Dynamic Large-Scale Chromosomal Rearrangements Fuel Rapid Adaptation in Yeast Populations

English version České info

Large-scale genome rearrangements have been observed in cells adapting to various selective conditions during laboratory evolution experiments. However, it remains unclear whether these types of mutations can be stably maintained in populations and how they impact the evolutionary trajectories. Here we show that chromosomal rearrangements contribute to extremely high copper tolerance in a set of natural yeast strains isolated from Evolution Canyon (EC), Israel. The chromosomal rearrangements in EC strains result in segmental duplications in chromosomes 7 and 8, which increase the copy number of genes involved in copper regulation, including the crucial transcriptional activator CUP2 and the metallothionein CUP1. The copy number of CUP2 is correlated with the level of copper tolerance, indicating that increasing dosages of a single transcriptional activator by chromosomal rearrangements has a profound effect on a regulatory pathway. By gene expression analysis and functional assays, we identified three previously unknown downstream targets of CUP2: PHO84, SCM4, and CIN2, all of which contributed to copper tolerance in EC strains. Finally, we conducted an evolution experiment to examine how cells maintained these changes in a fluctuating environment. Interestingly, the rearranged chromosomes were reverted back to the wild-type configuration at a high frequency and the recovered chromosome became fixed in less selective conditions. Our results suggest that transposon-mediated chromosomal rearrangements can be highly dynamic and can serve as a reversible mechanism during early stages of adaptive evolution.

Vyšlo v časopise: Dynamic Large-Scale Chromosomal Rearrangements Fuel Rapid Adaptation in Yeast Populations. PLoS Genet 9(1): e32767. doi:10.1371/journal.pgen.1003232
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003232

Souhrn

Zdroje

1. NadeauNJ, JigginsCD (2010) A golden age for evolutionary genetics? Genomic studies of adaptation in natural populations. Trends Genet 26: 484–492.

2. CowenLE (2008) The evolution of fungal drug resistance: modulating the trajectory from genotype to phenotype. Nat Rev Microbiol 6: 187–198.

3. KimHS, FayJC (2007) Genetic variation in the cysteine biosynthesis pathway causes sensitivity to pharmacological compounds. Proc Natl Acad Sci U S A 104: 19387–19391.

4. WillJL, KimHS, ClarkeJ, PainterJC, FayJC, et al. (2010) Incipient balancing selection through adaptive loss of aquaporins in natural Saccharomyces cerevisiae populations. PLoS Genet 6: e1000893 doi:10.1371/journal.pgen.1000893.

5. ZeylC (2004) Capturing the adaptive mutation in yeast. Res Microbiol 155: 217–223.

6. GerkeJ, LorenzK, CohenB (2009) Genetic interactions between transcription factors cause natural variation in yeast. Science 323: 498–501.

7. FidalgoM, BarralesRR, IbeasJI, JimenezJ (2006) Adaptive evolution by mutations in the FLO11 gene. Proc Natl Acad Sci U S A 103: 11228–11233.

8. AdamsJ, Puskas-RozsaS, SimlarJ, WilkeCM (1992) Adaptation and major chromosomal changes in populations of Saccharomyces cerevisiae. Curr Genet 22: 13–19.

9. PerepnikhatkaV, FischerFJ, NiimiM, BakerRA, CannonRD, et al. (1999) Specific chromosome alterations in fluconazole-resistant mutants of Candida albicans. J Bacteriol 181: 4041–4049.

10. KoszulR, CaburetS, DujonB, FischerG (2004) Eucaryotic genome evolution through the spontaneous duplication of large chromosomal segments. Embo J 23: 234–243.

11. RancatiG, PavelkaN, FlehartyB, NollA, TrimbleR, et al. (2008) Aneuploidy underlies rapid adaptive evolution of yeast cells deprived of a conserved cytokinesis motor. Cell 135: 879–893.

12. GreshamD, UsaiteR, GermannSM, LisbyM, BotsteinD, et al. (2010) Adaptation to diverse nitrogen-limited environments by deletion or extrachromosomal element formation of the GAP1 locus. Proc Natl Acad Sci U S A 107: 18551–18556.

13. DharR, SagesserR, WeikertC, YuanJ, WagnerA (2011) Adaptation of Saccharomyces cerevisiae to saline stress through laboratory evolution. J Evol Biol 24: 1135–1153.

14. DunhamMJ, BadraneH, FereaT, AdamsJ, BrownPO, et al. (2002) Characteristic genome rearrangements in experimental evolution of Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 99: 16144–16149.

15. GreshamD, DesaiMM, TuckerCM, JenqHT, PaiDA, et al. (2008) The repertoire and dynamics of evolutionary adaptations to controlled nutrient-limited environments in yeast. PLoS Genet 4: e1000303 doi:10.1371/journal.pgen.1000303.

16. Perez-OrtinJE, QuerolA, PuigS, BarrioE (2002) Molecular characterization of a chromosomal rearrangement involved in the adaptive evolution of yeast strains. Genome Res 12: 1533–1539.

17. SelmeckiA, ForcheA, BermanJ (2006) Aneuploidy and isochromosome formation in drug-resistant Candida albicans. Science 313: 367–370.

18. SelmeckiA, Gerami-NejadM, PaulsonC, ForcheA, BermanJ (2008) An isochromosome confers drug resistance in vivo by amplification of two genes, ERG11 and TAC1. Mol Microbiol 68: 624–641.

19. PolakovaS, BlumeC, ZarateJA, MentelM, Jorck-RambergD, et al. (2009) Formation of new chromosomes as a virulence mechanism in yeast Candida glabrata. Proc Natl Acad Sci U S A 106: 2688–2693.

20. ArguesoJL, CarazzolleMF, MieczkowskiPA, DuarteFM, NettoOV, et al. (2009) Genome structure of a Saccharomyces cerevisiae strain widely used in bioethanol production. Genome Res 19: 2258–2270.

21. LynchM, SungW, MorrisK, CoffeyN, LandryCR, et al. (2008) A genome-wide view of the spectrum of spontaneous mutations in yeast. Proc Natl Acad Sci U S A 105: 9272–9277.

22. NishantKT, WeiW, ManceraE, ArguesoJL, SchlattlA, et al. (2010) The baker's yeast diploid genome is remarkably stable in vegetative growth and meiosis. PLoS Genet 6: e1001109 doi:10.1371/journal.pgen.1001109.

23. Eyre-WalkerA, WoolfitM, PhelpsT (2006) The distribution of fitness effects of new deleterious amino acid mutations in humans. Genetics 173: 891–900.

24. SelmeckiAM, DulmageK, CowenLE, AndersonJB, BermanJ (2009) Acquisition of aneuploidy provides increased fitness during the evolution of antifungal drug resistance. PLoS Genet 5: e1000705 doi:10.1371/journal.pgen.1000705.

25. GarfinkelDJ (2005) Genome evolution mediated by Ty elements in Saccharomyces. Cytogenet Genome Res 110: 63–69.

26. LitiG, CarterDM, MosesAM, WarringerJ, PartsL, et al. (2009) Population genomics of domestic and wild yeasts. Nature 458: 337–341.

27. ChaRS, KlecknerN (2002) ATR homolog Mec1 promotes fork progression, thus averting breaks in replication slow zones. Science 297: 602–606.

28. LemoineFJ, DegtyarevaNP, LobachevK, PetesTD (2005) Chromosomal translocations in yeast induced by low levels of DNA polymerase a model for chromosome fragile sites. Cell 120: 587–598.

29. LobachevKS, GordeninDA, ResnickMA (2002) The Mre11 complex is required for repair of hairpin-capped double-strand breaks and prevention of chromosome rearrangements. Cell 108: 183–193.

30. MieczkowskiPA, LemoineFJ, PetesTD (2006) Recombination between retrotransposons as a source of chromosome rearrangements in the yeast Saccharomyces cerevisiae. DNA Repair (Amst) 5: 1010–1020.

31. RachidiN, BarreP, BlondinB (1999) Multiple Ty-mediated chromosomal translocations lead to karyotype changes in a wine strain of Saccharomyces cerevisiae. Mol Gen Genet 261: 841–850.

32. CasaregolaS, NguyenHV, LepingleA, BrignonP, GendreF, et al. (1998) A family of laboratory strains of Saccharomyces cerevisiae carry rearrangements involving chromosomes I and III. Yeast 14: 551–564.

33. UmezuK, HiraokaM, MoriM, MakiH (2002) Structural analysis of aberrant chromosomes that occur spontaneously in diploid Saccharomyces cerevisiae: retrotransposon Ty1 plays a crucial role in chromosomal rearrangements. Genetics 160: 97–110.

34. NevoE (1995) Asian, African and European Biota Meet at Evolution-Canyon Israel - Local Tests of Global Biodiversity and Genetic Diversity Patterns. Proceedings of the Royal Society of London Series B-Biological Sciences 262: 149–155.

35. NevoE (1997) Evolution in action across phylogeny caused by microclimatic stresses at “Evolution Canyon”. Theor Popul Biol 52: 231–243.

36. NevoE (2001) Evolution of genome-phenome diversity under environmental stress. Proc Natl Acad Sci U S A 98: 6233–6240.

37. LidzbarskyGA, ShkolnikT, NevoE (2009) Adaptive response to DNA-damaging agents in natural Saccharomyces cerevisiae populations from “Evolution Canyon”, Mt. Carmel, Israel. PLoS ONE 4: e5914 doi:10.1371/journal.pone.0005914.

38. ChangSL, LeuJY (2011) A tradeoff drives the evolution of reduced metal resistance in natural populations of yeast. PLoS Genet 7: e1002034 doi:10.1371/journal.pgen.1002034.

39. WelchJW, FogelS, CathalaG, KarinM (1983) Industrial yeasts display tandem gene iteration at the CUP1 region. Mol Cell Biol 3: 1353–1361.

40. WelchJ, FogelS, BuchmanC, KarinM (1989) The CUP2 gene product regulates the expression of the CUP1 gene, coding for yeast metallothionein. Embo J 8: 255–260.

41. MiyazakiS, NevoE, BohnertHJ (2005) Adaptive oxidative stress in yeast Saccharomyces cerevisiae: interslope genetic divergence in ‘Evolution Canyon’. Biol J Linn Soc 84: 103–117.

42. Katz EzovT, ChangSL, FrenkelZ, SegreAV, BahalulM, et al. (2010) Heterothallism in Saccharomyces cerevisiae isolates from nature: effect of HO locus on the mode of reproduction. Mol Ecol 19: 121–131.

43. EzovTK, Boger-NadjarE, FrenkelZ, KatsperovskiI, KemenyS, et al. (2006) Molecular-genetic biodiversity in a natural population of the yeast Saccharomyces cerevisiae from “Evolution Canyon”: microsatellite polymorphism, ploidy and controversial sexual status. Genetics 174: 1455–1468.

44. KaoKC, SherlockG (2008) Molecular characterization of clonal interference during adaptive evolution in asexual populations of Saccharomyces cerevisiae. Nat Genet 40: 1499–1504.

45. BuchmanC, SkrochP, WelchJ, FogelS, KarinM (1989) The CUP2 gene product, regulator of yeast metallothionein expression, is a copper-activated DNA-binding protein. Mol Cell Biol 9: 4091–4095.

46. JensenLT, HowardWR, StrainJJ, WingeDR, CulottaVC (1996) Enhanced effectiveness of copper ion buffering by CUP1 metallothionein compared with CRS5 metallothionein in Saccharomyces cerevisiae. J Biol Chem 271: 18514–18519.

47. GrallaEB, ThieleDJ, SilarP, ValentineJS (1991) ACE1, a copper-dependent transcription factor, activates expression of the yeast copper, zinc superoxide dismutase gene. Proc Natl Acad Sci U S A 88: 8558–8562.

48. KellisM, PattersonN, EndrizziM, BirrenB, LanderES (2003) Sequencing and comparison of yeast species to identify genes and regulatory elements. Nature 423: 241–254.

49. KoszulR, DujonB, FischerG (2006) Stability of large segmental duplications in the yeast genome. Genetics 172: 2211–2222.

50. TorresEM, SokolskyT, TuckerCM, ChanLY, BoselliM, et al. (2007) Effects of aneuploidy on cellular physiology and cell division in haploid yeast. Science 317: 916–924.

51. FereaTL, BotsteinD, BrownPO, RosenzweigRF (1999) Systematic changes in gene expression patterns following adaptive evolution in yeast. Proc Natl Acad Sci U S A 96: 9721–9726.

52. KvitekDJ, WillJL, GaschAP (2008) Variations in stress sensitivity and genomic expression in diverse S. cerevisiae isolates. PLoS Genet 4: e1000223 doi:10.1371/journal.pgen.1000223.

53. BruinsMR, KapilS, OehmeFW (2000) Microbial resistance to metals in the environment. Ecotoxicol Environ Saf 45: 198–207.

54. De FreitasJ, WintzH, KimJH, PoyntonH, FoxT, et al. (2003) Yeast, a model organism for iron and copper metabolism studies. Biometals 16: 185–197.

55. HaferburgG, KotheE (2007) Microbes and metals: interactions in the environment. J Basic Microbiol 47: 453–467.

56. Emsley J (2001) Nature's building blocks: An A-Z guide to the elemets. Oxford: Oxford University Press.

57. BesnardE, ChenuC, RobertM (2001) Influence of organic amendments on copper distribution among particle-size and density fractions in Champagne vineyard soils. Environ Pollut 112: 329–337.

58. MortimerRK (2000) Evolution and variation of the yeast (Saccharomyces) genome. Genome Res 10: 403–409.

59. AdamoGM, LottiM, TamasMJ, BroccaS (2012) Amplification of the CUP1 gene is associated with evolution of copper tolerance in Saccharomyces cerevisiae. Microbiology 158: 2325–2335.

60. FogelS, WelchJW (1982) Tandem gene amplification mediates copper resistance in yeast. Proc Natl Acad Sci U S A 79: 5342–5346.

61. WarringerJ, ZorgoE, CubillosFA, ZiaA, GjuvslandA, et al. (2011) Trait variation in yeast is defined by population history. PLoS Genet 7: e1002111 doi:10.1371/journal.pgen.1002111.

62. HoytMA, StearnsT, BotsteinD (1990) Chromosome instability mutants of Saccharomyces cerevisiae that are defective in microtubule-mediated processes. Mol Cell Biol 10: 223–234.

63. PanX, ReissmanS, DouglasNR, HuangZ, YuanDS, et al. (2010) Trivalent arsenic inhibits the functions of chaperonin complex. Genetics 186: 725–734.

64. SmithSA, KumarP, JohnstonI, RosamondJ (1992) SCM4, a gene that suppresses mutant cdc4 function in budding yeast. Mol Gen Genet 235: 285–291.

65. Bun-YaM, NishimuraM, HarashimaS, OshimaY (1991) The PHO84 gene of Saccharomyces cerevisiae encodes an inorganic phosphate transporter. Mol Cell Biol 11: 3229–3238.

66. JensenLT, Ajua-AlemanjiM, CulottaVC (2003) The Saccharomyces cerevisiae high affinity phosphate transporter encoded by PHO84 also functions in manganese homeostasis. J Biol Chem 278: 42036–42040.

67. KabirMA, AhmadA, GreenbergJR, WangYK, RustchenkoE (2005) Loss and gain of chromosome 5 controls growth of Candida albicans on sorbose due to dispersed redundant negative regulators. Proc Natl Acad Sci U S A 102: 12147–12152.

68. PavelkaN, RancatiG, ZhuJ, BradfordWD, SarafA, et al. (2010) Aneuploidy confers quantitative proteome changes and phenotypic variation in budding yeast. Nature 468: 321–325.

69. FischerG, JamesSA, RobertsIN, OliverSG, LouisEJ (2000) Chromosomal evolution in Saccharomyces. Nature 405: 451–454.

70. AguileraA (2002) The connection between transcription and genomic instability. Embo J 21: 195–201.

71. MorillonA, SpringerM, LesageP (2000) Activation of the Kss1 invasive-filamentous growth pathway induces Ty1 transcription and retrotransposition in Saccharomyces cerevisiae. Mol Cell Biol 20: 5766–5776.

72. ServantG, PennetierC, LesageP (2008) Remodeling yeast gene transcription by activating the Ty1 long terminal repeat retrotransposon under severe adenine deficiency. Mol Cell Biol 28: 5543–5554.

73. ItoH, FukudaY, MurataK, KimuraA (1983) Transformation of intact yeast cells treated with alkali cations. J Bacteriol 153: 163–168.

74. Guthrie C, Fink G (2004) Guide to yeast genetics and molecular and cell biology. San Diego: Elsevier Academic Press.

75. LieuPT, JozsiP, GillesP, PetersonT (2005) Development of a DNA-labeling system for array-based comparative genomic hybridization. J Biomol Tech 16: 104–111.

76. RobinsonMD, GrigullJ, MohammadN, HughesTR (2002) FunSpec: a web-based cluster interpreter for yeast. BMC Bioinformatics 3: 35.