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Ribosome traffic on mRNAs maps to gene ontology: genome-wide quantification of translation initiation rates and polysome size regulation
To understand the complex relationship governing transcript abundance and the level of the encoded protein, we integrate genome-wide experimental data of ribosomal density on mRNAs with a novel stochastic model describing ribosome traffic dynamics during translation elongation. This analysis reveals...
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Published in: | PLoS computational biology 2013-01, Vol.9 (1), p.e1002866-e1002866 |
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description | To understand the complex relationship governing transcript abundance and the level of the encoded protein, we integrate genome-wide experimental data of ribosomal density on mRNAs with a novel stochastic model describing ribosome traffic dynamics during translation elongation. This analysis reveals that codon arrangement, rather than simply codon bias, has a key role in determining translational efficiency. It also reveals that translation output is governed both by initiation efficiency and elongation dynamics. By integrating genome-wide experimental data sets with simulation of ribosome traffic on all Saccharomyces cerevisiae ORFs, mRNA-specific translation initiation rates are for the first time estimated across the entire transcriptome. Our analysis identifies different classes of mRNAs characterised by their initiation rates, their ribosome traffic dynamics, and by their response to ribosome availability. Strikingly, this classification based on translational dynamics maps onto key gene ontological classifications, revealing evolutionary optimisation of translation responses to be strongly influenced by gene function. |
doi_str_mv | 10.1371/journal.pcbi.1002866 |
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Strikingly, this classification based on translational dynamics maps onto key gene ontological classifications, revealing evolutionary optimisation of translation responses to be strongly influenced by gene function.</description><identifier>ISSN: 1553-7358</identifier><identifier>ISSN: 1553-734X</identifier><identifier>EISSN: 1553-7358</identifier><identifier>DOI: 10.1371/journal.pcbi.1002866</identifier><identifier>PMID: 23382661</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Biology ; Biotechnology ; Classification ; Codon ; Councils ; Gene expression ; Genetic translation ; Genetics ; Genome ; Genomes ; Genomics ; Life sciences ; Messenger RNA ; Models, Theoretical ; Ontology ; Physics ; Physiological aspects ; Polyribosomes - metabolism ; Protein Biosynthesis ; Proteins ; Ribosomes - metabolism ; RNA, Messenger - genetics ; RNA, Messenger - metabolism ; Stochastic models ; Stochastic Processes ; Yeast</subject><ispartof>PLoS computational biology, 2013-01, Vol.9 (1), p.e1002866-e1002866</ispartof><rights>COPYRIGHT 2013 Public Library of Science</rights><rights>2013 Ciandrini et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Ciandrini L, Stansfield I, Romano MC (2013) Ribosome Traffic on mRNAs Maps to Gene Ontology: Genome-wide Quantification of Translation Initiation Rates and Polysome Size Regulation. 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This analysis reveals that codon arrangement, rather than simply codon bias, has a key role in determining translational efficiency. It also reveals that translation output is governed both by initiation efficiency and elongation dynamics. By integrating genome-wide experimental data sets with simulation of ribosome traffic on all Saccharomyces cerevisiae ORFs, mRNA-specific translation initiation rates are for the first time estimated across the entire transcriptome. Our analysis identifies different classes of mRNAs characterised by their initiation rates, their ribosome traffic dynamics, and by their response to ribosome availability. Strikingly, this classification based on translational dynamics maps onto key gene ontological classifications, revealing evolutionary optimisation of translation responses to be strongly influenced by gene function.</description><subject>Biology</subject><subject>Biotechnology</subject><subject>Classification</subject><subject>Codon</subject><subject>Councils</subject><subject>Gene expression</subject><subject>Genetic translation</subject><subject>Genetics</subject><subject>Genome</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Life sciences</subject><subject>Messenger RNA</subject><subject>Models, Theoretical</subject><subject>Ontology</subject><subject>Physics</subject><subject>Physiological aspects</subject><subject>Polyribosomes - metabolism</subject><subject>Protein Biosynthesis</subject><subject>Proteins</subject><subject>Ribosomes - metabolism</subject><subject>RNA, Messenger - genetics</subject><subject>RNA, Messenger - metabolism</subject><subject>Stochastic models</subject><subject>Stochastic Processes</subject><subject>Yeast</subject><issn>1553-7358</issn><issn>1553-734X</issn><issn>1553-7358</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><sourceid>DOA</sourceid><recordid>eNqVkk1v1DAQhiMEoqXwDxBE4gKHXfwVx-GAtKr4WKkq0gJny3HGwavE3sYOsPwCfjbeJq26iAvywePx875jjybLnmK0xLTEr7d-HJzqljtd2yVGiAjO72WnuCjooqSFuH8nPskehbBFKIUVf5idEEoF4RyfZr83tvbB95DHQRljde5d3m8uVyHv1S7k0ectOEjZ6Dvf7t8cjglf_LAN5FejctEmlYo26bw5uLjQTUfrbLRTOKgIIVeuyXe-21_XC_YX5AO040Q_zh4Y1QV4Mu9n2df3776cf1xcfPqwPl9dLDSnNC4KbeqirE0FROCqgkZhYYQyhBTpqlS8VMASWTFAmLKi4ESD0Y1STQ2GCnqWPZ98d50Pcm5ikJhiSgoqGE7EeiIar7ZyN9heDXvplZXXCT-0Ug3R6g5kUzXIYCQI5YJp4KpSmggmENTcMCiT19u52lj30GhwqUHdkenxjbPfZOu_S1pwjBhLBi9ng8FfjRCi7G3Q0HXKgR_Tu1M5TgrGeUJf_IX--3fLiWpV-oB1xqe6Oq0Gequ9A2NTfkUJIpwl6yR4dSRITISfsVVjCHL9efMf7OUxyyZWDz6EAcxtVzCShwm_eb48TLicJzzJnt3t6K3oZqTpH3Xy-xE</recordid><startdate>20130101</startdate><enddate>20130101</enddate><creator>Ciandrini, Luca</creator><creator>Stansfield, Ian</creator><creator>Romano, M Carmen</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>ISN</scope><scope>ISR</scope><scope>3V.</scope><scope>7QO</scope><scope>7QP</scope><scope>7TK</scope><scope>7TM</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AL</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>JQ2</scope><scope>K7-</scope><scope>K9.</scope><scope>LK8</scope><scope>M0N</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>Q9U</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20130101</creationdate><title>Ribosome traffic on mRNAs maps to gene ontology: genome-wide quantification of translation initiation rates and polysome size regulation</title><author>Ciandrini, Luca ; Stansfield, Ian ; Romano, M Carmen</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c633t-5cfb57bf9e28199eda18f8af2255cf7a67ae463394e01345562cefcdaadbef383</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Biology</topic><topic>Biotechnology</topic><topic>Classification</topic><topic>Codon</topic><topic>Councils</topic><topic>Gene expression</topic><topic>Genetic translation</topic><topic>Genetics</topic><topic>Genome</topic><topic>Genomes</topic><topic>Genomics</topic><topic>Life sciences</topic><topic>Messenger RNA</topic><topic>Models, Theoretical</topic><topic>Ontology</topic><topic>Physics</topic><topic>Physiological aspects</topic><topic>Polyribosomes - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>Directory of Open Access Journals</collection><jtitle>PLoS computational biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Ciandrini, Luca</au><au>Stansfield, Ian</au><au>Romano, M Carmen</au><au>Rzhetsky, Andrey</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Ribosome traffic on mRNAs maps to gene ontology: genome-wide quantification of translation initiation rates and polysome size regulation</atitle><jtitle>PLoS computational biology</jtitle><addtitle>PLoS Comput Biol</addtitle><date>2013-01-01</date><risdate>2013</risdate><volume>9</volume><issue>1</issue><spage>e1002866</spage><epage>e1002866</epage><pages>e1002866-e1002866</pages><issn>1553-7358</issn><issn>1553-734X</issn><eissn>1553-7358</eissn><abstract>To understand the complex relationship governing transcript abundance and the level of the encoded protein, we integrate genome-wide experimental data of ribosomal density on mRNAs with a novel stochastic model describing ribosome traffic dynamics during translation elongation. This analysis reveals that codon arrangement, rather than simply codon bias, has a key role in determining translational efficiency. It also reveals that translation output is governed both by initiation efficiency and elongation dynamics. By integrating genome-wide experimental data sets with simulation of ribosome traffic on all Saccharomyces cerevisiae ORFs, mRNA-specific translation initiation rates are for the first time estimated across the entire transcriptome. Our analysis identifies different classes of mRNAs characterised by their initiation rates, their ribosome traffic dynamics, and by their response to ribosome availability. Strikingly, this classification based on translational dynamics maps onto key gene ontological classifications, revealing evolutionary optimisation of translation responses to be strongly influenced by gene function.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>23382661</pmid><doi>10.1371/journal.pcbi.1002866</doi><oa>free_for_read</oa></addata></record> |
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subjects | Biology Biotechnology Classification Codon Councils Gene expression Genetic translation Genetics Genome Genomes Genomics Life sciences Messenger RNA Models, Theoretical Ontology Physics Physiological aspects Polyribosomes - metabolism Protein Biosynthesis Proteins Ribosomes - metabolism RNA, Messenger - genetics RNA, Messenger - metabolism Stochastic models Stochastic Processes Yeast |
title | Ribosome traffic on mRNAs maps to gene ontology: genome-wide quantification of translation initiation rates and polysome size regulation |
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