Current Genetics

, Volume 64, Issue 5, pp 1001–1004 | Cite as

Frequent ploidy changes in growing yeast cultures

  • Yaniv Harari
  • Yoav Ram
  • Martin Kupiec


Ploidy is considered a very stable cellular characteristic. Although rare, changes in ploidy play important roles in the acquisition of long-term adaptations. Since these duplications allow the subsequent loss of individual chromosomes and accumulation of mutations, changes in ploidy can also cause genomic instability, and have been found to promote cancer. Despite the importance of the subject, measuring the rate of whole-genome duplications has proven extremely challenging. We have recently measured the rate of diploidization in yeast using long-term, in-lab experiments. We found that spontaneous diploidization occurs frequently, by two different mechanisms: endoreduplication and mating type switching. Despite its common occurrence, spontaneous diploidization is usually selected against, although it can be advantageous under some stressful conditions. Our results have implications for the understanding of evolutionary processes, as well as for the use of yeast cells in biotechnological applications.


Saccharomyces cerevisiae Ploidy Haploid Diploid Homothallism Heterothalism Genome duplication Endoreduplication Homologous recombination 



We thank present and past members of the Kupiec lab for support, ideas and technical help. This work was supported by Grants from the Minerva Stiftung, the Volkswagen Foundation and the Israel Science Foundation to MK and the Stanford Center for Computational, Evolutionary and Human Genomics to YR.


  1. Adamczyk J, Deregowska A, Panek A, Golec E, Lewinska A, Wnuk M (2016) Affected chromosome homeostasis and genomic instability of clonal yeast cultures. Curr Genet 62:405–418. CrossRefPubMedPubMedCentralGoogle Scholar
  2. Bell G (2010) Experimental genomics of fitness in yeast. Proc Biol Sci/R Soc 277:1459–1467. CrossRefGoogle Scholar
  3. Berman J, Hadany L (2012) Does stress induce (para)sex? Implications for Candida albicans evolution. Trends Genet 28:197–203. CrossRefPubMedPubMedCentralGoogle Scholar
  4. Chidi BS, Rossouw D, Bauer FF (2016) Identifying and assessing the impact of wine acid-related genes in yeast. Curr Genet 62:149–164. CrossRefPubMedPubMedCentralGoogle Scholar
  5. Cubillos FA (2016) Exploiting budding yeast natural variation for industrial processes. Curr Genet 62:745–751. CrossRefPubMedPubMedCentralGoogle Scholar
  6. Cuypers TD, Hogeweg P (2014) A synergism between adaptive effects and evolvability drives whole genome duplication to fixation. PLoS Comput Biol 10:e1003547. CrossRefPubMedPubMedCentralGoogle Scholar
  7. Desai MM, Fisher DS, Murray AW (2007) The speed of evolution and maintenance of variation in asexual populations. Curr Biol 17:385–394. CrossRefPubMedPubMedCentralGoogle Scholar
  8. Dunham MJ, Badrane H, Ferea T, Adams J, Brown PO, Rosenzweig F, Botstein D (2002) Characteristic genome rearrangements in experimental evolution of Saccharomyces cerevisiae. Proc Natl Acad Sci USA 99:16144–16149. CrossRefPubMedPubMedCentralGoogle Scholar
  9. Edgar BA, Orr-Weaver TL (2001) Endoreplication cell cycles: more for less. Cell 105:297–306 doiCrossRefPubMedCentralGoogle Scholar
  10. Fujiwara T, Bandi M, Nitta M, Ivanova EV, Bronson RT, Pellman D (2005) Cytokinesis failure generating tetraploids promotes tumorigenesis in p53-null cells. Nature 437:1043–1047. CrossRefPubMedPubMedCentralGoogle Scholar
  11. Gallone B, Steensels J, Prahl T, Soriaga L, Saels V, Herrera-Malaver B, Merlevede A, Roncoroni M, Voordeckers K, Miraglia L, Teiling C, Steffy B, Taylor M, Schwartz A, Richardson T, White C, Baele G, Maere S, Verstrepen KJ (2016) Domestication and divergence of Saccharomyces cerevisiae beer yeasts. Cell 166:1397–1410 e1316. CrossRefPubMedPubMedCentralGoogle Scholar
  12. Gerstein AC (2013) Mutational effects depend on ploidy level: all else is not equal. Biol Lett 9:20120614. CrossRefPubMedPubMedCentralGoogle Scholar
  13. Gerstein AC, Otto SP (2011) Cryptic fitness advantage: diploids invade haploid populations despite lacking any apparent advantage as measured by standard fitness assays. PLoS ONE 6:e26599. CrossRefPubMedPubMedCentralGoogle Scholar
  14. Gerstein AC, Chun HJ, Grant A, Otto SP (2006) Genomic convergence toward diploidy in Saccharomyces cerevisiae. PLoS Genet 2:e145. CrossRefPubMedPubMedCentralGoogle Scholar
  15. Gerstein AC, Lim H, Berman J, Hickman MA (2017) Ploidy tug-of-war: evolutionary and genetic environments influence the rate of ploidy drive in a human fungal pathogen. Evol Int J Org Evol 71:1025–1038. CrossRefGoogle Scholar
  16. Gore J, Youk H, van Oudenaarden A (2009) Snowdrift game dynamics and facultative cheating in yeast. Nature 459:253–256. CrossRefPubMedPubMedCentralGoogle Scholar
  17. Harari Y, Ram Y, Rappoport N, Hadany L, Kupiec M (2018) Spontaneous changes in ploidy are common in yeast. Curr Biol. CrossRefPubMedPubMedCentralGoogle Scholar
  18. Hou J, Schacherer J (2016) Negative epistasis: a route to intraspecific reproductive isolation in yeast? Curr Genet 62:25–29. CrossRefPubMedPubMedCentralGoogle Scholar
  19. Lang GI, Rice DP, Hickman MJ, Sodergren E, Weinstock GM, Botstein D, Desai MM (2013) Pervasive genetic hitchhiking and clonal interference in forty evolving yeast populations. Nature 500:571–574. CrossRefPubMedPubMedCentralGoogle Scholar
  20. Lee CS, Haber JE (2015) Mating-type gene switching in Saccharomyces cerevisiae. Microbiol Spectr. CrossRefPubMedPubMedCentralGoogle Scholar
  21. McDonald MJ, Hsieh YY, Yu YH, Chang SL, Leu JY (2012) The evolution of low mutation rates in experimental mutator populations of Saccharomyces cerevisiae. Curr Biol 22:1235–1240. CrossRefPubMedPubMedCentralGoogle Scholar
  22. Meiron H, Nahon E, Raveh D (1995) Identification of the heterothallic mutation in HO-endonuclease of S. cerevisiae using HO/ho chimeric genes. Curr Genet 28:367–373CrossRefPubMedCentralGoogle Scholar
  23. Ram Y, Hadany L (2016) Condition-dependent sex: who does it, when and why? Philos Trans R Soc Lond Ser B. CrossRefGoogle Scholar
  24. Ratcliff WC, Denison RF, Borrello M, Travisano M (2012) Experimental evolution of multicellularity. Proc Natl Acad Sci USA 109:1595–1600. CrossRefPubMedPubMedCentralGoogle Scholar
  25. Romano GH, Harari Y, Yehuda T, Podhorzer A, Rubinstein L, Shamir R, Gottlieb A, Silberberg Y, Pe’er D, Ruppin E, Sharan R, Kupiec M (2013) Environmental stresses disrupt telomere length homeostasis. PLoS Genet 9:e1003721. CrossRefPubMedPubMedCentralGoogle Scholar
  26. Sellis D, Kvitek DJ, Dunn B, Sherlock G, Petrov DA (2016) Heterozygote advantage is a common outcome of adaptation in Saccharomyces cerevisiae. Genetics 203:1401–1413. CrossRefPubMedPubMedCentralGoogle Scholar
  27. Selmecki AM, Maruvka YE, Richmond PA, Guillet M, Shoresh N, Sorenson AL, De S, Kishony R, Michor F, Dowell R, Pellman D (2015) Polyploidy can drive rapid adaptation in yeast. Nature 519:349–352. CrossRefPubMedPubMedCentralGoogle Scholar
  28. Snoek T, Verstrepen KJ, Voordeckers K (2016) How do yeast cells become tolerant to high ethanol concentrations? Curr Genet 62:475–480. CrossRefPubMedPubMedCentralGoogle Scholar
  29. Steensels J, Verstrepen KJ (2014) Taming wild yeast: potential of conventional and nonconventional yeasts in industrial fermentations. Annu Rev Microbiol 68:61–80. CrossRefPubMedPubMedCentralGoogle Scholar
  30. Storchova Z, Kuffer C (2008) The consequences of tetraploidy and aneuploidy. J Cell Sci 121:3859–3866. CrossRefPubMedPubMedCentralGoogle Scholar
  31. Thompson DA, Desai MM, Murray AW (2006) Ploidy controls the success of mutators and nature of mutations during budding yeast evolution. Curr Biol 16:1581–1590. CrossRefPubMedPubMedCentralGoogle Scholar
  32. Toprak E, Veres A, Michel JB, Chait R, Hartl DL, Kishony R (2012) Evolutionary paths to antibiotic resistance under dynamically sustained drug selection. Nat Genet 44:101–105. CrossRefGoogle Scholar
  33. Tosato V, Sims J, West N, Colombin M, Bruschi CV (2017) Post-translocational adaptation drives evolution through genetic selection and transcriptional shift in Saccharomyces cerevisiae. Curr Genet 63:281–292. CrossRefPubMedPubMedCentralGoogle Scholar
  34. Ungar L, Harari Y, Toren A, Kupiec M (2011) Tor complex 1 controls telomere length by affecting the level of Ku. Curr Biol 21:2115–2120. CrossRefPubMedPubMedCentralGoogle Scholar
  35. Venkataram S, Dunn B, Li Y, Agarwala A, Chang J, Ebel ER, Geiler-Samerotte K, Herissant L, Blundell JR, Levy SF, Fisher DS, Sherlock G, Petrov DA (2016) Development of a comprehensive genotype-to-fitness map of adaptation-driving mutations in yeast. Cell 166:1585–1596, e1522. CrossRefPubMedCentralGoogle Scholar
  36. Voordeckers K, Kominek J, Das A, Espinosa-Cantu A, De Maeyer D, Arslan A, Van Pee M, van der Zande E, Meert W, Yang Y, Zhu B, Marchal K, DeLuna A, Van Noort V, Jelier R, Verstrepen KJ (2015) Adaptation to high ethanol reveals complex evolutionary pathways. PLoS Genet 11:e1005635. CrossRefPubMedPubMedCentralGoogle Scholar
  37. Yona AH, Manor YS, Herbst RH, Romano GH, Mitchell A, Kupiec M, Pilpel Y, Dahan O (2012) Chromosomal duplication is a transient evolutionary solution to stress. Proc Natl Acad Sci USA 109:21010–21015. CrossRefPubMedPubMedCentralGoogle Scholar
  38. Zhang N, Cao L (2017) Starvation signals in yeast are integrated to coordinate metabolic reprogramming and stress response to ensure longevity. Curr Genet 63:839–843. CrossRefPubMedPubMedCentralGoogle Scholar
  39. Zhu YO, Siegal ML, Hall DW, Petrov DA (2014) Precise estimates of mutation rate and spectrum in yeast. Proc Natl Acad Sci USA 111:E2310-2318. CrossRefGoogle Scholar
  40. Zhu YO, Sherlock G, Petrov DA (2016) Whole genome analysis of 132 clinical Saccharomyces cerevisiae strains reveals extensive ploidy variation. G3 6:2421–2434. CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.School of Molecular Cell Biology & BiotechnologyTel Aviv UniversityTel AvivIsrael
  2. 2.Department of BiologyStanford UniversityStanfordUSA

Personalised recommendations