{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2024,8,11]],"date-time":"2024-08-11T14:30:57Z","timestamp":1723386657849},"reference-count":44,"publisher":"Oxford University Press (OUP)","issue":"18","license":[{"start":{"date-parts":[[2016,10,2]],"date-time":"2016-10-02T00:00:00Z","timestamp":1475366400000},"content-version":"vor","delay-in-days":1490,"URL":"http:\/\/creativecommons.org\/licenses\/by\/3.0"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2012,9,15]]},"abstract":"Abstract<\/jats:title>\n Motivation: The standard genetic code translates 61 codons into 20 amino acids using fewer than 61 transfer RNAs (tRNAs). This is possible because of the tRNA's ability to \u2018wobble\u2019 at the third base to decode more than one codon. Although the anticodon\u2013codon mapping of tRNA to mRNA is a prerequisite for certain codon usage indices and can contribute to the understanding of the evolution of alternative genetic codes, it is usually not determined experimentally because such assays are prohibitively expensive and elaborate. Instead, the codon reading is approximated from theoretical inferences of nucleotide binding, the wobble rules. Unfortunately, these rules fail to capture all of the nuances of codon reading. This study addresses the codon reading properties of tRNAs and their evolutionary impact on codon usage bias.<\/jats:p>\n Results: Using three different computational methods, the signal of tRNA decoding in codon usage bias is identified. The predictions by the methods generally agree with each other and compare well with experimental evidence of codon reading. This analysis suggests a revised codon reading for cytosolic tRNA in the yeast genome (Saccharomyces cerevisiae) that is more accurate than the common assignment by wobble rules. The results confirm the earlier observation that the wobble rules are not sufficient for a complete description of codon reading, because they depend on genome-specific factors. The computational methods presented here are applicable to any fully sequenced genome.<\/jats:p>\n Availability: By request from the author.<\/jats:p>\n Contact: \u00a0alexander.roth@isb-sib.ch<\/jats:p>","DOI":"10.1093\/bioinformatics\/bts403","type":"journal-article","created":{"date-parts":[[2012,9,7]],"date-time":"2012-09-07T20:35:22Z","timestamp":1347050122000},"page":"i340-i348","source":"Crossref","is-referenced-by-count":8,"title":["Decoding properties of tRNA leave a detectable signal in codon usage bias"],"prefix":"10.1093","volume":"28","author":[{"given":"Alexander C.","family":"Roth","sequence":"first","affiliation":[{"name":"Swiss Institute of Bioinformatics, and Department of Computer Science, ETH Zurich, 8092 Zurich, Switzerland"}]}],"member":"286","published-online":{"date-parts":[[2012,9,3]]},"reference":[{"key":"2023012513013515200_B1","doi-asserted-by":"crossref","first-page":"1345","DOI":"10.1016\/0300-9084(91)90163-U","article-title":"Wobble position modified nucleosides evolved to select transfer RNA codon recognition: a modified-wobble hypothesis","volume":"73","author":"Agris","year":"1991","journal-title":"Biochimie"},{"key":"2023012513013515200_B2","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.jmb.2006.11.046","article-title":"tRNA's wobble decoding of the genome: 40 years of modification","volume":"366","author":"Agris","year":"2007","journal-title":"J. Mol. Biol."},{"key":"2023012513013515200_B3","doi-asserted-by":"crossref","DOI":"10.1128\/ecosalplus.4.6.2","article-title":"Transfer RNA modification","volume-title":"Escherichia coli and Salmonella. Cellular and Molecular Biology","author":"Bj\u00f6rk","year":"2005"},{"key":"2023012513013515200_B4","doi-asserted-by":"crossref","first-page":"897","DOI":"10.1093\/genetics\/129.3.897","article-title":"The selection-mutation-drift theory of synonymous codon usage","volume":"129","author":"Bulmer","year":"1991","journal-title":"Genetics"},{"key":"2023012513013515200_B5","doi-asserted-by":"crossref","first-page":"355","DOI":"10.1016\/j.cell.2010.02.036","article-title":"A role for codon order in translation dynamics","volume":"141","author":"Cannarozzi","year":"2010","journal-title":"Cell"},{"key":"2023012513013515200_B6","doi-asserted-by":"crossref","first-page":"D93","DOI":"10.1093\/nar\/gkn787","article-title":"GtRNAdb: a database of transfer RNA genes detected in genomic sequence","volume":"37","author":"Chan","year":"2009","journal-title":"Nuc. Acids Res."},{"key":"2023012513013515200_B7","doi-asserted-by":"crossref","first-page":"548","DOI":"10.1016\/S0022-2836(66)80022-0","article-title":"Codon\u2013anticodon pairing: the wobble hypothesis","volume":"19","author":"Crick","year":"1966","journal-title":"J. Mol. Biol."},{"key":"2023012513013515200_B8","doi-asserted-by":"crossref","first-page":"683","DOI":"10.1093\/nar\/23.4.683","article-title":"Decoding with the A:I wobble pair is inefficient","volume":"23","author":"Curran","year":"1995","journal-title":"Nuc. Acids Res."},{"key":"2023012513013515200_B9","doi-asserted-by":"crossref","first-page":"153","DOI":"10.1016\/S0076-6879(07)25007-4","article-title":"Identification of genes encoding tRNA modification enzymes by comparative genomics","volume":"425","author":"de Cr\u00e9cy-Lagard","year":"2007","journal-title":"Methods Enzymol"},{"key":"2023012513013515200_B10","doi-asserted-by":"crossref","first-page":"649","DOI":"10.1006\/jmbi.1996.0428","article-title":"Co-variation of tRNA abundance and codon usage in Escherichia coli at different growth rates","volume":"260","author":"Dong","year":"1996","journal-title":"J. Mol. Biol."},{"key":"2023012513013515200_B11","doi-asserted-by":"crossref","first-page":"6976","DOI":"10.1093\/nar\/gkg897","article-title":"Unexpected correlations between gene expression and codon usage bias from microarray data for the whole Escherichia coli K-12 genome","volume":"31","author":"dos Reis","year":"2003","journal-title":"Nucl. Acids Res."},{"key":"2023012513013515200_B12","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1017\/S0033583500005254","article-title":"Costs of accuracy determined by a maximal growth rate constraint","volume":"17","author":"Ehrenberg","year":"1984","journal-title":"Q. Rev. Biophys."},{"key":"2023012513013515200_B13","doi-asserted-by":"crossref","first-page":"1718","DOI":"10.1126\/science.1083811","article-title":"Selective charging of tRNA isoacceptors explains patterns of codon usage","volume":"300","author":"Elf","year":"2003","journal-title":"Science"},{"key":"2023012513013515200_B14","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/11851561_1","article-title":"Measures of codon bias in yeast, the tRNA pairing index and possible DNA repair mechanisms","volume":"4175","author":"Friberg","year":"2006","journal-title":"Algor. Bioinform. Proce."},{"key":"2023012513013515200_B15","doi-asserted-by":"crossref","first-page":"211","DOI":"10.1016\/S0022-5193(74)80054-8","article-title":"Functional adaptation of tRNA population","volume":"43","author":"Garel","year":"1974","journal-title":"J. Theor. Biol."},{"key":"2023012513013515200_B16","doi-asserted-by":"crossref","first-page":"252","DOI":"10.1016\/j.febslet.2009.11.052","article-title":"Deciphering synonymous codons in the three domains of life: co-evolution with specific tRNA modification enzymes","volume":"584","author":"Grosjean","year":"2010","journal-title":"FEBS Lett."},{"key":"2023012513013515200_B17","first-page":"487","article-title":"Organization and expression of tRNA genes in Saccharomyces cerevisiae","volume-title":"The Molecular Biology of the Yeast Saccharomyces: Metabolism and Gene Expression","author":"Guthrie","year":"1982"},{"key":"2023012513013515200_B18","doi-asserted-by":"crossref","first-page":"617","DOI":"10.1146\/annurev.biochem.69.1.617","article-title":"Aminoacyl-tRNA synthesis","volume":"69","author":"Ibba","year":"2000","journal-title":"Annu. Rev. Biochem."},{"key":"2023012513013515200_B19","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/0022-2836(81)90363-6","article-title":"Correlation between the abundance of Escherichia coli transfer RNAs and the occurrence of the respective codons in its protein genes","volume":"146","author":"Ikemura","year":"1981","journal-title":"J. Mol. Biol."},{"key":"2023012513013515200_B20","doi-asserted-by":"crossref","first-page":"218","DOI":"10.1126\/science.1168978","article-title":"Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling","volume":"324","author":"Ingolia","year":"2009","journal-title":"Science"},{"key":"2023012513013515200_B21","doi-asserted-by":"crossref","first-page":"3301","DOI":"10.1128\/MCB.01542-07","article-title":"Eukaryotic wobble uridine modifications promote a functionally redundant decoding system","volume":"28","author":"Johansson","year":"2008","journal-title":"Mol. Cell Biol."},{"key":"2023012513013515200_B22","doi-asserted-by":"crossref","first-page":"933","DOI":"10.1016\/j.biochi.2004.08.006","article-title":"Transient idling of posttermination ribosomes ready to reinitiate protein synthesis","volume":"86","author":"Karamyshev","year":"2004","journal-title":"Biochimie"},{"key":"2023012513013515200_B23","doi-asserted-by":"crossref","first-page":"D563","DOI":"10.1093\/nar\/gkp871","article-title":"Ensembl genomes: extending ensembl across the taxonomic space","volume":"38","author":"Kersey","year":"2010","journal-title":"Nucl. Acids Res."},{"key":"2023012513013515200_B24","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1261\/rna.294907","article-title":"The frequency of translational misreading errors in E. coli is largely determined by tRNA competition","volume":"13","author":"Kramer","year":"2007","journal-title":"RNA"},{"key":"2023012513013515200_B25","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1007\/BF00260434","article-title":"The tRNA cycle and its relation to the rate of protein synthesis","volume":"12","author":"Liljenstr\u00f6m","year":"1985","journal-title":"Eur. Biophys J."},{"key":"2023012513013515200_B26","doi-asserted-by":"crossref","first-page":"955","DOI":"10.1093\/nar\/25.5.955","article-title":"tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence","volume":"25","author":"Lowe","year":"1997","journal-title":"Nucl. Acids Res."},{"key":"2023012513013515200_B27","doi-asserted-by":"crossref","first-page":"471","DOI":"10.1016\/S0021-9258(17)32740-0","article-title":"Codon-acticodon recognition in the valine codon family","volume":"252","author":"Mitra","year":"1977","journal-title":"J. Biol. Chem."},{"key":"2023012513013515200_B28","doi-asserted-by":"crossref","first-page":"334","DOI":"10.1016\/j.febslet.2009.11.066","article-title":"Development of the genetic code: insights from a fungal codon reassignment","volume":"584","author":"Moura","year":"2010","journal-title":"FEBS Lett."},{"key":"2023012513013515200_B29","doi-asserted-by":"crossref","first-page":"1186","DOI":"10.1038\/nsmb861","article-title":"The role of modifications in codon discrimination by tRNA(Lys)UUU","volume":"11","author":"Murphy","year":"2004","journal-title":"Nat. Struct. Mol. Biol."},{"key":"2023012513013515200_B30","doi-asserted-by":"crossref","first-page":"2151","DOI":"10.1261\/rna.731007","article-title":"The wobble hypothesis revisited: uridine-5-oxyacetic acid is critical for reading of G-ending codons","volume":"13","author":"N\u00e4svall","year":"2007","journal-title":"RNA"},{"key":"2023012513013515200_B31","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1146\/annurev.biochem.74.061903.155440","article-title":"Structural insights into translational fidelity","volume":"74","author":"Ogle","year":"2005","journal-title":"Annu. Rev. Biochem."},{"key":"2023012513013515200_B32","doi-asserted-by":"crossref","first-page":"273","DOI":"10.1128\/mr.53.3.273-298.1989","article-title":"Errors and alternatives in reading the universal genetic code","volume":"53","author":"Parker","year":"1989","journal-title":"Microbiol. Rev."},{"key":"2023012513013515200_B33","doi-asserted-by":"crossref","first-page":"322","DOI":"10.1006\/jmbi.1997.0942","article-title":"Transfer RNA gene redundancy and translational selection in Saccharomyces cerevisiae","volume":"268","author":"Percudani","year":"1997","journal-title":"J. Mol. Biol."},{"key":"2023012513013515200_B34","doi-asserted-by":"crossref","first-page":"133","DOI":"10.1016\/S0168-9525(00)02208-3","article-title":"Restricted wobble rules for eukaryotic genomes","volume":"17","author":"Percudani","year":"2001","journal-title":"Trends. Genet."},{"key":"2023012513013515200_B35","doi-asserted-by":"crossref","first-page":"32","DOI":"10.1038\/nrg2899","article-title":"Synonymous but not the same: the causes and consequences of codon bias","volume":"12","author":"Plotkin","year":"2011","journal-title":"Nat. Rev. Genet."},{"key":"2023012513013515200_B36","doi-asserted-by":"crossref","first-page":"e1002603","DOI":"10.1371\/journal.pgen.1002603","article-title":"Balanced codon usage optimizes eukaryotic translational efficiency","volume":"8","author":"Qian","year":"2012","journal-title":"PLoS Genet."},{"key":"2023012513013515200_B37","doi-asserted-by":"crossref","first-page":"267","DOI":"10.1109\/5.18626","article-title":"A tutorial on hidden, Markov models and selected applications in speech recognition","volume":"77","author":"Rabiner","year":"1989","journal-title":"Proc. IEEE"},{"key":"2023012513013515200_B38","doi-asserted-by":"crossref","first-page":"2129","DOI":"10.1093\/molbev\/msq102","article-title":"The influence of anticodon-codon interactions and modified bases on codon usage bias in bacteria","volume":"27","author":"Ran","year":"2010","journal-title":"Mol. Biol. Evol."},{"key":"2023012513013515200_B39","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1016\/S0079-6603(08)60006-9","article-title":"Recognition of tRNAs by aminoacyl-tRNA synthetases","volume":"41","author":"Schulman","year":"1991","journal-title":"Prog. Nucl. Acid Res. Mol. Biol."},{"key":"2023012513013515200_B40","doi-asserted-by":"crossref","first-page":"1089","DOI":"10.1007\/BF01936918","article-title":"The accuracy of aminoacylation\u2013ensuring the fidelity of the genetic code","volume":"46","author":"S\u00f6ll","year":"1990","journal-title":"Experientia"},{"key":"2023012513013515200_B41","doi-asserted-by":"crossref","first-page":"16","DOI":"10.1016\/j.jmb.2005.08.076","article-title":"Over expression of a tRNA(Leu) isoacceptor changes charging pattern of leucine tRNAs and reveals new codon reading","volume":"354","author":"S\u00f8rensen","year":"2005","journal-title":"J. Mol. Biol."},{"key":"2023012513013515200_B42","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1016\/0014-5793(94)00354-8","article-title":"Recognition of UUN codons by two leucine tRNA species from Escherichia coli","volume":"344","author":"Takai","year":"1994","journal-title":"FEBS Lett."},{"key":"2023012513013515200_B43","doi-asserted-by":"crossref","first-page":"344","DOI":"10.1016\/j.cell.2010.03.031","article-title":"An evolutionarily conserved mechanism for controlling the efficiency of protein translation","volume":"141","author":"Tuller","year":"2010","journal-title":"Cell"},{"key":"2023012513013515200_B44","first-page":"207","article-title":"Modified nucleosides and codon recognition","volume-title":"tRNA: Structure, Biosynthesis, and Function","author":"Yokoyama","year":"1995"}],"container-title":["Bioinformatics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/bioinformatics\/article-pdf\/28\/18\/i340\/48880637\/bioinformatics_28_18_i340.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/bioinformatics\/article-pdf\/28\/18\/i340\/48880637\/bioinformatics_28_18_i340.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,1,25]],"date-time":"2023-01-25T18:50:21Z","timestamp":1674672621000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/bioinformatics\/article\/28\/18\/i340\/248836"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2012,9,3]]},"references-count":44,"journal-issue":{"issue":"18","published-print":{"date-parts":[[2012,9,15]]}},"URL":"https:\/\/doi.org\/10.1093\/bioinformatics\/bts403","relation":{},"ISSN":["1367-4811","1367-4803"],"issn-type":[{"value":"1367-4811","type":"electronic"},{"value":"1367-4803","type":"print"}],"subject":[],"published-other":{"date-parts":[[2012,9,15]]},"published":{"date-parts":[[2012,9,3]]}}}