UPL3 Promotes BZR1 Degradation, Growth Arrest, and Seedling Survival under Starvation Stress in Arabidopsis.

Abstract

Sugar regulation of hormonal signaling is crucial for optimizing growth under normal conditions and survival under environmental stresses. Previous studies indicate that sugar starvation causes the degradation of BRASSINAZOLE RESISTANT 1 (BZR1), the master transcription factor of the brassinosteroid (BR) signaling pathway, to inhibit growth. The molecular connection between sugar signaling and BZR1 degradation remains unknown. To identify the proteins that mediate starvation-induced BZR1 degradation, here, we performed a quantitative proteomic analysis of BZR1 interactome under starvation and identified UBIQUITIN PROTEIN LIGASE 3 (UPL3) as a sugar-regulated protein that mediates BZR1 degradation and regulates growth and survival according to sugar availability. The upl3 mutants show increased BZR1 accumulation and seedling size compared to the wild type when grown under sugar-limiting conditions but not when grown on sugar-containing media, indicating UPL3 mediates BZR1 degradation and growth inhibition under sugar-limiting conditions. While increasing growth under short-term starvation, the upl3 mutations substantially reduced survival after long-term starvation treatment. The increased-growth phenotype of upl3 is also observed when Target Of Rapamycin (TOR) is inactivated but not when BR synthesis is blocked, consistent with UPL3 regulating BZR1 degradation downstream of sugar-TOR signaling. Further, the UPL3 protein level is increased post-transcriptionally by starvation and TOR inhibition but decreased by sugar treatment. Our study identifies UPL3 as a key molecular link for sugar regulation of BR signaling. Sugar-TOR signaling inhibits UPL3 to promote BZR1 accumulation and growth, thereby optimizing growth and survival according to sugar availability.