Plasticity in the meiotic epigenetic landscape of sex chromosomes in Caenorhabditis species

Braden J. Larson, Mike V. Van, Taylor Nakayama, Jo Anne Engebrecht

Research output: Contribution to journalArticle

5 Citations (Scopus)

Abstract

During meiosis in the heterogametic sex in some species, sex chromosomes undergo meiotic sex chromosome inactivation (MSCI), which results in acquisition of repressive chromatin and transcriptional silencing. In Caenorhabditis elegans, MSCI is mediated by MET-2 methyltransferase deposition of histone H3 lysine 9 dimethylation. Here we examined the meiotic chromatin landscape in germ lines of four Caenorhabditis species; C. remanei and C. brenneri represent ancestral gonochorism, while C. briggsae and C. elegans are two lineages that independently evolved hermaphroditism. While MSCI is conserved across all four species, repressive chromatin modifications are distinct and do not correlate with reproductive mode. In contrast to C. elegans and C. remanei germ cells where X chromosomes are enriched for histone H3 lysine 9 dimethylation, X chromosomes in C. briggsae and C. brenneri germ cells are enriched for histone H3 lysine 9 trimethylation. Inactivation of C. briggsae MET-2 resulted in germ-line X chromosome transcription and checkpoint activation. Further, both histone H3 lysine 9 di- and trimethylation were reduced in Cbr-met-2 mutant germ lines, suggesting that in contrast to C. elegans, H3 lysine 9 di- and trimethylation are interdependent. C. briggsae H3 lysine 9 trimethylation was redistributed in the presence of asynapsed chromosomes in a sex-specific manner in the related process of meiotic silencing of unsynapsed chromatin. However, these repressive marks did not influence X chromosome replication timing. Examination of additional Caenorhabditis species revealed diverse H3 lysine 9 methylation patterns on the X, suggesting that the sex chromosome epigenome evolves rapidly.

Original languageEnglish (US)
Pages (from-to)1641-1658
Number of pages18
JournalGenetics
Volume203
Issue number4
DOIs
StatePublished - Aug 1 2016

Fingerprint

Caenorhabditis
Sex Chromosomes
Epigenomics
Lysine
Germ Cells
Caenorhabditis elegans
X Chromosome
Chromatin
Histones
DNA Replication Timing
Chromosomes, Human, 6-12 and X
Disorders of Sex Development
Meiosis
Methylation
Transcriptional Activation
Chromosomes

Keywords

  • Genetics of sex
  • Histone methyltransferases
  • Meiosis
  • MSCI
  • MSUC
  • Sex chromosomes

ASJC Scopus subject areas

  • Genetics

Cite this

Plasticity in the meiotic epigenetic landscape of sex chromosomes in Caenorhabditis species. / Larson, Braden J.; Van, Mike V.; Nakayama, Taylor; Engebrecht, Jo Anne.

In: Genetics, Vol. 203, No. 4, 01.08.2016, p. 1641-1658.

Research output: Contribution to journalArticle

Larson, Braden J. ; Van, Mike V. ; Nakayama, Taylor ; Engebrecht, Jo Anne. / Plasticity in the meiotic epigenetic landscape of sex chromosomes in Caenorhabditis species. In: Genetics. 2016 ; Vol. 203, No. 4. pp. 1641-1658.
@article{9416cd57996c43b4bc701d1245a3be3b,
title = "Plasticity in the meiotic epigenetic landscape of sex chromosomes in Caenorhabditis species",
abstract = "During meiosis in the heterogametic sex in some species, sex chromosomes undergo meiotic sex chromosome inactivation (MSCI), which results in acquisition of repressive chromatin and transcriptional silencing. In Caenorhabditis elegans, MSCI is mediated by MET-2 methyltransferase deposition of histone H3 lysine 9 dimethylation. Here we examined the meiotic chromatin landscape in germ lines of four Caenorhabditis species; C. remanei and C. brenneri represent ancestral gonochorism, while C. briggsae and C. elegans are two lineages that independently evolved hermaphroditism. While MSCI is conserved across all four species, repressive chromatin modifications are distinct and do not correlate with reproductive mode. In contrast to C. elegans and C. remanei germ cells where X chromosomes are enriched for histone H3 lysine 9 dimethylation, X chromosomes in C. briggsae and C. brenneri germ cells are enriched for histone H3 lysine 9 trimethylation. Inactivation of C. briggsae MET-2 resulted in germ-line X chromosome transcription and checkpoint activation. Further, both histone H3 lysine 9 di- and trimethylation were reduced in Cbr-met-2 mutant germ lines, suggesting that in contrast to C. elegans, H3 lysine 9 di- and trimethylation are interdependent. C. briggsae H3 lysine 9 trimethylation was redistributed in the presence of asynapsed chromosomes in a sex-specific manner in the related process of meiotic silencing of unsynapsed chromatin. However, these repressive marks did not influence X chromosome replication timing. Examination of additional Caenorhabditis species revealed diverse H3 lysine 9 methylation patterns on the X, suggesting that the sex chromosome epigenome evolves rapidly.",
keywords = "Genetics of sex, Histone methyltransferases, Meiosis, MSCI, MSUC, Sex chromosomes",
author = "Larson, {Braden J.} and Van, {Mike V.} and Taylor Nakayama and Engebrecht, {Jo Anne}",
year = "2016",
month = "8",
day = "1",
doi = "10.1534/genetics.116.191130",
language = "English (US)",
volume = "203",
pages = "1641--1658",
journal = "Genetics",
issn = "0016-6731",
publisher = "Genetics Society of America",
number = "4",

}

TY - JOUR

T1 - Plasticity in the meiotic epigenetic landscape of sex chromosomes in Caenorhabditis species

AU - Larson, Braden J.

AU - Van, Mike V.

AU - Nakayama, Taylor

AU - Engebrecht, Jo Anne

PY - 2016/8/1

Y1 - 2016/8/1

N2 - During meiosis in the heterogametic sex in some species, sex chromosomes undergo meiotic sex chromosome inactivation (MSCI), which results in acquisition of repressive chromatin and transcriptional silencing. In Caenorhabditis elegans, MSCI is mediated by MET-2 methyltransferase deposition of histone H3 lysine 9 dimethylation. Here we examined the meiotic chromatin landscape in germ lines of four Caenorhabditis species; C. remanei and C. brenneri represent ancestral gonochorism, while C. briggsae and C. elegans are two lineages that independently evolved hermaphroditism. While MSCI is conserved across all four species, repressive chromatin modifications are distinct and do not correlate with reproductive mode. In contrast to C. elegans and C. remanei germ cells where X chromosomes are enriched for histone H3 lysine 9 dimethylation, X chromosomes in C. briggsae and C. brenneri germ cells are enriched for histone H3 lysine 9 trimethylation. Inactivation of C. briggsae MET-2 resulted in germ-line X chromosome transcription and checkpoint activation. Further, both histone H3 lysine 9 di- and trimethylation were reduced in Cbr-met-2 mutant germ lines, suggesting that in contrast to C. elegans, H3 lysine 9 di- and trimethylation are interdependent. C. briggsae H3 lysine 9 trimethylation was redistributed in the presence of asynapsed chromosomes in a sex-specific manner in the related process of meiotic silencing of unsynapsed chromatin. However, these repressive marks did not influence X chromosome replication timing. Examination of additional Caenorhabditis species revealed diverse H3 lysine 9 methylation patterns on the X, suggesting that the sex chromosome epigenome evolves rapidly.

AB - During meiosis in the heterogametic sex in some species, sex chromosomes undergo meiotic sex chromosome inactivation (MSCI), which results in acquisition of repressive chromatin and transcriptional silencing. In Caenorhabditis elegans, MSCI is mediated by MET-2 methyltransferase deposition of histone H3 lysine 9 dimethylation. Here we examined the meiotic chromatin landscape in germ lines of four Caenorhabditis species; C. remanei and C. brenneri represent ancestral gonochorism, while C. briggsae and C. elegans are two lineages that independently evolved hermaphroditism. While MSCI is conserved across all four species, repressive chromatin modifications are distinct and do not correlate with reproductive mode. In contrast to C. elegans and C. remanei germ cells where X chromosomes are enriched for histone H3 lysine 9 dimethylation, X chromosomes in C. briggsae and C. brenneri germ cells are enriched for histone H3 lysine 9 trimethylation. Inactivation of C. briggsae MET-2 resulted in germ-line X chromosome transcription and checkpoint activation. Further, both histone H3 lysine 9 di- and trimethylation were reduced in Cbr-met-2 mutant germ lines, suggesting that in contrast to C. elegans, H3 lysine 9 di- and trimethylation are interdependent. C. briggsae H3 lysine 9 trimethylation was redistributed in the presence of asynapsed chromosomes in a sex-specific manner in the related process of meiotic silencing of unsynapsed chromatin. However, these repressive marks did not influence X chromosome replication timing. Examination of additional Caenorhabditis species revealed diverse H3 lysine 9 methylation patterns on the X, suggesting that the sex chromosome epigenome evolves rapidly.

KW - Genetics of sex

KW - Histone methyltransferases

KW - Meiosis

KW - MSCI

KW - MSUC

KW - Sex chromosomes

UR - http://www.scopus.com/inward/record.url?scp=84981489578&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84981489578&partnerID=8YFLogxK

U2 - 10.1534/genetics.116.191130

DO - 10.1534/genetics.116.191130

M3 - Article

VL - 203

SP - 1641

EP - 1658

JO - Genetics

JF - Genetics

SN - 0016-6731

IS - 4

ER -