Chromatin accessibility mediated transcriptome changes contribute to flavor substance alterations and jasmonic acid hyperaccumulation during oolong tea withering process

During the oolong tea withering process, abiotic stresses induce significant changes in the content of various flavor substances and jasmonic acid (JA). However, the changes in chromatin accessibility during withering and their potential impact remain poorly understood. By integrating ATAC-seq, RNA-seq, metabolite, and hormone assays, we characterized the withering treatment-induced changes in chromatin accessibility, gene expression levels, important metabolite contents, and JA and JA-ILE contents. Additionally, we analyzed the effects of chromatin accessibility alterations on gene expression changes, content changes of important flavor substances, and JA hyperaccumulation. Our analysis identified a total of 3451 open- and 13 426 close-differentially accessible chromatin regions (DACRs) under withering treatment. Our findings indicate that close-DACRs-mediated down-regulated differentially expressed genes (DEGs) resulted in the reduced accumulation of multiple catechins during withering, whereas open-DACRs-mediated up-regulated DEGs contributed to the increased accumulation of important terpenoids, JA, JA-ILE and short-chain C5/C6 volatiles. We further highlighted important DACRs-mediated DEGs associated with the synthesis of catechins, terpenoids, JA and JA and short-chain C5/C6 volatiles and confirmed the broad effect of close-DACRs on catechin synthesis involving almost all enzymes in the pathway during withering. Importantly, we identified a novel MYB transcription factor (CsMYB83) regulating catechin synthesis and verified the binding of CsMYB83 in the promoter-DACRs regions of key catechin synthesis genes using DAP-seq. Overall, our results not only revealed a landscape of chromatin alters-mediated transcription, flavor substance and hormone changes under oolong tea withering, but also provided target genes for flavor improvement breeding in tea plant. This study highlights the important effect of altered chromatin accessibility-mediated transcriptional changes under oolong tea withering on the content alterations of flavor substances and jasmonic acid, and identifies a novel regulator (CsMYB83) that affects catechin synthesis.image