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

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 diploi...

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Published inCurrent 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
LanguageEnglish
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
Online AccessGet full text
ISSN0960-9822
1879-0445
1879-0445
DOI10.1016/j.cub.2021.10.023

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Abstract 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.
AbstractList 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. • Feminizer ( BPCU ) linked to the liverwort female sex chromosome was identified • BPCU regulates the autosomal sex-determining locus, FGMYB /S UF • 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.
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.
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.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.
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.
Author Iwasaki, Miyuki
Singh, Shilpi
Mochizuki, Takako
Kawamura, Shogo
Berger, Frédéric
Wanke, Dierk
Miyazaki, Motoki
Suetsugu, Noriyuki
Yasui, Yukiko
Montgomery, Sean A.
Nishihama, Ryuichi
Kajiwara, Tomoaki
Yamaoka, Shohei
Yagura, Masaru
Kuchitsu, Kazuyuki
Sakamoto, Mika
Yoshitake, Yoshihiro
Hashimoto, Kenji
Bowman, John L.
Yamato, Katsuyuki T.
Tanizawa, Yasuhiro
Nakamura, Yasukazu
Kohchi, Takayuki
Liu, Chang
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/34735792$$D View this record in MEDLINE/PubMed
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Fri Sep 05 10:43:24 EDT 2025
Mon Jul 21 06:03:17 EDT 2025
Tue Jul 01 01:57:18 EDT 2025
Thu Apr 24 22:57:58 EDT 2025
Fri Feb 23 02:43:43 EST 2024
IsDoiOpenAccess true
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Issue 24
Keywords sex differentiation
sex-determining gene
gametolog
sex chromosome evolution
Marchantia polymorpha
sex chromosome
haploid
feminizer
reproduction
Language English
License This is an open access article under the CC BY-NC-ND license.
Copyright © 2021 The Authors. Published by Elsevier Inc. All rights reserved.
This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
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Cell Press
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Snippet 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...
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SubjectTerms 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
Title Identification of the sex-determining factor in the liverwort Marchantia polymorpha reveals unique evolution of sex chromosomes in a haploid system
URI https://dx.doi.org/10.1016/j.cub.2021.10.023
https://www.ncbi.nlm.nih.gov/pubmed/34735792
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https://pubmed.ncbi.nlm.nih.gov/PMC8699743
Volume 31
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