Effects of nitrogen catabolite repression and di-ammonium phosphate addition during wine fermentation by a commercial strain of S. cerevisiae

Applied Microbiology and Biotechnology

Volumn 89, Issue 5, 2011, Pages 1537-1549

  Deed, Nathan K ^a   Van Vuuren, Hennie J J ^b   Gardner, Richard C ^a  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Fermentation; Microarrays; Nitrogen catabolite repression; Saccharomyces cerevisiae; Varietal thiols; Wine

Indexed keywords

AEROBIC GROWTH; ALCOHOLIC FERMENTATION; DELETION MUTANTS; DOUBLE MUTANTS; GENE REGULATIONS; GRAPE JUICE; LAG PHASE; MICROARRAY ANALYSIS; MUTANT STRAIN; NITROGEN CATABOLITE REPRESSION; S.CEREVISIAE; SACCHAROMYCES CEREVISIAE; VARIETAL THIOLS; WILD TYPES; WINE FERMENTATION; WINE YEAST;

AMMONIUM COMPOUNDS; FERMENTATION; FRUIT JUICES; FRUITS; GENES; MICROARRAYS; NITROGEN; SUGARS; YEAST;

WINE;

AMMONIUM DERIVATIVE; DIAMMONIUM PHOSPHATE; NITROGEN; SUGAR; THIOL; UNCLASSIFIED DRUG; VOLATILE AGENT;

CATABOLISM; FERMENTATION; NITROGEN; PHOSPHATE; THIOL; YEAST;

ARTICLE; CATABOLITE REPRESSION; CONTROLLED STUDY; DELETION MUTANT; DOWN REGULATION; FERMENTATION; FUNGAL STRAIN; FUNGUS GROWTH; GENE CONTROL; GENE EXPRESSION; GENE MUTATION; GENETIC TRANSCRIPTION; GRAPE JUICE; MICROARRAY ANALYSIS; NITROGEN METABOLISM; NONHUMAN; SACCHAROMYCES CEREVISIAE; STRAIN DIFFERENCE; UPREGULATION; WILD TYPE; WINE;

CATABOLITE REPRESSION; ETHANOL; FERMENTATION; GENE DELETION; NITROGEN; PHOSPHATES; PLANT EXTRACTS; SACCHAROMYCES CEREVISIAE; VITIS; WINE;

SACCHAROMYCES CEREVISIAE; VITACEAE;

EID: 79952575731     PISSN: 01757598     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00253-011-3084-y     Document Type: Article

References (46)

1. Beck T, Hall MN (1999) The TOR signalling pathway controls nuclear localization of nutrient-regulated transcription factors. Nature 402(6762):689-692 (Pubitemid 129516342)
2. Bell SJ, Henschke PA (2005) Implications of nitrogen nutrition for grapes, fermentation and wine. Aust J Grape Wine Res 11 (3):242-295
3. Beltran G (2005) Effect of low temperature fermentation and nitrogen content on wine yeast metabolism. Ph.D. thesis, Universitat Rovira i Virgili, Tarragona, Spain
4. Beltran G, Novo M, Rozès N, Mas A, Guillamón JM (2004) Nitrogen catabolite repression in Saccharomyces cerevisiae during wine fermentations. FEMS Yeast Res 4(6):625-632 (Pubitemid 38369136)
5. Beltran G, Esteve-Zarzoso B, Rozès N, Mas A, Guillamón JM (2005) Influence of the timing of nitrogen additions during synthetic grape must fermentations on fermentation kinetics and nitrogen consumption. J Agric Food Chem 53(4):996-1002 (Pubitemid 40270389)
6. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B Stat Methodol 57:289-300
7. Blinder D, Coschigano PW, Magasanik B (1996) Interaction of the GATA factor Gln3p with the nitrogen regulator Ure2p in Saccharomyces cerevisiae. J Bacteriol 178(15):4734-4736 (Pubitemid 26262268)
8. Bradbury JE, Richards KD, Niederer HA, Lee SA, Rod Dunbar P, Gardner RC (2006) A homozygous diploid subset of commercial wine yeast strains. Anton Leeuw Int J G 89(1):27-37
9. Coffman JA, Rai R, Loprete DM, Cunningham T, Svetlov V, Cooper TG (1997) Cross regulation of four GATA factors that control nitrogen catabolic gene expression in Saccharomyces cerevisiae. J Bacteriol 179(11):3416-3429 (Pubitemid 27232976)
10. Collart MA, Oliviero S (1995) Preparation of yeast RNA. In: Ausubel FM, Brent R, Kingston RE et al (eds) Current protocols in molecular biology. Wiley, New York, pp 3.12.11-13.12.14
11. Cooper TG (2002) Transmitting the signal of excess nitrogen in Saccharomyces cerevisiae from the Tor proteins to the GATA factors: connecting the dots. FEMS Microbiol Rev 26(3):223-238
12. Courchesne WE, Magasanik B (1988) Regulation of nitrogen assimilation in Saccharomyces cerevisiae: roles of the URE2 and GLN3 genes. J Bacteriol 170(2):708-713
13. Darriet P, Tominaga T, Lavigne V, Boidron JN, Dubourdieu D (1995) Identification of a powerful aromatic component of Vitis vinifera L. var Sauvignon wines: 4-mercapto-4-methylpentan-2-one. Flavour Fragr J 10(6):385-392
14. Dubourdieu D, Tominaga T, Masneuf I, Des Gachons CP, Murat ML (2006) The role of yeasts in grape flavor development during fermentation: the example of Sauvignon Blanc. Am J Enol Vitic 57(1):81-88
15. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, Hornik K, Hothorn T, Huber W, Lacus S, Irizarry R, Leisch F, Li C, Maechler M, Rossini AJ, Sawitzki G, Smith C, Smyth G, Tierney L, Yang JY, Zhang J (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5:R80
16. Giaever G, Chu AM, Ni L, Connelly C, Riles L, Véronneau S, Dow S, Lucau-Danila A, Anderson K, André B, Arkin AP, Astromoff A, El Bakkoury M, Bangham R, Benito R, Brachat S, Campanaro S, Curtiss M, Davis K, Deutschbauer A, Entian KD, Flaherty P, Foury F, Garfinkel DJ, Gerstein M, Gotte D, Güldener U, Hegemann JH, Hempel S, Herman Z, Jaramillo DF, Kelly DE, Kelly SL, Kötter P, LaBonte D, Lamb DC, Lan N, Liang H, Liao H, Liu L, Luo C, Lussier M, Mao R, Menard P, Ooi SL, Revuelta JL, Roberts CJ, Rose M, Ross-Macdonald P, Scherens B, Schimmack G, Shafer B, Shoemaker DD, Sookhai-Mahadeo S, Storms RK, Strathern JN, Valle G, Voet M, Volckaert G, Wang CY, Ward TR, Wilhelmy J, Winzeler EA, Yang Y, Yen G, Youngman E, Yu K, Bussey H, Boeke JD, Snyder M, Philippsen P, Davis RW, Johnston M (2002) Functional profiling of the Saccharomyces cerevisiae genome. Nature 418(6896):387-391 (Pubitemid 34826834)
17. Godard P, Urrestarazu A, Vissers S, Kontos K, Bontempi G, Van Helden J, André B (2007) Effect of 21 different nitrogen sources on global gene expression in the yeast Saccharomyces cerevisiae. Mol Cell Biol 27(8):3065-3086 (Pubitemid 46581319)
18. Grant-Preece PA, Pardon KH, Capone DL, Cordente AG, Sefton MA, Jeffery DW, Elsey GM (2010) Synthesis of wine thiol conjugates and labeled analogues: fermentation of the glutathione conjugate of 3-mercaptohexan-1-ol yields the corresponding cysteine conjugate and free thiol. J Agric Food Chem 58:1383-1389
19. Hofman-Bang J (1999) Nitrogen catabolite repression in Saccharomyces cerevisiae. Mol Biotechnol 12(1):35-73
20. Iraqui I, Vissers S, Bernard F, Craene JO, Boles E, Urrestarazu A, André B (1999) Amino acid signaling in Saccharomyces cerevisiae: a permease-like sensor of external amino acids and F-box protein Grr1p are required for transcriptional induction of the AGP1 gene, which encodes a broad-specificity amino acid permease. Mol Cell Biol 19:989-1001 (Pubitemid 29046843)
21. Jiranek V, Langridge P, Henschke PA (1995) Amino acid and ammonium utilization by Saccharomyces cerevisiae wine yeasts from a chemically defined medium. Am J Enol Vitic 46(1):75-83
22. Kobayashi H, Takase H, Kaneko K, Tanzawa F, Takata R, Suzuki S, Konno T (2010) Analysis of S-3-(hexan-1-ol)-glutathione and S-3-(hexan-1-ol)-L-cysteine in Vitis vinifera L. cv. Koshu for aromatic wines. Am J Enol Vitic 61:176-185
23. Lund CM, Thompson MK, Benkwitz F, Wohler MW, Triggs CM, Gardner R, Heymann H, Nicolau L (2009) New Zealand Sauvignon Blanc distinct flavor characteristics: sensory, chemical, and consumer aspects. Am J Enol Vitic 60(1):1-12
24. Magasanik B, Kaiser CA (2002) Nitrogen regulation in Saccharomyces cerevisiae. Gene 290(1-2):1-18 (Pubitemid 34615905)
25. Marini AM, Soussi-Boudekou S, Vissers S, Andre B (1997) A family of ammonium transporters in Saccharomyces cerevisiae. Mol Cell Biol 17(8):4282-4293 (Pubitemid 27318104)
26. Marks VD, Ho Sui SJ, Erasmus D, Van Der Merwe GK, Brumm J, Wasserman WW, Bryan J, Van Vuuren HJJ (2008) Dynamics of the yeast transcriptome during wine fermentation reveals a novel fermentation stress response. FEMS Yeast Res 8(1):35-52
27. Marks VD, Van Der Merwe GK, Van Vuuren HJJ (2008) Transcriptional profiling of wine yeast in fermenting grape juice: regulatory effect of diammonium phosphate. FEMS Yeast Res 3 (3):269-287 (Pubitemid 36411980)
28. MartinezMJ, Roy S, Archuletta AB,Wentzell PD, Santa Anna-Arriola S, Rodriguez AL, Aragon AD, Quiñones GA, Allen C, Werner-Washburne M (2004) Genomic analysis of stationary-phase and exit in Saccharomyces cerevisiae: gene expression and identification of novel essential genes. Mol Biol Cell 15(12):5295-5305 (Pubitemid 39564725)
29. Richards KD, Goddard MR, Gardner RC (2009) A database of microsatellite genotypes for Saccharomyces cerevisiae. Anton Leeuw Int J G 96(3):355-359
30. Riego L, Avendago A, DeLuna A, Rodríguez E, González A (2002) GDH1 expression is regulated by GLN3, GCN4, and HAP4 under respiratory growth. Biochem Biophys Res Commun 293 (1):79-85
31. Rossignol T, Dulau L, Julien A, Blondin B (2003) Genome-wide monitoring of wine yeast gene expression during alcoholic fermentation. Yeast 20(16):1369-1385 (Pubitemid 38016631)
32. Rowen DW, Esiobu N, Magasanik B (1997) Role of GATA factor Nil2p in nitrogen regulation of gene expression in Saccharomyces cerevisiae. J Bacteriol 179(11):3761-3766 (Pubitemid 27233020)
33. Salmon JM (1989) Effect of sugar transport inactivation in Saccharomyces cerevisiae on sluggish and stuck enological fermentations. Appl Environ Microbiol 55(4):953-958
34. Salmon JM, Barre P (1998) Improvement of nitrogen assimilation and fermentation kinetics under enological conditions by derepression of alternative nitrogen-assimilatory pathways in an industrial Saccharomyces cerevisiae strain. Appl Environ Microbiol 64 (10):3831-3837
35. Saparov SM, Liu K, Agre P, Pohl P (2007) Fast and selective ammonia transport by aquaporin-8. J Biol Chem 282(8):5296-5301 (Pubitemid 47093764)
36. Schacherer J, Shapiro JA, Ruderfer DM, Kruglyak L (2009) Comprehensive polymorphism survey elucidates population structure of Saccharomyces cerevisiae. Nature 458(7236):342-345
37. Smyth GK (2004) Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Statistical Applications in Genetics and Molecular Biology 3(1, Article 3). Available at: http://www.bepress.com/sagmb/vol3/iss1/art3
38. Smyth GK (2005) Limma: linear models for microarray data. In: Gentleman R, Carey V, Dudoit S, Irizarry R, Huber W (eds) Bioinformatics and computational biology solutions using R and bioconductor. Springer, New York, pp 397-420
39. Smyth GK, Michaud J, Scott H (2005) The use of within-array replicate spots for assessing differential expression in microarray experiments. Bioinformatics 21(9):2067-2075, http://bioinformatics.oxfordjournals.org/cgi/ content/short/2021/2069/2067 (Pubitemid 40668046)
40. Stanbrough M, Rowen DW, Magasanik B (1995) Role of the GATA factors Gln3p and Nil1p of Saccharomyces cerevisiae in the expression of nitrogen-regulated genes. Proc Natl Acad Sci USA 92(21):9450-9454
41. Subileau M, Schneider R, Salmon JM, Degryse E (2008a) New insights on 3-mercaptohexanol (3MH) biogenesis in Sauvignon Blanc wines: Cys-3MH and (E)-hexen-2-al are not the major precursors. J Agric Food Chem 56:9230-9235
42. Subileau M, Schneider R, Salmon JM, Degryse E (2008b) Nitrogen catabolite repression modulates the production of aromatic thiols characteristic of Sauvignon Blanc at the level of precursor transport. FEMS Yeast Res 8(5):771-780
43. Takagi H, Shichiri M, Takemura M, Mohri M, Nakamori S (2000) Saccharomyces cerevisiae S1278b has novel genes of the N-acetyltransferase gene superfamily required for L-proline analogue resistance. J Bacteriol 182(15):4249-4256 (Pubitemid 30463789)
44. Thibon C, Marullo P, Claisse O, Cullin C, Dubourdieu D, Tominaga T (2008) Nitrogen catabolic repression controls Saccharomyces cerevisiae volatile thiols release during wine fermentation. FEMS Yeast Res 8:1076-1086
45. Tominaga T, Furrer A, Henry R, Dubourdieu D (1998a) Identification of new volatile thiols in the aroma of Vitis vinifera L. var. Sauvignon Blanc wines. Flavour Fragr J 13(3):159-162 (Pubitemid 28352101)
46. Tominaga T, Murat ML, Dubourdieu D (1998b) Development of a method for analyzing the volatile thiols involved in the characteristic aroma of wines made from Vitis vinifera L. Cv. Sauvignon Blanc. J Agric Food Chem 46(3):1044-1048 (Pubitemid 128488112)