The genetic basis of salinity tolerance traits in Arctic charr (Salvelinus alpinus)

BMC Genetics

Volumn 12, Issue , 2011, Pages

  Norman, Joseph D ^a   Danzmann, Roy G ^a   Glebe, Brian ^b   Ferguson, Moira M ^a  

^a UNIVERSITY OF GUELPH   (Canada)

^b ST ANDREWS BIOLOGICAL STATION   (Canada)

Author keywords

Arctic charr; Duplicated genes; Na+ k+ atpase; Osmoregulation; Salinity tolerance; Salmonid fishes; Whole genome duplications; homeologies

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); FRESH WATER; MESSENGER RNA; SEA WATER; SODIUM ION;

ANIMAL EXPERIMENT; ARCTIC CHARR; ARTICLE; BODY SIZE; GENE DUPLICATION; GENETIC LINKAGE; GENOME; GENOMICS; GROWTH RATE; NONHUMAN; NUCLEOTIDE SEQUENCE; OSMOREGULATION; PLASMA OSMOLALITY; QUANTITATIVE TRAIT LOCUS; SALINITY; SALMONID; SALVELINUS ALPINUS; WHOLE GENOME DUPLICATION; ANIMAL; BODY WEIGHT; CHROMOSOME MAP; DNA SEQUENCE; ELECTROLYTE BALANCE; GENETICS; HOMEOSTASIS; ION TRANSPORT; PHENOTYPE; PHYSIOLOGY; SALT TOLERANCE; TROUT;

ONCORHYNCHUS MYKISS; PISCES; SALMONIDAE; SALVELINUS ALPINUS; SALVELINUS FONTINALIS; TELEOSTEI;

ANIMALS; BASE SEQUENCE; BODY WEIGHT; CHROMOSOME MAPPING; FRESH WATER; GENETIC LINKAGE; GENOME; HOMEOSTASIS; ION TRANSPORT; PHENOTYPE; QUANTITATIVE TRAIT LOCI; SALINITY; SALT-TOLERANCE; SEAWATER; SEQUENCE ANALYSIS, DNA; TROUT; WATER-ELECTROLYTE BALANCE;

EID: 80053172179     PISSN: None     EISSN: 14712156     Source Type: Journal    
DOI: 10.1186/1471-2156-12-81     Document Type: Article

References (56)

1. Marshall W, Grosell M. Ion transport, osmoregulation, and acid-base balance. The physiology of fishes 2006, 177-230. Boca Raton, FL: CRC Press, Evans D, Claiborne J, 3.
2. Silva P, Solomon R, Spokes K, Epstein F. Ouabain inhibition of gill Na-K-ATPase: relationship to active chloride transport. J Exp Zool 1977, 199:419-426. 10.1002/jez.1401990316, 139454.
3. Furuse M, Furuse K, Sasaki H, Tsukita S. Conversion of Zonulae occludentes from tight to leaky strand type by introducing claudin-2 into Madin-Darby canine kidney I cells. J Cell Biol 2001, 153(2):263-272. 10.1083/jcb.153.2.263, 2169456, 11309408.
4. Tipsmark CK, Kiilerich P, Nilsen TO, Ebbesson LOE, Stefansson SO, Madsen SS. Branchial expression patterns of claudin isoforms in Atlantic salmon during seawater acclimation and smoltification. Am J Physiol-Reg I 2008, 294(5):R1563-R1574.
5. Van Itallie CM, Rogan S, Yu A, Vidal LS, Holmes J, Anderson JM. Two splice variants of claudin-10 in the kidney create paracellular pores with different ion selectivities. Am J Physiol-Renal 2006, 291(6):F1288-F1299.
6. Richards JG, Semple JW, Bystriansky JS, Schulte PM. Na+/K+-ATPase (alpha-isoform switching in gills of rainbow trout (Oncorhynchus mykiss) during salinity transfer. J Exp Biol 2003, 206(24):4475-4486. 10.1242/jeb.00701, 14610032.
7. Bystriansky JS, Richards JG, Schulte PM, Ballantyne JS. Reciprocal expression of gill Na+/K+-ATPase alpha-subunit isoforms alpha 1a and alpha 1b during seawater acclimation of three salmonid fishes that vary in their salinity tolerance. J Exp Biol 2006, 209(10):1848-1858. 10.1242/jeb.02188, 16651551.
8. Mackie P, Wright PA, Glebe BD, Ballantyne JS. Osmoregulation and gene expression of Na+/K+ ATPase in families of Atlantic salmon (Salmo salar) smolts. Can J Fish Aqua Sci 2005, 62(11):2661-2672.
9. McCormick SD, Regish AM, Christensen AK. Distinct freshwater and seawater isoforms of Na(+)/K(+)-ATPase in gill chloride cells of Atlantic salmon. J Exp Biol 2009, 212(24):3994-4001. 10.1242/jeb.037275, 19946077.
10. Larsen PF, Nielsen EE, Koed A, Thomsen DS, Olsvik PA, Loeschcke V. Interpopulation differences in expression of candidate genes for salinity tolerance in winter migrating anadromous brown trout (Salmo trutta L.). BMC Genet 2008, 9:12. 2254441, 18230136.
11. Schmitz M. Seasonal-changes in hypoosmoregulatory ability in landlocked and anadromous populations of Arctic charr, Salvelinus alpinus, and Atlantic salmon, Salmo salar. Environ Biol Fish 1995, 42(4):401-412.
12. Singer TD, Clements KM, Semple JW, Schulte PM, Bystriansky JS, Finstad B, Fleming IA, McKinley RS. Seawater tolerance and gene expression in two strains of Atlantic salmon smolts. Can J Fish Aquat Sci 2002, 59(1):125-135.
13. Shrimpton JM, Patterson DA, Richards JG, Cooke SJ, Schulte PM, Hinch SG, Farrell AP. Ionoregulatory changes in different populations of maturing sockeye salmon Oncorhynchus nerka during ocean and river migration. J Exp Biol 2005, 208(21):4069-4078. 10.1242/jeb.01871, 16244166.
14. Nilsen TO, Ebbesson LOE, Madsen SS, McCormick SD, Andersson E, Bjornsson BT, Prunet P, Stefansson SO. Differential expression of gill Na+,K+-ATPase alpha- and beta-subunits, Na+,K+,2Cl(-) cotransporter and CFTR anion channel in juvenile anadromous and landlocked Atlantic salmon Salmo salar. J Exp Biol 2007, 210(16):2885-2896. 10.1242/jeb.002873, 17690237.
15. Hoar W. The physiology of smolting salmonids. Fish Physiology 1988, XIV:275-343. New York: Academic Press, Hoar W, Randall D.
16. Hiroi J, McCormick SD. Variation in salinity tolerance, gill Na+/K+-ATPase, Na+/K+/2Cl(-) cotransporter and mitochondria-rich cell distribution in three salmonids Salvelinus namaycush, Salvelinus fontinalis and Salmo salar. J Exp Biol 2007, 210(6):1015-1024. 10.1242/jeb.002030, 17337714.
17. Delabbio JL, Glebe BD, Sreedharan A. Variation in growth and survival between 2 anadromous strains of Canadian Arctic charr (Salvelinus alpinus) during long-term saltwater rearing. Aquaculture 1990, 85(1-4):259-270.
18. Nielsen C, Holdensaard G, Petersen HC, Bjornsson BT, Madsen SS. Genetic differences in physiology, growth hormone levels and migratory behaviour of Atlantic salmon smolts. J Fish Biol 2001, 59(1):28-44.
19. Boula D, Castric V, Bernatchez L, Audet C. Physiological, endocrine, and genetic bases of anadromy in the brook charr, Salvelinus fontinalis, of the Laval River (Quebec, Canada). Environ Biol Fish 2002, 64(1-3):229-242.
20. Handeland SO, Bjornsson BT, Arnesen AM, Stefansson SO. Seawater adaptation and growth of post-smolt Atlantic salmon (Salmo salar) of wild and farmed strains. Aquaculture 2003, 220(1-4):367-384.
21. Le Bras Y, Dechamp N, Krieg F, Filangi O, Guyomard R, Boussaha M, Bovenhuis H, Pottinger TG, Prunet P, Le Roy P, et al. Detection of QTL with effects on osmoregulation capacities in the rainbow trout (Oncorhynchus mykiss). BMC Genet 2011, 12:46. 3120726, 21569550.
22. Spring J. Vertebrate evolution by interspecific hybridisation - Are we polyploid?. Febs Lett 1997, 400(1):2-8. 10.1016/S0014-5793(96)01351-8, 9000502.
23. Jaillon O, Aury JM, Brunet F, Petit JL, Stange-Thomann N, Mauceli E, Bouneau L, Fischer C, Ozouf-Costaz C, Bernot A, et al. Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype. Nature 2004, 431(7011):946-957. 10.1038/nature03025, 15496914.
24. Allendorf F, Thorgaard G. Tetraploidy and the evolution of salmonid fishes. Evolutionary genetics of fishes 1984, 1-46. New York: Plenum Press, BJ T.
25. Allendorf FW, Danzmann RG. Secondary tetrasomic segregation of MDH-B and preferential pairing of homeologues in rainbow trout. Genetics 1997, 145(4):1083-1092. 1207878, 9093860.
26. Gharbi K, Ferguson MM, Danzmann RG. Characterization of Na, K-ATPase genes in Atlantic salmon (Salmo salar) and comparative genomic organization with rainbow trout (Oncorhynchus mykiss). Mol Genet Genomics 2005, 273(6):474-483. 10.1007/s00438-005-1135-8, 15883826.
27. Gharbi K, Semple JW, Ferguson MM, Schulte PM, Danzmann RG. Linkage arrangement of Na,K-ATPase genes in the tetraploid-derived genome of the rainbow trout (Oncorhynchus mykiss). Anim Genet 2004, 35(4):321-325. 10.1111/j.1365-2052.2004.01152.x, 15265073.
28. Danzmann RG, Cairney M, Davidson WS, Ferguson MM, Gharbi K, Guyomard R, Holm LE, Leder E, Okamoto N, Ozaki A, et al. A comparative analysis of the rainbow trout genome with 2 other species of fish (Arctic charr and Atlantic salmon) within the tetraploid derivative Salmonidae family (subfamily: Salmoninae). Genome 2005, 48(6):1037-1051. 10.1139/g05-067, 16391673.
29. Timusk E, Ferguson M, Moghadam H, Norman J, Wilson C, Danzmann R. Genome evolution in the fish family Salmonidae: generation of a brook charr genetic map and comparisons among charrs (Arctic charr and brook charr) with rainbow trout. BMC Genet 2011, 12:68. 3162921, 21798024.
30. Nichols KM, Edo AF, Wheeler PA, Thorgaard GH. The genetic basis of smoltification-related traits in Oncorhynchus mykiss. Genetics 2008, 179(3):1559-1575. 10.1534/genetics.107.084251, 2475755, 18562654.
31. Woram RA, McGowan C, Stout JA, Gharbi K, Ferguson MM, Hoyheim B, Davidson EA, Davidson WS, Rexroad C, Danzmann RG. A genetic linkage map for Arctic char (Salvelinus alpinus): evidence for higher recombination rates and segregation distortion in hybrid versus pure strain mapping parents. Genome 2004, 47(2):304-315. 10.1139/g03-127, 15060583.
32. Danzmann RG, Davidson EA, Ferguson MM, Gharbi K, Koop BF, Hoyheim B, Lien S, Lubieniecki KP, Moghadam HK, Park J, et al. Distribution of ancestral proto-Actinopterygian chromosome arms within the genomes of 4R-derivative salmonid fishes (Rainbow trout and Atlantic salmon). BMC Genomics 2008, 9:16. 10.1186/1471-2164-9-16, 2266913, 18194530.
33. Cutler CP, Cramb G. Two isoforms of the Na+/K+/2CI(-) cotransporter are expressed in the European eel (Anguilla anguilla). BBA-Biomembranes 2002, 1566(1-2):92-103. 10.1016/S0005-2736(02)00596-5, 12421541.
34. Chen JM, Cutler C, Jacques C, Boeuf G, Denamur E, Lecointre G, Mercier B, Cramb G, Ferec C. A combined analysis of the cystic fibrosis transmembrane conductance regulator: Implications for structure and disease models. Mol Biol Evol 2001, 18(9):1771-1788.
35. Moghadam HK, Ferguson MM, Rexroad CE, Coulibaly I, Danzmann RG. Genomic organization of the IGF1, IGF2, MYF5, MYF6 and GRF/PACAP genes across Salmoninae genera. Anim Genet 2007 2007, 38(5):527-532. 10.1111/j.1365-2052.2007.01645.x, 17894566.
36. Shamblott MJ, Cheng CM, Bolt D, Chen TT. Appearance of inslulin-like growth factor messanger RNA in the liver and pyloric ceca of a teleost in response to exogenous growth hormone. P Natl A Sci USA 1995, 92(15):6943-6946.
37. Bolton JP, Collie NL, Kawauchi H, Hirano T. Osmoregulatory actions of growht hormone in rainbow trout (Salmo gairdneri). J Endocrinol 1987, 112(1):63-68. 10.1677/joe.0.1120063, 3819633.
38. McCormick SD. Endocrine control of osmoregulation in teleost fish. Am Zool 2001, 41(4):781-794.
39. Pelis RM, McCormick SD. Effects of growth hormone and cortisol on Na+-K+-2Cl(-) cotransporter localization and abundance in the gills of Atlantic salmon. Gen Comp Endocr 2001, 124(2):134-143. 10.1006/gcen.2001.7703, 11703079.
40. Boutet I, Ky CLL, Bonhomme F. A transcriptomic approach of salinity response in the euryhaline teleost, Dicentrarchus labrax. Gene 2006, 379:40-50.
41. Kalujnaia S, McWilliam IS, Zaguinaiko VA, Feilen AL, Nicholson J, Hazon N, Cutler CP, Cramb G. Transcriptomic approach to the study of osmoregulation in the European eel Anguilla anguilla. Physiol Genomics 2007, 31(3):385-401. 10.1152/physiolgenomics.00059.2007, 17666525.
42. Evans TG, Somero GN. A microarray-based transcriptomic time-course of hyper- and hypo-osmotic stress signaling events in the euryhaline fish Gillichthys mirabilis: osmosensors to effectors. J Exp Biol 2008, 211(22):3636-3649. 10.1242/jeb.022160, 18978229.
43. Tine M, de Lorgeril J, D'Cotta H, Pepey E, Bonhomme F, Baroiller JF, Durand J-D. Transcriptional responses of the black-chinned tilapia Sarotherodon melanotheron to salinity extremes. Mar Genomics 2008, 1(2):37-46. 10.1016/j.margen.2008.06.001, 21798152.
44. Link K, Berishvili G, Shved N, D'Cotta H, Baroiller J-F, Reinecke M, Eppler E. Seawater and freshwater challenges affect the insulin-like growth factors IGF-I and IGF-II in liver and osmoregulatory organs of the tilapia. Mol Cell Endocrinol 2010, 327(1-2):40-46. 10.1016/j.mce.2010.05.011, 20621706.
45. Moghadam HK, Poissant J, Fotherby H, Haidle L, Ferguson MM, Danzmann RG. Quantitative trait loci for body weight, condition factor and age at sexual maturation in Arctic charr (Salvelinus alpinus): comparative analysis with rainbow trout (Oncorhynchus mykiss) and Atlantic salmon (Salmo salar). Mol Genet Genomics 2007, 277(6):647-661. 10.1007/s00438-007-0215-3, 17308931.
46. Mackay TFC. The genetic architecture of quantitative traits. Annu Rev Genet 2001, 35:303-339. 10.1146/annurev.genet.35.102401.090633, 11700286.
47. Cote G, Perry G, Blier P, Bernatchez L. The influence of gene-environment interactions on GHR and IGF-I expression and their association with growth in brook charr, Salvelinus fontinalis (Mitchill). BMC Genet 2007, 8:87. 2257973, 18154679.
48. Martyniuk CJ, Perry GML, Mogahadam HK, Ferguson MM, Danzmann RG. The genetic architecture of correlations among growth-related traits and male age at maturation in rainbow trout. J Fish Biol 2003, 63(3):746-764.
49. McCormick SD. Methods for non-lethal gill biopsy and measurement of Na+,K+-ATPase activity. Can J Fish Aquat Sci 1993, 50(3):656-658.
50. Ricker W. Growth rates and models. Fish Physiology 1979, VIII. New York: Academic Press, Hoar W, Randall D, Brett J.
51. Darvasi A, Weinreb A, Minke V, Weller JI, Soller M. Detecting marker-QTL linkage and estimating gene effect and map location using a saturated genetic map. Genetics 1993, 134(3):943-951. 1205528, 8349116.
52. Taggart JB, Hynes RA, Prodohl PA, Ferguson A. A simplified protocol for routine total DNA isolation from salmonid fishes. J Fish Biol 1992, 40(6):963-965.
53. Sakamoto T, Danzmann RG, Gharbi K, Howard P, Ozaki A, Khoo SK, Woram RA, Okamoto N, Ferguson MM, Holm LE, et al. A microsatellite linkage map of rainbow trout (Oncorhynchus mykiss) characterized by large sex-specific differences in recombination rates. Genetics 2000, 155(3):1331-1345. 1461176, 10880492.
54. Faculty webpage at the University of Guelph. , http://www.uoguelph.ca/~rdanzman/software.htm
55. MultiQTL Home Page. , http://www.multiqtl.com
56. Churchill GA, Doerge RW. Empirical threshold values for quantitative trait mapping. Genetics 1994, 138(3):963-971. 1206241, 7851788.