Exposure to environmental stress induces a transient epigenetic memory response in Arabidopsis

Environmental fluctuations occur constantly to varying extents, yet rarely cause detrimental effects to the survival of organisms. Most organisms adapt slowly to novel environments by selecting genetic variants; it has been suggested, however, that induced epigenetic changes could accelerate this process especially in non-motile organisms such as plants. Here we report the identification of epigenetically labile regions of the Arabidopsis genome that are targeted by transient de novo methylation and demethylation in response to hyperosmotic stress. These epigenetic changes are associated with transient adaptive phenotypic stress responses in the direct progeny; they correlate with gene expression changes that are partially mediated by methylation-associated longnoncoding RNAs. The effects, however, are not transmitted equally through male and female sexual lineages due to an active epigenetic reprogramming operating in male gametes. Furthermore, contrary to current views, this “stress memory” is rapidly lost in subsequent generations once normal conditions resume, i.e. in the absence of stress. Our data thus collectively indicate that plants have developed a highly dynamic “short-term memory” stress response, to perceive and respond to environmental stimuli via directing transient epigenetic changes to discrete loci, enabling direct off spring with mechanisms to cope with fluctuations in the environment