Dynamic Chromatin Accessibility and Transcriptional Regulation in the Eyes of Red Tilapia (Oreochromis sp.) in Response to Wintering Stress

Abstract

During wintering, red tilapia may develop variable black spots on their bodies, significantly reducing their market value. Understanding the mechanisms driving this phenomenon is essential for molecular improvements in body color. In this study, we investigated chromatin accessibility landscapes in the eyes of red tilapia with two distinct phenotypes (normal pure red and black spot) under wintering stress using ATAC-seq and RNA-seq analyses. We observed that approximately 32.7% of chromatin accessibility peaks were located in promoter regions, followed by intergenic regions (32.4%) and intronic regions (26.7%). One thousand two hundred twenty-nine differentially accessible regions (DARs) and 1448 differentially expressed genes (DEGs) were identified between the RS and DS groups. Notably, DEGs associated with melanin synthesis, including tyrp1, tyr, tyrp1b, pmela, slc24a5, and mlph, were significantly upregulated in the DS group, which aligns with the observed 1.85-fold increase in melanin content, compared to the RS group. 92 DEGs were associated with significant changes in chromatin accessibility between groups (R² = 0.8059; p < 0.0001), indicating potential regulatory relationships. Interestingly, 23.92% of the DARs were located on the chromosome 3. Specifically, a 2.5-fold difference in average peak height on LG3: 11,215,273–11,217,225 were observed between DS and RS tilapia. In the region, transcription factors including HSF1 and HSF2 were identified as key regulators of chromatin structure and gene expression under wintering stress. Our findings reveal that dynamic chromatin accessibility in the eyes of red tilapia facilitates adaptation to wintering stress by regulating visual signaling, melanin production, and downstream pigmentation.