Blocking constitutive autophagy rescues the loss of acquired heat resistance in Arabidopsis fes1a

High temperature is one of several major abiotic stresses that can cause substantial loss of crop yields. Heat shock proteins (HSPs) are key components of heat stress resistance. Mutation of FES1A, an auxiliary molecular chaperone of HSP70, leads to defective acquired thermotolerance. Autophagy is a positive regulator of basal thermotolerance and a negative regulator of heat stress memory, but its function in acquired thermotolerance is unclear. We found that blocking constitutive autophagy rescued the heat sensitivity of fes1a in Arabidopsis thaliana. Immunoblot and proteomic analyses showed that the rescue was not due to increased HSP levels. Instead, proteomic analysis and confocal microscopy studies revealed that knocking out the core autophagy-related (ATG) genes leads to accumulation of peroxisomes, thus upregulating the metabolic pathways within the peroxisomes. Accumulation of peroxisomes promotes both reactive oxygen species scavenging and indole-3-acetic acid (IAA) production in atg7 fes1a. Overexpression of ABCD1/PXA1/CTS, a peroxisomal ATP-binding cassette transporter, in atg7 fes1a leads to abnormal peroxisomal function and subsequently thermosensitivity. Moreover, we found that exogenous application of indole-3-butyric acid, IAA or naphthalene-1-acetic acid rescued fes1a heat sensitivity. We propose that autophagy is detrimental to the survival of the fes1a mutant, which has acquired thermosensitivity.