Dynamic metabolomics differentiates between carbon and energy starvation in recombinant saccharomyces cerevisiae fermenting xylose

Biotechnology for Biofuels

Volumn 5, Issue , 2012, Pages

  Bergdahl, Basti ^a   Heer, Dominik ^b   Sauer, Uwe ^b   Hahn Hägerdal, Bärbel ^a   Van Niel, Ed Wj ^a  

^a LUND UNIVERSITY   (Sweden)

^b ETH ZURICH   (Switzerland)

Author keywords

Bioethanol; Metabolic status; Metabolomics; Starvation; Xylose fermentation; Yeast metabolism

Indexed keywords

METABOLIC STATUS; METABOLOMICS; STARVATION; XYLOSE FERMENTATION; YEAST METABOLISM;

AMINO ACIDS; BIOETHANOL; BIOMOLECULES; CARBON; DYNAMICS; ENZYME ACTIVITY; ETHANOL; FERMENTATION; GENE EXPRESSION; GLUCOSE; METABOLISM; METABOLITES; YEAST;

STRAIN;

CARBON; CONCENTRATION (COMPOSITION); ETHANOL; FERMENTATION; METABOLISM; METABOLITE; MICROBIAL ACTIVITY; REACTION KINETICS; YEAST;

SACCHAROMYCES CEREVISIAE;

EID: 84860907188     PISSN: 17546834     EISSN: None     Source Type: Journal    
DOI: 10.1186/1754-6834-5-34     Document Type: Article

References (95)

1. Progress in metabolic engineering ofSaccharomyces cerevisiae. Nevoigt E, Microbiol Mol Biol Rev 2008 72 379 412 10.1128/MMBR.00025-07 18772282
2. Ethanol fermentation from biomass resources: Current state and prospects. Lin Y, Tanaka S, Appl Microbiol Biotechnol 2006 69 627 642 10.1007/s00253-005- 0229-x 16331454 (Pubitemid 43136522)
3. Compositional changes during storage of large round switchgrass bales. Wiselogel AE, Agblevor FA, Johnson DK, Deutch S, Fennell JA, Sanderson MA, Bioresour Technol 1996 56 103 109 10.1016/0960-8524(95)00171-9 (Pubitemid 26355450)
4. Evaluation of forestry biomass quality for the production of second-generation biofuels. Perez DD, Guillemain A, Berthelot A, N'Guyen-The N, De Morogues F, Gomes C, Cell Chem Technol 2010 44 1 14
5. Techno-economic evaluation of bioethanol production from three different lignocellulosic materials. Sassner P, Galbe M, Zacchi G, Biomass Bioenerg 2008 32 422 430 10.1016/j.biombioe.2007.10.014
6. Yeast metabolic engineering for hemicellulosic ethanol production. Van Vleet JH, Jeffries TW, Curr Opin Biotechnol 2009 20 300 306 10.1016/j.copbio. 2009.06.001 19545992
7. Ethanol production from xylose in engineeredSaccharomyces cerevisiaestrains: Current state and perspectives. Matsushika A, Inoue H, Kodaki T, Sawayama S, Appl Microbiol Biotechnol 2009 84 37 53 10.1007/s00253-009-2101- x 19572128
8. Towards industrial pentose-fermenting yeast strains. Hahn-Hagerdal B, Karhumaa K, Fonseca C, Spencer-Martins I, Gorwa-Grauslund MF, Appl Microbiol Biotechnol 2007 74 937 953 10.1007/s00253-006-0827-2 17294186 (Pubitemid 46434767)
9. Engineering primary metabolic pathways of industrial micro-organisms. Kern A, Tilley E, Hunter IS, Legisa M, Glieder A, J Biotechnol 2007 129 6 29 10.1016/j.jbiotec.2006.11.021 17196287 (Pubitemid 46400022)
10. Comparison of the xylose reductase-xylitol dehydrogenase and the xylose isomerase pathways for xylose fermentation by recombinantSaccharomyces cerevisiae. Karhumaa K, Sanchez RG, Hahn-Hagerdal B, Gorwa-Grauslund MF, Microb Cell Fact 2007 6 5 10.1186/1475-2859-6-5 17280608
11. Genetic traits beneficial for xylose utilization by recombinantSaccharomyces cerevisiae.Doctoral Thesis. Bengtsson O, Lund University, Division of Applied Microbiology 2008
12. NADH-linked aldose reductase-the key to anaerobic alcoholic fermentation of xylose by yeasts. Bruinenberg PM, de Bot PHM, van Dijken JP, Scheffers WA, Appl Microbiol Biotechnol 1984 19 256 260 (Pubitemid 14118231)
13. The role of redox balances in the anaerobic fermentation of xylose by yeasts. Bruinenberg PM, de Bot PHM, van Dijken JP, Scheffers WA, Appl Microbiol Biotechnol 1983 18 287 292 10.1007/BF00500493 (Pubitemid 14178387)
14. Xylose fermentation bySaccharomyces cerevisiae. Kotter P, Ciriacy M, Appl Microbiol Biotechnol 1993 38 776 783 10.1007/BF00167144
15. Development of efficient xylose fermentation inSaccharomyces cerevisiae: Xylose lsomerase as a key component. van Maris AJA, Winkler AA, Kuyper M, de Laat W, van Dijken JP, Pronk JT, Biofuels Springer-Verlag Berlin, Berlin, Olsson L, 2007 179 204 [Scheper T (Series Editor): Advances in Biochemical Engineering/Biotechnology, vol 108.] (Pubitemid 47434546)
16. Metabolite profiling of fungi and yeast: from phenotype to metabolome by MS and informatics. Smedsgaard J, Nielsen J, J Exp Bot 2005 56 273 286 15618299 (Pubitemid 40191444)
17. Towards a truly integrative biology through the functional genomics of yeast. Delneri D, Brancia FL, Oliver SG, Curr Opin Biotechnol 2001 12 87 91 10.1016/S0958-1669(00)00179-8 11167079 (Pubitemid 32843150)
18. Systems biology of microbial metabolism. Heinemann M, Sauer U, Curr Opin Microbiol 2010 13 337 343 10.1016/j.mib.2010.02.005 20219420
19. Regulation and control of metabolic fluxes in microbes. Gerosa L, Sauer U, Curr Opin Biotechnol 2011 22 566 575 10.1016/j.copbio.2011.04.016 21600757
20. Ultrahigh performance liquid chromatography-tandem mass spectrometry method for fast and robust quantification of anionic and aromatic metabolites. Buescher JM, Moco S, Sauer U, Zamboni N, Anal Chem 2010 82 4403 4412 10.1021/ac100101d 20433152
21. Investigation of limiting metabolic steps in the utilization of xylose by recombinantSaccharomyces cerevisiaeusing metabolic engineering. Karhumaa K, Hahn-Hägerdal B, Gorwa-Grauslund MF, Yeast 2005 22 359 368 10.1002/yea.1216 15806613 (Pubitemid 40561552)
22. Kinetic modeling reveals current limitations in the production of ethanol from xylose by recombinantSaccharomyces cerevisiae. Parachin NS, Bergdahl B, van Niel EWJ, Gorwa-Grauslund MF, Metab Eng 2011 13 508 517 10.1016/j.ymben. 2011.05.005 21642010
23. A tool for network-embedded thermodynamic analysis of quantitative metabolome data. Zamboni N, Kummel A, Heinemann M, anNET, BMC Bioinformatics 2008 9 199 10.1186/1471-2105-9-199 18416814 (Pubitemid 351587129)
24. Increased expression of the oxidative pentose phosphate pathway and gluconeogenesis in anaerobically growing xylose-utilizingSaccharomyces cerevisiae. Runquist D, Hahn-Hagerdal B, Bettiga M, Microb Cell Fact 2009 8 49 10.1186/1475-2859-8-49 19778438
25. A method for the determination of changes of glycolytic metabolites in yeast on a subsecond time scale using extraction at neutral pH. de Koning W, van Dam K, Anal Biochem 1992 204 118 123 10.1016/0003-2697(92)90149-2 1514678
26. anNET: A tool for networkembedded thermodynamic analysis of quantitative metabolome data. Zamboni N, Kummel A, Heinemann M, BMC Bioinformatics 2008 9 199 10.1186/1471-2105-9-199 18416814 (Pubitemid 351587129)
27. Connecting extracellular metabolomic measurements to intracellular flux states in yeast. Mo M, Palsson B, Herrgard M, BMC Syst Biol 2009 3 37 10.1186/1752-0509-3-37 19321003
28. Quantitative prediction of cellular metabolism with constraint-based models: the COBRA Toolbox. Becker SA, Feist AM, Mo ML, Hannum G, Palsson BO, Herrgard MJ, Nat Protocols 2007 2 727 738 10.1038/nprot.2007.99 (Pubitemid 47040034)
29. Intracellular fluxes in a recombinant xylose-utilizingSaccharomyces cerevisiaecultivated anaerobically at different dilution rates and feed concentrations. Wahlbom CF, Eliasson A, Hahn-Hägerdal B, Biotechnol Bioeng 2001 72 289 296 10.1002/1097-0290(20010205)72:3<289::AID-BIT5>3.0.CO;2-9 11135198 (Pubitemid 32099581)
30. Model-driven analysis of experimentally determined growth phenotypes for 465 yeast gene deletion mutants under 16 different conditions. Snitkin E, Dudley A, Janse D, Wong K, Church G, Segre D, Genome Biol 2008 9 140 10.1186/gb-2008-9-9-r140 18808699
31. Group contribution method for thermodynamic analysis of complex metabolic networks. Jankowski MD, Henry CS, Broadbelt LJ, Hatzimanikatis V, Biophys J 2008 95 1487 1499 10.1529/biophysj.107.124784 18645197
32. Limitations in xylosefermentingSaccharomyces cerevisiae, made evident through comprehensive metabolite profiling and thermodynamic analysis. Klimacek M, Krahulec S, Sauer U, Nidetzky B, Appl Environ Microbiol 2010 76 7566 7574 10.1128/AEM.01787-10 20889786
33. A comprehensive method for the quantification of the nonoxidative pentose phosphate pathway intermediates inSaccharomyces cerevisiaeby GC-IDMS. Cipollina C, ten Pierick A, Canelas AB, Seifar RM, van Maris AJA, van Dam JC, Heijnen JJ, J Chromatogr B 2009 877 3231 3236 10.1016/j.jchromb.2009.07.019
34. Full-scale model of glycolysis inSaccharomyces cerevisiae. Hynne F, Dano S, Sorensen PG, Biophys Chem 2001 94 121 163 10.1016/S0301-4622(01)00229-0 11744196 (Pubitemid 34015989)
35. Kinetic modeling to optimize pentose fermentation inZymomonas mobilis. Altintas MM, Eddy CK, Zhang M, McMillan JD, Kompala DS, Biotechnol Bioeng 2006 94 273 295 10.1002/bit.20843 16570322 (Pubitemid 43803779)
36. Adenylate energy charge inSaccharomyces cerevisiaeduring starvation. Ball WJ, Atkinson DE, J Bacteriol 1975 121 975 982 1090610
37. Limitations in xylose-fermentingSaccharomyces cerevisiae, made evident through comprehensive metabolite profiling and thermodynamic analysis. Klimacek M, Krahulec S, Sauer U, Nidetzky B, Appl Environ Microbiol 2010 76 7566 7574 10.1128/AEM.01787-10 20889786
38. Metabolome, transcriptome and metabolic flux analysis of arabinose fermentation by engineeredSaccharomyces cerevisiae. Wisselink HW, Cipollina C, Oud B, Crimi B, Heijnen JJ, Pronk JT, van Maris AJA, Metab Eng 2010 12 537 551 10.1016/j.ymben.2010.08.003 20816840
39. High activity of xylose reductase and xylitol dehydrogenase improves xylose fermentation by recombinantSaccharomyces cerevisiae. Karhumaa K, Fromanger R, Hahn-Hagerdal B, Gorwa-Grauslund MF, Appl Microbiol Biotechnol 2007 73 1039 1046 16977466 (Pubitemid 44974311)
40. Evolutionary engineering of mixed-sugar utilization by a xylose-fermenting Saccharomyces cerevisiae strain. Kuyper M, Toirkens MJ, Diderich JA, Winkler AA, van Dijken JP, Pronk JT, Fems Yeast Research 2005 5 925 934 10.1016/j.femsyr.2005.04.004 15949975 (Pubitemid 40941017)
41. Characterization of the effectiveness of hexose transporters for transporting xylose during glucose and xylose co-fermentation by a recombinant Saccharomyces yeast. Sedlak M, Ho NWY, Yeast 2004 21 671 684 10.1002/yea.1060 15197732 (Pubitemid 38868185)
42. Xylose transport studies with xylose-utilizing Saccharomyces cerevisiae strains expressing heterologous and homologous permeases. Saloheimo A, Rauta J, Stasyk OV, Sibirny AA, Penttila M, Ruohonen L, Appl Microbiol Biotechnol 2007 74 1041 1052 10.1007/s00253-006-0747-1 17180689 (Pubitemid 46434755)
43. The glucose/xylose facilitator Gxf1 fromCandida intermediaexpressed in a xylose-fermenting industrial strain ofSaccharomyces cerevisiaeincreases xylose uptake in SSCF of wheat straw. Fonseca C, Olofsson K, Ferreira C, Runquist D, Fonseca LL, Hahn-Hagerdal B, Liden G, Enzyme Microb Technol 2011 48 518 525 10.1016/j.enzmictec.2011.02.010 22113025
44. Stephanopoulos G, Aristidou A, Nielsen J, Metabolic Engineering: Principles and Methodologies Elsevier Academic Press, San Diego, CA, USA 1998
45. Characterization of the metabolic shift between oxidative and fermentative growth inSaccharomyces cerevisiaeby comparative C-13 flux analysis. Frick O, Wittmann C, Microb Cell Fact 2005 4 30 10.1186/1475-2859-4-30 16269086 (Pubitemid 41614835)
46. Contribution of the pentose-phosphate pathway to glucose metabolism inSaccharomyces cerevisiae: A critical analysis on the use of labelled glucose. Gancedo JM, Lagunas R, Plant Science Letters 1973 1 193 200 10.1016/0304- 4211(73)90044-8
47. Central carbon metabolism ofSaccharomyces cerevisiaeexplored by biosynthetic fractional13C labeling of common amino acids. Maaheimo H, Fiaux J, akar ZP, Bailey JE, Sauer U, Szyperski T, Eur J Biochem 2001 268 2464 2479 10.1046/j.1432-1327.2001.02126.x 11298766 (Pubitemid 32421602)
48. Intermediary metabolite concentrations in xylulose-fermenting and glucose-fermentingSaccharomyces cerevisiaecells. Senac T, Hahn-Hägerdal B, Appl Environ Microbiol 1990 56 120 126 16348083 (Pubitemid 20031189)
49. The non-oxidative pentose phosphate pathway controls the fermentation rate of xylulose but not of xylose inSaccharomyces cerevisiaeTMB3001. Johansson B, Hahn-Hagerdal B, Fems Yeast Research 2002 2 277 282 12702276
50. Genetic improvement ofSaccharomyces cerevisiaefor xylose fermentation. Chu BCH, Lee H, Biotechnol Adv 2007 25 425 441 10.1016/j.biotechadv.2007.04.001 17524590 (Pubitemid 47043375)
51. Phosphofructokinase-structure and control. Evans PR, Farrants GW, Hudson PJ, Philos Trans R Soc Lond B Biol Sci 1981 293 53 62 10.1098/rstb.1981.0059 6115424
52. Conservation of the metabolomic response to starvation across two divergent microbes. Brauer MJ, Yuan J, Bennett BD, Lu W, Kimball E, Botstein D, Rabinowitz JD, Proc Natl Acad Sci USA 2006 103 19302 19307 10.1073/pnas. 0609508103 17159141 (Pubitemid 46026027)
53. Control of ATP homeostasis during the respiro-fermentative transition in yeast. Walther T, Novo M, Roessger K, Letisse F, Loret M-O, Portais J-C, Francois J-M, Mol Syst Biol 2010 6 344 20087341
54. When transcriptome meets metabolome: fast cellular responses of yeast to sudden relief of glucose limitation. Kresnowati MTAP, van Winden WA, Almering MJH, ten Pierick A, Ras C, Knijnenburg TA, Daran-Lapujade P, Pronk JT, Heijnen JJ, Daran JM, Mol Syst Biol 2006 2 49 10.1038/msb4100083 16969341 (Pubitemid 46061059)
55. Different signals control the activation of glycolysis in the yeastSaccharomyces cerevisiae. Boles E, Zimmermann FK, Heinisch J, Yeast 1993 9 761 770 10.1002/yea.320090710 8368010 (Pubitemid 23228876)
56. Different internal metabolites trigger the induction of glycolytic gene expression in Saccharomyces cerevisiae. Mueller S, Boles E, May M, Zimmermann FK, J Bacteriol 1995 177 4517 4519 7635834
57. Regulation of pyruvate kinase by fructose 1,6-diphosphate inSaccharomyces cerevisiae. Barwell CJ, Woodward B, Brunt RV, Eur J Biochem 1971 18 59 64 10.1111/j.1432-1033.1971.tb01214.x 5540517
58. Stimulation of yeast phosphofructokinase activity by Fructose 2,6-bisphosphate. Gad A, Biochem Biophys Res Commun 1981 102 985 991 10.1016/0006-291X(81)91635-1 6458303
59. The mechanism by which glucose increases fructose 2,6-bisphosphate concentration inSaccharomyces cerevisiae- A cyclic-AMP-dependent activation of phosphofructokinase-2. Francois J, Vanschaftingen E, Hers HG, Eur J Biochem 1984 145 187 193 10.1111/j.1432-1033.1984.tb08539.x 6092080
60. Glucose signaling-mediated coordination of cell growth and cell cycle inSaccharomyces cerevisiae. Busti S, Coccetti P, Alberghina L, Vanoni M, Sensors 2010 10 6195 6240 10.3390/s100606195 22219709
61. Effect of glucose supplements on the fermentation of xylose byPachysolen tannophilus. Jeffries TW, Fady JH, Lightfoot EN, Biotechnology and Bioengineering 1985 27 171 176 10.1002/bit.260270211 18553652 (Pubitemid 15131899)
62. Simultaneous saccharification and co-fermentation of glucose and xylose in steam-pretreated corn stover at high fiber content withSaccharomyces cerevisiaeTMB3400. Ohgren K, Bengtsson O, Gorwa-Grauslund MF, Galbe M, Hahn-Hagerdal B, Zacchi G, Journal of Biotechnology 2006 126 488 498 10.1016/j.jbiotec.2006.05.001 16828190 (Pubitemid 44634813)
63. Fermentation of mixed glucose-xylose substrates by engineered strains ofSaccharomyces cerevisiae: Role of the coenzyme specificity of xylose reductase, and effect of glucose on xylose utilization. Krahulec S, Petschacher B, Wallner M, Longus K, Klimacek M, Nidetzky B, Microb Cell Fact 2010 10 9 16
64. Aromatic amino acid biosynthesis in the yeastSaccharomyces-cerevisiae- a model system for the regulation of a eukaryotic biosynthetic pathway. Braus GH, Microbiol Rev 1991 55 349 370 1943992 (Pubitemid 21895159)
65. Changes in the intracellular concentrations of the adenosine phosphates and nicotinamide adenine dinucleotides ofSaccharomyces cerevisiaeduring batch fermentation. Mauricio JC, Pareja M, Ortega JM, World J Microbiol Biotechnol 1995 11 196 201 10.1007/BF00704648
66. Transcription analysis of recombinantSaccharomyces cerevisiaereveals novel responses to xylose. Salusjarvi L, Pitkanen JP, Aristidou A, Ruohonen L, Penttila M, Appl Biochem Biotechnol 2006 128 237 261 10.1385/ABAB:128:3:237 16632884 (Pubitemid 43787205)
67. Furfural, 5-hydroxymethyl furfural, and acetoin act as external electron acceptors during anaerobic fermentation of xylose in recombinantSaccharomyces cerevisiae. Wahlbom CF, Hahn-Hagerdal B, Biotechnol Bioeng 2002 78 172 178 10.1002/bit.10188 11870608 (Pubitemid 34712341)
68. Molecular analysis of aSaccharomyces cerevisiaemutant with improved ability to utilize xylose shows enhanced expression of proteins involved in transport, initial xylose metabolism, and the pentose phosphate pathway. Wahlbom CF, Otero RRC, van Zyl WH, Hahn-Hagerdal B, Jonsson LJ, Appl Environ Microbiol 2003 69 740 746 10.1128/AEM.69.2.740-746.2003 12570990 (Pubitemid 36204799)
69. Saccharomyces cerevisiaeengineered for xylose metabolism exhibits a respiratory response. Jin YS, Laplaza JM, Jeffries TW, Appl Environ Microbiol 2004 70 6816 6825 10.1128/AEM.70.11.6816-6825.2004 15528549 (Pubitemid 39518594)
70. Investigation by 13C-NMR and tricarboxylic acid (TCA) deletion mutant analysis of pathways for succinate formation inSaccharomyces cerevisiaeduring anaerobic fermentation. Camarasa C, Grivet JP, Dequin S, Microbiology 2003 149 2669 2678 10.1099/mic.0.26007-0 12949191 (Pubitemid 37160741)
71. Glucose-induced degradation of the MDH2 isozyme of malate dehydrogenase in yeast. Minard KI, McAlisterhenn L, J Biol Chem 1992 267 17458 17464 1324938
72. Energy charge of adenylate pool as a regulatory parameter. Interaction with feedback modifiers. Atkinson DE, Biochemistry 1968 7 4030 4034 10.1021/bi00851a033 4972613
73. Intracellular accumulation of AMP as a cause for the decline in rate of ethanol-production bySaccharomyces cerevisiaeduring batch fermentation. Dombek KM, Ingram LO, Appl Environ Microbiol 1988 54 98 104 3278691
74. Microbial metabolic regulation by adenine nucleotide pools. Knowles CJ, Microbial Energetics: Twenty-Seventh Symposium of the Society for General Microbiology Cambridge University Press, Cambridge, Haddock BA, Hamilton WA, 1977 241 283
75. Adenine nucleotide concentrations and turnover rates. Their correlation with biological activity in bacteria and yeast. Chapman AG, Atkinson DE, Advances in microbial physiology Academic Press, London, Rose AH, Tempest DW, 1977 253 306
76. Regulation of cell-size in the yeastSacchaormyces cerevisiae. Johnston GC, Ehrhardt CW, Lorincz A, Carter BLA, J Bacteriol 1979 137 1 5 368010
77. Kinetic evidence for a critical rate of protein synthesis in theSaccharomyces cerevisiaeyeast cell cycle. Moore SA, J Biol Chem 1988 263 9674 9681 3290211
78. Role of guanine nucleotides in the regulation of the Ras/cAMP pathway inSaccharomyces cerevisiae. Rudoni S, Colombo S, Coccetti P, Martegani E, BBA Mol Cell Res 2001 1538 181 189 (Pubitemid 32402241)
79. Guanine nucleotide pool imbalance impairs multiple steps of protein synthesis and disrupts GCN4 translational control inSaccharomyces cerevisiae. Iglesias-Gato D, Martin-Marcos P, Santos MA, Hinnebusch AG, Tamame M, Genetics 2011 187 105 122 10.1534/genetics.110.122135 20980241
80. Molecular targets of guanine nucleotides in differentiation, proliferation and apoptosis. Yalowitz JA, Jayaram HN, Anticancer Res 2000 20 2329 2338 10953293 (Pubitemid 30614434)
81. In yeast, Ras proteins are controlling elements of adenylate cyclase. Toda T, Uno I, Ishikawa T, Powers S, Kataoka T, Broek D, Cameron S, Broach J, Matsumoto K, Wigler M, Cell 1985 40 27 36 10.1016/0092-8674(85)90305-8 2981630 (Pubitemid 15169303)
82. The Ras-adenylate cyclase pathway and cell cycle control inSaccharomyces cerevisiae. Thevelein JM, Antonie Van Leeuwenhoek 1992 62 109 130 10.1007/BF00584466 1444331
83. The molecular mechanics of eukaryotic translation. Kapp LD, Lorsch JR, Annu Rev Biochem 2004 73 657 704 10.1146/annurev.biochem.73.030403.080419 15189156 (Pubitemid 39050383)
84. Snf1 promotes phosphorylation of the alpha subunit of eukaryotic translation initiation factor 2 by activating Gcn2 and inhibiting phosphatases Glc7 and Sit4. Cherkasova V, Qiu H, Hinnebusch AG, Molecular and Cellular Biology 2010 30 2862 2873 10.1128/MCB.00183-10 20404097
85. Henderson JF, Paterson ARP, Nucleotide metabolism: an introduction Academic Press, New York 1973
86. Response of nucleoside diphosphate kinase to adenylate energy charge. Thompson FM, Atkinson DE, Biochem Biophys Res Commun 1971 45 1581 10.1016/0006-291X(71)90201-4 5166850
87. Partial deprivation of GTP initiates meiosis and sporulation inSaccharomyces cerevisiae. Varma A, Freese EB, Freese E, Mol Gen Genet 1985 201 1 6 10.1007/BF00397977 3903431 (Pubitemid 15234739)
88. Lethal accumulation of guanylic nucleotides inSaccharomyces cerevisiaeHPT1-deregulated mutants. Breton A, Pinson B, Coulpier F, Giraud MF, Dautant A, Daignan-Fornier B, Genetics 2008 178 815 824 10.1534/genetics.107. 083295 18245832 (Pubitemid 351398795)
89. Phenotypic consequences of purine nucleotide imbalance inSaccharomyces cerevisiae. Saint-Marc C, Pinson B, Coulpier F, Jourdren L, Lisova O, Daignan-Fornier B, Genetics 2009 183 529 538 10.1534/genetics.109.105858 19635936
90. A rapid and reliable method for metabolite extraction in yeast using boiling buffered ethanol. Gonzalez B, Francois J, Renaud M, Yeast 1997 13 1347 1355 10.1002/(SICI)1097-0061(199711)13:14<1347::AID-YEA176>3.0.CO;2-O 9392079
91. Miller JN, Miller JC, Statistics and Chemometrics for Analytical Chemistry Pearson Education Limited, Harlow 5 2005
92. Tutorial to robust statistics. Rousseeuw PJ, J Chemometr 1991 5 1 20 10.1002/cem.1180050103
93. Robust regression techniques-A useful alternative for the detection of outlier data in chemical analysis. Ortiz MC, Sarabia LA, Herrero A, Talanta 2006 70 499 512 10.1016/j.talanta.2005.12.058 18970799 (Pubitemid 44332473)
94. Visualization and analysis of molecular data. Scholz M, Selbig J, Metabolomics Humana Press, Totowa, USA 2007 87 104 [Walker JM (Series Editor): Methods in Molecular Biology, vol 358.]
95. Jolliffe IT, Principal component analysis Springer-Verlag, New York 2 2002