UPL3 promotes BZR1 degradation, growth arrest, and seedling survival under starvation stress in Arabidopsis.

Abstract

Sugar-mediated regulation of hormone signaling is crucial for optimizing growth under normal conditions and ensuring survival during environmental stress. Previous studies have shown that sugar starvation induces the degradation of BRASSINAZOLE RESISTANT 1 (BZR1), the master transcription factor of the brassinosteroid (BR) signaling pathway, thereby inhibiting growth. However, the molecular mechanism linking sugar signaling to BZR1 degradation remains unknown. To identify proteins that mediate starvation-induced BZR1 degradation, we performed a quantitative proteomic analysis of the BZR1 interactome under starvation conditions and identified UBIQUITIN PROTEIN LIGASE 3 (UPL3) as a sugar-regulated protein that promotes BZR1 degradation and regulates growth and survival in response to sugar availability. upl3 mutants showed increased BZR1 accumulation and larger seedling size compared to the wild type under sugar-limiting conditions, but not when grown on sugar-containing medium, which indicates that UPL3 mediates BZR1 degradation and growth inhibition under sugar-limited conditions. Although upl3 mutations promoted growth under short-term starvation, they substantially reduced survival under long-term starvation. The enhanced growth phenotype of upl3 was also observed when target of rapamycin (TOR) was inactivated, but not when BR biosynthesis was blocked, suggesting that UPL3 acts downstream of sugar-TOR signaling to regulate BZR1 degradation. Furthermore, UPL3 protein levels increased post-transcriptionally in response to starvation and TOR inhibition, and decreased upon sugar treatment. Our study identifies UPL3 as a key molecular link between sugar signaling and BR signaling. We propose that sugar-TOR signaling inhibits UPL3 to promote BZR1 accumulation and growth, thereby optimizing plant growth and survival in response to sugar availability.