Trna genes rapidly change in evolution to meet novel translational demands

eLife

Volumn 2013, Issue 2, 2013, Pages

  Yona, Avihu H ^a   Bloom Ackermann, Zohar ^a   Frumkin, Idan ^a   Hanson Smith, Victor ^b   Charpak Amikam, Yoav ^a   Feng, Qinghua ^c   Boeke, Jef D ^d,e   Dahan, Orna ^a   Pilpel, Yitzhak ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

^d JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; FLUOROOROTIC ACID; TRANSFER RNA; ANTICODON; FUNGAL RNA; SACCHAROMYCES CEREVISIAE PROTEIN;

ANTICODON; ARTICLE; CONTROLLED STUDY; EVOLUTIONARY ADAPTATION; FUNGUS GROWTH; GENE; GENE DELETION; GENE EXPRESSION; GENE SWITCHING; GENOME; NONHUMAN; PROTEIN FOLDING; PROTEIN QUALITY; RNA SEQUENCE; RNA TRANSLATION; SACCHAROMYCES CEREVISIAE; ADAPTATION; BIOSYNTHESIS; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; METABOLISM; MOLECULAR EVOLUTION; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; PHYSIOLOGICAL STRESS; TIME;

ADAPTATION, PHYSIOLOGICAL; ANTICODON; BASE SEQUENCE; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION, FUNGAL; HUMANS; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN FOLDING; RNA, FUNGAL; RNA, TRANSFER; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; STRESS, PHYSIOLOGICAL; TIME FACTORS;

EID: 84890955856     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.01339     Document Type: Article

References (75)

1. Akashi H. 1994. Synonymous codon usage in Drosophila melanogaster: natural selection and translational accuracy. Genetics 136:927-935.
2. Amstutz H, Munz P, Heyer WD, Leupoid U, Kohli J. 1985. Concerted evolution of tRNA genes: intergenic conversion among three unlinked serine tRNA genes in S. pombe. Cell 40:879-886. doi: 10.1016/0092-8674(85)90347-2.
3. Anisimova M, Gascuel O. 2006. Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. Systematic Biology 55:539-552. doi: 10.1080/10635150600755453.
4. Aström SU, von Pawel-Rammingen U, Byström AS. 1993. The yeast initiator tRNAMet can act as an elongator tRNA(Met) in vivo. Journal of Molecular Biology 233:43-58. doi: 10.1006/jmbi.1993.1483.
5. Begley U, Dyavaiah M, Patil A, Rooney JP, DiRenzo D, Young CM, Conklin DS, Zitomer RS, Begley TJ. 2007. Trm9-catalyzed tRNA modifications link translation to the DNA damage response. Molecular Cell 28:860-870. doi: 10.1016/j.molcel.2007.09.021.
6. Bermudez-Santana C, Attolini CS, Kirsten T, Engelhardt J, Prohaska SJ, Steigele S, Stadler PF. 2010. Genomic organization of eukaryotic tRNAs. BMC Genomics 11:270. doi: 10.1186/1471-2164-11-270.
7. Bloom-Ackermann Z, Navon S, Gingold H, Towers R, Pilpel Y, Dahan O. 2014. A Comprehensive tRNA deletion library unravels the genetic architecture of the tRNA pool. Public Library of Science Genetics 10:e1004084. doi: 10.1371/journal.pgen.1004084.
8. Boeke JD, LaCroute F, Fink GR. 1984. A positive selection for mutants lacking orotidine-5'-phosphate decarboxylase activity in yeast: 5-fluoro-orotic acid resistance. Molecular and General Genetics 197:345-346. doi: 10.1007/BF00330984.
9. Bulmer M. 1991. The selection-mutation-drift theory of synonymous codon usage. Genetics 129:897-907.
10. Byström AS, Fink GR. 1989. A functional analysis of the repeated methionine initiator tRNA genes (IMT) in yeast. Molecular and General Genetics 216:276-286. doi: 10.1007/BF00334366.
11. Cabrita LD, Dobson CM, Christodoulou J. 2010. Protein folding on the ribosome. Current Opinion In Structural Biology 20:33-45. doi: 10.1016/j.sbi.2010.01.005.
12. Chan PP, Lowe TM. 2009. GtRNAdb: a database of transfer RNA genes detected in genomic sequence. Nucleic Acids Research 37:D93-D97. doi: 10.1093/nar/gkn787.
13. Clare JJ, Belcourt M, Farabaugh PJ. 1988. Efficient translational frameshifting occurs within a conserved sequence of the overlap between the two genes of a yeast Ty1 transposon. Proceedings of the National Academy of Sciences of the United States of America 85:6816-6820. doi: 10.1073/pnas.85.18.6816.
14. Cochella L, Green R. 2005. An active role for tRNA in decoding beyond codon:anticodon pairing. Science 308:1178-1180. doi: 10.1126/science.1111408.
15. Cortazzo P, Cerveñansky C, Marín M, Reiss C, Ehrlich R, Deana A. 2002. Silent mutations affect in vivo protein folding in Escherichia coli. Biochemical and Biophysical Research 293:537-541. doi: 10.1016/S0006-291X(02)00226-7.
16. Crombie T, Swaffield JC, Brown AJ. 1992. Protein folding within the cell is influenced by controlled rates of polypeptide elongation. Journal of Molecular Biology 228:7-12. doi: 10.1016/0022-2836(92)90486-4.
17. Doherty A, McInerney JO. 2013. Translational selection frequently Overcomes genetic drift in shaping synonymous codon usage patterns in vertebrates. Molecular Biology and Evolution 30:2263-2267. doi: 10.1093/molbev/mst128.
18. Dong H, Nilsson L, Kurland CG. 1996. Co-variation of tRNA abundance and codon usage in Escherichia coli at different growth rates. Journal of Molecular Biology 260:649-663. doi: 10.1006/jmbi.1996.0428.
19. Dos Reis M, Savva R, Wernisch L. 2004. Solving the riddle of codon usage preferences: a test for translational selection. Nucleic Acids Research 32:5036-5044. doi: 10.1093/nar/gkh834.
20. Drummond DA, Wilke CO. 2008. Mistranslation-induced protein misfolding as a dominant constraint oncoding-sequence evolution. Cell 134:341-352. doi: 10.1016/j.cell.2008.05.042.
21. Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32:1792-1797. doi: 10.1093/nar/gkh340.
22. Gingold H, Dahan O, Pilpel Y. 2012. Dynamic changes in translational efficiency are deduced from codon usage of the transcriptome. Nucleic Acids Research 40:1-11. doi: 10.1093/nar/gks772.
23. 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.
24. Higgs PG, Ran W. 2008. Coevolution of codon usage and tRNA genes leads to alternative stable states of biased codon usage. Molecular Biology and Evolution 25:2279-2291. doi: 10.1093/molbev/msn173.
25. Hudson NJ, Gu Q, Nagaraj SH, Ding YS, Dalrymple BP, Reverter A. 2011. Eukaryotic evolutionary transitions are associated with extreme codon bias in functionally-related proteins. Public Library of Science One 6:e25457. doi: 10.1371/journal.pone.0025457.
26. Itoh T, Takemoto K, Mori H, Gojobori T. 1999. Evolutionary instability of operon structures disclosed by sequence comparisons of complete microbial genomes. Molecular Biology and Evolution 16:332-346. doi: 10.1093/oxfordjournals.molbev.a026114.
27. Kaganovich D, Kopito R, Frydman J. 2008. Misfolded proteins partition between two distinct quality control compartments. Nature 454:1088-1095. doi: 10.1038/nature07195.
28. Kanaya S, Yamada Y, Kudo Y, Ikemura T. 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.
29. Kawakami K, Pande S, Faiola B, Moore DP, Boeke JD, Farabaugh PJ, Strathern JN, Nakamura Y, Garfinkel DJ. 1993. A rare tRNA-Arg(CCU) that regulates Ty1 element ribosomal frameshifting is essential for Ty1 retrotransposition in Saccharomyces cerevisiae. Genetics 135:309-320.
30. Kolitz SE, Lorsch JR. 2010. Eukaryotic initiator tRNA: finely tuned and ready for action. FEBS Letters 584:396-404. doi: 10.1016/j.febslet.2009.11.047.
31. Komar AA, Lesnik T, Reiss C. 1999. Synonymous codon substitutions affect ribosome traffic and protein folding during in vitro translation. FEBS Letters 462:387-391. doi: 10.1016/S0014-5793(99)01566-5.
32. Konevega AL, Soboleva NG, Makhno VI, Semenkov YP, Wintermeyer W, Rodnina MV, Katunin VI. 2004. Purine bases at position 37 of tRNA stabilize codon-anticodon interaction in the ribosomal A site by stacking and Mg2+-dependent interactions. RNA 10:90-101. doi: 10.1261/rna.5142404.
33. Kramer G, Boehringer D, Ban N, Bukau B. 2009. The ribosome as a platform for co-translational processing, folding and targeting of newly synthesized proteins. Nature Structural and Molecular Biology 16:589-597. doi: 10.1038/nsmb.1614.
34. Kudla G, Murray A, Tollervey D, Plotkin J. 2009. Coding-sequence determinants of gene expression in Escherichia coli. Science 324:255-258. doi: 10.1126/science.1170160.
35. Lenski RE, Rose MR, Simpson SC, Tadler SC. 1991. Long-term experimental evolution in Escherichia coli. I. Adaptation and divergence during 2,000 generations. The American Naturalist 138:1315. doi: 10.1086/285289.
36. Lowe TM, Eddy SR. 1997. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Research 25:955-964.
37. Man O, Pilpel Y. 2007. Differential translation efficiency of orthologous genes is involved in phenotypic divergence of yeast species. Nature Genetics 39:415-421. doi: 10.1038/ng1967.
38. McClellan AJ, Scott MD, Frydman J. 2005. Folding and quality control of the VHL tumor suppressor proceed through distinct chaperone pathways. Cell 121:739-748. doi: 10.1016/j.cell.2005.03.024.
39. McFarlane RJ, Whitehall SK. 2009. tRNA genes in eukaryotic genome organization and reorganization. Cell Cycle 8:3102-3106. doi: 10.4161/cc.8.19.9625.
40. Müller EC, Wittmann-Liebold B. 1997. Phylogenetic relationship of organisms obtained by ribosomal protein comparison. Cellular and Molecular Life Sciences 53:34-50. doi: 10.1007/PL00000578.
41. Munz P, Amstutz H, Kohli J, Leupold U. 1982. Recombination between dispersed serine tRNA genes in Schizosaccharomyces pombe. Nature 300:225-231. doi: 10.1038/300225a0.
42. Olejniczak M, Dale T, Fahlman RP, Uhlenbeck OC. 2005. Idiosyncratic tuning of tRNAs to achieve uniform ribosome binding. Nature Structural & Molecular Biology 12:788-793. doi: 10.1038/nsmb978.
43. Parmley JL, Hurst LD. 2007. Exonic splicing regulatory elements skew synonymous codon usage near intron-exon boundaries in mammals. Molecular Biology and Evolution 24:1600-1603. doi: 10.1093/molbev/msm104.
44. Pavon-Eternod M, David A, Dittmar K, Berglund P, Pan T, Bennink JR, Yewdell JW. 2013a. Vaccinia and influenza A viruses select rather than adjust tRNAs to optimize translation. Nucleic Acids Research 41:1914-1921. doi: 10.1093/nar/gks986.
45. Pavon-Eternod M, Gomes S, Rosner MR, Pan T. 2013b. Overexpression of initiator methionine tRNA leads to global reprogramming of tRNA expression and increased proliferation in human epithelial cells. RNA 19:461-466. doi: 10.1261/rna.037507.112.
46. Pechmann S, Frydman J. 2012. Evolutionary conservation of codon optimality reveals hidden signatures of cotranslational folding. Nature Structural & Molecular Biology 20:1-8. doi: 10.1038/nsmb.2466.
47. Percudani R, Pavesi A, Ottonello S. 1997. Transfer RNA gene redundancy and translational selection in Saccharomyces cerevisiae. Journal of Molecular Biology 268:322-330. doi: 10.1006/jmbi.1997.0942.
48. Rao Y, Wu G, Wang Z, Chai X, Nie Q, Zhang X. 2011. Mutation bias is the driving force of codon usage in the Gallus gallus genome. DNA Research 18:499-512. doi: 10.1093/dnares/dsr035.
49. Rawlings TA, Collins TM, Bieler R. 2003. Changing identities: tRNA duplication and remolding within animal mitochondrial genomes. Proceedings of the National Academy of Sciences of the United States of America 100:15700-15705. doi: 10.1073/pnas.2535036100.
50. Rogers HH, Bergman CM, Griffiths-Jones S. 2010. The evolution of tRNA genes in Drosophila. Genome Biology and Evolution 2:467-477. doi: 10.1093/gbe/evq034.
51. Saikia M, Krokowski D, Guan BJ, Ivanov P, Parisien M, Hu GF, Anderson P, Pan T, Hatzoglou M. 2012. Genomewide identification and quantitative analysis of cleaved tRNA fragments induced by cellular stress. Journal of Biological Chemistry 287:42708-42725. doi: 10.1074/jbc.M112.371799.
52. Saks ME, Conery JS. 2007. Anticodon-dependent conservation of bacterial tRNA gene sequences. RNA 13:651-660. doi: 10.1261/rna.345907.
53. Saks ME, Sampson JR, Abelson J. 1998. Evolution of a transfer RNA gene through a point mutation in the anticodon. Science 279:1665-1670. doi: 10.1126/science.279.5357.1665.
54. Schmeing TM, Voorhees RM, Kelley AC, Ramakrishnan V. 2011. How mutations in tRNA distant from the anticodon affect the fidelity of decoding. Nature Structural & Molecular Biology 18:432-436. doi: 10.1038/nsmb.2003.
55. Schultz DW, Yarus M. 1994. tRNA structure and ribosomal function. I. tRNA nucleotide 27-43 mutations enhance first position wobble. Journal of Molecular Biology 235:1381-1394. doi: 10.1006/jmbi.1994.1095.
56. Sharp PM, Li WH. 1986a. An evolutionary perspective on synonymous codon usage in unicellular organisms. Journal of Molecular Evolution 24:28-38. doi: 10.1007/BF02099948.
57. Sharp PM, Li WH. 1986b. Codon usage in regulatory genes in Escherichia coli does not reflect selection for "rare" codons. Nucleic Acids Research 14:7737-7749. doi: 10.1093/nar/14.19.7737.
58. Sharp PM, Li WH. 1987. The codon Adaptation Index-a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Research 15:1281-1295. doi: 10.1093/nar/15.3.1281.
59. Stamatakis A. 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688-2690. doi: 10.1093/bioinformatics/btl446.
60. Stoletzki N, Eyre-Walker A. 2007. Synonymous codon usage in Escherichia coli: selection for translational accuracy. Molecular Biology and Evolution 24:374-381. doi: 10.1093/molbev/msl166.
61. Sukumaran J, Holder MT. 2010. DendroPy: a Python library for phylogenetic computing. Bioinformatics 26:1569-1571. doi: 10.1093/bioinformatics/btq228.
62. Teshima KM, Innan H. 2004. The effect of gene conversion on the divergence between duplicated genes. Genetics 166:1553-1560. doi: 10.1534/genetics.166.3.1553.
63. Thanaraj TA, Argos P. 1996. Ribosome-mediated translational pause and protein domain organization. Protein Science 5:1594-1612. doi: 10.1002/pro.5560050814.
64. Tsai C-J, Sauna ZE, Kimchi-Sarfaty C, Ambudkar SV, Gottesman MM, Nussinov R. 2008. Synonymous mutations and ribosome stalling can lead to altered folding pathways and distinct minima. Journal of Molecular Biology 383:281-291. doi: 10.1016/j.jmb.2008.08.012.
65. Tuller T, Carmi A, Vestsigian K, Navon S, Dorfan Y, Zaborske J, Pan T, Dahan O, Furman I, Pilpel Y. 2010. An evolutionarily conserved mechanism for controlling the efficiency of protein translation. Cell 141:344-354. doi: 10.1016/j.cell.2010.03.031.
66. Urrutia AO, Hurst LD. 2001. Codon usage bias covaries with expression breadth and the rate of synonymous evolution in humans, but this is not evidence for selection. Genetics 159:1191-1199.
67. Varenne S, Buc J, Lloubes R, Lazdunski C. 1984. Translation is a non-uniform process. Effect of tRNA availability on the rate of elongation of nascent polypeptide chains. Journal of Molecular Biology 180:549-576. doi: 10.1016/0022-2836(84)90027-5.
68. Von Pawel-Rammingen U, Aström S, Byström AS. 1992. Mutational analysis of conserved positions potentially important for initiator tRNA function in Saccharomyces cerevisiae. Molecular and Cellular Biology 12:1432-1442.
69. Widmann J, Harris J, Lozupone C. 2010. Stable tRNA-based phylogenies using only 76 nucleotides. RNA 1469-1477. doi: 10.1261/rna.726010.
70. Wilke CO, Drummond DA. 2010. Signatures of protein biophysics in coding sequence evolution. Current Opinion In Structural Biology 20:385-389. doi: 10.1016/j.sbi.2010.03.004.
71. Withers M, Wernisch L, dos Reis M. 2006. Archaeology and evolution of transfer RNA genes in the Escherichia coli genome. RNA 12:933-942. doi: 10.1261/rna.2272306.
72. Wolf YI, Rogozin IB, Kondrashov AS, Koonin EV. 2001. Genome alignment, evolution of prokaryotic genomeorganization, and prediction of gene function using genomic context. Genome Research 11:356-372. doi: 10.1101/gr.161901.
73. Zhang G, Hubalewska M, Ignatova Z. 2009. Transient ribosomal attenuation coordinates protein synthesis and co-translational folding. Nature Structural & Molecular Biology 16:274-280. doi: 10.1038/nsmb.1554.
74. Zhou T, Weems M, Wilke CO. 2009. Translationally optimal codons associate with structurally sensitive sites in proteins. Molecular Biology and Evolution 26:1571-1580. doi: 10.1093/molbev/msp070.
75. Zhou M, Guo J, Cha J, Chae M, Chen S, Barral JM, Sachs MS, Liu Y. 2013. Non-optimal codon usage affects expression, structure and function of clock protein FRQ. Nature 495:111-115. doi: 10.1038/nature11833.