Evolution of duplicated IgH loci in Atlantic salmon, Salmo salar

Abstract

BackgroundThe Atlantic salmon (Salmo salar) immunoglobulin heavy chain (IgH) locus possesses two parallel IgH isoloci (IGH-A and IGH-B), that are related to the genomic duplication event in the family Salmonidae. These duplicated IgH loci in Atlantic salmon provide a unique opportunity to examine the mechanisms of genome diversity and genome evolution of the IgH loci in vertebrates. In this study, we defined the structure of these loci in Atlantic salmon, and sequenced 24 bacterial artificial chromosome (BAC) clones that were assembled into the IGH-A (1.1 Mb) and IGH-B (0.9 Mb) loci. In addition, over 7,000 cDNA clones from the IgH variable (VH) region have been sequenced and analyzed.ResultsThe present study shows that the genomic organization of the duplicated IgH loci in Atlantic salmon differs from that in other teleosts and other vertebrates. The loci possess multiple Cτ genes upstream of the Cμ region, with three of the Cτ genes being functional. Moreover, the duplicated loci possess over 300 VH segments which could be classified into 18 families. This is the largest number of VH families currently defined in any vertebrate. There were significant structural differences between the two loci, indicating that both IGH-A and -B loci have evolved independently in the short time after the recent genome duplication approximately 60 mya.ConclusionsOur results indicate that the duplication of the IgH loci in Atlantic salmon significantly contributes to the increased diversity of the antibody repertoire, as compared with the single IgH locus in other vertebrates.

Unique Features of Fish Immune Repertoires: Particularities of Adaptive Immunity Within the Largest Group of Vertebrates

“…The structure of TCR and Ig loci resembles the one found in mammals, rather than the one of Chondrichthyans: TCR beta and alpha/delta as well as IgH loci are organized as translocons while IgL and TCR gamma are made of multiple clusters. An important feature of fish Ig loci is the very large number of VH gene segments found in many species, especially in salmonids (Yasuike et al 2010). Additionally, as bony fish underwent one or several additional genome-wide duplications (Petit et al 2004) compared to most tetrapod species, the number of loci has increased.…”

“…Additionally, as bony fish underwent one or several additional genome-wide duplications (Petit et al 2004) compared to most tetrapod species, the number of loci has increased. Thus, Salmo salar (Yasuike et al 2010), Oncorhynchus mykiss (Hansen et al 2005), Oryzias latipes (Magadán-Mompó et al 2011), and Gasterosteus aculeatus (Bao et al 2010; Gambón-Deza et al 2010) present more than one functional IgH locus per haplotype. Thus, as Chondrichthyans, polyploid Xenopus , and genetically manipulated models with multiple IgH loci such as mice triallelic for IgH, the clonality of the system in bony fish requires not only allelic exclusion but also locus exclusion (Du Pasquier and Hsu 1983; Barreto et al 2001).…”

Discovery and Characterization of Secretory IgD in Rainbow Trout: Secretory IgD Is Produced through a Novel Splicing Mechanism

“…Teleosts demonstrate remarkable plasticity in their d genomic arrangement, with many species possessing repeated blocks of exons encoding Cd2-4 (up to four repeats have been described) as well as duplicated d loci (3)(4)(5). In Atlantic salmon (Salmo salar), a salmon-specific genome duplication event (IGH-A and IGH-B) resulted in parallel d loci that have diverged from each other, resulting in an additional d2-4 repeat in the IGH-B locus (6). In channel catfish (Ictalurus punctatus), there are two functional copies of the d gene (7) on the same IGH locus.…”

Characterization of the Atlantic salmon (Salmo salar) brain-type fatty acid binding protein (fabp7) genes reveals the fates of teleost fabp7 genes following whole genome duplications

“…The fate of gene duplicates in a duplicated genome has been a lingering question in biology. Several studies have examined the evolution of duplicated genes in salmonids (e.g., Hansson and Hahn, 2008;Koop et al, 2008;Lai et al, 2009;Leong et al, 2010;Lukacs et al, 2007;McKay et al, 2004;Moghadam et al, 2005;Ostbye et al, 2007;Quinn et al, 2010;Yasuike et al, 2010). We are characterizing the structure, genome organization and expression patterns of members of the ilbp gene family in Atlantic salmon (S. salar) and other teleosts as this system can provide insight into the evolution and fates of genes that have experienced at least two rounds WGD.…”