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.

Highlights

  • It has been long recognized that transcriptional gene silencing (TGS) in plants is associated mainly with increased levels of DNA methylation [1,2]

  • Cytosine methylation in asymmetric CHH sequences cannot be maintained in a replicative manner and the RNA-dependent DNA methylation (RdDM) pathway leads to their methylation de novo through sequence-specific targeting with small interfering RNAs, and the mitotic persistence of TGS [7]

  • We report on heat-mediated release of epigenetic silencing and ectopic activation of the Arabidopsis thaliana endosperm-imprinted gene SDC

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Summary

Introduction

It has been long recognized that transcriptional gene silencing (TGS) in plants is associated mainly with increased levels of DNA methylation [1,2]. DNA methylation is found in cytosines (C) residing in CG, CHG and CHH sequence contexts (where H stands for A, T or C). Methyltransferase 1 (MET1) perpetuates CG methylation patterns during DNA replication. Cytosine methylation in asymmetric CHH sequences cannot be maintained in a replicative manner and the RNA-dependent DNA methylation (RdDM) pathway leads to their methylation de novo through sequence-specific targeting with small interfering RNAs, and the mitotic persistence of TGS [7]. De novo DNA methylation occurs in all sequence contexts and is mainly catalyzed by Domains Rearranged Methyltransferase 2 (DRM2) [3,8]

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