Duplication and Gene Conversion in the Drosophila melanogaster Genome

Using the genomic sequences of Drosophila melanogaster subgroup, the pattern of gene duplications was investigated with special attention to interlocus gene conversion. Our fine-scale analysis with careful visual inspections enabled accurate identification of a number of duplicated blocks (genomic regions). The orthologous parts of those duplicated blocks were also identified in the D. simulans and D. sechellia genomes, by which we were able to clearly classify the duplicated blocks into post- and pre-speciation blocks. We found 31 post-speciation duplicated genes, from which the rate of gene duplication (from one copy to two copies) is estimated to be 1.0×10−9 per single-copy gene per year. The role of interlocus gene conversion was observed in several respects in our data: (1) synonymous divergence between a duplicated pair is overall very low. Consequently, the gene duplication rate would be seriously overestimated by counting duplicated genes with low divergence; (2) the sizes of young duplicated blocks are generally large. We postulate that the degeneration of gene conversion around the edges could explain the shrinkage of “identifiable” duplicated regions; and (3) elevated paralogous divergence is observed around the edges in many duplicated blocks, supporting our gene conversion–degeneration model. Our analysis demonstrated that gene conversion between duplicated regions is a common and genome-wide phenomenon in the Drosophila genomes, and that its role should be especially significant in the early stages of duplicated genes. Based on a population genetic prediction, we applied a new genome-scan method to test for signatures of selection for neofunctionalization and found a strong signature in a pair of transporter genes.

[1]  Dr. Susumu Ohno Evolution by Gene Duplication , 1970, Springer Berlin Heidelberg.

[2]  Stephen M. Mount,et al.  The genome sequence of Drosophila melanogaster. , 2000, Science.

[3]  T. Ohta Evolution And Variation Of Multigene Families , 1981 .

[4]  Sudhir Kumar,et al.  MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment , 2004, Briefings Bioinform..

[5]  C. Ponting,et al.  Evolutionary rate analyses of orthologs and paralogs from 12 Drosophila genomes. , 2007, Genome research.

[6]  Colin N. Dewey,et al.  Discovery of functional elements in 12 Drosophila genomes using evolutionary signatures , 2007, Nature.

[7]  Naruya Saitou,et al.  Genome-Wide Search of Gene Conversions in Duplicated Genes of Mouse and Rat , 2006 .

[8]  N. Bianchi,et al.  Evolution of the Zfx and Zfy genes: rates and interdependence between the genes. , 1993, Molecular biology and evolution.

[9]  H. Shibata,et al.  Evolutionary relationships and sequence variation of alpha-amylase variants encoded by duplicated genes in the Amy locus of Drosophila melanogaster. , 1995, Genetics.

[10]  D. Petrov,et al.  High intrinsic rate of DNA loss in Drosophila , 1996, Nature.

[11]  J. Roman Arguello,et al.  Origination of an X-Linked Testes Chimeric Gene by Illegitimate Recombination in Drosophila , 2006, PLoS genetics.

[12]  Melanie A. Huntley,et al.  Evolution of genes and genomes on the Drosophila phylogeny , 2007, Nature.

[13]  Kenneth H. Wolfe,et al.  Gene Duplication and Gene Conversion in the Caenorhabditis elegans Genome , 1999, Journal of Molecular Evolution.

[14]  E. Koonin,et al.  Selection in the evolution of gene duplications , 2002, Genome Biology.

[15]  H. Innan The coalescent and infinite-site model of a small multigene family. , 2003, Genetics.

[16]  M. Kimura A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences , 1980, Journal of Molecular Evolution.

[17]  Justin O. Borevitz,et al.  Natural Selection Shapes Genome-Wide Patterns of Copy-Number Polymorphism in Drosophila melanogaster , 2008, Science.

[18]  V. Bryson,et al.  Evolving Genes and Proteins. , 1965, Science.

[19]  H. Innan A two-locus gene conversion model with selection and its application to the human RHCE and RHD genes , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[20]  J. Thompson,et al.  The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. , 1997, Nucleic acids research.

[21]  Wen-Hsiung Li Unbiased estimation of the rates of synonymous and nonsynonymous substitution , 2006, Journal of Molecular Evolution.

[22]  Hideki Innan,et al.  Very Low Gene Duplication Rate in the Yeast Genome , 2004, Science.

[23]  Z. Gu,et al.  Different evolutionary patterns between young duplicate genes in the human genome , 2003, Genome Biology.

[24]  J. Crow Genetics of Insect Resistance to Chemicals , 1957 .

[25]  Masatoshi Nei,et al.  Evolution of genes and proteins. , 1983 .

[26]  Hideki Innan,et al.  The Effect of Gene Conversion on the Divergence Between Duplicated Genes , 2004, Genetics.

[27]  G. Dover,et al.  Molecular drive: a cohesive mode of species evolution , 1982, Nature.

[28]  Victor B. Strelets,et al.  FlyBase: anatomical data, images and queries , 2005, Nucleic Acids Res..

[29]  A. Hughes,et al.  Evolution of duplicate genes in a tetraploid animal, Xenopus laevis. , 1993, Molecular biology and evolution.

[30]  Mira V. Han,et al.  Gene Family Evolution across 12 Drosophila Genomes , 2007, PLoS genetics.

[31]  Kosuke M. Teshima,et al.  Neofunctionalization of Duplicated Genes Under the Pressure of Gene Conversion , 2008, Genetics.

[32]  T Ohta,et al.  Allelic and nonallelic homology of a supergene family. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[33]  Xin Li,et al.  Repetitive Element-Mediated Recombination as a Mechanism for New Gene Origination in Drosophila , 2007, PLoS genetics.

[34]  F. Tajima,et al.  Simple methods for testing the molecular evolutionary clock hypothesis. , 1993, Genetics.

[35]  H. Innan A method for estimating the mutation, gene conversion and recombination parameters in small multigene families. , 2002, Genetics.

[36]  Deng Pan,et al.  Quantifying the major mechanisms of recent gene duplications in the human and mouse genomes: a novel strategy to estimate gene duplication rates , 2007, Genome Biology.

[37]  B. Birren,et al.  Sequencing and comparison of yeast species to identify genes and regulatory elements , 2003, Nature.

[38]  L. Fulton,et al.  Finding Functional Features in Saccharomyces Genomes by Phylogenetic Footprinting , 2003, Science.

[39]  T. Petes,et al.  Recombination between repeated genes in microorganisms. , 1988, Annual review of genetics.

[40]  M. Nei,et al.  Molecular phylogeny and divergence times of drosophilid species. , 1995, Molecular biology and evolution.

[41]  M. Ashburner,et al.  Relationships within the melanogaster species subgroup of the genus Drosophila (Sophophora) - II. Phylogenetic relationships between six species based upon polytene chromosome banding sequences , 1976, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[42]  P. C. Wensink,et al.  A comparison of the ribosomal DNA's of Xenopus laevis and Xenopus mulleri: the evolution of tandem genes. , 1972, Journal of molecular biology.

[43]  Anna-Sophie Fiston-Lavier,et al.  A model of segmental duplication formation in Drosophila melanogaster. , 2007, Genome research.

[44]  M. Lynch,et al.  The evolutionary fate and consequences of duplicate genes. , 2000, Science.

[45]  Kevin R. Thornton,et al.  Excess of amino acid substitutions relative to polymorphism between X-linked duplications in Drosophila melanogaster. , 2004, Molecular biology and evolution.

[46]  I. Paulsen,et al.  Major Facilitator Superfamily , 1998, Microbiology and Molecular Biology Reviews.

[47]  Guy Drouin,et al.  Characterization of the Gene Conversions Between the Multigene Family Members of the Yeast Genome , 2002, Journal of Molecular Evolution.

[48]  J. Hein,et al.  The coalescent with gene conversion. , 2000, Genetics.

[49]  Y. Kan,et al.  Rapid duplication and loss of genes coding for the alpha chains of hemoglobin. , 1980, Proceedings of the National Academy of Sciences of the United States of America.

[50]  Eugene V Koonin,et al.  A common framework for understanding the origin of genetic dominance and evolutionary fates of gene duplications. , 2004, Trends in genetics : TIG.

[51]  Z. Gu,et al.  Extent of gene duplication in the genomes of Drosophila, nematode, and yeast. , 2002, Molecular biology and evolution.