Brassinosteroids fine-tune secondary and primary sulfur metabolism through BZR1-mediated transcriptional regulation

Abstract

For adaptation to ever-changing environments, plants have evolved elaborate metabolic systems coupled to a regulatory network for optimal growth and defense. Regulation of plant secondary metabolic pathways such as glucosinolates (GSLs) by defense phytohormones in response to different stresses and nutrient deficiency has been intensively investigated, while how growth-promoting hormone balances plant secondary and primary metabolism has been largely unexplored. Here, we found that growth-promoting hormone brassinosteroid (BR) inhibits GSLs accumulation while enhancing biosynthesis of primary sulfur metabolites, including cysteine (Cys) and glutathione (GSH) both in Arabidopsis and Brassica crops, fine-tuning secondary and primary sulfur metabolism to promote plant growth. Furthermore, we demonstrate that of BRASSINAZOLE RESISTANT 1 (BZR1), the central component of BR signaling, exerts distinct transcriptional inhibition regulation on indolic and aliphatic GSL via direct MYB51 dependent repression of indolic GSL biosynthesis, while exerting partial MYB29 dependent repression of aliphatic GSL biosynthesis. Additionally, BZR1 directly activates the transcription of APR1 and APR2 which encodes rate-limiting enzyme adenosine 5′-phosphosulfate reductases in the primary sulfur metabolic pathway. In summary, our findings indicate that BR inhibits the biosynthesis of GSLs to prioritize sulfur usage for primary metabolites under normal growth conditions. These findings expand our understanding of BR promoting plant growth from a metabolism perspective.