The Code of Silence: Widespread Associations Between Synonymous Codon Biases and Gene Function

Journal of Molecular Evolution

Volumn 82, Issue 1, 2016, Pages 65-73

  Supek, Fran ^a,b,c  

^a RUDER BO KOVI INSTITUTE   (Croatia)

^b CENTRE FOR GENOMIC REGULATION CRG   (Spain)

^c UNIVERSITAT POMPEU FABRA   (Spain)

Author keywords

Codon usage bias; Gene function; Microbial ecology; Translation efficiency

Indexed keywords

CODON;

ARCHAEON; BACTERIUM; CODON; CONSENSUS SEQUENCE; FUNGUS; GENETICS; HUMAN; MOLECULAR EVOLUTION; NEOPLASM; OPEN READING FRAME; SILENT MUTATION;

ARCHAEA; BACTERIA; CODON; CONSENSUS SEQUENCE; EVOLUTION, MOLECULAR; FUNGI; HUMANS; NEOPLASMS; OPEN READING FRAMES; SILENT MUTATION;

EID: 84954401041     PISSN: 00222844     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00239-015-9714-8     Document Type: Review

References (106)

1. Agris PF, Vendeix FAP, Graham WD (2007) tRNA’s wobble decoding of the genome: 40 years of modification. J Mol Biol 366:1–13. doi:10.1016/j.jmb.2006.11.046
2. Akashi H (1994) Synonymous codon usage in Drosophila melanogaster: natural selection and translational accuracy. Genetics 136:927–935
3. Angov E (2011) Codon usage: nature’s roadmap to expression and folding of proteins. Biotechnol J 6:650–659. doi:10.1002/biot.201000332
4. Bentele K, Saffert P, Rauscher R et al (2013) Efficient translation initiation dictates codon usage at gene start. Mol Syst Biol 9:675. doi:10.1038/msb.2013.32
5. Brbić M, Warnecke T, Kriško A, Supek F (2015) Global shifts in genome and proteome composition are very tightly coupled. Genome Biol Evol 7:1519–1532. doi:10.1093/gbe/evv088
6. Bulmer M (1991) The selection-mutation-drift theory of synonymous codon usage. Genetics 129:897–907
7. Cáceres E, Eva C, Hurst LD (2013) The evolution, impact and properties of exonic splice enhancers. Genome Biol 14:R143. doi:10.1186/gb-2013-14-12-r143
8. Camiolo S, Farina L, Porceddu A (2012) The relation of codon bias to tissue-specific gene expression in Arabidopsis thaliana. Genetics 192:641–649. doi:10.1534/genetics.112.143677
9. Cannarozzi G, Schraudolph NN, Faty M et al (2010) A role for codon order in translation dynamics. Cell 141:355–367. doi:10.1016/j.cell.2010.02.036
10. Carbone A (2006) Computational prediction of genomic functional cores specific to different microbes. J Mol Evol 63:733–746. doi:10.1007/s00239-005-0250-9
11. Carbone A, Madden R (2005) Insights on the evolution of metabolic networks of unicellular translationally biased organisms from transcriptomic data and sequence analysis. J Mol Evol 61:456–469. doi:10.1007/s00239-004-0317-z
12. Chan CTY, Pang YLJ, Wenjun D et al (2012) Reprogramming of tRNA modifications controls the oxidative stress response by codon-biased translation of proteins. Nat Commun 3:937. doi:10.1038/ncomms1938
13. Chen SL, Lee W, Hottes AK et al (2004) Codon usage between genomes is constrained by genome-wide mutational processes. Proc Natl Acad Sci USA 101:3480–3485. doi:10.1073/pnas.0307827100
14. Chevance FFV, Le Guyon S, Hughes KT (2014) The effects of codon context on in vivo translation speed. PLoS Genet 10:e1004392. doi:10.1371/journal.pgen.1004392
15. Cruz J, Liu Y, Liang Y et al (2011) BacMap: an up-to-date electronic atlas of annotated bacterial genomes. Nucleic Acids Res 40:D599–D604. doi:10.1093/nar/gkr1105
16. Dalquen DA, Dessimoz C (2013) Bidirectional best hits miss many orthologs in duplication-rich clades such as plants and animals. Genome Biol Evol 5:1800–1806. doi:10.1093/gbe/evt132
17. Deane CM, Dong M, Huard FPE et al (2007) Cotranslational protein folding fact or fiction? Bioinformatics 23:i142–i148. doi:10.1093/bioinformatics/btm175
18. Dedon PC, Begley TJ (2014) A system of RNA modifications and biased codon use controls cellular stress response at the level of translation. Chem Res Toxicol 27:330–337. doi:10.1021/tx400438d
19. Dittmar KA, Sørensen MA, Elf J et al (2005) Selective charging of tRNA isoacceptors induced by amino-acid starvation. EMBO Rep 6:151–157. doi:10.1038/sj.embor.7400341
20. Dittmar KA, Goodenbour JM, Pan T (2006) Tissue-specific differences in human transfer RNA expression. PLoS Genet 2:e221. doi:10.1371/journal.pgen.0020221
21. Drummond DA, Wilke CO (2008) Mistranslation-induced protein misfolding as a dominant constraint on coding-sequence evolution. Cell 134:341–352. doi:10.1016/j.cell.2008.05.042
22. Duret L, Mouchiroud D (1999) Expression pattern and surprisingly, gene length shape codon usage in Caenorhabditis, Drosophila, and Arabidopsis. Proc Natl Acad Sci U S A 96:4482–4487
23. Elf J, Nilsson D, Tenson T, Ehrenberg M (2003) Selective charging of tRNA isoacceptors explains patterns of codon usage. Science 300:1718–1722. doi:10.1126/science.1083811
24. Fluman N, Navon S, Bibi E, Pilpel Y (2014) mRNA-programmed translation pauses in the targeting of E. coli membrane proteins. eLife 3:e03440. doi:10.7554/eLife.03440
25. Fraser HB, Hirsh AE, Wall DP, Eisen MB (2004) Coevolution of gene expression among interacting proteins. Proc Natl Acad Sci USA 101:9033–9038. doi:10.1073/pnas.0402591101
26. Frenkel-Morgenstern M, Danon T, Christian T et al (2012) Genes adopt non-optimal codon usage to generate cell cycle-dependent oscillations in protein levels. Mol Syst Biol 8:572. doi:10.1038/msb.2012.3
27. Gartner JJ, Parker SCJ, Prickett TD et al (2013) Whole-genome sequencing identifies a recurrent functional synonymous mutation in melanoma. Proc Natl Acad Sci USA 110:13481–13486. doi:10.1073/pnas.1304227110
28. Gingold H, Pilpel Y (2011) Determinants of translation efficiency and accuracy. Mol Syst Biol 7:481. doi:10.1038/msb.2011.14
29. Gingold H, Tehler D, Christoffersen NR et al (2014) A dual program for translation regulation in cellular proliferation and differentiation. Cell 158:1281–1292. doi:10.1016/j.cell.2014.08.011
30. Glyakina AV, Garbuzynskiy SO, Lobanov MY, Galzitskaya OV (2007) Different packing of external residues can explain differences in the thermostability of proteins from thermophilic and mesophilic organisms. Bioinformatics 23:2231–2238. doi:10.1093/bioinformatics/btm345
31. Goodman DB, Church GM, Kosuri S (2013) Causes and effects of N-terminal codon bias in bacterial genes. Science 342:475–479. doi:10.1126/science.1241934
32. Gouy M, Gautier C (1982) Codon usage in bacteria: correlation with gene expressivity. Nucleic Acids Res 10:7055–7074
33. Grosjean H, Henri G, de Crécy-Lagard V, Marck C (2010) Deciphering synonymous codons in the three domains of life: co-evolution with specific tRNA modification enzymes. FEBS Lett 584:252–264. doi:10.1016/j.febslet.2009.11.052
34. Guimaraes JC, Rocha M, Arkin AP (2014) Transcript level and sequence determinants of protein abundance and noise in Escherichia coli. Nucleic Acids Res 42:4791–4799. doi:10.1093/nar/gku126
35. Henkin TM, Yanofsky C (2002) Regulation by transcription attenuation in bacteria: how RNA provides instructions for transcription termination/antitermination decisions. BioEssays 24:700–707. doi:10.1002/bies.10125
36. Hershberg R, Petrov DA (2008) Selection on codon bias. Annu Rev Genet 42:287–299. doi:10.1146/annurev.genet.42.110807.091442
37. Hershberg R, Petrov DA (2009) General rules for optimal codon choice. PLoS Genet 5:e1000556. doi:10.1371/journal.pgen.1000556
38. Holt KE, Wertheim H, Zadoks RN et al (2015) Genomic analysis of diversity, population structure, virulence, and antimicrobial resistance in Klebsiella pneumoniae, an urgent threat to public health. Proc Natl Acad Sci USA 112:E3574–E3581. doi:10.1073/pnas.1501049112
39. Hunt RC, Simhadri VL, Iandoli M et al (2014) Exposing synonymous mutations. Trends Genet 30:308–321. doi:10.1016/j.tig.2014.04.006
40. Ikemura T (1985) Codon usage and tRNA content in unicellular and multicellular organisms. Mol Biol Evol 2:13–34
41. Kanaya S, Yamada Y et al (1999) Studies of codon usage and tRNA genes of 18 unicellular organisms and quantification of Bacillus subtilis tRNAs: gene expression level and species-specific diversity of codon usage based on multivariate analysis. Gene 238:143–155. doi:10.1016/s0378-1119(99)00225-5
42. Karlin S, Mrazek J (2000) Predicted highly expressed genes of diverse prokaryotic genomes. J Bacteriol 182:5238–5250. doi:10.1128/jb.182.18.5238-5250.2000
43. Karlin S, Brocchieri L, Campbell A et al (2005a) Genomic and proteomic comparisons between bacterial and archaeal genomes and related comparisons with the yeast and fly genomes. Proc Natl Acad Sci USA 102:7309–7314. doi:10.1073/pnas.0502314102
44. Karlin S, Mrázek J, Ma J, Brocchieri L (2005b) Predicted highly expressed genes in archaeal genomes. Proc Natl Acad Sci USA 102:7303–7308. doi:10.1073/pnas.0502313102
45. Kataoka M, Kosono S, Tsujimoto G (1999) Spatial and temporal regulation of protein expression by bldA within a Streptomyces lividans colony. FEBS Lett 462:425–429
46. Kensche PR, van Noort V, Dutilh BE, Huynen MA (2008) Practical and theoretical advances in predicting the function of a protein by its phylogenetic distribution. J R Soc Interface 5:151–170. doi:10.1098/rsif.2007.1047
47. Knight RD, Freeland SJ, Landweber LF (2001) A simple model based on mutation and selection explains trends in codon and amino-acid usage and GC composition within and across genomes. Genome Biol. doi:10.1186/gb-2001-2-4-research0010
48. Krisko A, Radman M (2010) Protein damage and death by radiation in Escherichia coli and Deinococcus radiodurans. Proc Natl Acad Sci USA 107:14373–14377. doi:10.1073/pnas.1009312107
49. Krisko A, Copic T, Gabaldón T et al (2014) Inferring gene function from evolutionary change in signatures of translation efficiency. Genome Biol 15:R44. doi:10.1186/gb-2014-15-3-r44
50. Kudla G, Murray AW, Tollervey D, Plotkin JB (2009) Coding-sequence determinants of gene expression in Escherichia coli. Science 324:255–258. doi:10.1126/science.1170160
51. Lampson BL, Pershing NLK, Prinz JA et al (2013) Rare codons regulate KRas oncogenesis. Curr Biol 23:70–75. doi:10.1016/j.cub.2012.11.031
52. Leskiw BK, Mah R, Lawlor EJ, Chater KF (1993) Accumulation of bldA-specified tRNA is temporally regulated in Streptomyces coelicolor A3(2). J Bacteriol 175:1995–2005
53. Mahlab S, Linial M (2014) Speed controls in translating secretory proteins in Eukaryotes—an evolutionary perspective. PLoS Comput Biol 10:e1003294. doi:10.1371/journal.pcbi.1003294
54. Man O, Pilpel Y (2007) Differential translation efficiency of orthologous genes is involved in phenotypic divergence of yeast species. Nat Genet 39:415–421. doi:10.1038/ng1967
55. Mizuguchi K, Sele M, Cubellis MV (2007) Environment specific substitution tables for thermophilic proteins. BMC Bioinformatics 8(Suppl 1):S15. doi:10.1186/1471-2105-8-S1-S15
56. Moriyama EN, Powell JR (1997) Codon usage bias and tRNA abundance in Drosophila. J Mol Evol 45:514–523
57. Najafabadi HS, Salavati R (2008) Sequence-based prediction of protein-protein interactions by means of codon usage. Genome Biol 9:R87. doi:10.1186/gb-2008-9-5-r87
58. Najafabadi HS, Goodarzi H, Salavati R (2009) Universal function-specificity of codon usage. Nucleic Acids Res 37:7014–7023. doi:10.1093/nar/gkp792
59. Nehrt NL, Clark WT, Radivojac P, Hahn MW (2011) Testing the ortholog conjecture with comparative functional genomic data from mammals. PLoS Comput Biol 7:e1002073. doi:10.1371/journal.pcbi.1002073
60. Nekrutenko A, Li W-H (2000) Assessment of compositional heterogeneity within and between Eukaryotic genomes. Genome Res 10:1986–1995. doi:10.1101/gr.153400
61. Novoa EM, Ribas de Pouplana L (2012) Speeding with control: codon usage, tRNAs, and ribosomes. Trends Genet 28:574–581. doi:10.1016/j.tig.2012.07.006
62. Novoa EM, Pavon-Eternod M, Pan T, Ribas de Pouplana L (2012) A Role for tRNA modifications in genome structure and codon usage. Cell 149:202–213. doi:10.1016/j.cell.2012.01.050
63. Oresic M, Dehn MHH, Korenblum DHH, Shalloway DHH (2003) Tracing specific synonymous codon-secondary structure correlations through evolution. J Mol Evol 56:473–484. doi:10.1007/s00239-002-2418-x
64. Pechmann S, Frydman J (2012) Evolutionary conservation of codon optimality reveals hidden signatures of cotranslational folding. Nat Struct Mol Biol 20:237–243. doi:10.1038/nsmb.2466
65. Pershing NLK, Lampson BL, Belsky JA et al (2015) Rare codons capacitate Kras-driven de novo tumorigenesis. J Clin Invest 125:222–233. doi:10.1172/JCI77627
66. Plotkin JB, Kudla G (2010) Synonymous but not the same: the causes and consequences of codon bias. Nat Rev Genet 12:32–42. doi:10.1038/nrg2899
67. Powell JR, Dion K (2015) Effects of codon usage on gene expression: empirical studies on Drosophila. J Mol Evol 80:219–226. doi:10.1007/s00239-015-9675-y
68. Presnyak V, Alhusaini N, Chen Y-H et al (2015) Codon optimality is a major determinant of mRNA stability. Cell 160:1111–1124. doi:10.1016/j.cell.2015.02.029
69. Quax TEF, Claassens NJ, Söll D, van der Oost J (2015) Codon bias as a Means to fine-tune gene expression. Mol Cell 59:149–161. doi:10.1016/j.molcel.2015.05.035
70. Ran W, Higgs PG (2010) The influence of anticodon-codon interactions and modified bases on codon usage bias in bacteria. Mol Biol Evol 27:2129–2140. doi:10.1093/molbev/msq102
71. Read TD, Massey RC (2014) Characterizing the genetic basis of bacterial phenotypes using genome-wide association studies: a new direction for bacteriology. Genome Med 6:109. doi:10.1186/s13073-014-0109-z
72. Reddy TBK, Thomas AD, Stamatis D et al (2015) The Genomes OnLine Database (GOLD) v. 5: a metadata management system based on a four level (meta)genome project classification. Nucleic Acids Res 43:D1099–D1106. doi:10.1093/nar/gku950
73. Retchless AC, Lawrence JG (2011) Quantification of codon selection for comparative bacterial genomics. BMC Genom 12:374. doi:10.1186/1471-2164-12-374
74. Rocha EPC (2004a) The replication-related organization of bacterial genomes. Microbiology 150:1609–1627. doi:10.1099/mic.0.26974-0
75. Rocha EPC (2004b) Codon usage bias from tRNA’s point of view: redundancy, specialization, and efficient decoding for translation optimization. Genome Res 14:2279–2286. doi:10.1101/gr.2896904
76. Rocha EPC, Feil EJ (2010) Mutational patterns cannot explain genome composition: are there any neutral sites in the genomes of bacteria? PLoS Genet 6:e1001104. doi:10.1371/journal.pgen.1001104
77. Salipante SJ, Roach DJ, Kitzman JO et al (2015) Large-scale genomic sequencing of extraintestinal pathogenic Escherichia coli strains. Genome Res 25:119–128. doi:10.1101/gr.180190.114
78. Sauna ZE, Kimchi-Sarfaty C (2011) Understanding the contribution of synonymous mutations to human disease. Nat Rev Genet 12:683–691. doi:10.1038/nrg3051
79. Saunders R, Deane CM (2010) Synonymous codon usage influences the local protein structure observed. Nucleic Acids Res 38:6719–6728. doi:10.1093/nar/gkq495
80. Shabalina SA, Spiridonov NA, Kashina A (2013) Sounds of silence: synonymous nucleotides as a key to biological regulation and complexity. Nucleic Acids Res 41:2073–2094. doi:10.1093/nar/gks1205
81. Sharp PM, Li W-H (1987) The codon adaptation index-a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res 15:1281–1295. doi:10.1093/nar/15.3.1281
82. Sharp PM, Tuohy TM, Mosurski KR (1986) Codon usage in yeast: cluster analysis clearly differentiates highly and lowly expressed genes. Nucleic Acids Res 14:5125–5143
83. Sharp PM, Averof M, Lloyd AT et al (1995) DNA sequence evolution: the sounds of silence. Philos Trans R Soc Lond B Biol Sci 349:241–247. doi:10.1098/rstb.1995.0108
84. Sharp PM, Bailes E, Grocock RJ et al (2005) Variation in the strength of selected codon usage bias among bacteria. Nucleic Acids Res 33:1141–1153. doi:10.1093/nar/gki242
85. Škunca N, Bošnjak M, Kriško A et al (2013) Phyletic profiling with cliques of orthologs is enhanced by signatures of paralogy relationships. PLoS Comput Biol 9:e1002852. doi:10.1371/journal.pcbi.1002852
86. Stoletzki N, Eyre-Walker A (2006) Synonymous codon usage in Escherichia coli: selection for translational accuracy. Mol Biol Evol 24:374–381. doi:10.1093/molbev/msl166
87. Supek F, Smuc T (2010) On relevance of codon usage to expression of synthetic and natural genes in Escherichia coli. Genetics 185:1129–1134. doi:10.1534/genetics.110.115477
88. Supek F, Vlahoviček K (2005) Comparison of codon usage measures and their applicability in prediction of microbial gene expressivity. BMC Bioinformatics 6:182. doi:10.1186/1471-2105-6-182
89. Supek F, Škunca N, Repar J et al (2010) Translational selection is ubiquitous in prokaryotes. PLoS Genet 6:e1001004. doi:10.1371/journal.pgen.1001004
90. Supek F, Miñana B, Valcárcel J et al (2014) Synonymous mutations frequently act as driver mutations in human cancers. Cell 156:1324–1335. doi:10.1016/j.cell.2014.01.051
91. Tsai C-J, Sauna ZE, Kimchi-Sarfaty C et al (2008) Synonymous mutations and ribosome stalling can lead to altered folding pathways and distinct minima. J Mol Biol 383:281–291. doi:10.1016/j.jmb.2008.08.012
92. Tuller T, Zur H (2015) Multiple roles of the coding sequence 5’ end in gene expression regulation. Nucleic Acids Res 43:13–28. doi:10.1093/nar/gku1313
93. Tuller T, Carmi A, Vestsigian K et al (2010a) An evolutionarily conserved mechanism for controlling the efficiency of protein translation. Cell 141:344–354. doi:10.1016/j.cell.2010.03.031
94. Tuller T, Waldman YY, Kupiec M, Ruppin E (2010b) Translation efficiency is determined by both codon bias and folding energy. Proc Natl Acad Sci USA 107:3645–3650. doi:10.1073/pnas.0909910107
95. UK10K Consortium (2015) The UK10K project identifies rare variants in health and disease. Nature. doi:10.1038/nature14962
96. Urrutia AO, Hurst LD (2003) The signature of selection mediated by expression on human genes. Genome Res 13:2260–2264. doi:10.1101/gr.641103
97. Von Mandach C, Merkl R (2010) Genes optimized by evolution for accurate and fast translation encode in Archaea and Bacteria a broad and characteristic spectrum of protein functions. BMC Genom 11:617. doi:10.1186/1471-2164-11-617
98. Wagner A (2000) Inferring lifestyle from gene expression patterns. Mol Biol Evol 17:1985–1987
99. Waldman YY, Tuller T, Keinan A, Ruppin E (2011) Selection for translation efficiency on synonymous polymorphisms in recent human evolution. Genome Biol Evol 3:749–761. doi:10.1093/gbe/evr076
100. Warnecke T, Hurst LD (2007) Evidence for a trade-off between translational efficiency and splicing regulation in determining synonymous codon usage in Drosophila melanogaster. Mol Biol Evol 24:2755–2762. doi:10.1093/molbev/msm210
101. Xia X (1998) How optimized is the translational machinery in Escherichia coli, Salmonella typhimurium and Saccharomyces cerevisiae? Genetics 149:37–44
102. Xu Y, Ma P, Shah P et al (2013) Non-optimal codon usage is a mechanism to achieve circadian clock conditionality. Nature 495:116–120. doi:10.1038/nature11942
103. Yang J-R, Chen X, Zhang J (2014) Codon-by-codon modulation of translational speed and accuracy via mRNA folding. PLoS Biol 12:e1001910. doi:10.1371/journal.pbio.1001910
104. Zaborske JM, DuMont VLB, Wallace EWJ et al (2014) A nutrient-driven tRNA modification alters translational fidelity and genome-wide protein coding across an animal genus. PLoS Biol 12:e1002015. doi:10.1371/journal.pbio.1002015
105. Zhou T, Weems M, Wilke CO (2009) Translationally optimal codons associate with structurally sensitive sites in proteins. Mol Biol Evol 26:1571–1580. doi:10.1093/molbev/msp070
106. Zhou M, Guo J, Cha J et al (2013) Non-optimal codon usage affects expression, structure and function of clock protein FRQ. Nature 495:111–115. doi:10.1038/nature11833