Role of selective autophagy receptors in tomato response to cold stress

Selective autophagy transports damaged organelles or proteins to the autophagosome for degradation through specific cargo receptors. In recent years, an increasing number of selective autophagy receptors in plants have been identified, and they are known to play critical roles in plant development, growth, and stress resistance. However, the exact functions of selective autophagy receptors in crop response to environmental stimuli, particularly cold stress, are largely unknown. In this study, twelve potential selective autophagy receptors were identified in tomato and revealed that cold stress induced the expression of selective autophagy receptor genes, secretory protein 62 (SEC62), next to BRCA1 gene 1a (NBR1a),and NBR1b, but not the expression of ATG8 Interacting Protein 2 (ATI2) and other selective autophagy receptors in tomato plants. Silencing these cold-induced selective autophagy receptor genes via virus-induced gene silencing reduced tomato cold tolerance, as indicated by visual phenotype, maximum photochemical efficiency, membrane integrity and autophagy production. Furthermore, the accumulation of cold-induced oxidized proteins and reactive oxygen species (ROS) increased in SEC62-, NBR1a-, or NBR1b-silenced plants, whereas no notable changes were observed between TRV control and ATI2-silenced plants. Additionally, the activities and expression of antioxidant enzymes, the ratio of reduced glutathione to oxidized glutathione, and the expression level of cold response genes decreased in SEC62-, NBR1a, or NBR1b-silenced plants compared with TRV control plants under cold stress. These results suggest that several selective autophagy receptors of tomato plants confer cold tolerance by inducing autophagy for the degradation of denatured proteins and activation of antioxidant and CBF pathways.