The odds of duplicate gene persistence after polyploidization

BackgroundGene duplication is an important biological phenomenon associated with genomic redundancy, degeneration, specialization, innovation, and speciation. After duplication, both copies continue functioning when natural selection favors duplicated protein function or expression, or when mutations make them functionally distinct before one copy is silenced.ResultsHere we quantify the degree to which genetic parameters related to gene expression, molecular evolution, and gene structure in a diploid frog - Silurana tropicalis - influence the odds of functional persistence of orthologous duplicate genes in a closely related tetraploid species - Xenopus laevis. Using public databases and 454 pyrosequencing, we obtained genetic and expression data from S. tropicalis orthologs of 3,387 X. laevis paralogs and 4,746 X. laevis singletons - the most comprehensive dataset for African clawed frogs yet analyzed. Using logistic regression, we demonstrate that the most important predictors of the odds of duplicate gene persistence in the tetraploid species are the total gene expression level and evenness of expression across tissues and development in the diploid species. Slow protein evolution and information density (fewer exons, shorter introns) in the diploid are also positively correlated with duplicate gene persistence in the tetraploid.ConclusionsOur findings suggest that a combination of factors contribute to duplicate gene persistence following whole genome duplication, but that the total expression level and evenness of expression across tissues and through development before duplication are most important. We speculate that these parameters are useful predictors of duplicate gene longevity after whole genome duplication in other taxa.

[1]  C. Pál,et al.  Highly expressed genes in yeast evolve slowly. , 2001, Genetics.

[2]  A. Riggs,et al.  Repositioning-dependent fate of duplicate genes. , 2005, DNA and cell biology.

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

[4]  Gregory S. Whitt,et al.  Evolution of the differential regulation of duplicate genes after polyploidization , 1979, Journal of Molecular Evolution.

[5]  Paul Richardson,et al.  Accelerated gene evolution and subfunctionalization in the pseudotetraploid frog Xenopus laevis , 2007, BMC Biology.

[6]  Wen-Hsiung Li,et al.  Mammalian housekeeping genes evolve more slowly than tissue-specific genes. , 2004, Molecular biology and evolution.

[7]  James A. Birchler,et al.  The gene balance hypothesis: implications for gene regulation, quantitative traits and evolution. , 2010, The New phytologist.

[8]  J. L. Cherry.  Expression Level, Evolutionary Rate, and the Cost of Expression , 2010, Genome biology and evolution.

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

[10]  A. Force,et al.  The probability of duplicate gene preservation by subfunctionalization. , 2000, Genetics.

[11]  D. Kahn,et al.  The Relationship among Gene Expression, the Evolution of Gene Dosage, and the Rate of Protein Evolution , 2010, PLoS genetics.

[12]  Sudhir Kumar,et al.  Gene Expression Intensity Shapes Evolutionary Rates of the Proteins Encoded by the Vertebrate Genome , 2004, Genetics.

[13]  A. Sidow.  Gen(om)e duplications in the evolution of early vertebrates. , 1996, Current opinion in genetics & development.

[14]  Brian C. Thomas,et al.  Following tetraploidy in an Arabidopsis ancestor, genes were removed preferentially from one homeolog leaving clusters enriched in dose-sensitive genes. , 2006, Genome research.

[15]  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.

[16]  O. Jaillon,et al.  Gene loss and evolutionary rates following whole-genome duplication in teleost fishes. , 2006, Molecular biology and evolution.

[17]  X. Gu,et al.  A preliminary analysis of gene pleiotropy estimated from protein sequences. , 2010, Journal of experimental zoology. Part B, Molecular and developmental evolution.

[18]  B. J. Evans,et al.  Genome evolution and speciation genetics of clawed frogs (Xenopus and Silurana). , 2008, Frontiers in bioscience : a journal and virtual library.

[19]  Dmitri A Petrov,et al.  Do disparate mechanisms of duplication add similar genes to the genome? , 2005, Trends in genetics : TIG.

[20]  Jeroen Raes,et al.  Nonrandom divergence of gene expression following gene and genome duplications in the flowering plant Arabidopsis thaliana , 2006, Genome Biology.

[21]  Andrew H Paterson,et al.  Buffering of crucial functions by paleologous duplicated genes may contribute cyclicality to angiosperm genome duplication. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[22]  Adam J. Bewick,et al.  EVOLUTION OF THE CLOSELY RELATED, SEX‐RELATED GENES DM‐W AND DMRT1 IN AFRICAN CLAWED FROGS (XENOPUS) , 2011, Evolution; international journal of organic evolution.

[23]  K. Hastings.  Strong evolutionary conservation of broadly expressed protein isoforms in the troponin I gene family and other vertebrate gene families , 1996, Journal of Molecular Evolution.

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

[25]  S. Yi,et al.  Correlated asymmetry of sequence and functional divergence between duplicate proteins of Saccharomyces cerevisiae. , 2006, Molecular biology and evolution.

[26]  L. Duret,et al.  Determinants of substitution rates in mammalian genes: expression pattern affects selection intensity but not mutation rate. , 2000, Molecular biology and evolution.

[27]  David Sankoff,et al.  The collapse of gene complement following whole genome duplication , 2010, BMC Genomics.

[28]  Brian C. Thomas,et al.  Gene-balanced duplications, like tetraploidy, provide predictable drive to increase morphological complexity. , 2006, Genome research.

[29]  K. H. Wolfe,et al.  Preferential subfunctionalization of slow-evolving genes after allopolyploidization in Xenopus laevis , 2008, Proceedings of the National Academy of Sciences.

[30]  N. Barkai,et al.  Comparative analysis indicates regulatory neofunctionalization of yeast duplicates , 2007, Genome Biology.

[31]  R. Guigó,et al.  Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia , 2006, Nature.

[32]  Takashi Makino,et al.  Ohnologs in the human genome are dosage balanced and frequently associated with disease , 2010, Proceedings of the National Academy of Sciences.

[33]  Frédéric J. J. Chain,et al.  Duplicate gene evolution and expression in the wake of vertebrate allopolyploidization , 2008, BMC Evolutionary Biology.

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

[35]  David L Robertson,et al.  All duplicates are not equal: the difference between small-scale and genome duplication , 2007, Genome Biology.

[36]  Ziheng Yang,et al.  PAML: a program package for phylogenetic analysis by maximum likelihood , 1997, Comput. Appl. Biosci..

[37]  A. Su,et al.  Gene expression evolves faster in narrowly than in broadly expressed mammalian genes. , 2005, Molecular biology and evolution.

[38]  Robert C. Edgar,et al.  MUSCLE: multiple sequence alignment with high accuracy and high throughput. , 2004, Nucleic acids research.

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

[40]  Andrew Ying-Fei Chang,et al.  Maintenance of duplicate genes and their functional redundancy by reduced expression. , 2010, Trends in genetics : TIG.

[41]  D. Petrov,et al.  Preferential Duplication of Conserved Proteins in Eukaryotic Genomes , 2004, PLoS biology.

[42]  W. Haerty,et al.  Ontogeny and phylogeny: molecular signatures of selection, constraint, and temporal pleiotropy in the development of Drosophila , 2009, BMC Biology.

[43]  Patrick C Phillips,et al.  ALLELIC DIVERGENCE PRECEDES AND PROMOTES GENE DUPLICATION , 2006, Evolution; international journal of organic evolution.

[44]  Russell B. Fletcher,et al.  The Genome of the Western Clawed Frog Xenopus tropicalis , 2010, Science.

[45]  S. Mane,et al.  Contrasting patterns of evolution following whole genome versus tandem duplication events in Populus. , 2012, Genome research.

[46]  Steven Maere,et al.  The gain and loss of genes during 600 million years of vertebrate evolution , 2006, Genome Biology.

[47]  Y Van de Peer,et al.  Genome duplication, divergent resolution and speciation. , 2001, Trends in genetics : TIG.

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

[49]  D. Kelley,et al.  A mitochondrial DNA phylogeny of African clawed frogs: phylogeography and implications for polyploid evolution. , 2004, Molecular phylogenetics and evolution.

[50]  Dmitri A. Petrov,et al.  Pervasive and Persistent Redundancy among Duplicated Genes in Yeast , 2008, PLoS genetics.

[51]  C. Pál,et al.  Dosage sensitivity and the evolution of gene families in yeast , 2003, Nature.

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

[53]  I. Gitelman.  Evolution of the vertebrate twist family and synfunctionalization: a mechanism for differential gene loss through merging of expression domains. , 2007, Molecular biology and evolution.

[54]  Wenfeng Qian,et al.  Gene Dosage and Gene Duplicability , 2008, Genetics.

[55]  Frédéric J. J. Chain,et al.  Multiple Mechanisms Promote the Retained Expression of Gene Duplicates in the Tetraploid Frog Xenopus laevis , 2006, PLoS genetics.

[56]  D. Liberles,et al.  Subfunctionalization of duplicated genes as a transition state to neofunctionalization , 2005, BMC Evolutionary Biology.

[57]  Sarah Barber,et al.  Sequencing and analysis of 10,967 full-length cDNA clones from Xenopus laevis and Xenopus tropicalis reveals post-tetraploidization transcriptome remodeling. , 2006, Genome research.

[58]  X. Gu,et al.  Tissue-driven hypothesis of genomic evolution and sequence-expression correlations , 2007, Proceedings of the National Academy of Sciences.

[59]  J. Chris Pires,et al.  Gene and genome duplications: the impact of dosage-sensitivity on the fate of nuclear genes , 2009, Chromosome Research.

[60]  T J Gibson,et al.  Genetic redundancy in vertebrates: polyploidy and persistence of genes encoding multidomain proteins. , 1998, Trends in genetics : TIG.