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GroEL dependency affects codon usage—support for a critical role of misfolding in gene evolution
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| Zeitschriftentitel: | Molecular Systems Biology |
|---|---|
| Personen und Körperschaften: | , |
| In: | Molecular Systems Biology, 6, 2010, 1 |
| Format: | E-Article |
| Sprache: | Englisch |
| veröffentlicht: |
Springer Science and Business Media LLC
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| Schlagwörter: |
| author_facet |
Warnecke, Tobias Hurst, Laurence D Warnecke, Tobias Hurst, Laurence D |
|---|---|
| author |
Warnecke, Tobias Hurst, Laurence D |
| spellingShingle |
Warnecke, Tobias Hurst, Laurence D Molecular Systems Biology GroEL dependency affects codon usage—support for a critical role of misfolding in gene evolution Applied Mathematics Computational Theory and Mathematics General Agricultural and Biological Sciences General Immunology and Microbiology General Biochemistry, Genetics and Molecular Biology Information Systems |
| author_sort |
warnecke, tobias |
| spelling |
Warnecke, Tobias Hurst, Laurence D 1744-4292 1744-4292 Springer Science and Business Media LLC Applied Mathematics Computational Theory and Mathematics General Agricultural and Biological Sciences General Immunology and Microbiology General Biochemistry, Genetics and Molecular Biology Information Systems http://dx.doi.org/10.1038/msb.2009.94 <jats:p>It has recently been suggested that the use of optimal codons limits mistranslation‐induced protein misfolding, yet evidence for this remains largely circumstantial. In contrast, molecular chaperones have long been recognized to play crucial roles in misfolding prevention and remedy. We propose that putative error limitation in <jats:italic>cis</jats:italic> can be elucidated by examining the interaction between codon usage and chaperoning processes. Using <jats:italic>Escherichia coli</jats:italic> as a model system, we find that codon optimality covaries with dependency on the chaperonin GroEL. Sporadic but not obligate substrates of GroEL exhibit higher average codon adaptation and are conspicuously enriched for optimal codons at structurally sensitive sites. Further, codon optimality of sporadic clients is more conserved in the <jats:italic>E. coli</jats:italic> clone <jats:italic>Shigella dysenteriae</jats:italic>. We suggest that highly expressed genes cannot routinely use GroEL for error control so that codon usage has evolved to provide complementary error limitation. These findings provide independent evidence for a role of misfolding in shaping gene evolution and highlight the need to co‐characterize adaptations in <jats:italic>cis</jats:italic> and <jats:italic>trans</jats:italic> to unravel the workings of integrated molecular systems.</jats:p> GroEL dependency affects codon usage—support for a critical role of misfolding in gene evolution Molecular Systems Biology |
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10.1038/msb.2009.94 |
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| title |
GroEL dependency affects codon usage—support for a critical role of misfolding in gene evolution |
| title_unstemmed |
GroEL dependency affects codon usage—support for a critical role of misfolding in gene evolution |
| title_full |
GroEL dependency affects codon usage—support for a critical role of misfolding in gene evolution |
| title_fullStr |
GroEL dependency affects codon usage—support for a critical role of misfolding in gene evolution |
| title_full_unstemmed |
GroEL dependency affects codon usage—support for a critical role of misfolding in gene evolution |
| title_short |
GroEL dependency affects codon usage—support for a critical role of misfolding in gene evolution |
| title_sort |
groel dependency affects codon usage—support for a critical role of misfolding in gene evolution |
| topic |
Applied Mathematics Computational Theory and Mathematics General Agricultural and Biological Sciences General Immunology and Microbiology General Biochemistry, Genetics and Molecular Biology Information Systems |
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http://dx.doi.org/10.1038/msb.2009.94 |
| publishDate |
2010 |
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| description |
<jats:p>It has recently been suggested that the use of optimal codons limits mistranslation‐induced protein misfolding, yet evidence for this remains largely circumstantial. In contrast, molecular chaperones have long been recognized to play crucial roles in misfolding prevention and remedy. We propose that putative error limitation in <jats:italic>cis</jats:italic> can be elucidated by examining the interaction between codon usage and chaperoning processes. Using <jats:italic>Escherichia coli</jats:italic> as a model system, we find that codon optimality covaries with dependency on the chaperonin GroEL. Sporadic but not obligate substrates of GroEL exhibit higher average codon adaptation and are conspicuously enriched for optimal codons at structurally sensitive sites. Further, codon optimality of sporadic clients is more conserved in the <jats:italic>E. coli</jats:italic> clone <jats:italic>Shigella dysenteriae</jats:italic>. We suggest that highly expressed genes cannot routinely use GroEL for error control so that codon usage has evolved to provide complementary error limitation. These findings provide independent evidence for a role of misfolding in shaping gene evolution and highlight the need to co‐characterize adaptations in <jats:italic>cis</jats:italic> and <jats:italic>trans</jats:italic> to unravel the workings of integrated molecular systems.</jats:p> |
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| description | <jats:p>It has recently been suggested that the use of optimal codons limits mistranslation‐induced protein misfolding, yet evidence for this remains largely circumstantial. In contrast, molecular chaperones have long been recognized to play crucial roles in misfolding prevention and remedy. We propose that putative error limitation in <jats:italic>cis</jats:italic> can be elucidated by examining the interaction between codon usage and chaperoning processes. Using <jats:italic>Escherichia coli</jats:italic> as a model system, we find that codon optimality covaries with dependency on the chaperonin GroEL. Sporadic but not obligate substrates of GroEL exhibit higher average codon adaptation and are conspicuously enriched for optimal codons at structurally sensitive sites. Further, codon optimality of sporadic clients is more conserved in the <jats:italic>E. coli</jats:italic> clone <jats:italic>Shigella dysenteriae</jats:italic>. We suggest that highly expressed genes cannot routinely use GroEL for error control so that codon usage has evolved to provide complementary error limitation. These findings provide independent evidence for a role of misfolding in shaping gene evolution and highlight the need to co‐characterize adaptations in <jats:italic>cis</jats:italic> and <jats:italic>trans</jats:italic> to unravel the workings of integrated molecular systems.</jats:p> |
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| spelling | Warnecke, Tobias Hurst, Laurence D 1744-4292 1744-4292 Springer Science and Business Media LLC Applied Mathematics Computational Theory and Mathematics General Agricultural and Biological Sciences General Immunology and Microbiology General Biochemistry, Genetics and Molecular Biology Information Systems http://dx.doi.org/10.1038/msb.2009.94 <jats:p>It has recently been suggested that the use of optimal codons limits mistranslation‐induced protein misfolding, yet evidence for this remains largely circumstantial. In contrast, molecular chaperones have long been recognized to play crucial roles in misfolding prevention and remedy. We propose that putative error limitation in <jats:italic>cis</jats:italic> can be elucidated by examining the interaction between codon usage and chaperoning processes. Using <jats:italic>Escherichia coli</jats:italic> as a model system, we find that codon optimality covaries with dependency on the chaperonin GroEL. Sporadic but not obligate substrates of GroEL exhibit higher average codon adaptation and are conspicuously enriched for optimal codons at structurally sensitive sites. Further, codon optimality of sporadic clients is more conserved in the <jats:italic>E. coli</jats:italic> clone <jats:italic>Shigella dysenteriae</jats:italic>. We suggest that highly expressed genes cannot routinely use GroEL for error control so that codon usage has evolved to provide complementary error limitation. These findings provide independent evidence for a role of misfolding in shaping gene evolution and highlight the need to co‐characterize adaptations in <jats:italic>cis</jats:italic> and <jats:italic>trans</jats:italic> to unravel the workings of integrated molecular systems.</jats:p> GroEL dependency affects codon usage—support for a critical role of misfolding in gene evolution Molecular Systems Biology |
| spellingShingle | Warnecke, Tobias, Hurst, Laurence D, Molecular Systems Biology, GroEL dependency affects codon usage—support for a critical role of misfolding in gene evolution, Applied Mathematics, Computational Theory and Mathematics, General Agricultural and Biological Sciences, General Immunology and Microbiology, General Biochemistry, Genetics and Molecular Biology, Information Systems |
| title | GroEL dependency affects codon usage—support for a critical role of misfolding in gene evolution |
| title_full | GroEL dependency affects codon usage—support for a critical role of misfolding in gene evolution |
| title_fullStr | GroEL dependency affects codon usage—support for a critical role of misfolding in gene evolution |
| title_full_unstemmed | GroEL dependency affects codon usage—support for a critical role of misfolding in gene evolution |
| title_short | GroEL dependency affects codon usage—support for a critical role of misfolding in gene evolution |
| title_sort | groel dependency affects codon usage—support for a critical role of misfolding in gene evolution |
| title_unstemmed | GroEL dependency affects codon usage—support for a critical role of misfolding in gene evolution |
| topic | Applied Mathematics, Computational Theory and Mathematics, General Agricultural and Biological Sciences, General Immunology and Microbiology, General Biochemistry, Genetics and Molecular Biology, Information Systems |
| url | http://dx.doi.org/10.1038/msb.2009.94 |