Duplication-degeneration as a mechanism of gene fission and the origin of new genes in Drosophila species

Gene fission and fusion, the processes by which a single gene is split into two separate genes and two adjacent genes are fused into a single gene, respectively, are among the primary processes that generate new genes. Despite their seeming reversibility, nothing is known about the mechanism of gene fission. Because the nucleotide sequences of fission genes record little about their origination process, conventional analysis of duplicate genes may not be powerful enough to unravel the underlying mechanism. In a survey for young genes in species of the Drosophila melanogaster subgroup using fluorescence in situ hybridization, we identified a young gene family, monkey king, whose genesis sheds light on the evolutionary process of gene fission. Its members originated 1–2 million years ago as retroposed duplicates and evolved into fission genes that separately encode protein domains from a multidomain ancestor. The mechanism underlying this process is gene duplication with subsequent partial degeneration.

[1]  L. Hellman,et al.  Isolation of cDNA clones for 42 different Krüppel-related zinc finger proteins expressed in the human monoblast cell line U-937. , 1995, DNA and cell biology.

[2]  A. J. Schroeder,et al.  The FlyBase database of the Drosophila Genome Projects and community literature. , 2002, Nucleic acids research.

[3]  M. Long,et al.  Natural selection and the origin of jingwei, a chimeric processed functional gene in Drosophila. , 1993, Science.

[4]  D. Hartl,et al.  Selective sweep of a newly evolved sperm-specific gene in Drosophila , 1998, Nature.

[5]  J. Volff,et al.  Subfunctionalization of duplicate mitf genes associated with differential degeneration of alternative exons in fish. , 2002, Genetics.

[6]  F. Lemeunier,et al.  Evolutionary novelties in islands: Drosophila santomea, a new melanogaster sister species from São Tomé , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[7]  A. Force,et al.  Preservation of duplicate genes by complementary, degenerative mutations. , 1999, Genetics.

[8]  Anton J. Enright,et al.  Protein interaction maps for complete genomes based on gene fusion events , 1999, Nature.

[9]  M. Long,et al.  The origin of the Jingwei gene and the complex modular structure of its parental gene, yellow emperor, in Drosophila melanogaster. , 2000, Molecular biology and evolution.

[10]  Sudhir Kumar,et al.  MEGA2: molecular evolutionary genetics analysis software , 2001, Bioinform..

[11]  J. Rogers,et al.  The origin and evolution of retroposons. , 1985, International review of cytology.

[12]  B. Snel,et al.  Genome evolution. Gene fusion versus gene fission. , 2000, Trends in Genetics.

[13]  J. Stone,et al.  Rapid evolution of cis-regulatory sequences via local point mutations. , 2001, Molecular biology and evolution.

[14]  Julio Rozas,et al.  DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis , 1999, Bioinform..

[15]  Josep M. Comeron,et al.  K-Estimator: calculation of the number of nucleotide substitutions per site and the confidence intervals , 1999, Bioinform..

[16]  W. Gelbart.  The FlyBase database of the Drosophila genome projects and community literature. , 2002, Nucleic acids research.

[17]  W. Li,et al.  Statistical tests of neutrality of mutations. , 1993, Genetics.

[18]  J. Brosius,et al.  Many G-protein-coupled receptors are encoded by retrogenes. , 1999, Trends in genetics : TIG.

[19]  R. Guigó,et al.  Fusion of the human gene for the polyubiquitination coeffector UEV1 with Kua, a newly identified gene. , 2000, Genome research.

[20]  Jeffrey R. Powell,et al.  Progress and Prospects in Evolutionary Biology: The Drosophila Model , 1997 .

[21]  F. Tajima.  Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. , 1989, Genetics.

[22]  J. Brosius,et al.  Retroposons--seeds of evolution. , 1991, Science.

[23]  Kevin R. Thornton,et al.  The origin of new genes: glimpses from the young and old , 2003, Nature Reviews Genetics.

[24]  Wen-Hsiung Li,et al.  The K(A)/K(S) ratio test for assessing the protein-coding potential of genomic regions: an empirical and simulation study. , 2002, Genome research.

[25]  A. Hughes.  The evolution of functionally novel proteins after gene duplication , 1994, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[26]  Justin C. Fay,et al.  Hitchhiking under positive Darwinian selection. , 2000, Genetics.

[27]  P. Zaphiropoulos,et al.  The human cytochrome P450 3A locus. Gene evolution by capture of downstream exons. , 2000, Gene.

[28]  E. Nevo,et al.  Origin of sphinx, a young chimeric RNA gene in Drosophila melanogaster , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[29]  M. Kreitman,et al.  Adaptive protein evolution at the Adh locus in Drosophila , 1991, Nature.