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DATE2023.06.09 #Press Releases

Sex chromosomes reveal how three sexes can co-exist in these algae

 

Based on genome data of sex-determining regions, researchers provide the first-ever explanation for the co-existence of three sexes in species.

 

June 09, 2023

 

Overview

Whole genome sequences of three sexes--female, male, and ‘bisexual’ which can mate with both unisex males and females--of the green algae Pleodorina starrii reveal the evolution in sex chromosome genes that explain their co-existence.

Though male and bisexual algae have identical male sex-determining regions in sex chromosomes, their expression differs during sexual reproduction.

The coexistence of the three sexes is not an evolutionary intermediate but a stable mating system.

The findings help us understand how sexes evolve and impact the study of sexual diversity in animals and plants.

 

A podcast explaining the paper in 2 minutes: https://podcasters.spotify.com/pod/show/rigakuru-utokyo-science/episodes/12--Sexual-diversity-explained-at-the-level-of-genes-e25o9re

 

Video: The algae swimming in water. Credit: Kohei Takahashi

Pleodorina starrii is a Japanese freshwater green alga living in colonies that look like soft spheres with green jellybean-like cells inside. The colonies can have either male or female sex cells. Male sex cells are small and mobile, while female sex cells are large and immobile.

Unlike human somatic cells, which are diploid with two sets of chromosomes, these algae are haploid with a single set of chromosomes. And that makes their mating system unique compared to ours. In 2021, Hisayoshi Nozaki, an Associate Professor at the University of Tokyo, and his team published a study showing that a freshwater alga evolved three different sexes that can breed with each other: males, females, and bisexuals.

Under nutrient-sufficient conditions, the colonies reproduce asexually and make clones. If they are starved of nitrogen, they reproduce sexually. During sexual reproduction, male colonies release clear sperm packets (the bundles of male gametes or sex cells) into the water that swim until they impregnate the female colonies. The female sex cells within the female colonies fuse with the male sex cells, undergo meiosis (cell division), and produce new haploid individuals of one of the three sexes. The third sex, which the researchers call bisexual, can produce both male and female. In other words, the bisexual strain can form a bisexual female colony or a bisexual male colony that can mate with unisex or bisexual strains of the opposite sex. 

Video: A sperm trying to enter a female colony with female sex cells. Credit: Kohei Takahashi

If two sexes were enough to reproduce, why did the species evolve a third sex? How the bisexual colonies evolved has been an evolutionary puzzle that challenged the research team because the co-existence of males, females, and bisexuals is often considered an unstable intermediate stage in evolution. To find clues to address the puzzle, they set to investigate the changes in the sex chromosomes of their evolutionary ancestors over time.

The team decoded the entire genome of Pleodorina starrii and learned that sex-determining regions in the ancestor algae reorganized over time. And that led to three sexes in this species. Males and bisexuals have the same genes in the sex-determining regions. But they differ in gene expression during sexual reproduction. So, the researchers predict that different gene regulation mechanisms might have evolved in males and bisexuals, thus allowing them to be evolutionarily viable sexes while having similar sex-determining genes.

 

Figure: A schematic of the "sex chromosome revolution" that occurred in P. starrii, as revealed in this study. The image on the left shows Pleodorina starrii which are algal cells that live as a colony within a transparent gelatinous membrane. Three sexes co-exist in P. starrii due to the re-organization of genes in their sex-determining region. “OTOKOGI” is a male-specific gene and FUS1 is a female-specific gene normally present in the female sex-determining region. Over time, all three sexes retained FUS1 in their autosomal chromosomes while males and bisexuals have OTOKOGI in their sex chromosomes. The coexistence of these genes plays crucial roles in the formation and function of male or female gametes. And the transcriptional regulation of these genes allows the coexistence of the three sexes.

 

Publication details


Journal Communications Biology
Title Reorganization of the ancestral sex-determining regions during the evolution of trioecy in Pleodorina starrii  
Authors
Kohei Takahashi, Shigekatsu Suzuki, Hiroko Kawai-Toyooka, Kayoko Yamamoto, Takashi Hamaji, Ryo Ootsuki, Haruyo Yamaguchi, Masanobu Kawachi, Tetsuya Higashiyama, and Hisayoshi Nozaki
DOI