A BIN2-GLK1 Signaling Module Integrates Brassinosteroid and Light Signaling to Repress Chloroplast Development in the Dark

Arabidopsis GLYCOGEN SYNTHASE KINASE 3 (GSK3)-like kinases play various roles in plant development, including chloroplast development, but the underlying molecular mechanism is not well defined. Here, we demonstrate that transcription factors GLK1 and GLK2 interact with and are phosphorylated by the BRASSINOSTEROID insensitive2 (BIN2). The loss-of-function mutant of BIN2 and its homologs, bin2-3 bil1 bil2, displays abnormal chloroplast development, whereas the gain-of-function mutant, bin2-1, exhibits insensitivity to BR-induced de-greening and reduced numbers of thylakoids per granum, suggesting that BIN2 positively regulates chloroplast development. Furthermore, BIN2 phosphorylates GLK1 at T175, T238, T248, and T256, and mutations of these phosphorylation sites alter GLK1 protein stability and DNA binding and impair plant responses to BRs/darkness. On the other hand, BRs and darkness repress the BIN2-GLK module to enhance BR/dark-mediated de-greening and impair the formation of the photosynthetic apparatus. Our results thus provide a mechanism by which BRs modulate photomorphogenesis and chloroplast development.