Spatial redistribution of key transcriptional regulators in brassinosteroid signaling

Abstract

Brassinosteroids (BRs) are steroid phytohormones required for plant growth and development. The perception of BRs at the plasma membrane initiates intracellular signaling and induces dephosphorylation of two key transcription factors, BZR1 and BZR2/BES1. Phosphorylation of these factors is modulated by the GSK3 kinase BIN2 and phosphatase BSU1 and, in turn, controls DNA binding, protein stabilization, or/and nuclear translocation of BZR1 and BZR2/BES1. However, cytosolic signaling events and the biological roles of phosphorylation in BR signaling are still largely unknown. Recently, we demonstrated that BZR1 itself acts as a cytosolic signaling mediator and regulates expression of BR-responsive genes via phosphorylation-mediated nucleocytoplasmic shuttling. BIN2-mediated phosphorylation mediates nuclear export of BZR1 via interaction with a 14-3-3 protein, while BR activated phosphatases induce nuclear import of BZR1. The temporal and spatial expression of BIN2 appears to be essential in BR signaling. In this addendum, we summarize new findings in BR signaling and discuss the possibility that light and brassinosteroid signals intersect at BIN2 expression.Brassinosteroids (BRs), a group of steroid phytohormones, are essential for plant growth and for developmental processes such as seed germination, stem elongation, vascular differentiation, photomorphogenesis, and stress responses. 1-4 BR initiates its signaling cascade through a plasma membrane-associated receptor kinase complex composed of BRI1 (BRaSSInoSteRoId InSenSItIVe 1) and BaK1 (BRI1 aSSoCIated ReCePtoR KInaSe1). [5][6][7] BR signals perceived at the membrane are transmitted to the nucleus and activate at least two key transcriptional regulators, BZR1 (BRaSSInaZoLe ReSIStant1) and BZR2/ BeS1 (BRaSSInaZoLe ReSIStant2/ BRI1-eMS-SUPPReSSoR 1) via dephosphorylation. 8,9 the phosphorylation status of the two transcriptional regulators is tightly regulated by the activity of the BIn2 kinase and BSU1 (BRI1 SUPPReSSoR1) phosphatase, and is currently regarded as the most reliable readout in BR signaling. [10][11][12] However, lack of accurate information on the mechanism of action and subcellular localization of each signaling component hinders understanding of the precise biological roles of phosphorylation events in BR signaling.Phosphorylation of BZR1 and BZR2/BeS1 may be involved in the protein stabilization, nuclear accumulation of these two factors, as well as their interaction with targeted dna cis-elements. In a recent issue of Plant Cell, 13 we clearly showed that phosphorylation of BZR1 plays a key role in dynamic shuttling of BZR1 between the cytoplasm and the nucleus. BR-activated phosphatases dephosphorylate BZR1 and induce rapid nuclear localization. In the absence of BR signaling, BIn2-mediated phosphorylation events increase nuclear export of BZR1 through an interaction with 14-3-3 proteins. In this study, we identified two functional domains including 10 serine/threonine residues together which have regulatory roles in BIn2-mediated phosphorylat...

Plasma Membrane Receptor Complexes

“…Oligomerization of the BRI1/BAK1 receptors and transphosphorylation of the kinase domains takes place (Wang et al, 2005;Wang and Chory, 2006). This inhibits, via an unknown pathway, the phosphorylation of BZR1 (for brassinazole resistant 1) by the BIN2 (for BR insensitive 2) kinase that, when phosphorylated, is translocated to (Ryu et al, 2008) and retained in the cytoplasm via 14-3-3 proteins (Gampala et al, 2007). Moreover, BR activates the phosphatase BSU1 (for BRI1 suppressor protein 1) that dephosphorylates BES1 (for BRI1 EMS suppressor 1).…”

Recent Advances in the Regulation of Brassinosteroid Signaling and Biosynthesis PathwaysF

“…Since the same domain is conserved in BES1, it is likely that BIN2 interacts with DM to phosphorylate BES1 as well. BIN2 phosphosphorylates BES1 and BZR1 at their central phosphorylation domain and inhibits their function likely through several different but non‐exclusive mechanisms, including targeted protein degradation, nuclear export and cytoplasmic retention by 14–3–3 s and decreased DNA binding of the BIN2‐phosphorylated protein (He et al 2002; Yin et al 2002b; Vert and Chory 2006; Bai et al 2007; Gampala et al 2007; Ryu et al 2007; Ryu et al 2008, 2010a).…”

Effects of Enhanced Resistance and Transcriptome Analysis of Twig Blight Disease by Exogenous Brassinolide in Myrica rubra

“…Notably, BRI1 and BAK1 are key receptor proteins located on the plasma membrane [28], whereas BZR1 and BES1 are important transcription factors (TFs) involved in the BR signaling pathway. These two TFs regulate the expression of downstream genes through dephosphorylation [29]. It was reported that exogenous BR significantly up-regulated the expression of BR signaling pathway genes in Malus hupehensis, such as MdBRI1, MdBAK1, and MdBZR1 [17].…”