The HSFA1B-HSP70-3 module regulates transgenerational thermomemory by modulating SGS3 stability in Arabidopsis

Heat waves triggered by a warming climate profoundly affect plant development and immunity. To ensure successful reproduction and transgenerational adaptation to stress, plants have evolved a sophisticated machinery to deploy transgenerational thermomemory of early flowering and attenuated immunity; this is associated with the induction of heat shock proteins (HSPs), which act as molecular chaperones to stabilize proteins under heat stress. However, how HSPs regulate plant transgenerational thermomemory remains largely elusive. Here, we show that HEAT SHOCK PROTEIN 70-3 (HSP70-3) interacts with SUPPRESSOR OF GENE SILENCING 3 (SGS3), a plant-specific RNA-binding protein whose transgenerational degradation is critical for transgenerational thermomemory in Arabidopsis (Arabidopsis thaliana). HSP70-3 competes with E3 ubiquitin ligase SGIP1 for SGS3 binding. Furthermore, HSP70-3 is directly targeted and activated by the heat-responsive transcription factor HSFA1B. The downregulation of HSFA1B in plants under long-term heat stress and their unstressed progeny contributes to the thermomemory repression of HSP70-3 expression. Consequently, diminished HSP70-3-mediated protection results in heat-induced SGS3 degradation by the E3 ligase SGIP1. Our results thus reveal an important regulatory module, HSFA1B-HSP70-3-SGS3, in transgenerational thermomemory, shedding light on the essential function of HSP molecular chaperones in the establishment of thermomemory in plants.