SWI/SNF chromatin remodeling determines brassinosteroid-induced transcriptional activation

The brassinosteroid (BR) hormone is a central modulator of plant growth, development, and responses to stresses by activating or repressing the expression of thousands of genes through the transcription factor BRASSINAZOLE-RESISTANT 1 (BZR1) and its homologues. However, the molecular mechanism that determines the transcriptional activation versus repression activity of BZR1 remains largely unclear. Here, we show that BZR1-responsive transcriptional activation at thousands of loci requires the Switch defective/sucrose non-fermentable (SWI/SNF)-complexes-mediated chromatin accessibility regulation. BR-activated BZR1 controls the activation or repression of thousands of BZR1 target genes through reprograming genome-wide chromatin accessibility landscape in Arabidopsis thaliana. BZR1 physically interacts with the BRAHMA (BRM)-Associated SWI/SNF complexes (BAS), co-localizes with BRM on the genome, and enhances BRM occupancy at sites of increased accessibility by BR. Loss of BRM abrogates the capacity of BZR1 to increase but not decrease chromatin accessibility, blocks BR-induced hypocotyl elongation, and diminishes BZR1-mediated transcriptional activation rather than repression. Together, our work reveals that the BAS chromatin remodeling complex is a critical epigenetic regulatory partner in dictating BZR1-mediated transcriptional activation ability, thus providing a long sought mechanistic explanation for how BR signaling activates gene transcription in shaping diverse developmental programs. TeaserBZR1-responsive transcriptional activation activity at thousands of loci requires the SWI/SNF-complexes-mediated chromatin accessibility regulation.