A Nutrient-Driven tRNA Modification Alters Translational Fidelity and Genome-wide Protein Coding across an Animal Genus
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{"title"=>"A Nutrient-Driven tRNA Modification Alters Translational Fidelity and Genome-wide Protein Coding across an Animal Genus", "type"=>"journal", "authors"=>[{"first_name"=>"John M.", "last_name"=>"Zaborske", "scopus_author_id"=>"6508281288"}, {"first_name"=>"Vanessa L.", "last_name"=>"Bauer DuMont", "scopus_author_id"=>"15753250100"}, {"first_name"=>"Edward W.J.", "last_name"=>"Wallace", "scopus_author_id"=>"36572978300"}, {"first_name"=>"Tao", "last_name"=>"Pan", "scopus_author_id"=>"7202203221"}, {"first_name"=>"Charles F.", "last_name"=>"Aquadro", "scopus_author_id"=>"7006405958"}, {"first_name"=>"D. Allan", "last_name"=>"Drummond", "scopus_author_id"=>"8524598400"}], "year"=>2014, "source"=>"PLoS Biology", "identifiers"=>{"pui"=>"602601598", "issn"=>"15457885", "isbn"=>"1545-7885", "doi"=>"10.1371/journal.pbio.1002015", "scopus"=>"2-s2.0-84924084262", "pmid"=>"25923688", "sgr"=>"84924084262"}, "id"=>"b5844da2-a2f3-3488-bbad-56ad203ffa16", "abstract"=>"Natural selection favors efficient expression of encoded proteins, but the causes, mechanisms, and fitness consequences of evolved coding changes remain an area of aggressive inquiry. We report a large-scale reversal in the relative translational accuracy of codons across 12 fly species in the Drosophila/Sophophora genus. Because the reversal involves pairs of codons that are read by the same genomically encoded tRNAs, we hypothesize, and show by direct measurement, that a tRNA anticodon modification from guanosine to queuosine has coevolved with these genomic changes. Queuosine modification is present in most organisms but its function remains unclear. Modification levels vary across developmental stages in D. melanogaster, and, consistent with a causal effect, genes maximally expressed at each stage display selection for codons that are most accurate given stage-specific queuosine modification levels. In a kinetic model, the known increased affinity of queuosine-modified tRNA for ribosomes increases the accuracy of cognate codons while reducing the accuracy of near-cognate codons. Levels of queuosine modification in D. melanogaster reflect bioavailability of the precursor queuine, which eukaryotes scavenge from the tRNAs of bacteria and absorb in the gut. These results reveal a strikingly direct mechanism by which recoding of entire genomes results from changes in utilization of a nutrient.", "link"=>"http://www.mendeley.com/research/nutrientdriven-trna-modification-alters-translational-fidelity-genomewide-protein-coding-across-anim", "reader_count"=>83, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>6, "Researcher"=>26, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>21, "Student > Postgraduate"=>7, "Other"=>1, "Student > Master"=>7, "Student > Bachelor"=>6, "Lecturer > Senior Lecturer"=>2, "Professor"=>4}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>6, "Researcher"=>26, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>21, "Student > Postgraduate"=>7, "Other"=>1, "Student > Master"=>7, "Student > Bachelor"=>6, "Lecturer > Senior Lecturer"=>2, "Professor"=>4}, "reader_count_by_subject_area"=>{"Environmental Science"=>3, "Biochemistry, Genetics and Molecular Biology"=>15, "Agricultural and Biological Sciences"=>56, "Medicine and Dentistry"=>2, "Pharmacology, Toxicology and Pharmaceutical Science"=>1, "Chemistry"=>1, "Social Sciences"=>1, "Computer Science"=>3}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>2}, "Chemistry"=>{"Chemistry"=>1}, "Social Sciences"=>{"Social Sciences"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>56}, "Computer Science"=>{"Computer Science"=>3}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>15}, "Environmental Science"=>{"Environmental Science"=>3}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}}, "reader_count_by_country"=>{"Czech Republic"=>2, "Netherlands"=>2, "United States"=>1, "United Kingdom"=>2, "India"=>1}, "group_count"=>3}

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  • {"files"=>["https://ndownloader.figshare.com/files/1831775"], "description"=>"<p>(A) Data from White and colleagues shows tRNA modification over the course of development, including three instar larval stages. (B) Akashi selection scores derived from genes maximally expressed at each of six developmental stages (0- and 3-hour embryos, larva, pupa, and adult males [M] and females [F]). Values from pooling both embryo stages and both adult stages are also shown between the two pooled groups. Test codons (red points) are those showing the strongest accuracy-selection shifts across the drosophilid phylogeny, hypothesized to be driven by queuosine tRNA modification (cf. <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002015#pbio-1002015-g001\" target=\"_blank\">Figure 1</a>). Control codons differ from test codons by a single nucleotide, highlighted. For test codons, the pooled embryo versus larva and versus pupa stage, and the larva and pupa stage versus pooled adult stages, are significant at <i>p</i><0.05 (one-tailed Wilcox signed-rank test). For control codons, all contrasts are insignificant using identical tests (<i>p</i>>0.2). Median values for test and control codons across all stages are shown as solid horizontal lines. Error bars show standard error on the mean. Gray lines show changes across each synonymous test-codon pair, and a solid red line tracks the mean value across pooled-embryo, larva, pupa, and pooled-adult stages. (C) Akashi selection scores for codons cognate to Q-modified tRNAs correlate with the Q-modification levels of these tRNAs. Modification levels for the three Asn isoaccepting tRNAs were averaged, and mean values for embryo, larva, pupa, and adult were used. Colors as in (A). Gray line shows linear best fit. Spearman rank correlation <i>r</i> = 0.61, <i>p</i><0.02 for raw values, and <i>r</i> = 0.63, <i>p</i><0.01 after subtracting means from each synonymous family.</p>", "links"=>[], "tags"=>["reversal", "fitness consequences", "Queuosine modification", "genomic changes", "ribosomes increases", "genomes results", "stage display selection", "precursor queuine", "translational accuracy", "Animal Genus Natural selection", "Modification levels", "mechanism", "eukaryotes scavenge", "coding changes", "genes maximally", "tRNA anticodon modification", "melanogaster"], "article_id"=>1266109, "categories"=>["Uncategorised"], "users"=>["John M. Zaborske", "Vanessa L. Bauer DuMont", "Edward W. J. Wallace", "Tao Pan", "Charles F. Aquadro", "D. Allan Drummond"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1002015.g004", "stats"=>{"downloads"=>0, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Queuosine_tRNA_modification_covaries_with_relative_codon_accuracy_across_developmental_stages_in_D_melanogaster_/1266109", "title"=>"Queuosine tRNA modification covaries with relative codon accuracy across developmental stages in <i>D. melanogaster</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-12-09 02:55:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/1831771"], "description"=>"<p>(A) Northern blot of total <i>D. melanogaster</i> third-instar larval tRNA using tRNA<sup>Tyr</sup>-specific probe resolves two major bands (left) after electrophoretic separation on an acryloyl aminophenylboronic acid gel (APB gel); when <i>cis</i>-diols are oxidized with periodate, tRNA runs as a single band (right). (B) APB gel measurements of Q modification produce similar stage-specific results to an independent method in <i>D. melanogaster</i>. (C) Separation of total tRNA from four species at two developmental stages by APB gel followed by Northern blotting using probes specific for each species' tRNA<sup>His</sup>, tRNA<sup>Asn</sup>, and tRNA<sup>Tyr</sup> reveals shifts in Q modification (<i>mel</i>, <i>D. melanogaster</i>; <i>pse</i>, <i>D. pseudoobscura</i>; <i>wil</i>, <i>D. willistoni</i>; <i>vir</i>, <i>D. virilis</i>). (D) Quantification of the data in (C) (cf. <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002015#pbio.1002015.s005\" target=\"_blank\">Data S1</a>); error bars show standard error in measurement. (E) The Akashi selection scores for NAU to NAC, over all genes, track the proportion of Q-modified tRNA in adult flies across species. Colors as in (D). Bars show standard error of the mean (SEM) for modification levels and 95% confidence interval for selection scores. Spearman rank correlation <i>r</i> = 0.61, <i>p</i><0.05 for raw values, and <i>r</i> = 0.73, <i>p</i><0.01 after subtracting means from each synonymous family.</p>", "links"=>[], "tags"=>["reversal", "fitness consequences", "Queuosine modification", "genomic changes", "ribosomes increases", "genomes results", "stage display selection", "precursor queuine", "translational accuracy", "Animal Genus Natural selection", "Modification levels", "mechanism", "eukaryotes scavenge", "coding changes", "genes maximally", "tRNA anticodon modification", "melanogaster"], "article_id"=>1266104, "categories"=>["Uncategorised"], "users"=>["John M. Zaborske", "Vanessa L. Bauer DuMont", "Edward W. J. Wallace", "Tao Pan", "Charles F. Aquadro", "D. Allan Drummond"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1002015.g003", "stats"=>{"downloads"=>1, "page_views"=>33, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Queuosine_tRNA_modification_covaries_with_relative_codon_accuracy_across_the_drosophilid_phylogeny_/1266104", "title"=>"Queuosine tRNA modification covaries with relative codon accuracy across the drosophilid phylogeny.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-12-09 02:55:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/1831803", "https://ndownloader.figshare.com/files/1831804", "https://ndownloader.figshare.com/files/1831805", "https://ndownloader.figshare.com/files/1831806", "https://ndownloader.figshare.com/files/1831807", "https://ndownloader.figshare.com/files/1831809"], "description"=>"<div><p>Natural selection favors efficient expression of encoded proteins, but the causes, mechanisms, and fitness consequences of evolved coding changes remain an area of aggressive inquiry. We report a large-scale reversal in the relative translational accuracy of codons across 12 fly species in the <i>Drosophila</i>/<i>Sophophora</i> genus. Because the reversal involves pairs of codons that are read by the same genomically encoded tRNAs, we hypothesize, and show by direct measurement, that a tRNA anticodon modification from guanosine to queuosine has coevolved with these genomic changes. Queuosine modification is present in most organisms but its function remains unclear. Modification levels vary across developmental stages in <i>D. melanogaster</i>, and, consistent with a causal effect, genes maximally expressed at each stage display selection for codons that are most accurate given stage-specific queuosine modification levels. In a kinetic model, the known increased affinity of queuosine-modified tRNA for ribosomes increases the accuracy of cognate codons while reducing the accuracy of near-cognate codons. Levels of queuosine modification in <i>D. melanogaster</i> reflect bioavailability of the precursor queuine, which eukaryotes scavenge from the tRNAs of bacteria and absorb in the gut. These results reveal a strikingly direct mechanism by which recoding of entire genomes results from changes in utilization of a nutrient.</p></div>", "links"=>[], "tags"=>["reversal", "fitness consequences", "Queuosine modification", "genomic changes", "ribosomes increases", "genomes results", "stage display selection", "precursor queuine", "translational accuracy", "Animal Genus Natural selection", "Modification levels", "mechanism", "eukaryotes scavenge", "coding changes", "genes maximally", "tRNA anticodon modification", "melanogaster"], "article_id"=>1266117, "categories"=>["Uncategorised"], "users"=>["John M. Zaborske", "Vanessa L. Bauer DuMont", "Edward W. J. Wallace", "Tao Pan", "Charles F. Aquadro", "D. Allan Drummond"], "doi"=>["https://dx.doi.org/10.1371/journal.pbio.1002015.s001", "https://dx.doi.org/10.1371/journal.pbio.1002015.s002", "https://dx.doi.org/10.1371/journal.pbio.1002015.s003", "https://dx.doi.org/10.1371/journal.pbio.1002015.s004", "https://dx.doi.org/10.1371/journal.pbio.1002015.s005", "https://dx.doi.org/10.1371/journal.pbio.1002015.s006"], "stats"=>{"downloads"=>23, "page_views"=>29, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_A_Nutrient_Driven_tRNA_Modification_Alters_Translational_Fidelity_and_Genome_wide_Protein_Coding_across_an_Animal_Genus_/1266117", "title"=>"A Nutrient-Driven tRNA Modification Alters Translational Fidelity and Genome-wide Protein Coding across an Animal Genus", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2014-12-09 02:55:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/1831766"], "description"=>"<p>(A) The sequence of <i>D. melanogaster</i> tRNA<sup>Tyr</sup> (after Suter and colleagues <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002015#pbio.1002015-Suter1\" target=\"_blank\">[62]</a>) shows modification of guanosine (G) to queuosine (Q) in the anticodon position corresponding to the third-position (wobble) base of the codon. Positions of <i>cis</i>-diol moieties are highlighted in gray. (B) Guanosine (top) and queuosine (bottom); <i>cis</i>-diol highlighted in gray. Arrows point toward the primary ribose moiety which is not shown. (C) Guanosine and queuosine binding cytosine (C, top) and uracil (U, bottom).</p>", "links"=>[], "tags"=>["reversal", "fitness consequences", "Queuosine modification", "genomic changes", "ribosomes increases", "genomes results", "stage display selection", "precursor queuine", "translational accuracy", "Animal Genus Natural selection", "Modification levels", "mechanism", "eukaryotes scavenge", "coding changes", "genes maximally", "tRNA anticodon modification", "melanogaster"], "article_id"=>1266099, "categories"=>["Uncategorised"], "users"=>["John M. Zaborske", "Vanessa L. Bauer DuMont", "Edward W. J. Wallace", "Tao Pan", "Charles F. Aquadro", "D. Allan Drummond", "D. Allan Drummond"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1002015.g002", "stats"=>{"downloads"=>5, "page_views"=>156, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Queuosine_modification_alters_features_of_tRNA_anticodons_/1266099", "title"=>"Queuosine modification alters features of tRNA anticodons.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-12-09 02:55:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/1831799"], "description"=>"<p>Akashi selection scores for test and control codon pairs.</p>", "links"=>[], "tags"=>["reversal", "fitness consequences", "Queuosine modification", "genomic changes", "ribosomes increases", "genomes results", "stage display selection", "precursor queuine", "translational accuracy", "Animal Genus Natural selection", "Modification levels", "mechanism", "eukaryotes scavenge", "coding changes", "genes maximally", "tRNA anticodon modification", "melanogaster"], "article_id"=>1266113, "categories"=>["Uncategorised"], "users"=>["John M. Zaborske", "Vanessa L. Bauer DuMont", "Edward W. J. Wallace", "Tao Pan", "Charles F. Aquadro", "D. Allan Drummond", "D. Allan Drummond"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1002015.t001", "stats"=>{"downloads"=>2, "page_views"=>73, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Akashi_selection_scores_for_test_and_control_codon_pairs_/1266113", "title"=>"Akashi selection scores for test and control codon pairs.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-12-09 02:55:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/1831765"], "description"=>"<p>(A) Overview of Akashi selection scores, the average population-scaled fitness difference between a synonymous codon change at a conserved amino acid site compared to the same change at variable site within the same gene. Selection scores are symmetric, such that score(codon X to codon Y) = −score(Y to X). All possible synonymous codon-to-codon pairs are shown, with the order of X and Y chosen such that the <i>D. melanogaster</i> values are positive. (B) Akashi selection scores for all 2-fold-degenerate C/U-ending codons. Error bars indicate 95% confidence intervals.</p>", "links"=>[], "tags"=>["reversal", "fitness consequences", "Queuosine modification", "genomic changes", "ribosomes increases", "genomes results", "stage display selection", "precursor queuine", "translational accuracy", "Animal Genus Natural selection", "Modification levels", "mechanism", "eukaryotes scavenge", "coding changes", "genes maximally", "tRNA anticodon modification", "melanogaster"], "article_id"=>1266098, "categories"=>["Uncategorised"], "users"=>["John M. Zaborske", "Vanessa L. Bauer DuMont", "Edward W. J. Wallace", "Tao Pan", "Charles F. Aquadro", "D. Allan Drummond", "D. Allan Drummond"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1002015.g001", "stats"=>{"downloads"=>0, "page_views"=>24, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Relative_codon_translational_accuracy_shifts_coherently_across_the_drosophilid_phylogeny_/1266098", "title"=>"Relative codon translational accuracy shifts coherently across the drosophilid phylogeny.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-12-09 02:55:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/1831798"], "description"=>"<p>(A) Schematic representation of tRNA and codon relationships. Black lines represent cognate tRNA/codon relationships, and gray lines represent non-cognate (misreading) relationships. (B) A kinetic model produces rates for each tRNA reading the two asparagine codons AAC and AAU (cf. <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002015#pbio.1002015.s006\" target=\"_blank\">Listing S1</a>). Misreading rates by tRNA<sup>Thr</sup>(IGU) are multiplied by 1,000 for visibility. The translation rate constant is proportional to the translation rate assuming equal tRNA concentrations, which we do for simplicity. (C) Graphical view of how rates given in (B) combine to produce speeds and error rates for each codon/tRNA pair. In the example, tRNA<sup>Asn</sup>(QUU) reads AAC faster and more accurately. In contrast, tRNA<sup>Asn</sup>(GUU) reads AAC faster, but AAU more accurately. (D) Quantitative error rates and translation speeds as a function of Q-modification in the model. (E) Modeled accuracy of the threonine codon ACC, which is assumed to be misread by tRNA<sup>Asn</sup>, changes with Q-modification, whereas ACG, which is not misread by tRNA<sup>Asn</sup>, does not, again resulting in a shift in relative accuracy.</p>", "links"=>[], "tags"=>["reversal", "fitness consequences", "Queuosine modification", "genomic changes", "ribosomes increases", "genomes results", "stage display selection", "precursor queuine", "translational accuracy", "Animal Genus Natural selection", "Modification levels", "mechanism", "eukaryotes scavenge", "coding changes", "genes maximally", "tRNA anticodon modification", "melanogaster"], "article_id"=>1266111, "categories"=>["Uncategorised"], "users"=>["John M. Zaborske", "Vanessa L. Bauer DuMont", "Edward W. J. Wallace", "Tao Pan", "Charles F. Aquadro", "D. Allan Drummond"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1002015.g005", "stats"=>{"downloads"=>1, "page_views"=>19, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_A_kinetic_competition_model_illustrates_how_Q_modification_alone_can_reverse_relative_codon_accuracy_/1266111", "title"=>"A kinetic competition model illustrates how Q modification alone can reverse relative codon accuracy.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-12-09 02:55:36"}

PMC Usage Stats | Further Information

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  • {"unique-ip"=>"7", "full-text"=>"6", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"5"}
  • {"unique-ip"=>"16", "full-text"=>"14", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2019", "month"=>"8"}
  • {"unique-ip"=>"8", "full-text"=>"10", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"9"}
  • {"unique-ip"=>"12", "full-text"=>"11", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2019", "month"=>"10"}
  • {"unique-ip"=>"10", "full-text"=>"3", "pdf"=>"7", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"12"}
  • {"unique-ip"=>"8", "full-text"=>"6", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"2"}

Relative Metric

{"start_date"=>"2014-01-01T00:00:00Z", "end_date"=>"2014-12-31T00:00:00Z", "subject_areas"=>[]}
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