Jump to ContentJump to Main Navigation
Show Summary Details
In This Section

Cellular and Molecular Biology Letters

Editor-in-Chief: /

IMPACT FACTOR increased in 2015: 1.753

SCImago Journal Rank (SJR) 2015: 0.788
Source Normalized Impact per Paper (SNIP) 2015: 0.645
Impact per Publication (IPP) 2015: 1.748

See all formats and pricing
In This Section
Volume 17, Issue 3 (Sep 2012)

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

Fernando Cardona
  • Instituto de Agroquímica y Tecnología de Alimentos, CSIC
  • Universitat de València
  • Email:
/ Marcel.Lí Olmo
  • Universitat de València
  • Email:
/ Agustín Aranda
  • Instituto de Agroquímica y Tecnología de Alimentos, CSIC
  • Email:
Published Online: 2012-06-17 | DOI: https://doi.org/10.2478/s11658-012-0017-4


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).

Keywords: SPI1; Phylogenetic origin; Transcriptional regulation; Post-diauxic; Nutrient starvation; PKA; PKC

  • [1] Ruis, H. and Schuller, C. Stress signaling in yeast. Bioessays, 17 (1995) 959–965. http://dx.doi.org/10.1002/bies.950171109 [Crossref]

  • [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. http://dx.doi.org/10.1111/j.1365-2958.1996.tb02461.x [Crossref]

  • [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. http://dx.doi.org/10.1371/journal.pgen.0040013 [Web of Science] [Crossref]

  • [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. http://dx.doi.org/10.1046/j.1365-2958.2001.02242.x [Crossref]

  • [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. http://dx.doi.org/10.1128/AEM.69.7.4019-4028.2003 [Crossref]

  • [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. http://dx.doi.org/10.1128/AEM.01476-06 [Crossref]

  • [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. http://dx.doi.org/10.1091/mbc.E07-05-0519 [Web of Science] [Crossref]

  • [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. [Crossref]

  • [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. [Crossref]

  • [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. http://dx.doi.org/10.1002/(SICI)1097-0061(20000130)16:2<139::AID-YEA512>3.0.CO;2-J [Crossref]

  • [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. http://dx.doi.org/10.1002/yea.1645 [Web of Science] [Crossref]

  • [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. http://dx.doi.org/10.1016/j.ijfoodmicro.2006.10.043 [Web of Science] [Crossref]

  • [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. http://dx.doi.org/10.1007/s00203-011-0696-7 [Crossref]

  • [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.

  • [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. http://dx.doi.org/10.1093/nar/25.24.4876 [Crossref]

  • [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. http://dx.doi.org/10.1101/gr.2821705 [Crossref]

  • [17] Castresana, J. Selection of conserved blocks from multiple alignments for their use in phylogenetic análisis. Mol. Biol. Evol. 17 (2000) 540–552. http://dx.doi.org/10.1093/oxfordjournals.molbev.a026334 [Crossref]

  • [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. http://dx.doi.org/10.1093/molbev/msm092

  • [19] Huelsenbeck, J.P. and Ronquist, F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics, 17 (2001) 754–755. http://dx.doi.org/10.1093/bioinformatics/17.8.754 [Crossref]

  • [20] Wolfe, K.H. Comparative genomics and genome evolution in yeasts. Philos. Trans. R. Soc. Lond. B. Biol Sci. 361 (2006) 403–412. http://dx.doi.org/10.1098/rstb.2005.1799 [Crossref]

  • [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. http://dx.doi.org/10.1101/gad.884001 [Crossref]

  • [22] Hohmann, S. Osmotic stress signaling and osmoadaptation in yeasts. Microbiol. Mol. Biol. Rev. 66 (2002) 300–372. http://dx.doi.org/10.1128/MMBR.66.2.300-372.2002 [Crossref]

  • [23] Scannell, D.R., Butler, G. and Wolfe, K.H. Yeast genome evolution-the origin of the species. Yeast, 24 (2007) 929–942. http://dx.doi.org/10.1002/yea.1515 [Web of Science] [Crossref]

  • [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. http://dx.doi.org/10.1091/mbc.E04-11-0968 [Crossref]

  • [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. http://dx.doi.org/10.1099/mic.0.035519-0 [Crossref]

  • [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. http://dx.doi.org/10.1073/pnas.93.23.13096 [Crossref]

  • [27] Aign, V. and Hoheisel, J.D. Analysis of nutrient-dependent transcript variations in Neurospora crassa. Fungal Genet. Biol. 40 (2003) 225–233. http://dx.doi.org/10.1016/S1087-1845(03)00106-3 [Crossref]

  • [28] Wolfe, K.H. and Shields, D.C. Molecular evidence for an ancient duplication of the entire yeast genome. Nature, 387 (1997) 708–713. http://dx.doi.org/10.1038/42711 [Crossref]

  • [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. http://dx.doi.org/10.1038/nature04187 [Crossref]

  • [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. http://dx.doi.org/10.1111/j.1567-1364.2008.00362.x [Crossref] [Web of Science]

  • [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. http://dx.doi.org/10.1128/MCB.20.22.8364-8372.2000 [Crossref]

  • [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. [Crossref]

  • [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. http://dx.doi.org/10.1073/pnas.0906546107 [Crossref]

  • [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. http://dx.doi.org/10.1128/EC.1.1.56-65.2002 [Crossref]

  • [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. http://dx.doi.org/10.1074/jbc.M311879200 [Crossref]

About the article

Published Online: 2012-06-17

Published in Print: 2012-09-01

Citation Information: Cellular and Molecular Biology Letters, ISSN (Online) 1689-1392, DOI: https://doi.org/10.2478/s11658-012-0017-4. Export Citation

© 2012 Versita Warsaw. This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License. (CC BY-NC-ND 3.0)

Comments (0)

Please log in or register to comment.
Log in