Phase separation of GRP7 facilitated by FERONIA-mediated phosphorylation inhibits mRNA translation to modulate plant temperature resilience

Abstract

Changes in ambient temperature profoundly affect plant growth and performance. Therefore, the molecular basis of plant acclimation to temperature fluctuation is of great interest. In this study, we discovered that GLYCINE-RICH RNA-BINDING PROTEIN 7 (GRP7) contributes to cold and heat tolerance in Arabidopsis thaliana. We found that exposure to a warm temperature rapidly induces GRP7 condensates in planta, which can be reversed by transfer to a lower temperature. Cell biology and biochemical assays revealed that GRP7 undergoes liquid–liquid phase separation (LLPS) in vivo and in vitro. LLPS of GRP7 in the cytoplasm contributes to the formation of stress granules that recruit RNA, along with the translation machinery component eukaryotic initiation factor 4E1 (eIF4E1) and the mRNA chaperones COLD SHOCK PROTEIN 1 (CSP1) and CSP3, to inhibit translation. Moreover, natural variations in GRP7 affecting the residue phosphorylated by the receptor kinase FERONIA alter its capacity to undergo LLPS and correlate with the adaptation of some Arabidopsis accessions to a wider temperature range. Taken together, our findings illustrate the role of translational control mediated by GRP7 LLPS to confer plants with temperature resilience.