The Valley-of-Death: Reciprocal sign epistasis constrains adaptive trajectories in a constant, nutrient limiting environment

Genomics

Volumn 104, Issue 6, 2014, Pages 431-437

  Chiotti, Kami E ^a   Kvitek, Daniel J ^b   Schmidt, Karen H ^a   Koniges, Gregory ^a   Schwartz, Katja ^b   Donckels, Elizabeth A ^b   Rosenzweig, Frank ^a   Sherlock, Gavin ^b  

^a UNIVERSITY OF MONTANA   (United States)

^b STANFORD UNIVERSITY   (United States)

Author keywords

Epistasis; Evolution; Genomics; Yeast

Indexed keywords

GLUCOSE; CULTURE MEDIUM; MTH1 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

ACE2 GENE; ADAPTIVE BEHAVIOR; ALLELE; ARTICLE; CONTROLLED STUDY; EPISTASIS; FUNGAL GENE; FUNGAL STRAIN; GENE AMPLIFICATION; GENE DOSAGE; GIN4 GENE; HXT6 GENE; HXT7 GENE; INDEL MUTATION; IRA2 GENE; LCB1 GENE; MISSENSE MUTATION; MIT1 GENE; MOLECULAR CLONING; MOLECULAR EVOLUTION; MTH1 GENE; MUK1 GENE; NONHUMAN; NONSENSE MUTATION; PBS2 GENE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RECIPROCAL SIGN EPISTASIS; REPRODUCTIVE FITNESS; SEQUENCE ANALYSIS; SINGLE NUCLEOTIDE POLYMORPHISM; WHOLE GENOME RESEQUENCING; ADAPTATION; CHEMISTRY; CULTURE MEDIUM; DIRECTED MOLECULAR EVOLUTION; GENETIC SELECTION; GENETICS; METABOLISM; MUTATION; SACCHAROMYCES CEREVISIAE;

ADAPTATION, BIOLOGICAL; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; CULTURE MEDIA; DIRECTED MOLECULAR EVOLUTION; EPISTASIS, GENETIC; EVOLUTION, MOLECULAR; GENE DOSAGE; GENETIC FITNESS; GLUCOSE; MUTATION; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SELECTION, GENETIC;

EID: 84941941076     PISSN: 08887543     EISSN: 10898646     Source Type: Journal    
DOI: 10.1016/j.ygeno.2014.10.011     Document Type: Article

References (63)

1. S.J. Gould, R.C. Lewontin, The spandrels of SanMarco and the Panglossian paradigm: a critique of the adaptationist programme, Containing papers of a biological character. Royal SocietyProc. R. Soc. Lond. Ser. B 205 (1979) 581-598.
2. R. Nielsen, Adaptionism-30 years after Gould and Lewontin, Evolution 63 (2009) 2487-2490.
3. S. Wright, The roles of mutation, inbreeding, crossbreeding and selection in evolution, Proceedings of the Sixth Congress on Genetics, Ithaca, New York, 1932, pp. 355-366.
4. S. Wright, Surfaces of selective value revisited, Am. Nat. 131 (1988) 115-123.
5. M.C. Whitlock, P.C. Phillips, F.B.G. Moore, S.J. Tonsor, Multiple fitness peaks and epistasis, Annu. Rev. Ecol. Syst. 26 (1995) 601-629.
6. D.M. Weinreich, N.F. Delaney, M.A. Depristo, D.L. Hartl, Darwinian evolution can follow only very few mutational paths to fitter proteins, Science 312 (2006) 111-114.
7. M.L. Salverda, E. Dellus, F.A. Gorter, A.J. Debets, J. van der Oost, R.F. Hoekstra, D.S. Tawfik, J.A. de Visser, Initial mutations direct alternative pathways of protein evolution, PLoS Genet. 7 (2011) e1001321.
8. I.S. Povolotskaya, F.A. Kondrashov, Sequence space and the ongoing expansion of the protein universe, Nature 465 (2010) 922-926.
9. D. Heckmann, S. Schulze, A. Denton, U. Gowik, P. Westhoff, A.P. Weber, M.J. Lercher, Predicting C4 photosynthesis evolution: modular, individually adaptive steps on a Mount Fuji fitness landscape, Cell 153 (2013) 1579-1588.
10. E.D. Brodie, Why evolutionary genetics does not always add up, in: J.B. Wolf, E.D. Brodie, M.J. Wade (Eds.), Epistasis and the Evolutionary Process, Oxford University Press, New York, 2000.
11. S. Gavrilets, Fitness Landscapes and the Origin of Species, Princeton University Press, 2004.
12. P.C. Phillips, Epistasis-the essential role of gene interactions in the structure and evolution of genetic systems, Nat. Rev. Genet. 9 (2008) 855-867.
13. F.J. Poelwijk, D.J. Kiviet, D.M. Weinreich, S.J. Tans, Empirical fitness landscapes reveal accessible evolutionary paths, Nature 445 (2007) 383-386.
14. M. Lunzer, S.P. Miller, R. Felsheim, A.M. Dean, The biochemical architecture of an ancient adaptive landscape, Science 310 (2005) 499-501.
15. G. Zhu, G.B. Golding, A.M. Dean, The selective cause of an ancient adaptation, Science 307 (2005) 1279-1282.
16. A. Dawid, D.J. Kiviet, M. Kogenaru, M. de Vos, S.J. Tans, Multiple peaks and reciprocal sign epistasis in an empirically determined genotype-phenotype landscape, Chaos 20 (2010) 026105.
17. H.H. Chou, H.C. Chiu, N.F. Delaney, D. Segre, C.J. Marx, Diminishing returns epistasis among beneficialmutations decelerates adaptation, Science 332 (2011) 1190-1192.
18. D.M. Weinreich, R.A. Watson, L. Chao, Perspective: sign epistasis and genetic constraint on evolutionary trajectories, Evolution 59 (2005) 1165-1174.
19. F.J. Poelwijk, S. Tanase-Nicola, D.J. Kiviet, S.J. Tans, Reciprocal sign epistasis is a necessary condition for multi-peaked fitness landscapes, J. Theor. Biol. 272 (2011) 141-144.
20. D.B. Weissman, M.M. Desai, D.S. Fisher, M.W. Feldman, The rate at which asexual populations cross fitness valleys, Theor. Popul. Biol. 75 (2009) 286-300.
21. E.R. Lozovsky, T. Chookajorn, K.M. Brown, M. Imwong, P.J. Shaw, S. Kamchonwongpaisan, D.E. Neafsey, D.M. Weinreich, D.L. Hartl, Stepwise acquisition of pyrimethamine resistance in the malaria parasite, Proc. Natl. Acad. Sci. U. S. A. 106 (2009) 12025-12030.
22. A. Wellner, M. Raitses Gurevich, D.S. Tawfik, Mechanisms of protein sequence divergence and incompatibility, PLoS Genet. 9 (2013) e1003665.
23. M. Lunzer, G.B. Golding, A.M. Dean, Pervasive cryptic epistasis in molecular evolution, PLoS Genet. 6 (2010) e1001162.
24. E.A. Ortlund, J.T. Bridgham, M.R. Redinbo, J.W. Thornton, Crystal structure of an ancient protein: evolution by conformational epistasis, Science 317 (2007) 1544-1548.
25. A.I. Khan, D.M. Dinh, D. Schneider, R.E. Lenski, T.F. Cooper, Negative epistasis between beneficial mutations in an evolving bacterial population, Science 332 (2011) 1193-1196.
26. T. Hinkley, J. Martins, C. Chappey, M. Haddad, E. Stawiski, J.M. Whitcomb, C.J. Petropoulos, S. Bonhoeffer, A systems analysis of mutational effects in HIV-1 protease and reverse transcriptase, Nat. Genet. 43 (2011) 487-489.
27. S. Trindade, A. Sousa, K.B. Xavier, F. Dionisio, M.G. Ferreira, I. Gordo, Positive epistasis drives the acquisition of multidrug resistance, PLoS Genet. 5 (2009) e1000578.
28. J.A. de Visser, S.C. Park, J. Krug, Exploring the effect of sex on empirical fitness landscapes, Am. Nat. 174 (Suppl. 1) (2009) S15-S30.
29. F.J. Poelwijk, D.J. Kiviet, S.J. Tans, Evolutionary potential of a duplicated repressor-operator pair: simulating pathways using mutation data, PLoS Comput. Biol. 2 (2006) e58.
30. J. da Silva, S.K. Wyatt, Fitness valleys constrain HIV-1's adaptation to its secondary chemokine coreceptor, J. Evol. Biol. 27 (2014) 604-615.
31. J. da Silva, M. Coetzer, R. Nedellec, C. Pastore, D.E. Mosier, Fitness epistasis and constraints on adaptation in a human immunodeficiency virus type 1 protein region, Genetics 185 (2010) 293-303.
32. J. Lalic, S.F. Elena, Magnitude and sign epistasis among deleterious mutations in a positive-sense plant RNA virus, Heredity 109 (2012) 71-77.
33. J. Yun, C. Rago, I. Cheong, R. Pagliarini, P. Angenendt, H. Rajagopalan, K. Schmidt, J.K. Willson, S. Markowitz, S. Zhou, L.A. Diaz Jr., V.E. Velculescu, C. Lengauer, K.W. Kinzler, B. Vogelstein, N. Papadopoulos, Glucose deprivation contributes to the development of KRAS pathway mutations in tumor cells, Science 325 (2009) 1555-1559.
34. B. Vogelstein, K.W. Kinzler, Cancer genes and the pathways they control, Nat. Med. 10 (2004) 789-799.
35. A. Stenzinger, V. Endris, N. Pfarr, M. Andrulis, K. Johrens, F. Klauschen, U. Siebolts, T. Wolf, P.S. Koch, M. Schulz, W. Hartschuh, S. Goerdt, J.K. Lennerz, C. Wickenhauser, W. Klapper, I. Anagnostopoulos, W. Weichert, Targeted ultra-deep sequencing reveals recurrent and mutually exclusive mutations of cancer genes in blastic plasmacytoid dendritic cell neoplasm, Oncotarget 5 (15) (2014) 6404-6413.
36. Z.S. Bao, H.M. Chen, M.Y. Yang, C.B. Zhang, K. Yu, W.L. Ye, B.Q. Hu, W. Yan, W. Zhang, J. Akers, V. Ramakrishnan, J. Li, B. Carter, Y.W. Liu, H.M. Hu, Z. Wang, M.Y. Li, K. Yao, X.G. Qiu, C.S. Kang, Y.P. You, X.L. Fan, W.S. Song, R.Q. Li, X.D. Su, C. Chen, T. Jiang, RNA-seq of 272 gliomas revealed a novel, recurrent PTPRZ1-MET fusion transcript in secondary glioblastomas, Genome Res. 24 (2014) 1765-1773.
37. A. Yoshizawa, S. Sumiyoshi, M. Sonobe, M. Kobayashi, T. Uehara, M. Fujimoto, T. Tsuruyama, H. Date, H. Haga, HER2 status in lung adenocarcinoma: a comparison of immunohistochemistry, fluorescence in situ hybridization (FISH), dual-ISH, and gene mutations, Lung Cancer 85 (3) (2014) 373-378.
38. K.M. Flynn, T.F. Cooper, F.B. Moore, V.S. Cooper, The environment affects epistatic interactions to alter the topology of an empirical fitness landscape, PLoS Genet. 9 (2013) e1003426.
39. D. Moradigaravand, R. Kouyos, T. Hinkley, M. Haddad, C.J. Petropoulos, J. Engelstadter, S. Bonhoeffer, Recombination accelerates adaptation on a large-scale empirical fitness landscape in HIV-1, PLoS Genet. 10 (2014) e1004439.
40. M.F. Schenk, I.G. Szendro, M.L. Salverda, J. Krug, J.A. de Visser, Patterns of epistasis between beneficial mutations in an antibiotic resistance gene, Mol. Biol. Evol. 30 (2013) 1779-1787.
41. D.J. Kvitek, G. Sherlock, Reciprocal sign epistasis between frequently experimentally evolved adaptive mutations causes a rugged fitness landscape, PLoS Genet. 7 (2011) e1002056.
42. C.J. Brown, K.M. Todd, R.F. Rosenzweig, Multiple duplications of yeast hexose transport genes in response to selection in a glucose-limited environment, Mol. Biol. Evol. 15 (1998) 931-942.
43. D. Gresham, M.M. Desai, C.M. Tucker, H.T. Jenq, D.A. Pai, A. Ward, C.G. DeSevo, D. Botstein, M.J. Dunham, The repertoire and dynamics of evolutionary adaptations to controlled nutrient-limited environments in yeast, PLoS Genet. 4 (2008) e1000303.
44. K.C. Kao, G. Sherlock, Molecular characterization of clonal interference during adaptive evolution in asexual populations of Saccharomyces cerevisiae, Nat. Genet. 40 (2008) 1499-1504.
45. C. Verduyn, E. Postma, W.A. Scheffers, J.P. Van Dijken, Effect of benzoic acid on metabolic fluxes in yeasts: a continuous-culture study on the regulation of respiration and alcoholic fermentation, Yeast 8 (1992) 501-517.
46. D.J. Kvitek, G. Sherlock, Whole genome, whole population sequencing reveals that loss of signaling networks is themajor adaptive strategy in a constant environment, PLoS Genet. 9 (2013) e1003972.
47. G.I. Lang, D.P. Rice, M.J. Hickman, E. Sodergren, G.M. Weinstock, D. Botstein, M.M. Desai, Pervasive genetic hitchhiking and clonal interference in forty evolving yeast populations, Nature 500 (2013) 571-574.
48. S. Kryazhimskiy, D.P. Rice, E.R. Jerison, M.M. Desai, Microbial evolution. Global epistasis makes adaptation predictable despite sequence-level stochasticity, Science 344 (2014) 1519-1522.
49. J.W. Wenger, J. Piotrowski, S. Nagarajan, K. Chiotti, G. Sherlock, F. Rosenzweig, Hunger artists: yeast adapted to carbon limitation show trade-offs under carbon sufficiency, PLoS Genet. 7 (2011) e1002202.
50. J.I. Roop, R.B. Brem, Rare variants in hypermutable genes underlie common morphology and growth traits in wild Saccharomyces paradoxus, Genetics 195 (2013) 513-525.
51. B. Oud, V. Guadalupe-Medina, J.F. Nijkamp, D. de Ridder, J.T. Pronk, A.J. van Maris, J.M. Daran, Genome duplication and mutations in ACE2 cause multicellular, fastsedimenting phenotypes in evolved Saccharomyces cerevisiae, Proc. Natl. Acad. Sci. U. S. A. 110 (2013) E4223-E4231.
52. A.L. Paulsel, A.J. Merz, D.P. Nickerson, Vps9 family protein Muk1 is the second Rab5 guanosine nucleotide exchange factor in budding yeast, J. Biol. Chem. 288 (2013) 18162-18171.
53. M. Cabrera, H. Arlt, N. Epp, J. Lachmann, J. Griffith, A. Perz, F. Reggiori, C. Ungermann, Functional separation of endosomal fusion factors and the class C core vacuole/endosome tethering (CORVET) complex in endosome biogenesis, J. Biol. Chem. 288 (2013) 5166-5175.
54. D. Mayhew, R.D. Mitra, Transcription factor regulation and chromosome dynamics during pseudohyphal growth, Mol. Biol. Cell 25 (2014) 2669-2676.
55. D.E. Dykhuizen, A.M. Dean, Experimental evolution from the bottom up, in: T. Garland Jr., M.R. Rose (Eds.), Experimental Evolution: Concepts, Methods, and Applications of Selection Experiments, University of California Press, 2009, pp. 67-87.
56. T.L. Ferea, D. Botstein, P.O. Brown, R.F. Rosenzweig, Systematic changes in gene expression patterns following adaptive evolution in yeast, Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 9721-9726.
57. A. Roy, D. Jouandot 2nd, K.H. Cho, J.H. Kim, Understanding the mechanism of glucose-induced relief of Rgt1-mediated repression in yeast, FEBS open bio 4 (2014) 105-111.
58. K.M. Flick, N. Spielewoy, T.I. Kalashnikova, M. Guaderrama, Q. Zhu, H.C. Chang, C. Wittenberg, Grr1-dependent inactivation of Mth1 mediates glucose-induced dissociation of Rgt1 fromHXT gene promoters, Mol. Biol. Cell 14 (2003) 3230-3241.
59. F. Winston, C. Dollard, S.L. Ricupero-Hovasse, Construction of a set of convenient Saccharomyces cerevisiae strains that are isogenic to S288C, Yeast 11 (1995) 53-55.
60. M. Martin, Cutadapt removes adapter sequences from high-throughput sequencing reads, EMBnet J. 17 (2011) 10-12.
61. H. Li, R. Durbin, Fast and accurate short read alignment with Burrows-Wheeler transform, Bioinformatics 25 (2009) 1754-1760.
62. M.A. DePristo, E. Banks, R. Poplin, K.V. Garimella, J.R. Maguire, C. Hartl, A.A. Philippakis, G. del Angel, M.A. Rivas, M. Hanna, A. McKenna, T.J. Fennell, A.M. Kernytsky, A.Y. Sivachenko, K. Cibulskis, S.B. Gabriel, D. Altshuler, M.J. Daly, A framework for variation discovery and genotyping using next-generation DNA sequencing data, Nat. Genet. 43 (2011) 491-498.
63. A. McKenna, M. Hanna, E. Banks, A. Sivachenko, K. Cibulskis, A. Kernytsky, K. Garimella, D. Altshuler, S. Gabriel, M. Daly, M.A. DePristo, The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data, Genome Res. 20 (2010) 1297-1303.