Skip to main content
SpringerLink
Log in

Numerous groups of chromosomal regional paralogies strongly indicate two genome doublings at the root of the vertebrates

  • Published:
Journal of Structural and Functional Genomics

Abstract

The appearance of the vertebrates demarcates some of the most far-reaching changes of structure and function seen during the evolution of the metazoans. These drastic changes of body plan and expansion of the central nervous system among other organs coincide with increased gene numbers. The presence of several groups of paralogous chromosomal regions in the human genome is a reflection of this increase. The simplest explanation for the existence of these paralogies would be two genome doublings with subsequent silencing of many genes. It is argued that gene localization data and the delineation of paralogous chromosomal regions give more reliable information about these types of events than dendrograms of gene families as gene relationships are often obscured by uneven replacement rates as well as other factors. Furthermore, the topographical relations of some paralogy groups are discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Adams, M.D., et al. (2000) The genome sequence of Drosophila melanogaster. Science, 287, 2185-2195.

    Google Scholar 

  • Bork, P. and Copley, R. (2001) Filling in the gaps. Nature, 409, 818-820.

    Google Scholar 

  • Burt, D.W., Bruley, C., Dunn, I.C., Jones, C.T., Ramage, A., Law, A.S., Morrice, D.R., Paton, I.R., Smith, J., Windsor, D., Sazanov, A., Fries, R. and Waddington, D. (1999) The dynamics of chromosome evolution in birds and mammals. Nature, 402, 411-413.

    Google Scholar 

  • Chaudhary, R., Raudsepp, T., Guan, X.-Y., Zhang, H. and Chowdhary, B.P. (1998) Zoo-FISH with microdissected arm specific paints for HSA2, 5, 6, 16, and 19 refines known homology with pig and horse chromosomes. Mamm. Genome, 9, 44-49.

    Google Scholar 

  • Chowdhary, B.P., Frönicke, L., Gustavsson, I. and Scherthan, H. (1996) Comparative analysis of the cattle and human genomes: Detection of ZOO-FISH and gene mapping-based chromosomal homologies. Mamm. Genome, 7, 297-302.

    Google Scholar 

  • Chowdhary, B.P., Raudsepp, T., Frönicke, L. and Scherthan, H. (1998) Emerging patterns of comparative genome organization in some mammalian species as revealed by zoo-FISH. Genome Res., 8,pp577-589.

    Google Scholar 

  • Ferrier, D.E.K., Minguillón, C., Holland, P.W.H. and Garcia-Fernández, J. (2000) The amphioxus Hox cluster: deuterostome posterior flexibility and Hox14. Evol. Dev., 2, 284-293.

    Google Scholar 

  • Frönicke, L., Chowdhary, B.P., Scherthan, H. and Gustavsson, I. (1996) A comparative map of the porcine and human genomes demonstrates ZOO-FISH and gene mapping-based chromosomal homologies. Mamm. Genome, 7, 285-290.

    Google Scholar 

  • Gibson, T.J. and Spring, J. (2000) Evidence in favour of ancient octaploidy in the vertebrate genome. Biochem. Soc. Trans., 28, 259-264.

    Google Scholar 

  • Hallböök, F., Kullander, K. and Lundin, L.-G. (2001) Evolution of the neurotrophins and their receptors. In Neurobiology of the Neurotrophins (Ed. Mocchetti, I.), FP Graham Publishing Co, Johnson City, TN, pp. 65-100.

    Google Scholar 

  • Holland, P.W.H. (1997) Vertebrate evolution: Something fishy about Hox genes. Curr. Biol., 7, R570-R572.

    Google Scholar 

  • Holland, P.W.H., Garcia-Fernández, J., Williams, N.A. and Sidow, A. (1994) Gene duplications and the origins of vertebrate development. Development Suppl., 125?133.

  • Hughes, A.L. (1999) Phylogenies of developmentally important proteins do not support the hypothesis of two rounds of genome duplication early in vertebrate history. J. Mol. Evol., 48, 565-576.

    Google Scholar 

  • Iwabe, N., Kuma, K. and Miyata, T. (1996) Evolution of gene families and relationship with organismal evolution: Rapid divergence of tissue-specific genes in the early evolution of chordates. Mol. Biol. Evol., 13, 483-493.

    Google Scholar 

  • Kasahara, M., Hayashi, M., Tanaka, K., et al. (1996) Chromosomal localization of the proteasome Z subunit gene reveals an ancient chromosomal duplication involving the major histocompatibility complex. Proc. Natl. Acad. Sci. USA, 93, 9096-9101.

    Google Scholar 

  • Katsanis, N., Fitzgibbon, J. and Fisher, E.M.C. (1996) Paralogy mapping: Identification of a region in the human MHC triplicated onto human chromosomes 1 and 9 allows the prediction and isolation of novel PBX and NOTCH loci. Genomics, 35, 101-108.

    Google Scholar 

  • Li, W.-H. (1997) Molecular Evolution. Sinauer Associates, Sunderland, MA.

    Google Scholar 

  • Lundin, L.-G. (1989) Gene homologies and the nerve system. In Genetics of Neuropsychiatric Diseases (Ed. Wetterberg, L.), Vol. 51, MacMillan Press, London, pp. 43-58.

    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.

    Google Scholar 

  • Lundin, L.-G. (1999) Gene duplications in early metazoan evolution. Sem. Cell Dev. Biol., 10, 523-530.

    Google Scholar 

  • Martin, A. (2001) Is tetralogy true? Lack of support for the 'one to-four rule'. Mol. Biol. Evol., 18, 89-93.

    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.

    Google Scholar 

  • Nadeau, J.H. and Sankoff, D. (1997) Comparable rates of gene loss and functional divergence after genome duplications early in vertebrate evolution. Genetics, 147, 1259-1266.

    Google Scholar 

  • Nadeau, J.H. and Sankoff, D. (1998) Counting on comparative maps. Trends Genet., 14, 495-501.

    Google Scholar 

  • O'Brien, S. J., Wienberg, J. and Lyons, L.A. (1997) Comparative genomics: lessons from cats. Trends Genet., 13, 393-99.

    Google Scholar 

  • Ohno, S. (1969) The role of gene duplication in vertebrate evolution. In The Biological Basis of Medicine (Eds., Bittar, E.D. and Bittar, N.), Vol. 4, Academic Press, London, pp. 109-132.

    Google Scholar 

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

    Google Scholar 

  • Ohno, S. (1998) The notion of the Cambrian pananimalia genome and a genomic difference that separated vertebrates from invertebrates. In Progress in Molecular and Subcellular Biology (Ed., Müller, W.E.G.), Vol. 21, Springer-Verlag, Berlin, pp. 97-117.

    Google Scholar 

  • Ohno, S., Wolf, U. and Atkin, N.B. (1968) Evolution from fish to mammals by gene duplication. Hereditas, 59, 169-187.

    Google Scholar 

  • Ono, K., Suga, H., Iwabe, N., Kuma, K. and Miyata, T. (1999) Multiple protein tyrosine phosphatases in sponges and explosive gene duplication in the early evolution of animals before the parazoan-eumetazoan split. J. Mol. Evol., 48, 654-662.

    Google Scholar 

  • Page, R.D.M. and Charleston, M.A. (1997) From gene to organismal phylogeny: Reconciled trees and the gene tree/species tree problem. Mol. Phylogenet. Evol., 7, 231-240.

    Google Scholar 

  • Patton, S.J., Luke, G.N. and Holland, P.W.H. (1998) Complex history of a chromosomal paralogy region: insights from Amphioxus aromatic amino acid hydroxylase genes and insulinrelated genes. Mol. Biol. Evol., 15, 1373-1380.

    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.

    Google Scholar 

  • Pollard, S.L. and Holland, P.W.H. (2000) Evidence for 14 homeobox gene clusters in human genome ancestry. Curr. Biol., 10, 1059-1062.

    Google Scholar 

  • Popovici, C., Leveugle, M., Birnbaum, D. and Coulier, F. (2001) Homeobox gene clusters and the human paralogy map. FEBS Lett., 491, 237-242.

    Google Scholar 

  • Postlethwait, J.H., Woods, I.G., Ngo-Hazelett, P., Yan, Y.-L., Kelly, P.D., Chu, F., Huang, H., Hill-Force, A. and Talbot, W.S. (2000) Zebrafish comparative genomics and the origins of vertebrate chromosomes. Genome Res., 10, 1890-1902.

    Google Scholar 

  • Raudsepp, T., Frönicke, L., Scherthan, H., Gustavsson, I. and Chowdhary, B.P. (1996) ZOO-FISH delineates conserved chromosomal segments in horse and man. Chromosome Res., 4, 218-225.

    Google Scholar 

  • Scherthan, H., Cremer, T., Arnason, U., Weier, H.-U., Lima-de-Faria, A. and Frönicke, L. (1994) Comparative chromosome painting discloses homologous segments in distantly related mammals. Nature Genet., 6, 342-347.

    Google Scholar 

  • Searle, A.G. and Selley, R.L. (1997) Tables of genetic homology. Mouse Genome, 95, 106-160.

    Google Scholar 

  • Sharman, A.C. and Holland, P.W.H. (1996) Conservation, duplication, and divergence of developmental genes during chordate evolution. Netherlands J. Zool., 46, 47-67.

    Google Scholar 

  • Shimeld, S.M. and Holland, P.W.H. (2000) Vertebrate innovations. Proc. Natl. Acad. Sci. USA, 97, 4449-4452.

    Google Scholar 

  • Sidow, A. (1996) Gen(om)e duplications in the evolution of early vertebrates. Curr. Opin. Genet. Dev., 6, 715-22.

    Google Scholar 

  • Simmen, M.W., Leitgeb, S., Clark, V.H., Jones, S. J. M. and Bird, A. (1998) Gene number in an invertebrate chordate, Ciona intestinalis. Proc. Natl. Acad. Sci. USA, 95, 4437-4440.

    Google Scholar 

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

    Google Scholar 

  • Smith, N.G.C., Knight, R. and Hurst, L.D. (1999) Vertebrate genome evolution: a slow shuffle or a big bang? BioEssays, 21, 697-703.

    Google Scholar 

  • Spring, J. (1997) Vertebrate evolution by interspecific hybridisation-are we polyploid? FEBS Lett., 400, 2-8.

    Google Scholar 

  • Spring, J., Goldberger, O.A., Jenkins, N.A., Gilbert, D.J., Copeland, N.G. and Bernfield, M. (1994) Mapping of the syndecan genes in the mouse: Linkage with members of the Myc gene family. Genomics, 21, 597-601.

    Google Scholar 

  • Suga, H., Hoshiyama, D., Kuraku, S., Katoh, K., Kubokawa, K. and Miyata, T. (1999a) Protein tyrosine kinase cDNAs from Amphioxus, hagfish, and lamprey: Isoform duplications around the divergence of cyclostomes and gnathostomes. J. Mol. Evol., 49, 601-608.

    Google Scholar 

  • Suga, H., Koyanagi, M., Hoshiyama, D., Ono, K., Iwabe, N., Kuma, K. and Miyata, T. (1999b) Extensive gene duplication in the early evolution of animals before the parazoan-eumetazoan split demonstrated by G proteins and protein tyrosine kinases from sponge and Hydra. J. Mol. Evol., 48, 646-653.

    Google Scholar 

  • Suga, H., Ono, K. and Miyata, T. (1999c) Multiple TGF-beta receptor related genes in sponge and ancient gene duplications before the parazoan-eumetazoan split. FEBS Lett., 453, 346-350.

    Google Scholar 

  • Wagner, A. (1998) The fate of duplicated genes: loss or new function? BioEssays, 20, 785-788.

    Google Scholar 

  • Wang, Y. and Gu, X. (2000) Evolutionary patterns of gene families generated in the early stage of vertebrates. J. Mol. Evol., 51, 88-96.

    Google Scholar 

  • Wolfe, K.H. and Shields, D.C. (1997) Molecular evidence for an ancient duplication of the entire yeast genome. Nature, 387, 708-713.

    Google Scholar 

  • Wraith, A., Törnsten, A., Chardon, P., Harbitz, I., Chowdhary, B.P., Andersson, L., Lundin, L.-G. and Larhammar, D. (2000) Evolution of the neuropeptide Y receptor family: Gene and chromosome duplications deduced from the cloning and mapping of the five receptor subtype genes in pig. Genome Res., 10, 302-310.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Neuroscience, BMC, Uppsala University, S−751 24, Uppsala, Sweden

    Lars-Gustav Lundin, Dan Larhammar & Finn Hallböök

Authors
  1. Lars-Gustav Lundin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dan Larhammar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Finn Hallböök
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Lars-Gustav Lundin.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lundin, LG., Larhammar, D. & Hallböök, F. Numerous groups of chromosomal regional paralogies strongly indicate two genome doublings at the root of the vertebrates. J Struct Func Genom 3, 53–63 (2003). https://doi.org/10.1023/A:1022600813840

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1022600813840

Search

Navigation