Structural determinants of the rate of protein evolution in yeast

Molecular Biology and Evolution

Volumn 23, Issue 9, 2006, Pages 1751-1761

  Bloom, Jesse D ^a   Drummond, D Allan ^b   Arnold, Frances H ^a   Wilke, Claus O ^c  

^a California Institute of Technology   (United States)

^b CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^c UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

Designability; Evolutionary rate; Principal component regression; Protein evolution; Protein structure; Yeast

Indexed keywords

FUNGAL PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CORRELATION ANALYSIS; MOLECULAR EVOLUTION; PROTEIN STRUCTURE; YEAST;

ANALYSIS OF VARIANCE; EVOLUTION, MOLECULAR; MODELS, GENETIC; OPEN READING FRAMES; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; REGRESSION ANALYSIS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SELECTION (GENETICS); SELECTION, GENETIC; STATISTICS, NONPARAMETRIC;

EID: 33748143748     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msl040     Document Type: Article

References (75)

1. Agrafioti I, Swire J, Abbott J, Huntley D, Butcher S, Stumpf MPH. 2005. Comparative analysis of the Saccharomyces cerevisiae and Caenorhabditis elegans protein interaction networks. BMC Evol Biol 5:23.
2. Altschul SF, Gish W, Miller W, Meyers EW, Lipman DJ. 1990. Basic local alignment search tool. J Mol Biol 215:403-10.
3. Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57:289-300.
4. Bloom JD, Adami C. 2003. Apparent dependence of protein evolutionary rate on number of interactions is linked to biases in protein-protein interactions data sets. BMC Evol Biol 3:21.
5. Bloom JD, Labthavikul ST, Otey CR, Arnold FH. 2006. Protein stability promotes evolvability. Proc Natl Acad Sci USA 103:5869-74.
6. Bloom JD, Silberg JJ, Wilke CO, Drummond DA, Adami C, Arnold FH. 2005. Thermodynamic prediction of protein neutrality. Proc Natl Acad Sci USA 102:606-11.
7. Brookfield JFY. 2000. What determines the rate of sequence evolution? Curr Biol 10:R410-1.
8. Brown CJ, Takayama S, Campen AM, Vise P, Marshall TW, Oldfield CJ, Williams CJ, Dunker AK. 2002. Evolutionary rate heterogeneity in proteins with long disordered regions. J Mol Evol 55:104-10.
9. Bustamante CD, Townsend JP, Hartl DL. 2000. Solvent accessibility and purifying selection within proteins of Escherichia coli and Salmonella enterica. Mol Biol Evol 17:301-8.
10. Chan HS, Bornberg-Bauer E. 2002. Perspectives on protein evolution from simple exact models. Appl Bioinformatics 1:121-44.
11. Coghlan A, Wolfe KH. 2000. Relationship of codon bias to mRNA concentration and protein length in Saccharomyces cerevisiae. Yeast 16:1131-45.
12. Creighton TE. 1992. Proteins: structures and molecular properties. 2nd ed. New York: Freeman.
13. Dean AM, Neuhauser C, Grenier E, Golding GB. 2002. The pattern of amino acid replacements in α/β-barrels. Mol Biol Evol 19:1846-64.
14. Dokholyan NV, Shakhnovich EI. 2001. Understanding heirarchical protein evolution from first principles. J Mol Biol 312:289-307.
15. Drummond DA, Bloom JD, Adami C, Wilke CO, Arnold FH. 2005. Why highly expressed proteins evolve slowly. Proc Natl Acad Sci USA 102:14338-43.
16. Drummond DA, Raval A, Wilke CO. 2006. A single determinant dominates the rate of yeast protein evolution. Mol Biol Evol 23:327-37.
17. England JL, Shakhnovich BE, Shakhnovich EI. 2003. Natural selection of more designable folds: a mechanism for thermophilic adaptation. Proc Natl Acad Sci USA 100:8727-31.
18. England JL, Shakhnovich EI. 2003. Structural determinant of protein designability. Phys Rev Lett 90:218101.
19. Fraser HB, Hirsh AE, Steinmetz LM, Scharfe C, Feldman MW. 2002. Evolutionary rate in the protein interaction network. Science 296:750-2.
20. Goldman N, Thorne JL, Jones DT. 1998. Assessing the impact of secondary structure and solvent accessibility on protein evolution. Genetics 149:445-58.
21. Govindarajan S, Goldstein RA. 1996. Why are some protein structures so common? Proc Natl Acad Sci USA 93:3341-5.
22. Govindarajan S, Goldstein RA. 1997. The foldability landscape of model proteins. Biopolymers 42:427-38.
23. Hahn MW, Conant GC, Wagner A. 2004. Molecular evolution in large genetic networks: does connectivity equal constraint? J Mol Evol 58:203-11.
24. Hahn MW, Kern AD. 2005. Comparative genomics of centrality and essentiality in three eukaryotic protein-interaction networks. Mol Biol Evol 22:803-6.
25. Hirsh AE, Fraser HB. 2001. Protein dispensability and rate of evolution. Nature 411:1046-9.
26. Holstege FCP, Jennings E, Wyrick JJ, Lee TI, Hengartner CJ, Green MR, Golub TR, Lander ES, Young RA. 1998. Dissecting the regulatory circuitry of a eukaryotic genome. Cell 95:717-28.
27. Hurst LD, Smith NGC. 1999. Do essential genes evolve slowly? Curr Biol 9:747-50.
28. Irbäck A, Troein C. 2002. Enumerating designing sequences in the HP model. J Biol Phys 28:1-15.
29. Jansen R, Gerstein M. 2000. Analysis of the yeast transcriptome with structural and functional categories: characterizing highly expressed proteins. Nucleic Acids Res 28:1481-8.
30. Jordan IK, Rogozin IB, Wolf YI, Koonin EV. 2002. Essential genes are more evolutionarily conserved than are nonessential genes in bacteria. Genome Res 12:962-8.
31. Jordan IK, Wolf YI, Koonin EV. 2003. No simple dependence between protein evolution rate and the number of protein-protein interactions: only the most prolific interactors tend to evolve slowly. BMC Evol Biol 3:1.
32. Kabsch W, Sander C. 1983. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22:2577-637.
33. King JL, Jukes TH. 1969. Non-darwinian evolution. Science 165:788-98.
34. Koehl P, Levitt M. 2002. Protein topology and stability define the space of allowed sequences. Proc Natl Acad Sci USA 99: 1280-5.
35. Kono H, Saven JG. 2001. Statistical theory for protein combinatorial libraries. Packing interactions, backbone flexibility, and the sequence variability of a main-chain structure. J Mol Biol 306:607-28.
36. Koshi JM, Goldstein RA. 1995. Context-dependent optimal substitution matrices. Protein Eng 8:641-5.
37. Kussell E. 2005. The designability hypothesis and protein evolution. Protein Pept Lett 12:111-6.
38. Larson SM, England JL, Desjarlais JR, Pande VS. 2002. Thoroughly sampling sequence space: large-scale protein design of structural ensembles. Protein Sci 11:2804-13.
39. Lemos B, Bettencourt BR, Meiklejohn CD, Hartl DL. 2005. Evolution of proteins and gene expression levels are coupled in Drosophila and are independently associated with mRNA abundance, protein length, and number of protein-protein interactions. Mol Biol Evol 22:1345-54.
40. Li H, Helling R, Tang C, Wingreen N. 1996. Emergence of preferred structures in a simple model of protein folding. Science 273:666-9.
41. Loeb DD, Swanstrom R, Everitt L, Manchester M, Stamper SE, Hutchison CA. 1989. Complete mutagenesis of the HIV-1 protease. Nature 340:397-400.
42. Mandel J. 1982. Use of the singular value decomposition in regression analysis. Am Stat 36:15-24.
43. Marais G, Duret L. 2001. Synonymous codon usage, accuracy of translation, and gene length in Caenorhabditis elegans. J Mol Evol 52:275-80.
44. Marsh L, Griffiths CS. 2005. Protein structural influences in rhodopsin evolution. Mol Biol Evol 22:894-904.
45. McConkey BJ, Sobolev V, Edelman M. 2002. Quantification of protein surfaces, volumes and atom-atom contacts using a constrained Voronoi procedure. Bioinformatics 18:1365-73.
46. Miller J, Zeng C, Wingreen NS, Tang C. 2002. Emergence of highly designable protein-backbone conformations in an off-lattice model. Proteins Struct Funct Genet 47:506-12.
47. Mirny LA, Shakhnovich EI. 1999. Universally conserved positions in protein folds: reading evolutionary signals about stability, folding kinetics and function. J Mol Biol 291: 177-96.
48. Munoz ET, Bogarad LD, Deem MW. 2004. Microarray and EST database estimates of mRNA expression levels differ: the protein length versus expression curve for C. elegans. BMC Genomics 5:30.
49. Murzin AG, Brenner SE, Hubbard T, Chothia C. 1995. SCOP: a structural classification of proteins database for the investigation of sequences and structures. J Mol Biol 247:536-40.
50. Ohta T, Kimura M. 1971. On the constancy of the evolutionary rate of cistrons. J Mol Evol 1:18-25.
51. Overington J, Donnelly D, Johnson MS, Šali A, Blundell TL. 1992. Environment-specific amino acid substitution tables: tertiary templates and prediction of protein folds. Protein Sci 1:216-26.
52. Pakula AA, Young VB, Sauer RT. 1986. Bacteriophage λ cro mutations: effects on activity and intracellular degradation. Proc Natl Acad Sci USA 83:8829-33.
53. Pal C, Papp B, Hurst LD. 2001. Highly expressed genes in yeast evolve slowly. Genetics 158:927-31.
54. Pal C, Papp B, Hurst LD. 2003. Rate of evolution and gene dispensability. Nature 421:496-7.
55. R Development Core Team. 2005. R: a language and environment for statistical computing. Vienna, Austria: R foundation for statistical computing.
56. Shakhnovich BE, Deeds E, Delisi C, Shakhnovich E. 2005. Protein structure and evolutionary history determine sequence space topology. Genome Res 15:385-92.
57. Shakhnovich EI. 1998. Protein design: a perspective from simple tractable models. Fold Des 3:R45-58.
58. Sharp P, Li W. 1987. The codon adaptation index - a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res 15:1281-95.
59. Shortle D, Lin B. 1985. Genetic analysis of staphylococcal nuclease: identification of three intragenic "global" suppressors of nuclease-minus mutations. Genetics 110:539-55.
60. Sokal RR, Rohlf FJ. 1994. Biometry. 3rd ed. New York: Freeman.
61. Thompson JD, Higgins DG, Gibson TJ. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-80.
62. Thorne JL, Goldman N, Jones DT. 1996. Combining protein evolution and secondary structure. Mol Biol Evol 13:666-73.
63. Tiana G, Broglia RA, Shakhnovich EI. 2000. Hiking in the energy landscape in sequence space: a bumpy road to good folders. Proteins 39:244-51.
64. Tiana G, Shakhnovich BE, Dokholyan NV, Shakhnovich EI. 2004. Imprint of evolution on protein structure. Proc Natl Acad Sci USA 101:2846-51.
65. Voigt CA, Mayo SL, Arnold FH, Wang ZG. 2001. Computational method to reduce the search space for directed protein evolution. Proc Natl Acad Sci USA 98:3778-83.
66. Wall DP, Fraser HB, Hirsh AE. 2003. Detecting putative orthologs. Bioinformatics 19:1710-1.
67. Wall DP, Hirsh AE, Fraser HB, Kumm J, Giaever G, Eisen MB, Feldman MW. 2005. Functional genomic analysis of the rates of protein evolution. Proc Natl Acad Sci USA 102:5483-8.
68. Wingreen NS, Li H, Tang C. 2004. Designability and thermal stability of protein structures. Polymer 45:699-705.
69. Wolynes PG. 1996. Symmetry and the energy landscapes of biomolecules. Proc Natl Acad Sci USA 93:14249-55.
70. Wroe R, Bornberg-Bauer E, Chan HS. 2005. Comparing folding codes in simple heteropolymer models of protein evolutionary landscape: robustness of the superfunnel paradigm. Biophys J 88:118-31.
71. Yang ZH. 1997. PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13:555-6.
72. Zhang J, He X. 2005. Significant impact of protein dispensability on the instantaneous rate of protein evolution. Mol Biol Evol 22:1147-55.
73. Zhang W, Sun ZB, Zou XW. 2005. Designability of protein structures on the hexagonal lattice model. Chin Phys Lett 22: 2133-6.
74. Zou JM, Saven JG. 2000. Statistical theory of combinatorial libraries of folding proteins: energetic discrimination of a target structure. J Mol Biol 296:281-94.
75. Zuckerkandl E, Pauling L. 1965. Evolutionary divergence and convergence in proteins. In: Bryson V, Vogel HJ, editors. Evolving genes and proteins. New York: Academic Press. p 97-166.