Skip to main content
  • Research Article
  • Published:

Phylogenetic origin and transcriptional regulation at the post-diauxic phase of SPI1, in Saccharomyces cerevisiae

Abstract

The gene SPI1, of Saccharomyces cerevisiae, encodes a cell wall protein that is induced in several stress conditions, particularly in the postdiauxic and stationary phases of growth. It has a paralogue, SED1, which shows some common features in expression regulation and in the null mutant phenotype. In this work we have identified homologues in other species of yeasts and filamentous fungi, and we have also elucidated some aspects of the origin of SPI1, by duplication and diversification of SED1. In terms of regulation, we have found that the expression in the post-diauxic phase is regulated by genes related to the PKA pathway and stress response (MSN2/4, YAK1, POP2, SOK2, PHD1, and PHO84) and by genes involved in the PKC pathway (WSC2, PKC1, and MPK1).

Abbreviations

AP:

adaptor protein

C:

control

GPI:

glycophosphatidylinositol

mRNA:

messenger RNA

OD:

optical density

te]ONPG:

ortho-nitrophenyl-β-galactoside

PD:

post-diauxic

PKA:

protein kinase A

PKC:

protein kinase C

S:

SD without glucose

SD:

synthetic defined medium

YPD:

yeast extract peptone dextrose medium

References

  1. Ruis, H. and Schuller, C. Stress signaling in yeast. Bioessays, 17 (1995) 959–965.

    Article  PubMed  CAS  Google Scholar 

  2. Werner-Washburne, M., Braun, E.L., Crawford, M.E. and Peck, V.M. Stationary phase in Saccharomyces cerevisiae. Mol. Microbiol. 19 (1996) 1159–1166.

    Article  PubMed  CAS  Google Scholar 

  3. Wei, M., Fabrizio, P., Hu, J., Ge, H., Cheng, C., Li, L. and Longo, V.D. Life span extension by calorie restriction depends on Rim15 and transcription factors downstream of Ras/PKA, Tor, and Sch9. PLoS Genet. 4 (2008) e13.

    Article  PubMed  Google Scholar 

  4. Kapteyn, J.C., ter Riet, B., Vink, E., Blad, S., De Nobel, H., Van Den Ende, H. and Klis, F M. Low external pH induces HOG1-dependent changes in the organization of the Saccharomyces cerevisiae, cell wall. Mol. Microbiol. 39 (2001) 469–479.

    Article  PubMed  CAS  Google Scholar 

  5. Simoes, T., Teixeira, M.C., Fernandes, A.R. and Sa-Correia, I. Adaptation of Saccharomyces cerevisiae, to the herbicide 2,4-dichlorophenoxyacetic acid, mediated by Msn2p- and Msn4p-regulated genes: important role of SPI1. Appl. Environ. Microbiol. 69 (2003) 4019–4028.

    Article  PubMed  CAS  Google Scholar 

  6. Simoes, T., Mira, N.P., Fernandes, A.R. and Sa-Correia, I. The SPI1, gene, encoding a glycosylphosphatidylinositol-anchored cell wall protein, plays a prominent role in the development of yeast resistance to lipophilic weakacid food preservatives. Appl. Environ. Microbiol. 72 (2006) 7168–7175.

    Article  PubMed  CAS  Google Scholar 

  7. Jin, R., Dobry, C.J., McCown, P.J. and Kumar, A. Large-scale analysis of yeast filamentous growth by systematic gene disruption and overexpression. Mol. Biol. Cell. 19 (2008) 284–296.

    Article  PubMed  CAS  Google Scholar 

  8. Alexander, M.R., Tyers, M., Perret, M., Craig, B.M., Fang, K.S. and Gustin, M.C. Regulation of cell cycle progression by Swe1p and Hog1p following hypertonic stress. Mol. Biol. Cell. 12 (2001) 53–62.

    PubMed  CAS  Google Scholar 

  9. Causton, H.C., Ren, B., Koh, S.S., Harbison, C.T., Kanin, E., Jennings, E.G., Lee, T.I., True, H.L., Lander, E.S. and Young, R.A. Remodeling of yeast genome expression in response to environmental changes. Mol. Biol. Cell. 12 (2001) 323–337.

    PubMed  CAS  Google Scholar 

  10. Puig, S. and Perez-Ortin, J.E. Stress response and expression patterns in wine fermentations of yeast genes induced at the diauxic shift. Yeast, 16 (2000) 139–148.

    Article  PubMed  CAS  Google Scholar 

  11. Cardona, F., Aranda, A. and del Olmo, M. Ubiquitin ligase Rsp5p is involved in the gene expression changes during nutrient limitation in Saccharomyces cerevisiae. Yeast, 26 (2009) 1–15.

    Article  PubMed  CAS  Google Scholar 

  12. Cardona, F., Carrasco, P., Perez-Ortin, J. E., del Olmo, M. and Aranda, A. A novel approach for the improvement of stress resistance in wine yeasts. Int. J. Food Microbiol. 114 (2007) 83–91.

    Article  PubMed  CAS  Google Scholar 

  13. Cardona, F., Orozco, H., Friant, S., Aranda, A. and del Olmo, M.L. The Saccharomyces cerevisiae, flavodoxin-like proteins Ycp4 and Rfs1 play a role in stress response and in the regulation of genes related to metabolism. Arch. Microbiol. 193 (2011) 515–525.

    Article  PubMed  CAS  Google Scholar 

  14. Shimoi, H., Kitagaki, H., Ohmori, H., Iimura, Y. and Ito, K. Sed1p is a major cell wall protein of Saccharomyces cerevisiae, in the stationary phase and is involved in lytic enzyme resistance. J. Bacteriol. 180 (1998) 3381–3387.

    PubMed  CAS  Google Scholar 

  15. Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F. and Higgins, D.G. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis Tools. Nucleic Acids Res. 25 (1997) 4876–4882.

    Article  PubMed  CAS  Google Scholar 

  16. Do, C.B., Mahabhashyam, M.S., Brudno, M. and Batzoglou, S. ProbCons: Probabilistic consistency-based multiple sequence alignment. Genome Res. 15 (2005) 330–340.

    Article  PubMed  CAS  Google Scholar 

  17. Castresana, J. Selection of conserved blocks from multiple alignments for their use in phylogenetic análisis. Mol. Biol. Evol. 17 (2000) 540–552.

    Article  PubMed  CAS  Google Scholar 

  18. Tamura, K., Dudley, J., Nei, M. and Kumar, S. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24 (2007) 1596–1599.

    Article  PubMed  CAS  Google Scholar 

  19. Huelsenbeck, J.P. and Ronquist, F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics, 17 (2001) 754–755.

    Article  PubMed  CAS  Google Scholar 

  20. Wolfe, K.H. Comparative genomics and genome evolution in yeasts. Philos. Trans. R. Soc. Lond. B. Biol Sci. 361 (2006) 403–412.

    Article  PubMed  CAS  Google Scholar 

  21. Moriya, H., Shimizu-Yoshida, Y., Omori, A., Iwashita, S., Katoh, M. and Sakai A. Yak1p, a DYRK family kinase, translocates to the nucleus and phosphorylates yeast Pop2p in response to a glucose signal. Genes Dev. 15 (2001) 1217–1228.

    Article  PubMed  CAS  Google Scholar 

  22. Hohmann, S. Osmotic stress signaling and osmoadaptation in yeasts. Microbiol. Mol. Biol. Rev. 66 (2002) 300–372.

    Article  PubMed  CAS  Google Scholar 

  23. Scannell, D.R., Butler, G. and Wolfe, K.H. Yeast genome evolution-the origin of the species. Yeast, 24 (2007) 929–942.

    Article  PubMed  CAS  Google Scholar 

  24. Brauer, M.J., Saldanha, A.J., Dolinski, K. and Botstein, D. Homeostatic adjustment and metabolic remodelling in glucose-limited yeast cultures. Mol. Biol. Cell. 16 (2005) 2503–2517.

    Article  PubMed  CAS  Google Scholar 

  25. de Morgan, A., Brodsky, L., Ronin, Y., Nevo, E., Korol, A. and Kashi, Y. Genome-wide analysis of DNA turnover and gene expression in stationaryphase Saccharomyces cerevisiae. Microbiology, 156 (2010) 1758–1571.

    Article  PubMed  Google Scholar 

  26. Bell-Pedersen, D., Shinohara, M.L., Loros, J.J. and Dunlap, J.C. Circadian clock-controlled genes isolated from Neurospora crassa, are late night-to early morning-specific. Proc. Natl. Acad. Sci. USA, 93 (1996) 13096–13101.

    Article  PubMed  CAS  Google Scholar 

  27. Aign, V. and Hoheisel, J.D. Analysis of nutrient-dependent transcript variations in Neurospora crassa. Fungal Genet. Biol. 40 (2003) 225–233.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  29. Ptacek, J., Devgan, G., Michaud, G., Zhu, H., Zhu, X., Fasolo, J., Guo, H., Jona, G., Breitkreutz, A., Sopko, R., McCartney, R.R., Schmidt, M.C., Rachidi, N., Lee, S.J., Mah, A.S., Meng, L., Stark, M.J., Stern, D.F., De Virgilio, C., Tyers, M., Andrews, B., Gerstein, M., Schweitzer B., Predki, P.F. and Snyder M. Global analysis of protein phosphorylation in yeast. Nature, 7068 (2005) 679–684.

    Article  Google Scholar 

  30. Wu, Q., James, S.A., Roberts, I.N., Moulton, V. and Huber, K.T. Exploring contradictory phylogenetic relationships in yeasts. FEMS Yeast Res. 8 (2008) 641–650.

    Article  PubMed  CAS  Google Scholar 

  31. Pan, X. and Heitman, J. Sok2 regulates yeast pseudohyphal differentiation via a transcription factor cascade that regulates cell-cell adhesion. Mol. Cell. Biol. 20 (2000) 8364–8372.

    Article  PubMed  CAS  Google Scholar 

  32. Gasch, A.P., Spellman, P.T., Kao, C.M., Carmel-Harel, O., Eisen, M.B., Storz, G., Botstein, D. and Brown, P.O. Genomic expression programs in the response of yeast cells to environmental changes. Mol. Biol. Cell. 11 (2000) 4241–4257.

    PubMed  CAS  Google Scholar 

  33. Popova, Y., Thayumanavan, P., Lonati, E., Agrochao, M. and Thevelein, J.M. Transport and signaling through the phosphate-binding site of the yeast Pho84 phosphate transceptor. Proc. Natl. Acad. Sci. USA, 107 (2010) 2890–2895.

    Article  PubMed  CAS  Google Scholar 

  34. Sobering, A.K., Jung, U.S., Lee, K.S. and Levin, D.E. Yeast Rpi1 is a putative transcriptional regulator that contributes to preparation for stationary phase. Eukaryot. Cell, 1 (2002) 56–65.

    Article  PubMed  CAS  Google Scholar 

  35. Belli, G., Molina, M.M., Garcia-Martinez, J., Perez-Ortin, J.E. and Herrero, E. Saccharomyces cerevisiae, glutaredoxin 5-deficient cells subjected to continuous oxidizing conditions are affected in the expression of specific sets of genes. J. Biol. Chem. 279 (2004) 12386–12395.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Fernando Cardona.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cardona, F., Del Olmo, M. & Aranda, A. Phylogenetic origin and transcriptional regulation at the post-diauxic phase of SPI1, in Saccharomyces cerevisiae . Cell Mol Biol Lett 17, 393–407 (2012). https://doi.org/10.2478/s11658-012-0017-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.2478/s11658-012-0017-4

Key words