Epigenetic patterns maintained in early Caenorhabditis elegans embryos can be established by gene activity in the parental germ cells

PLoS Genet. 2011 Jun;7(6):e1001391. doi: 10.1371/journal.pgen.1001391. Epub 2011 Jun 9.

Abstract

Epigenetic information, such as parental imprints, can be transmitted with genetic information from parent to offspring through the germ line. Recent reports show that histone modifications can be transmitted through sperm as a component of this information transfer. How the information that is transferred is established in the parent and maintained in the offspring is poorly understood. We previously described a form of imprinted X inactivation in Caenorhabditis elegans where dimethylation on histone 3 at lysine 4 (H3K4me2), a mark of active chromatin, is excluded from the paternal X chromosome (Xp) during spermatogenesis and persists through early cell divisions in the embryo. Based on the observation that the Xp (unlike the maternal X or any autosome) is largely transcriptionally inactive in the paternal germ line, we hypothesized that transcriptional activity in the parent germ line may influence epigenetic information inherited by and maintained in the embryo. We report that chromatin modifications and histone variant patterns assembled in the germ line can be retained in mature gametes. Furthermore, despite extensive chromatin remodeling events at fertilization, the modification patterns arriving with the gametes are largely retained in the early embryo. Using transgenes, we observe that expression in the parental germline correlates with differential chromatin assembly that is replicated and maintained in the early embryo. Expression in the adult germ cells also correlates with more robust expression in the somatic lineages of the offspring. These results suggest that differential expression in the parental germ lines may provide a potential mechanism for the establishment of parent-of-origin epigenomic content. This content can be maintained and may heritably affect gene expression in the offspring.

Publication types

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

MeSH terms

  • Animals
  • Caenorhabditis elegans / embryology*
  • Caenorhabditis elegans / genetics*
  • Caenorhabditis elegans / metabolism
  • Chromatin / metabolism
  • DNA Methylation
  • Embryo, Nonmammalian / metabolism*
  • Epigenesis, Genetic*
  • Gene Expression Regulation, Developmental
  • Germ Cells / cytology*
  • Germ Cells / metabolism
  • Histones / genetics
  • Histones / metabolism
  • Male

Substances

  • Chromatin
  • Histones