Heat-induced release of epigenetic silencing reveals the concealed role of an imprinted plant gene

PLoS Genet. 2014 Nov 20;10(11):e1004806. doi: 10.1371/journal.pgen.1004806. eCollection 2014 Nov.

Abstract

Epigenetic mechanisms suppress the transcription of transposons and DNA repeats; however, this suppression can be transiently released under prolonged heat stress. Here we show that the Arabidopsis thaliana imprinted gene SDC, which is silent during vegetative growth due to DNA methylation, is activated by heat and contributes to recovery from stress. SDC activation seems to involve epigenetic mechanisms but not canonical heat-shock perception and signaling. The heat-mediated transcriptional induction of SDC occurs particularly in young developing leaves and is proportional to the level of stress. However, this occurs only above a certain window of absolute temperatures and, thus, resembles a thermal-sensing mechanism. In addition, the re-silencing kinetics during recovery can be entrained by repeated heat stress cycles, suggesting that epigenetic regulation in plants may conserve memory of stress experience. We further demonstrate that SDC contributes to the recovery of plant biomass after stress. We propose that transcriptional gene silencing, known to be involved in gene imprinting, is also co-opted in the specific tuning of SDC expression upon heat stress and subsequent recovery. It is therefore possible that dynamic properties of the epigenetic landscape associated with silenced or imprinted genes may contribute to regulation of their expression in response to environmental challenges.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis / genetics
  • Arabidopsis / growth & development
  • Arabidopsis Proteins / genetics*
  • DNA Methylation / genetics*
  • DNA Transposable Elements / genetics
  • Epigenesis, Genetic*
  • F-Box Proteins / genetics*
  • Gene Expression Regulation, Plant
  • Gene Silencing
  • Genomic Imprinting / genetics*
  • Heat-Shock Response / genetics
  • Heat-Shock Response / physiology
  • Repetitive Sequences, Nucleic Acid / genetics
  • Seedlings / genetics
  • Seedlings / growth & development
  • Transcription, Genetic*

Substances

  • Arabidopsis Proteins
  • DNA Transposable Elements
  • F-Box Proteins
  • SDC protein, Arabidopsis

Grants and funding

Research is supported by a European Research Counsel grant 322621-EVOBREED and Gatsby Charitable Foundation Fellowship GAT3273-GLE. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.