Evidence for Hox gene duplication in rainbow trout (Oncorhynchus mykiss): A tetraploid model species

Journal of Molecular Evolution

Volumn 61, Issue 6, 2005, Pages 804-818

  Moghadam, Hooman K ^a   Ferguson, Moira M ^a   Danzmann, Roy G ^a  

^a UNIVERSITY OF GUELPH   (Canada)

Author keywords

Genetic map; Hox genes; Polyploid; Rainbow trout; Salmonids; Teleost

Indexed keywords

ARTICLE; FISH GENETICS; GENE CLUSTER; GENE DUPLICATION; GENE LOCATION; GENETIC LINKAGE; HOX GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; RAINBOW TROUT; TETRAPLOIDY;

ANIMALS; BASE SEQUENCE; EVOLUTION, MOLECULAR; GENE DUPLICATION; GENES, HOMEOBOX; HUMANS; MODELS, ANIMAL; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; ONCORHYNCHUS MYKISS; PHYLOGENY; POLYPLOIDY; SEQUENCE ALIGNMENT;

ONCORHYNCHUS MYKISS; SALMONIDAE; TELEOSTEI; VERTEBRATA;

EID: 27744471365     PISSN: 00222844     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00239-004-0230-5     Document Type: Article

References (85)

1. Agellon LB, Davies SL, Lin CM, Chen TT, Powers DA (1988) Rainbow trout has two genes for growth hormone. Mol Reprod Dev 1:11-17
2. Allendorf FW, Danzmann RG (1997) Secondary tetrasomic segregation of MDH-B and preferential pairing of homeologues in rainbow trout. Genetics 145:1083-1092
3. Allendorf FW, Thorgaard GH (1984) Tetraploidy and the evolution of salmonid fish. In: Turner JB (ed) Evolutionary genetics of fish. Plenum Press, New York, pp 1-53
4. Allendorf FW, Sebb JE, Knudsen KL, Thorgaard GH, Leary RF (1986) Gene-centromere mapping of 25 loci in rainbow trout. J Hered 77:307-312
5. Amores A, Force A, Yan YL, Loly L, Amemiya C, Fritz A, Ho RK, Langeland J, Prince V, Wang YL, Westerfield M, Ekker M, Postlethwait JH (1998) Zebrafish Hox clusters and vertebrate genome evolution. Science 282:1711-1714
6. Amores A, Suzuki T, Yan YL, Pomeroy J, Singer A, Amemiya C, Postlethwait JH (2004) Developmental roles of pufferfish Hox clusters and genome evolution in ray-fin fish. Genome Res 14:1-10
7. Aparicio S, Hawker K, Cottage A, Mikawa Y, Zuo L, Venkatesh B, Chen E, Krumlauf R, Brenner S (1997) Organization of the Fugu rubripes Hox clusters: Evidence for continuing evolution of vertebrate Hox complexes. Nat Genet 16:79-83
8. Bardakci F, Skibinski DO (1994) Application of the RAPD technique in tilapia fish: Species and subspecies identification. Heredity 73:117-123
9. Boyd M, Lanyon WG, Connor JM (1993) Screening for molecular pathologies in Lesch-Nyhan syndrome. Hum Mutat 2:127-130
10. Bruce AE, Oates AC, Prince VE, Ho RK (2001) Additional Hox clusters in the zebrafish: Divergent expression patterns belie equivalent activities of duplicate Hoxb5 gene. Evol Dev 3:127-144
11. Campanella JJ, Bitincka L, Smalley J (2003) MatGAT: An application that generates similarity/identity matrices using protein or DNA sequences. BMC Bioinform 4:29
12. Carroll RL (1988) Vertebrate paleontology and evolution. Freeman, New York
13. Chiu CH, Dewar K, Wagner GP, Takahashi K, Ruddle F, Ledje C, Bartsch P, Scemama JL, Stellwag E, Fried C, Prohaska SJ, Stadler PF, Amemiya CT (2004) Bichir HoxA cluster sequence reveals surprising trends in ray-finned fish genomic evolution. Genome Res 14:11-17
14. Danzmann RG, Jackson TR, Ferguson MM (1999) Epistasis in allelic expression at upper temperature tolerance QTL in rainbow trout. Aquaculture 173:45-58
15. de Rosa R, Grenier JK, Andreevas T, Cook CE, Adoutte A, Akam M, Carroll SB, Balavoine G (1999) Hox genes in brachiopods and priapulids and protostome evolution. Nature 399:772-776
16. Dorschner MO, Phillips RB (1999) Comparative analysis of two NRAMP loci from rainbow trout. DNA Cell Biol 18:573-583
17. Estoup A, Presa P, Krieg F, Vaiman D, Guyomard R (1993) (CT)n and (GT)n microsatellites: A new class of genetic markers for Salmo trutta L (brown trout). Heredity 71:488-496
18. Ferrier DE (2004) Hox genes: Did the vertebrate ancestor have a Hox14? Curr Biol 14:210-211
19. Ferrier DE, Minguillon C, Holland PW, Garcia-Fernàndez J (2000) The amphioxus Hox cluster: Deuterostome posterior flexibility and Hox14. Evol Dev 2:284-293
20. Fjose A, Molven A, Eiken HG (1988) Molecular cloning and characterization of homeobox-containing genes from Atlantic salmon. Gene 62:141-152
21. Force A, Lynch M, Pickett FB, Amores A, Yan YL, Postlethwait J (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151:1531-1545
22. Ganguly A, Rock MJ, Prockop DJ (1993) Conformation sensitive gel electrophoresis for rapid detection of single base differences in double stranded PCR products and DNA fragments: Evidence for solvent induced bends in DNA heteroduplexes. Proc Natl Acad Sci USA 90:10325-10329
23. Garcia-Fernàndez J, Holland PWH (1994) Archetypal organization of the amphioxus Hox gene cluster. Nature 370:563-566
24. Glavac D, Dean M (1993) Optimization of the single-strand conformation polymorphism (SSCP) technique for detection of point mutations. Hum Mutat 2:404-414
25. Hartley SE (1987) The chromosomes of salmonid fish. Biol Rev 62:197-214
26. Hayashi K, Yandell DW (1993) How sensitive is PCR-SSCP? Hum Mutat 2:338-346
27. Hughes AL, Friedman R (2003) 2R or not 2R: Testing hypotheses of genome duplication in early vertebrates. J Struct Funct Genomics 3:85-93
28. Jackson TR, Ferguson MM, Danzmann RG, Fishback AG, Ihssen PE, O'Connell M, Crease TJ (1998) Identification of two QTL influencing upper temperature tolerance in three rainbow trout (Oncorhynchus mykiss) half-sib families. Heredity 80:143-151
29. Johnson KR, Wright JE Jr, May B (1987) Linkage relationships reflecting ancestral tetraploidy in salmonid fish. Genetics 116:579-591
30. Jozefowicz C, McClintock J, Prince V (2003) The fates of zebrafish Hox gene duplicates. J Struct Funct Genomics 3:185-194
31. Kappen C, Schughart K, Ruddle FH (1989) Two steps in the evolution of Antennapedia-class vertebrate homeobox genes. Proc Natl Acad Sci USA 86:5459-5463
32. Krumlauf R (1994) Hox genes in vertebrate development. Cell 78:191-201
33. Kumar S, Tamura K, Jakobsen IB, Nei M (2001) MEGA2: Molecular evolutionary genetics analysis software. Bioinformatics 17:1244-1245
34. Ladjali-Mohammedi K, Grapin-Botton A, Bonnin MA, Le Douarin NM (2001) Distribution of Hox genes in the chicken genome reveals a new segment of conservation between human and chicken. Cytogenet Cell Genet 92:157-161
35. Larhammar D, Lundin LG, Hallbook F (2002) The human Hox-bearing chromosome regions did arise by block or chromosome (or even genome) duplications. Genome Res 12:1910-1920
36. Leder EH, Danzmann RG, Ferguson MM (2004) Comparison of GNRH3 genes across salmonid genera. Anim Genet 35:126-129
37. Ledje C, Kim CB, Ruddle FH (2002) Characterization of Hox genes in the Bichir, Polypterus palmas. J Exp Zool 294:107-111
38. Málaga-Trillo E, Meyer A (2001) Genome duplications and accelerated evolution of Hox genes and cluster architecture in teleost fish. Am Zool 41:676-686
39. McGinnis W, Krumlauf R (1992) Homeobox genes and axial patterning. Cell 68:283-302
40. Meyer A, Málaga-Trillo E (1999) Vertebrate genomics: More fishy tales about Hox genes. Curr Biol 9:210-213
41. Meyer A, Schartl M (1999) Gene and genome duplications in vertebrates: The one-to-four (-to-eight in fish) rule and the evolution of novel gene functions. Curr Opin Cell Biol 11:699-704
42. Misof BY, Wagner GP (1995) Evidence for four Hox clusters in Killifish Fundulus heteroclitus (Teleostei). Mol Phylogenet Evol 5:309-322
43. Misof BY, Blanco MJ, Wagner GP (1996) PCR survey of Hox genes of the zebrafish: New sequence information and evolutionary implications. J Exp Zool 274:193-206
44. Mito T, Endo K (2000) PCR survey of Hox genes in the Crinoid and Ophiuroid: Evidence for anterior conservation and posterior expansion in the echinoderm Hox gene cluster. Mol Phylogenet Evol 14:375-388
45. Morgenstern B (1999) DIALIGN 2: Improvement of the segment-to-segment approach to multiple sequence alignment. Bioinformatics 15:211-218
46. Naruse K, Fukamachi S, Mitani H, Kondo M, Matsuoka T, Kondo S, Hanamura N, Morita Y, Hasegawa K, Nishigaki R, Shimada A, Wada H, Kusakabe T, Suzuki N, Kinoshita M, Kanamori A, Terado T, Kimura H, Nonaka M, Shima A (2000) A detailed linkage map of medaka, Oryzias latipes: Comparative genomics and genome evolution. Genetics 154:1773-1784
47. Naruse K, Tanaka M, Mita K, Shima A, Postlethwait J, Mitani H (2004) A medaka gene map: The trace of ancestral vertebrate proto-chromosomes revealed by comparative gene mapping. Genome Res 14:820-827
48. Nelson JS (1994) Fish of the world. 3rd ed. John Wiley and Sons, New York
49. Nichols KM, Young WP, Danzmann RG, Robison BD, Rexroad C, Noakes M, Phillips RB, Bentzen P, Spies I, Knudsen K, Allendorf FW, Cunningham BM, Brunelli J, Zhang H, Ristow S, Drew R, Brown KH, Wheeler PA, Thorgaard GH (2003) A consolidated linkage map for rainbow trout (Oncorhynchus mykiss). Anim Genet 34:102-115
50. Oakley TH, Phillips RB (1999) Phylogeny of salmonine fish based on growth hormone introns: Atlantic (Salmo) and Pacific (Oncorhynchus) salmon are not sister taxa. Mol Phylogenet Evol 11:381-393
51. Ohno S (1970) Evolution by gene duplication. Springer Verlag, New York
52. Ohno S, Muramoto J, Klein J, Atkin NB (1969) Diploid-tetraploid relationship in clupeoid and salmonoid fish. In: Darlington CD, Lewis KR (eds) Chromosomes today, vol 2. Oliver and Boyd, Edinburgh, pp 139-147
53. O'Malley KG, Sakamoto T, Danzmann RG, Ferguson MM (2003) Quantitative trait loci for spawning date and body weight in rainbow trout: testing for conserved effects across ancestrally duplicated chromosomes. J Hered 94:273-284
54. Orita M, Iwahana H, Kanazawa H, Hayashi K, Sekiya T (1989a) Detection of polymorphisms of human DNA by gel electrophoresis as single strand conformation polymorphisms. Proc Natl Acad Sci USA 86:2766-2770
55. Orita M, Suzuki Y, Sekiya T, Hayashi K (1989b) Rapid and sensitive detection of point mutations and DNA polyporphisms using the polymerase chain reaction. Genomics 5:874-879
56. Pavell AM, Stellwag EJ (1994) Survey of Hox-like genes in the teleost Morone saxatilis: Implications for evolution of the Hox gene family. Mol Mar Biol Biotechnol 33:149-157
57. Phillips RB, Rab P (2001) Chromosome evolution in the Salmonidae (Pisces): An update. Biol Rev Camb Philos Soc 76:1-25
58. Phillips RB, Zimmerman A, Noakes MA, Palti Y, Morasch MR, Eiben L, Ristow SS, Thorgaard GH, Hansen JD (2003) Physical and genetic mapping of the rainbow trout major histocompatibility regions: Evidence for duplication of the class I region. Immunogenetics 55:561-569
59. Postlethwait JH, Woods IG, Ngo-Hazelett P, Yan YL, Kelly PD, Chu F, Huang H, Hill-Force A, Talbot WS (2000) Zebrafish comparative genomics and the origins of vertebrate chromosomes. Genome Res 10:1890-1902
60. Powers TP, Amemiya CT (2004) Evidence for a Hox14 paralog group in vertebrates. Curr Biol 14:R183-R184
61. Prince VE (2002) The Hox paradox: More complex(es) than imagined. Dev Biol 249:1-15
62. Prince VE, Joly L, Ekker M, Ho RK (1998) Zebrafish Hox genes: Genomic organization and modified colinear expression patterns in the trunk. Development 125:407-420
63. Prohaska SJ, Stadler PF (2004) The duplication of the Hox gene clusters in teleost fish. Theor Biosci 123:89-110
64. Sakamoto T, Danzmann RG, Okamoto N, Ferguson MM, Ihssen PE (1999) Linkage analysis of quantitative trait loci associated with spawning time in rainbow trout (Oncorhynchus mykiss). Aquaculture 173:33-43
65. Sakamoto T, Danzmann RG, Gharbi K, Howard P, Ozaki A, Khoo SK, Woram RA, Okamoto N, Ferguson MM, Holm LE, 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
66. Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74:5463-5467
67. Santini S, Boore JL, Meyer A (2003) Evolutionary conservation of regulatory elements in vertebrate Hox gene clusters. Genome Res 13:1111-1122
68. Schughart K, Kappen C, Ruddle FH (1989) Duplication of large genomic regions during the evolution of vertebrate homeobox genes. Proc Natl Acad Sci USA 86:7067-7071
69. Scott MP (1992) Vertebrate homeobox gene nomenclature. Cell 71:551-553
70. Sidow A (1996) Gen(om)e duplications in the evolution of early vertebrates. Curr Opin Genet Dev 6:715-722
71. Skrabanek L, Wolfe KH (1998) Eukaryote genome duplication - Where's the evidence? Curr Opin Genet Dev 8:694-700
72. Snell EA, Scemama JL, Stellwag EJ (1999) Genomic organization of the Hoxa4-Hoxa10 region from Morone saxatilis: implications for Hox gene evolution among vertebrates. J Exp Zool 285:41-9
73. Sybenga J (1972) General cytogenetics. American Elsevier, New York
74. Taggart JB, Hynes RA, Prodohl PA, Ferguson A (1992) A simplified protocol for routine total DNA isolation from salmonid fish. J Fish Biol 40:963-965
75. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTALX windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24:4876-4882
76. Tindall KR, Kunkel TA (1988) Fidelity of DNA synthesis by the Thermus aquaticus DNA polymerase. Biochemistry 27:6008-6013
77. Vandepoele K, De Vos W, Taylor JS, Meyer A, Van de Peer Y (2004) Major events in the genome evolution of vertebrates: paranome age and size differ considerably between ray-finned fish and land vertebrates. Proc Natl Acad Sci USA 101:1638-1643
78. Voorrips RE (2002) Mapchart: Software for the graphical presentation of linkage maps and QTLs. J Hered 93:77-78
79. Voss SR, Smith JJ, Gardiner DM, Parichy DM (2001) Conserved vertebrate chromosome segments in the large salamander genome. Genetics 158:735-746
80. Wittbrodt J, Meyer A, Schartl M (1998) More genes in fish. BioEssay 20:511-515
81. Woram RA, Gharbi K, Sakamoto T, Hoyheim B, Holm L, Naish K, McGowan C, Ferguson MM, Phillips RB, Stein J, Guyomard R, Cairney M, Taggart JB, Powell R, Davidson W, Danzmann RG (2003) Comparative genome analysis of the primary sex-determining locus in salmonid fish. Genome Res 13:272-280
82. Woram RA, McGowan C, Stout JA, Gharbi K, Ferguson MM, Hoyheim B, Davidson EA, Davidson WS, Rexroad C, Danzmann RG (2004) 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 47:304-315
83. Wright JE Jr, Johnson K, Hollister A, May B (1983) Meiotic models to explain classical linkage, pseudolinkage, and chromosome pairing in tetraploid derivative salmonid genomes. Isozymes Curr Top Biol Med Res 10:239-260
84. Young WP, Wheeler PA, Coryell VH, Keim P, Thorgaard GH (1998) A detailed linkage map of rainbow trout produced using doubled haploids. Genetics 148:839-850
85. Zhang J, Nei M (1996) Evolution of Antennapedia class homeobox genes. Genetics 142:295-303