BZR1 mediates brassinosteroid-induced autophagy and nitrogen starvation tolerance in tomato.

Autophagy, an innate cellular destructive mechanism, plays crucial roles in plant development and responses to stress. Although autophagy can be stimulated or suppressed by multiple molecular processes, the role of phytohormone signaling in autophagy is unclear. Here, we demonstrate that the transcripts of autophagy-related genes (ATGs) and the formation of autophagosomes are triggered by enhanced levels of brassinosteroid (BR). Furthermore, the BR-activated transcription factor brassinazole resistant 1 (BZR1), a positive regulator of the BR signaling pathway, was involved in BR-induced autophagy. Treatment with BR enhanced the formation of autophagosomes and the transcripts of ATGs in BZR1-overexpressing plants, while the effects of BR were compromised in BZR1-silenced plants. Yeast one-hybrid and chromatin immunoprecipitation coupled with qPCR analysis revealed that BZR1 bound to the promoters of ATG2 and ATG6. BR-induced formation of autophagosomes was decreased in ATG2- and ATG6-silenced plants. Moreover, exogenous application of BR enhanced chlorophyll content and autophagosomes formation, and decreased accumulation of ubiquitinated proteins under nitrogen starvation. Leaf chlorosis and chlorophyll degradation were exacerbated in BZR1-silenced plants and the BR biosynthetic mutant d^im, but alleviated in BZR1- and BZR1-1D-overexpressing plants under nitrogen starvation. Meanwhile, nitrogen starvation-induced ATGs expression and autophagosome formation were compromised in both BZR1-silenced and d^im plants, but increased in BZR1- and BZR1-1D-overexpressing plants. Taken together, our results suggest that BZR1-dependent BR signaling upregulates ATGs expression and autophagosome formation, which plays a critical role in plant response to nitrogen starvation in tomato.