The surprising negative correlation of gene length and optimal codon use - Disentangling translational selection from GC-biased gene conversion in yeast

BMC Evolutionary Biology

Volumn 11, Issue 1, 2011, Pages

  Stoletzki, Nina ^a,b,c  

^a UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY OF SUSSEX   (United Kingdom)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

cause of correlation; GC biased gene conversion; optimal codon use

Indexed keywords

CORRELATION; EVOLUTIONARY BIOLOGY; GENE EXPRESSION; GENETIC ANALYSIS; RECOMBINATION; YEAST;

EUKARYOTA;

FUNGAL PROTEIN;

ARTICLE; CODON; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PROTEIN SYNTHESIS; SACCHAROMYCES CEREVISIAE;

BASE SEQUENCE; CODON; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; PROTEIN BIOSYNTHESIS; SACCHAROMYCES CEREVISIAE;

EID: 79953805331     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/1471-2148-11-93     Document Type: Article

References (77)

1. The selection-mutation-drift theory of synonymous codon usage. M Bulmer, Genetics 1991 129 897 907 1752426
2. Translational selection and molecular evolution. H Akashi A Eyre-Walker, Curr Opinion Genet & Dev 1998 8 688 693 (Pubitemid 28558532)
3. Gene expression and molecular evolution. H Akashi, Curr Opin Genetics & Dev 2001 11 660 666 (Pubitemid 33000338)
4. Evolution of synonymous codon usage in metazoans. L Duret, Curr Opin Genet Dev 2002 12 640 649 10.1016/S0959-437X(02)00353-2 12433576 (Pubitemid 35335981)
5. Absolute in vivo translation rates of individual codons in Escherichia coli. The two glutamic acid codons GAA and GAG are translated with a threefold difference in rate. MA Sorensen S Petersen, J Mol Biol 1991 222 265 280 10.1016/0022-2836(91)90211-N 1960727 (Pubitemid 121004006)
6. Codon preferences in free-living microorganisms. SGE Andersen CG Kurland, Microbiol Rev 1990 54 198 210 2194095
7. Errors and alternatives in reading the universal genetic code. J Parker, Microbiol Rev 1989 53 273 298 2677635
8. In vivo introduction of unpreferred synonymous codons into the Drosophila Adh gene results in reduced levels of ADH protein. DB Carlini W Stephan, Genetics 2003 163 239 243 12586711 (Pubitemid 36222668)
9. Synonymous codon bias is related to gene length in Escherichia coli: selection for translational accuracy? A Eyre-Walker, Mol Biol Evol 1996 13 864 872 8754221 (Pubitemid 26240090)
10. Relationship of codon bias to mRNA concentration and protein length in Saccharomyces cerevisiae. A Coghlan KH Wolfe, Yeast 2000 16 1131 1145 10.1002/1097-0061(20000915)16:12<1131::AID-YEA609>3.0.CO;2-F 10953085
11. Gene length and codon usage bias in Drosophila melanogaster, Saccharomyces cerevisiae and Escherichia coli. EN Moriyama JR Powell, Nucleic Acid Research 1998 26 13 3188 3193 10.1093/nar/26.13.3188 (Pubitemid 28288917)
12. Synonymous Codon Usage in Escherichia coli: Selection for Translational Accuracy. N Stoletzki A Eyre-Walker, Mol Biol Evol 2007 24 374 381 10.1093/molbev/msl166 17101719 (Pubitemid 46204370)
13. Synonymous Codon Usage in Drosophila melanogaster: Natural Selection and Translational Accuracy. H Akashi, Genetics 1994 136 927 935 8005445 (Pubitemid 24085643)
14. Synonymous Codon Usage, Accuracy of Translation, and Gene Length in Caenorhabditis elegans. G Marais L Duret, J Mol Evol 2001 52 275 280 11428464
15. Mistranslation-Induced Protein Misfolding as a Dominant Constraint on Coding-Sequence Evolution. DA Drummond CO Wilke, Cell 2008 134 2341 352 10.1016/j.cell.2008.05.042 (Pubitemid 352010328)
16. Natural selection on synonymous sites is correlated with gene length and recombination in Drosophila. JM Comeron M Kreitman M Aguade, Genetics 1999 151 239 249 9872963 (Pubitemid 29031891)
17. Expression pattern and, surprisingly, gene length shape codon usage in Caenorhabditis, Drosophila, and Arabidopsis. L Duret D Mouchiroud, Proc Natl Acad Sci USA 1999 96 4482 4487 10.1073/pnas.96.8.4482 10200288 (Pubitemid 29190362)
18. Selective and Mutational Patterns Associated With Gene Expression in Humans: Influence on Synonymous Composition and Intron Presence. JM Comeron, Genetics 2004 167 1293 1304 10.1534/genetics.104.026351 15280243 (Pubitemid 39045637)
19. Translational Selection and Yeast Proteome Evolution. H Akashi, Genetics 2003 164 1291 1303 12930740 (Pubitemid 37102197)
20. Neutral effect of recombination on base composition. G Marais D Mouchiroud L Duret, Genet Res Camb 2003 81 79 87 10.1017/S0016672302006079 (Pubitemid 36575831)
21. Molecular Evolution Between Drosophila melanogaster and D. simulans: Reduced Codon Bias, Faster Rates of Amino Acid Substitution, and Larger Proteins in D. melanogaster. H Akashi, Genetics 1996 144 1297 1307 8913769
22. The effect of linkage on limits to artificial selection. WG Hill A Robertson, Genet Res 1966 8 3 269 94 10.1017/S0016672300010156 5980116
23. Linkage limits the power of natural selection in Drosophila. A Betancourt D Presgraves, Proc Natl Acad Sci USA 2002 99 13616 13620 10.1073/pnas.212277199 12370444 (Pubitemid 35215429)
24. The correlation between intron length and recombination in Drosophila: dynamic equilibrium between mutational and selective forces. JM Comeron M Kreitman, Genetics 2000 156 1175 1190 11063693
25. Population, evolutionary and genomic consequences of interference selection. JM Comeron M Kreitman, Genetics 2002 161 389 410 12019253 (Pubitemid 34564066)
26. Intragenic Hill-Robertson Interference influences selection intensity on synonymous mutations in Drosophila. JM Comeron TB Guthrie, Mol Biol Evol 2005 22 2519 2530 10.1093/molbev/msi246 16120803 (Pubitemid 41661388)
27. Background selection in single genes may explain patterns of codon bias. L Loewe B Charlesworth, Genetics 2007 175 1381 1393 10.1534/genetics.106.065557 17194784 (Pubitemid 46798238)
28. The effects of Hill-Robertson Interference between weakly selected mutations on patterns of molecular evolution and variation. GAT McVean B Charlesworth, Genetics 2000 155 929 944 10835411 (Pubitemid 30397140)
29. Intragenic spatial patterns of codon usage bias in prokaryotic and eukaryotic genomes. H Qin WB Wu JM Comeron M Kreitman WH Li, Genetics 2004 168 2245 2260 10.1534/genetics.104.030866 15611189 (Pubitemid 40066358)
30. Reduced natural selection associated with low recombination in Drosophila melanogaster. RM Kliman J Hey, Mol Biol Evol 1993 10 1239 1258 8277853 (Pubitemid 23352608)
31. Interactions between natural selection, recombination and gene density in the genes of Drosophila. J Hey RM Kliman, Genetics 2002 160 595 608 11861564 (Pubitemid 34194533)
32. Hill-Robertson interference in Drosophila melanogaster: reply to Marais, Mouchiroud and Duret. RM Kliman J Hey, Genet Res Camb 2003 81 89 90 10.1017/S0016672302006067 (Pubitemid 36575832)
33. Recombination and mammalian genome evolution. A Eyre-Walker, Proc Roy Soc London Series B 1993 252 237 243 10.1098/rspb.1993.0071 (Pubitemid 23210755)
34. Integrating genomics, bioinformatics, and classical genetics to study the effects of recombination on genome evolution. JA Birdsell, Mol Biol Evol 2002 19 1181 1197 12082137 (Pubitemid 34743242)
35. GC-biased segregation of non-coding polymorphisms in Drosophila. N Galtier E Bazin N Bierne, Genetics 2006 172 221 228 10.1534/genetics.105.046524 16157668 (Pubitemid 43345485)
36. Biased gene conversion: implications for genome and sex evolution. G Marais, TRENDS in Genetics 2003 19 6 330 338 10.1016/S0168-9525(03)00116-1 12801726 (Pubitemid 36694616)
37. Does recombination improve selection on codon usage? Lessons from a nematode and fly complete genomes. G Marais D Mouchiroud L Duret, Proc Natl Acad Sci USA 2001 10 5688 5692 98 10.1073/pnas.091427698 (Pubitemid 32435703)
38. Review Codon Usage and tRNA Content in Unicellular and Multicellular Organisms. T Ikemura, Mol Biol Evol 1985 2 13 34 3916708 (Pubitemid 15152046)
39. Transfer RNA gene redundancy and translational selection in Saccharomyces cerevisiae. R Percudani A Pavesi S Ottonello, J Mol Biol 1997 268 322 330 10.1006/jmbi.1997.0942 9159473 (Pubitemid 27208057)
40. Assessing the Determinants of Evolutionary Rates in the Presence of Noise. JB Plotkin HB Fraser, Mol Biol Evol 2007 24 113 1121 10.1093/molbev/ msm044 (Pubitemid 47343649)
41. Single Determinant Dominates the Rate of Yeast Protein Evolution. DA Drummond A Raval COA Wilke, Mol Biol Evol 2006 23 327 337 10.1093/molbev/msj038 16237209 (Pubitemid 43100047)
42. Relationship between transcription and initiation of meiotic recombination: toward chromatin accessibility. A Nicolas, Proc Natl Acad Sci USA 1998 95 87 89 10.1073/pnas.95.1.87 9419331 (Pubitemid 28103909)
43. Evidence for selection on synonymous mutations affecting stability of mRNA secondary structure in mammals. JV Chamary LD Hurst, Genome Biol 2005 6 75 10.1186/gb-2005-6-9-r75 16168082
44. mRNAs have greater negative folding free energies than shuffled or codon choice randomized sequences. W Seffens D Digby, Nucleic Acids Res 1999 27 1578 1584 10.1093/nar/27.7.1578 10075987 (Pubitemid 29209532)
45. Widespread selection for Local RNA secondary Structure in Coding Regions of Bacterial Genes. L Katz CB Burge, Genome Research 2003 13 2042 2051 10.1101/gr.1257503 12952875 (Pubitemid 37161761)
46. Conflicting selection pressures on synonymous codon use in yeast indicate selection on mRNA secondary structures. N Stoletzki, BMC Evolutionary Biology 2008 8 224 10.1186/1471-2148-8-224 18671878
47. Patterns of base composition within the genes of Drosophila melanogaster. RM Kliman A Eyre-Walker, J Mol Evol 1998 46 534 541 10.1007/PL00006334 9545464 (Pubitemid 28194459)
48. Reduced synonymous substitution rate at the start of enterobacterial genes. A Eyre-Walker M Bulmer, Nucleic Acid Research 1993 21 19 4599 4603 10.1093/nar/21.19.4599 (Pubitemid 23292727)
49. On the Genetic Basis of Variation and Heterogeneity of DNA Base Composition. N Sueoka, Proc Natl Acad Sci USA 1962 48 582 591 10.1073/pnas.48.4.582 13918161
50. A genome-wide view of the spectrum of spontaneous mutations in yeast. M Lynch W Sung K Morris N Coffey CR Landry EB Dopman WJ Dickinson K Okamoto S Kulkarni DL Hartl WK Thomas, Proc Natl Acad Sci USA 2008 105 9272 9277 10.1073/pnas.0803466105 18583475
51. The Double-Strand-Break Repair Model for Recombination. JW Szostak TL Orr-Weaver RJ Rothstein FW Stahl, Cell 1983 33 25 35 10.1016/0092-8674(83)90331- 8 6380756 (Pubitemid 13096431)
52. Recombination at work for meiosis. KN Smith A Nicolas, Curr Opin Genet Dev 1998 8 200 211 10.1016/S0959-437X(98)80142-1 9610411 (Pubitemid 28206284)
53. The relationship between homology length and crossing over during the repair of a broken chromosome. O Inbar B Liefshitz G Bitan M Kupiec, J Biol Chem 2000 275 40 30833 30838 10.1074/jbc.C000133200 10924495
54. Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. F Paques JE Haber, Microbiology and Molecular Biology Reviews 1999 63 2 349 404 10357855 (Pubitemid 29264976)
55. Clustering of meiotic double-strand breaks on yeast chromosome III. F Baudat A Nicolas, Proc Natl Acad Sci USA 1997 94 5213 5218 10.1073/pnas.94.10. 5213 9144217 (Pubitemid 27214763)
56. Global mapping of meiotic recombination hotspots and coldspots in the yeast. JL Gerton J DeRisi R Shroff M Lichten PO Brown TD Petes, Saccharomyces cerevisiae
57. Distribution of meiotic recombination sites. B de Massy, TRENDS in Genetics 2003 18 9 514 522 10.1016/S0168-9525(03)00201-4 (Pubitemid 37101092)
58. The many faces of mismatch repair in meiosis. RH Borts SR Chambers MFF Abdulah, Mutation Research 2000 451 129 150 10.1016/S0027-5107(00)00044-0 10915869 (Pubitemid 30488108)
59. Analysis of a Gene Conversion Gradient at the HIS4 Locus in Saccharomyces cerevisiae. P Detloff MA White TD Petes, Genetics 1992 132 113 123 1398048
60. Patterns of Heteroduplex Formation Associated With the Initiation of Meiotic Recombination in the Yeast Saccharomyces cerevisiae. JD Merker M Dominska TD TD Petes, Genetics 2003 165 47 63 14504217 (Pubitemid 37204055)
61. Mutagenesis from Meiotic Recombination Is Not a Primary Driver of Sequence Divergence between Saccharomyces Species. M Noor, Mol Biol Evol 2008 25 2439 2444 10.1093/molbev/msn186 18723832
62. Protein Rates of Evolution Are Predicted by Double-Strand Break Events, Independent of Crossing-over Rates. CC Weber LD Hurst, Gen Biol Evol 2009 1 340 349 10.1093/gbe/evp033
63. Biased Gene Conversion Affects Patterns of Codon Usage and Amino Acid Usage in the Saccharomyces sensu stricto Group of Yeasts. RJ Harrison B Charlesworth, Mol Biol Evol 2011 28 117 129 10.1093/molbev/msq191 20656793
64. Adaptation or biased gene conversion? Extending the null hypothesis of molecular evolution. N Galtier L Duret, Trends in Genetics 2007 23 6 273 277 10.1016/j.tig.2007.03.011 17418442 (Pubitemid 46770896)
65. GC-biased gene conversion promotes the fixation of deleterious amino acid changes in primates. N Galtier L Duret S Glemin V Ranwez, Trends in Genetics 2009 25 1 1 5 10.1016/j.tig.2008.10.011 19027980
66. Hotspots of Biased Nucleotide Substitutions in Human Genes. J Berglund KS Pollard MT Webster, PLOS Biology 2009 7 1 0045 0062 10.1371/journal.pbio. 1000026
67. The Impact of Recombination on Nucleotide Substitutions in the Human Genome. L Duret P Arndt, PLOS Genetics 2008 5 5 1000071 10.1371/journal.pgen. 1000071 (Pubitemid 351811507)
68. Intense and highly localized gene conversion activity in human meiotic crossover hotspots. AJ Jeffreys CA May, Nature Genetics 2004 36 2 151 156 10.1038/ng1287 14704667 (Pubitemid 38174373)
69. Endonucleotic cleavage of eukaryotic mRNAs with stalls in translation elongation. MK Doma R Parker, Nature 2006 440 561 564 10.1038/nature04530 16554824
70. A genome-wide view of the spectrum of spontaneous mutations in yeast. M Lynch W Sung K Morris N Coffey CR Landry EB Dopman WJ Dickinson K Okamoto S Kulkarni DL Hartl WK Thomas, Proc Natl Acad Sci USA 2008 105 9272 9277 10.1073/pnas.0803466105 18583475
71. A relationship between GC-content and coding sequence length. JL Oliver A Marin, J Mol Evol 1996 43 216 223 10.1007/BF02338829 8703087 (Pubitemid 26315123)
72. Effects of GC content and mutational pressure on the lengths of exons and coding sequences. X Xia Z Xie WH Li, J Mol Evol 2003 56 362 370 10.1007/s00239-002-2406-1 12612839 (Pubitemid 36279040)
73. Dissecting the regulatory cicuity of a eukaryotic genome. FC Holstege EG Jennings JJ Wyrick TI Lee CJ Hengartner MR Green TR Golub ES Lander RA Young, Cell 1998 95 717 728 10.1016/S0092-8674(00)81641-4 9845373 (Pubitemid 28544132)
74. High-resolution mapping of meiotic crossovers and non-crossovers in yeast. E Mancera R Bourgon A Brozzi W Huber LM Steinmetz, Nature 2008 454 479 485 Proc Natl Acad Sci USA 2000, 97(21): 11383-11390 10.1038/nature07135 18615017
75. Mapping Meiotic Single-Strand DNA Reveals a New Landscape of DNA Double-Strand Breaks in Saccharomyces cerevisiae. C Buhler V Borde M Lichten, PLoS Biol 2007 5 324 10.1371/journal.pbio.0050324 18076285
76. Association of Mre11p with Double-Strand Break Sites during Yeast Meiosis. V Borde W Lin E Novikov JH Petrini M Lichten A Nicolas, Mol Cell 2004 13 3389 401 10.1016/S1097-2765(04)00034-6 (Pubitemid 38229811)
77. Selection conflicts, gene expression, and codon usage trends in yeast. RM Kliman N Irving M Santiago, J Mol Biol 2003 57 1 98 109 (Pubitemid 36920454)