Modelling the Efficiency of Codon–tRNA Interactions Based on Codon Usage Bias

The tRNA adaptation index (tAI) is a widely used measure of the efficiency by which a coding sequence is recognized by the intra-cellular tRNA pool. This index includes among others weights that represent wobble interactions between codons and tRNA molecules. Currently, these weights are based only on the gene expression in Saccharomyces cerevisiae. However, the efficiencies of the different codon–tRNA interactions are expected to vary among different organisms. In this study, we suggest a new approach for adjusting the tAI weights to any target model organism without the need for gene expression measurements. Our method is based on optimizing the correlation between the tAI and a measure of codon usage bias. Here, we show that in non-fungal the new tAI weights predict protein abundance significantly better than the traditional tAI weights. The unique tRNA–codon adaptation weights computed for 100 different organisms exhibit a significant correlation with evolutionary distance. The reported results demonstrate the usefulness of the new measure in future genomic studies.

[1]  D. Frishman,et al.  Protein abundance profiling of the Escherichia coli cytosol , 2008, BMC Genomics.

[2]  L. Duret,et al.  Expression pattern and, surprisingly, gene length shape codon usage in Caenorhabditis, Drosophila, and Arabidopsis. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[3]  U. Gophna,et al.  Reconstructing ancestral gene content by coevolution. , 2010, Genome research.

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

[5]  M. Bergdoll,et al.  Arabidopsis tRNA Adenosine Deaminase Arginine Edits the Wobble Nucleotide of Chloroplast tRNAArg(ACG) and Is Essential for Efficient Chloroplast Translation[W] , 2009, The Plant Cell Online.

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

[7]  G. Kramer,et al.  Structure, Function, and Genetics of Ribosomes , 1986, Springer Series in Molecular Biology.

[8]  W. Fiers,et al.  Preferential codon usage in prokaryotic genes: the optimal codon-anticodon interaction energy and the selective codon usage in efficiently expressed genes. , 1982, Gene.

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

[10]  M. Yusupov,et al.  One core, two shells: bacterial and eukaryotic ribosomes , 2012, Nature Structural &Molecular Biology.

[11]  Eytan Ruppin,et al.  Translation efficiency is determined by both codon bias and folding energy , 2010, Proceedings of the National Academy of Sciences.

[12]  M. Gouy,et al.  Codon catalog usage and the genome hypothesis. , 1980, Nucleic acids research.

[13]  Ivan Erill,et al.  Relative Codon Adaptation: A Generic Codon Bias Index for Prediction of Gene Expression , 2010, DNA research : an international journal for rapid publication of reports on genes and genomes.

[14]  Nicholas T. Ingolia,et al.  Ribosome Profiling of Mouse Embryonic Stem Cells Reveals the Complexity and Dynamics of Mammalian Proteomes , 2011, Cell.

[15]  P. Sharp,et al.  The codon Adaptation Index--a measure of directional synonymous codon usage bias, and its potential applications. , 1987, Nucleic acids research.

[16]  Lippincott-Schwartz,et al.  Supporting Online Material Materials and Methods Som Text Figs. S1 to S8 Table S1 Movies S1 to S3 a " Silent " Polymorphism in the Mdr1 Gene Changes Substrate Specificity Corrected 30 November 2007; See Last Page , 2022 .

[17]  Tsutomu Suzuki,et al.  molecular mechanism of lysidine synthesis that determines tRNA identity and codon recognition. , 2005, Molecular cell.

[18]  D. Söll,et al.  Agmatidine, a modified cytidine in the anticodon of archaeal tRNAIle, base pairs with adenosine but not with guanosine , 2010, Proceedings of the National Academy of Sciences.

[19]  Eytan Ruppin,et al.  Determinants of Protein Abundance and Translation Efficiency in S. cerevisiae , 2007, PLoS Comput. Biol..

[20]  J. MacQueen.  Some methods for classification and analysis of multivariate observations , 1967 .

[21]  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.

[22]  L. Hurst,et al.  Hearing silence: non-neutral evolution at synonymous sites in mammals , 2006, Nature Reviews Genetics.

[23]  T. Ohama,et al.  Role of GC-biased mutation pressure on synonymous codon choice in Micrococcus luteus, a bacterium with a high genomic GC-content. , 1990, Nucleic acids research.

[24]  S. Behura,et al.  Codon usage bias: causative factors, quantification methods and genome‐wide patterns: with emphasis on insect genomes , 2013, Biological reviews of the Cambridge Philosophical Society.

[25]  Paul M. Sharp,et al.  Codon usage in Caenorhabditis elegans: delineation of translational selection and mutational biases , 1994, Nucleic Acids Res..

[26]  J. Werren,et al.  Comparative analysis of nuclear tRNA genes of Nasonia vitripennis and other arthropods, and relationships to codon usage bias , 2010, Insect molecular biology.

[27]  Satyabrata Sahoo,et al.  Predicting Gene Expression Level from Relative Codon Usage Bias: An Application to Escherichia coli Genome , 2009, DNA research : an international journal for rapid publication of reports on genes and genomes.

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

[29]  F. Crick.  Codon--anticodon pairing: the wobble hypothesis. , 1966, Journal of molecular biology.

[30]  T. Ikemura.  Codon usage and tRNA content in unicellular and multicellular organisms. , 1985, Molecular biology and evolution.

[31]  D. Posada,et al.  Coalescent Simulation of Intracodon Recombination , 2010, Genetics.

[32]  Aleksey Y. Ogurtsov,et al.  A periodic pattern of mRNA secondary structure created by the genetic code , 2006, Nucleic acids research.

[33]  E. Marcotte,et al.  Absolute protein expression profiling estimates the relative contributions of transcriptional and translational regulation , 2007, Nature Biotechnology.

[34]  V. Lim,et al.  Analysis of codon:anticodon interactions within the ribosome provides new insights into codon reading and the genetic code structure. , 2001, RNA.

[35]  Tsutomu Suzuki,et al.  Wobble Inosine tRNA Modification Is Essential to Cell Cycle Progression in G1/S and G2/M Transitions in Fission Yeast* , 2007, Journal of Biological Chemistry.

[36]  C. Kurland.  Codon bias and gene expression , 1991, FEBS letters.

[37]  E. Marcotte,et al.  Global signatures of protein and mRNA expression levelsw , 2009 .

[38]  M. A. Gorovsky,et al.  DNase I sensitivity of ribosomal genes in isolated nucleosome core particles , 1980, Nucleic Acids Res..

[39]  D. Severson,et al.  Coadaptation of isoacceptor tRNA genes and codon usage bias for translation efficiency in Aedes aegypti and Anopheles gambiae , 2011, Insect molecular biology.

[40]  Yitzhak Pilpel,et al.  Differential translation efficiency of orthologous genes is involved in phenotypic divergence of yeast species , 2007, Nature Genetics.

[41]  Tamir Tuller,et al.  Transcript features alone enable accurate prediction and understanding of gene expression in S. cerevisiae , 2013, BMC Bioinformatics.

[42]  Lorenz Wernisch,et al.  Unexpected correlations between gene expression and codon usage bias from microarray data for the whole Escherichia coli K-12 genome. , 2003, Nucleic Acids Research.

[43]  P. Agris.  Wobble position modified nucleosides evolved to select transfer RNA codon recognition: a modified-wobble hypothesis. , 1991, Biochimie.

[44]  N. W. Davis,et al.  The complete genome sequence of Escherichia coli K-12. , 1997, Science.

[45]  David W. Digby,et al.  mRNAs have greater negative folding free energies than shuffled or codon choice randomized sequences. , 1999, Nucleic acids research.

[46]  E. Rocha.  Codon usage bias from tRNA's point of view: redundancy, specialization, and efficient decoding for translation optimization. , 2004, Genome research.

[47]  C. Wilke,et al.  Why highly expressed proteins evolve slowly. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[48]  H. L. Le Roy,et al.  Proceedings of the Fifth Berkeley Symposium on Mathematical Statistics and Probability; Vol. IV , 1969 .

[49]  Patricio Jeraldo,et al.  The Genetic Code , 2006 .

[50]  Y. Pilpel,et al.  An Evolutionarily Conserved Mechanism for Controlling the Efficiency of Protein Translation , 2010, Cell.

[51]  F. Murphy,et al.  Structure of a purine-purine wobble base pair in the decoding center of the ribosome , 2004, Nature Structural &Molecular Biology.

[52]  A. Ivanov,et al.  Comparative proteomic and transcriptomic profiling of the fission yeast Schizosaccharomyces pombe , 2007, Molecular systems biology.

[53]  A. Rich,et al.  Identification and characterization of a human tRNA-specific adenosine deaminase related to the ADAR family of pre-mRNA editing enzymes. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[54]  Alex P. Reynolds,et al.  Exonic Transcription Factor Binding Directs Codon Choice and Affects Protein Evolution , 2013, Science.

[55]  U. RajBhandary.  Modified bases and aminoacylation , 1988, Nature.

[56]  M. Kimura.  Genetic variability maintained in a finite population due to mutational production of neutral and nearly neutral isoalleles. , 1968, Genetical research.

[57]  Reinhard Wolf,et al.  Coding-Sequence Determinants of Gene Expression in Escherichia coli , 2009 .

[58]  J. Yates,et al.  Large-scale analysis of the yeast proteome by multidimensional protein identification technology , 2001, Nature Biotechnology.

[59]  M. Kimura.  Genetic variability maintained in a finite population due to mutational production of neutral and nearly neutral isoalleles. , 1968, Genetical research.

[60]  John A. Nelder,et al.  A Simplex Method for Function Minimization , 1965, Comput. J..

[61]  Z. Tu,et al.  Identification and characterization of odorant‐binding protein 1 gene from the Asian malaria mosquito, Anopheles stephensi , 2010, Insect molecular biology.

[62]  Michal Linial,et al.  Conservation of the relative tRNA composition in healthy and cancerous tissues. , 2012, RNA.

[63]  Fran Supek,et al.  On Relevance of Codon Usage to Expression of Synthetic and Natural Genes in Escherichia coli , 2010, Genetics.

[64]  K. H. Wolfe,et al.  Relationship of codon bias to mRNA concentration and protein length in Saccharomyces cerevisiae , 2000, Yeast.

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

[66]  Milana Frenkel-Morgenstern,et al.  Genes adopt non-optimal codon usage to generate cell cycle-dependent oscillations in protein levels , 2012, Molecular systems biology.

[67]  Jianzhi Zhang,et al.  Balanced Codon Usage Optimizes Eukaryotic Translational Efficiency , 2012, PLoS genetics.

[68]  W. Keller,et al.  tadA, an essential tRNA‐specific adenosine deaminase from Escherichia coli , 2002, The EMBO journal.

[69]  J. Bennetzen,et al.  Codon selection in yeast. , 1982, The Journal of biological chemistry.

[70]  B. Futcher,et al.  A Sampling of the Yeast Proteome , 1999, Molecular and Cellular Biology.

[71]  P. Hugenholtz,et al.  Genome sequences of rare, uncultured bacteria obtained by differential coverage binning of multiple metagenomes , 2013, Nature Biotechnology.

[72]  S. Kanaya,et al.  Studies of codon usage and tRNA genes of 18 unicellular organisms and quantification of Bacillus subtilis tRNAs: gene expression level and species-specific diversity of codon usage based on multivariate analysis. , 1999, Gene.

[73]  T. Pan,et al.  A Role for tRNA Modifications in Genome Structure and Codon Usage , 2012, Cell.

[74]  M. Gerstein,et al.  Comparing protein abundance and mRNA expression levels on a genomic scale , 2003, Genome Biology.

[75]  T. Ikemura.  Correlation between the abundance of yeast transfer RNAs and the occurrence of the respective codons in protein genes. Differences in synonymous codon choice patterns of yeast and Escherichia coli with reference to the abundance of isoaccepting transfer RNAs. , 1982, Journal of molecular biology.

[76]  P. Sharp,et al.  Variation in the strength of selected codon usage bias among bacteria , 2005, Nucleic acids research.