Regulation of the nuclear activities of brassinosteroid signaling

Abstract

Brassinosteroids (BRs) are important plant growth hormones that largely rely on transcription factors (TFs) to regulate a variety of plant physiological/developmental processes. Past genetic and biochemical studies have identified two key TFs and interacting partners that play major roles in regulating many BR-responsive genes, while genome-wide microarray experiments have discovered at least 50 BR-regulated TFs. However, little is known how these TFs function or whether additional TFs are involved in BR signaling. In the past few years, genetic studies and yeast one/two-hybrid screens coupled with microarray and chromatin immunoprecipitation experiments not only revealed new roles of the key regulatory TFs but also implicated additional TFs and other nuclear proteins in regulating the nuclear activities of BR signaling in Arabidopsis and rice.

Figure 1

The potential roles of BES1 and BR-related TFs in plant development. (A). In Arabidopsis flowers, BES1 likely binds to the promoters of known anther/pollen regulatory TFs and a female gametophytic receptor-like kinase FERONIA to affect anther/pollen development and pollen discharge, respectively. (B). In Arabidopsis embryos, BIM1 physically and genetically interact with DRN and PVH to regulate cotyledon development while an auxin-dependent MP directly activates the expression of DRN and ATBS1 (encoding an atypical bHLH protein recently implicated in BR signaling [33]) to control embryonic cotyledon and root development, respectively. (C). In Arabidopsis root, auxin induces the BRX expression likely though an ARF and promotes the translocation of BRX from the cell surface to the nucleus where it activates the CPD expression crucial for BR biosynthesis.

Figure 2

The involvement of bHLH proteins and TFs of other families in BR signaling. (A). In Arabidopsis, BR induces AIF1 and PRE1 but inhibits ATBS1 and AtIBH1 with BZR1 binding to both PRE1 and AtIBH1 promoters. ATBS1 binds AIF1, thus inhibiting AIF1 dimerization with yet to be discovered bHLH proteins (X) that activate a subset of BR-responsive genes, while PRE1 heterodimerizes with AtIBH1 that functions as a negative regulator of BR-mediated cell elongation. BR also induces the expression of TCP1, which encodes a non-canonical bHLH protein that binds and activates the DWF4 promoter to stimulate BR biosynthesis, and stimulate the AtMYB30 gene, a directly target of BES1. BES1 was shown to interact with AtMYB30 on the promoters of some BR-responses genes to amplify BR signaling. (B). In rice, BR induces BU1 and ILI1 but suppresses IBH1 and DLT with OsBZR1 binding to the promoters of ILI1, IBH1, and DLT. ILI1 heterodimerizes with and thus inhibits IBH1 that blocks BR signaling; while DLT promotes BR signaling and plays a role in feedback regulation, likely by activating BR-upregulated genes and OsBZR1. The BR signaling in rice might also be negatively regulated by three SVP-type MADS proteins that likely localize in the cytosol [60].

Figure 3

BES1-mediated recruitment of elongation factors and histone-modifying proteins. BES1 not only binds histone-modifying proteins ELF6 and REF6 in the promoters of BR-responsive genes to initiate their transcription, most likely through demethylating histone H3 and altering chromatin structure, but also recruits elongation factors to the phosphorylated C-terminal domain (CTD-P) of the RNA polymerase II (RNAPII) within the transcribed regions of BR-regulated genes to promote the production and export of their mRNAs.