Abstract
The chromatin remodeler BRAHMA (BRM) is a Trithorax Group (TrxG) protein that antagonizes the functions of Polycomb Group (PcG) proteins in fly and mammals. Recent studies also implicate such a role for Arabidopsis (Arabidopsis thaliana) BRM but the molecular mechanisms underlying the antagonism are unclear. To understand the interplay between BRM and PcG during plant development, we performed a genome-wide analysis of trimethylated histone H3 lysine 27 (H3K27me3) in brm mutant seedlings by chromatin immunoprecipitation followed by next generation sequencing (ChIP-seq). Increased H3K27me3 deposition at several hundred genes was observed in brm mutants and this increase was partially supressed by removal of the H3K27 methyltransferase CURLY LEAF (CLF) or SWINGER (SWN). ChIP experiments demonstrated that BRM directly binds to a subset of the genes and prevents the inappropriate association and/or activity of PcG proteins at these loci. Together, these results indicate a crucial role of BRM in restricting the inappropriate activity of PcG during plant development. The key flowering repressor gene SHORT VEGETATIVE PHASE (SVP) is such a BRM target. In brm mutants, elevated PcG occupancy at SVP accompanies a dramatic increase in H3K27me3 levels at this locus and a concomitant reduction of SVP expression. Further, our gain- and loss-of-function genetic evidence establishes that BRM controls flowering time by directly activating SVP expression. This work reveals a genome-wide functional interplay between BRM and PcG and provides new insights into the impacts of these proteins in plant growth and development.
Highlights
Plant development takes place in distinct phases, each of which is characterized by the activation of a particular set of genes and the repression of others
SHORT VEGETATIVE PHASE (SVP) is highly expressed during the vegetative phase to promote growth, but the mechanism by which the high expression level of SVP is maintained remains unknown
We report a genome-wide study to examine the functional interplay between the BRM chromatin remodeler and the Polycomb Group (PcG) proteins that catalyze trimethylation of lysine 27 on histone H3 (H3K27me3), a histone mark normally associated with transcriptionally repressed genes
Summary
Plant development takes place in distinct phases, each of which is characterized by the activation of a particular set of genes and the repression of others. Precise control of gene expression in each phase is crucial for proper growth and development. In Arabidopsis, a repressor complex that consists of two MADS box transcription factors, FLOWERING LOCUS C (FLC) and SVP, serves as a negative regulator of flowering time by directly repressing the expression of the floral pathway integrators FLOWERING LOCUS T (FT) and SUPPRESSOR OF OVEREXPRESSION OF CO 1 (SOC1) [1,5,6]. SVP is highly expressed during the vegetative phase [5,7], but is down-regulated during the floral transition by the autonomous and gibberellin (GA) pathways [5], which results in the de-repression of FT and SOC1 to promote flowering. Despite its key role in controlling flowering time, the mechanisms by which SVP expression is regulated are still unknown. No positive regulator(s) of SVP expression in the vegetative phase have been identified
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