Dynamic regulation of protein homeostasis underlies acquired thermotolerance in Arabidopsis

Rapid climate change demands the development of heat-resilient plants. Elevated temperatures perturb cellular protein homeostasis, and its timely restoration is crucial for plant survival after stress. Thermopriming, which involves pre-exposure to sublethal heat stress, has emerged as a promising strategy for enhancing heat stress tolerance. However, the impact of thermopriming on protein homeostasis remains unclear. Here, we demonstrate that priming-mediated acquired thermotolerance involves the dynamic regulation of protein maintenance and clearance mechanisms. Priming facilitates the activation of heat shock response (HSR) via HSFA1, and unfolded protein response (UPR). Simultaneously, priming induces the protein clearance pathway, namely autophagy, potentially through the dynamic modulation of autophagy-negative regulators. Contrastingly, unprimed seedlings fail to mount HSR and UPR, resulting in disrupted proteostasis and the accumulation of aggregates, and ultimately fail to survive. While the loss of UPR was found to have a minimal impact on priming-mediated outcomes, the HSR response proved essential, as its absence led to lethality under heat stress. Additionally, the absence of HSR was found to enhance the autophagy response post-stress. Our results highlight 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, HSR and UPR responses to maintain proteostasis.