Multi-omics analysis of the co-expression features of specific neighboring gene pairs suggests an association with catechin regulation in Camellia sinensis

Background: The arrangement and positioning of genes on chromosomes are non-random in plant genomes. Adjacent gene pairs often exhibit similar co-expression patterns and regulatory mechanisms. However, the genomic and epigenetic features influencing such co-expression, particularly in perennial crops like tea ( Camellia sinensis ), remain largely uncharacterized. Results: Firstly, we identified 771 specific neighboring gene pairs (SNGs) in Camellia sinensis (YK10) and investigated the contributions of intergenic distance and gene length to SNGs co-expression. Results indicated that intergenic distance was significantly negatively correlated with co-expression strength, while gene length showed a positive correlation. Furthermore, these two features exerted synergistic effects with threshold characteristics. Secondly, we integrated multi-omics data including transcriptome, ATAC-seq, Hi-C and histone modification data to explore the factors influencing their co-expression and functional significance and found that SNGs marked by either ATAC-seq or H3K27ac peaks displayed significantly higher expression levels, suggesting that epigenetic regulation promotes co-expression. Thirdly, we employed logistic regression models to individually assess the contributions of nine factors—ATAC-seq, H3K27ac, Hi-C, GO, distance, length, promoter, enhancer, and expression level—to the co-expression of SNGs. Finally, by integrating co-expression networks with metabolic profiles, several transcription factors potentially involved in the regulation of catechin metabolic pathways were identified. Conclusions: Collectively, this study reveals a multilayered regulatory framework governing SNG co-expression and provides theoretical insights and candidate regulators for understanding metabolic regulation in tea plants.