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.

  • Article
  • Published:

The core meiotic transcriptome in budding yeasts

Nature Genetics volume 26, pages 415–423 (2000)Cite this article

Abstract

We used high-density oligonucleotide microarrays to analyse the genomes and meiotic expression patterns of two yeast strains, SK1 and W303, that display distinct kinetics and efficiencies of sporulation. Hybridization of genomic DNA to arrays revealed numerous gene deletions and polymorphisms in both backgrounds. The expression analysis yielded approximately 1,600 meiotically regulated genes in each strain, with a core set of approximately 60% displaying similar patterns in both strains. Most of these (95%) are MATa/MATα-dependent and are not similarly expressed in near-isogenic meiosis-deficient controls. The transcript profiles correlate with the distribution of defined meiotic promoter elements and with the time of known gene function.

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: Genomic variation in SK1 and W303.
Figure 2: Meiotic landmarks in SK1 and W303.
Figure 3: Regulated transcription in SK1 and W303 during sporulation and starvation.
Figure 4: Clustered patterns of gene expression during sporulation.
Figure 5: Correlation of gene expression in SK1 and W303.
Figure 6: Average expression profiles of well-correlated genes in SK1 and W303.
Figure 7: Cluster comparisons.

Similar content being viewed by others

References

  1. Kupiec, M., Byers, B., Esposito, R.E. & Mitchell, A.P. Meiosis and sporulation. in Saccharomyces cerevisiae 889–1036 (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, 1997).

    Google Scholar 

  2. Freire, R. et al. Human and mouse homologs of Schizosaccharomyces pombe rad1(+) and Saccharomyces cerevisiae RAD17: linkage to checkpoint control and mammalian meiosis. Genes Dev. 12, 2560–2573 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. McKim, K.S. & Hayashi-Hagihara, A. mei-W68 in Drosophila melanogaster encodes a Spo11 homolog: evidence that the mechanism for initiating meiotic recombination is conserved. Genes Dev. 12, 2932–2942 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Edelmann, W. et al. Mammalian MutS homologue 5 is required for chromosome pairing in meiosis. Nature Genet. 21, 123–127 (1999).

    Article  CAS  PubMed  Google Scholar 

  5. Zalevsky, J., MacQueen, A., Duffy, J., Kemphues, K. & Villeneuve, A. Crossing over during Caenorhabditis elegans meiosis requires a conserved MutS-based pathway that is partially dispensable in budding yeast. Genetics 153, 1271–1283 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Mitchell, A.P. Control of meiotic gene expression in Saccharomyces cerevisiae. Microbiol. Rev. 58, 56–70 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Strich, R. et al. UME6 is a key regulator of nitrogen repression and meiotic development. Genes Dev. 8, 796–810 (1994).

    Article  CAS  PubMed  Google Scholar 

  8. Anderson, S.F., Steber, C.M., Esposito, R.E. & Coleman, J.E. UME6, a negative regulator of meiosis in Saccharomyces cerevisiae, contains a C-terminal Zn2Cys6 binuclear cluster that binds the URS1 DNA sequence in a zinc-dependent manner. Protein Sci. 4, 1832–1843 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Bowdish, K.S., Yuan, H.E. & Mitchell, A.P. Positive control of yeast meiotic genes by the negative regulator UME6. Mol. Cell. Biol. 15, 2955–2961 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Steber, C.M. & Esposito, R.E. UME6 is a central component of a developmental regulatory switch controlling meiosis-specific gene expression. Proc. Natl Acad. Sci. USA 92, 12490–12494 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Rubin-Bejerano, I., Mandel, S., Robzyk, K. & Kassir, Y. Induction of meiosis in Saccharomyces cerevisiae depends on conversion of the transcriptional represssor Ume6 to a positive regulator by its regulated association with the transcriptional activator Ime1. Mol. Cell. Biol. 16, 2518–2526 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Gailus-Durner, V., Xie, J., Chintamaneni, C. & Vershon, A.K. Participation of the yeast activator Abf1 in meiosis-specific expression of the HOP1 gene. Mol. Cell. Biol. 16, 2777–2786 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Ozsarac, N., Straffon, M.J., Dalton, H.E. & Dawes, I.W. Regulation of gene expression during meiosis in Saccharomyces cerevisiae: SPR3 is controlled by both ABFI and a new sporulation control element. Mol. Cell. Biol. 17, 1152–1159 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Chu, S. & Herskowitz, I. Gametogenesis in yeast is regulated by a transcriptional cascade dependent on Ndt80. Mol. Cell 1, 685–696 (1998).

    Article  CAS  PubMed  Google Scholar 

  15. Hepworth, S.R., Friesen, H. & Segall, J. NDT80 and the meiotic recombination checkpoint regulate expression of middle sporulation-specific genes in Saccharomyces cerevisiae. Mol. Cell. Biol. 18, 5750–5761 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Surosky, R.T. & Esposito, R.E. Early meiotic transcripts are highly unstable in Saccharomyces cerevisiae. Mol. Cell. Biol. 12, 3948–3958 (1992).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Chu, S. et al. The transcriptional program of sporulation in budding yeast. Science 282, 699–705 (1998).

    Article  CAS  PubMed  Google Scholar 

  18. Winzeler, E.A. et al. Direct allelic variation scanning of the yeast genome. Science 281, 1194–1197 (1998).

    Article  CAS  PubMed  Google Scholar 

  19. Padmore, R., Cao, L. & Kleckner, N. Temporal comparison of recombination and synaptonemal complex formation during meiosis in S. cerevisiae. Cell 66, 1239–1256 (1991).

    Article  CAS  PubMed  Google Scholar 

  20. Cho, R.J. et al. A genome-wide transcriptional analysis of the mitotic cell cycle. Mol. Cell 2, 65–73 (1998).

    Article  CAS  PubMed  Google Scholar 

  21. Wodicka, L., Dong, H., Mittmann, M., Ho, M.H. & Lockhart, D.J. Genome-wide expression monitoring in Saccharomyces cerevisiae. Nature Biotechnol. 15, 1359–1367 (1997).

    Article  CAS  Google Scholar 

  22. Eisen, M.B., Spellman, P.T., Brown, P.O. & Botstein, D. Cluster analysis and display of genome-wide expression patterns. Proc. Natl Acad. Sci. USA 95, 14863–14868 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Atcheson, C.L., DiDomenico, B., Frackman, S., Esposito, R.E. & Elder, R.T. Isolation, DNA sequence, and regulation of a meiosis-specific eukaryotic recombination gene. Proc. Natl Acad. Sci. USA 84, 8035–8039 (1987).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Buckingham, L.E. et al. Nucleotide sequence and promoter analysis of SPO13, a meiosis-specific gene of Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA 87, 9406–9410 (1990).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Briza, P., Breitenbach, M., Ellinger, A. & Segall, J. Isolation of two developmentally regulated genes involved in spore wall maturation in Saccharomyces cerevisiae. Genes Dev. 4, 1775–1789 (1990).

    Article  CAS  PubMed  Google Scholar 

  26. Dorsman, J.C. et al. An ARS/silencer binding factor also activates two ribosomal protein genes in yeast. Nucleic Acid Res. 17, 4917–4923 (1989).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Della Seta, F., Treich, I., Buhler, J.M. & Sentenac, A. ABF1 binding sites in yeast RNA polymerase genes. J. Biol. Chem. 265, 15168–15175 (1990).

    CAS  PubMed  Google Scholar 

  28. Planta, R.J., Goncalves, P.M. & Mager, W.H. Global regulators of ribosome biosynthesis in yeast. Biochem. Cell Biol. 73, 825–834 (1995).

    Article  CAS  PubMed  Google Scholar 

  29. Rolfes, R.J., Zhang, F. & Hinnebusch, A.G. The transcriptional activators BAS1, BAS2, and ABF1 bind positive regulatory sites as the critical elements for adenine regulation of ADE5,7. J. Biol. Chem. 272, 13343–13354 (1997).

    Article  CAS  PubMed  Google Scholar 

  30. Pierce, M. et al. Transcriptional regulation of the SMK1 mitogen-activated protein kinase gene during meiotic development in Saccharomyces cerevisiae. Mol. Cell. Biol. 18, 5970–5980 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Sumrada, R.A. & Cooper, T.G. Ubiquitous upstream repression sequences control activation of the inducible arginase gene in yeast. Proc. Natl Acad. Sci. USA 84, 3997–4001 (1987).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Sweet, D.H., Jang, Y.K. & Sancar, G.B. Role of UME6 in transcriptional regulation of a DNA repair gene in Saccharomyces cerevisiae. Mol. Cell. Biol. 17, 6223–6235 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Hepworth, S.R., Ebisuzaki, L.K. & Segall, J. A 15-base-pair element activates the SPS4 gene midway through sporulation in Saccharomyces cerevisiae. Mol. Cell. Biol. 15, 3934–3944 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Ross-Macdonald, P. et al. Large-scale analysis of the genome by transposon tagging and gene disruption. Nature 402, 413–418 (1999).

    Article  CAS  PubMed  Google Scholar 

  35. Dujon, B. European Functional Analysis Network (EUROFAN) and the functional analysis of the Saccharomyces cerevisiae genome. Electrophoresis 19, 617–624 (1998).

    Article  CAS  PubMed  Google Scholar 

  36. Covitz, P.A. & Mitchell, A.P. Repression by the yeast meiotic inhibitor RME1. Genes Dev. 7, 1598–1608 (1993).

    Article  CAS  PubMed  Google Scholar 

  37. Esposito, M.S. & Esposito, R.E. The genetic control of sporulation in Saccharomyces. I. The isolation of temperature-sensitive sporulation-deficient mutants. Genetics 61, 79–89 (1969).

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Esposito, R.E. & Klapholz, S. Meiosis and ascospore development. in The Molecular Biology of the Yeast Saccharomyces: Life Cycle and Inheritance (eds Stratern, J.N., Jones, E.W. & Broach, J.R.) 211–287 (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, 1981).

    Google Scholar 

  39. Kaback, D.B. & Feldberg, L.R. Saccharomyces cerevisiae exhibits a sporulation-specific temporal pattern of transcript accumulation. Mol. Cell. Biol. 5, 751–761 (1985).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Strich, R., Woontner, M. & Scott, J. Mutations in ARS1 increase the rate of simple loss of plasmids in Saccharomyces cerevisiae. Yeast 2, 169–178 (1986).

    Article  CAS  PubMed  Google Scholar 

  41. Klapholz, S., Waddell, C.S. & Esposito, R.E. The role of the SPO11 gene in meiotic recombination in yeast. Genetics 110, 187–216 (1985).

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Bishop, D.K., Park, D., Xu, L. & Kleckner, N. DMC1: a meiosis-specific yeast homolog of E. coli recA required for recombination, synaptonemal complex formation, and cell cycle progression. Cell 69, 439–456 (1992).

    Article  CAS  PubMed  Google Scholar 

  43. Lockhart, D.J. et al. Expression monitoring by hybridization to high-density oligonucleotide arrays. Nature Biotechnol. 14, 1675–1680 (1996).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank L.H. Rutkowski and B.K. Washburn for critical reading of the manuscript; S. Fuller for on-line support of GeneSpring; J. Clark, C. Sarrauste de Menthière and B. Masdoua for help in designing the web sites and constructing the database; and J. Demaille, A. Fernandez and N. Lamb at the IGH for hosting M.P. during the final stages of the data analysis. This work was supported by NIH grants 1R01GM29182 (to R.E.E.) and 1RO1HG01633 (to R.W.D.). M.P. was supported by a Max Kade postdoctoral fellowship and in part by grant RG0533 (to A.F. and N.L.).

Author information

Author notes

  1. Michael Primig

    Present address: Institut de Génétique Humaine, Montpellier, France

  2. Michael Primig and Roy M. Williams: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Molecular Genetics and Cell Biology, The University of Chicago, Chicago, Illinois, USA

    Michael Primig, Roy M. Williams, Gela G. Tevzadze & Rochelle Easton Esposito

  2. Department of Biochemistry, Stanford University Medical School, Stanford, California, USA

    Roy M. Williams, Elizabeth A. Winzeler, Seung Y. Hwang & Ronald W. Davis

  3. Silicon Genetics, San Carlos, California, USA

    Andrew R. Conway

Authors
  1. Michael Primig
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Roy M. Williams
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Elizabeth A. Winzeler
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gela G. Tevzadze
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Andrew R. Conway
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Seung Y. Hwang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ronald W. Davis
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Rochelle Easton Esposito
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rochelle Easton Esposito.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Primig, M., Williams, R., Winzeler, E. et al. The core meiotic transcriptome in budding yeasts. Nat Genet 26, 415–423 (2000). https://doi.org/10.1038/82539

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/82539

This article is cited by

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