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Trade-offs between tRNA abundance and mRNA secondary structure support smoothing of translation elongation rate

  • Translation of protein from mRNA is a complex multi-step process that occurs at a non-uniform rate. Variability in ribosome speed along an mRNA enables refinement of the proteome and plays a critical role in protein biogenesis. Detailed single protein studies have found both tRNA abundance and mRNA secondary structure as key modulators of translation elongation rate, but recent genome-wide ribosome profiling experiments have not observed significant influence of either on translation efficiency. Here we provide evidence that this results from an inherent trade-off between these factors. We find codons pairing to high-abundance tRNAs are preferentially used in regions of high secondary structure content, while codons read by significantly less abundant tRNAs are located in lowly structured regions. By considering long stretches of high and low mRNA secondary structure in Saccharomyces cerevisiae and Escherichia coli and comparing them to randomized-gene models and experimental expression data, we were able to distinguish clearTranslation of protein from mRNA is a complex multi-step process that occurs at a non-uniform rate. Variability in ribosome speed along an mRNA enables refinement of the proteome and plays a critical role in protein biogenesis. Detailed single protein studies have found both tRNA abundance and mRNA secondary structure as key modulators of translation elongation rate, but recent genome-wide ribosome profiling experiments have not observed significant influence of either on translation efficiency. Here we provide evidence that this results from an inherent trade-off between these factors. We find codons pairing to high-abundance tRNAs are preferentially used in regions of high secondary structure content, while codons read by significantly less abundant tRNAs are located in lowly structured regions. By considering long stretches of high and low mRNA secondary structure in Saccharomyces cerevisiae and Escherichia coli and comparing them to randomized-gene models and experimental expression data, we were able to distinguish clear selective pressures and increased protein expression for specific codon choices. The trade-off between secondary structure and tRNA-concentration based codon choice allows for compensation of their independent effects on translation, helping to smooth overall translational speed and reducing the chance of potentially detrimental points of excessively slow or fast ribosome movement.show moreshow less

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Metadaten
Author:Thomas E. Gorochowski, Zoya IgnatovaGND, Roel A. L. Bovenberg, Johannes A. Roubos
URN:urn:nbn:de:kobv:517-opus4-441340
DOI:https://doi.org/10.25932/publishup-44134
ISSN:1866-8372
Parent Title (German):Postprints der Universität Potsdam : Mathematisch-Naturwissenschaftliche Reihe
Series (Serial Number):Postprints der Universität Potsdam : Mathematisch-Naturwissenschaftliche Reihe (816)
Document Type:Postprint
Language:English
Date of first Publication:2020/02/12
Year of Completion:2015
Publishing Institution:Universität Potsdam
Release Date:2020/02/12
Tag:Escherichia-coli genome; bias; codon adaptation index; folding free-energies; gene-expression; in-vivo; protein-synthesis; sequence determinants; single ribosomes; usage
Issue:816
Pagenumber:13
Source:Nucleic Acids Research 43 (2015) 6 DOI: 10.1093/nar/gkv199
Organizational units:Mathematisch-Naturwissenschaftliche Fakultät
Dewey Decimal Classification:5 Naturwissenschaften und Mathematik / 57 Biowissenschaften; Biologie / 570 Biowissenschaften; Biologie
Peer Review:Referiert
Publication Way:Open Access
Licence (German):License LogoCreative Commons - Namensnennung, 4.0 International
Notes extern:Bibliographieeintrag der Originalveröffentlichung/Quelle