Tomato HsfA1a plays a critical role in plant drought tolerance by activating <i>ATG</i> genes and inducing autophagy

<div><p>Autophagy plays critical roles in plant responses to stress. In contrast to the wealth of information concerning the core process of plant autophagosome assembly, our understanding of the regulation of autophagy is limited. In this study, we demonstrated that transcription factor HsfA1a played a critical role in tomato tolerance to drought stress, in part through its positive role in induction of autophagy under drought stress. <i>HsfA1a</i> expression was induced by drought stress. Virus-induced <i>HsfA1a</i> gene silencing reduced while its overexpression increased plant drought tolerance based on both symptoms and membrane integrity. <i>HsfA1a</i>-silenced plants were more sensitive to endogenous ABA-mediated stomatal closure, while its overexpression lines were resistant under drought stress, indicating that phytohormone ABA did not play a major role in <i>HsfA1a</i>-induced drought tolerance. On the other hand, <i>HsfA1a</i>-silenced plants increased while its overexpression decreased the levels of insoluble proteins which were highly ubiquitinated under drought stress. Furthermore, drought stress induced numerous <i>ATGs</i> expression and autophagosome formation in wild-type plants. The expression of <i>ATG10</i> and <i>ATG18f</i>, and the formation of autophagosomes were compromised in <i>HsfA1a</i>-silenced plants but were enhanced in <i>HsfA1a</i>-overexpressing plants. Both electrophoretic mobility shift assay and chromatin immunoprecipitation coupled with qPCR analysis revealed that HsfA1a bound to <i>ATG10</i> and <i>ATG18f</i> gene promoters. Silencing of <i>ATG10</i> and <i>ATG18f</i> reduced HsfA1a-induced drought tolerance and autophagosome formation in plants overexpressing <i>HsfA1a</i>. These results demonstrate that HsfA1a induces drought tolerance by activating <i>ATG</i> genes and inducing autophagy, which may promote plant survival by degrading ubiquitinated protein aggregates under drought stress.</p></div>