BSKs Mediate Signal Transduction from the Receptor Kinase BRI1 in Arabidopsis

Abstract

Brassinosteroids bind to the extracellular domain of the receptor kinase BRI1 to activate a signal transduction cascade that regulates nuclear gene expression and plant development. Many components of the brassinosteroid signaling pathway have been identified and studied in detail. However, the substrate of BRI1 kinase that transduces the signal to downstream components remains unknown. Proteomic studies of plasma membrane proteins lead to the identification of three homologous BR-signaling kinases (BSK1, BSK2 and BSK3). The BSKs are phosphorylated by BRI1 in vitro and interact with BRI1 in vivo. Genetic and transgenic studies demonstrate that the BSKs represent a small family of kinases that activate BR signaling downstream of BRI1. These results demonstrate that BSKs are the substrates of BRI1 kinase that activate downstream BR signal transduction. One-sentence summaryBrassinosteroid signaling kinases identified by proteomics Cell-surface receptor kinases activate cellular signal transduction pathways upon perception of extracellular signals, thereby mediating cellular responses to the environment and to other cells. The Arabidopsis genome encodes over 400 receptor-like kinases (RLKs) (1). Some of these RLKs function in growth regulation and plant responses to hormonal and environmental signals. However, the molecular mechanism of RLK signaling to immediate downstream components remains poorly understood, as no RLK substrate that mediates signal transduction has been established in Arabidopsis (2). BRI1 is an RLK that functions as the major receptor for the steroid hormones brassinosteroids (2). Brassinosteroids bind the extracellular domain of BRI1 to activate its kinase activity, initiating a signal transduction cascade that regulates nuclear gene expression and a wide range of developmental and physiological processes ( fig. S1) (3). Many components of the BR signaling pathway have been identified and much detail has been revealed about how BR activates BRI1(4-8) and how phosphorylation by downstream GSK3-like kinase BIN2 regulates the activity of the nuclear transcription factors that mediate §To whom correspondence should be addressed:

Plant GSK3 proteins regulate xylem cell differentiation downstream of TDIF–TDR signalling

“…In the BR signalling at the cell surface, BRASSINOSTEROID-SIGNALLING KINASES (BSKs), which are known to function as cytoplasmic protein kinases, dissociate from BRI1 receptor complexes upon BRs perception 42 . This dissociation allows BSKs to interact with BRI1 SUPPRESSOR 1 (BSU1) 42,43 , which is a protein phosphatase and inactivates BIN2 by dephosphorylation 43 . We revealed that the PM-localized LRR-RLK TDR is closely associated with GSK3s including BIN2.…”

Functional importance of BAK1 tyrosine phosphorylation in vivo

“…Brassinosteroid signaling kinase 1 (BSK1) may be the first downstream component that is phosphorylated by BRI1, which then activates the protein phosphatase BSU1 that can dephosphorylate/inactivate BIN2 (a glycogen synthase 3 protein kinase), which is the kinase that phosphorylates the transcription factors BZR1 and BZR2/BES1. 11 As a result, dephosphorylation of the transcription factors is promoted, which allows them to move into the nucleus to up or downregulate the many genes that are controlled by BR signaling. 12,13 The Arabidopsis genome contains more than 600 receptor-like kinase homologues.…”

Structural basis for the impact of phosphorylation on the activation of plant receptor-like kinase BAK1

“…Our study has provided clear structural evidence to support the previous speculation [5] that the initial phosphorylation of the BAK1 activation loop locks BAK1 kinase in the active conformation. BAK1 in turn phosphorylates and fully activates the ligand-binding RLK, which phosphorylates downstream substrates for signal transduction and the development of the innate immune responses of plants [14,15].…”