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Differential genome duplication and fish diversity

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Abstract

The duplication of genes and entire genomes arebelieved to be important mechanisms underlyingmorphological variation and functionalinnovation in the evolution of life andespecially for the broad diversity observed inthe speciation of fishes. How did these fishspecies and their genetic diversity arise? Theoccurrence of three rounds of genomeduplication during vertebrate evolution mightexplain why many gene families are typicallyabout half the size in land vertebrates as theyare in fishes. However, mechanisms of geneticdiversity in fish lineages need to be furtherexplained. Here we propose that differentialgenome duplication of from two to six roundsoccurred in different fish lines, offering newopportunities during the radiation of fishlineages. This model provides a fundamentalbasis for the understanding of theirspeciation, diversity and evolution.

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References

  • Allendorf, F.W. and Thorgaard, G.H. (1984) Polypoidy and the evolution of salmonid fishes. In: Turner, B.J. (ed.), The Evolutionary Genetics of Fishes. New York and London, Plenum Press, pp. 1-53.

    Chapter  Google Scholar 

  • Amores, A., Force, A., Yan, Y.L., Joly, L., Amemiya, C., Fritz, A., Ho, R.K., Langeland, J., Prince, V., Wang, Y.L., Westerfield, M., Ekker, M. and Postlethwait, J.H. (1998) Zebrafish hox clusters and vertebrate genome evolution. Science 282, 1711-1714.

    Article  CAS  PubMed  Google Scholar 

  • Aparicio, S., Hawker, K., Cottage, A., Mikawa, Y., Zuo, L., Venkatesh, B., Chen, E., Krumlauf, R. and Brenner S. (1997) Organization of the Fugu rubripes Hox clusters: evidence for continuing evolution of vertebrate Hox complexes. Nat. Genet. 16, 79-83.

    Article  CAS  PubMed  Google Scholar 

  • Aparicio, S. (2000) Vertebrate evolution recent perspectives from fish. Trends Genet. 16, 54-56.

    Article  CAS  PubMed  Google Scholar 

  • Chiang, E.F., Pai, C.I., Wyatt, M., Yan, Y.L., Postlethwait, J. and Chung, B. (2001) Two sox9 genes on duplicated zebrafish chromosomes: expression of similar transcription activators in distinct sites. Dev. Biol. 231, 149-163.

    Article  CAS  PubMed  Google Scholar 

  • Dingerkus, G. and Howell, W.M. (1976) Karyotypic analysis and evidence of tetraploidy in the North American paddlefish Polyodon spathula. Science 194, 842-844.

    Article  CAS  PubMed  Google Scholar 

  • Ferris, S.D. and Whitt, G.S. (1977a) The evolution of duplicate gene expression in the carp (Cyprinus carpio). Experimentia 33, 1299-1301.

    Article  CAS  Google Scholar 

  • Ferris, S.D. and Whitt, G.S. (1977b) Loss of duplicate gene expression after polyploidization. Nature 265, 258-260.

    Article  CAS  PubMed  Google Scholar 

  • Ferris, S.D. and Whitt, G.S. (1979) Evolution of the differential regulation of duplicate genes after polyploidization. J. Mol. Evol. 12, 267-317.

    Article  CAS  PubMed  Google Scholar 

  • Ferris, S.D. and Whitt, G.S. (1980) Genetic variability in species with extensive gene duplication: the tetraploid catostomid fishes. Am. Nat. 115, 650-666.

    Article  Google Scholar 

  • Fisher, S.E., Shaklee, J.B., Ferris, S.D. and Whitt, G.S. (1980) Evolution of five multilocus isozyme systems in the chordates. Genetica 52/52, 73-85.

    Google Scholar 

  • Fisher, S.E. and Whitt, G.S. (1978) Evolution of isozyme loci and their differential tissue expression. J. Mol. Evol. 12, 25-55.

    Article  CAS  PubMed  Google Scholar 

  • Force, A., Lynch, M., Pickett, F.B., Amores, A., Yan, Y.L. and Postlethwait, J. (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151, 1531-1545.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Garcia-Fernandez, J. and Holland, P.W. (1994) Archetypal organization of the amphioxus Hox cluster. Nature 370, 563-566.

    Article  CAS  PubMed  Google Scholar 

  • De Grandi, A., Calvari, V., Bertini, V., Bulfone, A., Peverali, G., Camerino, G., Borsani, G. and Guioli, S. (2000) The expression patternof a mouse doublesex-related gene is consistent with a role in gonagal differentiation. Mech. Dev. 90, 323-326.

    Article  CAS  PubMed  Google Scholar 

  • Holland, P.W. (1997) Vertebrate evolution: something fishy about Hox genes. Curr. Biol. 7, 570-572.

    Article  Google Scholar 

  • Holland, P.W. and Garcia-Fernandez, J. (1996) Hox genes and chordate evolution. Dev. Biol. 173, 382-395.

    Article  CAS  PubMed  Google Scholar 

  • Huang, X., Cheng, H., Guo, Y., Liu, L., Gui J. and Zhou, R. (2002) A conserved family of doublesex-related genes from fishes. J. Exp. Zool. 294, 63-67.

    Article  CAS  PubMed  Google Scholar 

  • Kurosawa, G., Yamada, K., Ishiguro, H. and Hori, H. (1999) Hox gene complexity in medaka fish may be similar to that in puffer-fish rather than zebrafish. Biochem. Biophys. Res. Commun. 260, 66-70.

    Article  CAS  PubMed  Google Scholar 

  • Li, Y., Li, K. and Zhou, D. (1983) Cellular DNA content of fourteen species of fresh water fishes. Acta Genetica Sinica 10, 384-389.

    Google Scholar 

  • Lundin, L.G. (1993) Evolution of the vertebrate genome as reflected in paralogous chromosomal regions in man and the house mouse. Genomics 16, 1-19.

    Article  CAS  PubMed  Google Scholar 

  • Lynch, M. and Conery, J.S. (2000) The evolutionary fate and consequences of duplicate genes. Science 290, 1151-1155.

    Article  CAS  PubMed  Google Scholar 

  • Lynch, M. and Force, A. G. (2000) The origin of interspecific genomic incompatibility via gene duplication. Am. Nat. 156, 590-605.

    Article  Google Scholar 

  • Marchand, O., Govoroun, M., D'Cotta, H., McMeel, O., Lareyre, J., Bernot, A., Laudet, V. and Guiguen, Y. (2000) DMRT1 expression during gonadal differentiation and spermatogenesis in the rainbow trout, Oncorhynchus mykiss. Biochim. Biophys. Acta. 1493, 180-187.

    Article  CAS  PubMed  Google Scholar 

  • Markert, C.L., Shaklee, J.B. and Whitt, G.S. (1975) Evolution of a gene. Science 189, 102-114.

    Article  CAS  PubMed  Google Scholar 

  • Meyer, A. and Malaga-Trillo, E. (1999) Vertebrate genomics: more fishy tales about hox genes. Curr. Biol. 9, 210-213.

    Article  Google Scholar 

  • Meyer, A. and 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.

    Article  CAS  PubMed  Google Scholar 

  • Mirsky, A. and Ris, H. (1951) The desoxyribonucleic acid content of animal cells and its evolutionary significance. J. Gen. Physiol. 34, 451-463.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Muramoto, J.E., Ohno, S. and Atkin, N.B. (1968) On the diploid state of the fish order Ostariophysi. Chromosoma 24, 59-66.

    Article  CAS  PubMed  Google Scholar 

  • 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. and Shima, A. (2000) A detailed linkage map of medaka, Oryzias latipes: comparative genomics and genome evolution. Genetics 154, 1773-1784.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ohno, S. (1970) Evolution by Gene Duplication, New York, Springer-Verlag.

    Book  Google Scholar 

  • Ohno, S. (1999) The one-to-four rule and paralogues of sex-determining gene. Cell Mol. Life Sci. 55, 824-830.

    Article  CAS  PubMed  Google Scholar 

  • Ohno, S., Muramoto, J., Steinus, C., Christian, L., Kittrell, W.A. and Atkin, N.B. (1969) Microchromosomes in holocephalian, Chondrostean and holostean fishes. Chromosoma 26, 35-40.

    Article  CAS  PubMed  Google Scholar 

  • Ottolenghi, C., Veitia, R., Quintana-Murci, L., Torchard, D., Scapoli, L., Souleyreau-Therville, N., Beckmann, J., Fellous, M. and McElreavey, K. (2000) The region on 9p associated with 46, XY sex reversal contains several transcripts expressed in the urogenital system and a novel doublesex-related domain. Genomics 64, 170-178.

    Article  CAS  PubMed  Google Scholar 

  • Pebusque, M.J., Coulier, F., Birnbaum, D. and Pontarotti, P. (1998) Ancient large-scale genome duplications: phylogenetic and linkage analyses shed light on chordate genome evolution. Mol. Biol. Evol. 15, 1145-1159.

    Article  CAS  PubMed  Google Scholar 

  • Postlethwait, J.H., Yan, Y.-L., Gates, M.A., Horne, S., Amores, A., Brownlie, A., Adriana Donovan, A., Egan, E.S., Force, A., Gong, Z., Goutel, C., Fritz, A., Kelsh, R., Knapik, E., Liao, E., Paw, B., Ransom, D., Singer, A., Thomson, M., Abduljabbar, T.S., Yelick, P., Beier, D., Joly, J.-S., Larhammar, D., Rosa, F., Westerfield, M., Zon, L.I., Johnson, S.L. and Talbot, W.S. (1998) Vertebrate genome evolution and zebrafish gene map. Nat. Genet. 18, 345-349.

    Article  CAS  PubMed  Google Scholar 

  • Prince, V.E., Joly, L., Ekker, M. and Ho, R.K. (1998) Zebrafish Hox genes: genome organization and modified colinear expression patterns in the trunk. Development 125, 407-420.

    CAS  PubMed  Google Scholar 

  • Raymond, C.S., Kettlewell, J.R., Hirsch, B., Bardwell, V.J. and Zarkower, D. (1999) Expression of Dmrt1 in the genital ridge of mouse and chicken embryos suggest a role in vertebrate sexual development. Dev. Biol. 215, 208-220.

    Article  CAS  PubMed  Google Scholar 

  • Robinson-Rechavi, M., Marchand, O., Escriva, H., Bardet, P.L., Zelus, D., Hughes, S. and Laudet, V. (2001) Euteleost fish genomes are characterized by expansion of gene families. Genome Res. 11, 781-788.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Skrabanek, L. and Wolfe, K.H. (1998) Eukaryotic genome duplication-where's the evidence? Curr. Opin. Genet. Dev. 8, 694-700.

    Article  CAS  PubMed  Google Scholar 

  • Taylor, J.S., Van de Peer, Y. and Meyer, A. (2001) Genome duplication, divergent resolution and speciation. Trends Genet. 17, 299-301.

    Article  CAS  PubMed  Google Scholar 

  • Venkatesh, B. Gilligan, P. and Brenner, S. (2000) Fugu: a compact vertebrate reference genome. FEBS Lett. 476, 3-7.

    Article  CAS  PubMed  Google Scholar 

  • Vervoort, A. (1980) Tetraploidy in Protopterus (Dipnoi). Experimentia 36, 294-295.

    Article  Google Scholar 

  • Vogel, G. (1999) Double genes may explain fish diversity. Science 281, 1119-1120.

    Article  Google Scholar 

  • Wachtel, S. and Tiersch, T. (1993) Variations in genome mass. Comp. Biochem. Physiol. 104B, 207-213.

    CAS  Google Scholar 

  • Wagner, A. (2001) Birth and death of duplicated genes in completely sequenced eukaryotes. Trends Genet. 17, 237-239.

    Article  CAS  PubMed  Google Scholar 

  • Wittbrodt, J., Meyer, A. and Schartl, M. (1998) More genes in fish? Bioessays 20, 511-515.

    Article  Google Scholar 

  • Yi, M., Yu, Q., Huang, X., Liu, J., Guo, Y., Liu, L. and Zhou, R. (2001) Painting the chromosomes of fishes with human sex chrosome-specific DNA probes. Acta Genetica Sinica 28, 1-6.

    CAS  PubMed  Google Scholar 

  • Yu, X., Zhou, D., Li, Y., Li, K. and Zhou M. (1989) Chromosomes of Chinese Fresh-water Fishes, Beijing, Beijing Science Press.

    Google Scholar 

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Authors and Affiliations

  1. Department of Genetics and Center for Developmental Biology, College of Life Sciences, Wuhan University, Wuhan, 430072, P. R. China

    Rongjia Zhou & Hanhua Cheng

  2. Aquaculture Research Station, Louisiana Agricultural Experiment Station, Louisiana State University Agricultural Center, Baton Rouge, LA, 70803, USA

    Terrence R. Tiersch

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  1. Rongjia Zhou
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  2. Hanhua Cheng
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Correspondence to Rongjia Zhou.

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Zhou, R., Cheng, H. & Tiersch, T.R. Differential genome duplication and fish diversity. Reviews in Fish Biology and Fisheries 11, 331–337 (2002). https://doi.org/10.1023/A:1021395506705

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