Abstract
BackgroundThe two homologous iron-binding lobes of transferrins are thought to have evolved by gene duplication of an ancestral monolobal form, but any conserved synteny between bilobal and monolobal transferrin loci remains unexplored. The important role played by transferrin in the resistance to invading pathogens makes this polymorphic gene a highly valuable candidate for studying adaptive divergence among local populations.ResultsThe Atlantic cod genome was shown to harbour two tandem duplicated serum transferrin genes (Tf1, Tf2), a melanotransferrin gene (MTf), and a monolobal transferrin gene (Omp). Whereas Tf1 and Tf2 were differentially expressed in liver and brain, the Omp transcript was restricted to the otoliths. Fish, chicken and mammals showed highly conserved syntenic regions in which monolobal and bilobal transferrins reside, but contrasting with tetrapods, the fish transferrin genes are positioned on three different linkage groups. Sequence alignment of cod Tf1 cDNAs from Northeast (NE) and Northwest (NW) Atlantic populations revealed 22 single nucleotide polymorphisms (SNP) causing the replacement of 16 amino acids, including eight surface residues revealed by the modelled 3D-structures, that might influence the binding of pathogens for removal of iron. SNP analysis of a total of 375 individuals from 14 trans-Atlantic populations showed that the Tf1-NE variant was almost fixed in the Baltic cod and predominated in the other NE Atlantic populations, whereas the NW Atlantic populations were more heterozygous and showed high frequencies of the Tf-NW SNP alleles.ConclusionsThe highly conserved synteny between fish and tetrapod transferrin loci infers that the fusion of tandem duplicated Omp-like genes gave rise to the modern transferrins. The multiple nonsynonymous substitutions in cod Tf1 with putative structural effects, together with highly divergent allele frequencies among different cod populations, strongly suggest evidence for positive selection and local adaptation in trans-Atlantic cod populations.
Highlights
The two homologous iron-binding lobes of transferrins are thought to have evolved by gene duplication of an ancestral monolobal form, but any conserved synteny between bilobal and monolobal transferrin loci remains unexplored
The allelic variant of cod Tf1 identified in the two Northeast Atlantic populations was named Tf1-NE
The identification of four transferrin genes in the Atlantic cod genome adds novel information to our knowledge about the evolution of the transferrin gene family by documenting 1) the expression of tandem duplicated transferrin genes, 2) presence of both bilobal and monolobal transferrin forms in the fish genome, 3) highly conserved synteny between fish monolobal and tetrapod bilobal transferrin loci, and 4) evidence of positive selection acting on a tandem duplicated transferrin gene in trans-Atlantic cod populations
Summary
The two homologous iron-binding lobes of transferrins are thought to have evolved by gene duplication of an ancestral monolobal form, but any conserved synteny between bilobal and monolobal transferrin loci remains unexplored. The important role played by transferrin in the resistance to invading pathogens makes this polymorphic gene a highly valuable candidate for studying adaptive divergence among local populations. The latter study provided evidence for local adaptation in cod populations by identifying molecular mechanisms underlying the different oxygen binding properties of the cod hemoglobins in temperate and Arctic waters. An alternative strategy for identifying adaptive population divergence is to scan transcriptome databases, or the whole genome when available, for polymorphic loci to be analysed in different populations [5]. Evidence of directional selection in Atlantic cod was provided by genotyping multiple gene-associated single nucleotide polymorphisms (SNPs) in Northeast and Northwest Atlantic populations [12,13,14]. Documentation of molecular changes underlying adaptive traits requires additional information about the specific genes involved and the regulatory or structural implications of the identified mutations
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