Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Engineering evolution to study speciation in yeasts

Nature volume 422, pages 68–72 (2003)Cite this article

Abstract

The Saccharomyces ‘sensu stricto’ yeasts are a group of species that will mate with one another, but interspecific pairings produce sterile hybrids. A retrospective analysis of their genomes revealed that translocations between the chromosomes of these species do not correlate with the group's sequence-based phylogeny1 (that is, translocations do not drive the process of speciation). However, that analysis was unable to infer what contribution such rearrangements make to reproductive isolation between these organisms. Here, we report experiments that take an interventionist, rather than a retrospective approach to studying speciation, by reconfiguring the Saccharomyces cerevisiae genome so that it is collinear with that of Saccharomyces mikatae. We demonstrate that this imposed genomic collinearity allows the generation of interspecific hybrids that produce a large proportion of spores that are viable, but extensively aneuploid. We obtained similar results in crosses between wild-type S. cerevisiae and the naturally collinear species Saccharomyces paradoxus, but not with non-collinear crosses. This controlled comparison of the effect of chromosomal translocation on species barriers suggests a mechanism for the generation of redundancy in the S. cerevisiae genome2.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Strategy to create reciprocal translocations in yeast.
Figure 2: Discrimination between S. cerevisiae and S. mikatae chromosomes in hybrid zygotes.
Figure 3: Diagnostic PCR for each of the 16 chromosomes of the two parent species reveals the extent of aneuploidy in the meiotic progeny of hybrid zygotes 1 (tetrads A and B) and 3 (tetrads C and D).

Similar content being viewed by others

References

  1. Fischer, G. et al. Chromosomal evolution in Saccharomyces. Nature 405, 451–454 (2000)

    Article  ADS  CAS  Google Scholar 

  2. Goffeau, A. et al. Life with 6000 genes. Science 274, 546–567 (1996)

    Article  ADS  CAS  Google Scholar 

  3. Naumov, G. I. in The Expanding Realm of Yeast-like Fungi (eds de Hoog, G. S., Smith, M. T. & Weyman, A. C. M.) (Elsevier, Amsterdam, 1987)

    Google Scholar 

  4. Naumov, G. I., James, S. A., Naumova, E. S., Louis, E. J. & Roberts, I. N. Three new species in the Saccharomyces sensu stricto complex: Saccharomyces cariocanus, Saccharomyces kudriavzevii and Saccharomyces mikatae. Int. J. Syst. Evol. Microbiol. 50, 1931–1942 (2000)

    Article  CAS  Google Scholar 

  5. Ryu, S. L., Murooka, Y. & Kaneko, Y. Reciprocal translocation at duplicated RPL2 loci might cause speciation of Saccharomyces bayanus and Saccharomyces cerevisiae. Curr. Genet. 33, 345–351 (1998)

    Article  CAS  Google Scholar 

  6. Naumov, G. I., Naumova, E. S. & Querol, A. Genetic study of natural introgression supports delimitation of biological species in the Saccharomyces sensu stricto complex. System. Appl. Microbiol. 20, 595–601 (1997)

    Article  Google Scholar 

  7. Marinoni, G. et al. Horizontal transfer of genetic material among Saccharomyces yeasts. J. Bacteriol. 181, 6488–6496 (1999)

    CAS  Google Scholar 

  8. Seoighe, C. & Wolfe, K. H. Yeast genome evolution in the post-genome era. Curr. Opin. Microbiol. 2, 548–554 (1999)

    Article  CAS  Google Scholar 

  9. Delneri, D. et al. Exploring redundancy in the yeast genome: an improved strategy for the use of the cre-loxP system. Gene 252, 127–135 (2000)

    Article  CAS  Google Scholar 

  10. Saccharomyces Genome Database. 〈http://genome-www4.stanford.edu/cgi-bin/FUNGI/FungiMap〉.

  11. Delneri, D., Gardner, D. C. J. & Oliver, S. G. Analysis of the seven-member AAD gene set demonstrates that genetic redundancy in yeast may be more apparent than real. Genetics 153, 1591–1600 (1999)

    CAS  Google Scholar 

  12. Bengtsson, B. O. & Bodmer, W. F. The fitness of human translocation carriers. Ann. Human Genet. 40, 253–257 (1976)

    Article  CAS  Google Scholar 

  13. Loidl, J., Jin, Q.-W. & Jantsch, M. Meiotic pairing and segregation of translocation quadrivalents in yeast. Chromosoma 107, 247–254 (1998)

    Article  CAS  Google Scholar 

  14. Fischer, G., Neuvéglise, C., Durrens, P., Gaillardin, C. & Dujon, B. Evolution of gene order in the genomes of two related yeast species. Genome Res. 11, 2009–2019 (2001)

    Article  CAS  Google Scholar 

  15. Lynch, M., O'Hely, M., Walsh, B. & Force, A. The probability of preservation of a newly arisen gene duplicate. Genetics 159, 1789–1804 (2001)

    CAS  Google Scholar 

  16. Ramsey, J. & Schemske, D. W. Pathways, mechanisms, and rate of polyploid formation in flowering plants. Annu. Rev. Ecol. Syst. 29, 467–501 (1998)

    Article  Google Scholar 

  17. Sebastiani, F., Barberio, C., Casalone, E., Cavalieri, D. & Polsinelli, M. Crosses between Saccharomyces cerevisiae and Saccharomyces bayanus generate fertile hybrids. Res. Microbiol. 153, 53–58 (2002)

    Article  CAS  Google Scholar 

  18. Tamai, Y., Momma, T., Yoshimoto, H. & Kaneko, Y. Co-existence of two types of chromosome in the bottom-fermenting yeast, Saccharomyces pastorianus. Yeast 14, 923–937 (1998)

    Article  CAS  Google Scholar 

  19. Kielland-Brandt, M. C., Nilson-Tillgren, T., Peterson, J. G. L., Holemberg, S. & Gjermansen, C. in Yeast Genetics (eds Spencer, J. F. T., Spencer, D. M. & Smith, A. R. W.) 421–438 (Springer, New York, 1983)

    Book  Google Scholar 

  20. Wolfe, K. H. & Shields, D. C. Molecular evidence for an ancient duplication of the entire yeast genome. Nature 387, 708–713 (1997)

    Article  ADS  CAS  Google Scholar 

  21. Llorente, B. et al. Genomic exploration of the hemiascomycetous yeasts: 20. Evolution of gene redundancy compared to Saccharomyces cerevisiae. FEBS Lett. 487, 122–133 (2000)

    Article  CAS  Google Scholar 

  22. Greig, D., Borts, R. H., Louis, E. J. & Travisano, M. Epistasis and hybrid sterility in Saccharomyces. Proc. R. Soc. Lond. B. 269, 1167–1671 (2002)

    Article  Google Scholar 

  23. Hunter, N., Chambers, S. R., Louis, E. J. & Borts, R. H. The mismatch repair system contributes to meiotic sterility in an interspecific yeast. EMBO J. 15, 1726–1733 (1996)

    Article  CAS  Google Scholar 

  24. Adams, A., Gottschling, D. E., Kaiser, C. A. & Stearns, T. in Methods in Yeast Genetics (ed. Dickerson, M. M.) 145–175 (Cold Spring Harbor Laboratory Press, New York, 1997)

    Google Scholar 

  25. Gietz, R. D., Schiestl, R. H., Willems, A. R. & Woods, R. A. Studies on the transformation of intact yeast cells by the LiAc/SS-DNA/PEG procedure. Yeast 11, 355–360 (1995)

    Article  CAS  Google Scholar 

  26. Gardner, D. C. J., Heale, S. M., Stateva, L. I. & Oliver, S. G. Treatment of yeast cells with wall lytic enzymes is not required to prepare chromosomes for pulsed-field gel analysis. Yeast 9, 1053–1055 (1993)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by grants from the Biotechnology and Biological Sciences Research Council (to E.J.L., I.N.R. and S.G.O.) and the Wellcome Trust (to S.G.O.). We thank S. James and L. Lockhart for their help in some early analyses, and B. Dujon for discussions.

Author information

Author notes

  1. Isabelle Colson

    Present address: School of Biological Sciences, University of Wales at Bangor, Brambell Building, Deiniol Road, Bangor, LL57 2UW, UK

  2. Sofia Grammenoudi

    Present address: Alexander Fleming Biomedical Science Research Centre, 14–16 Fleming Street, 16672, Vari, Greece

  3. Daniela Delneri, Isabelle Colson and Ian N. Roberts: These authors contributed equally to this work

Authors and Affiliations

  1. School of Biological Sciences, University of Manchester, 2.205 Stopford Building, Oxford Road, M13 9PT, Manchester, UK

    Daniela Delneri, Isabelle Colson, Sofia Grammenoudi & Stephen G. Oliver

  2. National Collection of Yeast Cultures, Institute of Food Research, Norwich Research Park, Colney, NR4 7UA, Norwich, UK

    Ian N. Roberts

  3. Department of Genetics, University of Leicester, University Road, LE1 7RH, Leicester, UK

    Edward J. Louis

Authors
  1. Daniela Delneri
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Isabelle Colson
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sofia Grammenoudi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ian N. Roberts
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Edward J. Louis
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Stephen G. Oliver
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Stephen G. Oliver.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Supplementary information

41586_2003_BFnature01418_MOESM1_ESM.doc

Supplementary Information: Description of the strategy for engineering the translocations into S.cerevisiae, and two Tables listing all the oligonucleotides used in this work. (DOC 46 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Delneri, D., Colson, I., Grammenoudi, S. et al. Engineering evolution to study speciation in yeasts. Nature 422, 68–72 (2003). https://doi.org/10.1038/nature01418

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature01418

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing