Nucleotide composition affects codon usage toward the 3'-end
Autoři:
Fouad Zahdeh aff001; Liran Carmel aff001
Působiště autorů:
Department of Genetics, The Alexander Silberman Institute of Life Sciences, Faculty of Science, The Hebrew University of Jerusalem, Edmond J. Safra Campus, Givat Ram, Jerusalem, Israel
aff001; Hereditary Research Lab, Life Sciences Department, Bethlehem University, Bethlehem, Palestinian authority
aff002
Vyšlo v časopise:
PLoS ONE 14(12)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0225633
Souhrn
The 3’-end of the coding sequence in several species is known to show specific codon usage bias. Several factors have been suggested to underlie this phenomenon, including selection against translation efficiency, selection for translation accuracy, and selection against RNA folding. All are supported by some evidence, but there is no general agreement as to which factors are the main determinants. Nor is it known how universal this phenomenon is, and whether the same factors explain it in different species. To answer these questions, we developed a measure that quantifies the codon usage bias at the gene end, and used it to compute this bias for 91 species that span the three domains of life. In addition, we characterized the codons in each species by features that allow discrimination between the different factors. Combining all these data, we were able to show that there is a universal trend to favor AT-rich codons toward the gene end. Moreover, we suggest that this trend is explained by avoidance from forming RNA secondary structures around the stop codon, which may interfere with normal translation termination.
Klíčová slova:
Gene expression – Eukaryota – Messenger RNA – Protein translation – Transfer RNA – RNA structure – Prokaryotic cells – Translation termination
Zdroje
1. Man O, Pilpel Y. Differential translation efficiency of orthologous genes is involved in phenotypic divergence of yeast species. Nat Genet. 2007;39(3):415–21. doi: 10.1038/ng1967 17277776.
2. Hiraoka Y, Kawamata K, Haraguchi T, Chikashige Y. Codon usage bias is correlated with gene expression levels in the fission yeast Schizosaccharomyces pombe. Genes Cells. 2009;14(4):499–509. doi: 10.1111/j.1365-2443.2009.01284.x 19335619.
3. Ikemura T. 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. J Mol Biol. 1981;151(3):389–409. doi: 10.1016/0022-2836(81)90003-6 6175758.
4. Ikemura T. Codon usage and tRNA content in unicellular and multicellular organisms. Mol Biol Evol. 1985;2(1):13–34. doi: 10.1093/oxfordjournals.molbev.a040335 3916708.
5. Andersson SG, Kurland CG. Codon preferences in free-living microorganisms. Microbiol Rev. 1990;54(2):198–210. 2194095; PubMed Central PMCID: PMC372768.
6. Sharp PM, Stenico M, Peden JF, Lloyd AT. Codon usage: mutational bias, translational selection, or both? Biochem Soc Trans. 1993;21(4):835–41. doi: 10.1042/bst0210835 8132077.
7. dos Reis M, Savva R, Wernisch L. Solving the riddle of codon usage preferences: a test for translational selection. Nucleic Acids Res. 2004;32(17):5036–44. doi: 10.1093/nar/gkh834 15448185; PubMed Central PMCID: PMC521650.
8. Akashi H. Gene expression and molecular evolution. Curr Opin Genet Dev. 2001;11(6):660–6. doi: 10.1016/s0959-437x(00)00250-1 11682310.
9. Wallace EW, Airoldi EM, Drummond DA. Estimating selection on synonymous codon usage from noisy experimental data. Mol Biol Evol. 2013;30(6):1438–53. doi: 10.1093/molbev/mst051 23493257; PubMed Central PMCID: PMC3649678.
10. Bulmer M. The selection-mutation-drift theory of synonymous codon usage. Genetics. 1991;129(3):897–907. 1752426; PubMed Central PMCID: PMC1204756.
11. Akashi H. Synonymous codon usage in Drosophila melanogaster: natural selection and translational accuracy. Genetics. 1994;136(3):927–35. 8005445; PubMed Central PMCID: PMC1205897.
12. Dong H, Nilsson L, Kurland CG. Co-variation of tRNA abundance and codon usage in Escherichia coli at different growth rates. J Mol Biol. 1996;260(5):649–63. doi: 10.1006/jmbi.1996.0428 8709146.
13. Kramer EB, Farabaugh PJ. The frequency of translational misreading errors in E. coli is largely determined by tRNA competition. RNA. 2007;13(1):87–96. doi: 10.1261/rna.294907 17095544; PubMed Central PMCID: PMC1705757.
14. Qian W, Yang JR, Pearson NM, Maclean C, Zhang J. Balanced codon usage optimizes eukaryotic translational efficiency. PLoS Genet. 2012;8(3):e1002603. doi: 10.1371/journal.pgen.1002603 22479199; PubMed Central PMCID: PMC3315465.
15. Hershberg R, Petrov DA. Selection on codon bias. Annu Rev Genet. 2008;42:287–99. doi: 10.1146/annurev.genet.42.110807.091442 18983258.
16. Sharp PM, Averof M, Lloyd AT, Matassi G, Peden JF. DNA sequence evolution: the sounds of silence. Philos Trans R Soc Lond B Biol Sci. 1995;349(1329):241–7. doi: 10.1098/rstb.1995.0108 8577834.
17. Urrutia AO, Hurst LD. Codon usage bias covaries with expression breadth and the rate of synonymous evolution in humans, but this is not evidence for selection. Genetics. 2001;159(3):1191–9. 11729162; PubMed Central PMCID: PMC1461876.
18. Lafay B, Atherton JC, Sharp PM. Absence of translationally selected synonymous codon usage bias in Helicobacter pylori. Microbiology. 2000;146 (Pt 4):851–60. doi: 10.1099/00221287-146-4-851 10784043.
19. Galtier N, Piganeau G, Mouchiroud D, Duret L. GC-content evolution in mammalian genomes: the biased gene conversion hypothesis. Genetics. 2001;159(2):907–11. 11693127; PubMed Central PMCID: PMC1461818.
20. Begun DJ. The frequency distribution of nucleotide variation in Drosophila simulans. Mol Biol Evol. 2001;18(7):1343–52. doi: 10.1093/oxfordjournals.molbev.a003918 11420372.
21. Berg OG. Selection intensity for codon bias and the effective population size of Escherichia coli. Genetics. 1996;142(4):1379–82. 8846914; PubMed Central PMCID: PMC1207134.
22. Li WH. Models of nearly neutral mutations with particular implications for nonrandom usage of synonymous codons. J Mol Evol. 1987;24(4):337–45. doi: 10.1007/bf02134132 3110426.
23. Marais G, Mouchiroud D, Duret L. Neutral effect of recombination on base composition in Drosophila. Genet Res. 2003;81(2):79–87. doi: 10.1017/s0016672302006079 12872909.
24. Marais G, Mouchiroud D, Duret L. Does recombination improve selection on codon usage? Lessons from nematode and fly complete genomes. Proc Natl Acad Sci U S A. 2001;98(10):5688–92. doi: 10.1073/pnas.091427698 11320215; PubMed Central PMCID: PMC33274.
25. Qin H, Wu WB, Comeron JM, Kreitman M, Li WH. Intragenic spatial patterns of codon usage bias in prokaryotic and eukaryotic genomes. Genetics. 2004;168(4):2245–60. doi: 10.1534/genetics.104.030866 15611189; PubMed Central PMCID: PMC1448744.
26. Comeron JM, Kreitman M. Population, evolutionary and genomic consequences of interference selection. Genetics. 2002;161(1):389–410. 12019253; PubMed Central PMCID: PMC1462104.
27. Hill WG, Robertson A. The effect of linkage on limits to artificial selection. Genet Res. 1966;8(3):269–94. 5980116.
28. Carlini DB, Chen Y, Stephan W. The relationship between third-codon position nucleotide content, codon bias, mRNA secondary structure and gene expression in the drosophilid alcohol dehydrogenase genes Adh and Adhr. Genetics. 2001;159(2):623–33. 11606539; PubMed Central PMCID: PMC1461829.
29. Eyre-Walker A, Bulmer M. Reduced synonymous substitution rate at the start of enterobacterial genes. Nucleic Acids Res. 1993;21(19):4599–603. doi: 10.1093/nar/21.19.4599 8233796; PubMed Central PMCID: PMC311196.
30. Chen Y, Carlini DB, Baines JF, Parsch J, Braverman JM, Tanda S, et al. RNA secondary structure and compensatory evolution. Genes Genet Syst. 1999;74(6):271–86. doi: 10.1266/ggs.74.271 10791023.
31. Rocha EP, Danchin A, Viari A. Translation in Bacillus subtilis: roles and trends of initiation and termination, insights from a genome analysis. Nucleic Acids Res. 1999;27(17):3567–76. doi: 10.1093/nar/27.17.3567 10446248; PubMed Central PMCID: PMC148602.
32. Keller TE, Mis SD, Jia KE, Wilke CO. Reduced mRNA secondary-structure stability near the start codon indicates functional genes in prokaryotes. Genome Biol Evol. 2012;4(2):80–8. doi: 10.1093/gbe/evr129 22138151; PubMed Central PMCID: PMC3269970.
33. Gu W, Zhou T, Wilke CO. A universal trend of reduced mRNA stability near the translation-initiation site in prokaryotes and eukaryotes. PLoS Comput Biol. 2010;6(2):e1000664. doi: 10.1371/journal.pcbi.1000664 20140241; PubMed Central PMCID: PMC2816680.
34. Bentele K, Saffert P, Rauscher R, Ignatova Z, Bluthgen N. Efficient translation initiation dictates codon usage at gene start. Mol Syst Biol. 2013;9:675. doi: 10.1038/msb.2013.32 23774758; PubMed Central PMCID: PMC3964316.
35. Tuller T, Carmi A, Vestsigian K, Navon S, Dorfan Y, Zaborske J, et al. An evolutionarily conserved mechanism for controlling the efficiency of protein translation. Cell. 2010;141(2):344–54. doi: 10.1016/j.cell.2010.03.031 20403328.
36. Eyre-Walker A. The close proximity of Escherichia coli genes: consequences for stop codon and synonymous codon use. J Mol Evol. 1996;42(2):73–8. doi: 10.1007/bf02198830 8919857.
37. Eyre-Walker A. Synonymous codon bias is related to gene length in Escherichia coli: selection for translational accuracy? Mol Biol Evol. 1996;13(6):864–72. 8754221.
38. Bulmer M. Codon usage and intragenic position. J Theor Biol. 1988;133(1):67–71. doi: 10.1016/s0022-5193(88)80024-9 3066998.
39. Kurland CG. Translational accuracy and the fitness of bacteria. Annu Rev Genet. 1992;26:29–50. doi: 10.1146/annurev.ge.26.120192.000333 1482115.
40. Cusack BP, Arndt PF, Duret L, Roest Crollius H. Preventing dangerous nonsense: selection for robustness to transcriptional error in human genes. PLoS Genet. 2011;7(10):e1002276. doi: 10.1371/journal.pgen.1002276 22022272; PubMed Central PMCID: PMC3192821.
41. Maquat LE. Nonsense-mediated mRNA decay: splicing, translation and mRNP dynamics. Nat Rev Mol Cell Biol. 2004;5(2):89–99. doi: 10.1038/nrm1310 15040442.
42. Katz L, Burge CB. Widespread selection for local RNA secondary structure in coding regions of bacterial genes. Genome Res. 2003;13(9):2042–51. doi: 10.1101/gr.1257503 12952875; PubMed Central PMCID: PMC403678.
43. Sharp PM, Li WH. The codon Adaptation Index—a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res. 1987;15(3):1281–95. doi: 10.1093/nar/15.3.1281 3547335; PubMed Central PMCID: PMC340524.
44. dos Reis M, Wernisch L, Savva R. Unexpected correlations between gene expression and codon usage bias from microarray data for the whole Escherichia coli K-12 genome. Nucleic Acids Res. 2003;31(23):6976–85. doi: 10.1093/nar/gkg897 14627830; PubMed Central PMCID: PMC290265.
45. Wright F. The 'effective number of codons' used in a gene. Gene. 1990;87(1):23–9. doi: 10.1016/0378-1119(90)90491-9 2110097.
46. Sharp PM, Tuohy TM, Mosurski KR. Codon usage in yeast: cluster analysis clearly differentiates highly and lowly expressed genes. Nucleic Acids Res. 1986;14(13):5125–43. doi: 10.1093/nar/14.13.5125 3526280; PubMed Central PMCID: PMC311530.
47. Hockenberry AJ, Sirer MI, Amaral LA, Jewett MC. Quantifying position-dependent codon usage bias. Mol Biol Evol. 2014;31(7):1880–93. Epub 2014/04/09. doi: 10.1093/molbev/msu126 24710515; PubMed Central PMCID: PMC4069614.
48. Bjornsson A, Mottagui-Tabar S, Isaksson LA. Structure of the C-terminal end of the nascent peptide influences translation termination. EMBO J. 1996;15(7):1696–704. 8612594; PubMed Central PMCID: PMC450081.
49. Tuller T, Zur H. Multiple roles of the coding sequence 5' end in gene expression regulation. Nucleic Acids Res. 2015;43(1):13–28. Epub 2014/12/17. doi: 10.1093/nar/gku1313 25505165; PubMed Central PMCID: PMC4288200.
50. Webster MT, Hurst LD. Direct and indirect consequences of meiotic recombination: implications for genome evolution. Trends Genet. 2012;28(3):101–9. doi: 10.1016/j.tig.2011.11.002 22154475.
51. Zhang J, Kuo CC, Chen L. GC content around splice sites affects splicing through pre-mRNA secondary structures. BMC Genomics. 2011;12:90. doi: 10.1186/1471-2164-12-90 21281513; PubMed Central PMCID: PMC3041747.
52. Sabi R, Tuller T. Modelling the efficiency of codon-tRNA interactions based on codon usage bias. DNA Res. 2014;21(5):511–26. doi: 10.1093/dnares/dsu017 24906480; PubMed Central PMCID: PMC4195497.
53. Seffens W, Digby D. mRNAs have greater negative folding free energies than shuffled or codon choice randomized sequences. Nucleic Acids Res. 1999;27(7):1578–84. doi: 10.1093/nar/27.7.1578 10075987; PubMed Central PMCID: PMC148359.
54. Plat T. RNA Structure and function. New York, NY: Cold Spring Harbour Laboratory Press; 1998.
55. Carpousis AJ, Vanzo NF, Raynal LC. mRNA degradation. A tale of poly(A) and multiprotein machines. Trends Genet. 1999;15(1):24–8. doi: 10.1016/s0168-9525(98)01627-8 10087930.
56. Tate WP, Mannering SA. Three, four or more: the translational stop signal at length. Mol Microbiol. 1996;21(2):213–9. doi: 10.1046/j.1365-2958.1996.6391352.x 8858577.
57. Zahdeh F, Carmel L. The role of nucleotide composition in premature termination codon recognition. BMC Bioinformatics. 2016;17(1):519. doi: 10.1186/s12859-016-1384-z 27927164.
58. Yates A, Akanni W, Amode MR, Barrell D, Billis K, Carvalho-Silva D, et al. Ensembl 2016. Nucleic Acids Res. 2016;44(D1):D710–6. doi: 10.1093/nar/gkv1157 26687719; PubMed Central PMCID: PMC4702834.
59. The Genotype-Tissue Expression (GTEx) project. Nat Genet. 2013;45(6):580–5. Epub 2013/05/30. doi: 10.1038/ng.2653 23715323; PubMed Central PMCID: PMC4010069.
Článok vyšiel v časopise
PLOS One
2019 Číslo 12
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- Nejasný stín na plicích – kazuistika
- Masturbační chování žen v ČR − dotazníková studie
- Těžké menstruační krvácení může značit poruchu krevní srážlivosti. Jaký management vyšetření a léčby je v takovém případě vhodný?
- Fixní kombinace paracetamol/kodein nabízí synergické analgetické účinky
Najčítanejšie v tomto čísle
- Methylsulfonylmethane increases osteogenesis and regulates the mineralization of the matrix by transglutaminase 2 in SHED cells
- Oregano powder reduces Streptococcus and increases SCFA concentration in a mixed bacterial culture assay
- The characteristic of patulous eustachian tube patients diagnosed by the JOS diagnostic criteria
- Parametric CAD modeling for open source scientific hardware: Comparing OpenSCAD and FreeCAD Python scripts