Haplotype‐resolved genome reveals allele‐aware epigenetic and 3D chromatin regulation of heterosis in the tea hybrid

Heterosis, widely used in plant breeding to enhance yield and quality, is not yet fully understood at the allelic level, particularly in woody plants such as Camellia sinensis, the tea plant. In this study, the first haplotype (HA)-resolved genome of JGY, the most widely cultivated hybrid oolong tea cultivar in China, is presented, and the contribution of its epigenetic and 3D genomic features to heterosis is explored. It was revealed that CHG methylation in gene bodies serves as a key epigenetic predictor of allele-specific expression (ASE), as identified by machine learning models. Additionally, it was shown that allele-specific chromatin accessibility plays a significant role in regulating ASE, with specific chromatin regions in the promoter of CsDXS2, a key enzyme in the methylerythritol phosphate (MEP) terpene biosynthesis pathway, being responsible for the modulation of its expression through CsBZIP48. Furthermore, HA-resolved Hi-C analysis uncovered large-scale chromatin reorganization in the hybrid, including A/B compartment switching and topologically associating domain (TAD) reorganization, which are linked to changes in gene expression, particularly in aroma-related genes. These findings highlight the coordinated reprogramming of parental epigenetic and 3D genomic features during hybridization and provide new insights into the molecular mechanisms underlying heterosis in woody plants.