Quinn NL et al. (2010), Genomic organization and evolution of the Atlan...

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BMC Genomics 2010 Oct 05;11:539. doi: 10.1186/1471-2164-11-539.

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Genomic organization and evolution of the Atlantic salmon hemoglobin repertoire.

Quinn NL , Boroevich KA , Lubieniecki KP , Chow W , Davidson EA , Phillips RB , Koop BF , Davidson WS .

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BACKGROUND: The genomes of salmonids are considered pseudo-tetraploid undergoing reversion to a stable diploid state. Given the genome duplication and extensive biological data available for salmonids, they are excellent model organisms for studying comparative genomics, evolutionary processes, fates of duplicated genes and the genetic and physiological processes associated with complex behavioral phenotypes. The evolution of the tetrapod hemoglobin genes is well studied; however, little is known about the genomic organization and evolution of teleost hemoglobin genes, particularly those of salmonids. The Atlantic salmon serves as a representative salmonid species for genomics studies. Given the well documented role of hemoglobin in adaptation to varied environmental conditions as well as its use as a model protein for evolutionary analyses, an understanding of the genomic structure and organization of the Atlantic salmon α and β hemoglobin genes is of great interest. RESULTS: We identified four bacterial artificial chromosomes (BACs) comprising two hemoglobin gene clusters spanning the entire α and β hemoglobin gene repertoire of the Atlantic salmon genome. Their chromosomal locations were established using fluorescence in situ hybridization (FISH) analysis and linkage mapping, demonstrating that the two clusters are located on separate chromosomes. The BACs were sequenced and assembled into scaffolds, which were annotated for putatively functional and pseudogenized hemoglobin-like genes. This revealed that the tail-to-tail organization and alternating pattern of the α and β hemoglobin genes are well conserved in both clusters, as well as that the Atlantic salmon genome houses substantially more hemoglobin genes, including non-Bohr β globin genes, than the genomes of other teleosts that have been sequenced. CONCLUSIONS: We suggest that the most parsimonious evolutionary path leading to the present organization of the Atlantic salmon hemoglobin genes involves the loss of a single hemoglobin gene cluster after the whole genome duplication (WGD) at the base of the teleost radiation but prior to the salmonid-specific WGD, which then produced the duplicated copies seen today. We also propose that the relatively high number of hemoglobin genes as well as the presence of non-Bohr β hemoglobin genes may be due to the dynamic life history of salmon and the diverse environmental conditions that the species encounters.Data deposition: BACs S0155C07 and S0079J05 (fps135): GenBank GQ898924; BACs S0055H05 and S0014B03 (fps1046): GenBank GQ898925.

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Species referenced: Xenopus
Genes referenced: fes sp6

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	Figure 1. Genomic organization of the Atlantic salmon hemoglobin gene clusters. A) Schematic representation of the region of Atlantic salmon chromosome 6 containing the hemoglobin genes. Sequence reads for this region assembled into one solid sequence contig (ctg 41). B) Schematic representation of the region of Atlantic salmon chromosome 3 containing the hemoglobin genes. Sequence contigs are indicated by horizontal green lines. Î² hemoglobin genes are indicated in blue; Î± hemoglobin genes are indicated in red. Arrows indicate strand of transcription. All hemoglobin gene names begin with SsaChr6 or SsaChr3 for chromosome 6 and chromosome 3, respectively, followed by Î± or Î² and a number indicating the order of the genes. SP6 and T7 ends of overlapping BACs are indicated by grey arrows. Thus, the regions between the arrows indicate BAC overlapping regions. bN: Non-Bohr Î² hemoglobins.
	Figure 2. Merged female linkage maps for Atlantic salmon SALMAP families Br5 and Br6 showing linkage groups 4 and 11. Microsatellite marker Ssa10067BSFU (underlined), representing fps1046 was informative in both the Altantic salmon SALMAP families (Br5 and Br6) and mapped to linkage group 4. Microsatellite Ssa0516BSFU (underlined) was informative in the Br6 family and mapped to linkage group 11.
	Figure 3. Comparative synteny of hemoglobin gene clusters among sequenced teleost species. Schematic representation of annotated genes within the regions surrounding the hemoglobin gene clusters for Atlantic salmon and four annotated teleost genomes (O. latipes, D. rerio, G. aculeatus, T. nigroviridis). Colored blocks indicate shared or common genes as specified in the Figure legend. Black blocks indicate genes that are not shared within the indicated regions of any other species. Distances between genes vary (i.e., figure is not to scale); the start and end of the chromsome/group region is shown in base pairs (bp) for each of the annotated teleost genomes. Solid lines between predicted genes indicate that the order and orientation of the predicted gene relative to those neighboring it is known, whereas for Atlantic salmon fps 135 (chromosome 3), a single black dot between predicted genes indicates that the relative location of the predicted genes compared to those joined by solid lines is known, but their order and orientation (i.e., that of the sequence contigs on which they reside) relative to one another is not. Arrows indicate the direction of transcription of the gene relative to the location of the hemoglobin gene cluster; lack of an arrow indicates that the relative direction of transcription cannot be determined. For D. rerio chromsome 3, the gene for ELAV-like protein was found distantly downstream of the nearest common gene (Arylakylamine N-acetyltransferase 2), as indicated by the distance shown, with numerous predicted genes in between.
	Figure 4. Phylogenetic tree of teleost and Xenopus tropicalis Î± hemoglobins. The Î± hemoglobin cDNAs (exclusive of untranslated regions) annotated within the Ensembl 54 database for medaka, zebrafish, tetraodon, stickleback and X. tropicalis, as well as those identified in Atlantic salmon here and the hemoglobin genes identified as embryonic within rainbow trout [28] were independently aligned using EBioX [70]. Phylogenetic trees were constructed using the a Bayesian approach with (5 runs, 100,000 generations, 40% burn-in period) within the TOPALi V.2 software package [71] running the MrBayes program [72] under the best selected model (SYM). For simplicity, as well as to clearly indicate the source chromosome of the gene, the teleostean hemoglobin genes were named using the same system used to name those of Atlantic salmon. That is, an abbreviated three letter (genus species) name followed by chromosome/linkage group name followed by Î± or Î² followed by a number indicating the sequential order of the genes from 5' to 3' as defined by Ensembl (Additional file 4, Table S3). Hemoglobin genes that were previously identified via expression analysis as being expressed exclusively during embryogenesis, and that are identified as embryonic within the Ensembl 54 database are denoted with "emb" following the assigned gene name. Branch numbers indicate posterior probabilities.
	Figure 5. Phylogenetic tree of teleost and Xenopus tropicalis Î² hemoglobins. The Î² hemoglobin cDNAs (exclusive of untranslated regions) annotated within the Ensembl 54 database for medaka, zebrafish, tetraodon, stickleback and X. tropicalis, as well as those identified in Atlantic salmon here and the hemoglobin genes identified as embryonic within rainbow trout [28] were independently aligned using EBioX [70]. Phylogenetic trees were constructed using the a Bayesian approach with (5 runs, 100,000 generations, 40% burn-in period) within the TOPALi V.2 software package [71] running the MrBayes program [72] under the best selected model (SYM). For simplicity, as well as to clearly indicate the source chromosome of the gene, the teleostean hemoglobin genes were named using the same system used to name those of Atlantic salmon. That is, an abbreviated three letter (genus species) name followed by chromosome/linkage group name followed by Î± or Î² followed by a number indicating the sequential order of the genes from 5' to 3' as defined by Ensembl (Additional file 4, Table S3). Hemoglobin genes that were previously identified via expression analysis as being expressed exclusively during embryogenesis, and that are identified as embryonic within the Ensembl 54 database are denoted with "emb" following the assigned gene name. Branch numbers indicate posterior probabilities.
	Figure 6. Schematic representation of the evolution of teleostean hemoglobin gene clusters. Whole genome duplication (WGD) events are indicated by grey diamonds. The two hemoglobin gene clusters resulting from the teleost WGD are represented as (1) and (2) for Cluster 1 and Cluster 2, respectively (see text). Loss of a hemoglobin gene cluster by excision is indicated by a diagonal slash across that cluster. Although the genome sequence is available for the pufferfish, T. rubripes, the fugu genome was not included in this analysis because the published hemoglobin arrangement of two hemoglobin gene clusters, one containing only Î± hemoglobin genes and one containing both Î± and Î² hemoglobin genes [15] did not agree with the annotation results of the latest fugu genome assembly reported within the Ensembl database.

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