Chloroplast Signaling Gates Thermotolerance in Arabidopsis

Temperature is a key environmental variable influencing plant growth and survival. Protection against high temperature stress in eukaryotes is coordinated by heat shock factors (HSFs), transcription factors that activate the expression of protective chaperones such as HEAT SHOCK PROTEIN 70 (HSP70); however, the pathway by which temperature is sensed and integrated with other environmental signals into adaptive responses is not well understood. Plants are exposed to considerable diurnal variation in temperature, and we have found that there is diurnal variation in thermotolerance in Arabidopsis thaliana, with maximal thermotolerance coinciding with higher HSP70 expression during the day. In a forward genetic screen, we identified a key role for the chloroplast in controlling this response, suggesting that light-induced chloroplast signaling plays a key role. Consistent with this, we are able to globally activate binding of HSFA1a to its targets by altering redox status in planta independently of a heat shock. [Display omitted] •There is a diurnal pattern of basal thermotolerance in Arabidopsis•Thermotolerance correlates with diurnal expression patterns of heat-associated genes•Chloroplast mutants have greater heat shock gene expression and thermotolerance•A chloroplast generated light signal gates HSFA1 and heat shock gene expression Plants are most resilient to heat stress during the day, a response controlled by HSFA1 transcription factors activating heat shock genes. Dickinson et al. find that perturbations of chloroplast electron transport affect heat shock gene expression. They show that HSFA1 activity is gated by a light-dependent chloroplast signal.