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

Pepper (Capsicum) is among the most widely cultivated and consumed vegetable crops worldwide. Although 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 multiomics approach to investigate transcriptome and epigenome dynamics during pepper fruit pericarp development and ripening. Our analyses reveal coordinated changes in epigenetic modifications accompanying transcriptome reprogramming. Changes in H3K27ac are closely associated with chromatin accessibility dynamics, and H3K27me3 dynamics may contribute to the transition from fruit growth to ripening. Construction of a transcriptional regulatory network suggests that several ripening regulators identified in climacteric tomato may also play critical roles in governing ripening in nonclimacteric pepper. During ripening, DNA methylation, particularly in the CG and CHG contexts, undergoes global demethylation, especially at promoter regions, accompanied by increased chromatin accessibility and likely enhances transcription factor binding. Such global demethylation resembles that observed in tomato, suggesting a potentially conserved regulatory mechanism during fruit development within the Solanaceae family. Furthermore, comparative analyses between pepper and tomato reveal conserved epigenetic regulation of key ripening-associated transcription factors, alongside distinct regulation of ethylene biosynthesis. We also demonstrate transcriptional and epigenetic regulation of carotenoid and vitamin C biosynthesis pathways in pepper. Collectively, this study provides a comprehensive resource for mechanistic dissection and comparative analysis of pepper fruit development and ripening, with potential applications for crop improvement. To facilitate data exploration, the datasets have been integrated into an online browser at http://pepperfruitatlas.org.