In eubacteria, unlike eukaryotes, there is no evidence for selection favouring fail-safe 3' additional stop codons
Errors throughout gene expression are likely deleterious, hence genomes are under selection to ameliorate their consequences. Additional stop codons (ASCs) are in-frame nonsense 'codons' downstream of the primary stop which may be read by translational machinery should the primary stop hav...
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Published in | PLoS genetics Vol. 15; no. 9; p. e1008386 |
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Main Authors | , |
Format | Journal Article |
Language | English |
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17.09.2019
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Abstract | Errors throughout gene expression are likely deleterious, hence genomes are under selection to ameliorate their consequences. Additional stop codons (ASCs) are in-frame nonsense 'codons' downstream of the primary stop which may be read by translational machinery should the primary stop have been accidentally read through. Prior evidence in several eukaryotes suggests that ASCs are selected to prevent potentially-deleterious consequences of read-through. We extend this evidence showing that enrichment of ASCs is common but not universal for single cell eukaryotes. By contrast, there is limited evidence as to whether the same is true in other taxa. Here, we provide the first systematic test of the hypothesis that ASCs act as a fail-safe mechanism in eubacteria, a group with high read-through rates. Contra to the predictions of the hypothesis we find: there is paucity, not enrichment, of ASCs downstream; substitutions that degrade stops are more frequent in-frame than out-of-frame in 3' sequence; highly expressed genes are no more likely to have ASCs than lowly expressed genes; usage of the leakiest primary stop (TGA) in highly expressed genes does not predict ASC enrichment even compared to usage of non-leaky stops (TAA) in lowly expressed genes, beyond downstream codon +1. Any effect at the codon immediately proximal to the primary stop can be accounted for by a preference for a T/U residue immediately following the stop, although if anything, TT- and TC- starting codons are preferred. We conclude that there is no compelling evidence for ASC selection in eubacteria. This presents an unusual case in which the same error could be solved by the same mechanism in eukaryotes and prokaryotes but is not. We discuss two possible explanations: that, owing to the absence of nonsense mediated decay, bacteria may solve read-through via gene truncation and in eukaryotes certain prion states cause raised read-through rates. |
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AbstractList | Errors throughout gene expression are likely deleterious, hence genomes are under selection to ameliorate their consequences. Additional stop codons (ASCs) are in-frame nonsense ‘codons’ downstream of the primary stop which may be read by translational machinery should the primary stop have been accidentally read through. Prior evidence in several eukaryotes suggests that ASCs are selected to prevent potentially-deleterious consequences of read-through. We extend this evidence showing that enrichment of ASCs is common but not universal for single cell eukaryotes. By contrast, there is limited evidence as to whether the same is true in other taxa. Here, we provide the first systematic test of the hypothesis that ASCs act as a fail-safe mechanism in eubacteria, a group with high read-through rates. Contra to the predictions of the hypothesis we find: there is paucity, not enrichment, of ASCs downstream; substitutions that degrade stops are more frequent in-frame than out-of-frame in 3’ sequence; highly expressed genes are no more likely to have ASCs than lowly expressed genes; usage of the leakiest primary stop (TGA) in highly expressed genes does not predict ASC enrichment even compared to usage of non-leaky stops (TAA) in lowly expressed genes, beyond downstream codon +1. Any effect at the codon immediately proximal to the primary stop can be accounted for by a preference for a T/U residue immediately following the stop, although if anything, TT- and TC- starting codons are preferred. We conclude that there is no compelling evidence for ASC selection in eubacteria. This presents an unusual case in which the same error could be solved by the same mechanism in eukaryotes and prokaryotes but is not. We discuss two possible explanations: that, owing to the absence of nonsense mediated decay, bacteria may solve read-through via gene truncation and in eukaryotes certain prion states cause raised read-through rates. Errors throughout gene expression are likely deleterious, hence genomes are under selection to ameliorate their consequences. Additional stop codons (ASCs) are in-frame nonsense ‘codons’ downstream of the primary stop which may be read by translational machinery should the primary stop have been accidentally read through. Prior evidence in several eukaryotes suggests that ASCs are selected to prevent potentially-deleterious consequences of read-through. We extend this evidence showing that enrichment of ASCs is common but not universal for single cell eukaryotes. By contrast, there is limited evidence as to whether the same is true in other taxa. Here, we provide the first systematic test of the hypothesis that ASCs act as a fail-safe mechanism in eubacteria, a group with high read-through rates. Contra to the predictions of the hypothesis we find: there is paucity, not enrichment, of ASCs downstream; substitutions that degrade stops are more frequent in-frame than out-of-frame in 3’ sequence; highly expressed genes are no more likely to have ASCs than lowly expressed genes; usage of the leakiest primary stop (TGA) in highly expressed genes does not predict ASC enrichment even compared to usage of non-leaky stops (TAA) in lowly expressed genes, beyond downstream codon +1. Any effect at the codon immediately proximal to the primary stop can be accounted for by a preference for a T/U residue immediately following the stop, although if anything, TT- and TC- starting codons are preferred. We conclude that there is no compelling evidence for ASC selection in eubacteria. This presents an unusual case in which the same error could be solved by the same mechanism in eukaryotes and prokaryotes but is not. We discuss two possible explanations: that, owing to the absence of nonsense mediated decay, bacteria may solve read-through via gene truncation and in eukaryotes certain prion states cause raised read-through rates. In all organisms, gene expression is error-prone. One such error, translational read-through, occurs where the primary stop codon of an expressed gene is missed by the translational machinery. Failure to terminate is likely to be costly, hence genomes are under selection to prevent this from happening. One proposed error-proofing strategy involves in-frame proximal additional stop codons (ASCs) which may act as a ‘fail-safe’ mechanism by providing another opportunity for translation to terminate. There is evidence for ASC enrichment in several eukaryotes. We extend this evidence showing it to be common but not universal in single celled eukaryotes. However, the situation in bacteria is poorly understood, despite bacteria having high read-through rates. Here, we test the fail-safe hypothesis within a broad range of bacteria. To our surprise, we find that not only are ASCs not enriched, but they may even be selected against. This provides evidence for an unusual circumstance where eukaryotes and prokaryotes could solve the same problem the same way but don’t. What are we to make of this? We suggest that if read-through is the problem, ASCs are not necessarily the expected solution. Owing to the absence of nonsense-mediated decay, a process that makes gene truncation in eukaryotes less viable, we propose bacteria may rescue a leaky stop by mutation that creates a new stop upstream. Alternatively, raised read-through rates in some particular conditions in eukaryotes might explain the difference. |
Audience | Academic |
Author | Hurst, Laurence D Ho, Alexander T |
AuthorAffiliation | University of Warwick, UNITED KINGDOM Milner Centre for Evolution, University of Bath, Bath, United Kingdom |
AuthorAffiliation_xml | – name: Milner Centre for Evolution, University of Bath, Bath, United Kingdom – name: University of Warwick, UNITED KINGDOM |
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BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31527909$$D View this record in MEDLINE/PubMed |
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CitedBy_id | crossref_primary_10_1093_gbe_evac115 crossref_primary_10_1093_molbev_msaa046 crossref_primary_10_1093_molbev_msaa210 crossref_primary_10_1039_D3TB01805A crossref_primary_10_1371_journal_pbio_3001588 crossref_primary_10_3390_life12030431 crossref_primary_10_1093_molbev_msab326 crossref_primary_10_1371_journal_pone_0237405 |
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Copyright | COPYRIGHT 2019 Public Library of Science 2019 Ho, Hurst. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. 2019 Ho, Hurst 2019 Ho, Hurst |
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Snippet | Errors throughout gene expression are likely deleterious, hence genomes are under selection to ameliorate their consequences. Additional stop codons (ASCs) are... |
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SubjectTerms | 3' Untranslated Regions - genetics Bacteria Bacteria - genetics Biochemistry Biology and Life Sciences Codon, Nonsense - genetics Codon, Terminator - genetics Codons Costs E coli Eukaryota - genetics Evolution Evolution, Molecular Gene expression Gene Expression - genetics Genes Genome Genomes Genomics Hypotheses Informatics Mutation Nonsense Mediated mRNA Decay - genetics Observations Open Reading Frames - genetics Physiological aspects Prokaryotes Proteins Studies |
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Title | In eubacteria, unlike eukaryotes, there is no evidence for selection favouring fail-safe 3' additional stop codons |
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