Skip to main content
PMC home page
Cellular & Molecular Biology Letters logoLink to Cellular & Molecular Biology Letters
. 2012 May 18;17(3):393–407. doi: 10.2478/s11658-012-0017-4

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

Fernando Cardona 1,2,✉, MarcelLí Del Olmo 2, Agustín Aranda 1
PMCID: PMC6275683  PMID: 22610976

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).

Electronic Supplementary Material

Supplementary material is available for this article at 10.2478/s11658-012-0017-4 and is accessible for authorized users.

Key words: SPI1, Phylogenetic origin, Transcriptional regulation, Post-diauxic, Nutrient starvation, PKA, PKC

Full Text

The Full Text of this article is available as a PDF (573.2 KB).

Abbreviations used

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., Schuller C. Stress signaling in yeast. Bioessays. 1995;17:959–965. doi: 10.1002/bies.950171109. [DOI] [PubMed] [Google Scholar]
  • 2.Werner-Washburne M., Braun E.L., Crawford M.E., Peck V.M. Stationary phase in Saccharomyces cerevisiae. Mol. Microbiol. 1996;19:1159–1166. doi: 10.1111/j.1365-2958.1996.tb02461.x. [DOI] [PubMed] [Google Scholar]
  • 3.Wei M., Fabrizio P., Hu J., Ge H., Cheng C., Li L., Longo V.D. Life span extension by calorie restriction depends on Rim15 and transcription factors downstream of Ras/PKA, Tor, and Sch9. PLoS Genet. 2008;4:e13. doi: 10.1371/journal.pgen.0040013. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 4.Kapteyn J.C., ter Riet B., Vink E., Blad S., De Nobel H., Van Den Ende H., Klis F. M. Low external pH induces HOG1-dependent changes in the organization of the Saccharomyces cerevisiae, cell wall. Mol. Microbiol. 2001;39:469–479. doi: 10.1046/j.1365-2958.2001.02242.x. [DOI] [PubMed] [Google Scholar]
  • 5.Simoes T., Teixeira M.C., Fernandes A.R., 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. 2003;69:4019–4028. doi: 10.1128/AEM.69.7.4019-4028.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 6.Simoes T., Mira N.P., Fernandes A.R., 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. 2006;72:7168–7175. doi: 10.1128/AEM.01476-06. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 7.Jin R., Dobry C.J., McCown P.J., Kumar A. Large-scale analysis of yeast filamentous growth by systematic gene disruption and overexpression. Mol. Biol. Cell. 2008;19:284–296. doi: 10.1091/mbc.E07-05-0519. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 8.Alexander M.R., Tyers M., Perret M., Craig B.M., Fang K.S., Gustin M.C. Regulation of cell cycle progression by Swe1p and Hog1p following hypertonic stress. Mol. Biol. Cell. 2001;12:53–62. doi: 10.1091/mbc.12.1.53. [DOI] [PMC free article] [PubMed] [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., Young R.A. Remodeling of yeast genome expression in response to environmental changes. Mol. Biol. Cell. 2001;12:323–337. doi: 10.1091/mbc.12.2.323. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 10.Puig S., Perez-Ortin J.E. Stress response and expression patterns in wine fermentations of yeast genes induced at the diauxic shift. Yeast. 2000;16:139–148. doi: 10.1002/(SICI)1097-0061(20000130)16:2<139::AID-YEA512>3.0.CO;2-J. [DOI] [PubMed] [Google Scholar]
  • 11.Cardona F., Aranda A., del Olmo M. Ubiquitin ligase Rsp5p is involved in the gene expression changes during nutrient limitation in Saccharomyces cerevisiae. Yeast. 2009;26:1–15. doi: 10.1002/yea.1645. [DOI] [PubMed] [Google Scholar]
  • 12.Cardona F., Carrasco P., Perez-Ortin J. E., del Olmo M., Aranda A. A novel approach for the improvement of stress resistance in wine yeasts. Int. J. Food Microbiol. 2007;114:83–91. doi: 10.1016/j.ijfoodmicro.2006.10.043. [DOI] [PubMed] [Google Scholar]
  • 13.Cardona F., Orozco H., Friant S., Aranda A., 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. 2011;193:515–525. doi: 10.1007/s00203-011-0696-7. [DOI] [PubMed] [Google Scholar]
  • 14.Shimoi H., Kitagaki H., Ohmori H., Iimura Y., 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. 1998;180:3381–3387. doi: 10.1128/jb.180.13.3381-3387.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 15.Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., Higgins D.G. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis Tools. Nucleic Acids Res. 1997;25:4876–4882. doi: 10.1093/nar/25.24.4876. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 16.Do C.B., Mahabhashyam M.S., Brudno M., Batzoglou S. ProbCons: Probabilistic consistency-based multiple sequence alignment. Genome Res. 2005;15:330–340. doi: 10.1101/gr.2821705. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 17.Castresana J. Selection of conserved blocks from multiple alignments for their use in phylogenetic análisis. Mol. Biol. Evol. 2000;17:540–552. doi: 10.1093/oxfordjournals.molbev.a026334. [DOI] [PubMed] [Google Scholar]
  • 18.Tamura K., Dudley J., Nei M., Kumar S. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 2007;24:1596–1599. doi: 10.1093/molbev/msm092. [DOI] [PubMed] [Google Scholar]
  • 19.Huelsenbeck J.P., Ronquist F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics. 2001;17:754–755. doi: 10.1093/bioinformatics/17.8.754. [DOI] [PubMed] [Google Scholar]
  • 20.Wolfe K.H. Comparative genomics and genome evolution in yeasts. Philos. Trans. R. Soc. Lond. B. Biol Sci. 2006;361:403–412. doi: 10.1098/rstb.2005.1799. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 21.Moriya H., Shimizu-Yoshida Y., Omori A., Iwashita S., Katoh M., Sakai A. Yak1p, a DYRK family kinase, translocates to the nucleus and phosphorylates yeast Pop2p in response to a glucose signal. Genes Dev. 2001;15:1217–1228. doi: 10.1101/gad.884001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 22.Hohmann S. Osmotic stress signaling and osmoadaptation in yeasts. Microbiol. Mol. Biol. Rev. 2002;66:300–372. doi: 10.1128/MMBR.66.2.300-372.2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 23.Scannell D.R., Butler G., Wolfe K.H. Yeast genome evolution-the origin of the species. Yeast. 2007;24:929–942. doi: 10.1002/yea.1515. [DOI] [PubMed] [Google Scholar]
  • 24.Brauer M.J., Saldanha A.J., Dolinski K., Botstein D. Homeostatic adjustment and metabolic remodelling in glucose-limited yeast cultures. Mol. Biol. Cell. 2005;16:2503–2517. doi: 10.1091/mbc.E04-11-0968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 25.de Morgan A., Brodsky L., Ronin Y., Nevo E., Korol A., Kashi Y. Genome-wide analysis of DNA turnover and gene expression in stationaryphase Saccharomyces cerevisiae. Microbiology. 2010;156:1758–1571. doi: 10.1099/mic.0.035519-0. [DOI] [PubMed] [Google Scholar]
  • 26.Bell-Pedersen D., Shinohara M.L., Loros J.J., Dunlap J.C. Circadian clock-controlled genes isolated from Neurospora crassa, are late night-to early morning-specific. Proc. Natl. Acad. Sci. USA. 1996;93:13096–13101. doi: 10.1073/pnas.93.23.13096. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 27.Aign V., Hoheisel J.D. Analysis of nutrient-dependent transcript variations in Neurospora crassa. Fungal Genet. Biol. 2003;40:225–233. doi: 10.1016/S1087-1845(03)00106-3. [DOI] [PubMed] [Google Scholar]
  • 28.Wolfe K.H., Shields D.C. Molecular evidence for an ancient duplication of the entire yeast genome. Nature. 1997;387:708–713. doi: 10.1038/42711. [DOI] [PubMed] [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., Snyder M. Global analysis of protein phosphorylation in yeast. Nature. 2005;7068:679–684. doi: 10.1038/nature04187. [DOI] [PubMed] [Google Scholar]
  • 30.Wu Q., James S.A., Roberts I.N., Moulton V., Huber K.T. Exploring contradictory phylogenetic relationships in yeasts. FEMS Yeast Res. 2008;8:641–650. doi: 10.1111/j.1567-1364.2008.00362.x. [DOI] [PubMed] [Google Scholar]
  • 31.Pan X., Heitman J. Sok2 regulates yeast pseudohyphal differentiation via a transcription factor cascade that regulates cell-cell adhesion. Mol. Cell. Biol. 2000;20:8364–8372. doi: 10.1128/MCB.20.22.8364-8372.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 32.Gasch A.P., Spellman P.T., Kao C.M., Carmel-Harel O., Eisen M.B., Storz G., Botstein D., Brown P.O. Genomic expression programs in the response of yeast cells to environmental changes. Mol. Biol. Cell. 2000;11:4241–4257. doi: 10.1091/mbc.11.12.4241. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 33.Popova Y., Thayumanavan P., Lonati E., Agrochao M., Thevelein J.M. Transport and signaling through the phosphate-binding site of the yeast Pho84 phosphate transceptor. Proc. Natl. Acad. Sci. USA. 2010;107:2890–2895. doi: 10.1073/pnas.0906546107. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 34.Sobering A.K., Jung U.S., Lee K.S., Levin D.E. Yeast Rpi1 is a putative transcriptional regulator that contributes to preparation for stationary phase. Eukaryot. Cell. 2002;1:56–65. doi: 10.1128/EC.1.1.56-65.2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 35.Belli G., Molina M.M., Garcia-Martinez J., Perez-Ortin J.E., 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. 2004;279:12386–12395. doi: 10.1074/jbc.M311879200. [DOI] [PubMed] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

11658_2012_17_MOESM1_ESM.pdf (1.2MB, pdf)

Supplementary material, approximately 1.8 MB.

Articles from Cellular & Molecular Biology Letters are provided here courtesy of BMC

RESOURCES