Volvox africanus, which retained several different V. africanus hallmark features of an SDR. The SDLR includes a large Significance region resembling the female SDR of the presumptive heterothallic ancestor, whereas most genes from the male SDR are absent. How- Evolutionary transitions between species with separate sexes ever, we found a multicopy array of the male-determining gene, and species in which individuals have both sex functions have MID, in a different genomic location from the SDLR. Thus, in V. wide-ranging biological implications. It is largely unknown how africanus, an ancestrally female genotype may have acquired MID such transitions occur in systems with haploid male- and female- and thereby gained male traits. determining chromosomes in algae and bryophytes. We inves- tigated such a transition in the algal genus Volvox by making evolution | sex | Volvox | heterothallism | homothallism whole-genome sequences of two closely related species, one of which is heterothallic (with distinct males and females) and the s first noted by Darwin when studying plant sexuality, self- other homothallic (with only bisexual, self-compatible individ- Afertilization can lead to inbreeding depression, though this uals). The heterothallic species harbors a sex-determining region potential disadvantage relative to outcrossing can be offset by (SDR), while the homothallic species retains a nearly intact higher probability of fertilization success (1, 2). Thus, transitions female-derived SDR-like region and separate regions containing between inbreeding and outbreeding mating systems attract the key male genes. Thus, an ancestral female has probably become attention of evolutionary biologists and have been documented homothallic by acquiring genes that confer male functions. in sexual systems across a broad range of taxa including animals, land plants, algae (Fig. 1), protists, and fungi (3–9). Hermaphroditic Author contributions: K.Y., T.H., and H. Nozaki designed research; K.Y., T.H., H.K.-T., R.M., mating systems in diploid animals and plants are fairly com- F.T., Y.N., M.K., H. Noguchi, Y.M., J.G.U., A.T., and H. Nozaki performed research; K.Y., mon, and the evolution of hermaphroditism in animals has been T.H., H.K.-T., R.M., F.T., Y.N., M.K., H. Noguchi, Y.M., A.T., and H. Nozaki analyzed data; – and K.Y., J.G.U., A.T., and H. Nozaki wrote the paper. extensively studied (10 12). The molecular genetic bases of her- The authors declare no competing interest. maphroditism have also been recently studied in several flowering This article is a PNAS Direct Submission. plants (13–15). This open access article is distributed under Creative Commons Attribution-NonCommercial- In haploid organisms, two basic types of mating systems are NoDerivatives License 4.0 (CC BY-NC-ND). recognized: heterothallic (with two or more self-incompatible 1Present address: Research and Development Initiative, Chuo University, Tokyo 112-8551, mating types in isogamous species or with males and females in Japan. anisogamous/oogamous species) and homothallic (self-compatible 2Present address: Department of Frontier Bioscience, Hosei University, Tokyo 184-8584, with isogamy or bisexual with anisogamy/oogamy) (SI Appendix, Japan. Table S1). In heterothallic species, gamete compatibility in isogamy 3To whom correspondence may be addressed. Email: [email protected]. or maleness versus femaleness is usually determined by a single This article contains supporting information online at https://www.pnas.org/lookup/suppl/ complex locus on a chromosome (9). The process by which this doi:10.1073/pnas.2100712118/-/DCSupplemental. genetic system breaks down to allow a single genotype to acquire Published May 19, 2021. PNAS 2021 Vol. 118 No. 21 e2100712118 https://doi.org/10.1073/pnas.2100712118 | 1of8 Downloaded by guest on October 1, 2021 A B C D G F E H Fig. 1. Schematic representation of life cycles of two closely related species of Volvox sect. Merrillosphaera (SI Appendix, Fig. S1) showing different sexual systems (heterothallism and homothallism), based on Nozaki et al. (29). Note gonidia (g) in asexual spheroids and sperm packets (sp) and eggs (e) in sexual spheroids. (A) NIES-3781. (B) NIES-3783. (C and D) NIES-3782. (E and H) NIES-3784. (F and G) NIES-3780. For materials and methods of light micrographs, refer to Nozaki et al. (29). All photographs are original. genes present on ancestral SDRs in UV chromosomes after to have occurred after the transition from isogamy to anisogamy/ transitions to homothallism are unknown. oogamy (21). However, the timing of the SDR expansion in the The volvocine green algal lineage is an especially well-studied genus Volvox and its significance with respect to the evolution of evolutionary model for investigating the origins of sexes and sexual dimorphism remain unknown. transitions in sexuality, because it includes extant organisms with To date, genomic studies of volvocine green algae have fo- a graded range of sexual or mating phenotypes from unicellular cused on heterothallic species (Fig. 2), but most genera within isogamous Chlamydomonas through genera with increasing degrees this lineage have members that also underwent transitions from of sexual dimorphism, such as multicellular, isogamous Gonium, heterothallism to homothallism (7). These algae are found in and oogamous Volvox (Fig. 2) (17–22). In heterothallic species of freshwater habitats and form a dormant diploid zygote with a the isogamous volvocine genera such as Chlamydomonas,there resistant wall that allows it to survive under unfavorable condi- are two mating-types, plus and minus, both of which are needed tions; diploidy in the zygote could be of selective value for survival for sexual reproduction (9). Ferris and Goodenough (23) char- when chromosomal damage and mutation may be occurring at acterized the first mating-type locus (MT)inChlamydomonas increased frequencies (26). Thus, transitions from heterothallism reinhardtii, which was discovered to have features similar to those to homothallism in the volvocine algae may be favored for pro- of a typical SDR, including large size and suppressed recombi- duction of the resistant diploid cells (zygotes) by self-fertilization. nation. Subsequent studies of heterothallic species of multicellular
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