Integrated transcriptomic and miRNA analyses reveal skin stress-response networks associated with pigmentation regulation in golden-backed crucian carp under heat and UV exposure

The dorsal skin of golden-backed crucian carp ( Carassius auratus , GBCC) exhibits a stable golden coloration, yet its molecular regulation under environmental stress remains unclear. In this study, integrated transcriptome and miRNA sequencing were conducted on skin tissues exposed to control conditions, high temperature (34 °C), ultraviolet (UV) radiation, and combined heat and UV exposure for 48 h. The number of differentially expressed genes and miRNAs increased with stress complexity. KEGG analysis showed that stress-responsive genes were mainly enriched in the MAPK, PI3K-Akt signaling pathways, glycine, serine, threonine, arachidonic acid metabolisms, and protein processing in the endoplasmic reticulum. Melanogenesis-related changes were most evident under UV exposure, but mitf was significantly up-regulated under heat stress, whereas its expression change under UV exposure did not reach the differential-expression threshold. Mfuzz clustering and WGCNA revealed dynamic metabolic reprogramming and treatment-associated co-expression modules linked to antioxidant, inflammatory, apoptotic, and pigmentation-related processes. Differentially expressed miRNAs also increased with stress complexity. Integrated miRNA–mRNA analysis showed that these miRNAs mainly targeted genes involved in the MAPK and PI3K-Akt pathways, including hsp72 , hsp90 , pp5 , and redd1 . These results suggested coordinated post-transcriptional regulation during stress responses. Overall, combined heat and UV stress induced extensive molecular reprogramming in GBCC skin, characterized by enhanced stress-defense signaling and altered pigmentation-associated regulation. These findings provide new insight into the molecular relationship between environmental adaptation and pigmentation maintenance in fish.