Dynamic epigenetic and transcriptional regulatory network in pepper fruit development and ripening

Abstract

Pepper (Capsicum) is among the most widely cultivated and consumed vegetable crops worldwide. Although extensive studies in model fruit crops such as tomato have provided insights into the genetic and epigenetic regulation of fruit development and ripening, comparable knowledge in pepper remains limited. Here, we employ a multi- omics approach to investigate transcriptome and epigenome dynamics during pepper fruit pericarp development and ripening. Our analyses reveal coordinated changes in chromatin accessibility and histone modifications accompanying transcriptome reprogramming, with changes in H3K27ac closely associated with chromatin accessibility dynamics, and H3K27me3 dynamics potentially contributing to the transition from fruit growth to ripening. Moreover, construction of the transcriptional regulatory network underlying pepper fruit development and ripening suggests that several ripening regulators identified in the climacteric tomato may also play critical roles in governing ripening in the non-climacteric pepper. During ripening, DNA methylation, particularly in the CG and CHG contexts, undergoes global demethylation, especially at promoter regions, which is accompanied by increased chromatin accessibility and likely enhances transcription factor binding activity. We further demonstrate transcriptional and epigenetic regulation of carotenoid and ascorbic acid (vitamin C) biosynthesis pathways. Collectively, this study provides a comprehensive resource for mechanistic dissection and comparative analysis of fruit development and ripening, with practical implications for improving key fruit traits.