Chromatin accessibility mediated by CHROMATIN REMODELING 11 promotes chilling tolerance in rice

Abstract Chromatin remodeling plays a crucial role in controlling gene transcription by modifying chromatin structure. However, the involvement of chromatin remodeling in plant stress responses, especially cold tolerance, through chromatin accessibility remains largely unexplored. Here, we report that rice (Oryza sativa L.) CHROMATIN REMODELING 11 (OsCHR11) positively regulates chilling tolerance by enhancing chromatin accessibility and facilitating changes in gene expression. Loss-of-function mutants of OsCHR11 exhibited increased susceptibility to chilling stress compared to wild-type rice plants. Transcriptome analysis revealed that the chr11 mutant displays diminished transcriptomic responses to chilling. Additionally, assay for transposase-accessible chromatin indicated that chilling treatment increases chromatin accessibility in the promoter regions, and this process depended on OsCHR11 function. Chromatin immunoprecipitation sequencing showed that OsCHR11 is physically associated with the promoters of cold-responsive genes. Integrated multiomics analysis further demonstrated a correlation between OsCHR11 enrichment and chromatin accessibility, as well as a correlation between chromatin accessibility and gene expression. Furthermore, OsCHR11 is required for the full expression of key cold-response genes, including those involved in trehalose biosynthesis. The exogenous application of trehalose partially rescued the chilling-susceptible phenotype of the chr11 mutant, suggesting that trehalose biosynthesis contributes to the chilling tolerance promoted by OsCHR11. Collectively, these findings indicate that OsCHR11 enhances cold tolerance in plants, likely by increasing chromatin accessibility and elevating the expression levels of cold-response genes in response to chilling.