Transposon insertion in pmel17 rewired skin and muscle transcriptomes in Mozambique tilapia

Abstract The pmel17 gene plays a crucial role in melanin pigmentation. Our previous studies showed that in Mozambique tilapia, a transposon inserted into the 3’ untranslated region (3′ UTR) of pmel17 resulted in the silencing of pmel17 and led to the loss of melanin pigments (golden mutant phenotype). Additionally, the transposon insertion caused reduced growth performance and increased locomotion. In this study, to investigate the mechanisms underlying these phenotypic changes, we sequenced transcriptomes of the skin and muscle samples collected from wildtype and mutant tilapias. A total of 51 and 141 differentially expressed genes (DEGs) were identified in the skin and muscle transcriptomes, respectively. DEGs in the skin were primarily down-regulated in golden genotypes and associated with neural crest development and melanin pigmentation pathways. Besides these DEGs involved in the classic melanin pigmentation pathway of vertebrates, 14 DEGs were also observed to be related to melanogenesis. In muscle transcriptomes, there was an enrichment of GO terms associated with growth factors and cellular lipid catabolic processes. Specifically, DEGs related to growth factor binding exhibited a down-regulation, while those related to lipid metabolism showed an up-regulation in mutant genotypes. These findings agree with observed phenotypic changes. Furthermore, several DEGs associated with muscle function and mobility were up-regulated. Our study sheds light on how a single mutation in a gene can modulate multiple phenotypes by rewiring gene regulation networks. The research also provides valuable insights into the complex genetic mechanisms underlying the regulation of diverse phenotypic traits by a single gene.