Molecular Genetics and Genomics

, Volume 276, Issue 2, pp 170–186 | Cite as

Transcriptome profiling of Saccharomyces cerevisiae during a transition from fermentative to glycerol-based respiratory growth reveals extensive metabolic and structural remodeling

  • George G. Roberts
  • Alan P. HudsonEmail author
Original Paper


Transcriptome analyses using a wild-type strain of Saccharomyces cerevisiae were performed to assess the overall pattern of gene expression during the transition from glucose-based fermentative to glycerol-based respiratory growth. These experiments revealed a complex suite of metabolic and structural changes associated with the adaptation process. Alterations in gene expression leading to remodeling of various membrane transport systems and the cortical actin cytoskeleton were observed. Transition to respiratory growth was accompanied by alterations in transcript patterns demonstrating not only a general stress response, as seen in earlier studies, but also the oxidative and osmotic stress responses. In some contrast to earlier studies, these experiments identified modulation of expression for many genes specifying transcription factors during the transition to glycerol-based growth. Importantly and unexpectedly, an ordered series of changes was seen in transcript levels from genes encoding components of the TFIID, SAGA (Spt-Ada-Gcn5-Acetyltransferase), and SLIK (Saga LIKe) complexes and all three RNA polymerases, suggesting a modulation of structure for the basal transcriptional machinery during adaptation to respiratory growth. In concert with data given in earlier studies, the results presented here highlight important aspects of metabolic and other adaptations to respiratory growth in yeast that are common to utilization of multiple carbon sources. Importantly, they also identify aspects specific to adaptation of this organism to growth on glycerol as sole carbon source.


Respiratory growth Metabolic reprograming Metabolic shift Environmental adaptation Saccharomyces cerevisiae Microarray analysis 



This work was supported by a grant from Department of Veterans Affairs Medical Research Service to APH. We are grateful to Prof. Craig N. Giroux (Wayne State University) for many helpful discussions. We also thank Annette Thelen of the Michigan State University Genomics Technology Support Facility for her expert assistance in performing the RNA fragmentation, microarray hybridizations, and flagging expression values with MAS 5.0.


  1. Affymetrix (2000) Affymetrix GeneChip expression analysis technical manual. Santa Clara, CAGoogle Scholar
  2. Backhus L, DeRisi J, Brown PO, Bisson L (2001) Functional genomic analysis of a commercial wine strain of Saccharomyces cerevisiae under differing nitrogen conditions. FEMS Yeast Res 1:111–125PubMedCrossRefGoogle Scholar
  3. Boorsma A, Bussemaker H (2005) T-Profiler; a web-tool to infer transcriptional module activity from gene expression data. Nucleic Acid Res 33:W592–W595PubMedCrossRefGoogle Scholar
  4. Brauer MJ, Saldanha AJ, Dolinski K, Botstein D (2005) Homeostatic adjustment and metabolic remodeling in glucose-limited yeast cultures. Mol Biol Cell 16:2503–2517PubMedCrossRefGoogle Scholar
  5. Carlson M (1999) Glucose repression in yeast. Curr Opin Microbiol 2:202–207PubMedCrossRefGoogle Scholar
  6. DeRisi JL, Iyer VR, Brown PO (1997) Exploring the metabolic and genetic control of gene expression on a genomic scale. Science 278:680–686PubMedCrossRefGoogle Scholar
  7. Ferreira C, van Voorst F, Martins A, Neves L, Oliveira R, Kielland-Brandt MC, Lucas C, Brandt A (2005) A member of the sugar transporter family, Stl1p is the glycerol/H+ symporter in Saccharomyces cerevisiae. Mol Biol Cell 16:2068–2076PubMedCrossRefGoogle Scholar
  8. Gancedo JM (1998) Yeast carbon catabolite repression. Microbiol Mol Biol Rev 62:334–361PubMedGoogle Scholar
  9. Gasch AP, Spellman PT, Kao CM, Carmel-Harel O, Eisen MB, Storz G, Botstein D, Brown PO (2000) Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 11:4241–4257PubMedGoogle Scholar
  10. Jazwinski SM (2005) The retrograde response links metabolism with stress responses, chromatin-dependent gene activation, and genome stability in yeast aging. Gene 354:22–27PubMedCrossRefGoogle Scholar
  11. Larsson C, Pahlman IL, Ansell R, Rigoulet M, Adler L, Gustafsson L (1998) The importance of the glycerol-3-phosphate shuttle during aerobic growth of Saccharomyces cerevisiae. Yeast 14:347–357PubMedCrossRefGoogle Scholar
  12. Lu L, Roberts GR, Oszust C, Hudson AP (2005) The YJR127C/ZMS1 gene product is involved in glycerol-based respiratory growth of the yeast Saccharomyces cerevisiae. Curr Genet 48:235–246PubMedCrossRefGoogle Scholar
  13. McEntee CM, Hudson AP (1989) Preparation of RNA from unspheroplasted yeast cells (Saccharomyces cerevisiae). Anal Biochem 176:303–306PubMedCrossRefGoogle Scholar
  14. Ohlmeier S, Kastaniotis J, Hiltunen JK, Bergmann U (2004) The yeast mitochondrial proteome, a study of fermentative and respiratory growth 279:3956–3979Google Scholar
  15. Pavlik P, Simon M, Schuster T, Ruis H (1993) The glycerol kinase (GUT1) gene of Saccharomyces cerevisiae: cloning and characterization. Curr Genet 24:21–25PubMedCrossRefGoogle Scholar
  16. Rønnow B and Kielland-Brandt MC (1993) GUT2, a gene for mitochondrial glycerol 3-phosphate dehydrogenase of Saccharomyces cerevisiae. Yeast 9:1121–1130PubMedCrossRefGoogle Scholar
  17. Rep M, Krantz M, Thevelein JM, Hohmann S (2000) The transcriptional response of Saccharomyces cerevisiae to osmotic shock. Hot1p and Msn2p/Msn4p are required for the induction of subsets of high osmolarity glycerol pathway-dependent genes. J Biol Chem 275:8290–8300PubMedCrossRefGoogle Scholar
  18. Rolland F, Winderickx J, Thevelein JM (2002) Glucose-sensing and -signaling mechanisms in yeast. FEMS Yeast Res 2:185–201Google Scholar
  19. Sambrook D, Russell DW (eds) (2001) Molecular cloning: a laboratory manual. CSHL Press, Cold Spring Harbor, New York, pp 7.31–7.34Google Scholar
  20. Schüller HJ (2003) Transcriptional control of nonfermentative metabolism in the yeast Saccharomyces cerevisiae. Curr Genet 43:139–160PubMedGoogle Scholar
  21. Sherman F (2002) Getting started with yeast. In: Guthrie C, Fink GR (eds) Guide to yeast genetics and molecular biology. Meth Enzymol, vol 350. Academic Press, San Diego, pp 3–41Google Scholar
  22. ter Linde JJ, Liang H, Davis W, Steensma HY, van Dijken JP, Pronk JT (1999) Genome-wide transcriptional analysis of aerobic and anaerobic chemostat cultures of Saccharomyces cerevisiae. J Bacteriol 181:7409–7413PubMedGoogle Scholar
  23. Uesono Y, Ashe M, Toh-e A (2004) Simultaneous yet independent regulation of actin cytoskeletal organization and translation initiation by glucose in Saccharomyces cerevisiae. Mol Biol Cell 15:1544–1556PubMedCrossRefGoogle Scholar
  24. Valadi A, Granath K, Gustafsson L, Adler L (2004) Distinct intracellular localization of Gpd1p and Gpd2p, the two yeast isoforms of NAD+-dependent glycerol-3-phosphate dehydrogenase, explains their different contributions to redox-driven glycerol production. J Biol Chem 279:39677–39685PubMedCrossRefGoogle Scholar
  25. Zakrzewska A, Boorsma A, Brul S, Hellingwerf KJ, Klis F (2005) Transcriptional response of Saccharomyces cerevisiae to the plasma membrane-perturbing compound chitosan. Eukar Cell 4:703–715CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  1. 1.Department Immunology and MicrobiologyWayne State University School of MedicineDetroitUSA
  2. 2.Department of Veterans Affairs Medical CenterMedical Research ServiceDetroitUSA

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