Abstract
The significance of gene duplication in provisioning raw materials for the evolution of genomic diversity is widely recognized, but the early evolutionary dynamics of duplicate genes remain obscure. To elucidate the structural characteristics of newly arisen gene duplicates at infancy and their subsequent evolutionary properties, we analyzed gene pairs with < or =10% divergence at synonymous sites within the genome of Caenorhabditis elegans. Structural heterogeneity between duplicate copies is present very early in their evolutionary history and is maintained over longer evolutionary timescales, suggesting that duplications across gene boundaries in conjunction with shuffling events have at least as much potential to contribute to long-term evolution as do fully redundant (complete) duplicates. The median duplication span of 1.4 kb falls short of the average gene length in C. elegans (2.5 kb), suggesting that partial gene duplications are frequent. Most gene duplicates reside close to the parent copy at inception, often as tandem inverted loci, and appear to disperse in the genome as they age, as a result of reduced survivorship of duplicates located in proximity to the ancestral copy. We propose that illegitimate recombination events leading to inverted duplications play a disproportionately large role in gene duplication within this genome in comparison with other mechanisms.
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- Achaz G., Coissac E., Viari A., Netter P. Analysis of intrachromosomal duplications in yeast Saccharomyces cerevisiae: a possible model for their origin. Mol Biol Evol. 2000 Aug;17(8):1268–1275. doi: 10.1093/oxfordjournals.molbev.a026410. [DOI] [PubMed] [Google Scholar]
- Achaz G., Netter P., Coissac E. Study of intrachromosomal duplications among the eukaryote genomes. Mol Biol Evol. 2001 Dec;18(12):2280–2288. doi: 10.1093/oxfordjournals.molbev.a003774. [DOI] [PubMed] [Google Scholar]
- Anderson R. P., Roth J. R. Tandem genetic duplications in phage and bacteria. Annu Rev Microbiol. 1977;31:473–505. doi: 10.1146/annurev.mi.31.100177.002353. [DOI] [PubMed] [Google Scholar]
- Bae Y. S., Kawasaki I., Ikeda H., Liu L. F. Illegitimate recombination mediated by calf thymus DNA topoisomerase II in vitro. Proc Natl Acad Sci U S A. 1988 Apr;85(7):2076–2080. doi: 10.1073/pnas.85.7.2076. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Begun D. J. Origin and evolution of a new gene descended from alcohol dehydrogenase in Drosophila. Genetics. 1997 Feb;145(2):375–382. doi: 10.1093/genetics/145.2.375. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chen L., DeVries A. L., Cheng C. H. Evolution of antifreeze glycoprotein gene from a trypsinogen gene in Antarctic notothenioid fish. Proc Natl Acad Sci U S A. 1997 Apr 15;94(8):3811–3816. doi: 10.1073/pnas.94.8.3811. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Coghlan Avril, Wolfe Kenneth H. Fourfold faster rate of genome rearrangement in nematodes than in Drosophila. Genome Res. 2002 Jun;12(6):857–867. doi: 10.1101/gr.172702. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cohen S., Hassin D., Karby S., Lavi S. Hairpin structures are the primary amplification products: a novel mechanism for generation of inverted repeats during gene amplification. Mol Cell Biol. 1994 Dec;14(12):7782–7791. doi: 10.1128/mcb.14.12.7782. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Drouin Guy. Characterization of the gene conversions between the multigene family members of the yeast genome. J Mol Evol. 2002 Jul;55(1):14–23. doi: 10.1007/s00239-001-0085-y. [DOI] [PubMed] [Google Scholar]
- Dunham I., Shimizu N., Roe B. A., Chissoe S., Hunt A. R., Collins J. E., Bruskiewich R., Beare D. M., Clamp M., Smink L. J. The DNA sequence of human chromosome 22. Nature. 1999 Dec 2;402(6761):489–495. doi: 10.1038/990031. [DOI] [PubMed] [Google Scholar]
- Duret L., Mouchiroud D. Expression pattern and, surprisingly, gene length shape codon usage in Caenorhabditis, Drosophila, and Arabidopsis. Proc Natl Acad Sci U S A. 1999 Apr 13;96(8):4482–4487. doi: 10.1073/pnas.96.8.4482. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fischer G., Neuvéglise C., Durrens P., Gaillardin C., Dujon B. Evolution of gene order in the genomes of two related yeast species. Genome Res. 2001 Dec;11(12):2009–2019. doi: 10.1101/gr.212701. [DOI] [PubMed] [Google Scholar]
- Force A., Lynch M., Pickett F. B., Amores A., Yan Y. L., Postlethwait J. Preservation of duplicate genes by complementary, degenerative mutations. Genetics. 1999 Apr;151(4):1531–1545. doi: 10.1093/genetics/151.4.1531. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Galitski T., Roth J. R. Pathways for homologous recombination between chromosomal direct repeats in Salmonella typhimurium. Genetics. 1997 Jul;146(3):751–767. doi: 10.1093/genetics/146.3.751. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gilley J., Fried M. Extensive gene order differences within regions of conserved synteny between the Fugu and human genomes: implications for chromosomal evolution and the cloning of disease genes. Hum Mol Genet. 1999 Jul;8(7):1313–1320. doi: 10.1093/hmg/8.7.1313. [DOI] [PubMed] [Google Scholar]
- Gordon A. J., Halliday J. A. Inversions with deletions and duplications. Genetics. 1995 May;140(1):411–414. doi: 10.1093/genetics/140.1.411. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gu Zhenglong, Steinmetz Lars M., Gu Xun, Scharfe Curt, Davis Ronald W., Li Wen-Hsiung. Role of duplicate genes in genetic robustness against null mutations. Nature. 2003 Jan 2;421(6918):63–66. doi: 10.1038/nature01198. [DOI] [PubMed] [Google Scholar]
- Harrison P. M., Echols N., Gerstein M. B. Digging for dead genes: an analysis of the characteristics of the pseudogene population in the Caenorhabditis elegans genome. Nucleic Acids Res. 2001 Feb 1;29(3):818–830. doi: 10.1093/nar/29.3.818. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Higgins D. G., Bleasby A. J., Fuchs R. CLUSTAL V: improved software for multiple sequence alignment. Comput Appl Biosci. 1992 Apr;8(2):189–191. doi: 10.1093/bioinformatics/8.2.189. [DOI] [PubMed] [Google Scholar]
- Holt Suzan J., Cress William A., Van Staden Johannes. Evidence for dynamic alteration in histone gene clusters of Caenorhabditis elegans: a topoisomerase II connection? Genet Res. 2002 Feb;79(1):11–22. doi: 10.1017/s0016672301005390. [DOI] [PubMed] [Google Scholar]
- Hughes A. L. The evolution of functionally novel proteins after gene duplication. Proc Biol Sci. 1994 May 23;256(1346):119–124. doi: 10.1098/rspb.1994.0058. [DOI] [PubMed] [Google Scholar]
- Hyrien O., Debatisse M., Buttin G., de Saint Vincent B. R. The multicopy appearance of a large inverted duplication and the sequence at the inversion joint suggest a new model for gene amplification. EMBO J. 1988 Feb;7(2):407–417. doi: 10.1002/j.1460-2075.1988.tb02828.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kimura M., King J. L. Fixation of a deleterious allele at one of two "duplicate" loci by mutation pressure and random drift. Proc Natl Acad Sci U S A. 1979 Jun;76(6):2858–2861. doi: 10.1073/pnas.76.6.2858. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Krakauer D. C., Nowak M. A. Evolutionary preservation of redundant duplicated genes. Semin Cell Dev Biol. 1999 Oct;10(5):555–559. doi: 10.1006/scdb.1999.0337. [DOI] [PubMed] [Google Scholar]
- Lercher Martin J., Blumenthal Thomas, Hurst Laurence D. Coexpression of neighboring genes in Caenorhabditis elegans is mostly due to operons and duplicate genes. Genome Res. 2003 Feb;13(2):238–243. doi: 10.1101/gr.553803. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lin C. T., Lin W. H., Lyu Y. L., Whang-Peng J. Inverted repeats as genetic elements for promoting DNA inverted duplication: implications in gene amplification. Nucleic Acids Res. 2001 Sep 1;29(17):3529–3538. doi: 10.1093/nar/29.17.3529. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Llorente B., Malpertuy A., Neuvéglise C., de Montigny J., Aigle M., Artiguenave F., Blandin G., Bolotin-Fukuhara M., Bon E., Brottier P. Genomic exploration of the hemiascomycetous yeasts: 18. Comparative analysis of chromosome maps and synteny with Saccharomyces cerevisiae. FEBS Lett. 2000 Dec 22;487(1):101–112. doi: 10.1016/s0014-5793(00)02289-4. [DOI] [PubMed] [Google Scholar]
- Long M., Langley C. H. Natural selection and the origin of jingwei, a chimeric processed functional gene in Drosophila. Science. 1993 Apr 2;260(5104):91–95. doi: 10.1126/science.7682012. [DOI] [PubMed] [Google Scholar]
- Lootens S., Burnett J., Friedman T. B. An intraspecific gene duplication polymorphism of the urate oxidase gene of Drosophila virilis: a genetic and molecular analysis. Mol Biol Evol. 1993 May;10(3):635–646. doi: 10.1093/oxfordjournals.molbev.a040028. [DOI] [PubMed] [Google Scholar]
- Lovett S. T., Gluckman T. J., Simon P. J., Sutera V. A., Jr, Drapkin P. T. Recombination between repeats in Escherichia coli by a recA-independent, proximity-sensitive mechanism. Mol Gen Genet. 1994 Nov 1;245(3):294–300. doi: 10.1007/BF00290109. [DOI] [PubMed] [Google Scholar]
- Lyckegaard E. M., Clark A. G. Ribosomal DNA and Stellate gene copy number variation on the Y chromosome of Drosophila melanogaster. Proc Natl Acad Sci U S A. 1989 Mar;86(6):1944–1948. doi: 10.1073/pnas.86.6.1944. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lynch M., Conery J. S. The evolutionary fate and consequences of duplicate genes. Science. 2000 Nov 10;290(5494):1151–1155. doi: 10.1126/science.290.5494.1151. [DOI] [PubMed] [Google Scholar]
- Lynch M., Force A. The probability of duplicate gene preservation by subfunctionalization. Genetics. 2000 Jan;154(1):459–473. doi: 10.1093/genetics/154.1.459. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lynch M., O'Hely M., Walsh B., Force A. The probability of preservation of a newly arisen gene duplicate. Genetics. 2001 Dec;159(4):1789–1804. doi: 10.1093/genetics/159.4.1789. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Maroni G., Wise J., Young J. E., Otto E. Metallothionein gene duplications and metal tolerance in natural populations of Drosophila melanogaster. Genetics. 1987 Dec;117(4):739–744. doi: 10.1093/genetics/117.4.739. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nowak M. A., Boerlijst M. C., Cooke J., Smith J. M. Evolution of genetic redundancy. Nature. 1997 Jul 10;388(6638):167–171. doi: 10.1038/40618. [DOI] [PubMed] [Google Scholar]
- Nurminsky D. I., Nurminskaya M. V., De Aguiar D., Hartl D. L. Selective sweep of a newly evolved sperm-specific gene in Drosophila. Nature. 1998 Dec 10;396(6711):572–575. doi: 10.1038/25126. [DOI] [PubMed] [Google Scholar]
- Ohta T. Simulating evolution by gene duplication. Genetics. 1987 Jan;115(1):207–213. doi: 10.1093/genetics/115.1.207. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ohta T. Time for acquiring a new gene by duplication. Proc Natl Acad Sci U S A. 1988 May;85(10):3509–3512. doi: 10.1073/pnas.85.10.3509. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Passananti C., Davies B., Ford M., Fried M. Structure of an inverted duplication formed as a first step in a gene amplification event: implications for a model of gene amplification. EMBO J. 1987 Jun;6(6):1697–1703. doi: 10.1002/j.1460-2075.1987.tb02420.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Patthy L. Evolution of the proteases of blood coagulation and fibrinolysis by assembly from modules. Cell. 1985 Jul;41(3):657–663. doi: 10.1016/s0092-8674(85)80046-5. [DOI] [PubMed] [Google Scholar]
- Petes T. D., Hill C. W. Recombination between repeated genes in microorganisms. Annu Rev Genet. 1988;22:147–168. doi: 10.1146/annurev.ge.22.120188.001051. [DOI] [PubMed] [Google Scholar]
- Rubin G. M., Yandell M. D., Wortman J. R., Gabor Miklos G. L., Nelson C. R., Hariharan I. K., Fortini M. E., Li P. W., Apweiler R., Fleischmann W. Comparative genomics of the eukaryotes. Science. 2000 Mar 24;287(5461):2204–2215. doi: 10.1126/science.287.5461.2204. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sawyer S. Statistical tests for detecting gene conversion. Mol Biol Evol. 1989 Sep;6(5):526–538. doi: 10.1093/oxfordjournals.molbev.a040567. [DOI] [PubMed] [Google Scholar]
- Semple C., Wolfe K. H. Gene duplication and gene conversion in the Caenorhabditis elegans genome. J Mol Evol. 1999 May;48(5):555–564. doi: 10.1007/pl00006498. [DOI] [PubMed] [Google Scholar]
- Smith J. M. Analyzing the mosaic structure of genes. J Mol Evol. 1992 Feb;34(2):126–129. doi: 10.1007/BF00182389. [DOI] [PubMed] [Google Scholar]
- Stein L., Sternberg P., Durbin R., Thierry-Mieg J., Spieth J. WormBase: network access to the genome and biology of Caenorhabditis elegans. Nucleic Acids Res. 2001 Jan 1;29(1):82–86. doi: 10.1093/nar/29.1.82. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Takahata N., Maruyama T. Polymorphism and loss of duplicate gene expression: a theoretical study with application of tetraploid fish. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4521–4525. doi: 10.1073/pnas.76.9.4521. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Theodore L., Ho A. S., Maroni G. Recent evolutionary history of the metallothionein gene Mtn in Drosophila. Genet Res. 1991 Dec;58(3):203–210. doi: 10.1017/s0016672300029955. [DOI] [PubMed] [Google Scholar]
- Thomson T. M., Lozano J. J., Loukili N., Carrió R., Serras F., Cormand B., Valeri M., Díaz V. M., Abril J., Burset M. Fusion of the human gene for the polyubiquitination coeffector UEV1 with Kua, a newly identified gene. Genome Res. 2000 Nov;10(11):1743–1756. doi: 10.1101/gr.gr-1405r. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Vellai T., Vida G. The origin of eukaryotes: the difference between prokaryotic and eukaryotic cells. Proc Biol Sci. 1999 Aug 7;266(1428):1571–1577. doi: 10.1098/rspb.1999.0817. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Walsh J. B. How often do duplicated genes evolve new functions? Genetics. 1995 Jan;139(1):421–428. doi: 10.1093/genetics/139.1.421. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Watterson G. A. On the time for gene silencing at duplicate Loci. Genetics. 1983 Nov;105(3):745–766. doi: 10.1093/genetics/105.3.745. [DOI] [PMC free article] [PubMed] [Google Scholar]