Gene gain and loss drive the diversification of gig immune genes in teleosts: structural and regulatory insights from Atlantic salmon.

Abstract

Interferon-stimulated genes (ISGs) are key players in vertebrate antiviral immunity. Among teleost ISGs, the grass carp reovirus-induced gene (gig) families 1 and 2 (gig1 and gig2, respectively) are absent in mammals but conserved in fish and amphibians, and they have been implicated in resistance to viral infections across several aquaculture species. In particular, gig1 and gig2 genes are transcriptionally induced by viral stimuli in teleosts such as zebrafish, grass carp, and salmonids, and recent studies have highlighted their potential involvement in resistance to economically important diseases like pancreas disease in Atlantic salmon. Yet, the rapid evolution of these genes hinders a comprehensive understanding of their diversification process and regulatory mechanisms. The present study investigated gig gene evolution across teleosts, with a focus on Atlantic salmon (Salmo salar). Phylogenetic analysis across representative ray-finned fishes (Actinopterygii), including both teleost species as well as non-teleost outgroups such as the spotted gar (Holostei), indicated that gig1 is restricted to teleosts, with no identifiable homologs in non-teleost lineages. In contrast, gig2 genes are present in both teleosts and the spotted gar, suggesting an origin prior to the teleost-specific whole genome duplication (Ts3R), likely in early non-amniote vertebrates. Comparison of gig gene expansion across species revealed that multiple whole-genome duplication events drove lineage-specific expansions, particularly of gig2 in salmonids. Structural and transcriptomic analyses of Atlantic salmon gigs showed that the two gene families differ in domain composition, repeat content, and regulation. Our findings underscore the complex interplay of duplication history, structural divergence, and transcriptional regulation in shaping immune gene repertoires in teleosts, with implications for understanding host-pathogen interactions and aquaculture disease responses.