Selection on codon bias in yeast: A transcriptional hypothesis

Nucleic Acids Research

Volumn 41, Issue 20, 2013, Pages 9382-9395

  Trotta, Edoardo ^a  

^a INSTITUTE OF TRANSLATIONAL PHARMACOLOGY   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

AMINOACYL TRANSFER RNA; MESSENGER RNA; MESSENGER RNA PRECURSOR; TRANSFER RNA;

ARTICLE; CODON USAGE; EVOLUTIONARY ADAPTATION; EXPERIMENTAL STUDY; GENE EXPRESSION; GENETIC ANALYSIS; GENETIC CORRELATION; GENETIC SELECTION; INTRON; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECONDARY STRUCTURE; RNA FOLDING; RNA SPLICING; RNA STABILITY; RNA STRUCTURE; THEORETICAL STUDY; TRANSCRIPTION REGULATION; YEAST;

BASE COMPOSITION; CODON; CODON, INITIATOR; CODON, TERMINATOR; DNA, INTERGENIC; INTRONS; MUTATION; NUCLEOSOMES; RNA FOLDING; RNA, MESSENGER; RNA, TRANSFER; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SELECTION, GENETIC; THERMODYNAMICS; TRANSCRIPTION, GENETIC;

EID: 84890069561     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt740     Document Type: Article

References (55)

1. Ikemura, T. (1985) Codon usage and tRNA content in unicellular and multicellular organisms. Mol. Biol. Evol., 2, 13-34.
2. Bennetzen, J.L. and Hall, B.D. (1982) Codon selection in yeast. J. Biol. Chem., 257, 3026-3031.
3. Gouy, M. and Gautier, C. (1982) Codon usage in bacteria: correlation with gene expressivity. Nucleic Acids Res., 10, 7055-7074.
4. Post, L.E., Strycharz, G.D., Nomura, M., Lewis, H. and Dennis, P.P. (1979) Nucleotide sequence of the ribosomal protein gene cluster adjacent to the gene for RNA polymerase subunit beta in Escherichia coli. Proc. Natl Acad. Sci. USA, 76, 1697-1701.
5. Bulmer, M. (1987) Coevolution of codon usage and transfer RNA abundance. Nature, 325, 728-730.
6. Sharp, P.M. and Li, W.H. (1986) An evolutionary perspective on synonymous codon usage in unicellular organisms. J. Mol. Evol., 24, 28-38.
7. Hershberg, R. and Petrov, D.A. (2008) Selection on codon bias. Annu. Rev. Genet., 42, 287-299.
8. Sueoka, N. (1988) Directional mutation pressure and neutral molecular evolution. Proc. Natl Acad. Sci. USA, 85, 2653-2657.
9. Chen, S.L., Lee, W., Hottes, A.K., Shapiro, L. and McAdams, H.H. (2004) Codon usage between genomes is constrained by genomewide mutational processes. Proc. Natl Acad. Sci. USA, 101, 3480-3485.
10. Rocha, E.P. and Feil, E.J. (2010) Mutational patterns cannot explain genome composition: are there any neutral sites in the genomes of bacteriäPLoS Genet., 6, e1001104.
11. Plotkin, J.B. and Kudla, G. (2011) Synonymous but not the same: the causes and consequences of codon bias. Nat. Rev. Genet., 12, 32-42.
12. Ikemura, T. (1981) 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., 151, 389-409.
13. Stoletzki, N. and Eyre-Walker, A. (2007) Synonymous codon usage in Escherichia coli: selection for translational accuracy. Mol. Biol. Evol., 24, 374-381.
14. Ikemura, T. (1982) Correlation between the abundance of yeast transfer RNAs and the occurrence of the respective codons in protein genes. Differences in synonymous codon choice patterns of yeast and Escherichia coli with reference to the abundance of isoaccepting transfer RNAs. J. Mol. Biol., 158, 573-597.
15. Behura, S.K. and Severson, D.W. (2013) Codon usage bias: causative factors, quantification methods and genome-wide patterns: with emphasis on insect genomes. Biol. Rev. Camb. Philos. Soc., 88, 49-61.
16. Zur, H. and Tuller, T. (2012) Strong association between mRNA folding strength and protein abundance in S. cerevisiae. EMBO Reports, 13, 272-277.
17. Zamft, B., Bintu, L., Ishibashi, T. and Bustamante, C. (2012) Nascent RNA structure modulates the transcriptional dynamics of RNA polymerases. Proc. Natl Acad. Sci. USA, 109, 8948-8953.
18. Wan, Y., Kertesz, M., Spitale, R.C., Segal, E. and Chang, H.Y. (2011) Understanding the transcriptome through RNA structure. Nat. Rev. Genet., 12, 641-655.
19. Nagalakshmi, U., Wang, Z., Waern, K., Shou, C., Raha, D., Gerstein, M. and Snyder, M. (2008) The transcriptional landscape of the yeast genome defined by RNA sequencing. Science, 320, 1344-1349.
20. Holstege, F.C., Jennings, E.G., Wyrick, J.J., Lee, T.I., Hengartner, C.J., Green, M.R., Golub, T.R., Lander, E.S. and Young, R.A. (1998) Dissecting the regulatory circuitry of a eukaryotic genome. Cell, 95, 717-728.
21. David, L., Huber, W., Granovskaia, M., Toedling, J., Palm, C.J., Bofkin, L., Jones, T., Davis, R.W. and Steinmetz, L.M. (2006) A high-resolution map of transcription in the yeast genome. Proc. Natl Acad. Sci. USA, 103, 5320-5325.
22. Yassour, M., Kaplan, T., Fraser, H.B., Levin, J.Z., Pfiffner, J., Adiconis, X., Schroth, G., Luo, S., Khrebtukova, I., Gnirke, A. et al. (2009) Ab initio construction of a eukaryotic transcriptome by massively parallel mRNA sequencing. Proc. Natl Acad. Sci. USA, 106, 3264-3269.
23. Lu, P., Vogel, C., Wang, R., Yao, X. and Marcotte, E.M. (2007) Absolute protein expression profiling estimates the relative contributions of transcriptional and translational regulation. Nat. Biotechnol., 25, 117-124.
24. Kraeva, R.I., Krastev, D.B., Roguev, A., Ivanova, A., Nedelcheva-Veleva, M.N. and Stoynov, S.S. (2007) Stability of mRNA/DNA and DNA/DNA duplexes affects mRNA transcription. PLoS One, 2, e290.
25. Kaplan, N., Moore, I.K., Fondufe-Mittendorf, Y., Gossett, A.J., Tillo, D., Field, Y., LeProust, E.M., Hughes, T.R., Lieb, J.D., Widom, J. et al. (2009) The DNA-encoded nucleosome organization of a eukaryotic genome. Nature, 458, 362-366.
26. Trotta, E. (2011) The 3-base periodicity and codon usage of coding sequences are correlated with gene expression at the level of transcription elongation. PLoS One, 6, e21590.
27. Kertesz, M., Wan, Y., Mazor, E., Rinn, J.L., Nutter, R.C., Chang, H.Y. and Segal, E. (2010) Genome-wide measurement of RNA secondary structure in yeast. Nature, 467, 103-107.
28. Markham, N.R. and Zuker, M. (2008) UNAFold: software for nucleic acid folding and hybridization. Methods Mol. Biol., 453, 3-31.
29. Peden, J.F. (1999) Analysis of codon usage. Ph.D. Thesis. University of Nottingham, UK.
30. Ponty, Y., Termier, M. and Denise, A. (2006) GenRGenS: software for generating random genomic sequences and structures. Bioinformatics, 22, 1534-1535.
31. Knuth, D.E. (1997) The Art of Computer Programming, Vol. 2, 3rd edn. Seminumerical Algorithms. Addison-Wesley Longman Publishing Co., Inc, Boston, MA, USA.
32. Tillo, D. and Hughes, T.R. (2009) G+C content dominates intrinsic nucleosome occupancy. BMC Bioinformatics, 10, 442.
33. Hodges, C., Bintu, L., Lubkowska, L., Kashlev, M. and Bustamante, C. (2009) Nucleosomal fluctuations govern the transcription dynamics of RNA polymerase II. Science, 325, 626-628.
34. Perales, R. and Bentley, D. (2009) ''Cotranscriptionality'': the transcription elongation complex as a nexus for nuclear transactions. Mol. Cell, 36, 178-191.
35. Carrillo Oesterreich, F., Preibisch, S. and Neugebauer, K.M. (2010) Global analysis of nascent RNA reveals transcriptional pausing in terminal exons. Mol. Cell, 40, 571-581.
36. Vinogradov, A.E. (2001) Intron length and codon usage. J. Mol. Evol., 52, 2-5.
37. Korostelev, A.A. (2011) Structural aspects of translation termination on the ribosome. RNA, 17, 1409-1421.
38. Percudani, R., Pavesi, A. and Ottonello, S. (1997) Transfer RNA gene redundancy and translational selection in Saccharomyces cerevisiae. J. Mol. Biol., 268, 322-330.
39. Tuller, T., Carmi, A., Vestsigian, K., Navon, S., Dorfan, Y., Zaborske, J., Pan, T., Dahan, O., Furman, I. and Pilpel, Y. (2010) An evolutionarily conserved mechanism for controlling the efficiency of protein translation. Cell, 141, 344-354.
40. Strazewski, P., Biala, E., Gabriel, K. and McClain, W.H. (1999) The relationship of thermodynamic stability at a G x U recognition site to tRNA aminoacylation specificity. RNA, 5, 1490-1494.
41. Gingold, H. and Pilpel, Y. (2011) Determinants of translation efficiency and accuracy. Mol. Syst. Biol., 7, 481.
42. Shabalina, S.A., Ogurtsov, A.Y. and Spiridonov, N.A. (2006) A periodic pattern of mRNA secondary structure created by the genetic code. Nucleic Acids Res., 34, 2428-2437.
43. Lind, P.A. and Andersson, D.I. (2013) Fitness costs of synonymous mutations in the rpsT gene can be compensated by restoring mRNA base pairing. PLoS One, 8, e63373.
44. Kober, K.M. and Pogson, G.H. (2013) Genome-Wide Patterns of Codon Bias Are Shaped by Natural Selection in the Purple Sea Urchin, Strongylocentrotus purpuratus. G3 (Bathseda), 3, 1069-1083.
45. Akashi, H. (1994) Synonymous codon usage in Drosophila melanogaster: natural selection and translational accuracy. Genetics, 136, 927-935.
46. Waldman, Y.Y., Tuller, T., Shlomi, T., Sharan, R. and Ruppin, E. (2010) Translation efficiency in humans: tissue specificity, global optimization and differences between developmental stages. Nucleic Acids Res., 38, 2964-2974.
47. Dittmar, K.A., Goodenbour, J.M. and Pan, T. (2006) Tissue-specific differences in human transfer RNA expression. PLoS Genet., 2, e221.
48. Hoekema, A., Kastelein, R.A., Vasser, M. and de Boer, H.A. (1987) Codon replacement in the PGK1 gene of Saccharomyces cerevisiae: experimental approach to study the role of biased codon usage in gene expression. Mol. Cell Biol., 7, 2914-2924.
49. Tokuoka, M., Tanaka, M., Ono, K., Takagi, S., Shintani, T. and Gomi, K. (2008) Codon optimization increases steady-state mRNA levels in Aspergillus oryzae heterologous gene expression. Appl. Environ. Microbiol., 74, 6538-6546.
50. Koda, A., Bogaki, T., Minetoki, T. and Hirotsune, M. (2005) High expression of a synthetic gene encoding potato alpha-glucan phosphorylase in Aspergillus niger. J. Biosci. Bioeng., 100, 531-537.
51. Gu, W., Ding, J., Wang, X., de Kluyver, R.L., Saunders, N.A., Frazer, I.H. and Zhao, K.N. (2007) Generalized substitution of isoencoding codons shortens the duration of papillomavirus L1 protein expression in transiently gene-transfected keratinocytes due to cell differentiation. Nucleic Acids Res., 35, 4820-4832.
52. Novoa, E.M. and Ribas de Pouplana, L. (2012) Speeding with control: codon usage, tRNAs, and ribosomes. Trends Genet., 28, 574-581.
53. Ghaemmaghami, S., Huh, W.K., Bower, K., Howson, R.W., Belle, A., Dephoure, N., O'Shea, E.K. and Weissman, J.S. (2003) Global analysis of protein expression in yeast. Nature, 425, 737-741.
54. Qin, H., Wu, W.B., Comeron, J.M., Kreitman, M. and Li, W.H. (2004) Intragenic spatial patterns of codon usage bias in prokaryotic and eukaryotic genomes. Genetics, 168, 2245-2260.
55. Bentele, K., Saffert, P., Rauscher, R., Ignatova, Z. and Bluthgen, N. (2013) Efficient translation initiation dictates codon usage at gene start. Mol. Syst. Biol., 9, 675.