Hyperosmotic stress memory in Arabidopsis is mediated by distinct epigenetically labile sites in the genome and is restricted in the male germline by DNA glycosylase activity

Elife. 2016 May 31;5:e13546. doi: 10.7554/eLife.13546.

Abstract

Inducible epigenetic changes in eukaryotes are believed to enable rapid adaptation to environmental fluctuations. We have found distinct regions of the Arabidopsis genome that are susceptible to DNA (de)methylation in response to hyperosmotic stress. The stress-induced epigenetic changes are associated with conditionally heritable adaptive phenotypic stress responses. However, these stress responses are primarily transmitted to the next generation through the female lineage due to widespread DNA glycosylase activity in the male germline, and extensively reset in the absence of stress. Using the CNI1/ATL31 locus as an example, we demonstrate that epigenetically targeted sequences function as distantly-acting control elements of antisense long non-coding RNAs, which in turn regulate targeted gene expression in response to stress. Collectively, our findings reveal that plants use a highly dynamic maternal 'short-term stress memory' with which to respond to adverse external conditions. This transient memory relies on the DNA methylation machinery and associated transcriptional changes to extend the phenotypic plasticity accessible to the immediate offspring.

Keywords: a. thaliana; adaptation; computational biology; environment; epigenetic; evolutionary biology; genomics; memory; systems biology.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis / drug effects*
  • Arabidopsis / genetics
  • Arabidopsis / metabolism
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism
  • Chromosome Mapping
  • DNA Glycosylases / genetics
  • DNA Glycosylases / metabolism
  • DNA Methylation
  • Epigenesis, Genetic
  • Gene Expression Regulation, Plant*
  • Genetic Loci
  • Genome, Plant*
  • Germ Cells
  • Inheritance Patterns*
  • Osmotic Pressure*
  • Sodium Chloride / pharmacology*
  • Stress, Physiological

Substances

  • Arabidopsis Proteins
  • Sodium Chloride
  • DNA Glycosylases

Grant support

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.