The elucidation of stress memory inheritance in Brassica rapa plants.

Andriy Bilichak,Dawson Fogen,Nina Kepeshchuk,Rafal Wã³Ycicki,Igor Kovalchuk,Yaroslav Ilnytskyy

doi:10.3389/fpls.2015.00005

Andriy Bilichak, Dawson Fogen + Show 4 more

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https://doi.org/10.3389/fpls.2015.00005

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Abstract

Plants are able to maintain the memory of stress exposure throughout their ontogenesis and faithfully propagate it into the next generation. Recent evidence argues for the epigenetic nature of this phenomenon. Small RNAs (smRNAs) are one of the vital epigenetic factors because they can both affect gene expression at the place of their generation and maintain non-cell-autonomous gene regulation. Here, we have made an attempt to decipher the contribution of smRNAs to the heat-shock-induced transgenerational inheritance in Brassica rapa plants using sequencing technology. To do this, we have generated comprehensive profiles of a transcriptome and a small RNAome (smRNAome) from somatic and reproductive tissues of stressed plants and their untreated progeny. We have demonstrated that the highest tissue-specific alterations in the transcriptome and smRNAome profile are detected in tissues that were not directly exposed to stress, namely, in the endosperm and pollen. Importantly, we have revealed that the progeny of stressed plants exhibit the highest fluctuations at the smRNAome level but not at the transcriptome level. Additionally, we have uncovered the existence of heat-inducible and transgenerationally transmitted tRNA-derived small RNA fragments in plants. Finally, we suggest that miR168 and braAGO1 are involved in the stress-induced transgenerational inheritance in plants.

Highlights

Plants constantly interact with environmental factors that can either benefit or jeopardize their homeostasis depending on the intensity and nature of factors encountered
We demonstrated a comprehensive profile of gene expression following heat shock in somatic and reproductive parental tissues and in the untreated progeny of exposed plants
We found that the highest oscillations of gene expression were observed not in parental tissues that were directly exposed to stress but in the developmentally distant untreated seeds, suggesting the existence of a mitotically and meiotically transmitted signal of plant stress response (Figure 1)

Summary

Introduction

Plants constantly interact with environmental factors that can either benefit or jeopardize their homeostasis depending on the intensity and nature of factors encountered. Stress-induced alterations in the transcriptome profile have been shown to be both stressand tissue-specific, the general stress response (GSR) that has been extensively studied in yeast and animals is present in plants (Kreps et al, 2002; Kultz, 2005; Dinneny et al, 2008; Walley and Dehesh, 2010; Iyer-Pascuzzi et al, 2011). Plants may trigger immediate specific gene expression changes to cope with a particular stressor, transgenerational inheritance and responses to stress seem to involve non-specific priming of stress-responsive genes. Distinct epigenetic mediators of multigenerational inheritance of stress memory have been recently identified in two animal models—Drosophila (Seong et al, 2011) and C. elegans (Buckley et al, 2012), which makes it tempting to argue for the existence of similar transgenerational mediators in plants

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