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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.

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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).

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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.

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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
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Corresponding author

Correspondence to Stephen G. Oliver.

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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)

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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

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