Heat-Induced Release of Epigenetic Silencing Reveals the Concealed Role of an Imprinted Plant Gene

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.

Author Summary

In plants, expression of certain imprinted genes is restricted to embryo nourishing tissue, the endosperm. Since these genes are silenced by epigenetic mechanisms during vegetative growth, it has been assumed that they have no role in this phase of the plant life cycle. Here, we report on heat-mediated release of epigenetic silencing and ectopic activation of the Arabidopsis thaliana endosperm-imprinted gene SDC. The stress induced activation of SDC involves epigenetic regulation but not the canonical heat-shock perception and signaling, and it seems to be required for efficient growth recovery after the stress. Our results exemplify a potential concealed role of an imprinted gene in plant responses to environmental challenges.