Large Scale Comparative Codon-Pair Context Analysis Unveils General Rules that Fine-Tune Evolution of mRNA Primary Structure

Background Codon usage and codon-pair context are important gene primary structure features that influence mRNA decoding fidelity. In order to identify general rules that shape codon-pair context and minimize mRNA decoding error, we have carried out a large scale comparative codon-pair context analysis of 119 fully sequenced genomes. Methodologies/Principal Findings We have developed mathematical and software tools for large scale comparative codon-pair context analysis. These methodologies unveiled general and species specific codon-pair context rules that govern evolution of mRNAs in the 3 domains of life. We show that evolution of bacterial and archeal mRNA primary structure is mainly dependent on constraints imposed by the translational machinery, while in eukaryotes DNA methylation and tri-nucleotide repeats impose strong biases on codon-pair context. Conclusions The data highlight fundamental differences between prokaryotic and eukaryotic mRNA decoding rules, which are partially independent of codon usage.

[1]  O. Berg,et al.  Codon bias in Escherichia coli: the influence of codon context on mutation and selection. , 1997, Nucleic acids research.

[2]  M Yarus,et al.  Rates of aminoacyl-tRNA selection at 29 sense codons in vivo. , 1989, Journal of molecular biology.

[3]  Thomas B. L. Kirkwood,et al.  Accuracy in molecular processes : its control and relevance to living systems , 1986 .

[4]  P. Farabaugh,et al.  Ribosome structure: revisiting the connection between translational accuracy and unconventional decoding , 2002, Trends in Biochemical Sciences.

[5]  E. J. Murgola,et al.  Codon context effects in missense suppression. , 1984, Journal of molecular biology.

[6]  Steven E. Jacobsen,et al.  Gardening the genome: DNA methylation in Arabidopsis thaliana , 2005, Nature Reviews Genetics.

[7]  M. Ehrenberg,et al.  The accuracy of codon recognition by polypeptide release factors. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[8]  D. Forsdyke,et al.  Thermophilic bacteria strictly obey Szybalski's transcription direction rule and politely purine-load RNAs with both adenine and guanine. , 2000, Genome research.

[9]  Manuel A. S. Santos,et al.  Comparative context analysis of codon pairs on an ORFeome scale , 2005, Genome Biology.

[10]  S. Ottonello,et al.  Selection at the wobble position of codons read by the same tRNA in Saccharomyces cerevisiae. , 1999, Molecular biology and evolution.

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

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

[13]  Sean D. Hooper,et al.  Detection of Genes with Atypical Nucleotide Sequence in Microbial Genomes , 2002, Journal of Molecular Evolution.

[14]  Shu-Bing Qian,et al.  Quantitating protein synthesis, degradation, and endogenous antigen processing. , 2003, Immunity.

[15]  W. Tate,et al.  Hidden infidelities of the translational stop signal. , 1996, Progress in nucleic acid research and molecular biology.

[16]  P. Farabaugh,et al.  The frequency of translational misreading errors in E. coli is largely determined by tRNA competition. , 2006, RNA.

[17]  S. Karlin,et al.  Genome signature comparisons among prokaryote, plasmid, and mitochondrial DNA. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[18]  Nairanjana Dasgupta,et al.  Analyzing Categorical Data , 2004, Technometrics.

[19]  Gabriela R. Moura,et al.  Statistical, Computational and Visualization Methodologies to Unveil Gene Primary Structure Features , 2006, Methods of Information in Medicine.

[20]  K. Robertson.  DNA methylation and human disease , 2005, Nature Reviews Genetics.

[21]  R. Buckingham,et al.  The accuracy of mRNA—tRNA recognition , 1986 .

[22]  R. Buckingham.  Codon context , 2005, Experientia.

[23]  A. Danchin,et al.  Universal replication biases in bacteria , 1999, Molecular microbiology.

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

[25]  R. Weiss,et al.  Towards a genetic dissection of the basis of triplet decoding, and its natural subversion: programmed reading frame shifts and hops. , 1991, Annual review of genetics.

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

[27]  P. Yen,et al.  Polymorphisms associated with the DAZ genes on the human Y chromosome. , 2005, Genomics.

[28]  Mark Johnston,et al.  After the Duplication: Gene Loss and Adaptation in Saccharomyces Genomes , 2006, Genetics.

[29]  S. Haberman.  The Analysis of Residuals in Cross-Classified Tables , 1973 .

[30]  Isabelle Hatin,et al.  The major 5' determinant in stop codon read-through involves two adjacent adenines. , 2004, Nucleic acids research.

[31]  K Nishikawa,et al.  Genes from nine genomes are separated into their organisms in the dinucleotide composition space. , 1998, DNA research : an international journal for rapid publication of reports on genes and genomes.

[32]  Branko Borstnik,et al.  Tandem repeats in protein coding regions of primate genes. , 2002, Genome research.

[33]  Simone Campanoni.  Competition , 1866, Nature.

[34]  F. Taddei,et al.  Over-representation of repeats in stress response genes: a strategy to increase versatility under stressful conditions? , 2002, Nucleic acids research.

[35]  Liane Gagnier,et al.  Genomic deletions and precise removal of transposable elements mediated by short identical DNA segments in primates. , 2005, Genome research.

[36]  S. Hooper,et al.  Gradients in nucleotide and codon usage along Escherichia coli genes. , 2000, Nucleic acids research.

[37]  Alexei Fedorov,et al.  Regularities of context-dependent codon bias in eukaryotic genes. , 2002, Nucleic acids research.

[38]  K Nishikawa,et al.  Differences in dinucleotide frequencies of human, yeast, and Escherichia coli genes. , 1997, DNA research : an international journal for rapid publication of reports on genes and genomes.

[39]  Fredj Tekaia,et al.  Amino acid composition of genomes, lifestyles of organisms, and evolutionary trends: a global picture with correspondence analysis. , 2002, Gene.

[40]  J A Koziol,et al.  Evolution of the genome and the genetic code: selection at the dinucleotide level by methylation and polyribonucleotide cleavage. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[41]  L. Hood,et al.  Understanding the adaptation of Halobacterium species NRC-1 to its extreme environment through computational analysis of its genome sequence. , 2001, Genome research.

[42]  Ivan Ivanov,et al.  Missing Codon Pairs in the Genome of Escherichia Coli , 2002, Bioinform..

[43]  J. Duan,et al.  Mammalian Mutation Pressure, Synonymous Codon Choice, and mRNA Degradation , 2003, Journal of Molecular Evolution.

[44]  G. W. Hatfield,et al.  Nonrandom utilization of codon pairs in Escherichia coli. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[45]  R. Thompson,et al.  Codon choice and gene expression: synonymous codons differ in translational accuracy. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[46]  V. Ramakrishnan,et al.  First published online as a Review in Advance on February 25, 2005 STRUCTURAL INSIGHTS INTO TRANSLATIONAL , 2022 .

[47]  Raymond F. Gesteland,et al.  Computational identification of putative programmed translational frameshift sites , 2002, Bioinform..

[48]  Selection of aminoacyl-tRNAs at sense codons: the size of the tRNA variable loop determines whether the immediate 3' nucleotide to the codon has a context effect. , 1995, Nucleic acids research.

[49]  Henri Grosjean,et al.  tRNomics: analysis of tRNA genes from 50 genomes of Eukarya, Archaea, and Bacteria reveals anticodon-sparing strategies and domain-specific features. , 2002, RNA.

[50]  Ian Stansfield,et al.  tRNA properties help shape codon pair preferences in open reading frames , 2006, Nucleic acids research.

[51]  G. W. Hatfield,et al.  Codon Pair Utilization Biases Influence Translational Elongation Step Times (*) , 1995, The Journal of Biological Chemistry.

[52]  Sandrine Caburet,et al.  A Genomic Basis for the Evolution of Vertebrate Transcription Factors Containing Amino Acid Runs , 2004, Genetics.

[53]  M. Rodnina,et al.  Fidelity of aminoacyl-tRNA selection on the ribosome: kinetic and structural mechanisms. , 2001, Annual review of biochemistry.

[54]  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.

[55]  G. McVean,et al.  Evolutionary Lability of Context-Dependent Codon Bias in Bacteria , 2000, Journal of Molecular Evolution.

[56]  Jeffrey S. Simonoff,et al.  Analyzing Categorical Data , 2003 .