Plant response to intermittent heat stress involves modulation of mRNA translation efficiency

Acquired thermotolerance (also known as priming) is the ability of cells or organisms to survive acute heat stress if preceded by a milder one. In plants, acquired thermotolerance has been studied mainly at the transcriptional level, including recent descriptions of sophisticated regulatory circuits that are essential for this learning capacity. Here, we tested the involvement of polysome-related processes [translation and cotranslational mRNA decay (CTRD)] in Arabidopsis (Arabidopsis thaliana) thermotolerance using two heat stress regimes with and without a priming event. We found that priming is essential to restore the general translational potential of plants shortly after acute heat stress. We observed that mRNAs not involved in heat stress suffered from reduced translation efficiency at high temperatures, whereas heat stress-related mRNAs were translated more efficiently under the same condition. We also showed that the induction of the unfolded protein response (UPR) pathway in acute heat stress is favored by a previous priming event and that, in the absence of priming, ER-translated mRNAs become preferential targets of CTRD. Finally, we present evidence that CTRD can specifically regulate more than a thousand genes during heat stress and should be considered as an independent gene regulatory mechanism.