Old genes experience stronger translational selection than young genes.

Selection on synonymous codon usage for translation efficiency and/or accuracy has been identified as a widespread mechanism in many living organisms. However, it remains unknown whether translational selection associates closely with gene age and acts differentially on genes with different evolutionary ages. To address this issue, here we investigate the strength of translational selection acting on different aged genes in human. Our results show that old genes present stronger translational selection than young genes, demonstrating that translational selection correlates positively with gene age. We further explore the difference of translational selection in duplicates vs. singletons and in housekeeping vs. tissue-specific genes. We find that translational selection acts comparably in old singletons and old duplicates and stronger translational selection in old genes is contributed primarily by housekeeping genes. For young genes, contrastingly, singletons experience stronger translational selection than duplicates, presumably due to redundant function of duplicated genes during their early evolutionary stage. Taken together, our results indicate that translational selection acting on a gene would not be constant during all stages of evolution, associating closely with gene age.

[1]  Arnold J Levine,et al.  Tissue-specific codon usage and the expression of human genes. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

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

[3]  Z. Yang,et al.  Substitution rates in Drosophila nuclear genes: implications for translational selection. , 2001, Genetics.

[4]  W. Gu,et al.  Selection on synonymous sites for increased accessibility around miRNA binding sites in plants. , 2012, Molecular biology and evolution.

[5]  J. Plotkin,et al.  Synonymous but not the same: the causes and consequences of codon bias , 2011, Nature Reviews Genetics.

[6]  S. Teichmann,et al.  Gene regulatory network growth by duplication , 2004, Nature Genetics.

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

[8]  Sridhar Hannenhalli,et al.  Young proteins experience more variable selection pressures than old proteins. , 2010, Genome research.

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

[10]  Peer Bork,et al.  Younger Genes Are Less Likely to Be Essential than Older Genes, and Duplicates Are Less Likely to Be Essential than Singletons of the Same Age , 2012, Molecular biology and evolution.

[11]  Tao Pan,et al.  Tissue-Specific Differences in Human Transfer RNA Expression , 2006, PLoS genetics.

[12]  H. Akashi.  Synonymous codon usage in Drosophila melanogaster: natural selection and translational accuracy. , 1994, Genetics.

[13]  Ruth Hershberg,et al.  Selection on codon bias. , 2008, Annual review of genetics.

[14]  Anushya Muruganujan,et al.  PANTHER in 2013: modeling the evolution of gene function, and other gene attributes, in the context of phylogenetic trees , 2012, Nucleic Acids Res..

[15]  J. McInerney,et al.  Translational selection frequently overcomes genetic drift in shaping synonymous codon usage patterns in vertebrates. , 2013, Molecular biology and evolution.

[16]  Qingpo Liu.  Mutational Bias and Translational Selection Shaping the Codon Usage Pattern of Tissue-Specific Genes in Rice , 2012, PloS one.

[17]  Diethard Tautz,et al.  An Ancient Evolutionary Origin of Genes Associated with Human Genetic Diseases , 2008, Molecular biology and evolution.

[18]  Sudhir Kumar,et al.  Tree of Life Reveals Clock-Like Speciation and Diversification , 2014, Molecular biology and evolution.

[19]  Jelena Repar,et al.  Translational Selection Is Ubiquitous in Prokaryotes , 2010, PLoS genetics.

[20]  M. Long,et al.  Accelerated Recruitment of New Brain Development Genes into the Human Genome , 2011, PLoS biology.

[21]  S. Ohno.  Evolution by Gene Duplication , 1971 .

[22]  Wen-Hsiung Li,et al.  An evolutionary perspective on synonymous codon usage in unicellular organisms , 1986, Journal of Molecular Evolution.

[23]  Alison K. Hottes,et al.  Codon usage between genomes is constrained by genome-wide mutational processes. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[24]  Martin A. Nowak,et al.  Evolution of genetic redundancy , 1997, Nature.

[25]  Jun Li,et al.  Codon Deviation Coefficient: a novel measure for estimating codon usage bias and its statistical significance , 2012, BMC Bioinformatics.

[26]  Hiroshi Akashi,et al.  Translational selection and yeast proteome evolution. , 2003, Genetics.

[27]  Peng Cui,et al.  Translational selection in human: more pronounced in housekeeping genes , 2014, Biology Direct.

[28]  Q. Nie,et al.  Mutation Bias is the Driving Force of Codon Usage in the Gallus gallus genome , 2011, DNA research : an international journal for rapid publication of reports on genes and genomes.

[29]  Henrik Kaessmann,et al.  Origins, evolution, and phenotypic impact of new genes. , 2010, Genome research.

[30]  Bairong Shen,et al.  New genes drive the evolution of gene interaction networks in the human and mouse genomes , 2015, Genome Biology.

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

[32]  X. Xia,et al.  An improved implementation of effective number of codons (nc). , 2013, Molecular biology and evolution.

[33]  G. von Heijne,et al.  Tissue-based map of the human proteome , 2015, Science.

[34]  Yun Ding,et al.  On the origin of new genes in Drosophila. , 2008, Genome research.

[35]  A. Eyre-Walker,et al.  Synonymous codon usage in Escherichia coli: selection for translational accuracy. , 2006, Molecular biology and evolution.

[36]  Doron Lancet,et al.  Genome-wide midrange transcription profiles reveal expression level relationships in human tissue specification , 2005, Bioinform..

[37]  D. Tautz,et al.  The evolutionary origin of orphan genes , 2011, Nature Reviews Genetics.

[38]  D. Tautz,et al.  Phylogenetic patterns of emergence of new genes support a model of frequent de novo evolution , 2013, BMC Genomics.

[39]  Alessandra Carbone,et al.  Codon adaptation index as a measure of dominating codon bias , 2003, Bioinform..

[40]  Nicholas W. VanKuren,et al.  New gene evolution: little did we know. , 2013, Annual review of genetics.

[41]  T. Ikemura.  Correlation between the abundance of Escherichia coli transfer RNAs and the occurrence of the respective codons in its protein genes: a proposal for a synonymous codon choice that is optimal for the E. coli translational system. , 1981, Journal of molecular biology.

[42]  Yizhar Lavner,et al.  Codon bias as a factor in regulating expression via translation rate in the human genome. , 2005, Gene.

[43]  Doron Lancet,et al.  Alternative splicing and gene duplication are inversely correlated evolutionary mechanisms , 2005, Nature Genetics.

[44]  B. Gaut,et al.  Factors that contribute to variation in evolutionary rate among Arabidopsis genes. , 2011, Molecular biology and evolution.

[45]  Patricia P. Chan,et al.  GtRNAdb: a database of transfer RNA genes detected in genomic sequence , 2008, Nucleic Acids Res..

[46]  M. Albà,et al.  Inverse relationship between evolutionary rate and age of mammalian genes. , 2005, Molecular biology and evolution.

[47]  M. Bulmer.  The selection-mutation-drift theory of synonymous codon usage. , 1991, Genetics.

[48]  Tong Zhou,et al.  Detecting positive and purifying selection at synonymous sites in yeast and worm. , 2010, Molecular biology and evolution.

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

[50]  H. Akashi,et al.  Translational selection and molecular evolution. , 1998, Current opinion in genetics & development.

[51]  Araxi O. Urrutia,et al.  The signature of selection mediated by expression on human genes. , 2003, Genome research.

[52]  A. Pavesi,et al.  Transfer RNA gene redundancy and translational selection in Saccharomyces cerevisiae. , 1997, Journal of molecular biology.

[53]  Li Zhao,et al.  Origin and Spread of de Novo Genes in Drosophila melanogaster Populations , 2014, Science.

[54]  L. Wernisch,et al.  Solving the riddle of codon usage preferences: a test for translational selection. , 2004, Nucleic acids research.

[55]  Eugene V Koonin,et al.  The universal distribution of evolutionary rates of genes and distinct characteristics of eukaryotic genes of different apparent ages , 2009, Proceedings of the National Academy of Sciences.

[56]  L. Duret,et al.  tRNA gene number and codon usage in the C. elegans genome are co-adapted for optimal translation of highly expressed genes. , 2000, Trends in genetics : TIG.

[57]  B. Morton,et al.  Selective constraints on codon usage of nuclear genes from Arabidopsis thaliana. , 2006, Molecular biology and evolution.

[58]  X. Gu,et al.  Asymmetric evolution of human transcription factor regulatory networks. , 2014, Molecular biology and evolution.

[59]  Laurent Duret,et al.  Evolution of synonymous codon usage in metazoans. , 2002, Current opinion in genetics & development.

[60]  Eugene V Koonin,et al.  Duplicated genes evolve slower than singletons despite the initial rate increase , 2004, BMC Evolutionary Biology.

[61]  F. Wright.  The 'effective number of codons' used in a gene. , 1990, Gene.

[62]  G. Bernardi,et al.  Translational selection on codon usage in Xenopus laevis. , 2001, Molecular biology and evolution.

[63]  Lorenz Wernisch,et al.  Estimating Translational Selection in Eukaryotic Genomes , 2008, Molecular biology and evolution.