Variation in Release Factor Abundance Is Not Needed to Explain Trends in Bacterial Stop Codon Usage
Abstract In bacteria stop codons are recognized by one of two class I release factors (RF1) recognizing TAG, RF2 recognizing TGA, and TAA being recognized by both. Variation across bacteria in the relative abundance of RF1 and RF2 is thus hypothesized to select for different TGA/TAG usage. This has...
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Published in | Molecular biology and evolution Vol. 39; no. 1 |
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Main Authors | , |
Format | Journal Article |
Language | English |
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Oxford University Press
07.01.2022
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Abstract | Abstract
In bacteria stop codons are recognized by one of two class I release factors (RF1) recognizing TAG, RF2 recognizing TGA, and TAA being recognized by both. Variation across bacteria in the relative abundance of RF1 and RF2 is thus hypothesized to select for different TGA/TAG usage. This has been supported by correlations between TAG:TGA ratios and RF1:RF2 ratios across multiple bacterial species, potentially also explaining why TAG usage is approximately constant despite extensive variation in GC content. It is, however, possible that stop codon trends are determined by other forces and that RF ratios adapt to stop codon usage, rather than vice versa. Here, we determine which direction of the causal arrow is the more parsimonious. Our results support the notion that RF1/RF2 ratios become adapted to stop codon usage as the same trends, notably the anomalous TAG behavior, are seen in contexts where RF1:RF2 ratios cannot be, or are unlikely to be, causative, that is, at 3′untranslated sites never used for translation termination, in intragenomic analyses, and across archaeal species (that possess only one RF1). We conclude that specifics of RF biology are unlikely to fully explain TGA/TAG relative usage. We discuss why the causal relationships for the evolution of synonymous stop codon usage might be different from those affecting synonymous sense codon usage, noting that transitions between TGA and TAG require two-point mutations one of which is likely to be deleterious. |
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AbstractList | In bacteria stop codons are recognized by one of two class I release factors (RF1) recognizing TAG, RF2 recognizing TGA, and TAA being recognized by both. Variation across bacteria in the relative abundance of RF1 and RF2 is thus hypothesized to select for different TGA/TAG usage. This has been supported by correlations between TAG:TGA ratios and RF1:RF2 ratios across multiple bacterial species, potentially also explaining why TAG usage is approximately constant despite extensive variation in GC content. It is, however, possible that stop codon trends are determined by other forces and that RF ratios adapt to stop codon usage, rather than vice versa. Here, we determine which direction of the causal arrow is the more parsimonious. Our results support the notion that RF1/RF2 ratios become adapted to stop codon usage as the same trends, notably the anomalous TAG behavior, are seen in contexts where RF1:RF2 ratios cannot be, or are unlikely to be, causative, that is, at 3untranslated sites never used for translation termination, in intragenomic analyses, and across archaeal species (that possess only one RF1). We conclude that specifics of RF biology are unlikely to fully explain TGA/TAG relative usage. We discuss why the causal relationships for the evolution of synonymous stop codon usage might be different from those affecting synonymous sense codon usage, noting that transitions between TGA and TAG require two-point mutations one of which is likely to be deleterious. Key words: release factor, stop codons, translation termination, molecular evolution. Abstract In bacteria stop codons are recognized by one of two class I release factors (RF1) recognizing TAG, RF2 recognizing TGA, and TAA being recognized by both. Variation across bacteria in the relative abundance of RF1 and RF2 is thus hypothesized to select for different TGA/TAG usage. This has been supported by correlations between TAG:TGA ratios and RF1:RF2 ratios across multiple bacterial species, potentially also explaining why TAG usage is approximately constant despite extensive variation in GC content. It is, however, possible that stop codon trends are determined by other forces and that RF ratios adapt to stop codon usage, rather than vice versa. Here, we determine which direction of the causal arrow is the more parsimonious. Our results support the notion that RF1/RF2 ratios become adapted to stop codon usage as the same trends, notably the anomalous TAG behavior, are seen in contexts where RF1:RF2 ratios cannot be, or are unlikely to be, causative, that is, at 3′untranslated sites never used for translation termination, in intragenomic analyses, and across archaeal species (that possess only one RF1). We conclude that specifics of RF biology are unlikely to fully explain TGA/TAG relative usage. We discuss why the causal relationships for the evolution of synonymous stop codon usage might be different from those affecting synonymous sense codon usage, noting that transitions between TGA and TAG require two-point mutations one of which is likely to be deleterious. In bacteria stop codons are recognized by one of two class I release factors (RF1) recognizing TAG, RF2 recognizing TGA, and TAA being recognized by both. Variation across bacteria in the relative abundance of RF1 and RF2 is thus hypothesized to select for different TGA/TAG usage. This has been supported by correlations between TAG:TGA ratios and RF1:RF2 ratios across multiple bacterial species, potentially also explaining why TAG usage is approximately constant despite extensive variation in GC content. It is, however, possible that stop codon trends are determined by other forces and that RF ratios adapt to stop codon usage, rather than vice versa. Here, we determine which direction of the causal arrow is the more parsimonious. Our results support the notion that RF1/RF2 ratios become adapted to stop codon usage as the same trends, notably the anomalous TAG behavior, are seen in contexts where RF1:RF2 ratios cannot be, or are unlikely to be, causative, that is, at 3′untranslated sites never used for translation termination, in intragenomic analyses, and across archaeal species (that possess only one RF1). We conclude that specifics of RF biology are unlikely to fully explain TGA/TAG relative usage. We discuss why the causal relationships for the evolution of synonymous stop codon usage might be different from those affecting synonymous sense codon usage, noting that transitions between TGA and TAG require two-point mutations one of which is likely to be deleterious. |
Audience | Academic |
Author | Hurst, Laurence D Ho, Alexander T |
AuthorAffiliation | Milner Centre for Evolution, University of Bath , Bath, United Kingdom |
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Author_xml | – sequence: 1 givenname: Alexander T orcidid: 0000-0001-7824-8709 surname: Ho fullname: Ho, Alexander T email: a.t.ho@bath.ac.uk organization: Milner Centre for Evolution, University of Bath, Bath, United Kingdom – sequence: 2 givenname: Laurence D orcidid: 0000-0002-1002-1054 surname: Hurst fullname: Hurst, Laurence D organization: Milner Centre for Evolution, University of Bath, Bath, United Kingdom |
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Cites_doi | 10.1371/journal.pgen.1008141 10.1093/molbev/msq102 10.1038/s41598-017-12619-6 10.1504/IJCBDD.2014.061645 10.1186/s12864-016-2692-4 10.1074/jbc.M114.606632 10.1038/msb.2010.59 10.1038/s41559-017-0425-y 10.1038/35080577 10.1126/science.1241459 10.1073/pnas.82.11.3616 10.1093/genetics/159.2.907 10.1093/nar/18.22.6517 10.1006/jmbi.1993.1124 10.1128/mr.53.3.273-298.1989 10.1093/molbev/msx116 10.1128/MCB.17.6.3164 10.1371/journal.pgen.1007254 10.1093/nar/gks660 10.1534/genetics.114.162842 10.1006/bbrc.1995.1775 10.1371/journal.pgen.1001115 10.1093/dnares/dsx030 10.1016/S0014-5793(02)02301-3 10.1371/journal.pgen.1008386 10.1016/S0959-437X(98)80038-5 10.1016/0378-1119(88)90553-7 10.1038/286123a0 10.1371/journal.pgen.1004941 10.1186/gb-2005-6-4-r31 10.1101/cshperspect.a032664 10.1093/molbev/msn173 10.1093/oxfordjournals.molbev.a026368 10.1093/genetics/149.1.37 10.1016/S1097-2765(01)00415-4 10.1038/s41598-018-27570-3 10.1093/nar/gkx1315 10.1146/annurev-genom-082908-150001 10.1371/journal.pgen.1001107 10.1093/molbev/msw107 10.1186/1745-6150-7-30 10.1038/msb.2011.14 10.1534/genetics.116.193961 10.1016/0022-2836(81)90003-6 10.1186/gb-2001-2-4-research0010 10.1093/molbev/msaa129 10.1371/journal.pgen.1008493 10.1093/molbev/msu087 10.1371/journal.pgen.1002603 10.1093/molbev/msaa210 10.1093/molbev/msr005 10.1016/0022-2836(73)90299-4 10.3390/ijms20081981 10.1111/j.1601-5223.1998.00173.x 10.1371/journal.pgen.1004363 10.1371/journal.pone.0127911 10.1007/BF02109476 10.1016/0022-2836(89)90260-X 10.1038/nrg2899 10.1093/molbev/msg022 10.4161/cc.8.19.9625 10.1016/S0168-1656(98)00073-X 10.1038/sj.embor.7400538 10.1007/s00239-009-9220-y 10.1038/372701a0 10.1038/283041a0 10.1016/0022-2836(84)90027-5 |
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Keywords | translation termination release factor molecular evolution stop codons |
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References | Adachi (2022012520025482800_msab326-B2) 2009; 68 Strigini (2022012520025482800_msab326-B60) 1973; 75 Higgs (2022012520025482800_msab326-B24) 2008; 25 Jackson (2022012520025482800_msab326-B31) 2012 Sanchez (2022012520025482800_msab326-B55) 1998; 63 Vogel (2022012520025482800_msab326-B66) 2010; 6 Hershberg (2022012520025482800_msab326-B23) 2010; 6 Korkmaz (2022012520025482800_msab326-B35) 2014; 289 Tate (2022012520025482800_msab326-B61) 1999; 64 Craigen (2022012520025482800_msab326-B10) 1985; 82 McFarlane (2022012520025482800_msab326-B45) 2009; 8 Weissman (2022012520025482800_msab326-B69) 2019; 15 Donly (2022012520025482800_msab326-B13) 1990; 18 Burroughs (2022012520025482800_msab326-B7) 2019; 20 Lajoie (2022012520025482800_msab326-B37) 2013; 342 Duret (2022012520025482800_msab326-B15) 2009; 10 Grosjean (2022012520025482800_msab326-B22) 2014; 10 Qian (2022012520025482800_msab326-B52) 2012; 8 van Weringh (2022012520025482800_msab326-B63) 2011; 28 Du (2022012520025482800_msab326-B14) 2017; 24 Galtier (2022012520025482800_msab326-B19) 2001; 159 Jorgensen (2022012520025482800_msab326-B32) 1993; 230 Chithambaram (2022012520025482800_msab326-B9) 2014; 197 Frolova (2022012520025482800_msab326-B18) 1994; 372 Gingold (2022012520025482800_msab326-B21) 2011; 7 Bossi (2022012520025482800_msab326-B6) 1980; 286 Foerstner (2022012520025482800_msab326-B17) 2005; 6 Wei (2022012520025482800_msab326-B68) 2016; 33 Geller (2022012520025482800_msab326-B20) 1980; 283 Belinky (2022012520025482800_msab326-B5) 2017; 7 McEwan (2022012520025482800_msab326-B44) 1998; 128 Parker (2022012520025482800_msab326-B48) 1989; 53 Cridge (2022012520025482800_msab326-B11) 2018; 46 Abdalaal (2022012520025482800_msab326-B1) 2020; 37 Chithambaram (2022012520025482800_msab326-B8) 2014; 31 Panicker (2022012520025482800_msab326-B47) 2015; 10 Ikemura (2022012520025482800_msab326-B29) 1981; 151 Lassalle (2022012520025482800_msab326-B38) 2015; 11 Akashi (2022012520025482800_msab326-B3) 1998; 8 Kumar (2022012520025482800_msab326-B36) 2017; 34 Major (2022012520025482800_msab326-B43) 2002; 514 Wei (2022012520025482800_msab326-B67) 2017; 205 Long (2022012520025482800_msab326-B42) 2018; 2 Shields (2022012520025482800_msab326-B57) 1990; 31 Rodnina (2022012520025482800_msab326-B54) 2018; 10 Trotta (2022012520025482800_msab326-B62) 2016; 17 Varenne (2022012520025482800_msab326-B64) 1984; 180 Ho (2022012520025482800_msab326-B26) 2021; 38 Liang (2022012520025482800_msab326-B41) 2005; 6 Knight (2022012520025482800_msab326-B33) 2001; 2 Kobayashi (2022012520025482800_msab326-B34) 2012; 40 Li (2022012520025482800_msab326-B40) 2019; 15 Sorensen (2022012520025482800_msab326-B59) 1989; 207 Ikemura (2022012520025482800_msab326-B28) 1992 Ho (2022012520025482800_msab326-B27) 2019; 15 Hildebrand (2022012520025482800_msab326-B25) 2010; 6 Plotkin (2022012520025482800_msab326-B49) 2011; 12 Sharp (2022012520025482800_msab326-B56) 1988; 63 Povolotskaya (2022012520025482800_msab326-B50) 2012; 7 Xia (2022012520025482800_msab326-B70) 1998; 149 Smith (2022012520025482800_msab326-B58) 2018; 14 Eyre-Walker (2022012520025482800_msab326-B16) 2001; 2 Vestergaard (2022012520025482800_msab326-B65) 2001; 8 Inagaki (2022012520025482800_msab326-B30) 2000; 17 Prabhakaran (2022012520025482800_msab326-B51) 2014; 7 Le Goff (2022012520025482800_msab326-B39) 1997; 17 Ran (2022012520025482800_msab326-B53) 2010; 27 Belinky (2022012520025482800_msab326-B4) 2018; 8 Daubin (2022012520025482800_msab326-B12) 2003; 20 Meng (2022012520025482800_msab326-B46) 1995; 211 |
References_xml | – volume: 15 start-page: e1008141 issue: 5 year: 2019 ident: 2022012520025482800_msab326-B40 article-title: Stop-codon read-through arises largely from molecular errors and is generally nonadaptive publication-title: PLoS Genet doi: 10.1371/journal.pgen.1008141 contributor: fullname: Li – volume: 27 start-page: 2129 issue: 9 year: 2010 ident: 2022012520025482800_msab326-B53 article-title: The influence of anticodon-codon interactions and modified bases on codon usage bias in bacteria publication-title: Mol Biol Evol doi: 10.1093/molbev/msq102 contributor: fullname: Ran – volume: 7 start-page: 12422 issue: 1 year: 2017 ident: 2022012520025482800_msab326-B5 article-title: Selection on start codons in prokaryotes and potential compensatory nucleotide substitutions publication-title: Sci Rep doi: 10.1038/s41598-017-12619-6 contributor: fullname: Belinky – volume: 7 start-page: 168 issue: 2–3 year: 2014 ident: 2022012520025482800_msab326-B51 article-title: Aeromonas phages encode tRNAs for their overused codons publication-title: Int J Comput Biol Drug Des doi: 10.1504/IJCBDD.2014.061645 contributor: fullname: Prabhakaran – volume: 17 start-page: 366 issue: 17 year: 2016 ident: 2022012520025482800_msab326-B62 article-title: Selective forces and mutational biases drive stop codon usage in the human genome: a comparison with sense codon usage publication-title: BMC Genomics doi: 10.1186/s12864-016-2692-4 contributor: fullname: Trotta – volume: 289 start-page: 30334 issue: 44 year: 2014 ident: 2022012520025482800_msab326-B35 article-title: Comprehensive analysis of stop codon usage in bacteria and its correlation with release factor abundance publication-title: J Biol Chem doi: 10.1074/jbc.M114.606632 contributor: fullname: Korkmaz – volume: 6 start-page: 400 issue: 1 year: 2010 ident: 2022012520025482800_msab326-B66 article-title: Sequence signatures and mRNA concentration can explain two-thirds of protein abundance variation in a human cell line publication-title: Mol Syst Biol doi: 10.1038/msb.2010.59 contributor: fullname: Vogel – start-page: 45 volume-title: Advances in protein chemistry and structural biology year: 2012 ident: 2022012520025482800_msab326-B31 contributor: fullname: Jackson – volume: 2 start-page: 237 issue: 2 year: 2018 ident: 2022012520025482800_msab326-B42 article-title: Evolutionary determinants of genome-wide nucleotide composition publication-title: Nat Ecol Evol doi: 10.1038/s41559-017-0425-y contributor: fullname: Long – volume: 2 start-page: 549 issue: 7 year: 2001 ident: 2022012520025482800_msab326-B16 article-title: The evolution of isochores publication-title: Nat Rev Genet doi: 10.1038/35080577 contributor: fullname: Eyre-Walker – volume: 342 start-page: 357 issue: 6156 year: 2013 ident: 2022012520025482800_msab326-B37 article-title: Genomically recoded organisms expand biological functions publication-title: Science doi: 10.1126/science.1241459 contributor: fullname: Lajoie – volume: 82 start-page: 3616 issue: 11 year: 1985 ident: 2022012520025482800_msab326-B10 article-title: Bacterial peptide chain release factors: conserved primary structure and possible frameshift regulation of release factor 2 publication-title: Proc Natl Acad Sci USA doi: 10.1073/pnas.82.11.3616 contributor: fullname: Craigen – volume: 159 start-page: 907 issue: 2 year: 2001 ident: 2022012520025482800_msab326-B19 article-title: GC-content evolution in mammalian genomes: the biased gene conversion hypothesis publication-title: Genetics doi: 10.1093/genetics/159.2.907 contributor: fullname: Galtier – volume: 18 start-page: 6517 issue: 22 year: 1990 ident: 2022012520025482800_msab326-B13 article-title: Frameshift autoregulation in the gene for Escherichia coli release factor 2: partly functional mutants result in frameshift enhancement publication-title: Nucleic Acids Res doi: 10.1093/nar/18.22.6517 contributor: fullname: Donly – volume: 230 start-page: 41 issue: 1 year: 1993 ident: 2022012520025482800_msab326-B32 article-title: Release factor-dependent false stops are infrequent in Escherichia coli publication-title: J Mol Biol doi: 10.1006/jmbi.1993.1124 contributor: fullname: Jorgensen – volume: 53 start-page: 273 issue: 3 year: 1989 ident: 2022012520025482800_msab326-B48 article-title: Errors and alternatives in reading the universal genetic code publication-title: Microbiol Rev doi: 10.1128/mr.53.3.273-298.1989 contributor: fullname: Parker – volume: 34 start-page: 1812 issue: 7 year: 2017 ident: 2022012520025482800_msab326-B36 article-title: TimeTree: a resource for timelines, timetrees, and divergence times publication-title: Mol Biol Evol doi: 10.1093/molbev/msx116 contributor: fullname: Kumar – volume: 17 start-page: 3164 issue: 6 year: 1997 ident: 2022012520025482800_msab326-B39 article-title: Overexpression of human release factor 1 alone was an antisuppressor effect in human cells publication-title: Mol Cell Biol doi: 10.1128/MCB.17.6.3164 contributor: fullname: Le Goff – volume: 14 start-page: e1007254 issue: 3 year: 2018 ident: 2022012520025482800_msab326-B58 article-title: Large scale variation in the rate of germ-line de novo mutation, base composition, divergence and diversity in humans publication-title: PLoS Genet doi: 10.1371/journal.pgen.1007254 contributor: fullname: Smith – volume: 40 start-page: 9319 issue: 18 year: 2012 ident: 2022012520025482800_msab326-B34 article-title: Structural basis for translation termination by archaeal RF1 and GTP-bound EF1 alpha complex publication-title: Nucleic Acids Res doi: 10.1093/nar/gks660 contributor: fullname: Kobayashi – volume: 197 start-page: 301 issue: 1 year: 2014 ident: 2022012520025482800_msab326-B9 article-title: The effect of mutation and selection on codon adaptation in Escherichia coli bacteriophage publication-title: Genetics doi: 10.1534/genetics.114.162842 contributor: fullname: Chithambaram – start-page: 87 volume-title: Transfer RNA in protein synthesis year: 1992 ident: 2022012520025482800_msab326-B28 contributor: fullname: Ikemura – volume: 211 start-page: 40 issue: 1 year: 1995 ident: 2022012520025482800_msab326-B46 article-title: Analysis of translational termination of recombinant human methionyl-neurotrophin 3 in Escherichia coli publication-title: Biochem Biophys Res Commun doi: 10.1006/bbrc.1995.1775 contributor: fullname: Meng – volume: 6 start-page: e1001115 issue: 9 year: 2010 ident: 2022012520025482800_msab326-B23 article-title: Evidence that mutation is universally biased towards AT in bacteria publication-title: PLoS Genet doi: 10.1371/journal.pgen.1001115 contributor: fullname: Hershberg – volume: 24 start-page: 623 issue: 6 year: 2017 ident: 2022012520025482800_msab326-B14 article-title: Co-adaption of tRNA gene copy number and amino acid usage influences translation rates in three life domains publication-title: DNA Res doi: 10.1093/dnares/dsx030 contributor: fullname: Du – volume: 514 start-page: 84 issue: 1 year: 2002 ident: 2022012520025482800_msab326-B43 article-title: Tandem termination signals: myth or reality? publication-title: FEBS Lett doi: 10.1016/S0014-5793(02)02301-3 contributor: fullname: Major – volume: 15 start-page: e1008386 issue: 9 year: 2019 ident: 2022012520025482800_msab326-B27 article-title: In eubacteria, unlike eukaryotes, there is no evidence for selection favouring fail-safe 3' additional stop codons publication-title: PLoS Genet doi: 10.1371/journal.pgen.1008386 contributor: fullname: Ho – volume: 8 start-page: 688 issue: 6 year: 1998 ident: 2022012520025482800_msab326-B3 article-title: Translational selection and molecular evolution publication-title: Curr Opin Genet Dev doi: 10.1016/S0959-437X(98)80038-5 contributor: fullname: Akashi – volume: 63 start-page: 141 issue: 1 year: 1988 ident: 2022012520025482800_msab326-B56 article-title: Selective differences among translation termination codons publication-title: Gene doi: 10.1016/0378-1119(88)90553-7 contributor: fullname: Sharp – volume: 286 start-page: 123 issue: 5769 year: 1980 ident: 2022012520025482800_msab326-B6 article-title: The influence of codon context on genetic-code translation publication-title: Nature doi: 10.1038/286123a0 contributor: fullname: Bossi – volume: 11 start-page: e1004941 issue: 2 year: 2015 ident: 2022012520025482800_msab326-B38 article-title: GC-content evolution in bacterial genomes: the biased gene conversion hypothesis expands publication-title: PLoS Genet doi: 10.1371/journal.pgen.1004941 contributor: fullname: Lassalle – volume: 6 start-page: R31 issue: 4 year: 2005 ident: 2022012520025482800_msab326-B41 article-title: Conservation of tandem stop codons in yeasts publication-title: Genome Biol doi: 10.1186/gb-2005-6-4-r31 contributor: fullname: Liang – volume: 10 start-page: a032664 issue: 9 year: 2018 ident: 2022012520025482800_msab326-B54 article-title: Translation in prokaryotes publication-title: Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a032664 contributor: fullname: Rodnina – volume: 25 start-page: 2279 issue: 11 year: 2008 ident: 2022012520025482800_msab326-B24 article-title: Coevolution of codon usage and tRNA genes leads to alternative stable states of biased codon usage publication-title: Mol Biol Evol doi: 10.1093/molbev/msn173 contributor: fullname: Higgs – volume: 17 start-page: 882 issue: 6 year: 2000 ident: 2022012520025482800_msab326-B30 article-title: Evolution of the eukaryotic translation termination system: origins of release factors publication-title: Mol Biol Evol doi: 10.1093/oxfordjournals.molbev.a026368 contributor: fullname: Inagaki – volume: 149 start-page: 37 issue: 1 year: 1998 ident: 2022012520025482800_msab326-B70 article-title: How optimized is the translational machinery in Escherichia coli, Salmonella typhimurium and Saccharomyces cerevisiae? publication-title: Genetics doi: 10.1093/genetics/149.1.37 contributor: fullname: Xia – volume: 64 start-page: 1342 issue: 12 year: 1999 ident: 2022012520025482800_msab326-B61 article-title: UGA: a dual signal for ‘stop’ and for recoding in protein synthesis publication-title: Biochemistry (Mosc) contributor: fullname: Tate – volume: 8 start-page: 1375 issue: 6 year: 2001 ident: 2022012520025482800_msab326-B65 article-title: Bacterial polypeptide release factor RF2 is structurally distinct from eukaryotic eRF1 publication-title: Mol Cell doi: 10.1016/S1097-2765(01)00415-4 contributor: fullname: Vestergaard – volume: 8 start-page: 9260 issue: 1 year: 2018 ident: 2022012520025482800_msab326-B4 article-title: Purifying and positive selection in the evolution of stop codons publication-title: Sci Rep doi: 10.1038/s41598-018-27570-3 contributor: fullname: Belinky – volume: 46 start-page: 1927 issue: 4 year: 2018 ident: 2022012520025482800_msab326-B11 article-title: Eukaryotic translational termination efficiency is influenced by the 3' nucleotides within the ribosomal mRNA channel publication-title: Nucleic Acids Res doi: 10.1093/nar/gkx1315 contributor: fullname: Cridge – volume: 10 start-page: 285 issue: 1 year: 2009 ident: 2022012520025482800_msab326-B15 article-title: Biased gene conversion and the evolution of mammalian genomic landscapes publication-title: Annu Rev Genomics Hum Genet doi: 10.1146/annurev-genom-082908-150001 contributor: fullname: Duret – volume: 6 start-page: e1001107 issue: 9 year: 2010 ident: 2022012520025482800_msab326-B25 article-title: Evidence of selection upon genomic GC-content in bacteria publication-title: PLoS Genet doi: 10.1371/journal.pgen.1001107 contributor: fullname: Hildebrand – volume: 33 start-page: 2357 issue: 9 year: 2016 ident: 2022012520025482800_msab326-B68 article-title: Coevolution between stop codon usage and release factors in bacterial species publication-title: Mol Biol Evol doi: 10.1093/molbev/msw107 contributor: fullname: Wei – volume: 7 start-page: 30 issue: 1 year: 2012 ident: 2022012520025482800_msab326-B50 article-title: Stop codons in bacteria are not selectively equivalent publication-title: Biol Direct doi: 10.1186/1745-6150-7-30 contributor: fullname: Povolotskaya – volume: 7 start-page: 481 issue: 1 year: 2011 ident: 2022012520025482800_msab326-B21 article-title: Determinants of translation efficiency and accuracy publication-title: Mol Syst Biol doi: 10.1038/msb.2011.14 contributor: fullname: Gingold – volume: 205 start-page: 539 issue: 2 year: 2017 ident: 2022012520025482800_msab326-B67 article-title: The role of +4U as an extended translation termination signal in bacteria publication-title: Genetics doi: 10.1534/genetics.116.193961 contributor: fullname: Wei – volume: 151 start-page: 389 issue: 3 year: 1981 ident: 2022012520025482800_msab326-B29 article-title: Correlation between the abundance of Escherichia coli transfer RNAs and the occurrence of the respective codons in its protein genes: a proposal for a synonymous codon choice that is optimal for the E. coli translational system publication-title: J Mol Biol doi: 10.1016/0022-2836(81)90003-6 contributor: fullname: Ikemura – volume: 2 start-page: RESEARCH0010 issue: 4 year: 2001 ident: 2022012520025482800_msab326-B33 article-title: A simple model based on mutation and selection explains trends in codon and amino-acid usage and GC composition within and across genomes publication-title: Genome Biol doi: 10.1186/gb-2001-2-4-research0010 contributor: fullname: Knight – volume: 37 start-page: 2918 issue: 10 year: 2020 ident: 2022012520025482800_msab326-B1 article-title: Collateral toxicity limits the evolution of bacterial release factor 2 toward total omnipotence publication-title: Mol Biol Evol doi: 10.1093/molbev/msaa129 contributor: fullname: Abdalaal – volume: 15 start-page: e1008493 issue: 11 year: 2019 ident: 2022012520025482800_msab326-B69 article-title: Linking high GC content to the repair of double strand breaks in prokaryotic genomes publication-title: PLoS Genet doi: 10.1371/journal.pgen.1008493 contributor: fullname: Weissman – volume: 31 start-page: 1606 issue: 6 year: 2014 ident: 2022012520025482800_msab326-B8 article-title: Differential codon adaptation between dsDNA and ssDNA phages in Escherichia coli publication-title: Mol Biol Evol doi: 10.1093/molbev/msu087 contributor: fullname: Chithambaram – volume: 8 start-page: e1002603 issue: 3 year: 2012 ident: 2022012520025482800_msab326-B52 article-title: Balanced codon usage optimizes eukaryotic translational efficiency publication-title: PLoS Genet doi: 10.1371/journal.pgen.1002603 contributor: fullname: Qian – volume: 38 start-page: 244 issue: 1 year: 2021 ident: 2022012520025482800_msab326-B26 article-title: Effective population size predicts local rates but not local mitigation of read-through errors in eukaryotic genes publication-title: Mol Biol Evol doi: 10.1093/molbev/msaa210 contributor: fullname: Ho – volume: 28 start-page: 1827 issue: 6 year: 2011 ident: 2022012520025482800_msab326-B63 article-title: HIV-1 modulates the tRNA pool to improve translation efficiency publication-title: Mol Biol Evol doi: 10.1093/molbev/msr005 contributor: fullname: van Weringh – volume: 75 start-page: 659 issue: 4 year: 1973 ident: 2022012520025482800_msab326-B60 article-title: Analysis of specific misreading in Escherichia coli publication-title: J Mol Biol doi: 10.1016/0022-2836(73)90299-4 contributor: fullname: Strigini – volume: 20 start-page: 1981 issue: 8 year: 2019 ident: 2022012520025482800_msab326-B7 article-title: The origin and evolution of release factors: implications for translation termination, ribosome rescue, and quality control pathways publication-title: Int J Mol Sci doi: 10.3390/ijms20081981 contributor: fullname: Burroughs – volume: 128 start-page: 173 issue: 2 year: 1998 ident: 2022012520025482800_msab326-B44 article-title: Nitrogen-fixing aerobic bacteria have higher genomic GC content than non-fixing species within the same genus publication-title: Hereditas doi: 10.1111/j.1601-5223.1998.00173.x contributor: fullname: McEwan – volume: 10 start-page: e1004363 issue: 5 year: 2014 ident: 2022012520025482800_msab326-B22 article-title: Predicting the minimal translation apparatus: lessons from the reductive evolution of mollicutes publication-title: PLoS Genet doi: 10.1371/journal.pgen.1004363 contributor: fullname: Grosjean – volume: 10 start-page: e0127911 issue: 5 year: 2015 ident: 2022012520025482800_msab326-B47 article-title: The effect of an alternate start codon on heterologous expression of a PhoA fusion protein in Mycoplasma gallisepticum publication-title: PLoS One doi: 10.1371/journal.pone.0127911 contributor: fullname: Panicker – volume: 31 start-page: 71 issue: 2 year: 1990 ident: 2022012520025482800_msab326-B57 article-title: Switches in species-specific codon preferences: the influence of mutation biases publication-title: J Mol Evol doi: 10.1007/BF02109476 contributor: fullname: Shields – volume: 207 start-page: 365 issue: 2 year: 1989 ident: 2022012520025482800_msab326-B59 article-title: Codon usage determines translation rate in Escherichia coli publication-title: J Mol Biol doi: 10.1016/0022-2836(89)90260-X contributor: fullname: Sorensen – volume: 12 start-page: 32 issue: 1 year: 2011 ident: 2022012520025482800_msab326-B49 article-title: Synonymous but not the same: the causes and consequences of codon bias publication-title: Nat Rev Genet doi: 10.1038/nrg2899 contributor: fullname: Plotkin – volume: 20 start-page: 471 issue: 4 year: 2003 ident: 2022012520025482800_msab326-B12 article-title: G+C3 structuring along the genome: a common feature in prokaryotes publication-title: Mol Biol Evol doi: 10.1093/molbev/msg022 contributor: fullname: Daubin – volume: 8 start-page: 3102 issue: 19 year: 2009 ident: 2022012520025482800_msab326-B45 article-title: tRNA genes in eukaryotic genome organization and reorganization publication-title: Cell Cycle doi: 10.4161/cc.8.19.9625 contributor: fullname: McFarlane – volume: 63 start-page: 179 issue: 3 year: 1998 ident: 2022012520025482800_msab326-B55 article-title: Elimination of an HuIFN alpha 2b readthrough species, produced in Escherichia coli, by replacing its natural translational stop signal publication-title: J Biotechnol doi: 10.1016/S0168-1656(98)00073-X contributor: fullname: Sanchez – volume: 6 start-page: 1208 issue: 12 year: 2005 ident: 2022012520025482800_msab326-B17 article-title: Environments shape the nucleotide composition of genomes publication-title: EMBO Rep doi: 10.1038/sj.embor.7400538 contributor: fullname: Foerstner – volume: 68 start-page: 424 issue: 4 year: 2009 ident: 2022012520025482800_msab326-B2 article-title: Tandem stop codons in ciliates that reassign stop codons publication-title: J Mol Evol doi: 10.1007/s00239-009-9220-y contributor: fullname: Adachi – volume: 372 start-page: 701 issue: 6507 year: 1994 ident: 2022012520025482800_msab326-B18 article-title: A highly conserved eukaryotic protein family possessing properties of polypeptide chain release factor publication-title: Nature doi: 10.1038/372701a0 contributor: fullname: Frolova – volume: 283 start-page: 41 issue: 5742 year: 1980 ident: 2022012520025482800_msab326-B20 article-title: A UGA termination suppression tRNATrp active in rabbit reticulocytes publication-title: Nature doi: 10.1038/283041a0 contributor: fullname: Geller – volume: 180 start-page: 549 issue: 3 year: 1984 ident: 2022012520025482800_msab326-B64 article-title: Translation is a non-uniform process: effect of tRNA availability on the rate of elongation of nascent polypeptide chains publication-title: J Mol Biol doi: 10.1016/0022-2836(84)90027-5 contributor: fullname: Varenne |
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In bacteria stop codons are recognized by one of two class I release factors (RF1) recognizing TAG, RF2 recognizing TGA, and TAA being recognized by... In bacteria stop codons are recognized by one of two class I release factors (RF1) recognizing TAG, RF2 recognizing TGA, and TAA being recognized by both.... |
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SubjectTerms | Analysis Bacteria Bacteria - genetics Base Composition Codon Codon Usage Codon, Terminator Discoveries Genetic translation Peptide Termination Factors - genetics |
Title | Variation in Release Factor Abundance Is Not Needed to Explain Trends in Bacterial Stop Codon Usage |
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