Epigenetic Regulation of Repetitive Elements Is Attenuated by Prolonged Heat Stress in Arabidopsis

Ales Pecinka,Marisa Rosa,Huy Q Dinh,Tuncay Baubec,Nicole Lettner,Ortrun Mittelsten Scheid

doi:10.1105/tpc.110.078493

Abstract

Epigenetic factors determine responses to internal and external stimuli in eukaryotic organisms. Whether and how environmental conditions feed back to the epigenetic landscape is more a matter of suggestion than of substantiation. Plants are suitable organisms with which to address this question due to their sessile lifestyle and diversification of epigenetic regulators. We show that several repetitive elements of Arabidopsis thaliana that are under epigenetic regulation by transcriptional gene silencing at ambient temperatures and upon short term heat exposure become activated by prolonged heat stress. Activation can occur without loss of DNA methylation and with only minor changes to histone modifications but is accompanied by loss of nucleosomes and by heterochromatin decondensation. Whereas decondensation persists, nucleosome loading and transcriptional silencing are restored upon recovery from heat stress but are delayed in mutants with impaired chromatin assembly functions. The results provide evidence that environmental conditions can override epigenetic regulation, at least transiently, which might open a window for more permanent epigenetic changes.

Highlights

Terrestrial plants are inevitably exposed to temperature changes, and their sessile lifestyle requires that they deal with daily and seasonal temperature fluctuations in situ
To investigate whether heat stress has an effect on epigenetically regulated transcription, we exposed 21-d-old in vitro grown plants of line L5, carrying a single insert of a multicopy P35S:GUS gene suppressed by transcriptional gene silencing (TGS) (Morel et al, 2000; Probst et al, 2004), to different regimes of elevated temperature and screened for transcriptional activation of b-glucuronidase (GUS) by histochemical staining
Whereas short heat stress (SHS) for 3 h at 378C had no visible effect, very strong GUS expression was achieved with long heat stress (LHS) for 30 h at 378C (Figure 1A)

Summary

Introduction

Terrestrial plants are inevitably exposed to temperature changes, and their sessile lifestyle requires that they deal with daily and seasonal temperature fluctuations in situ. In addition to sophisticated adaptation mechanisms for these regular variations, they have developed additional signaling, repair, and response functions that are activated upon heat stress exerted by exceptionally high temperatures. Key components of this heat response, among several other pathways involved in protecting various cellular functions and induced upon extreme heat, are heat shock proteins and their corresponding heat shock transcription factors (Kotak et al, 2007). Heat stress leads to increased genetic instability and higher rates of somatic homologous recombination (Lebel et al, 1993; Pecinka et al, 2009).

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Results

Conclusion