The HsfA1a-BAG5b module mediates thermotolerance through activating autophagy in tomato

Abstract

Heat shock transcription factors (Hsfs) and B-cell lymphoma2 (Bcl-2)-associated athanogene (BAG) proteins are essential for plant responses to high-temperature stress. Autophagy plays a crucial role in plant stress resistance by maintaining intracellular homeostasis. However, the mechanisms by which BAG proteins mediate Hsf-induced autophagy to enhance thermotolerance remain unclear. Here, we found that HsfA1a enhances tomato (Solanum lycopersicum L.) thermotolerance by inducing autophagy to degrade ubiquitinated proteins. HsfA1a directly binds to the BAG5b promoter to activate its expression and also interacts with BAG5b both in vitro and in vivo. The HsfA1a–BAG5b interaction enhances the HsfA1a-mediated transcriptional activation of BAG5b and the autophagy-related gene ATG10. BAG5b-overexpressing plants exhibited enhanced thermotolerance and increased autophagosome accumulation, whereas bag5b mutant plants were hypersensitive to high-temperature stress and showed inhibited autophagosome formation. Furthermore, knockout of BAG5b or ATG10 in HsfA1a-overexpressing plants compromised HsfA1a-induced thermotolerance and autophagosome formation. Taken together, our data reveal that HsfA1a promotes BAG5b expression by binding to its promoter under high-temperature stress. Subsequently, BAG5b interacts with HsfA1a to activate ATG10 expression, which promotes autophagosome formation to degrade ubiquitinated protein aggregates, ultimately enhancing tomato thermotolerance.