Identification of genes preventing transgenerational transmission of stress-induced epigenetic states

Proc Natl Acad Sci U S A. 2014 Jun 10;111(23):8547-52. doi: 10.1073/pnas.1402275111. Epub 2014 May 27.

Abstract

Examples of transgenerational transmission of environmentally induced epigenetic traits remain rare and disputed. Abiotic stress can release the transcription of epigenetically suppressed transposons and, noticeably, this activation is only transient. Therefore, it is likely that mechanisms countering the mitotic and meiotic inheritance of stress-triggered chromatin changes must exist but are undefined. To reveal these mechanisms, we screened for Arabidopsis mutants impaired in the resetting of stress-induced loss of epigenetic silencing and found that two chromatin regulators, Decrease in DNA methylation1 (DDM1) and Morpheus' Molecule1 (MOM1), act redundantly to restore prestress state and thus erase "epigenetic stress memory". In ddm1 mutants, stress hyperactivates heterochromatic transcription and transcription persists longer than in the wild type. However, this newly acquired state is not transmitted to the progeny. Strikingly, although stress-induced transcription in mom1 mutants is as rapidly silenced as in wild type, in ddm1 mom1 double mutants, transcriptional signatures of stress are able to persist and are found in the progeny of plants stressed as small seedlings. Our results reveal an important, previously unidentified function of DDM1 and MOM1 in rapid resetting of stress induced epigenetic states, and therefore also in preventing their mitotic propagation and transgenerational inheritance.

Keywords: DNA methylation; chromatin regulation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • ATPases Associated with Diverse Cellular Activities
  • Arabidopsis / genetics
  • Arabidopsis / metabolism
  • Arabidopsis Proteins / genetics*
  • DNA Methylation
  • DNA-Binding Proteins / genetics*
  • Epigenesis, Genetic / genetics*
  • Gene Expression Regulation, Plant
  • Hot Temperature
  • Inheritance Patterns
  • Mutation
  • Nuclear Proteins / genetics*
  • Plants, Genetically Modified
  • Reverse Transcriptase Polymerase Chain Reaction
  • Stress, Physiological / genetics*
  • Transcription Factors / genetics*
  • Transcription, Genetic

Substances

  • Arabidopsis Proteins
  • DDM1 protein, Arabidopsis
  • DNA-Binding Proteins
  • Nuclear Proteins
  • Transcription Factors
  • ATPases Associated with Diverse Cellular Activities
  • MOM protein, Arabidopsis