An integrative multi-omics analysis of histone modifications and DNA methylation reveals the epigenomic landscape in apple under drought stress.

Epigenetic regulation plays a key role in plant development and stress response processes. Although previous studies have found that epigenetic modifications are involved in the drought response in apple, a comprehensive epigenomic profile of the response of apple to drought is needed. To characterize epigenomic profiles during the response of apple to drought, we conducted transcriptome, whole-genome bisulfite sequencing, and ChIP-seq analyses of six histone modifications (H3ac, H3K9ac, H3K14ac, H3K4me3, H3K27me3, and H3K36me3) in Malus hupehensis at 0, 3, 6, and 9 days after drought treatment. The greatest changes in differentially expressed genes were observed after 6 days of drought treatment. However, the highest levels of DNA methylation near the gene region were observed after only 3 days of drought treatment. The global enrichment of six histone modifications slightly decreased under drought treatment. Up-regulated drought-responsive genes with higher fold changes were associated with the hypo-regulation of H3K27me3, and up-regulated genes with lower fold changes were associated with the hyper-regulation of H3K4me3. Many drought-responsive genes such as MYB88, NCED3, and JAZ1 are regulated by epigenetic modifications. We verified the functions of two candidate drought-responsive genes regulated by multiple epigenetic modifications, MdABI5 (regulated by H3K14ac and H3K27me3) and MdOCP3 (regulated by H3K9ac and H3K36me3) in the drought response. The phenotypes of transgenic apple under drought showed that MdABI5 and MdOCP3 positively regulate drought tolerance in apple. Our results provide new insights t for studies of the molecular mechanism of epigenetic modifications and have implications for improving the drought resistance of apple.