Skip to main content
PMC home page
Genetics logoLink to Genetics
. 2003 Dec;165(4):1745–1759. doi: 10.1093/genetics/165.4.1745

Genome-wide amplifications caused by chromosomal rearrangements play a major role in the adaptive evolution of natural yeast.

Juan J Infante 1, Kenneth M Dombek 1, Laureana Rebordinos 1, Jesús M Cantoral 1, Elton T Young 1
PMCID: PMC1462916  PMID: 14704163

Abstract

The relative importance of gross chromosomal rearrangements to adaptive evolution has not been precisely defined. The Saccharomyces cerevisiae flor yeast strains offer significant advantages for the study of molecular evolution since they have recently evolved to a high degree of specialization in a very restrictive environment. Using DNA microarray technology, we have compared the genomes of two prominent variants of S. cerevisiae flor yeast strains. The strains differ from one another in the DNA copy number of 116 genomic regions that comprise 38% of the genome. In most cases, these regions are amplicons flanked by repeated sequences or other recombination hotspots previously described as regions where double-strand breaks occur. The presence of genes that confer specific characteristics to the flor yeast within the amplicons supports the role of chromosomal rearrangements as a major mechanism of adaptive evolution in S. cerevisiae. We propose that nonallelic interactions are enhanced by ethanol- and acetaldehyde-induced double-strand breaks in the chromosomal DNA, which are repaired by pathways that yield gross chromosomal rearrangements. This mechanism of chromosomal evolution could also account for the sexual isolation shown among the flor yeast.

Full Text

The Full Text of this article is available as a PDF (269.9 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Aguilera A., Chávez S., Malagón F. Mitotic recombination in yeast: elements controlling its incidence. Yeast. 2000 Jun 15;16(8):731–754. doi: 10.1002/1097-0061(20000615)16:8<731::AID-YEA586>3.0.CO;2-L. [DOI] [PubMed] [Google Scholar]
  2. Aguilera Andrés. The connection between transcription and genomic instability. EMBO J. 2002 Feb 1;21(3):195–201. doi: 10.1093/emboj/21.3.195. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Avery A. M., Avery S. V. Saccharomyces cerevisiae expresses three phospholipid hydroperoxide glutathione peroxidases. J Biol Chem. 2001 Jul 9;276(36):33730–33735. doi: 10.1074/jbc.M105672200. [DOI] [PubMed] [Google Scholar]
  4. Benítez T., Martínez P., Codón A. C. Genetic constitution of industrial yeast. Microbiologia. 1996 Sep;12(3):371–384. [PubMed] [Google Scholar]
  5. Budroni M., Giordano G., Pinna G., Farris G. A. A genetic study of natural flor strains of Saccharomyces cerevisiae isolated during biological ageing from Sardinian wines. J Appl Microbiol. 2000 Oct;89(4):657–662. doi: 10.1046/j.1365-2672.2000.01163.x. [DOI] [PubMed] [Google Scholar]
  6. Castrejón Francisco, Codón Antonio C., Cubero Beatriz, Benítez Tahía. Acetaldehyde and ethanol are responsible for mitochondrial DNA (mtDNA) restriction fragment length polymorphism (RFLP) in flor yeasts. Syst Appl Microbiol. 2002 Oct;25(3):462–467. doi: 10.1078/0723-2020-00127. [DOI] [PubMed] [Google Scholar]
  7. Cavalieri D., Townsend J. P., Hartl D. L. Manifold anomalies in gene expression in a vineyard isolate of Saccharomyces cerevisiae revealed by DNA microarray analysis. Proc Natl Acad Sci U S A. 2000 Oct 24;97(22):12369–12374. doi: 10.1073/pnas.210395297. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cha Rita S., Kleckner Nancy. ATR homolog Mec1 promotes fork progression, thus averting breaks in replication slow zones. Science. 2002 Jul 26;297(5581):602–606. doi: 10.1126/science.1071398. [DOI] [PubMed] [Google Scholar]
  9. Chi Z., Arneborg N. Relationship between lipid composition, frequency of ethanol-induced respiratory deficient mutants, and ethanol tolerance in Saccharomyces cerevisiae. J Appl Microbiol. 1999 Jun;86(6):1047–1052. doi: 10.1046/j.1365-2672.1999.00793.x. [DOI] [PubMed] [Google Scholar]
  10. Codón A. C., Benítez T., Korhola M. Chromosomal polymorphism and adaptation to specific industrial environments of Saccharomyces strains. Appl Microbiol Biotechnol. 1998 Feb;49(2):154–163. doi: 10.1007/s002530051152. [DOI] [PubMed] [Google Scholar]
  11. Contamine V., Picard M. Maintenance and integrity of the mitochondrial genome: a plethora of nuclear genes in the budding yeast. Microbiol Mol Biol Rev. 2000 Jun;64(2):281–315. doi: 10.1128/mmbr.64.2.281-315.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Delneri Daniela, Colson Isabelle, Grammenoudi Sofia, Roberts Ian N., Louis Edward J., Oliver Stephen G. Engineering evolution to study speciation in yeasts. Nature. 2003 Mar 6;422(6927):68–72. doi: 10.1038/nature01418. [DOI] [PubMed] [Google Scholar]
  13. Dunham Maitreya J., Badrane Hassan, Ferea Tracy, Adams Julian, Brown Patrick O., Rosenzweig Frank, Botstein David. Characteristic genome rearrangements in experimental evolution of Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 2002 Nov 21;99(25):16144–16149. doi: 10.1073/pnas.242624799. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Esteve-Zarzoso B., Peris-Torán M. J., García-Maiquez E., Uruburu F., Querol A. Yeast population dynamics during the fermentation and biological aging of sherry wines. Appl Environ Microbiol. 2001 May;67(5):2056–2061. doi: 10.1128/AEM.67.5.2056-2061.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Fernádez-Espinar M. T., Esteve-Zarzoso B., Querol A., Barrio E. RFLP analysis of the ribosomal internal transcribed spacers and the 5.8S rRNA gene region of the genus Saccharomyces: a fast method for species identification and the differentiation of flor yeasts. Antonie Van Leeuwenhoek. 2000 Jul;78(1):87–97. doi: 10.1023/a:1002741800609. [DOI] [PubMed] [Google Scholar]
  16. Fischer G., James S. A., Roberts I. N., Oliver S. G., Louis E. J. Chromosomal evolution in Saccharomyces. Nature. 2000 May 25;405(6785):451–454. doi: 10.1038/35013058. [DOI] [PubMed] [Google Scholar]
  17. Gachotte D., Eckstein J., Barbuch R., Hughes T., Roberts C., Bard M. A novel gene conserved from yeast to humans is involved in sterol biosynthesis. J Lipid Res. 2001 Jan;42(1):150–154. [PubMed] [Google Scholar]
  18. Gerton J. L., DeRisi J., Shroff R., Lichten M., Brown P. O., Petes T. D. Global mapping of meiotic recombination hotspots and coldspots in the yeast Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 2000 Oct 10;97(21):11383–11390. doi: 10.1073/pnas.97.21.11383. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Guijo S., Mauricio J. C., Salmon J. M., Ortega J. M. Determination of the relative ploidy in different Saccharomyces cerevisiae strains used for fermentation and 'flor' film ageing of dry sherry-type wines. Yeast. 1997 Feb;13(2):101–117. doi: 10.1002/(SICI)1097-0061(199702)13:2<101::AID-YEA66>3.0.CO;2-H. [DOI] [PubMed] [Google Scholar]
  20. Hauser N. C., Fellenberg K., Gil R., Bastuck S., Hoheisel J. D., Pérez-Ortín J. E. Whole genome analysis of a wine yeast strain. Comp Funct Genomics. 2001;2(2):69–79. doi: 10.1002/cfg.73. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Ibeas J. I., Jimenez J. Genomic complexity and chromosomal rearrangements in wine-laboratory yeast hybrids. Curr Genet. 1996 Nov;30(5):410–416. doi: 10.1007/s002940050150. [DOI] [PubMed] [Google Scholar]
  22. Jensen L. T., Howard W. R., Strain J. J., Winge D. R., Culotta V. C. Enhanced effectiveness of copper ion buffering by CUP1 metallothionein compared with CRS5 metallothionein in Saccharomyces cerevisiae. J Biol Chem. 1996 Aug 2;271(31):18514–18519. doi: 10.1074/jbc.271.31.18514. [DOI] [PubMed] [Google Scholar]
  23. Jiménez J., Benítez T. Yeast cell viability under conditions of high temperature and ethanol concentrations depends on the mitochondrial genome. Curr Genet. 1988 Jun;13(6):461–469. doi: 10.1007/BF02427751. [DOI] [PubMed] [Google Scholar]
  24. Kao L. R., Megraw T. L., Chae C. B. SHM1: a multicopy suppressor of a temperature-sensitive null mutation in the HMG1-like abf2 gene. Yeast. 1996 Sep 30;12(12):1239–1250. doi: 10.1002/(sici)1097-0061(19960930)12:12<1239::aid-yea17>3.0.co;2-8. [DOI] [PubMed] [Google Scholar]
  25. Kolodner Richard D., Putnam Christopher D., Myung Kyungjae. Maintenance of genome stability in Saccharomyces cerevisiae. Science. 2002 Jul 26;297(5581):552–557. doi: 10.1126/science.1075277. [DOI] [PubMed] [Google Scholar]
  26. Kramer K. M., Brock J. A., Bloom K., Moore J. K., Haber J. E. Two different types of double-strand breaks in Saccharomyces cerevisiae are repaired by similar RAD52-independent, nonhomologous recombination events. Mol Cell Biol. 1994 Feb;14(2):1293–1301. doi: 10.1128/mcb.14.2.1293. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Larroy Carol, Fernández M. Rosario, González Eva, Parés Xavier, Biosca Josep A. Characterization of the Saccharomyces cerevisiae YMR318C (ADH6) gene product as a broad specificity NADPH-dependent alcohol dehydrogenase: relevance in aldehyde reduction. Biochem J. 2002 Jan 1;361(Pt 1):163–172. doi: 10.1042/0264-6021:3610163. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Lewis L. K., Resnick M. A. Tying up loose ends: nonhomologous end-joining in Saccharomyces cerevisiae. Mutat Res. 2000 Jun 30;451(1-2):71–89. doi: 10.1016/s0027-5107(00)00041-5. [DOI] [PubMed] [Google Scholar]
  29. Martínez P., Codón A. C., Pérez L., Benítez T. Physiological and molecular characterization of flor yeasts: polymorphism of flor yeast populations. Yeast. 1995 Nov;11(14):1399–1411. doi: 10.1002/yea.320111408. [DOI] [PubMed] [Google Scholar]
  30. Mauricio J. C., Valero E., Millán C., Ortega J. M. Changes in nitrogen compounds in must and wine during fermentation and biological aging by flor yeasts. J Agric Food Chem. 2001 Jul;49(7):3310–3315. doi: 10.1021/jf010005v. [DOI] [PubMed] [Google Scholar]
  31. Moore I. K., Martin M. P., Paquin C. E. Telomere sequences at the novel joints of four independent amplifications in Saccharomyces cerevisiae. Environ Mol Mutagen. 2000;36(2):105–112. [PubMed] [Google Scholar]
  32. Mortimer R. K. Evolution and variation of the yeast (Saccharomyces) genome. Genome Res. 2000 Apr;10(4):403–409. doi: 10.1101/gr.10.4.403. [DOI] [PubMed] [Google Scholar]
  33. Pollack J. R., Perou C. M., Alizadeh A. A., Eisen M. B., Pergamenschikov A., Williams C. F., Jeffrey S. S., Botstein D., Brown P. O. Genome-wide analysis of DNA copy-number changes using cDNA microarrays. Nat Genet. 1999 Sep;23(1):41–46. doi: 10.1038/12640. [DOI] [PubMed] [Google Scholar]
  34. Prado Félix, Cortés-Ledesma Felipe, Huertas Pablo, Aguilera Andrés. Mitotic recombination in Saccharomyces cerevisiae. Curr Genet. 2002 Nov 29;42(4):185–198. doi: 10.1007/s00294-002-0346-3. [DOI] [PubMed] [Google Scholar]
  35. Pretorius I. S. Tailoring wine yeast for the new millennium: novel approaches to the ancient art of winemaking. Yeast. 2000 Jun 15;16(8):675–729. doi: 10.1002/1097-0061(20000615)16:8<675::AID-YEA585>3.0.CO;2-B. [DOI] [PubMed] [Google Scholar]
  36. Puig S., Querol A., Barrio E., Pérez-Ortín J. E. Mitotic recombination and genetic changes in Saccharomyces cerevisiae during wine fermentation. Appl Environ Microbiol. 2000 May;66(5):2057–2061. doi: 10.1128/aem.66.5.2057-2061.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Pérez-Ortín José E., Querol Amparo, Puig Sergi, Barrio Eladio. Molecular characterization of a chromosomal rearrangement involved in the adaptive evolution of yeast strains. Genome Res. 2002 Oct;12(10):1533–1539. doi: 10.1101/gr.436602. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Rachidi N., Barre P., Blondin B. Multiple Ty-mediated chromosomal translocations lead to karyotype changes in a wine strain of Saccharomyces cerevisiae. Mol Gen Genet. 1999 Jun;261(4-5):841–850. doi: 10.1007/s004380050028. [DOI] [PubMed] [Google Scholar]
  39. Remize F., Andrieu E., Dequin S. Engineering of the pyruvate dehydrogenase bypass in Saccharomyces cerevisiae: role of the cytosolic Mg(2+) and mitochondrial K(+) acetaldehyde dehydrogenases Ald6p and Ald4p in acetate formation during alcoholic fermentation. Appl Environ Microbiol. 2000 Aug;66(8):3151–3159. doi: 10.1128/aem.66.8.3151-3159.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Reynolds T. B., Fink G. R. Bakers' yeast, a model for fungal biofilm formation. Science. 2001 Feb 2;291(5505):878–881. doi: 10.1126/science.291.5505.878. [DOI] [PubMed] [Google Scholar]
  41. Ristow H., Seyfarth A., Lochmann E. R. Chromosomal damages by ethanol and acetaldehyde in Saccharomyces cerevisiae as studied by pulsed field gel electrophoresis. Mutat Res. 1995 Feb;326(2):165–170. doi: 10.1016/0027-5107(94)00165-2. [DOI] [PubMed] [Google Scholar]
  42. Rønnow B., Kielland-Brandt M. C. GUT2, a gene for mitochondrial glycerol 3-phosphate dehydrogenase of Saccharomyces cerevisiae. Yeast. 1993 Oct;9(10):1121–1130. doi: 10.1002/yea.320091013. [DOI] [PubMed] [Google Scholar]
  43. Sancho E. D., Hernandez E., Rodriguez-Navarro A. Presumed Sexual Isolation in Yeast Populations during Production of Sherrylike Wine. Appl Environ Microbiol. 1986 Feb;51(2):395–397. doi: 10.1128/aem.51.2.395-397.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Sniegowski P. D., Gerrish P. J., Lenski R. E. Evolution of high mutation rates in experimental populations of E. coli. Nature. 1997 Jun 12;387(6634):703–705. doi: 10.1038/42701. [DOI] [PubMed] [Google Scholar]
  45. Wicksteed B. L., Collins I., Dershowitz A., Stateva L. I., Green R. P., Oliver S. G., Brown A. J., Newlon C. S. A physical comparison of chromosome III in six strains of Saccharomyces cerevisiae. Yeast. 1994 Jan;10(1):39–57. doi: 10.1002/yea.320100105. [DOI] [PubMed] [Google Scholar]
  46. Wills C. Production of yeast alcohol dehydrogenase isoenzymes by selection. Nature. 1976 May 6;261(5555):26–29. doi: 10.1038/261026a0. [DOI] [PubMed] [Google Scholar]
  47. Wolfe K. H., Shields D. C. Molecular evidence for an ancient duplication of the entire yeast genome. Nature. 1997 Jun 12;387(6634):708–713. doi: 10.1038/42711. [DOI] [PubMed] [Google Scholar]
  48. Young E. T., Sloan J., Miller B., Li N., van Riper K., Dombek K. M. Evolution of a glucose-regulated ADH gene in the genus Saccharomyces. Gene. 2000 Mar 21;245(2):299–309. doi: 10.1016/s0378-1119(00)00035-4. [DOI] [PubMed] [Google Scholar]
  49. Yu Xin, Gabriel Abram. Ku-dependent and Ku-independent end-joining pathways lead to chromosomal rearrangements during double-strand break repair in Saccharomyces cerevisiae. Genetics. 2003 Mar;163(3):843–856. doi: 10.1093/genetics/163.3.843. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES