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Environmental Dependence of Genetic Constraint


The epistatic interactions that underlie evolutionary constraint have mainly been studied for constant external conditions. However, environmental changes may modulate epistasis and hence affect genetic constraints. Here we investigate genetic constraints in the adaptive evolution of a novel regulatory function in variable environments, using the lac repressor, LacI, as a model system. We have systematically reconstructed mutational trajectories from wild type LacI to three different variants that each exhibit an inverse response to the inducing ligand IPTG, and analyzed the higher-order interactions between genetic and environmental changes. We find epistasis to depend strongly on the environment. As a result, mutational steps essential to inversion but inaccessible by positive selection in one environment, become accessible in another. We present a graphical method to analyze the observed complex higher-order interactions between multiple mutations and environmental change, and show how the interactions can be explained by a combination of mutational effects on allostery and thermodynamic stability. This dependency of genetic constraint on the environment should fundamentally affect evolutionary dynamics and affects the interpretation of phylogenetic data.


Vyšlo v časopise: Environmental Dependence of Genetic Constraint. PLoS Genet 9(6): e32767. doi:10.1371/journal.pgen.1003580
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003580

Souhrn

The epistatic interactions that underlie evolutionary constraint have mainly been studied for constant external conditions. However, environmental changes may modulate epistasis and hence affect genetic constraints. Here we investigate genetic constraints in the adaptive evolution of a novel regulatory function in variable environments, using the lac repressor, LacI, as a model system. We have systematically reconstructed mutational trajectories from wild type LacI to three different variants that each exhibit an inverse response to the inducing ligand IPTG, and analyzed the higher-order interactions between genetic and environmental changes. We find epistasis to depend strongly on the environment. As a result, mutational steps essential to inversion but inaccessible by positive selection in one environment, become accessible in another. We present a graphical method to analyze the observed complex higher-order interactions between multiple mutations and environmental change, and show how the interactions can be explained by a combination of mutational effects on allostery and thermodynamic stability. This dependency of genetic constraint on the environment should fundamentally affect evolutionary dynamics and affects the interpretation of phylogenetic data.


Zdroje

1. WrightS (1932) The roles of mutation, inbreeding, crossbreeding and selection in evolution. In: Proceedings of the Sixth International Congress of Genetics 1: 356–366.

2. LunzerM, MillerSP, FelsheimR, DeanAM (2005) The biochemical architecture of an ancient adaptive landscape. Science 310: 499–501.

3. WeinreichDM, DelaneyNF, DepristoMA, HartlDL (2006) Darwinian evolution can follow only very few mutational paths to fitter proteins. Science 312: 111–114.

4. PoelwijkFJ, KivietDJ, WeinreichDM, TansSJ (2007) Empirical fitness landscapes reveal accessible evolutionary paths. Nature 445: 383–386.

5. BridghamJT, CarrollSM, ThorntonJW (2006) Evolution of hormone-receptor complexity by molecular exploitation. Science 312: 97–101.

6. WeinreichDM (2005) The rank ordering of genotypic fitness values predicts genetic constraint on natural selection on landscapes lacking sign epistasis. Genetics 171: 1397–1405.

7. KvitekDJ, SherlockG (2011) Reciprocal Sign Epistasis between Frequently Experimentally Evolved Adaptive Mutations Causes a Rugged Fitness Landscape. PLoS Genet 7: e1002056.

8. de VisserJA, ParkSC, KrugJ (2009) Exploring the effect of sex on empirical fitness landscapes. Am Nat 174(Suppl 1): S15–30.

9. PoelwijkFJ, Tanase-NicolaS, KivietDJ, TansSJ (2011) Reciprocal sign epistasis is a necessary condition for multi-peaked fitness landscapes. J Theor Biol 272: 141–144.

10. BreenMS, KemenaC, VlasovPK, NotredameC, KondrashovFA (2012) Epistasis as the primary factor in molecular evolution. Nature 490: 535–538.

11. SchluterD, ConteGL (2009) Genetics and ecological speciation. Proc Natl Acad Sci U S A 106(Suppl 1): 9955–9962.

12. ViaS (2002) The ecological genetics of speciation. Am Nat 159(Suppl 3): S1–7.

13. WadeMJ, GoodnightCJ (1998) Genetics and adaptation in metapopulations: When nature does many small experiments. Evolution 52: 1537–1553.

14. OrtlundEA, BridghamJT, RedinboMR, ThorntonJW (2007) Crystal structure of an ancient protein: evolution by conformational epistasis. Science 317: 1544–1548.

15. MillerSP, LunzerM, DeanAM (2006) Direct demonstration of an adaptive constraint. Science 314: 458–461.

16. DeWitt TJ, Scheiner SM (2004) Phenotypic plasticity. Functional and conceptual approaches. Oxford: Oxford University Press.

17. Pigliucci M (2001) Phenotypic plasticity. Beyond nature and nurture. Scheiner SM, editor. Baltimore and London: The Johns Hopkins University Press.

18. KubinakJL, RuffJS, HyzerCW, SlevPR, PottsWK (2012) Experimental viral evolution to specific host MHC genotypes reveals fitness and virulence trade-offs in alternative MHC types. Proc Natl Acad Sci U S A 109: 3422–3427.

19. BataillonT, ZhangT, KassenR (2011) Cost of Adaptation and Fitness Effects of Beneficial Mutations in Pseudomonas fluorescens. Genetics 189(3): 939–49.

20. RemoldS (2012) Understanding specialism when the Jack of all trades can be the master of all. Proc Biol Sci 279: 4861–4869.

21. RemoldSK, LenskiRE (2004) Pervasive joint influence of epistasis and plasticity on mutational effects in Escherichia coli. Nat Genet 36: 423–426.

22. BohannanBJM, TravisanoM, LenskiRE (1999) Epistatic interactions can lower the cost of resistance to multiple consumers. Evolution 53: 292–295.

23. LalicJ, ElenaSF Epistasis between mutations is host-dependent for an RNA virus. Biol Lett

24. TanL, SereneS, ChaoHX, GoreJ (2011) Hidden randomness between fitness landscapes limits reverse evolution. Phys Rev Lett 106: 198102.

25. LindseyHA, GallieJ, TaylorS, KerrB (2013) Evolutionary rescue from extinction is contingent on a lower rate of environmental change. Nature 494: 463–467.

26. HallAR, IlesJC, MacLeanRC (2011) The fitness cost of rifampicin resistance in Pseudomonas aeruginosa depends on demand for RNA polymerase. Genetics 187: 817–822.

27. JacobF, MonodJ (1961) Genetic regulatory mechanisms in the synthesis of proteins. J Mol Biol 3: 318–356.

28. Poelwijk FrankJ, de Vos MarjonGJ, Tans SanderJ (2011) Tradeoffs and Optimality in the Evolution of Gene Regulation. Cell 146: 462–470.

29. GillespieJH (1984) Molecular evolution over the mutational landscape. Evolution 38: 1116–1129.

30. WhitlockMC, PhillipsPC, MooreFBG, TonsorSJ (1995) Multiple Fitness Peaks and Epistasis. Annu Rev Ecol Syst 26: 601–629.

31. DawidA, KivietDJ, KogenaruM, de VosM, TansSJ (2010) Multiple peaks and reciprocal sign epistasis in an empirically determined genotype-phenotype landscape. Chaos 20: 026105.

32. LewisM, SochorM, DaberR (2011) Allostery via an Order-Disorder Transition. Comment to Cell (2011) 146: 462–470 School of Medicine University of Pennsylvania.

33. FlynnTC, Swint-KruseL, KongY, BoothC, MatthewsKS, et al. (2003) Allosteric transition pathways in the lactose repressor protein core domains: asymmetric motions in a homodimer. Protein Sci 12: 2523–2541.

34. LewisM, ChangG, HortonNC, KercherMA, PaceHC, et al. (1996) Crystal structure of teh Lactose Operon Repressor and Its Complexes with DNA and Inducer. Science 271: 1247–1254.

35. ZhanH, CamargoM, MatthewsKS Positions 94–98 of the lactose repressor N-subdomain monomer-monomer interface are critical for allosteric communication. Biochemistry 49: 8636–8645.

36. WylieCS, ShakhnovichEI (2011) A biophysical protein folding model accounts for most mutational fitness effects in viruses. Proc Natl Acad Sci U S A 108: 9916–9921.

37. TokurikiN, StricherF, SerranoL, TawfikDS (2008) How protein stability and new functions trade off. PLoS Comput Biol 4: e1000002.

38. ChenP, ShakhnovichEI (2009) Lethal mutagenesis in viruses and bacteria. Genetics 183: 639–650.

39. GueroisR, NielsenJE, SerranoL (2002) Predicting changes in the stability of proteins and protein complexes: a study of more than 1000 mutations. J Mol Biol 320: 369–387.

40. Van DurmeJ, DelgadoJ, StricherF, SerranoL, SchymkowitzJ, et al. (2011) A graphical interface for the FoldX forcefield. Bioinformatics 27: 1711–1712.

41. SuiterAM, BanzigerO, DeanAM (2003) Fitness consequences of a regulatory polymorphism in a seasonal environment. Proc Natl Acad Sci U S A 100: 12782–12786.

42. JessupCM, BohannanBJ (2008) The shape of an ecological trade-off varies with environment. Ecol Lett 11: 947–959.

43. HawthorneDJ, ViaS (2001) Genetic linkage of ecological specialization and reproductive isolation in pea aphids. Nature 412: 904–907.

44. WoodsR, SchneiderD, WinkworthCL, RileyMA, LenskiRE (2006) Tests of parallel molecular evolution in a long-term experiment with Escherichia coli. Proc Natl Acad Sci U S A 103: 9107–9112.

45. RaineyPB, TravisanoM (1998) Adaptive radiation in a heterogeneous environment. Nature 394: 69–72.

46. TravisanoM, MongoldJA, BennettAF, LenskiRE (1995) Experimental tests of the roles of adaptation, chance, and history in evolution. Science 267: 87–90.

47. KashtanN, NoorE, AlonU (2007) Varying environments can speed up evolution. Proc Natl Acad Sci U S A 104: 13711–13716.

48. TanL, GoreJ (2012) Slowly switching between environments facilitates reverse evolution in small populations. Evolution 66: 3144–3154.

49. KolaczkowskiB, ThorntonJW (2008) A mixed branch length model of heterotachy improves phylogenetic accuracy. Mol Biol Evol 25: 1054–1066.

50. LopezP, CasaneD, PhilippeH (2002) Heterotachy, an important process in protein evolution. Mol Biol Evol 19: 1–7.

51. LunzerM, GoldingGB, DeanAM (2010) Pervasive cryptic epistasis in molecular evolution. PLoS Genet 6: e1001162.

52. KolaczkowskiB, ThorntonJW (2004) Performance of maximum parsimony and likelihood phylogenetics when evolution is heterogeneous. Nature 431: 980–984.

53. KolaczkowskiB, ThorntonJW (2009) Long-branch attraction bias and inconsistency in Bayesian phylogenetics. PLoS One 4: e7891.

54. StefankovicD, VigodaE (2007) Pitfalls of heterogeneous processes for phylogenetic reconstruction. Syst Biol 56: 113–124.

55. KucharskiA, GogJR (2012) Influenza emergence in the face of evolutionary constraints. Proc Biol Sci 279: 645–652.

56. HerfstS, SchrauwenEJ, LinsterM, ChutinimitkulS, de WitE, et al. (2012) Airborne transmission of influenza A/H5N1 virus between ferrets. Science 336: 1534–1541.

57. Gould SJ (1989) Wonderful Life: The Burgess Shale and the Nature of History. New York: W.W. Norton & Company.

58. CasadabanMJ, CohenSN (1980) Analysis of gene control signals by DNA fusion and cloning in Escherichia coli. J Mol Biol 138: 179–207.

59. LutzR, BujardH (1997) Independent and tight regulation of transcriptional units in Escherichia coli via the LacR/O, the TetR/O and AraC/I1-I2 regulatory elements. Nucleic Acids Res 25: 1203–1210.

60. AmannE, OchsB, AbelKJ (1988) Tightly regulated tac promoter vectors useful for the expression of unfused and fused proteins in Escherichia coli. Gene 69: 301–315.

61. BlattnerFR, PlunkettG3rd, BlochCA, PernaNT, BurlandV, et al. (1997) The complete genome sequence of Escherichia coli K-12. Science 277: 1453–1462.

62. KriegerE, KoraimannG, VriendG (2002) Increasing the precision of comparative models with YASARA NOVA–a self-parameterizing force field. Proteins 47: 393–402.

63. BellCE, LewisM (2000) A closer view of the conformation of the Lac repressor bound to operator. Nat Struct Biol 7: 209–214.

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Genetika Reprodukčná medicína

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PLOS Genetics


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