FUST1 is a heat-responsive switch for global translation in plants

Adequate reprogramming of global translation under stress is of critical importance to cell survival in eukaryotes. The phosphorylation of eukaryotic initiation factor-2α is a major pathway for stress-induced translational arrest in animals. Here we report that eIF2α phosphorylation is not induced by heat in Arabidopsis. Instead, we identify an uncharacterized protein, FUST1, that can directly sense heat and initiate translational shutdown in Arabidopsis. FUST1 exhibits heat-dependent condensation both in vivo and in vitro, which is mainly driven by its prion-like domain (PrLD). Molecular dynamic simulation reveals that PrLD undergoes conformational rearrangements and engages more inter-amino acid interactions as temperature increases. Mutations that block this conformational change also diminish FUST1 condensation in vitro and in vivo and impair heat tolerance. FUST1 condensates preferentially partition mRNAs of greater length via electrostatic interactions, recruit translation repressors and RNA decapping and deadenylation factors. Importantly, disruption of FUST1 condensation dramatically compromises translational arrest under heat. As a result, FUST1 condensation precedes and is necessary for the assembly of heat stress granules. These findings thus uncover FUST1 as a molecular switch for translation under heat stress and shed light on engineering of heat-adaptable crops. Ten-day-old Arabidopsis seedlings with genotype Col-0 and fust1 were either treated with physiological temperature (22 ℃), or subjected to heatshock (37 ℃). For each genotype-temperature combination, 2 biological replicates were profiled with RNA-seq and Ribo-seq.