Summary
Zebrafish has two duplicate copies of many genes present in single copy in the human genome. Most gene duplicates map in duplicate chromosome segments, suggesting that they are the remnants of a whole genome duplication event. When did this event occur? To address this question, we mapped zebrafish orthologues of genes on human chromosome 20 (Hsa20). The results showed that LG11 and LG23 contain many orthologues of Hsa20 loci, including duplicates of SNAIL, TOPOISOMERASE-1, and KRML. Phylogenetic analysis showed that these chromosome segments were duplicated before the divergence of Cypriniform and Tetraodontiform fishes, as would be predicted by the hypothesis that a genome duplication event happened before the teleost radiation. Because differential loss of gene duplicates can facilitate reproductive isolation, and because gene duplication can foster the evolution of developmental innovations, we suggest the hypothesis that genome duplication in ray fin fish facilitated the teleost radiation, an explosion of diversity that produced half of all vertebrate species.
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References
Amores A, Force A, Yan Y-L, Joly L, Amemiya C, Fritz A, Ho R, Langeland J, Prince V, Wang Y-L, Westerfield M, Ekker M, Postlethwait JH (1998) Zebrafish hox clusters and vertebrate genome evolution. Science 282: 1711–1714
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
Bailey GS, Poulter RTM, Stockwell PA (1978) Gene duplication in tetraploid fish: model for gene silencing at unlinked duplicated loci. Proc Natl Acad Sci USA 75: 5575–5579
Barbazuk WB, Korf I, Kadavi C, Heyen J, Tate S, Wun E, Bedell JA, McPherson JD, Johnson SL (2000) The syntenic relationship of the zebrafish and human genomes. Genome Res 10: 1351–1358
Efron B, Gong G. (1983) A leisurely look at the bootstrap, the jacknife, and cross-validation. Am Stat 37: 36–48
Ekker M, Wegner J, Akimenko MA, Westerfield M (1992) Coordinate embryonic expression of three zebrafish engrailed genes. Development 116: 1001–1010
Elgar G, Clark M, Green A, Sandford R (1997). How good a model is the Fugu genome? Nature 387: 140
Felsenstein J (1985) Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39, 783–791
Ferris SD, Whitt GS (1977) Loss of duplicate gene expression after polyploidization. Nature 265: 258–260
Ferris SD, Whitt GS (1979) Evolution of the differential regulation of duplicate genes after polyploidization. J Mol Evol 12: 267–317
Force A, Lynch M, Pickett FB, Amores A, Yan Y-L, Postlethwait J (1999) The preservation of duplicate genes by complementary degenerative mutations. Genetics 151: 1531–1545
Gallardo MH, Bickham JW, Honeycutt RL, Ojeda RA, Köhler N (1999) Discovery of tetraploidy in a mammal: The red viscacha rat is unaffected by having double the usual number of chromosomes. Nature 401: 341
Gates MA, Kim L, Egan ES, Cardozo T, Sirotkin HI, Dougan ST, Lashkari D, Abagyan R, Schier AF, Talbot WS (1999) A genetic linkage map for zebrafish:comparative analysis and localization of genes and expressed sequences. Genome Res 9: 334–347
Haldane JBS (1933) The part played by recurrent mutation in evolution. Am Nat 67: 5–9
Hammerschmidt M, Nusslein-Volhard C (1993) The expression of a zebrafish gene homologous to Drosophila snail suggests a conserved function in invertebrate and vertebrate gastrulation. Development 119: 1107–1118
Hughes A L (1994) The evolution of functionally novel proteins after gene duplication. Proc R Soc London Ser B 256, 119–124
Kelly PD, Chu F, Woods IG, Ngo-Hazelett P,Cardozo T, Huang H, Kimm F, Liao L, Yan Y-L, Zhou Y, Johnson SL, Abagyan R, Schier AF, Postlethwait JH, Talbot WS (2000) Genetic linkage mapping of zebrafish genes and ESTs. Genome Res 10: 558–567
Kumar S, Hedges SB (1998) A molecular timescale for vertebrate evolution. Nature 392: 917–920
Larhammar D, Risinger C (1994) Molecular genetic aspects of tetraploidy in the common carp Cyprinus carpio. Mol Phylogenet Evol 3: 59–68
Li W-H (1980) Rate of gene silencing at duplicate loci: a theoretical study and interpretation of data from tetraploid fishes. Genetics 95: 237–258
Ludwig A, Belfiore NM, Pitra C, Svirsky V, Jenneckens I (2001) Genome duplication events and functional reduction of ploidy levels in sturgeon ( Acipenser, Huso and Scaphirhynchus). Genetics 158: 1203–1215
Lynch M, Force AG (2000a) The origin of interspecific genomic incompatibility via gene duplication. Am Nat 156: 590–605
Lynch, M, Force AG (2000b) The probability of duplicate gene preservation by subfunctionalization. Genetics 154: 459–473
Manzanares M, Locascio A, Nieto MA (2001) The increasing complexity of the Snail gene superfamily in metazoan evolution. Trends Genet 17: 178–181
Moens CB, Yan Y-L, Appel B, Force AG, Kimmel CB (1996) valentino, a zebrafish gene required for normal hindbrain segmentation. Development 122: 3981–3990
Morizot DC (1990) Use of fish gene maps to predict ancestral vertebrate genome organization. In: Ogita Z-I, Markert CL (Eds) Isozymes: structure, function, and use in biology and medicine. Wiley-Liss, New York, pp. 207–234
Morizot DC, Nairn RS, Walter RB, Kazianis S (1998) The linkage map of Xiphophorus fishes. ILAR J 39: 237–248
Murphy WJ, Sun S, Chen Z, Yuhki N, Hirschmann D, Menotti-Raymond M, O’Brien SJ (2000) A radiation hybrid map of the cat genome:implications for comparative mapping. Genome Res 10: 691–702
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
Nei M, Roychoudhury AK (1973) Probability of fixation of nonfunctional genes at duplicate loci. Am Nat 107: 362–372
Nelson JS (1994) Fishes of the world. Wiley-Interscience, New York
Nitiss JL (1998) Investigating the biological functions of DNA topoisomerases in eukaryotic cells. Biochim Biophys Acta 1400: 63–81
Ohno S (1970) Evolution by gene duplication. Springer-Verlag, Heidelberg
Phillips R, Rab P (2001) Chromosome evolution in the Salmonidae (Pisces):an update. Biol Rev Camb Philos Soc 76: 1–25
Postlethwait J, Johnson S, Midson CN, Talbot WS, Gates M, Ballinger EW, Africa D, Andrews R, Carl T, Eisen JS, Home S, Kimmel CB, HutchinsonM, Johnson M, Rodriguez A (1994) A genetic map for the zebrafish. Science 264: 699–703
Postlethwait JH,Yan Y-L, Gates M, Horne S, Amores A, Brownlie A, Donovan A, Egan E, Force A, Gong Z, Goutel C, Fritz A, Kelsh R, Knapik E, Liao E, Paw P, Ransom D, Singer A, Thomson M, Abduljabbar TS, Yelick P, Beier D, Joly J-S, Larhammar D, Rosa F, Westerfield M, Zon LI, Johnson SL, Talbot WS (1998) Vertebrate genome evolution and the zebrafish gene map. Nat Genet 18: 345–349
Postlethwait JH, Woods IG, Ngo-Hazelett P, Yan Y-L, 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
Santini F, Tyler JC (1999) A new phylogenetic hypothesis for the order Tetraodontiformes (Teleostei, Pisces), with placement of the most fossil basal lineages. Am Zool 39:10A.
Schvarzstein M, Kirn A, Haffter P, Cordes SP (1999) Expression of zkrml2, a homologue of the Krmll/val segmentation gene, during embryonic patterning of the zebrafish. Mech Dev 80: 223–226
Smith S, Metcalfe JA, Elgar G (2000) Identification and analysis of two snail genes in the pufferfish (Fugu rubripes) and mapping of human SNA to 20q. Gene 247: 119–128.
Smith S, Metcalfe JA, Elgar G (2001) Characterisation of two topoisomerase 1 genes in the pufferfish (Fugu rubripes) Gene 265: 195–204
Stoltzfus A (1999) On the possibility of constructive neutral evolution. J Mol Biol 49: 169181
Swofford DL, Olsen GJ, Waddell PJ, Hillis DM (1996) Phylogenetic inference. In: Hillis DM, Moritz C, Mable BK (Eds) Molecular systematics, Sinauer, Sunderland MA, pp 407–514
Takahata N, Maruyama T, (1979) Polymorphism and loss of duplicate gene expression: a theoretical study with application to tetraploid fish. Proc Natl Acad Sci USA 76: 45214525
Thiebaud CH, Fischberg M (1977) DNA content in the genus Xenopus. Chromosoma 59: 253–257
Thisse C, Thisse B, Schilling TF, Postlethwait JH (1993) Structure of the zebrafish snaill gene and its expression in wild-type, spadetail and no tail mutant embryos. Development 119: 1203–1215
Thisse C, Thisse B, Postlethwait JH (1995) Expression of snail2, a second member of the zebrafish Snail family, in cephalic mesendoderm and presumptive neural crest of wild-type and spadetail mutant embryos. Dev Biol 172: 86–99
Uyeno T, Smith GR (1972) Tetraploid origin of the karyotype of catostomid fishes. Science 175: 644–646
Watterson GA (1983) On the time for gene silencing at duplicate loci. Genetics 105: 745–766.
Woods IG, Kelly PD, Chue F, Ngo-Hazelett P, Yan Y-L, Huang H, Postlethwait JH, Talbot WS (2000) A comparative map of the zebrafish genome. Genome Res 10: 1903–1914.
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Postlethwait, J.H., Amores, A., Yan, YL., Austin, C. (2003). Duplication of a portion of human chromosome 20q containing Topoisomerase (Top1)and Snail genes provides evidence on genome expansion and the radiation of teleost fish. In: Shimizu, N., Aoki, T., Hirono, I., Takashima, F. (eds) Aquatic Genomics. Springer, Tokyo. https://doi.org/10.1007/978-4-431-65938-9_2
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DOI: https://doi.org/10.1007/978-4-431-65938-9_2
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