Enrichment of H3K9me2 on Unsynapsed Chromatin in<i>Caenorhabditis elegans</i>Does Not Target<i>de Novo</i>Sites

Guo, Yiqing; Yang, Bing; Li, Yini; Xu, Xia; Maine, Eleanor M.

doi:10.1534/g3.115.019828

Cited by 13 publications

(15 citation statements)

References 65 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…One surprising feature of meiotic silencing in Caenorhabditis is that there are variable and relatively subtle effects on transcription (Checchi and Engebrecht 2011a;Guo et al 2015) (Figure 6 and Figure 7), suggesting that transcriptional silencing does not solely explain the function of MSCI/MSUC. However, additional methyltransferases, as supported by our data, and perhaps other chromatin modifications, contribute to silencing and so the full phenotypic consequence of a failure in meiotic silencing is not known.…”

Section: Why Meiotic Silencing In Caenorhabditis?mentioning

confidence: 99%

Plasticity in the Meiotic Epigenetic Landscape of Sex Chromosomes inCaenorhabditisSpecies

Larson

Van

Nakayama³

et al. 2016

Genetics

View full text Add to dashboard Cite

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.

show abstract

Section: Why Meiotic Silencing In Caenorhabditis?mentioning

confidence: 99%

Plasticity in the Meiotic Epigenetic Landscape of Sex Chromosomes inCaenorhabditisSpecies

Larson

Van

Nakayama³

et al. 2016

Genetics

View full text Add to dashboard Cite

show abstract

“…Despite its similarity to the Meiotic Silencing of Unpaired Chromatin (MSUC) process observed in other organisms, genes along unsynapsed chromosomes may not be repressed (Checchi and Engebrecht, 2011). It is thus not clear what consequences result from H3K9me2 enrichment, as it doesn't appear to target genomic regions de novo on unsynapsed X chromosomes in him-8 mutant hermaphrodites, nor are there obvious transcriptional changes (GUO et al 2015). The enrichment for H3K9me2 in unsynapsed chromatin may be a simple consequence of defects in SC assembly and meiotic chromatin reorganization.…”

Section: A Sex Specific Checkpoint At the Initiation Of Synapsismentioning

confidence: 98%

Multiple Sex-Specific Differences in the Regulation of Meiotic Progression inC. elegans

Kempfer

2020

Preprint

View full text Add to dashboard Cite

Meiosis is a highly conserved sexual process, yet significant differences exist between males and females in meiotic regulation in many species. Meiotic progression in C. elegans males proceeds more rapidly than female meiosis, suggesting that female meiotic regulation may be more stringent than in males. We have identified multiple differences in the regulation of synapsis, including a difference that suggests the presence of a female-specific meiotic checkpoint that senses the proper initiation of synapsis. This checkpoint is detected by sex differences in the targeting of histone H3 lysine 9 dimethylation (H3K9me2) to unsynapsed chromatin.During oogenic meiosis in hermaphrodites, the failure to initiate synapsis leads to failure to target H3K9me2 enrichment on unsynapsed chromosomes. Loss of the pachytene checkpoint does not reintroduce H3K9me2 enrichment in hermaphrodites, indicating these checkpoints are separable. In contrast, widespread H3K9me2 enrichment occurs as a result of loss of synapsis initiation in both male meiosis and during spermatogenic meiosis in larval XX hermaphrodites. Additionally, male synapsis is insensitive to loss of the dynein motor light chain DLC-1 and to elevated temperatures, whereas female synapsis is prevented by both conditions. We also show that loss of spindle assembly checkpoint proteins, which provide a kinetic barrier to meiotic progression and are required for DLC-1-dependent synapsis phenotypes in hermaphrodites, does not speed up the rate of synapsis in spermatogenic meiosis . These results indicate that meiosis proceeds more rapidly in males because males lack barriers to meiotic progression that are activated by defective synapsis initiation in females.

show abstract

“…Previous work on H3K9me2 in C. elegans focused on its distribution in broad domains on autosomal arms and the role of H3K9me2 in repressing repetitive sequences (Ikegami et al 2010;Liu et al 2011;Guo et al 2015;Zeller et al 2016). Little investigation has been done into what role the more narrowly focused H3K9me2 found in promoters may be serving in gene regulation.…”

Section: H3k9me2 Promoter Peaks Are Distributed Along the Length Of Amentioning

confidence: 99%

“…In the Drosophila ovary, loss of H3K9me3 leads to up-regulation of testis-specific transcripts that change the fate of ovarian germ cells, leading to sterility (Smolko et al 2018). As in C. elegans, prior investigations of H3K9 methylation loss in Drosophila had focused primarily on up-regulation of repetitive elements (Rangan et al 2011;Wang et al 2011;Guo et al 2015;Zeller et al 2016). However, it is clear that H3K9me2/3 loss leading to up-regulation of small sets of coding genes in a tissue-specific manner can have profound effects on cellular fate and function.…”

Section: Repression Of Germline Gene Expression In the Soma Is Vitalmentioning

confidence: 99%

“…set-25 is not a synMuv B gene and its potential role in regulating germline gene expression in the soma has not been tested. Several studies have analyzed the roles in C. elegans of H3K9me2 and H3K9me3 in regulating the interaction of heterochromatin with the nuclear periphery and repression of repetitive elements (Meister et al 2010;Towbin et al 2012;Guo et al 2015;Zeller et al 2016). Both of these functions primarily rely on the high enrichment of H3K9 methylation on the heterochromatic arms of the autosomes (Ikegami et al 2010;Liu et al 2011;Garrigues et al 2015;Evans et al 2016).…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

LIN-15B promotes enrichment of H3K9me2 on the promoters of a subset of germline genes that are repressed in somatic cells in C. elegans

Rechtsteiner

Costello

Egelhofer

et al. 2018

Preprint

View full text Add to dashboard Cite

Running title: H3K9me2 on synMuv B target genesABSTRACT Repression of germline-promoting genes in somatic cells is critical for somatic development and function. To study how germline genes are repressed in somatic tissues, we analyzed key histone modifications in three Caenorhabditis elegans synMuv B mutants, lin-15B, lin-35, and lin-37, all of which display ectopic expression of germline genes in the soma. LIN-35 and LIN-37 are members of the conserved DREAM complex. LIN-15B has been proposed to work with the DREAM complex but has not been shown biochemically to be a complex member. We found that in wild-type worms synMuv B target genes and germline genes are enriched for the repressive histone modification dimethylation of histone H3 on lysine 9(H3K9me2) at their promoters. Genes with H3K9me2 promoter localization are distributed across the autosomes and not biased toward autosomal arms like broad H3K9me2 domains.Both synMuv B targets and germline genes display dramatic reduction of H3K9me2 promoter localization in lin-15B mutants, but much weaker reduction in lin-35 and lin-37 mutants. This is the first major difference reported between lin-15B and DREAM complex mutants, which likely represents a difference in molecular function for these synMuv B proteins. In support of the pivotal role of H3K9me2 in regulation of germline genes through LIN-15B, global loss of H3K9me2 but not H3K9me3 results in phenotypes similar to synMuv B mutants, high temperature larval arrest and ectopic expression of germline genes in the soma. We propose that LIN-15B-driven enrichment of H3K9me2 on promoters of germline genes contributes to repression of those genes in somatic tissues.

show abstract

Enrichment of H3K9me2 on Unsynapsed Chromatin inCaenorhabditis elegansDoes Not Targetde NovoSites

Cited by 13 publications

References 65 publications

Plasticity in the Meiotic Epigenetic Landscape of Sex Chromosomes inCaenorhabditisSpecies

Plasticity in the Meiotic Epigenetic Landscape of Sex Chromosomes inCaenorhabditisSpecies

Multiple Sex-Specific Differences in the Regulation of Meiotic Progression inC. elegans

LIN-15B promotes enrichment of H3K9me2 on the promoters of a subset of germline genes that are repressed in somatic cells in C. elegans

Contact Info

Product

Resources

About