Identification of the sex-determining factor in the liverwort Marchantia polymorpha reveals unique evolution of sex chromosomes in a haploid system

• Published in: Current biology Vol. 31; no. 24; pp. 5522 - 5532.e7
• Main Authors: Iwasaki, Miyuki, Kajiwara, Tomoaki, Yasui, Yukiko, Yoshitake, Yoshihiro, Miyazaki, Motoki, Kawamura, Shogo, Suetsugu, Noriyuki, Nishihama, Ryuichi, Yamaoka, Shohei, Wanke, Dierk, Hashimoto, Kenji, Kuchitsu, Kazuyuki, Montgomery, Sean A., Singh, Shilpi, Tanizawa, Yasuhiro, Yagura, Masaru, Mochizuki, Takako, Sakamoto, Mika, Nakamura, Yasukazu, Liu, Chang, Berger, Frédéric, Yamato, Katsuyuki T., Bowman, John L., Kohchi, Takayuki
• Format: Journal Article
• Language: English
• Published: England Elsevier Inc 20.12.2021; Cell Press
• Subjects: Evolution, Molecular; feminizer; gametolog; haploid; Haploidy; Marchantia - genetics; Marchantia polymorpha; Phylogeny; reproduction; sex chromosome; sex chromosome evolution; Sex Chromosomes - genetics; sex differentiation; sex-determining gene; sex differentiation; sex-determining gene; gametolog; sex chromosome evolution; Marchantia polymorpha; sex chromosome; haploid; feminizer; reproduction
• ISSN: 0960-9822; 1879-0445; 1879-0445
• DOI: 10.1016/j.cub.2021.10.023

Sex determination is a central process for sexual reproduction and is often regulated by a sex determinant encoded on a sex chromosome. Rules that govern the evolution of sex chromosomes via specialization and degeneration following the evolution of a sex determinant have been well studied in diploid organisms. However, distinct predictions apply to sex chromosomes in organisms where sex is determined in the haploid phase of the life cycle: both sex chromosomes, female U and male V, are expected to maintain their gene functions, even though both are non-recombining. This is in contrast to the X-Y (or Z-W) asymmetry and Y (W) chromosome degeneration in XY (ZW) systems of diploids. Here, we provide evidence that sex chromosomes diverged early during the evolution of haploid liverworts and identify the sex determinant on the Marchantia polymorpha U chromosome. This gene, Feminizer, encodes a member of the plant-specific BASIC PENTACYSTEINE transcription factor family. It triggers female differentiation via regulation of the autosomal sex-determining locus of FEMALE GAMETOPHYTE MYB and SUPPRESSOR OF FEMINIZATION. Phylogenetic analyses of Feminizer and other sex chromosome genes indicate dimorphic sex chromosomes had already been established 430 mya in the ancestral liverwort. Feminizer also plays a role in reproductive induction that is shared with its gametolog on the V chromosome, suggesting an ancestral function, distinct from sex determination, was retained by the gametologs. This implies ancestral functions can be preserved after the acquisition of a sex determination mechanism during the evolution of a dominant haploid sex chromosome system. [Display omitted] •Feminizer (BPCU) linked to the liverwort female sex chromosome was identified•BPCU regulates the autosomal sex-determining locus, FGMYB/SUF•BPCU additionally shares a function for reproductive induction with its gametolog•The liverwort sex chromosomes are the oldest among any other known systems Iwasaki et al. identify a female sex determinant, Feminizer, on the female sex chromosome of a haploid plant, Marchantia polymorpha. Unexpectedly, Feminizer also plays a role in reproductive induction, which is shared by its male gametolog. The liverwort sex chromosomes diverged around 430 mya, older than any known sex chromosome systems.