An experimentally determined evolutionary model dramatically improves phylogenetic fit

Molecular Biology and Evolution

Volumn 31, Issue 8, 2014, Pages 1956-1978

  Bloom, Jesse D ^a  

^a Fred Hutchinson Cancer Research Center   (United States)

Author keywords

codon model; deep mutational scanning; influenza; nucleoprotein; phylogenetics; substitution model

Indexed keywords

VIRUS NUCLEOPROTEIN; CODON; CORE PROTEIN;

AMINO ACID SUBSTITUTION; ARTICLE; CODON; GENETIC CONSERVATION; GENETIC MODEL; INDEL MUTATION; INFLUENZA VIRUS; MOLECULAR PHYLOGENY; MUTAGENESIS; MUTATION RATE; NONHUMAN; NUCLEOTIDE SEQUENCE; REPRODUCTIVE FITNESS; REVERSE TRANSCRIPTION; SINGLE NUCLEOTIDE POLYMORPHISM; STOP CODON; VIRION; VIRUS MUTANT; VIRUS MUTATION; ALGORITHM; BIOLOGICAL MODEL; GENETICS; HIGH THROUGHPUT SEQUENCING; METABOLISM; MOLECULAR EVOLUTION; MOLECULAR GENETICS; ORTHOMYXOVIRUS; PHYLOGENY;

ALGORITHMS; CODON; EVOLUTION, MOLECULAR; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; MUTATION RATE; ORTHOMYXOVIRIDAE; PHYLOGENY; VIRAL CORE PROTEINS;

EID: 84905001681     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msu173     Document Type: Article

References (74)

1. Araya CL, Fowler DM. 2011. Deep mutational scanning: Assessing protein function on a massive scale. Trends Biotechnol. 29:435-442
2. Ashenberg O, Gong LI, Bloom JD. 2013. Mutational effects on stability are largely conserved during protein evolution. Proc Natl Acad Sci U S A. 110:21071-21076
3. Bao Y, Bolotov P, Dernovoy D, Kiryutin B, Zaslavsky L, Tatusova T, Ostell J, Lipman D. 2008. The influenza virus resource at the National Center for Biotechnology Information. J Virol. 82:596-601
4. Bershtein S, Segal M, Bekerman R, Tokuriki N, Tawfik DS. 2006. Robustness-epistasis link shapes the fitness landscape of a randomly drifting protein. Nature 444:929-932
5. Bloom JD, Gong LI, Baltimore D. 2010. Permissive secondary mutations enable the evolution of influenza oseltamivir resistance. Science 328: 1272-1275
6. Bloom JD, Labthavikul ST, Otey CR, Arnold FH. 2006. Protein stability promotes evolvability. Proc Natl Acad Sci U S A. 103:5869-5874
7. Bloom JD, Raval A, Wilke CO. 2007. Thermodynamics of neutral protein evolution. Genetics 175:255-266
8. Bloom JD, Silberg JJ, Wilke CO, Drummond DA, Adami C, Arnold FH. 2005. Thermodynamic prediction of protein neutrality. Proc Natl Acad Sci U S A. 102:606-611
9. Cirino PC, Mayer KM, Umeno D. 2003. Directed evolution library creation: Methods and protocols Generating mutant libraries using error-prone PCR. Humana Press. p. 3-9
10. Crooks GE, Hon G, Chandonia JM, Brenner SE. 2004. Weblogo: A sequence logo generator. Genome Res. 14:1188-1190
11. Dang CC, Le QS, Gascuel O, Le VS. 2010. Flu, an amino acid substitution model for influenza proteins. BMC Evol Biol. 10:99
12. De Maio N, Holmes I, Schlötterer C, Kosiol C. 2013. Estimating empirical codon hidden Markov models. Mol Biol Evol. 30:725-736
13. Desai MM, Fisher DS. 2007. Beneficial mutation-selection balance and the effect of linkage on positive selection. Genetics 176:1759-1798
14. Felsenstein J. 1973. Maximum likelihood and minimum-step methods for estimating evolutionary trees from data on discrete characters. Syst Zool. 22:240-249
15. Felsenstein J. 1981. Evolutionary trees from DNA sequences: A maximum likelihood approach. J Mol Evol. 17:368-376
16. Firnberg E, Ostermeier M. 2012. PFunkel: Efficient, expansive, user-defined mutagenesis. PLoS One 7:e52031
17. Fowler DM, Araya CL, Fleishman SJ, Kellogg EH, Stephany JJ, Baker D, Fields S. 2010. High-resolution mapping of protein sequencefunction relationships. Nat Methods. 7:741-746
18. Gil M, Zanetti MS, Zoller S, Anisimova M. 2013. CodonPhyML: Fast maximum likelihood phylogeny estimation under codon substitution models. Mol Biol Evol. 30:1270-1280
19. Goldman N, Thorne JL, Jones DT. 1998. Assessing the impact of secondary structure and solvent accessibility on protein evolution. Genetics 149:445-458
20. Goldman N, Yang Z. 1994. A codon-based model of nucleotide substitution probabilities for protein-coding DNA sequences. Mol Biol Evol. 11:725-736
21. Gong LI, Suchard MA, Bloom JD. 2013. Stability-mediated epistasis constrains the evolution of an influenza protein. eLife 2:e00631
22. Goto H, Kawaoka Y. 1998. A novel mechanism for the acquisition of virulence by a human influenza a virus. Proc Natl Acad Sci U S A. 95: 10224-10228
23. Halligan DL, Keightley PD. 2009. Spontaneous mutation accumulation studies in evolutionary genetics. Annu Rev Ecol Evol Syst. 40:151-172
24. Halpern AL, Bruno WJ. 1998. Evolutionary distances for protein-coding sequences: Modeling site-specific residue frequencies. Mol Biol Evol. 15:910-917
25. Hiatt JB, Patwardhan RP, Turner EH, Lee C, Shendure J. 2010. Parallel, tagdirected assembly of locally derived short sequence reads. Nat Methods. 7:119-122
26. Hoffmann E, Neumann G, Kawaoka Y, Hobom G, Webster RG. 2000. A DNA transfection system for generation of influenza A virus from eight plasmids. Proc Natl Acad Sci U S A. 97:6108-6113
27. Hou Y, Zhang H, MiranDa L, Lin S. 2010. Serious overestimation in quantitative PCR by circular (supercoiled) plasmid standard: Microalgal pcna as the model gene. PLoS One 5:e9545
28. Huelsenbeck JP, Ronquist F, Nielsen R, Bollback JP. 2001. Bayesian inference of phylogeny and its impact on evolutionary biology. Science 294:2310-2314
29. Jain PC, Varadarajan R. 2014. A rapid, efficient, and economical inverse polymerase chain reaction-based method for generating a site saturation mutant library. Anal Biochem. 449:90-98
30. Joosten RP, Te Beek TA, Krieger E, Hekkelman ML, Hooft RW, Schneider R, Sander C, Vriend G. 2011. A series of PDB related databases for everyday needs. Nucleic Acids Res. 39:D411-D419
31. Kabsch W, Sander C. 1983. Dictionary of protein secondary structure: Pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22:2577-2637
32. Kleinman CL, Rodrigue N, Lartillot N, Philippe H. 2010. Statistical potentials for improved structurally constrained evolutionary models. Mol Biol Evol. 27:1546-1560
33. Kosiol C, Holmes I, Goldman N. 2007. An empirical codon model for protein sequence evolution. Mol Biol Evol. 24:1464-1479
34. Krasnitz M, Levine AJ, Rabadan R. 2008. Anomalies in the influenza virus genome database: New biology or laboratory errors? J Virology 82: 8947-8950
35. Lartillot N, Philippe H. 2004. A Bayesian mixture model for across-site heterogeneities in the amino-Acid replacement process. Mol Biol Evol. 21:1095-1109
36. Le SQ, Lartillot N, Gascuel O. 2008. Phylogenetic mixture models for proteins. Philos Trans R Soc B. 363:3965-3976
37. Lou DI, Hussmann JA, McBee RM, Acevedo A, Andino R, Press WH, Sawyer SL. 2013. High-Throughput DNA sequencing errors are reduced by orders of magnitude using circle sequencing. Proc Natl Acad Sci U S A. 110:19872-19877
38. Lunzer M, Golding GB, Dean AM. 2010. Pervasive cryptic epistasis in molecular evolution. PLoS Genet. 6:e1001162
39. Marsh GA, Rabadán R, Levine AJ, Palese P. 2008. Highly conserved regions of influenza a virus polymerase gene segments are critical for efficient viral RNA packaging. J Virology. 82:2295-2304
40. Melamed D, Young DL, Gamble CE, Miller CR, Fields S. 2013. Deep mutational scanning of an RRM domain of the Saccharomyces cerevisiae poly (a)-binding protein. RNA 19:1537-1551
41. Metropolis N, Rosenbluth AW, Rosenbluth MN, Teller AH, Teller E. 1953. Equation of state calculations by fast computing machines. J Chem Phys. 21:1087-1092
42. Neumann G, Watanabe T, Ito H, Watanabe S, Goto H, Gao P, Hughes M, Perez DR, Donis R, Hoffmann E, et al. 1999. Generation of influenza A viruses entirely from cloned cDNAs. Proc Natl Acad Sci U S A. 96: 9345-9350
43. Neylon C. 2004. Chemical and biochemical strategies for the randomization of protein encoding DNA sequences: Library construction methods for directed evolution. Nucleic Acids Res. 32:1448-1459
44. Ogliore R, Huss G, Nagashima K. 2011. Ratio estimation in SIMS analysis. Nucl Instr Meth Phys Res B. 269:1910-1918
45. Parvin J, Moscona A, Pan W, Leider J, Palese P. 1986. Measurement of the mutation rates of animal viruses: Influenza a virus and poliovirus type 1. J Virology. 59:377-383
46. Pearson K. 1910. On the constants of index-distributions as deduced from the like constants for the components of the ratio, with special reference to the opsonic index. Biometrika 7:531-541
47. Pond SK, Delport W, Muse SV, Scheffler K. 2010. Correcting the bias of empirical frequency parameter estimators in codon models. PLoS One 5:e11230
48. Pond SL, Frost SD, Muse SV. 2005. HyPhy: Hypothesis testing using phylogenies. Bioinformatics 21:676-679
49. Portela A, Digard P. 2002. The influenza virus nucleoprotein: A multifunctional RNA-binding protein pivotal to virus replication. J Gen Virol. 83:723-734
50. PosaDa D, Buckley TR. 2004. Model selection and model averaging in phylogenetics: Advantages of Akaike information criterion and Bayesian approaches over likelihood ratio tests. Syst Biol. 53:793-808
51. Potapov V, Cohen M, Schreiber G. 2009. Assessing computationalmethods for predicting protein stability upon mutation: Good on average but not in the details. Prot Eng Des Sel. 22:553-560
52. Rice P, Longden I, Bleasby A. 2000. Emboss: The European molecular biology open software suite. Trends Genet. 16:276-277
53. Rodrigue N. 2013. On the statistical interpretation of site-specific variables in phylogeny-based substitution models. Genetics 193:557-564
54. Rodrigue N, Kleinman CL, Philippe H, Lartillot N. 2009. Computational methods for evaluating phylogenetic models of coding sequence evolution with dependence between codons. Mol Biol Evol. 26: 1663-1676
55. Rodrigue N, Philippe H, Lartillot N. 2010. Mutation-selection models of coding sequence evolution with site-heterogeneous amino acid fitness profiles. Proc Natl Acad Sci U S A. 107:4629-4634
56. Roscoe BP, Thayer KM, Zeldovich KB, Fushman D, Bolon DN. 2013. Analyses of the effects of all ubiquitin point mutants on yeast growth rate. J Mol Biol. 425(8):1363-1377
57. Schmitt MW, Kennedy SR, Salk JJ, Fox EJ, Hiatt JB, Loeb LA. 2012. Detection of ultra-rare mutations by next-generation sequencing. Proc Natl Acad Sci U S A. 109:14508-14513
58. Schneider TD, Stephens RM. 1990. Sequence logos: A new way to display consensus sequences. Nucleic Acids Res. 18:6097-6100
59. Serrano L, Day AG, Fersht AR. 1993. Step-wise mutation of barnase to binase: A procedure for engineering increased stability of proteins and an experimental analysis of the evolution of protein stability. J Mol Biol. 233:305-312
60. Stamatakis A. 2006. Raxml-vi-hpc: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688-2690
61. Starita LM, PruneDa JN, Lo RS, Fowler DM, Kim HJ, Hiatt JB, Shendure J, Brzovic PS, Fields S, Klevit RE. 2013. Activity-enhancing mutations in an e3 ubiquitin ligase identified by high-Throughput mutagenesis. Proc Natl Acad Sci U S A. 110:E1263-E1272
62. Tamuri AU, dos Reis M, Goldstein RA. 2012. Estimating the distribution of selection coefficients from phylogenetic data using sitewise mutation-selection models. Genetics 190:1101-1115
63. Tamuri AU, Goldman N, Dos Reis M. 2014. A penalized likelihood method for estimating the distribution of selection coefficients from phylogenetic data. Genetics 197:257-271
64. Thorne JL, Choi SC, Yu J, Higgs PG, Kishino H. 2007. Population genetics without intraspecific data. Mol Biol Evol. 24:1667-1677
65. Thorne JL, Goldman N, Jones DT. 1996. Combining protein evolution and secondary structure. Mol Biol Evol. 13:666-673
66. Tien M, Meyer AG, Spielman SJ, Wilke CO. 2013. Maximum allowed solvent accessibilites of residues in proteins. PLoS One 8:e80635
67. Traxlmayr MW, Hasenhindl C, Hackl M, Stadlmayr G, Rybka JD, Borth N, Grillari J, Rüker F, Obinger C. 2012. Construction of a stability landscape of the CH3 domain of human igg1 by combining directed evolution with high throughput sequencing. JMol Biol. 423:397-412
68. Wang HC, Li K, Susko E, Roger AJ. 2008. A class frequencymixture model that adjusts for site-specific amino acid frequencies and improves inference of protein phylogeny. BMC Evol Biol. 8:331
69. Wu CH, Suchard MA, Drummond AJ. 2013. Bayesian selection of nucleotide substitution models and their site assignments. Mol Biol Evol. 30:669-688
70. Yang Z. 1994. Maximum likelihood phylogenetic estimation from DNA sequences with variable rates over sites: Approximate methods. J Mol Evol. 39:306-314
71. Yang Z, Nielsen R. 1998. Synonymous and nonsynonymous rate variation in nuclear genes of mammals. J Mol Evol. 46:409-418
72. Yang Z, Nielsen R, Goldman N, Pedersen AMK. 2000. Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 155:431-449
73. Yang Z, Wong WS, Nielsen R. 2005. Bayes empirical Bayes inference of amino acid sites under positive selection. Mol Biol Evol. 22: 1107-1118
74. Ye Q, Krug RM, Tao YJ. 2006. The mechanism by which influenza a virus nucleoprotein forms oligomers and binds RNA. Nature 444: 1078-1082.