Disruption of yarrowia lipolytica TPS1 gene encoding trehalose-6-P synthase does not affect growth in glucose but impairs growth at high temperature

PLoS ONE

Volumn 6, Issue 9, 2011, Pages

  Flores, Carmen Lisset ^a   Gancedo, Carlos ^a   Petit, Thomas ^b  

^a INSTITUTO DE INVESTIGACIONES BIOMÉDICAS ALBERTO SOLS   (Spain)

^b UNIVERSITÉ DE LA RÉUNION   (France)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOKINASE; GLUCOSE; HEXOKINASE; MESSENGER RNA; PROTEIN KINASE; PROTEIN MCK1; SYNTHETASE; TREHALASE; TREHALOSE 6 PHOSPHATE SYNTHETASE; UNCLASSIFIED DRUG; GLUCOSYLTRANSFERASE; TREHALOSE; TREHALOSE-6-PHOSPHATE SYNTHASE;

ARTICLE; CONTROLLED STUDY; DIPLOIDY; DRY WEIGHT; ENZYME INHIBITION; ESSENTIAL GENE; FUNGAL GENE; FUNGAL STRAIN; FUNGUS GROWTH; FUNGUS MUTANT; GENE DISRUPTION; GENE EXPRESSION REGULATION; GENETIC COMPLEMENTATION; HEAT STRESS; HEAT TREATMENT; HIGH TEMPERATURE; HOMOZYGOTE; MEIOSIS; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PHOSPHORYLATION; PROMOTER REGION; SEQUENCE HOMOLOGY; SPOROGENESIS; TPS1 GENE; TPS2 GENE; TPS3 GENE; YARROWIA LIPOLYTICA; CHROMOSOME; DRUG EFFECT; FUNGUS SPORE; GENETICS; GROWTH, DEVELOPMENT AND AGING; HEAT SHOCK RESPONSE; METABOLISM; MOLECULAR GENETICS; MUTATION; PHYSIOLOGY; TEMPERATURE; YARROWIA;

SACCHAROMYCES CEREVISIAE; YARROWIA LIPOLYTICA;

CHROMOSOMES, FUNGAL; CLONING, MOLECULAR; GLUCOSE; GLUCOSYLTRANSFERASES; HEAT-SHOCK RESPONSE; MOLECULAR SEQUENCE DATA; MUTATION; SPORES, FUNGAL; TEMPERATURE; TREHALASE; TREHALOSE; YARROWIA;

EID: 80052617547     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0023695     Document Type: Article

References (90)

1. Elbein AD, Pan YT, Pastuszak I, Carroll D, (2003) New insights on trehalose: a multifunctional molecule. Glycobiology 13: 17-27.
2. Gancedo C, Flores CL, (2004) The importance of a functional trehalose biosynthetic pathway for the life of yeasts and fungi. FEMS Yeast Res 4: 351-359.
3. Cabib E, Leloir LF, (1958) The biosyntesis of trehalose phosphate. J Biol Chem 231: 259-275.
4. Bell W, Klaassen P, Ohnacker M, Boller T, Herweijer M, et al. (1992) Characterization of the 56-kDa subunit of yeast trehalose-6-phosphate synthase and cloning of its gene reveal its identity with the product of CIF1, a regulator of carbon catabolite inactivation. Eur J Biochem 209: 951-959.
5. De Virgilio C, Burckert N, Bell W, Jeno P, Boller T, et al. (1993) Disruption of TPS2, the gene encoding the 100-kDa subunit of the trehalose-6-phosphate synthase/phosphatase complex in Saccharomyces cerevisiae, causes accumulation of trehalose-6-phosphate and loss of trehalose-6-phosphate phosphatase activity. Eur J Biochem 212: 315-323.
6. Reinders A, Burckert N, Hohmann S, Thevelein JM, Boller T, et al. (1997) Structural analysis of the subunits of the trehalose-6-phosphate synthase/phosphatase complex in Saccharomyces cerevisiae and their function during heat shock. Mol Microbiol 24: 687-695.
7. Chen Q, Haddad GG, (2004) Role of trehalose phosphate synthase and trehalose during hypoxia: from flies to mammals. J Exp Biol 207: 3125-3129.
8. Kormish JD, McGhee JD, (2005) The C. elegans lethal gut-obstructed gob-1 gene is trehalose-6-phosphate phosphatase. Dev Biol 287: 35-47.
9. Paul MJ, Primavesi LF, Jhurreea D, Zhang Y, (2008) Trehalose metabolism and signaling. Annu Rev Plant Biol 59: 417-441.
10. Gonzalez MI, Stucka R, Blazquez MA, Feldmann H, Gancedo C, (1992) Molecular cloning of CIF1, a yeast gene necessary for growth on glucose. Yeast 8: 183-192.
11. Luyten K, de Koning W, Tesseur I, Ruiz MC, Ramos J, et al. (1993) Disruption of the Kluyveromyces lactis GGS1 gene causes inability to grow on glucose and fructose and is suppressed by mutations that reduce sugar uptake. Eur J Biochem 217: 701-713.
12. Blazquez MA, Lagunas R, Gancedo C, Gancedo JM, (1993) Trehalose-6-phosphate, a new regulator of yeast glycolysis that inhibits hexokinases. FEBS Lett 329: 51-54.
13. Teusink B, Walsh MC, van Dam K, Westerhoff HV, (1998) The danger of metabolic pathways with turbo design. Trends Biochem Sci 23: 162-169.
14. Reinders A, Romano I, Wiemken A, De Virgilio C, (1999) The thermophilic yeast Hansenula polymorpha does not require trehalose synthesis for growth at high temperatures but does for normal acquisition of thermotolerance. J Bacteriol 181: 4665-4668.
15. Petit T, Gancedo C, (1999) Molecular cloning and characterization of the gene HXK1 encoding the hexokinase from Yarrowia lipolytica. Yeast 15: 1573-1584.
16. Dujon B, (2006) Yeasts illustrate the molecular mechanisms of eukaryotic genome evolution. Trends Genet 22: 375-387.
17. Morin M, Monteoliva L, Insenser M, Gil C, Dominguez A, (2007) Proteomic analysis reveals metabolic changes during yeast to hypha transition in Yarrowia lipolytica. J Mass Spectrom 42: 1453-1462.
18. Holz M, Forster A, Mauersberger S, Barth G, (2009) Aconitase overexpression changes the product ratio of citric acid production by Yarrowia lipolytica. Appl Microbiol Biotechnol 81: 1087-1096.
19. Kamzolova SV, Shishkanova NV, Morgunov IG, Finogenova TV, (2003) Oxygen requirements for growth and citric acid production of Yarrowia lipolytica. FEMS Yeast Res 3: 217-222.
20. Madzak C, Gaillardin C, Beckerich JM, (2004) Heterologous protein expression and secretion in the non-conventional yeast Yarrowia lipolytica: a review. J Biotechnol 109: 63-81.
21. Beopoulos A, Cescut J, Haddouche R, Uribelarrea JL, Molina-Jouve C, et al. (2009) Yarrowia lipolytica as a model for bio-oil production. Prog Lipid Res 48: 375-387.
22. Sakai Y, Oku M, van der Klei IJ, Kiel JA, (2006) Pexophagy: autophagic degradation of peroxisomes. Biochim Biophys Acta 1763: 1767-1775.
23. Flores CL, Martinez-Costa OH, Sanchez V, Gancedo C, Aragon JJ, (2005) The dimorphic yeast Yarrowia lipolytica possesses an atypical phosphofructokinase: characterization of the enzyme and its encoding gene. Microbiology 151: 1465-1474.
24. Hirai M, Tanaka A, Fukui S, (1975) Difference in pyruvate kinase regulation among three groups of yeasts. Biochim Biophys Acta 391: 282-291.
25. Le Dall M, Nicaud J, Treton BY, Gaillardin CM, (1996) The 3-phosphoglycerate kinase gene of the yeast Yarrowia lipolytica de-represses on gluconeogenic substrates. Curr Genet 29: 446-456.
26. Flores CL, Gancedo C, (2005) Yarrowia lipolytica mutants devoid of pyruvate carboxylase activity show an unusual growth phenotype. Eukaryot Cell 4: 356-364.
27. Jardon R, Gancedo C, Flores CL, (2008) The gluconeogenic enzyme fructose-1,6-bisphosphatase is dispensable for growth of the yeast Yarrowia lipolytica in gluconeogenic substrates. Eukaryot Cell 7: 1742-1749.
28. Arisan-Atac I, Wolschek MF, Kubicek CP, (1996) Trehalose-6-phosphate synthase A affects citrate accumulation by Aspergillus niger under conditions of high glycolytic flux. FEMS Microbiol Lett 140: 77-83.
29. Wolschek M, Kubicek CP, (1998) Biochemistry of citric acid accumulation by Aspergillus niger. In: Kristiansen B, Linden J, Mattey M, editors. Citric acid biotechnology London Taylor and Francis pp. 11-33.
30. Gaillardin CM, Charoy V, Heslot H, (1973) A study of copulation, sporulation and meiotic segregation in Candida lipolytica. Arch Mikrobiol 92: 69-83.
31. Yarrow D, (1998) Methods for the isolation maintenance and identification of yeasts. In: Kurtzman CP, Fell JW, editors. The yeasts: A taxonomic study New York Elsevier pp. 77-100.
32. Lopez MC, Nicaud JM, Skinner HB, Vergnolle C, Kader JC, et al. (1994) A phosphatidylinositol/phosphatidylcholine transfer protein is required for differentiation of the dimorphic yeast Yarrowia lipolytica from the yeast to the mycelial form. J Cell Biol 125: 113-127.
33. Nuttley WM, Brade AM, Eitzen GA, Glover JR, Aitchison JD, et al. (1993) Rapid identification and characterization of peroxisomal assembly mutants in Yarrowia lipolytica. Yeast 9: 507-517.
34. Barth G, Gaillardin C, (1996) Yarrowia lipolytica. In: Wolf K, editors. Nonconventional yeasts in biotechnology Berlin Heidelberg New York Springer pp. 313-388.
35. Ito H, Fukuda Y, Murata K, Kimura A, (1983) Transformation of intact yeast cells treated with alkali cations. J Bacteriol 153: 163-168.
36. Navas MA, Cerdan S, Gancedo JM, (1993) Futile cycles in Saccharomyces cerevisiae strains expressing the gluconeogenic enzymes during growth on glucose. Proc Natl Acad Sci U S A 90: 1290-1294.
37. Sikorski RS, Hieter P, (1989) A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122: 19-27.
38. Becker DM, Fikes JD, Guarente L, (1991) A cDNA encoding a human CCAAT-binding protein cloned by functional complementation in yeast. Proc Natl Acad Sci U S A 88: 1968-1972.
39. Blanchin-Roland S, Cordero Otero RR, Gaillardin C, (1994) Two upstream activation sequences control the expression of the XPR2 gene in the yeast Yarrowia lipolytica. Mol Cell Biol 14: 327-338.
40. Wang H, Le Clainche A, Le Dall MT, Wache Y, Pagot Y, et al. (1998) Cloning and characterization of the peroxisomal acyl CoA oxidase ACO3 gene from the alkane-utilizing yeast Yarrowia lipolytica. Yeast 14: 1373-1386.
41. Gaillardin C, Ribet AM, (1987) LEU2 directed expression of beta-galactosidase activity and phleomycin resistance in Yarrowia lipolytica. Curr Genet 11: 369-375.
42. Sherman DJ, Martin T, Nikolski M, Cayla C, Souciet JL, et al. (2009) Genolevures: protein families and synteny among complete hemiascomycetous yeast proteomes and genomes. Nucleic Acids Res 37: D550-554.
43. Belinchon MM, Flores CL, Gancedo JM, (2004) Sampling Saccharomyces cerevisiae cells by rapid filtration improves the yield of mRNAs. FEMS Yeast Res 4: 751-756.
44. Wallenfels K, (1962) [23] [beta]-Galactosidase (crystalline). In: Sidney PC, Nathan OK, editors. Methods in Enzymology Academic Press pp. 212-219.
45. Kienle I, Burgert M, Holzer H, (1993) Assay of trehalose with acid trehalase purified from Saccharomyces cerevisiae. Yeast 9: 607-611.
46. Gamo FJ, Portillo F, Gancedo C, (1993) Characterization of mutations that overcome the toxic effect of glucose on phosphoglucose isomerase less strains of Saccharomyces cerevisiae. FEMS Microbiol Lett 106: 233-237.
47. Bergmeyer HU, Bergmeyer J, Grassi M, (1987) Methods of enzymatic analysis. In: Bergmeyer HU, editors. Verlag Chemie.
48. Conway EJ, Downey M, (1950) An outer metabolic region of the yeast cell. Biochem J 47: 347-355.
49. Thevelein JM, Hohmann S, (1995) Trehalose synthase: guard to the gate of glycolysis in yeast? Trends Biochem Sci 20: 3-10.
50. Kobayashi N, McEntee K, (1993) Identification of cis and trans components of a novel heat shock stress regulatory pathway in Saccharomyces cerevisiae. Mol Cell Biol 13: 248-256.
51. Bulman AL, Hubl ST, Nelson HC, (2001) The DNA-binding domain of yeast heat shock transcription factor independently regulates both the N- and C-terminal activation domains. J Biol Chem 276: 40254-40262.
52. Conlin LK, Nelson HC, (2007) The natural osmolyte trehalose is a positive regulator of the heat-induced activity of yeast heat shock transcription factor. Mol Cell Biol 27: 1505-1515.
53. Marchler G, Schuller C, Adam G, Ruis H, (1993) A Saccharomyces cerevisiae UAS element controlled by protein kinase A activates transcription in response to a variety of stress conditions. EMBO J 12: 1997-2003.
54. Moradas-Ferreira P, Costa V, Piper P, Mager W, (1996) The molecular defences against reactive oxygen species in yeast. Mol Microbiol 19: 651-658.
55. Gancedo JM, Clifton D, Fraenkel DG, (1977) Yeast hexokinase mutants. J Biol Chem 252: 4443-4444.
56. Herrero P, Galindez J, Ruiz N, Martinez-Campa C, Moreno F, (1995) Transcriptional regulation of the Saccharomyces cerevisiae HXK1, HXK2 and GLK1 genes. Yeast 11: 137-144.
57. Swanson RN, Conesa C, Lefebvre O, Carles C, Ruet A, et al. (1991) Isolation of TFC1, a gene encoding one of two DNA-binding subunits of yeast transcription factor tau (TFIIIC). Proc Natl Acad Sci U S A 88: 4887-4891.
58. Huang Y, Hamada M, Maraia RJ, (2000) Isolation and cloning of four subunits of a fission yeast TFIIIC complex that includes an ortholog of the human regulatory protein TFIIICbeta. J Biol Chem 275: 31480-31487.
59. Goddijn OJ, Verwoerd TC, Voogd E, Krutwagen RW, de Graaf PT, et al. (1997) Inhibition of trehalase activity enhances trehalose accumulation in transgenic plants. Plant Physiol 113: 181-190.
60. Müller J, Aeschbacher RA, Wingler A, Boller T, Wiemken A, (2001) Trehalose and trehalase in Arabidopsis. Plant Physiol 125: 1086-1093.
61. Müller J, Boller T, Wiemken A, (1995) Effects of validamycin A, a potent trehalase inhibitor, and phytohormones on trehalose metabolism in roots and root nodules of soybean and cowpea. Planta 197: 362-368.
62. Arguelles JC, (1997) Thermotolerance and trehalose accumulation induced by heat shock in yeast cells of Candida albicans. FEMS Microbiol Lett 146: 65-71.
63. Kandror O, Bretschneider N, Kreydin E, Cavalieri D, Goldberg AL, (2004) Yeast adapt to near-freezing temperatures by STRE/Msn2,4-dependent induction of trehalose synthesis and certain molecular chaperones. Mol Cell 13: 771-781.
64. Martinez-Pastor MT, Marchler G, Schuller C, Marchler-Bauer A, Ruis H, et al. (1996) The Saccharomyces cerevisiae zinc finger proteins Msn2p and Msn4p are required for transcriptional induction through the stress response element (STRE). EMBO J 15: 2227-2235.
65. Ye Y, Zhu Y, Pan L, Li L, Wang X, et al. (2009) Gaining insight into the response logic of Saccharomyces cerevisiae to heat shock by combining expression profiles with metabolic pathways. Biochem Biophys Res Commun 385: 357-362.
66. Hurtado CA, Rachubinski RA, (1999) MHY1 encodes a C2H2-type zinc finger protein that promotes dimorphic transition in the yeast Yarrowia lipolytica. J Bacteriol 181: 3051-3057.
67. Neves MJ, Hohmann S, Bell W, Dumortier F, Luyten K, et al. (1995) Control of glucose influx into glycolysis and pleiotropic effects studied in different isogenic sets of Saccharomyces cerevisiae mutants in trehalose biosynthesis. Curr Genet 27: 110-122.
68. De Silva-Udawatta MN, Cannon JF, (2001) Roles of trehalose phosphate synthase in yeast glycogen metabolism and sporulation. Mol Microbiol 40: 1345-1356.
69. Wolschek MF, Kubicek CP, (1997) The filamentous fungus Aspergillus niger contains two "differentially regulated" trehalose-6-phosphate synthase-encoding genes, tpsA and tpsB. J Biol Chem 272: 2729-2735.
70. Al-Bader N, Vanier G, Liu H, Gravelat FN, Urb M, et al. (2010) Role of trehalose biosynthesis in Aspergillus fumigatus development, stress response, and virulence. Infect Immun 78: 3007-3018.
71. Adachi N, Lieber MR, (2002) Bidirectional gene organization: a common architectural feature of the human genome. Cell 109: 807-809.
72. Davila Lopez M, Martinez Guerra JJ, Samuelsson T, (2010) Analysis of gene order conservation in eukaryotes identifies transcriptionally and functionally linked genes. PLoS One 5: e10654.
73. Tzvetkov M, Klopprogge C, Zelder O, Liebl W, (2003) Genetic dissection of trehalose biosynthesis in Corynebacterium glutamicum: inactivation of trehalose production leads to impaired growth and an altered cell wall lipid composition. Microbiology 149: 1659-1673.
74. Eastmond PJ, van Dijken AJ, Spielman M, Kerr A, Tissier AF, et al. (2002) Trehalose-6-phosphate synthase 1, which catalyses the first step in trehalose synthesis, is essential for Arabidopsis embryo maturation. Plant J 29: 225-235.
75. Petit T, Blazquez MA, Gancedo C, (1996) Schizosaccharomyces pombe possesses an unusual and a conventional hexokinase: biochemical and molecular characterization of both hexokinases. FEBS Lett 378: 185-189.
76. Blazquez MA, Stucka R, Feldmann H, Gancedo C, (1994) Trehalose-6-P synthase is dispensable for growth on glucose but not for spore germination in Schizosaccharomyces pombe. J Bacteriol 176: 3895-3902.
77. Kramarenko T, Karp H, Jarviste A, Alamae T, (2000) Sugar repression in the methylotrophic yeast Hansenula polymorpha studied by using hexokinase-negative, glucokinase-negative and double kinase-negative mutants. Folia Microbiol (Praha) 45: 521-529.
78. Fillinger S, Chaveroche MK, van Dijck P, de Vries R, Ruijter G, et al. (2001) Trehalose is required for the acquisition of tolerance to a variety of stresses in the filamentous fungus Aspergillus nidulans. Microbiology 147: 1851-1862.
79. Wilson JE, (2003) Isozymes of mammalian hexokinase: structure, subcellular localization and metabolic function. J Exp Biol 206: 2049-2057.
80. Van Aelst L, Hohmann S, Bulaya B, de Koning W, Sierkstra L, et al. (1993) Molecular cloning of a gene involved in glucose sensing in the yeast Saccharomyces cerevisiae. Mol Microbiol 8: 927-943.
81. Lin X, Heitman J, (2005) Chlamydospore formation during hyphal growth in Cryptococcus neoformans. Eukaryot Cell 4: 1746-1754.
82. Lowe RG, Lord M, Rybak K, Trengove RD, Oliver RP, et al. (2009) Trehalose biosynthesis is involved in sporulation of Stagonospora nodorum. Fungal Genet Biol 46: 381-389.
83. Kretschmer A, Wagner F, (1983) Characterization of biosynthetic intermediates of trehalose dicorynomycolate from Rhodococcus erithropolis grown on n-alcanes. Biochim Biophys Acta 753: 306-313.
84. Vergne I, Daffe M, (1998) Interaction of mycobacterial glycolipids with host cells. Front Biosci 3: d865-876.
85. Amaral PF, Lehocky M, Barros-Timmons AM, Rocha-Leao MH, Coelho MA, et al. (2006) Cell surface characterization of Yarrowia lipolytica IMUFRJ 50682. Yeast 23: 867-877.
86. Castells-Roca L, Garcia-Martinez J, Moreno J, Herrero E, Belli G, et al. (2011) Heat shock response in yeast involves changes in both transcription rates and mRNA stabilities. PLoS One 6: e17272.
87. Francois J, Parrou JL, (2001) Reserve carbohydrates metabolism in the yeast Saccharomyces cerevisiae. FEMS Microbiol Rev 25: 125-145.
88. Barth G, Gaillardin C, (1997) Physiology and genetics of the dimorphic fungus Yarrowia lipolytica. FEMS Microbiol Rev 19: 219-237.
89. Ngamskulrungroj P, Himmelreich U, Breger JA, Wilson C, Chayakulkeeree M, et al. (2009) The trehalose synthesis pathway is an integral part of the virulence composite for Cryptococcus gattii. Infect Immun 77: 4584-4596.
90. Cherry JM, Ball C, Weng S, Juvik G, Schmidt R, et al. (1997) Genetic and physical maps of Saccharomyces cerevisiae. Nature 387: 67-73.