Temperature is sensed both on and inside a cell. How the interior of a plant cell senses external heat stress to orchestrate thermotolerance remains unknown. Here we identify an uncharacterized protein that we named as FUST1, being indispensable for heat stress tolerance 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 under heat stress temperatures. Mutations that block this conformational switch also diminish FUST1 condensation in vitro and in vivo and impair heat tolerance. FUST1 condensates associate with stress granule (SG) components and translation factors. Importantly, FUST1 condensation precedes thereby drives the assembly of stress granules. Loss of FUST1 condensation impairs the translational shutdown under heat stress. FUST1 is present in all land plants and its heat-dependent condensation is conserved. These findings thus uncover plant FUST1 as a heat stress sensor that mediates heat tolerance via its condensation.