Transcriptional network regulation of the brassinosteroid signaling pathway by the BES1-TPL-HDA19 co-repressor complex

Main conclusion The brassinosteroid-related BES1 and BZR1 transcription factors dynamically modulate downstream gene networks via the TPL-HDA19 co-repressor complex in BR-signaling pathways in Arabidopsis thaliana. Brassinosteroids (BRs) are plant steroid hormones that are essential for diverse growth and developmental processes across the whole life cycle of plants. In Arabidopsis thaliana, the BR-related transcription factors BRI1-EMS-SUPPRESSOR 1 (BES1) and BRASSINAZOLE-RESISTANT 1 (BZR1) regulate a range of global gene expression in response to BR and several external signaling cues; however, the molecular mechanisms by which they mediate the reprogramming of downstream transcription remain unclear. We here report that formation of a protein complex between BES1 and BZR1 and Histone Deacetylase 19 (HDA19) via the conserved ERF-associated amphiphilic repression (EAR) motif proved essential for regulation of BR-signaling-related gene expression. Defects in BR-related functions of BES1 and BZR1 proteins containing a mutated EAR motif were completely rescued by artificial fusion with EAR-repression domain (SRDX), TOPLESS (TPL), or HDA19 proteins. RNA-sequencing analysis of Arabidopsis plants over-expressing bes1-DmEAR or bes1-DmEAR-HDA19 revealed an essential role for HDA19 activity in regulation of BES1/BZR1-mediated BR signaling. In addition to BR-related gene expression, the BES1-HDA19 transcription factor complex was important for abiotic stress-related drought stress tolerance and organ boundary formation. These results suggested that integrating activation of BR-signaling pathways with the formation of the protein complex containing BES1/BZR1 and TPL-HDA19 via the EAR motif was important in fine-tuning BR-related gene networks in plants.