SWI/SNF chromatin remodeling factor BRAHMA promotes de novo shoot regeneration by epigenetic priming via H3K27me3 removal.

Plants have a remarkable capacity for regeneration. Recent studies have identified associations between plant regeneration and epigenetic regulators, thereby supporting the hypothesis that dynamic gene expression changes occur during the regeneration process. Notably, the association with chromatin remodeling factors remains to be elucidated. In this study, we demonstrated that BRAHMA (BRM), a core ATPase of the BRM-associated SWI/SNF (BAS) chromatin remodeling complex, plays a crucial role in the shoot regeneration process via root-derived callus formation. Phenotypic and transcriptomic analyses demonstrated that BRM exerts a substantial effect on the transition of gene expression from callus formation to shoot regeneration. Furthermore, epigenomic analysis revealed that BRM contributes to the removal of the silencing mark H3K27me3 indirectly from shoot regeneration-related genes during callus formation, suggesting cooperative functions with plant-specific H3K27me3 demethylases. The transcriptional activation of shoot regeneration-related genes from which H3K27me3 was removed during callus formation did not occur until shoot induction. This suggests that BRM is involved in epigenetic priming, which puts shoot regeneration-related genes in a primed state that allows gene expression immediately after shoot induction. We identified 24 BRM-mediated epigenetic priming targets, which are not expressed during callus formation but are rapidly transcribed after shoot induction. Furthermore, out of these targets, the transcription factor NGATHA 3 (NGA3) and the glycine-rich protein DEFECTIVELY ORGANIZED TRIBUTARIES 1 (DOT1), are involved in the shoot regeneration process through epigenetic priming.