Protein Subcellular Relocalization in the Evolution of Yeast Singleton and Duplicate Genes

Gene duplication is the primary source of new genes, but the mechanisms underlying the functional divergence and retention of duplicate genes are not well understood. Because eukaryotic proteins are localized to subcellular structures and localization can be altered by a single amino acid replacement, it was recently proposed that protein subcellular relocalization (PSR) plays an important role in the functional divergence and retention of duplicate genes. Although numerous examples of distinct subcellular localizations of paralogous proteins have been reported, it is unknown whether PSR occurs more frequently after gene duplication than without duplication. By analyzing experimentally determined and computationally predicted genome-wide protein subcellular localization data of the budding yeast Saccharomyces cerevisiae and two other fungi (Schizosaccharomyces pombe and Kluyveromyces waltii), we show that even singleton genes have an appreciable rate of relocalization in evolution and that duplicate genes do not relocalize more frequently than singletons. These results suggest that subcellular relocalization is unlikely to have been a major mechanism for duplicate gene retention and functional divergence at the genomic scale.

[1]  Jianzhi Zhang,et al.  Rapid Subfunctionalization Accompanied by Prolonged and Substantial Neofunctionalization in Duplicate Gene Evolution , 2005, Genetics.

[2]  Natalia Maltsev,et al.  Higher Gene Duplicabilities for Metabolic Proteins Than for Nonmetabolic Proteins in Yeast and E. coli , 2004, Journal of Molecular Evolution.

[3]  O. Pines,et al.  Single translation—dual destination: mechanisms of dual protein targeting in eukaryotes , 2005, EMBO reports.

[4]  Ronald W. Davis,et al.  Systematic screen for human disease genes in yeast , 2002, Nature Genetics.

[5]  Oliver Kohlbacher,et al.  MultiLoc: prediction of protein subcellular localization using N-terminal targeting sequences, sequence motifs and amino acid composition , 2006, Bioinform..

[6]  K. H. Wolfe,et al.  Divergence of spatial gene expression profiles following species-specific gene duplications in human and mouse. , 2004, Genome Research.

[7]  Jianzhi Zhang,et al.  Gene Complexity and Gene Duplicability , 2005, Current Biology.

[8]  Jianzhi Zhang,et al.  Higher duplicability of less important genes in yeast genomes. , 2006, Molecular biology and evolution.

[9]  Henrik Kaessmann,et al.  Mitochondrial Targeting Adaptation of the Hominoid-Specific Glutamate Dehydrogenase Driven by Positive Darwinian Selection , 2008, PLoS genetics.

[10]  Henrik Kaessmann,et al.  Birth and Rapid Subcellular Adaptation of a Hominoid-Specific CDC14 Protein , 2008, PLoS biology.

[11]  Kenneth H. Wolfe,et al.  Turning a hobby into a job: How duplicated genes find new functions , 2008, Nature Reviews Genetics.

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

[13]  Jianzhi Zhang,et al.  Null mutations in human and mouse orthologs frequently result in different phenotypes , 2008, Proceedings of the National Academy of Sciences.

[14]  B. Birren,et al.  Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae , 2004, Nature.

[15]  Zhiyong Lu,et al.  Proteome Analyst: custom predictions with explanations in a web-based tool for high-throughput proteome annotations , 2004, Nucleic Acids Res..

[16]  A. Stoltzfus.  On the Possibility of Constructive Neutral Evolution , 1999, Journal of Molecular Evolution.

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

[18]  Thomas Meitinger,et al.  MitoP2: the mitochondrial proteome database—now including mouse data , 2005, Nucleic Acids Res..

[19]  N. Friedman,et al.  Natural history and evolutionary principles of gene duplication in fungi , 2007, Nature.

[20]  Scott A. Rifkin,et al.  Duplicate genes increase gene expression diversity within and between species , 2004, Nature Genetics.

[21]  Yang Dai,et al.  An SVM-based system for predicting protein subnuclear localizations , 2005, BMC Bioinformatics.

[22]  Jianzhi Zhang.  Evolution by gene duplication: an update , 2003 .

[23]  E. O’Shea,et al.  Global analysis of protein expression in yeast , 2003, Nature.

[24]  A. Millar,et al.  What makes a mitochondrion? , 2003, Genome Biology.

[25]  D. Nicolae,et al.  Rapid divergence in expression between duplicate genes inferred from microarray data. , 2002, Trends in genetics : TIG.

[26]  N. Pfanner,et al.  The Mitochondrial Proteome: From Inventory to Function , 2008, Cell.

[27]  M. Robinson‐Rechavi,et al.  How confident can we be that orthologs are similar, but paralogs differ? , 2009, Trends in genetics : TIG.

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

[29]  Kuo-Chen Chou,et al.  Large‐scale plant protein subcellular location prediction , 2007, Journal of cellular biochemistry.

[30]  Paul Horton,et al.  Nucleic Acids Research Advance Access published May 21, 2007 WoLF PSORT: protein localization predictor , 2007 .

[31]  Henrik Kaessmann,et al.  Functional diversification of duplicate genes through subcellular adaptation of encoded proteins , 2008, Genome Biology.

[32]  Y. Hiraoka,et al.  ORFeome cloning and global analysis of protein localization in the fission yeast Schizosaccharomyces pombe , 2006, Nature Biotechnology.

[33]  E. O’Shea,et al.  Global analysis of protein localization in budding yeast , 2003, Nature.

[34]  M. Gerstein,et al.  Subcellular localization of the yeast proteome. , 2002, Genes & development.

[35]  R. Geeta,et al.  Protein subcellular relocalization: a new perspective on the origin of novel genes. , 2007, Trends in ecology & evolution.

[36]  Jenn-Kang Hwang,et al.  Prediction of protein subcellular localization , 2006, Proteins.

[37]  Chittibabu Guda,et al.  pTARGET: a web server for predicting protein subcellular localization , 2006, Nucleic Acids Res..

[38]  K. H. Wolfe,et al.  Molecular evidence for an ancient duplication of the entire yeast genome , 1997, Nature.