Dynamic regulation of protein homeostasis underlies acquired thermotolerance in Arabidopsis thaliana

Rapid climate change necessitates the development of heat-stress resilient plants. Elevated temperatures perturb cellular protein homeostasis, and its timely restoration is critical for plant survival post-stress. Thermopriming, which involves pre-exposure to sublethal heat stress, has emerged as a promising approach to enhance heat stress tolerance. However, the impact of thermopriming on protein homeostasis remains unclear. This study demonstrates that priming-mediated short-term acquired thermotolerance involves dynamic regulation of protein maintenance (HSPs) and clearance (autophagy) mechanisms. Priming facilitates an increase in HSP abundance through HSFA1 activation. Concurrently, priming induces autophagy through dynamic modulation of autophagy-negative regulators through IRE1’s-mRNA degradation activity. Contrarily, unprimed seedlings fail to exhibit such coordinated regulation, resulting in disrupted proteostasis and fail to survive. While the loss of IRE1 had minimal impact on priming-mediated outcomes, HSFA1 proved essential, as its absence led to lethality under heat stress. This underscores the critical role of protein maintenance mechanisms over clearance pathways in ensuring survival. Taken together, our study demonstrates that thermopriming enhances heat stress resilience by temporally coordinating autophagy and chaperone responses to maintain proteostasis.