Phenotypic heterogeneity promotes adaptive evolution

PLoS Biology

Volumn 15, Issue 5, 2017, Pages

  Bódi, Zoltán ^a   Farkas, Zoltán ^a   Nevozhay, Dmitry ^b,c   Kalapis, Dorottya ^a   Lázár, Viktória ^a   Csörgő, Bálint ^a   Nyerges, Ákos ^a   Szamecz, Béla ^a   Fekete, Gergely ^a   Papp, Balázs ^a   Araújo, Hugo ^d   Oliveira, José L ^d   Moura, Gabriela ^e   Santos, Manuel A S ^e   Székely Jr, Tamás ^f,g   Balázsi, Gábor ^b,f,g   Pál, Csaba ^a  

^a INSTITUTE OF BIOCHEMISTRY   (Hungary)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^c FAR EASTERN FEDERAL UNIVERSITY   (Russian Federation)

^d UNIVERSITY OF AVEIRO   (Portugal)

^e UNIVERSITY OF AVEIRO   (Portugal)

^f STONY BROOK UNIVERSITY   (United States)

^g St Francis Hospital The Heart Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CONTROLLED STUDY; ENVIRONMENTAL STRESS; EVOLUTIONARY ADAPTATION; GENE EXPRESSION; GENE MUTATION; GENETIC HETEROGENEITY; GENETIC VARIATION; GENOME ANALYSIS; GENOTYPE; MOLECULAR EVOLUTION; MUTATION RATE; NONHUMAN; PHENOTYPE; POSITIVE FEEDBACK; SACCHAROMYCES CEREVISIAE; SYNTHETIC BIOLOGY; ADAPTATION; ANTIFUNGAL RESISTANCE; EVOLUTION; FUNGAL GENE; GENETICS; MUTATION;

ADAPTATION, BIOLOGICAL; BIOLOGICAL EVOLUTION; DRUG RESISTANCE, FUNGAL; GENES, FUNGAL; MUTATION; PHENOTYPE; SACCHAROMYCES CEREVISIAE;

EID: 85020231053     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.2000644     Document Type: Article

References (63)

1. Jablonka E, Lamb MJ, Précis of Evolution in Four Dimensions. Behav Brain Sci. 2007;30: 353–365. doi: 10.1017/S0140525X07002221 18081952
2. Schlichting C, Pigliucci M, Phenotypic Evolution: A Reaction Norm Perspective. Sinauer; 1998.
3. West-Eberhard MJ, Developmental Plasticity and Evolution. OUPUSA; 2003.
4. Balázsi G, van Oudenaarden A, Collins JJ, Cellular Decision-Making and Biological Noise: From Microbes to Mammals. Cell. 2011;144: 910–925. doi: 10.1016/j.cell.2011.01.030 21414483
5. Tyedmers J, Madariaga ML, Lindquist S, Prion Switching in Response to Environmental Stress. PLoS Biol. 2008;6: e294. doi: 10.1371/journal.pbio.0060294 19067491
6. Levy SF, Ziv N, Siegal ML, Bet Hedging in Yeast by Heterogeneous, Age-Correlated Expression of a Stress Protectant. PLoS Biol. 2012;10: e1001325. doi: 10.1371/journal.pbio.1001325 22589700
7. Baldwin JM, A New Factor in Evolution. Am Nat. 1896;30: 441–451.
8. Hinton GE, Nowlan SJ, How learning can guide evolution. Complex Syst. 1987;1: 495–502.
9. Tawfik DS, Messy biology and the origins of evolutionary innovations. Nat Chem Biol. 2010;6: 692–696. doi: 10.1038/nchembio.441 20852602
10. Wagner A, The Origins of Evolutionary Innovations: A Theory of Transformative Change in Living Systems. OUPOxford; 2011.
11. Acar M, Mettetal JT, van Oudenaarden A, Stochastic switching as a survival strategy in fluctuating environments. Nat Genet. 2008;40: 471–475. doi: 10.1038/ng.110 18362885
12. Beaumont HJE, Gallie J, Kost C, Ferguson GC, Rainey PB, Experimental evolution of bet hedging. Nature. 2009;462: 90–93. doi: 10.1038/nature08504 19890329
13. Paenke I, Sendhoff B, Kawecki TJ, Influence of Plasticity and Learning on Evolution under Directional Selection. Am Nat. 2007;170: E47–E58. doi: 10.1086/518952 17874367
14. Price TD, Qvarnström A, Irwin DE, The role of phenotypic plasticity in driving genetic evolution. Proc R Soc Lond B Biol Sci. 2003;270: 1433–1440. doi: 10.1098/rspb.2003.2372
15. Ancel LW, Fontana W, Plasticity, evolvability, and modularity in RNA. J Exp Zool. 2000;288: 242–283. 11069142
16. Wang Z, Zhang J, Impact of gene expression noise on organismal fitness and the efficacy of natural selection. Proc Natl Acad Sci. 2011;108: E67–E76. doi: 10.1073/pnas.1100059108 21464323
17. Sato K, Ito Y, Yomo T, Kaneko K, On the relation between fluctuation and response in biological systems. Proc Natl Acad Sci. 2003;100: 14086–14090. doi: 10.1073/pnas.2334996100 14615583
18. Balaban NQ, Merrin J, Chait R, Kowalik L, Leibler S, Bacterial persistence as a phenotypic switch. Science. 2004;305: 1622–1625. doi: 10.1126/science.1099390 15308767
19. Frank SA, Rosner MR, Nonheritable Cellular Variability Accelerates the Evolutionary Processes of Cancer. PLoS Biol. 2012;10: e1001296. doi: 10.1371/journal.pbio.1001296 22509130
20. Ghalambor CK, Hoke KL, Ruell EW, Fischer EK, Reznick DN, Hughes KA, Non-adaptive plasticity potentiates rapid adaptive evolution of gene expression in. Nature. 2015;525: 372–375. doi: 10.1038/nature15256 26331546
21. Eldar A, Elowitz MB, Functional roles for noise in genetic circuits. Nature. 2010;467: 167–173. doi: 10.1038/nature09326 20829787
22. Nevozhay D, Adams RM, Van Itallie E, Bennett MR, Balázsi G, Mapping the environmental fitness landscape of a synthetic gene circuit. PLoS Comput Biol. 2012;8: e1002480. doi: 10.1371/journal.pcbi.1002480 22511863
23. Urlinger S, Baron U, Thellmann M, Hasan MT, Bujard H, Hillen W, Exploring the sequence space for tetracycline-dependent transcriptional activators: Novel mutations yield expanded range and sensitivity. Proc Natl Acad Sci U S A. 2000;97: 7963–7968. doi: 10.1073/pnas.130192197 10859354
24. Becskei A, Séraphin B, Serrano L, Positive feedback in eukaryotic gene networks: cell differentiation by graded to binary response conversion. EMBO J. 2001;20: 2528–2535. doi: 10.1093/emboj/20.10.2528 11350942
25. Anderson JB, Sirjusingh C, Parsons AB, Boone C, Wickens C, Cowen LE, et al. Mode of selection and experimental evolution of antifungal drug resistance in Saccharomyces cerevisiae. Genetics. 2003;163: 1287–1298. 12702675
26. Egner R, Mahé Y, Pandjaitan R, Kuchler K, Endocytosis and vacuolar degradation of the plasma membrane-localized Pdr5 ATP-binding cassette multidrug transporter in Saccharomyces cerevisiae. Mol Cell Biol. 1995;15: 5879–5887. 7565740
27. Blake WJ, Balázsi G, Kohanski MA, Isaacs FJ, Murphy KF, Kuang Y, et al. Phenotypic consequences of promoter-mediated transcriptional noise. Mol Cell. 2006;24: 853–865. doi: 10.1016/j.molcel.2006.11.003 17189188
28. Gonzalez C, Ray JCJ, Manhart M, Adams RM, Nevozhay D, Morozov AV, et al. Stress-response balance drives the evolution of a network module and its host genome. Mol Syst Biol. 2015;11: 827–827. doi: 10.15252/msb.20156185 26324468
29. Huang M-E, Rio A-G, Nicolas A, Kolodner RD, A genomewide screen in Saccharomyces cerevisiae for genes that suppress the accumulation of mutations. Proc Natl Acad Sci. 2003;100: 11529–11534. doi: 10.1073/pnas.2035018100 12972632
30. Serero A, Jubin C, Loeillet S, Legoix-Né P, Nicolas AG, Mutational landscape of yeast mutator strains. Proc Natl Acad Sci. 2014;111: 1897–1902. doi: 10.1073/pnas.1314423111 24449905
31. Taddei F, Radman M, Maynard-Smith J, Toupance B, Gouyon PH, Godelle B, Role of mutator alleles in adaptive evolution. Nature. 1997;387: 700–702. doi: 10.1038/42696 9192893
32. Frank SA, Natural selection. II. Developmental variability and evolutionary rate*. J Evol Biol. 2011;24: 2310–2320. doi: 10.1111/j.1420-9101.2011.02373.x 21939464
33. Belenky P, Camacho D, Collins JJ, Fungicidal Drugs Induce a Common Oxidative Damage Cellular Death Pathway. Cell Rep. 2013;3: 350–358. doi: 10.1016/j.celrep.2012.12.021 23416050
34. Ackermann M, A functional perspective on phenotypic heterogeneity in microorganisms. Nat Rev Microbiol. 2015;13: 497–508. doi: 10.1038/nrmicro3491 26145732
35. Levis NA, Pfennig DW, Evaluating “Plasticity-First” Evolution in Nature: Key Criteria and Empirical Approaches. Trends Ecol Evol. 2016;31: 563–574. doi: 10.1016/j.tree.2016.03.012 27067134
36. Holland SL, Reader T, Dyer PS, Avery SV, Phenotypic heterogeneity is a selected trait in natural yeast populations subject to environmental stress: Phenotypic heterogeneity is a selected trait. Environ Microbiol. 2014;16: 1729–1740. doi: 10.1111/1462-2920.12243 24000788
37. Price MN, Deutschbauer AM, Skerker JM, Wetmore KM, Ruths T, Mar JS, et al. Indirect and suboptimal control of gene expression is widespread in bacteria. Mol Syst Biol. 2013;9: 660. doi: 10.1038/msb.2013.16 23591776
38. Fischer E, Sauer U, Large-scale in vivo flux analysis shows rigidity and suboptimal performance of Bacillus subtilis metabolism. Nat Genet. 2005;37: 636–640. doi: 10.1038/ng1555 15880104
39. Ito Y, Toyota H, Kaneko K, Yomo T, How selection affects phenotypic fluctuation. Mol Syst Biol. 2009;5: 264. doi: 10.1038/msb.2009.23 19401676
40. Zhang Z, Qian W, Zhang J, Positive selection for elevated gene expression noise in yeast. Mol Syst Biol. 2009;5: 299. doi: 10.1038/msb.2009.58 19690568
41. Tokuriki N, Stricher F, Serrano L, Tawfik DS, How Protein Stability and New Functions Trade Off. PLoS Comput Biol. 2008;4: e1000002. doi: 10.1371/journal.pcbi.1000002 18463696
42. Huh W-K, Falvo JV, Gerke LC, Carroll AS, Howson RW, Weissman JS, et al. Global analysis of protein localization in budding yeast. Nature. 2003;425: 686–691. doi: 10.1038/nature02026 14562095
43. Gietz RD, Schiestl RH, High-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method. Nat Protoc. 2007;2: 31–34. doi: 10.1038/nprot.2007.13 17401334
44. Giaever G, Chu AM, Ni L, Connelly C, Riles L, Véronneau S, et al. Functional profiling of the Saccharomyces cerevisiae genome. Nature. 2002;418: 387–391. doi: 10.1038/nature00935 12140549
45. Tong AHY, Boone C, Synthetic genetic array analysis in Saccharomyces cerevisiae. Methods Mol Biol Clifton NJ. 2006;313: 171–192.
46. Suzuki S, Horinouchi T, Furusawa C, Prediction of antibiotic resistance by gene expression profiles. Nat Commun. 2014;5: 5792. doi: 10.1038/ncomms6792 25517437
47. Jung PP, Christian N, Kay DP, Skupin A, Linster CL, Protocols and Programs for High-Throughput Growth and Aging Phenotyping in Yeast. PLoS ONE. 2015;10. doi: 10.1371/journal.pone.0119807
48. Lundblad V, Struhl K, Yeast. Current Protocols in Molecular Biology. John Wiley & Sons, Inc.; 2008.
49. Foster PL, Methods for Determining Spontaneous Mutation Rates. Methods Enzymol. 2006;409: 195–213. doi: 10.1016/S0076-6879(05)09012-9 16793403
50. Lea DE, Coulson CA, The distribution of the numbers of mutants in bacterial populations. J Genet. 1949;49: 264–285. 24536673
51. Hall BM, Ma C-X, Liang P, Singh KK, Fluctuation AnaLysis CalculatOR: a web tool for the determination of mutation rate using Luria–Delbrück fluctuation analysis. Bioinformatics. 2009;25: 1564–1565. doi: 10.1093/bioinformatics/btp253 19369502
52. Wiegand I, Hilpert K, Hancock REW, Agar and broth dilution methods to determine the minimal inhibitory concentration (MIC) of antimicrobial substances. Nat Protoc. 2008;3: 163–175. doi: 10.1038/nprot.2007.521 18274517
53. Szamecz B, Boross G, Kalapis D, Kovács K, Fekete G, Farkas Z, et al. The Genomic Landscape of Compensatory Evolution. PLoS Biol. 2014;12: e1001935. doi: 10.1371/journal.pbio.1001935 25157590
54. Warringer J, Blomberg A, Automated screening in environmental arrays allows analysis of quantitative phenotypic profiles in Saccharomyces cerevisiae. Yeast Chichester Engl. 2003;20: 53–67. doi: 10.1002/yea.931
55. Warringer J, Ericson E, Fernandez L, Nerman O, Blomberg A, High-resolution yeast phenomics resolves different physiological features in the saline response. Proc Natl Acad Sci U S A. 2003;100: 15724–15729. doi: 10.1073/pnas.2435976100 14676322
56. Yu J-H, Hamari Z, Han K-H, Seo J-A, Reyes-Domínguez Y, Scazzocchio C, Double-joint PCR: a PCR-based molecular tool for gene manipulations in filamentous fungi. Fungal Genet Biol FG B. 2004;41: 973–981. doi: 10.1016/j.fgb.2004.08.001 15465386
57. Li H, Durbin R, Fast and accurate long-read alignment with Burrows–Wheeler transform. Bioinformatics. 2010;26: 589–595. doi: 10.1093/bioinformatics/btp698 20080505
58. McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 2010;20: 1297–1303. doi: 10.1101/gr.107524.110 20644199
59. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The Sequence Alignment/Map format and SAMtools. Bioinforma Oxf Engl. 2009;25: 2078–2079. doi: 10.1093/bioinformatics/btp352
60. Xie C, Tammi MT, CNV-seq, a new method to detect copy number variation using high-throughput sequencing. BMC Bioinformatics. 2009;10: 80. doi: 10.1186/1471-2105-10-80 19267900
61. Smit A, Hubley R, Green P. RepeatMasker Open-4.0. http://www.repeatmasker.org. 2013;
62. DiCarlo JE, Norville JE, Mali P, Rios X, Aach J, Church GM, Genome engineering in Saccharomyces cerevisiae using CRISPR-Cas systems. Nucleic Acids Res. 2013;41: 4336–4343. doi: 10.1093/nar/gkt135 23460208
63. Benatuil L, Perez JM, Belk J, Hsieh C-M, An improved yeast transformation method for the generation of very large human antibody libraries. Protein Eng Des Sel PEDS. 2010;23: 155–159. doi: 10.1093/protein/gzq002 20130105