Dynamic regulation of proteostasis underlies thermopriming-mediated acquired thermotolerance in Arabidopsis

Rapid climate change necessitates the development of heat-resilient plants. Elevated temperatures disrupt cellular protein homeostasis (proteostasis), and its timely restoration is crucial for plant survival following heat stress. Thermopriming, defined as pre-exposure to sublethal heat stress, has emerged as a promising strategy for enhancing heat tolerance. However, the impact of thermopriming on proteostasis remains unclear. Here, we demonstrate that priming-mediated acquired thermotolerance involves the dynamic regulation of protein maintenance and clearance pathways. Thermopriming facilitates activation of the heat shock response (HSR) via HSFA1 and the unfolded protein response (UPR). Concurrently, priming induces the protein clearance pathway, autophagy, potentially through dynamic modulation of autophagy-negative regulators. In contrast, unprimed seedlings fail to mount effective HSR and UPR responses, resulting in disrupted proteostasis, protein aggregate accumulation, and ultimately loss of viability under heat stress. While loss of UPR has minimal impact on priming-mediated thermotolerance, the HSR is essential, as its absence leads to lethality under heat stress. Notably, loss of HSR further enhances autophagy following stress. Our results highlight the critical role of protein maintenance mechanisms over clearance pathways in ensuring survival. Taken together, these findings demonstrate that thermopriming enhances heat stress resilience by temporally coordinating autophagy, HSR, and UPR to maintain proteostasis.