The capacity of plants to survive exposure to a variety of environmental stresses is of prime importance for food production, especially in the context of global warming. Global climate change is expected to result in a 1.5 to 5.8°C increases in temperature by 2100 and crop yields are predicted to decrease approximately 10% for every one-degree increase in temperature (USDA Release no. 501.09, 2009). Exceptionally high summer temperature is already leading to strong reduction in crop yield and plant are more then ever exposed to extremes of temperature that, combined to other stresses such as drought, is negatively impacting agricultural production worldwide. How climatic variations impact plant life cycles is therefore an urgent question to address in order to improve stress tolerance and adapt agriculture to future rises in temperature. Currently, we have a limited knowledge of the basic molecular mechanisms by which plants survive to stress. Therefore, studying the regulation of gene expression in response to environmental cues is fundamental to understand how plants grow and develop. Recent studies indicate that post-transcriptional regulation of gene expression plays a vital role in stress response and that a radical reprogramming of mRNA decay could be involved. We recently discovered that plant drastically reprogram mRNA decay during heat stress. Indeed, we observed that the RNA-binding protein LARP1 associates during heat stress (15 min at 38°C) with the 5’-3’ exonuclease XRN4 to set up a massive heat-induced mRNA decay process that apparently targets more that 4500 mRNAs in Arabidopsis seedlings. LARP1 is specially required to address XRN4 to polysomes during heat stress, suggesting that part of the degradation is directly initiated on mRNAs engaged in translation. We have also shown by preliminary work that xrn4 mutant plants are clearly affected in their capacity to survive to at least one heat stress regime. Overall, these results strongly suggest that plants regulate the heat stress response at the post-transcriptional level by inducing an essential targeted mRNA decay process. Following this pioneer work, many questions still remain on the biological properties of this Heat-Stress Mediated Decay (H-SMD) including: 1) what is the complete repertoire of Arabidopsis thaliana mRNAs targeted by H-SMD? 2) what other molecular actors are involved ? 3) How mRNAs are selected to be targets of H-SMD and, 4) what is the physiological importance for the plant of this process. In this program we will address these questions by combining biochemical, genetic and phenotypic approaches but also by using new genome-wide technologies. Indeed, using an original pulse-chase non-radioactive labeling method, we will perform a genome-wide analysis of plant mRNAs half-life at 20°C and 38°C. We will also evaluate the general importance of RNA epigenetic modifications (i.e. the presence of patterns of N6-methyladenosines) for mRNA stability at 20°C and 38°C. Most studies so far addressed the plant thermotolerance response at the transcriptional levels. A major originality of this work is to postulate that a post-transcriptional process is also determinant for the plant to acquire thermotolerance properties. Our four interrelated workpackages will allow determining the physiological importance of mRNA decay for plant survival to heat stress. The two partners of the project are highly complementary and have already collaborated on the initial characterization of the heat-induced decay pathway. Partner 1 has a strong expertise in molecular studies of mRNA metabolism and epigenetic regulations. Partner 2 has strong expertise in phenotyping methods to explore thermotolerance diversity and is an international expert of the plant heat stress response. Bringing together these two partners will lead to a tighter integration of the research efforts in this exciting and innovative area of RNA epigenomics and plant stress adaptation.
