Genomic arrangement of salinity tolerance QTLs in salmonids: A comparative analysis of Atlantic salmon (Salmo salar) with Arctic charr (Salvelinus alpinus) and rainbow trout (Oncorhynchus mykiss)

Abstract

BackgroundQuantitative trait locus (QTL) studies show that variation in salinity tolerance in Arctic charr and rainbow trout has a genetic basis, even though both these species have low to moderate salinity tolerance capacities. QTL were observed to localize to homologous linkage group segments within putative chromosomal regions possessing multiple candidate genes. We compared salinity tolerance QTL in rainbow trout and Arctic charr to those detected in a higher salinity tolerant species, Atlantic salmon. The highly derived karyotype of Atlantic salmon allows for the assessment of whether disparity in salinity tolerance in salmonids is associated with differences in genetic architecture. To facilitate these comparisons, we examined the genomic synteny patterns of key candidate genes in the other model teleost fishes that have experienced three whole-genome duplication (3R) events which preceded a fourth (4R) whole genome duplication event common to all salmonid species.ResultsNine linkage groups contained chromosome-wide significant QTL (AS-2, -4p, -4q, -5, -9, -12p, -12q, -14q -17q, -22, and −23), while a single genome-wide significant QTL was located on AS-4q. Salmonid genomes shared the greatest marker homology with the genome of three-spined stickleback. All linkage group arms in Atlantic salmon were syntenic with at least one stickleback chromosome, while 18 arms had multiple affinities. Arm fusions in Atlantic salmon were often between multiple regions bearing salinity tolerance QTL. Nine linkage groups in Arctic charr and six linkage group arms in rainbow trout currently have no synteny alignments with stickleback chromosomes, while eight rainbow trout linkage group arms were syntenic with multiple stickleback chromosomes. Rearrangements in the stickleback lineage involving fusions of ancestral arm segments could account for the 21 chromosome pairs observed in the stickleback karyotype.ConclusionsSalinity tolerance in salmonids from three genera is to some extent controlled by the same loci. Synteny between QTL in salmonids and candidate genes in stickleback suggests genetic variation at candidate gene loci could affect salinity tolerance in all three salmonids investigated. Candidate genes often occur in pairs on chromosomes, and synteny patterns indicate these pairs are generally conserved in 2R, 3R, and 4R genomes. Synteny maps also suggest that the Atlantic salmon genome contains three larger syntenic combinations of candidate genes that are not evident in any of the other 2R, 3R, or 4R genomes examined. These larger synteny tracts appear to have resulted from ancestral arm fusions that occurred in the Atlantic salmon ancestor. We hypothesize that the superior hypo-osmoregulatory efficiency that is characteristic of Atlantic salmon may be related to these clusters.

An integrated transcriptomic and comparative genomic analysis of differential gene expression in Arctic charr (Salvelinus alpinus) following seawater exposure

“…For instance, candidate genes in salmonids show evidence of clustering along linkage groups (Norman et al, 2012) and similar patterns are evident on model teleost chromosomes (e.g. medaka, stickleback, zebrafish) (Norman et al, 2012) and on reconstructed proto-actinopterygian ancestral chromosomes (Kasahara et al, 2007). Current data indicate that interchromosomal rearrangements in the Atlantic salmon genome have produced unique combinations of salinity tolerance candidate genes, which may be related to the high salinity tolerance capacity that is characteristic of this species (Norman et al, 2012).…”

“…Clustered genes in vertebrates are more likely to be co-expressed (Hurst et al, 2004;Ng et al, 2009;Woo et al, 2010) and co-methylated (McGowan et al, 2011) and thus are more likely to be involved in the same or closely related biological pathways. For instance, candidate genes in salmonids show evidence of clustering along linkage groups (Norman et al, 2012) and similar patterns are evident on model teleost chromosomes (e.g. medaka, stickleback, zebrafish) (Norman et al, 2012) and on reconstructed proto-actinopterygian ancestral chromosomes (Kasahara et al, 2007).…”

“…medaka, stickleback, zebrafish) (Norman et al, 2012) and on reconstructed proto-actinopterygian ancestral chromosomes (Kasahara et al, 2007). Current data indicate that interchromosomal rearrangements in the Atlantic salmon genome have produced unique combinations of salinity tolerance candidate genes, which may be related to the high salinity tolerance capacity that is characteristic of this species (Norman et al, 2012). However, these observations are based on relatively few candidate genes.…”

“…Within species, quantitative trait locus (i.e. QTL) studies indicate that variation has a genetic basis (Le Bras et al, 2011;Norman et al, 2011;Norman et al, 2012). Genes differentially regulated in Arctic charr (Salvelinus alpinus) with contrasting salinity tolerance capacities have been identified using large-scale gene expression analysis on gill tissue.…”

Genetic and genomic analyses for economically important traits and their applications in molecular breeding of cultured fish

“…Sun et al [76] located a cold resistance locus on common carp LG5. Rengmark et al [77] reported a high salinity-tolerance gene, while Norman et al [78] compared QTLs for salinity tolerance among the salmonid genomes and found that the QTLs were distributed on nine different LGs.…”