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Characterization of Na, K-ATPase genes in Atlantic salmon (Salmo salar) and comparative genomic organization with rainbow trout (Oncorhynchus mykiss)

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Abstract

A combination of molecular and in silico approaches was employed to assemble a survey of Na, K-ATPase genes contained in the ancestrally tetraploid genome of the Atlantic salmon (Salmo salar). Molecular characterization of genomic clones coding for the α subunit revealed two single genes (α1a and α2) and two pairs of presumably homeologous genes (α1b/i-ii and α1c/i-ii). Each of the six genes showed high sequence similarity to isoforms previously isolated from rainbow trout and extensive structural differences relative to putative orthologs in the human genome. In silico analysis of expressed sequence tag (EST) collections indicated that at least five α (α1a, α1b, α1c, α2, and α3) and four β (β1a, β1b, β2, and β3b) subunit isoforms are expressed in Atlantic salmon. Meiotic linkage analysis further showed that Na, K-ATPase genes are dispersed throughout the salmon genome, with the exception of two multigene clusters on linkage groups AS-22 and AS-28. Duplicate gene copies for the isoform α1b were assigned to linkage groups with multiple homeologous anchors (AS-22 and AS-23), while β2 duplicates suggested a new homeologous affinity between AS-05 and AS-28. In addition, the comparison of linkage arrangements with rainbow trout also showed that the genomic organization of Na, K-ATPase genes is consistent with the evolutionary conservation of syntenic chromosome regions between these species.

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References

  • Allendorf FW, Thorgaard GH (1984) Tetraploidy and the evolution of salmonid fishes. In: Turner BJ ed Evolutionary genetics of fishes. Plenum Press, New York, pp1–53

    Google Scholar 

  • Allendorf FW, Seeb JE, Knudsen KL, Thorgaard GH, Leary RF (1986) Gene-centromere mapping of 25 loci in rainbow trout. J Hered 77:307–312

    Google Scholar 

  • Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search program. Nucleic Acids Res 25:3389–3402

    Article  CAS  PubMed  Google Scholar 

  • Bardakci F, Skibinski DOF (1994) Application of the RAPD technique in tilapia fish: species and subspecies identification. Heredity 73:117–123

    CAS  PubMed  Google Scholar 

  • Blanco G, Mercer RW (1998) Isozymes of the Na-K-ATPase: heterogeneity in structure, diversity in function. Am J Physiol 275:F633–F650

    CAS  PubMed  Google Scholar 

  • Blasiole B, Canfield V, Degrave A, Thisse C, Thisse B, Rajarao J, Levenson R (2002) Cloning, mapping, and developmental expression of a sixth zebrafish Na,K-ATPase alpha1 subunit gene (atp1a1a.5). Gene Expr Patterns 2:243–246

    Article  CAS  PubMed  Google Scholar 

  • Brendel V, Xing L, Zhu W (2004) Gene structure prediction from consensus spliced alignment of multiple ESTs matching the same genomic locus. Bioinformatics 20:1157–1169

    Article  CAS  PubMed  Google Scholar 

  • D’Cotta H, Valotaire C, Le Gac F, Prunet P (2000) Synthesis of gill Na+-K+-ATPase in Atlantic salmon smolts: differences in α-mRNA and α-protein levels. Am J Physiol 278:R101–R110

    CAS  Google Scholar 

  • Delalande JM, Rescan PY (1999) Differential expression of two nonallelic MyoD genes in developing and adult myotomal musculature of the trout (Oncorhynchus mykiss). Dev Genes Evol 209:432–437

    Article  CAS  PubMed  Google Scholar 

  • Gharbi K, Semple JW, Ferguson MM, Schulte PM, Danzmann RG (2004) Linkage arrangement of Na, K-ATPase genes in the tetraploid-derived genome of the rainbow trout (Oncorhynchus mykiss). Anim Genet 35:321–325

    Article  CAS  PubMed  Google Scholar 

  • Guyomard R (1986) Gene segregation in gynogenetic brown trout (Salmo trutta L.): systematically high frequencies of post-reduction. Genet Sel Evol 18:385–392

    Google Scholar 

  • Hartley SE (1987) The chromosomes of salmonid fishes. Biol Rev 62:197–214

    Article  Google Scholar 

  • Henikoff S, Henikoff JG (1992) Amino acid substitution matrices from protein blocks. Proc Natl Acad Sci USA 89:10915–10909

    CAS  PubMed  Google Scholar 

  • Hoar WC (1988) The physiology of smolting salmonids. In: Hoar WS, Randall DJ eds Fish physiology, vol 11B. Academic Press, London, pp275–343

  • Jackson TR, Ferguson MM, Danzmann RG, Fishback AG, Ihssen PE, O’Connell, Crease TJ (1998) Identification of two QTL influencing upper temperature tolerance in three rainbow trout (Oncorhynchus mykiss) half-sib families. Heredity 80:143–151

    Article  Google Scholar 

  • Johnson KR, Wright JE Jr, May B (1987) Linkage relationships reflecting ancestral tetraploidy in salmonid fish. Genetics 116:579–591

    CAS  PubMed  Google Scholar 

  • Marshall WS (2002) Na+, Cl-, Ca2+ and Zn2+ transport by fish gills: retrospective review and prospective synthesis. J Exp Biol 293:264–283

    CAS  Google Scholar 

  • Mobasheri A, Avila J, Cozar-Castellano I, Brownleader MD, Trevan M, Francis MJ, Lamb JF, Martin-Vasallo P (2000) Na+, K+-ATPase isozyme diversity: comparative biochemistry and physiological implications of novel functional interactions. Biosci Rep 20:51–91

    Article  CAS  PubMed  Google Scholar 

  • Nichols KM, et al (2003) A consolidated linkage map for rainbow trout (Oncorhynchus mykiss). Anim Genet 34:102–115

    Article  CAS  PubMed  Google Scholar 

  • Pressley TA (1992) Phylogenetic conservation of isoform-specific regions within alpha-subunit of Na(+)-K(+)-ATPase. Am J Physiol 262:C743–C751

    CAS  PubMed  Google Scholar 

  • Quackenbush J, Cho J, Lee D, Liang F, Holt I, Karamycheva S, Parvizi B, Pertea G, Sultana R, White J (2001) The TIGR Gene Indices: analysis of gene transcript sequences in highly sampled eukaryotic species. Nucleic Acids Res 29:159–164

    Article  CAS  PubMed  Google Scholar 

  • Rajarao SJ, Canfield VA, Mohideen MA, Yan YL, Postlethwait JH, Cheng KC, Levenson R (2001) The repertoire of Na,K-ATPase alpha and beta subunit genes expressed in the zebrafish, Danio rerio. Genome Res 11:1211–1220

    Article  CAS  PubMed  Google Scholar 

  • Rescan PY, Jutel I, Ralliere C (2001) Two myostatin genes are differentially expressed in myotomal muscles of the trout (Oncorhynchus mykiss). J Exp Biol 204:3523–3529

    CAS  PubMed  Google Scholar 

  • Richards JG, Semple JW, Bystriansky J, Schulte PM (2003) Na+/K+ ATPase α isoform switching in gills of rainbow trout (Oncorhynchus mykiss) during salinity transfer. J Exp Biol 206:4475–4486

    Article  CAS  PubMed  Google Scholar 

  • Sakamoto T, Danzmann RG, Gharbi K, Howard P, Ozaki A, Khoo SK, Woram RA, Okamoto N, Ferguson MM, Holm L-E, Guyomard R, Hoyheim B (2000) A microsatellite linkage map of rainbow trout (Oncorhynchus mykiss) characterized by large sex-specific differences in recombination rates. Genetics 155:1331–1345

    CAS  PubMed  Google Scholar 

  • Seidelin M, Madsen SS, Cutler CP, Cramb G (2001) Expression of gill vacuolar-type H+-ATPase B subunit, and Na+, K+-ATPase α1 and β1 subunit messenger RNAs in smolting Salmo salar. Zool Sci 18:315–324

    Article  CAS  Google Scholar 

  • Serluca FC, Sidow A, Mably JD, Fishman MC (2001) Partitioning of tissue expression accompanies multiple duplications of the Na+/K+ ATPase α subunit gene. Genome Res 11:1625–1631

    Article  CAS  PubMed  Google Scholar 

  • Singer TD, Clements KM, Semple JW, Schulte PM, Brystriansky JS, Finstad B, Fleming IA, McKinley RS (2002) Seawater tolerance and gene expression in two strains of Atlantic salmon smolts. Can J Fish Aquat Sci 59:125–135

    Article  CAS  Google Scholar 

  • Therien AG, Blostein R (2000) Mechanisms of sodium pump regulation. Am J Physiol Cell Physiol 279:C541–C566

    CAS  PubMed  Google Scholar 

  • Voorrips RE (2002) Mapchart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78

    Article  CAS  PubMed  Google Scholar 

  • Woram RA, et al (2003) Comparative genome analysis of the primary sex-determining locus in salmonid fishes. Genome Res 13:272–280

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors thank Patricia Schulte and Jeff Semple for sharing data prior to publication, Dan Lee for assistance with the Atlantic salmon Gene Index, and Xia Yue for technical support in the laboratory. Atlantic salmon DNA samples were kindly provided by John Taggart as part of the SALMAP collaboration. This work was funded by AquaNet, the Canadian Network of Centres of Excellence for Aquaculture (Project AP10) and the Natural Sciences and Engineering Research Council of Canada (Strategic Projects).

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Correspondence to Roy G. Danzmann.

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Communicated by G. Georgiev

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Gharbi, K., Ferguson, M.M. & Danzmann, R.G. Characterization of Na, K-ATPase genes in Atlantic salmon (Salmo salar) and comparative genomic organization with rainbow trout (Oncorhynchus mykiss). Mol Genet Genomics 273, 474–483 (2005). https://doi.org/10.1007/s00438-005-1135-8

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  • DOI: https://doi.org/10.1007/s00438-005-1135-8

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