Weighted correlation network analysis of the genes in the eyes of juvenile Plectropomus leopardus provide novel insights into the molecular mechanisms of the adaptation to the background color.

Plectropomus leopardus is a valuable marine fish whose skin color is strongly affected by the background color. However, the influence of the visual sense on the skin color variation of P. leopardus remains unknown. In the present study, transcriptome analysis was used to examine the visual response mechanism under different background colors. Paraffin sections of the eyes showed that the background color caused morphological changes in the pigment cells (PCs) and outer nuclear layer (ONL) and the darkening of the iris color. The transcriptome analysis results indicated that the gene expressions in the eyes of P. leopardus were significantly different for different background colors. We identified 4845, 3069, 5874, and 6309 differentially expressed genes (DEGs) in the pairwise comparisons of white vs. initial, blue vs. initial, red vs. initial, and black vs. initial groups, respectively. Some hub genes and key pathways regulating the adaptive mechanism of P. leopardus's eyes to the background color were identified, i.e., the JAK-STAT, mTOR, and Ras signaling pathways, and the ndufb7, slc6a13, and novel.3553 gene. This adaptation was achieved through the synthesis of stress proteins and energy balance supply mediated by hub genes and key pathways. In addition, the phenylalanine metabolism, tyrosine metabolism, and actin cytoskeleton-related processes or pathways and genes were responsible for iris and skin color adaptation. In summary, we inferred that stress protein synthesis, phenylalanine metabolism, and energy homeostasis were critical stress pathways for P. leopardus to adapt its skin color to the environment. These new findings indicate that the P. leopardus skin color variation may have been caused by the environmental adaption of the eyes. The results provide new insights into the molecular mechanisms underlying the skin color adaptation of P. leopardus.