1887

Microbiology Society logo

Volume 157, Issue 5

KlHsl1 is a component of glycerol response pathways in the milk yeast Free

Abstract

In , () encodes a serine-threonine protein kinase involved in cell cycle control and morphogenesis. Deletion of its putative orthologue in , , gives rise to sensitivity to the respiratory inhibitor antimycin A (AA). Resistance to AA on glucose (Rag phenotype) is associated with genes () required for glucose metabolism/glycolysis. To understand the relationship between and , and Δ mutant strains were investigated. The analysis showed that all the mutants contained a phosphorylated form of Hog1 and displayed an inability to synthesize/accumulate glycerol as a compatible solute. In addition, mutants also showed alterations in both cell wall and membrane fatty acids. The pleiotropic defects of these strains indicate that a common pathway regulates glucose utilization and stress response mechanisms, suggesting impaired adaptation of the plasma membrane/cell wall during the respiratory–fermentative transition. KlHsl1 could be the link between these adaptive pathways and the morphogenetic checkpoint.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
Funding
This study was supported by the:
  • University of Rome – La Sapienza (Award  ‘Ateneo’ 2008)
© 2011 SGM
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.044040-0
2011-05-01
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/micro/157/5/1509.html?itemId=/content/journal/micro/10.1099/mic.0.044040-0&mimeType=html&fmt=ahah

References

  1. Albertyn J., Hohmann S., Thevelein J. M., Prior B. A. ( 1994). GPD1, which encodes glycerol-3-phosphate dehydrogenase, is essential for growth under osmotic stress in Saccharomyces cerevisiae, and its expression is regulated by the high-osmolarity glycerol response pathway. Mol Cell Biol 14:4135–4144[PubMed]
     [Google Scholar]
  2. Ansell R., Granath K., Hohmann S., Thevelein J. M., Adler L. ( 1997). The two isoenzymes for yeast NAD+-dependent glycerol 3-phosphate dehydrogenase encoded by GPD1 and GPD2 have distinct roles in osmoadaptation and redox regulation. EMBO J 16:2179–2187 [View Article][PubMed]
     [Google Scholar]
  3. Bermejo C., Rodríguez E., García R., Rodríguez-Peña J. M., Rodríguez de la Concepción M. L., Rivas C., Arias P., Nombela C., Posas F., Arroyo J. ( 2008). The sequential activation of the yeast HOG and SLT2 pathways is required for cell survival to cell wall stress. Mol Biol Cell 19:1113–1124 [View Article][PubMed]
     [Google Scholar]
  4. Betina S., Goffrini P., Ferrero I., Wésolowski-Louvel M. ( 2001). RAG4 gene encodes a glucose sensor in Kluyveromyces lactis . Genetics 158:541–548[PubMed]
     [Google Scholar]
  5. Bianchi M. M., Tizzani L., Destruelle M., Frontali L., Wésolowski-Louvel M. ( 1996). The ‘petite-negative’ yeast Kluyveromyces lactis has a single gene expressing pyruvate decarboxylase activity. Mol Microbiol 19:27–36 [View Article][PubMed]
     [Google Scholar]
  6. Billard P., Ménart S., Blaisonneau J., Bolotin-Fukuhara M., Fukuhara H., Wésolowski-Louvel M. ( 1996). Glucose uptake in Kluyveromyces lactis: role of the HGT1 gene in glucose transport. J Bacteriol 178:5860–5866[PubMed]
     [Google Scholar]
  7. Björkqvist S., Ansell R., Adler L., Lidén G. ( 1997). Physiological response to anaerobicity of glycerol-3-phosphate dehydrogenase mutants of Saccharomyces cerevisiae . Appl Environ Microbiol 63:128–132[PubMed]
     [Google Scholar]
  8. Blaisonneau J., Fukuhara H., Wésolowski-Louvel M. ( 1997). The Kluyveromyces lactis equivalent of casein kinase I is required for the transcription of the gene encoding the low-affinity glucose permease. Mol Gen Genet 253:469–477 [View Article][PubMed]
     [Google Scholar]
  9. Bligh E. G., Dyer W. J. ( 1959). A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917[PubMed] [CrossRef]
     [Google Scholar]
  10. Blomberg A., Adler L. ( 1992). Physiology of osmotolerance in fungi. Adv Microb Physiol 33:145–212 [View Article][PubMed]
     [Google Scholar]
  11. Booher R. N., Deshaies R. J., Kirschner M. W. ( 1993). Properties of Saccharomyces cerevisiae wee1 and its differential regulation of p34CDC28 in response to G1 and G2 cyclins. EMBO J 12:3417–3426[PubMed]
     [Google Scholar]
  12. Breunig K. D., Bolotin-Fukuhara M., Bianchi M. M., Bourgarel D., Falcone C., Ferrero I. I. I, Frontali L., Goffrini P., Krijger J. J., Mazzoni C. ( 2000). Regulation of primary carbon metabolism in Kluyveromyces lactis . Enzyme Microb Technol 26:771–780 [View Article][PubMed]
     [Google Scholar]
  13. Burton J. L., Solomon M. J. ( 2000). Hsl1p, a Swe1p inhibitor, is degraded via the anaphase-promoting complex. Mol Cell Biol 20:4614–4625 [View Article][PubMed]
     [Google Scholar]
  14. Casey G. P., Ingledew W. M. ( 1986). Ethanol tolerance in yeasts. Crit Rev Microbiol 13:219–280 [View Article][PubMed]
     [Google Scholar]
  15. Clotet J., Escoté X., Adrover M. A., Yaakov G., Garí E., Aldea M., de Nadal E., Posas F. ( 2006). Phosphorylation of Hsl1 by Hog1 leads to a G2 arrest essential for cell survival at high osmolarity. EMBO J 25:2338–2346 [View Article][PubMed]
     [Google Scholar]
  16. De Deken R. H. ( 1966). The Crabtree effect: a regulatory system in yeast. J Gen Microbiol 44:149–156[PubMed] [CrossRef]
     [Google Scholar]
  17. Diaz-Ruiz R., Uribe-Carvajal S., Devin A., Rigoulet M. ( 2009). Tumor cell energy metabolism and its common features with yeast metabolism. Biochim Biophys Acta 1796:252–265[PubMed]
     [Google Scholar]
  18. Gancedo J. M. ( 1998). Yeast carbon catabolite repression. Microbiol Mol Biol Rev 62:334–361[PubMed]
     [Google Scholar]
  19. Goffrini P. ( 2007). A respiratory-deficient mutation associated with high salt sensitivity in Kluyveromyces lactis . FEM Yeast Res 7:180–187 [View Article][PubMed]
     [Google Scholar]
  20. Goffrini P., Algeri A. A., Donnini C., Wésolowski-Louvel M., Ferrero I. ( 1989). RAG1 and RAG2: nuclear genes involved in the dependence/independence on mitochondrial respiratory function for growth on sugars. Yeast 5:99–106 [View Article][PubMed]
     [Google Scholar]
  21. Goffrini P., Wésolowski-Louvel M., Ferrero I. ( 1991). A phosphoglucose isomerase gene is involved in the Rag phenotype of the yeast Kluyveromyces lactis . Mol Gen Genet 228:401–409 [View Article][PubMed]
     [Google Scholar]
  22. González-Siso M. I., Freire-Picos M. A., Ramil E., González-Domínguez M., Rodríguez Torres A., Cerdán M. E. ( 2000). Respirofermentative metabolism in Kluyveromyces lactis: Insights and perspectives. Enzyme Microb Technol 26:699–705 [View Article][PubMed]
     [Google Scholar]
  23. Heipieper H. J., Isken S., Saliola M. ( 2000). Ethanol tolerance and membrane fatty acid adaptation in adh multiple and null mutants of Kluyveromyces lactis . Res Microbiol 151:777–784 [View Article][PubMed]
     [Google Scholar]
  24. Hikkel I., Gbelská Y., van der Aart Q. J., Lubecu G., Subík J. ( 1997). Cloning and characterization of KlCOX18, a gene required for activity of cytochrome oxidase in Kluyveromyces lactis . Curr Genet 32:267–272 [View Article][PubMed]
     [Google Scholar]
  25. Hnatova M., Wésolowski-Louvel M., Dieppois G., Deffaud J., Lemaire M. ( 2008). Characterization of KlGRR1 and SMS1 genes, two new elements of the glucose signaling pathway of Kluyveromyces lactis . Eukaryot Cell 7:1299–1308 [View Article][PubMed]
     [Google Scholar]
  26. Hohmann S. ( 2002). Osmotic stress signaling and osmoadaptation in yeasts. Microbiol Mol Biol Rev 66:300–372 [View Article][PubMed]
     [Google Scholar]
  27. Hohmann S. ( 2009). Control of high osmolarity signalling in the yeast Saccharomyces cerevisiae . FEBS Lett 583:4025–4029 [View Article][PubMed]
     [Google Scholar]
  28. Jones R. P., Greenfield P. F. ( 1987). Ethanol and the fluidity of the yeast plasma membrane. Yeast 3:223–232 [View Article][PubMed]
     [Google Scholar]
  29. Kirchrath L., Lorberg A., Schmitz H. P., Gengenbacher U., Heinisch J. J. ( 2000). Comparative genetic and physiological studies of the MAP kinase Mpk1p from Kluyveromyces lactis and Saccharomyces cerevisiae . J Mol Biol 300:743–758 [View Article][PubMed]
     [Google Scholar]
  30. Klipp E., Nordlander B., Krüger R., Gennemark P., Hohmann S. ( 2005). Integrative model of the response of yeast to osmotic shock. Nat Biotechnol 23:975–982 [View Article][PubMed]
     [Google Scholar]
  31. Lemaire M., Wésolowski-Louvel M. ( 2004). Enolase and glycolytic flux play a role in the regulation of the glucose permease gene RAG1 of Kluyveromyces lactis . Genetics 168:723–731 [View Article][PubMed]
     [Google Scholar]
  32. Lew D. J. ( 2003). The morphogenesis checkpoint: how yeast cells watch their figures. Curr Opin Cell Biol 15:648–653 [View Article][PubMed]
     [Google Scholar]
  33. Ma X.-J., Lu Q., Grunstein M. ( 1996). A search for proteins that interact genetically with histone H3 and H4 amino termini uncovers novel regulators of the Swe1 kinase in Saccharomyces cerevisiae . Genes Dev 10:1327–1340 [View Article][PubMed]
     [Google Scholar]
  34. McMillan J. N., Longtine M. S., Sia R. A. L., Theesfeld C. L., Bardes E. S., Pringle J. R., Lew D. J. ( 1999). The morphogenesis checkpoint in Saccharomyces cerevisiae: cell cycle control of Swe1p degradation by Hsl1p and Hsl7p. Mol Cell Biol 19:6929–6939[PubMed]
     [Google Scholar]
  35. Neil H., Lemaire M., Wésolowski-Louvel M. ( 2004). Regulation of glycolysis in Kluyveromyces lactis: role of KlGCR1 and KlGCR2 in glucose uptake and catabolism. Curr Genet 45:129–139 [View Article][PubMed]
     [Google Scholar]
  36. Overkamp K. M., Bakker B. M., Steensma H. Y., van Dijken J. P., Pronk J. T. ( 2002). Two mechanisms for oxidation of cytosolic NADPH by Kluyveromyces lactis mitochondria. Yeast 19:813–824 [View Article][PubMed]
     [Google Scholar]
  37. Parks L. W., Smith S. J., Crowley J. H. ( 1995). Biochemical and physiological effects of sterol alterations in yeast – a review. Lipids 30:227–230 [View Article][PubMed]
     [Google Scholar]
  38. Popolo L., Gualtieri T., Ragni E. ( 2001). The yeast cell-wall salvage pathway. Med Mycol 39:Suppl. 1111–121[PubMed] [CrossRef]
     [Google Scholar]
  39. Prentki M., Madiraju S. R. M. ( 2008). Glycerolipid metabolism and signaling in health and disease. Endocr Rev 29:647–676 [View Article][PubMed]
     [Google Scholar]
  40. Prior C., Mamessier P., Fukuhara H., Chen X. J., Wésolowski-Louvel M. ( 1993). The hexokinase gene is required for transcriptional regulation of the glucose transporter gene RAG1 in Kluyveromyces lactis . Mol Cell Biol 13:3882–3889[PubMed]
     [Google Scholar]
  41. Prior C., Tizzani L., Fukuhara H., Wésolowski-Louvel M. ( 1996). RAG3 gene and transcriptional regulation of the pyruvate decarboxylase gene in Kluyveromyces lactis . Mol Microbiol 20:765–772 [View Article][PubMed]
     [Google Scholar]
  42. Ptacek J., Devgan G., Michaud G., Zhu H., Zhu X., Fasolo J., Guo H., Jona G., Breitkreutz A. et al. ( 2005). Global analysis of protein phosphorylation in yeast. Nature 438:679–684 [View Article][PubMed]
     [Google Scholar]
  43. Rodicio R., Buchwald U., Schmitz H. P., Heinisch J. J. ( 2008). Dissecting sensor functions in cell wall integrity signaling in Kluyveromyces lactis . Fungal Genet Biol 45:422–435 [View Article][PubMed]
     [Google Scholar]
  44. Rubenstein E. M., Schmidt M. C. ( 2007). Mechanisms regulating the protein kinases of Saccharomyces cerevisiae . Eukaryot Cell 6:571–583 [View Article][PubMed]
     [Google Scholar]
  45. Serrano R., Marquez J. A., Rios G. ( 1997). Crucial factors in salt stress tolerance.. Yeast Stress Response147–170 Hohmann S., Mager W. H. New York: Springer;
     [Google Scholar]
  46. Sia R. A. L., Bardes E. S. G., Lew D. J. ( 1998). Control of Swe1p degradation by the morphogenesis checkpoint. EMBO J 17:6678–6688 [View Article][PubMed]
     [Google Scholar]
  47. Steensma H. Y., Ter Linde J. J. ( 2001). Plasmids with the Cre-recombinase and the dominant nat marker, suitable for use in prototrophic strains of Saccharomyces cerevisiae and Kluyveromyces lactis . Yeast 18:469–472 [View Article][PubMed]
     [Google Scholar]
  48. Tamás M. J., Luyten K., Sutherland F. C. W., Hernandez A., Albertyn J., Valadi H., Li H., Prior B. A., Kilian S. G. et al. ( 1999). Fps1p controls the accumulation and release of the compatible solute glycerol in yeast osmoregulation. Mol Microbiol 31:1087–1104 [View Article][PubMed]
     [Google Scholar]
  49. Tamás M. J., Karlgren S., Bill R. M., Hedfalk K., Allegri L., Ferreira M., Thevelein J. M., Rydström J., Mullins J. G. L., Hohmann S. ( 2003). A short regulatory domain restricts glycerol transport through yeast Fps1p. J Biol Chem 278:6337–6345 [View Article][PubMed]
     [Google Scholar]
  50. Tanaka S., Nojima H. ( 1996). Nik1: a Nim1-like protein kinase of S. cerevisiae interacts with the Cdc28 complex and regulates cell cycle progression. Genes Cells 1:905–921 [View Article][PubMed]
     [Google Scholar]
  51. Uccelletti D., Mancini P., Farina F., Morrone S., Palleschi C. ( 1999). Inactivation of the KIPMR1 gene of Kluyveromyces lactis results in defective cell-wall morphogenesis. Microbiology 145:1079–1087 [View Article][PubMed]
     [Google Scholar]
  52. Uccelletti D., Pacelli V., Mancini P., Palleschi C. ( 2000). vga mutants of Kluyveromyces lactis show cell integrity defects. Yeast 16:1161–1171 [View Article][PubMed]
     [Google Scholar]
  53. van Dijken J. P., Scheffers W. A. ( 1986). Redox balances in the metabolism of sugars by yeast. FEMS Microbiol Letts 32:199–224 [CrossRef]
     [Google Scholar]
  54. Wésolowski–Louvel M., Prior C., Bornecque D., Fukuhara H. ( 1992a). Rag− mutations involved in glucose metabolism in yeast: isolation and genetic characterization. Yeast 8:711–719 [View Article]
     [Google Scholar]
  55. Wésolowski-Louvel M., Goffrini P., Ferrero I., Fukuhara H. ( 1992b). Glucose transport in the yeast Kluyveromyces lactis. I. Properties of an inducible low-affinity glucose transporter gene. Mol Gen Genet 233:89–96[PubMed] [CrossRef]
     [Google Scholar]
  56. Yazawa H., Iwahashi H., Kamisaka Y., Kimura K., Uemura H. ( 2009). Production of polyunsaturated fatty acids in yeast Saccharomyces cerevisiae and its relation to alkaline pH tolerance. Yeast 26:167–184 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.044040-0
Loading
KlHsl1 is a component of glycerol response pathways in the milk yeast Kluyveromyces lactis
Microbiology 157, 1509 (2011); https://doi.org/10.1099/mic.0.044040-0
/content/journal/micro/10.1099/mic.0.044040-0
/content/journal/micro/10.1099/mic.0.044040-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error