Recurrent Rearrangement during Adaptive Evolution in an Interspecific Yeast Hybrid Suggests a Model for Rapid Introgression

English version České info

Genome rearrangements are associated with eukaryotic evolutionary processes ranging from tumorigenesis to speciation. Rearrangements are especially common following interspecific hybridization, and some of these could be expected to have strong selective value. To test this expectation we created de novo interspecific yeast hybrids between two diverged but largely syntenic Saccharomyces species, S. cerevisiae and S. uvarum, then experimentally evolved them under continuous ammonium limitation. We discovered that a characteristic interspecific genome rearrangement arose multiple times in independently evolved populations. We uncovered nine different breakpoints, all occurring in a narrow ∼1-kb region of chromosome 14, and all producing an “interspecific fusion junction” within the MEP2 gene coding sequence, such that the 5′ portion derives from S. cerevisiae and the 3′ portion derives from S. uvarum. In most cases the rearrangements altered both chromosomes, resulting in what can be considered to be an introgression of a several-kb region of S. uvarum into an otherwise intact S. cerevisiae chromosome 14, while the homeologous S. uvarum chromosome 14 experienced an interspecific reciprocal translocation at the same breakpoint within MEP2, yielding a chimaeric chromosome; these events result in the presence in the cell of two MEP2 fusion genes having identical breakpoints. Given that MEP2 encodes for a high-affinity ammonium permease, that MEP2 fusion genes arise repeatedly under ammonium-limitation, and that three independent evolved isolates carrying MEP2 fusion genes are each more fit than their common ancestor, the novel MEP2 fusion genes are very likely adaptive under ammonium limitation. Our results suggest that, when homoploid hybrids form, the admixture of two genomes enables swift and otherwise unavailable evolutionary innovations. Furthermore, the architecture of the MEP2 rearrangement suggests a model for rapid introgression, a phenomenon seen in numerous eukaryotic phyla, that does not require repeated backcrossing to one of the parental species.

Vyšlo v časopise: Recurrent Rearrangement during Adaptive Evolution in an Interspecific Yeast Hybrid Suggests a Model for Rapid Introgression. PLoS Genet 9(3): e32767. doi:10.1371/journal.pgen.1003366
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003366

Souhrn

Zdroje

1. GreavesM, MaleyCC (2012) Clonal evolution in cancer. Nature 481: 306–313 doi:10.1038/nature10762.

2. PodlahaO, RiesterM, DeS, MichorF (2012) Evolution of the cancer genome. Trends Genet 28: 155–163 doi:10.1016/j.tig.2012.01.003.

3. GrossBL, RiesebergLH (2005) The ecological genetics of homoploid hybrid speciation. Journal of Heredity 96: 241–252 doi:10.1093/jhered/esi026.

4. GreigD, LouisEJ, BortsRH, TravisanoM (2002) Hybrid speciation in experimental populations of yeast. Science (New York, NY) 298: 1773–1775 doi:10.1126/science.1076374.

5. HiraiH, TaguchiT, SaitohY, KawanakaM, SugiyamaH, et al. (2000) Chromosomal differentiation of the Schistosoma japonicum complex. Int J Parasitol 30: 441–452.

6. MavarezJ, LinaresM (2008) Homoploid hybrid speciation in animals. Mol Ecol 17: 4181–4185 doi:10.1111/j.1365-294X.2008.03898.x.

7. MavarezJ, SalazarCA, BerminghamE, SalcedoC, JigginsCD, et al. (2006) Speciation by hybridization in Heliconius butterflies. Nat Cell Biol 441: 868–871 doi:10.1038/nature04738.

8. de Barros LopesM, BellonJR, ShirleyNJ, GanterPF (2002) Evidence for multiple interspecific hybridization in Saccharomyces sensu stricto species. FEMS Yeast Research 1: 323–331.

9. LitiG, PeruffoA, JamesSA, RobertsIN, LouisEJ (2005) Inferences of evolutionary relationships from a population survey of LTR-retrotransposons and telomeric-associated sequences in the Saccharomyces sensu stricto complex. Yeast 22: 177–192 doi:10.1002/yea.1200.

10. QuerolA, BondU (2009) The complex and dynamic genomes of industrial yeasts. FEMS Microbiology Letters 293: 1–10 doi:10.1111/j.1574-6968.2008.01480.x.

11. LitiG, BartonDBH, LouisEJ (2006) Sequence diversity, reproductive isolation and species concepts in Saccharomyces. Genetics 174: 839–850 doi:10.1534/genetics.106.062166.

12. GreigD (2008) Reproductive isolation in Saccharomyces. Heredity (Edinb) 102: 39–44 doi:10.1038/hdy.2008.73.

13. MacleanCJ, GreigD (2011) Reciprocal gene loss following experimental whole-genome duplication causes reproductive isolation in yeast. Evolution 65: 932–945 doi:10.1111/j.1558-5646.2010.01171.x.

14. AndersonE, HubrichtL (1938) Hybridization in Tradescantia. III. The evidence for introgressive hybridization. American Journal of Botany 25: 396–402.

15. DowlingTE, SecorCL (1997) The role of hybridization and introgression in the diversificataion of animals. Annu Rev Ecol Syst 28: 593–619.

16. DowlingTE, DeMaraisBD (1993) Evolutionary significance of introgressive hybridization in cyprinid fishes. Nature 362: 444–446.

17. MalletJ (2005) Hybridization as an invasion of the genome. Trends in Ecology & Evolution 20: 229–237 doi:10.1016/j.tree.2005.02.010.

18. ZhangH, SkeltonA, GardnerRC, GoddardMR (2010) Saccharomyces paradoxus and Saccharomyces cerevisiae reside on oak trees in New Zealand: evidence for migration from Europe and interspecies hybrids. FEMS Yeast Research 10: 941–947 doi:10.1111/j.1567-1364.2010.00681.x.

19. WeiW, McCuskerJH, HymanRW, JonesT, NingY, et al. (2007) Genome sequencing and comparative analysis of Saccharomyces cerevisiae strain YJM789. Proc Natl Acad Sci USA 104: 12825–12830 doi:10.1073/pnas.0701291104.

20. MullerLAH, McCuskerJH (2009) A multispecies-based taxonomic microarray reveals interspecies hybridization and introgression in Saccharomyces cerevisiae. FEMS Yeast Research 9: 143–152 doi:10.1111/j.1567-1364.2008.00464.x.

21. UsherJ, BondU (2009) Recombination between homoeologous chromosomes of lager yeasts leads to loss of function of the hybrid GPH1 gene. Appl Environ Microbiol 75: 4573–4579 doi:10.1128/AEM.00351-09.

22. DonigerSW, KimHS, SwainD, CorcueraD, WilliamsM, et al. (2008) A catalog of neutral and deleterious polymorphism in yeast. PLoS Genet 4: e1000183 doi:10.1371/journal.pgen.1000183.

23. EsbergA, MullerLAH, McCuskerJH (2011) Genomic structure of and genome-wide recombination in the Saccharomyces cerevisiae S288C progenitor isolate EM93. PLoS ONE 6: e25211 doi:10.1371/journal.pone.0025211.

24. DequinS, CasaregolaS (2011) The genomes of fermentative Saccharomyces. C R Biol 334: 687–693 doi:10.1016/j.crvi.2011.05.019.

25. NaumovaES, NaumovGI, (null), (null), Masneuf-PomarèdeI (2011) Genetic diversity study of the yeast Saccharomyces bayanus var. uvarum reveals introgressed subtelomeric Saccharomyces cerevisiae genes. Research in Microbiology 162: 204–213 doi:10.1016/j.resmic.2010.09.023.

26. RoncoroniM, SantiagoM, HooksDO, MoroneyS, HarschMJ, et al. (2011) The yeast IRC7 gene encodes a β-lyase responsible for production of the varietal thiol 4-mercapto-4-methylpentan-2-one in wine. Food Microbiology 28: 926–935 doi:10.1016/j.fm.2011.01.002.

27. ErnyC, RaoultP, AlaisA, ButterlinG, DelobelP, et al. (2012) Ecological success of a group of Saccharomyces cerevisiae/Saccharomyces kudriavzevii hybrids in the Northern European wine making environment. Appl Environ Microbiol doi:10.1128/AEM.06752-11.

28. DunnB, RichterC, KvitekDJ, PughT, SherlockG (2012) Analysis of the Saccharomyces cerevisiae pan-genome reveals a pool of copy number variants distributed in diverse yeast strains from differing industrial environments. Genome Res 22: 908–924 doi:10.1101/gr.130310.111.

29. DujonB (2010) Yeast evolutionary genomics. Nature Reviews Genetics 11: 512–524 doi:10.1038/nrg2811.

30. SalzburgerW, BaricS, SturmbauerC (2002) Speciation via introgressive hybridization in East African cichlids? Mol Ecol 11: 619–625.

31. VershininAV, AllnuttTR, KnoxMR, AmbroseMJ, EllisTHN (2003) Transposable elements reveal the impact of introgression, rather than transposition, in Pisum diversity, evolution, and domestication. Molecular Biology and Evolution 20: 2067–2075 doi:10.1093/molbev/msg220.

32. RiesebergLH, ArcherMA, WayneRK (1999) Transgressive segregation, adaptation and speciation. Heredity (Edinb) 83: 363–372.

33. TwyfordAD, EnnosRA (2012) Next-generation hybridization and introgression. Heredity (Edinb) 108: 179–189 doi:10.1038/hdy.2011.68.

34. McClintockB (1983) The significance of responses of the genome to challenge. Nobel lecture 1–20.

35. WaghmareSK, BruschiCV (2005) Differential chromosome control of ploidy in the yeast Saccharomyces cerevisiae. Yeast 22: 625–639 doi:10.1002/yea.1226.

36. ZeylC, VanderfordT, CarterM (2003) An evolutionary advantage of haploidy in large yeast populations. Science (New York, NY) 299: 555–558 doi:10.1126/science.1078417.

37. KellisM, PattersonN, EndrizziM, BirrenB, LanderES (2003) Sequencing and comparison of yeast species to identify genes and regulatory elements. Nature 423: 241–254 doi:10.1038/nature01644.

38. BrownCA, MurrayAW, VerstrepenKJ (2010) Rapid expansion and functional divergence of subtelomeric gene families in yeasts. Curr Biol 20: 895–903 doi:10.1016/j.cub.2010.04.027.

39. VitousekPM, HowarthRW (1991) Nitrogen limitation on land and in the sea: How can it occur? Biogeochemistry 13: 87–115.

40. GoddardMR, BradfordMA (2003) The adaptive response of a natural microbial population to carbon- and nitrogen-limitation. Ecology Letters 6: 594–598.

41. ColemanMC, FishR, BlockDE (2007) Temperature-dependent kinetic model for nitrogen-limited wine fermentations. Appl Environ Microbiol 73: 5875–5884 doi:10.1128/AEM.00670-07.

42. PiotrowskiJS, NagarajanS, KrollE, StanberyA, ChiottiKE, et al. (2012) Different selective pressures lead to different genomic outcomes as newly-formed hybrid yeasts evolve. BMC Evolutionary Biology 12: 46 doi:10.1186/1471-2148-12-46.

43. 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 USA 107: 18551–18556 doi:10.1073/pnas.1014023107.

44. WengerJW, PiotrowskiJ, NagarajanS, ChiottiK, SherlockG, et al. (2011) Hunger artists: yeast adapted to carbon limitation show trade-offs under carbon sufficiency. PLoS Genet 7: e1002202 doi:10.1371/journal.pgen.1002202.

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

46. KobayashiT, HeckDJ, NomuraM, HoriuchiT (1998) Expansion and contraction of ribosomal DNA repeats in Saccharomyces cerevisiae: requirement of replication fork blocking (Fob1) protein and the role of RNA polymerase I. Genes Dev 12: 3821–3830.

47. MariniAM, VissersS, UrrestarazuA, AndréB (1994) Cloning and expression of the MEP1 gene encoding an ammonium transporter in Saccharomyces cerevisiae. EMBO J 13: 3456–3463.

48. BoeckstaensM, AndréB, MariniAM (2007) The yeast ammonium transport protein Mep2 and its positive regulator, the Npr1 kinase, play an important role in normal and pseudohyphal growth on various nitrogen media through retrieval of excreted ammonium. Mol Microbiol 64: 534–546 doi:10.1111/j.1365-2958.2007.05681.x.

49. FritschES, SchachererJ, Bleykasten-GrosshansC, SoucietJ-L, PotierS, et al. (2009) Influence of genetic background on the occurrence of chromosomal rearrangements in Saccharomyces cerevisiae. BMC Genomics 10: 99 doi:10.1186/1471-2164-10-99.

50. PutnamCD, PennaneachV, KolodnerRD (2005) Saccharomyces cerevisiae as a model system to define the chromosomal instability phenotype. Mol Cell Biol 25: 7226–7238 doi:10.1128/MCB.25.16.7226-7238.2005.

51. VernonM, LobachevK, PetesTD (2008) High rates of “unselected” aneuploidy and chromosome rearrangements in tel1 mec1 haploid yeast strains. Genetics 179: 237–247 doi:10.1534/genetics.107.086603.

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

53. DunhamMJ, BadraneH, FereaT, AdamsJ, BrownPO, et al. (2002) Characteristic genome rearrangements in experimental evolution of Saccharomyces cerevisiae. Proc Natl Acad Sci USA 99: 16144–16149 doi:10.1073/pnas.242624799.

54. CoyleS, KrollE (2008) Starvation induces genomic rearrangements and starvation-resilient phenotypes in yeast. Molecular Biology and Evolution 25: 310–318 doi:10.1093/molbev/msm256.

55. QuerolA, Fernández-EspinarMT, del OlmoM-L, BarrioE (2003) Adaptive evolution of wine yeast. Int J Food Microbiol 86: 3–10.

56. StambukBU, DunnB, AlvesSL, DuvalEH, SherlockG (2009) Industrial fuel ethanol yeasts contain adaptive copy number changes in genes involved in vitamin B1 and B6 biosynthesis. Genome Res 19: 2271–2278 doi:10.1101/gr.094276.109.

57. MartínezC, GacS, LavinA, GangaM (2004) Genomic characterization of Saccharomyces cerevisiae strains isolated from wine-producing areas in South America. J Appl Microbiol 96: 1161–1168 doi:10.1111/j.1365-2672.2004.02255.x.

58. LucenaBTL, Silva-FilhoEA, CoimbraMRM, MoraisJOF, SimõesDA, et al. (2007) Chromosome instability in industrial strains of Saccharomyces cerevisiae batch cultivated under laboratory conditions. Genet Mol Res 6: 1072–1084.

59. LitiG, CarterDM, MosesAM, WarringerJ, PartsL, et al. (2009) Population genomics of domestic and wild yeasts. Nature 458: 337–341 doi:10.1038/nature07743.

60. GonzálezSS, BarrioE, GafnerJ, QuerolA (2006) Natural hybrids from Saccharomyces cerevisiae, Saccharomyces bayanus and Saccharomyces kudriavzevii in wine fermentations. FEMS Yeast Research 6: 1221–1234 doi:10.1111/j.1567-1364.2006.00126.x.

61. GonzálezSS, BarrioE, QuerolA (2008) Molecular characterization of new natural hybrids of Saccharomyces cerevisiae and S. kudriavzevii in brewing. Appl Environ Microbiol 74: 2314–2320 doi:10.1128/AEM.01867-07.

62. DunnB, SherlockG (2008) Reconstruction of the genome origins and evolution of the hybrid lager yeast Saccharomyces pastorianus. Genome Res 18: 1610–1623 doi:10.1101/gr.076075.108.

63. BellochC, Pérez-TorradoR, GonzálezSS, Pérez-OrtínJE, García-MartínezJ, et al. (2009) Chimeric genomes of natural hybrids of Saccharomyces cerevisiae and Saccharomyces kudriavzevii. Appl Environ Microbiol 75: 2534–2544 doi:10.1128/AEM.02282-08.

64. LouisVL, DesponsL, FriedrichA, MartinT, DurrensP, et al. (2012) Pichia sorbitophila, an Interspecies Yeast Hybrid, Reveals Early Steps of Genome Resolution After Polyploidization. G3 (Bethesda) 2: 299–311 doi:10.1534/g3.111.000745/-/DC1.

65. 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.

66. KaessmannH (2010) Origins, evolution, and phenotypic impact of new genes. Genome Res 20: 1313–1326 doi:10.1101/gr.101386.109.

67. RogersRL, BedfordT, LyonsAM, HartlDL (2010) Adaptive impact of the chimeric gene Quetzalcoatl in Drosophila melanogaster. Proc Natl Acad Sci USA 107: 10943–10948 doi:10.1073/pnas.1006503107.

68. CrameriA, RaillardSA, BermudezE, StemmerWP (1998) DNA shuffling of a family of genes from diverse species accelerates directed evolution. Nature 391: 288–291 doi:10.1038/34663.

69. MitelmanF, JohanssonB, MertensF (2007) The impact of translocations and gene fusions on cancer causation. Nat Rev Cancer 7: 233–245 doi:10.1038/nrc2091.

70. Kubitschek HE (1970) Introduction to research with continuous cultures. Englewood Cliffs, NJ: Prentice Hall. 1 pp.

71. Monod J (1958) Recherches sur la croissance des cultures bacteriennes. Paris: Hermann & cie. 1 pp.

72. KaoKC, SherlockG (2008) Molecular characterization of clonal interference during adaptive evolution in asexual populations of Saccharomyces cerevisiae. Nat Genet 40: 1499–1504 doi:10.1038/ng.280.

73. MariniA-M, Soussi-BoudekouS, VissersS, AndréB (1997) A Family of Ammonium Transporters in Saccharomyces cerevisiae. Mol Cell Biol 17: 4282–4293.

74. RutherfordJC, ChuaG, HughesT, CardenasME, HeitmanJ (2008) A Mep2-dependent transcriptional profile links permease function to gene expression during pseudohyphal growth in Saccharomyces cerevisiae. Mol Biol Cell 19: 3028–3039 doi:10.1091/mbc.E08-01-0033.

75. MariniAM, SpringaelJY, FrommerWB, AndréB (2000) Cross-talk between ammonium transporters in yeast and interference by the soybean SAT1 protein. Mol Microbiol 35: 378–385.

76. SzostakJW, Orr-WeaverTL, RothsteinRJ, StahlFW (1983) The double-strand-break repair model for recombination. Cell 33: 25–35.

77. BernsteinKA, RothsteinR (2009) At loose ends: Resecting a double-strand break. Cell 137: 807–810 doi:10.1016/j.cell.2009.05.007.

78. LlorenteB, SmithCE, SymingtonLS (2008) Break-induced replication: what is it and what is it for? Cell cycle (Georgetown, Tex) 7: 859–864.

79. HaberJE (1999) DNA recombination: the replication connection. Trends Biochem Sci 24: 271–275.

80. LaRocqueJR, StarkJM, OhJ, BojilovaE, YusaK, et al. (2011) Interhomolog recombination and loss of heterozygosity in wild-type and Bloom syndrome helicase (BLM)-deficient mammalian cells. Proc Natl Acad Sci USA 108: 11971–11976 doi:10.1073/pnas.1104421108.

81. SmithCE, LlorenteB, SymingtonLS (2007) Template switching during break-induced replication. Nature 447: 102–105 doi:10.1038/nature05723.

82. KeelingPJ, PalmerJD (2008) Horizontal gene transfer in eukaryotic evolution. Nature Reviews Genetics 9: 605–618 doi:10.1038/nrg2386.

83. GaleoteV, BigeyF, BeyneE, NovoM, LegrasJ-L, et al. (2011) Amplification of a Zygosaccharomyces bailii DNA Segment in Wine Yeast Genomes by Extrachromosomal Circular DNA Formation. PLoS ONE 6: e17872 doi:10.1371/journal.pone.0017872.g008.

84. NovoM, BigeyF, BeyneE, GaleoteV, GavoryF, et al. (2009) Eukaryote-to-eukaryote gene transfer events revealed by the genome sequence of the wine yeast Saccharomyces cerevisiae EC1118. Proc Natl Acad Sci USA 106: 16333–16338 doi:10.1073/pnas.0904673106.

85. BoerVM, de WindeJH, PronkJT, PiperMDW (2003) The genome-wide transcriptional responses of Saccharomyces cerevisiae grown on glucose in aerobic chemostat cultures limited for carbon, nitrogen, phosphorus, or sulfur. J Biol Chem 278: 3265–3274 doi:10.1074/jbc.M209759200.

86. VerduynC, PostmaE, ScheffersW, Van DijkenJ (1992) Effect of benzoic acid on metabolic fluxes in yeasts: a continuous-culture study on the regulation of respiration and alcoholic fermentation. Yeast 8: 501–517.

87. WillisR, SchwabG, GentryC (1993) Elimination of interferences in the colorimetric analysis of ammonium in water and soil extracts. Communications in Soil Science and Plant Analysis 24: 1009–1019.

88. CarleG, OlsonMV (1985) An electrophoretic karyotype for yeast. Proc Natl Acad Sci USA 82: 3756–3760.

89. ChuG, VollrathD, DavisRW (986AD) Separation of large DNA molecules by contour-clamped homogeneous electric fields. Science (New York, NY) 234: 1582–1585.

90. AwadIA, ReesCA, Hernandez-BoussardT, BallCA, SherlockG (2004) Caryoscope: An Open Source Java application for viewing microarray data in a genomic context. BMC Bioinformatics 5: 151 doi:10.1186/1471-2105-5-151.

91. SchwartzK, WengerJW, DunnB, SherlockG (2012) APJ1 and GRE3 homologs work in concert to allow growth in xylose in a natural Saccharomyces sensu stricto hybrid yeast. Genetics 191: 621–632 doi:10.1534/genetics.112.140053.

92. LiH, DurbinR (2010) Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics 26: 589–595 doi:10.1093/bioinformatics/btp698.

93. McKennaA, HannaM, BanksE, SivachenkoA, CibulskisK, et al. (2010) The Genome Analysis Toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20: 1297–1303 doi:10.1101/gr.107524.110.

94. DePristoMA, BanksE, PoplinR, GarimellaKV, MaguireJR, et al. (2011) A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet 43: 491–498 doi:10.1038/ng.806.

95. LiH, HandsakerB, WysokerA, FennellT, RuanJ, et al. (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078–2079 doi:10.1093/bioinformatics/btp352.

96. LeeA, HansenKD, BullardJ, DudoitS, SherlockG (2008) Novel low abundance and transient RNAs in yeast revealed by tiling microarrays and ultra high–throughput sequencing are not conserved across closely related yeast species. PLoS Genet 4: e1000299 doi:10.1371/journal.pgen.1000299.t002.

97. BullardJH, MostovoyY, DudoitS, BremRB (2010) Polygenic and directional regulatory evolution across pathways in Saccharomyces. Proc Natl Acad Sci USA 107: 5058–5063 doi:10.1073/pnas.0912959107.

98. EdgarRC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792–1797 doi:10.1093/nar/gkh340.

99. KvitekDJ, SherlockG (2011) Reciprocal sign epistasis between frequently experimentally evolved adaptive mutations causes a rugged fitness landscape. PLoS Genet 7: e1002056 doi:10.1371/journal.pgen.1002056.