A nutrient-driven tRNA modification alters translational fidelity and genome-wide protein coding across an animal genus.
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 Droso...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2014-12-01
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| Series: | PLoS Biology |
| Online Access: | https://doi.org/10.1371/journal.pbio.1002015 |
| _version_ | 1819031321864830976 |
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| author | John M Zaborske Vanessa L Bauer DuMont Edward W J Wallace Tao Pan Charles F Aquadro D Allan Drummond |
| author_facet | John M Zaborske Vanessa L Bauer DuMont Edward W J Wallace Tao Pan Charles F Aquadro D Allan Drummond |
| author_sort | John M Zaborske |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-12-21T06:44:12Z |
| format | Article |
| id | doaj.art-188428a8e76041d283d970c8e04a15fd |
| institution | Directory Open Access Journal |
| issn | 1544-9173 1545-7885 |
| language | English |
| last_indexed | 2024-12-21T06:44:12Z |
| publishDate | 2014-12-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Biology |
| spelling | doaj.art-188428a8e76041d283d970c8e04a15fd2022-12-21T19:12:38ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852014-12-011212e100201510.1371/journal.pbio.1002015A nutrient-driven tRNA modification alters translational fidelity and genome-wide protein coding across an animal genus.John M ZaborskeVanessa L Bauer DuMontEdward W J WallaceTao PanCharles F AquadroD Allan DrummondNatural 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.https://doi.org/10.1371/journal.pbio.1002015 |
| spellingShingle | John M Zaborske Vanessa L Bauer DuMont Edward W J Wallace Tao Pan Charles F Aquadro D Allan Drummond A nutrient-driven tRNA modification alters translational fidelity and genome-wide protein coding across an animal genus. PLoS Biology |
| title | A nutrient-driven tRNA modification alters translational fidelity and genome-wide protein coding across an animal genus. |
| title_full | A nutrient-driven tRNA modification alters translational fidelity and genome-wide protein coding across an animal genus. |
| title_fullStr | A nutrient-driven tRNA modification alters translational fidelity and genome-wide protein coding across an animal genus. |
| title_full_unstemmed | A nutrient-driven tRNA modification alters translational fidelity and genome-wide protein coding across an animal genus. |
| title_short | A nutrient-driven tRNA modification alters translational fidelity and genome-wide protein coding across an animal genus. |
| title_sort | nutrient driven trna modification alters translational fidelity and genome wide protein coding across an animal genus |
| url | https://doi.org/10.1371/journal.pbio.1002015 |
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