Proteome-wide evidence for enhanced positive Darwinian selection within intrinsically disordered regions in proteins

Genome Biology

Volumn 12, Issue 7, 2011, Pages

  Nilsson, Johan ^a   Grahn, Mats ^a   Wright, Anthony P H ^a,b  

^a School of Life Sciences Södertörn University   (Sweden)

^b KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEOME; PROTEIN;

ALPHA HELIX; ARTICLE; CONTROLLED STUDY; FUNGAL GENETICS; FUNGAL STRAIN; GENE SEQUENCE; GENETIC SELECTION; GENOME ANALYSIS; GENOMICS; MOLECULAR BIOLOGY; PHYLOGENY; POPULATION GENETICS; PROTEIN DEFECT; PROTEIN FUNCTION; SACCHAROMYCES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES PARADOXUS; SEQUENCE ALIGNMENT; SINGLE NUCLEOTIDE POLYMORPHISM; STRUCTURE ANALYSIS; ADAPTATION; CHEMISTRY; CODON; FUNGAL GENOME; GENETICS; METABOLISM; OPEN READING FRAME; PROTEIN SECONDARY STRUCTURE; SACCHAROMYCETALES; SPECIES DIFFERENCE;

SACCHAROMYCES CEREVISIAE; SACCHAROMYCES PARADOXUS; SACCHAROMYCETALES;

ADAPTATION, BIOLOGICAL; CODON; GENOME, FUNGAL; OPEN READING FRAMES; POLYMORPHISM, SINGLE NUCLEOTIDE; PROTEIN STRUCTURE, SECONDARY; PROTEINS; PROTEOME; SACCHAROMYCETALES; SELECTION, GENETIC; SPECIES SPECIFICITY;

EID: 79960555958     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2011-12-7-r65     Document Type: Article

References (78)

1. Kimura M. Evolutionary rate at the molecular level. Nature 1968, 217:624-626. 10.1038/217624a0, 5637732.
2. MacCallum C, Hill E. Being positive about selection. PLoS Biol 2006, 4:e87. 10.1371/journal.pbio.0040087, 1400604, 16524343.
3. Sabeti P, Reich D, Higgins J, Levine H, Richter D, Schaffner S, Gabriel S, Platko J, Patterson N, McDonald G, Ackerman H, Campbell S, Altshuler D, Cooper R, Kwiatkowski D, Ward R, Lander E. Detecting recent positive selection in the human genome from haplotype structure. Nature 2002, 419:832-837. 10.1038/nature01140, 12397357.
4. Tang K, Thornton K, Stoneking M. A new approach for using genome scans to detect recent positive selection in the human genome. PLoS Biol 2007, 5:e171. 10.1371/journal.pbio.0050171, 1892573, 17579516.
5. Yang Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 2007, 24:1586-1591. 10.1093/molbev/msm088, 17483113.
6. Chen S, Hung C, Xu J, Reigstad C, Magrini V, Sabo A, Blasiar D, Bieri T, Meyer R, Ozersky P, Armstrong J, Fulton R, Latreille J, Spieth J, Hooton T, Mardis E, Hultgren S, Gordon J. Identification of genes subject to positive selection in uropathogenic strains of Escherichia coli: a comparative genomics approach. Proc Natl Acad Sci USA 2006, 103:5977-5982. 10.1073/pnas.0600938103, 1424661, 16585510.
7. Nielsen R, Bustamante C, Clark A, Glanowski S, Sackton T, Hubisz M, Fledel-Alon A, Tanenbaum D, Civello D, White T, Sninsky J, Adams M, Cargill M. A scan for positively selected genes in the genomes of humans and chimpanzees. PLoS Biol 2005, 3:e170. 10.1371/journal.pbio.0030170, 1088278, 15869325.
8. Petersen L, Bollback J, Dimmic M, Hubisz M, Nielsen R. Genes under positive selection in Escherichia coli. Genome Res 2007, 17:1336-1343. 10.1101/gr.6254707, 1950902, 17675366.
9. Ramensky V, Bork P, Sunyaev S. Human non-synonymous SNPs: server and survey. Nucleic Acids Res 2002, 30:3894-3900. 10.1093/nar/gkf493, 137415, 12202775.
10. The International HapMap Consortium The International HapMap Project. Nature 2003, 426:789-796. 10.1038/nature02168, 14685227, The International HapMap Consortium.
11. Kirschner M, Gerhart J. Evolvability. Proc Natl Acad Sci USA 1998, 95:8420-8427. 10.1073/pnas.95.15.8420, 33871, 9671692.
12. Pigliucci M. Is evolvability evolvable?. Nat Rev Genet 2008, 9:75-82. 10.1038/nrg2278, 18059367.
13. Pigliucci M. Do we need an extended evolutionary synthesis?. Evol Int J Org Evol 2007, 61:2743-2749.
14. Cowen L, Lindquist S. Hsp90 potentiates the rapid evolution of new traits: drug resistance in diverse fungi. Science 2005, 309:2185-2189. 10.1126/science.1118370, 16195452.
15. Parter M, Kashtan N, Alon U. Facilitated variation: how evolution learns from past environments to generalize to new environments. PLoS Comput Biol 2008, 4:e1000206. 10.1371/journal.pcbi.1000206, 2563028, 18989390.
16. Wagner A. Robustness, evolvability, and neutrality. FEBS Lett 2005, 579:1772-1778. 10.1016/j.febslet.2005.01.063, 15763550.
17. Wagner A. Robustness and evolvability: a paradox resolved. Proc Biol Sci 2008, 275:91-100. 10.1098/rspb.2007.1137, 2562401, 17971325.
18. Dunker A, Oldfield C, Meng J, Romero P, Yang J, Chen J, Vacic V, Obradovic Z, Uversky V. The unfoldomics decade: an update on intrinsically disordered proteins. BMC Genomics 2008, 9(Suppl 2):S1. 10.1186/1471-2164-9-S2-S1, 2559873, 18831774.
19. Fink A. Natively unfolded proteins. Curr Opin Struct Biol 2005, 15:35-41. 10.1016/j.sbi.2005.01.002, 15718131.
20. Lobley A, Swindells M, Orengo C, Jones D. Inferring function using patterns of native disorder in proteins. PLoS Comput Biol 2007, 3:e162. 10.1371/journal.pcbi.0030162, 1950950, 17722973.
21. Wright PE, Dyson HJ. Linking folding and binding. Curr Opin Struct Biol 2009, 19:31-38. 10.1016/j.sbi.2008.12.003, 2675572, 19157855.
22. Tompa P, Dosztanyi Z, Simon I. Prevalent structural disorder in E. coli and S. cerevisiae proteomes. J Proteome Res 2006, 5:1996-2000. 10.1021/pr0600881, 16889422.
23. Bogatyreva NS, Finkelstein AV, Galzitskaya OV. Trend of amino acid composition of proteins of different taxa. J Bioinformatics Comput Biol 2006, 4:597-608.
24. Goffeau A, Barrell B, Bussey H, Davis R, Dujon B, Feldmann H, Galibert F, Hoheisel J, Jacq C, Johnston M, Louis E, Mewes H, Murakami Y, Philippsen P, Tettelin H, Oliver S. Life with 6000 genes. Science 1996, 274:546. 10.1126/science.274.5287.546, 8849441.
25. Ghaemmaghami S, Huh W, Bower K, Howson R, Belle A, Dephoure N, O'Shea E, Weissman J. Global analysis of protein expression in yeast. Nature 2003, 425:737-741. 10.1038/nature02046, 14562106.
26. Cliften P, Sudarsanam P, Desikan A, Fulton L, Fulton B, Majors J, Waterston R, Cohen B, Johnston M. Finding functional features in Saccharomyces genomes by phylogenetic footprinting. Science 2003, 301:71-76. 10.1126/science.1084337, 12775844.
27. Dujon B, Sherman D, Fischer G, Durrens P, Casaregola S, Lafontaine I, Montigny JD, Marck C, Neuvéglise C, Talla E, Goffard N, Frangeul L, Aigle M, Anthouard V, Babour A, Barbe V, Barnay S, Blanchin S, Beckerich J, Beyne E, Bleykasten C, Boisramé A, Boyer J, Cattolico L, Confanioleri F, Daruvar AD, Despons L, Fabre E, Fairhead C, Ferry-Dumazet H, et al. Genome evolution in yeasts. Nature 2004, 430:35-44. 10.1038/nature02579, 15229592.
28. Kellis M, Patterson N, Endrizzi M, Birren B, Lander E. Sequencing and comparison of yeast species to identify genes and regulatory elements. Nature 2003, 423:241-254. 10.1038/nature01644, 12748633.
29. Rossignol T, Lechat P, Cuomo C, Zeng Q, Moszer I, d'Enfert C. CandidaDB: a multi-genome database for Candida species and related Saccharomycotina. Nucleic Acids Res 2008, (36 Database):D557-561.
30. Liti G, Carter D, Moses A, Warringer J, Parts L, James S, Davey R, Roberts I, Burt A, Koufopanou V, Tsai I, Bergman C, Bensasson D, O'Kelly M, Oudenaarden A, Barton D, Bailes E, Nguyen A, Jones M, Quail M, Goodhead I, Sims S, Smith F, Blomberg A, Durbin R, Louis E. Population genomics of domestic and wild yeasts. Nature 2009, 458:337-341. 10.1038/nature07743, 2659681, 19212322.
31. Schaefer C, Schlessinger A, Rost B. Protein secondary structure appears to be robust under in silico evolution while protein disorder appears not to be. Bioinformatics 2010, 26:625-631. 10.1093/bioinformatics/btq012, 2828120, 20081223.
32. Tompa P, Kalmar L. Power law distribution defines structural disorder as a structural element directly linked with function. J Mol Biol 2010, 403:346-350. 10.1016/j.jmb.2010.07.044, 20816987.
33. Chen J, Romero P, Uversky V, Dunker A. Conservation of intrinsic disorder in protein domains and families: I. A database of conserved predicted disordered regions. J Proteome Res 2006, 5:879-887. 10.1021/pr060048x, 2543136, 16602695.
34. Ruepp A, Zollner A, Maier D, Albermann K, Hani J, Mokrejs M, Güldener ITU, Mannhaupt G, Münsterkötter M, Mewes H. The FunCat, a functional annotation scheme for systematic classification of proteins from whole genomes. Nucleic Acids Res 2004, 32:5539-5545. 10.1093/nar/gkh894, 524302, 15486203.
35. Mayrose I, Doron-Faigenboim A, Bacharach E, Pupko T. Towards realistic codon models: among site variability and dependency of synonymous and non-synonymous rates. Bioinformatics 2007, 23:i319-327. 10.1093/bioinformatics/btm176, 17646313.
36. Nozawa M, Suzuki Y, Nei M. Reliabilities of identifying positive selection by the branch-site and the site-prediction methods. Proc Natl Acad Sci USA 2009, 106:6700-6705. 10.1073/pnas.0901855106, 2672471, 19339501.
37. Luo C, Lu X, Stubbs L, Kim J. Rapid evolution of a recently retroposed transcription factor YY2 in mammalian genomes. Genomics 2006, 87:348-355. 10.1016/j.ygeno.2005.11.001, 16377127.
38. Maiti S, Doskow J, Sutton K, Nhim R, Lawlor D, Levan K, Lindsey J, Wilkinson M. The Pem homeobox gene: rapid evolution of the homeodomain, X chromosomal localization, and expression in reproductive tissue. Genomics 1996, 34:304-316. 10.1006/geno.1996.0291, 8786129.
39. Zhang J, Webb D, Podlaha O. Accelerated protein evolution and origins of human-specific features: Foxp2 as an example. Genetics 2002, 162:1825-1835. 1462353, 12524352.
40. Beskow A, Wright AP. Comparative analysis of regulatory transcription factors in Schizosaccharomyces pombe and budding yeasts. Yeast 2006, 23:929-935. 10.1002/yea.1413, 17072884.
41. Arnold F, Wintrode P, Miyazaki K, Gershenson A. How enzymes adapt: lessons from directed evolution. Trends Biochem Sci 2001, 26:100-106. 10.1016/S0968-0004(00)01755-2, 11166567.
42. Bloom J, Wilke C, Arnold F, Adami C. Stability and the evolvability of function in a model protein. Biophys J 2004, 86:2758-2764. 10.1016/S0006-3495(04)74329-5, 1304146, 15111394.
43. Basu M, Carmel L, Rogozin I, Koonin E. Evolution of protein domain promiscuity in eukaryotes. Genome Res 2008, 18:449-461. 10.1101/gr.6943508, 2259109, 18230802.
44. Shimizu K, Toh H. Interaction between intrinsically disordered proteins frequently occurs in a human protein-protein interaction network. J Mol Biol 2009, 392:1253-1265. 10.1016/j.jmb.2009.07.088, 19660471.
45. King M, Wilson A. Evolution at two levels in humans and chimpanzees. Science 1975, 188:107-116. 10.1126/science.1090005, 1090005.
46. Hsia C, McGinnis W. Evolution of transcription factor function. Curr Opin Genet Dev 2003, 13:199-206. 10.1016/S0959-437X(03)00017-0, 12672498.
47. Tirosh I, Barkai N, Verstrepen KJ. Promoter architecture and the evolvability of gene expression. J Biol 2009, 8:95. 10.1186/jbiol204, 2804285, 20017897.
48. Choi JK, Kim YJ. Epigenetic regulation and the variability of gene expression. Nat Genet 2008, 40:141-147. 10.1038/ng.2007.58, 18227874.
49. Tirosh I, Reikhav S, Levy AA, Barkai N. A yeast hybrid provides insight into the evolution of gene expression regulation. Science 2009, 324:659-662. 10.1126/science.1169766, 19407207.
50. Wittkopp PJ, Haerum BK, Clark AG. Evolutionary changes in cis and trans gene regulation. Nature 2004, 430:85-88. 10.1038/nature02698, 15229602.
51. Lynch V, Wagner G. Resurrecting the role of transcription factor change in developmental evolution. Evolution 2008, 62:2131-2154. 10.1111/j.1558-5646.2008.00440.x, 18564379.
52. Liu J, Narayanan B, Oldfield C, Su E, Uversky V, Dunker A. Intrinsic disorder in transcription factors. Biochemistry 2006, 45:6873-6888. 10.1021/bi0602718, 2538555, 16734424.
53. McEwan IJ, Dahlman-Wright K, Ford J, Wright AP. Functional interaction of the c-Myc transactivation domain with the TATA binding protein: evidence for an induced fit model of transactivation domain folding. Biochemistry 1996, 35:9584-9593. 10.1021/bi960793v, 8755740.
54. Radhakrishnan I, Perez-Alvarado GC, Parker D, Dyson HJ, Montminy MR, Wright PE. Solution structure of the KIX domain of CBP bound to the transactivation domain of CREB: a model for activator:coactivator interactions. Cell 1997, 91:741-752. 10.1016/S0092-8674(00)80463-8, 9413984.
55. Ferreira ME, Hermann S, Prochasson P, Workman JL, Berndt KD, Wright AP. Mechanism of transcription factor recruitment by acidic activators. J Biol Chem 2005, 280:21779-21784. 10.1074/jbc.M502627200, 15826952.
56. Hermann S, Berndt KD, Wright AP. How transcriptional activators bind target proteins. J Biol Chem 2001, 276:40127-40132. 10.1074/jbc.M103793200, 11514548.
57. Sanger FTP. , ftp://ftp.sanger.ac.uk/pub/dmc/yeast
58. Saccharomyces Genome Database. , http://www.yeastgenome.org
59. Rice P, Longden I, Bleasby A. EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet 2000, 16:276-277. 10.1016/S0168-9525(00)02024-2, 10827456.
60. Subramanian A, Weyer-Menkhoff J, Kaufmann M, Morgenstern B. DIALIGN-T: an improved algorithm for segment-based multiple sequence alignment. BMC Bioinformatics 2005, 6:66. 10.1186/1471-2105-6-66, 1087830, 15784139.
61. Anisimova M, Nielsen R, Yang Z. Effect of recombination on the accuracy of the likelihood method for detecting positive selection at amino acid sites. Genetics 2003, 164:1229-1236. 1462615, 12871927.
62. Sawyer S. Statistical tests for detecting gene conversion. Mol Biol Evol 1989, 6:526-538.
63. Jones D. Protein secondary structure prediction based on position-specific scoring matrices. J Mol Biol 1999, 292:195-202. 10.1006/jmbi.1999.3091, 10493868.
64. Peng K, Radivojac P, Vucetic S, Dunker A, Obradovic Z. Length-dependent prediction of protein intrinsic disorder. BMC Bioinformatics 2006, 7:208. 10.1186/1471-2105-7-208, 1479845, 16618368.
65. Bordoli L, Kiefer F, Schwede T. Assessment of disorder predictions in CASP7. Proteins 2007, 69(Suppl 8):129-136.
66. Jones D, Taylor W, Thornton J. A model recognition approach to the prediction of all-helical membrane protein structure and topology. Biochemistry 1994, 33:3038-3049. 10.1021/bi00176a037, 8130217.
67. PFAM database. , ftp://ftp.sanger.ac.uk//pub/databases/Pfam//releases/Pfam25.0/pdbmap.gz
68. Pond S, Frost S, Muse S. HyPhy: hypothesis testing using phylogenies. Bioinformatics 2005, 21:676-679. 10.1093/bioinformatics/bti079, 15509596.
69. Tajima F, Nei M. Estimation of evolutionary distance between nucleotide sequences. Mol Biol Evol 1984, 1:269-285.
70. Hasegawa M, Kishino H, Yano T. Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 1985, 22:160-174. 10.1007/BF02101694, 3934395.
71. McDonald J, Kreitman M. Adaptive protein evolution at the Adh locus in Drosophila. Nature 1991, 351:652-654. 10.1038/351652a0, 1904993.
72. Thornton T. Libsequence: a C++ class library for evolutionary genetic analysis. Bioinformatics 2003, 19:2325-2327. 10.1093/bioinformatics/btg316, 14630667.
73. Kimura M. The Neutral Theory of Molecular Evolution 1983, Cambridge: Cambridge Univeristy Press.
74. Fay J, Wycoff G, Wu C-I. Positive and negative selection on the human genome. Genetics 2001, 158:1227-1234. 1461725, 11454770.
75. Charlesworth J, Eyre-Walker A. The McDonald-Kreitman test and slightly deleterious mutations. Mol Biol Evol 2008, 25:1007-1015. 10.1093/molbev/msn005, 18195052.
76. Chakrabarti S, Lanczycki C. Analysis and prediction of functionally important sites in proteins. Protein Sci 2007, 16:4-13. 10.1110/ps.062506407, 2222836, 17192586.
77. Lanczycki C, Chakrabarti S. A tool for the prediction of functionally important sites in proteins using a library of functional templates. Bioinformation 2008, 2:279-283. 2374371, 18478080.
78. Finn R, Tate J, Mistry J, Coggill P, Sammut S, Hotz H, Ceric G, Forslund K, Eddy S, Sonnhammer E, Bateman A. The Pfam protein families database. Nucleic Acids Res 2008, 36:D281-D288. 10.1093/nar/gkn226, 2238907, 18039703.