BES1 Accumulates in the Nucleus in Response to Brassinosteroids to Regulate Gene Expression and Promote Stem Elongation

Abstract

Plant steroid hormones, known as brassinosteroids (BRs), signal through a plasma membrane localized receptor kinase BRI1. We identified bes1, a semidominant suppressor of bri1, which exhibits constitutive BR response phenotypes including long and bending petioles, curly leaves, accelerated senescence, and constitutive expression of BR-response genes. BES1 accumulates in the nucleus in response to BRs. BES1 is phosphorylated and appears to be destabilized by the glycogen synthase kinase-3 (GSK-3) BIN2, a negative regulator of the BR pathway. These results establish a signaling cascade for BRs with similarities to the Wnt pathway, in which signaling through cell surface receptors leads to inactivation of a GSK-3 allowing accumulation of a nuclear protein that regulates target gene expression.

The brassinosteroid signal transduction pathway

“…BZR1 encodes a nuclear protein and a P234L mutation in bzr1-1D stabilizes the protein. Same mutation in BZR1's closest homolog, BZR2/BES1, was later identified in a bri1 suppressor screen [44]. BZR1 and BES1/BZR2 show 88% sequence identity and their phosphorylation and accumulation are similarly regulated by BR and BIN2 [42,44,46].…”

“…Same mutation in BZR1's closest homolog, BZR2/BES1, was later identified in a bri1 suppressor screen [44]. BZR1 and BES1/BZR2 show 88% sequence identity and their phosphorylation and accumulation are similarly regulated by BR and BIN2 [42,44,46]. While both bzr1-1D and bes1-D suppress bri1 and bin2 and are resistant to brassinazole, they show opposite cell elongation phenotypes when grown in the light.…”

“…While both bzr1-1D and bes1-D suppress bri1 and bin2 and are resistant to brassinazole, they show opposite cell elongation phenotypes when grown in the light. The bzr1-1D plants grown in the light show weak dwarfism with reduced hypocotyl and petiole lengths, while bes1-D has elongated organs [42,44]. The bzr1-1D plants contain reduced level of BR due to increased feedback inhibition of BR synthesis, and its weak dwarf phenotype can be rescued by BR treatment.…”

“…Downstream components of this cascade include the BIN2 kinase, the BSU1 phosphatase, and the transcription factors BZR1 [42,43] and its homolog BES1/BZR2 [44,45]. BZR1 and BES1/BZR2 are substrates of the BIN2 kinase [44,46] and BSU1 phosphatase [47], and phosphorylated BZR1 is degraded by the proteasome [46].…”

“…Like animal GSK3 kinases that inhibit the activity of their substrates, BIN2 functions as a negative regulator in BR signal transduction. Dominant mutations of bin2 that increase the kinase activity or overexpression of the wild type BIN2 gene causes bri1-like BR insensitive phenotypes [52][53][54], which is associated with increased phosphorylation and reduced accumulation of BZR1 and BES1 [44,46]. BIN2 interacts with and phosphorylates BZR1 and BES1 in yeast and in vitro.…”