Caenorhabditis elegans establishes germline versus soma by balancing inherited histone methylation

Development. 2021 Feb 10;148(3):dev196600. doi: 10.1242/dev.196600.

Abstract

Formation of a zygote is coupled with extensive epigenetic reprogramming to enable appropriate inheritance of histone methylation and prevent developmental delays. In Caenorhabditis elegans, this reprogramming is mediated by the H3K4me2 demethylase SPR-5 and the H3K9 methyltransferase, MET-2. In contrast, the H3K36 methyltransferase MES-4 maintains H3K36me2/3 at germline genes between generations to facilitate re-establishment of the germline. To determine whether the MES-4 germline inheritance pathway antagonizes spr-5; met-2 reprogramming, we examined the interaction between these two pathways. We found that the developmental delay of spr-5; met-2 mutant progeny is associated with ectopic H3K36me3 and the ectopic expression of MES-4-targeted germline genes in somatic tissues. Furthermore, the developmental delay is dependent upon MES-4 and the H3K4 methyltransferase, SET-2. We propose that MES-4 prevents crucial germline genes from being repressed by antagonizing maternal spr-5; met-2 reprogramming. Thus, the balance of inherited histone modifications is necessary to distinguish germline versus soma and prevent developmental delay.This article has an associated 'The people behind the papers' interview.

Keywords: Caenorhabditis elegans; Developmental delay; Epigenetics; Histone methylation; Maternal reprogramming; Transgenerational inheritance.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Caenorhabditis elegans / genetics
  • Caenorhabditis elegans / metabolism*
  • Caenorhabditis elegans Proteins / metabolism
  • Carisoprodol / metabolism*
  • Epigenesis, Genetic
  • Epigenomics
  • Gene Expression
  • Gene Knockdown Techniques
  • Germ Cells / metabolism*
  • Histones / metabolism*
  • Methylation
  • Protein Processing, Post-Translational

Substances

  • Caenorhabditis elegans Proteins
  • Histones
  • Mes-4 protein, C elegans
  • histone H3 trimethyl Lys4
  • Carisoprodol