期刊论文详细信息
BMC Genomics
Deciphering regulatory variation of THI genes in alcoholic fermentation indicate an impact of Thi3p on PDC1 expression
Bruno Blondin1  Isabelle Sanchez1  Pierre Delobel1  Chloé Ambroset1  Christian Brion1 
[1] Université Montpellier 1, UMR1083, Science pour l’Œnologie, 2 Place Viala, F-34060, Montpellier, France
关键词: Expression regulation;    eQTL;    Fermentation;    Wine yeast;    Pyruvate decarboxylase;    Thiamine;   
Others  :  1127440
DOI  :  10.1186/1471-2164-15-1085
 received in 2014-09-09, accepted in 2014-11-26,  发布年份 2014
PDF
【 摘 要 】

Background

Thiamine availability is involved in glycolytic flux and fermentation efficiency. A deficiency of this vitamin may be responsible for sluggish fermentations in wine making. Therefore, both thiamine uptake and de novo synthesis could have key roles in fermentation processes. Thiamine biosynthesis is regulated in response to thiamine availability and is coordinated by the thiamine sensor Thi3p, which activates Pdc2p and Thi2p. We used a genetic approach to identify quantitative trait loci (QTLs) in wine yeast and we discovered that a set of thiamine genes displayed expression-QTL on a common locus, which contains the thiamine regulator THI3.

Results

We deciphered here the source of these regulatory variations of the THI and PDC genes. We showed that alteration of THI3 results in reduced expression of the genes involved in thiamine biosynthesis (THI11/12/13 and THI74) and increased expression of the pyruvate decarboxylase gene PDC1. Functional analysis of the allelic effect of THI3 confirmed the control of the THI and PDC1 genes. We observed, however, only a small effect of the THI3 on fermentation kinetics. We demonstrated that the expression levels of several THI genes are correlated with fermentation rate, suggesting that decarboxylation activity could drive gene expression through a modulation of thiamine content. Our data also reveals a new role of Thi3p in the regulation of the main pyruvate decarboxylase gene, PDC1.

Conclusions

This highlights a switch from PDC1 to PDC5 gene expression during thiamine deficiency, which may improve the thiamine affinity or conservation during the enzymatic reaction. In addition, we observed that the lab allele of THI3 and of the thiamin transporter THI7 have diverged from the original alleles, consistent with an adaptation of lab strains to rich media containing an excess of thiamine.

【 授权许可】

   
2014 Brion et al.; licensee BioMed Central.

【 预 览 】
附件列表
Files Size Format View
20150220161131698.pdf 1325KB PDF download
Figure 8. 56KB Image download
Figure 7. 41KB Image download
Figure 6. 50KB Image download
Figure 5. 73KB Image download
Figure 4. 48KB Image download
Figure 3. 55KB Image download
Figure 2. 44KB Image download
Figure 1. 61KB Image download
【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

Figure 7.

Figure 8.

【 参考文献 】
  • [1]Nielsen J: It Is All about Metabolic Fluxes. J Bacteriol 2003, 185:7031-7035.
  • [2]Camarasa C, Sanchez I, Brial P, Bigey F, Dequin S: Phenotypic landscape of Saccharomyces cerevisiae during wine fermentation: evidence for origin-dependent metabolic traits. PLoS ONE 2011, 6:e25147.
  • [3]Ough CS, Davenport M, Joseph K: Effects of Certain Vitamins on Growth and Fermentation Rate of Several Commercial Active Dry Wine Yeasts. Am J Enol Vitic 1989, 40:208-213.
  • [4]Bataillon M, Rico A, Sablayrolles J-M, Salmon J-M, Barre P: Early thiamin assimilation by yeasts under enological conditions: Impact on alcoholic fermentation kinetics. J Ferment Bioeng 1996, 82:145-150.
  • [5]Nosaka K, Onozuka M, Konno H, Akaji K: Thiamin-dependent transactivation activity of PDC2 in Saccharomyces cerevisiae. FEBS Lett 2008, 582:3991-3996.
  • [6]Nosaka K: Recent progress in understanding thiamin biosynthesis and its genetic regulation in Saccharomyces cerevisiae. Appl Microbiol Biotechnol 2006, 72:30-40.
  • [7]Nosaka K, Esaki H, Onozuka M, Konno H, Hattori Y, Akaji K: Facilitated recruitment of Pdc2p, a yeast transcriptional activator, in response to thiamin starvation. FEMS Microbiol Lett 2012, 330:140-147.
  • [8]Raghuram V, Lobo Z, Maitra P: PDC2, a yeast gene essential for synthesis of pyruvate decarboxylase, encodes a novel transcription factor. J Genet 1994, 73:17-32.
  • [9]Muller EH, Richards EJ, Norbeck J, Byrne KL, Karlsson KA, Pretorius GH, Meacock PA, Blomberg A, Hohmann S: Thiamine repression and pyruvate decarboxylase autoregulation independently control the expression of the Saccharomyces cerevisiae PDC5 gene. FEBS Lett 1999, 449:245-250.
  • [10]Rossignol T, Dulau L, Julien A, Blondin B: Genome-wide monitoring of wine yeast gene expression during alcoholic fermentation. Yeast 2003, 20:1369-1385.
  • [11]McCourt JA, Nixon PF, Duggleby RG: Thiamin nutrition and catalysis-induced instability of thiamin diphosphate. Br J Nutr 2006, 96:636-638.
  • [12]Steinmetz LM, Sinha H, Richards DR, Spiegelman JI, Oefner PJ, McCusker JH, Davis RW: Dissecting the architecture of a quantitative trait locus in yeast. Nature 2002, 416:326-330.
  • [13]Hu XH, Wang MH, Tan T, Li JR, Yang H, Leach L, Zhang RM, Luo ZW: Genetic dissection of ethanol tolerance in the budding yeast Saccharomyces cerevisiae. Genetics 2007, 175:1479-1487.
  • [14]Cubillos FA, Billi E, Zörgö E, Parts L, Fargier P, Omholt S, Blomberg A, Warringer J, Louis EJ, Liti G: Assessing the complex architecture of polygenic traits in diverged yeast populations. Mol Ecol 2011, 20:1401-1413.
  • [15]Brem RB, Yvert G, Clinton R, Kruglyak L: Genetic dissection of transcriptional regulation in budding yeast. Science 2002, 296:752-755.
  • [16]Brion C, Ambroset C, Sanchez I, Legras J-L, Blondin B: Differential adaptation to multi-stressed conditions of wine fermentation revealed by variations in yeast regulatory networks. BMC Genomics 2013, 14:681. BioMed Central Full Text
  • [17]Ambroset C, Petit M, Brion C, Sanchez I, Delobel P, Guérin C, Chiapello H, Nicolas P, Bigey F, Dequin S, Blondin B: Deciphering the Molecular Basis of Wine Yeast Fermentation Traits Using a Combined Genetic and Genomic Approach. G3: Genes, Genomes, Genetics 2011, 1:263-281.
  • [18]Llorente B, Fairhead C, Dujon B: Genetic redundancy and gene fusion in the genome of the Baker’s yeast Saccharomyces cerevisiae: functional characterization of a three-member gene family involved in the thiamine biosynthetic pathway. Mol Microbiol 1999, 32:1140-1152.
  • [19]Stolz J, Vielreicher M: Tpn1p, the plasma membrane vitamin B6 transporter of Saccharomyces cerevisiae. J Biol Chem 2003, 278:18990-18996.
  • [20]Delneri D, Gardner DC, Oliver SG: Analysis of the seven-member AAD gene set demonstrates that genetic redundancy in yeast may be more apparent than real. Genetics 1999, 153:1591-1600.
  • [21]Liti G, Carter DM, Moses AM, Warringer J, Parts L, James SA, Davey RP, Roberts IN, Burt A, Koufopanou V, Tsai IJ, Bergman CM, Bensasson D, O’Kelly MJT, van Oudenaarden A, Barton DBH, Bailes E, Nguyen AN, Jones M, Quail MA, Goodhead I, Sims S, Smith F, Blomberg A, Durbin R, Louis EJ: Population genomics of domestic and wild yeasts. Nature 2009, 458:337-341.
  • [22]Nosaka K, Onozuka M, Konno H, Kawasaki Y, Nishimura H, Sano M, Akaji K: Genetic regulation mediated by thiamin pyrophosphate-binding motif in Saccharomyces cerevisiae. Mol Microbiol 2005, 58:467-479.
  • [23]Mojzita D, Hohmann S: Pdc2 coordinates expression of the THI regulon in the yeast Saccharomyces cerevisiae. Mol Genet Genomics 2006, 276:147-161.
  • [24]Kvitek DJ, Will JL, Gasch AP: Variations in stress sensitivity and genomic expression in diverse S. cerevisiae isolates. PLoS Genet 2008, 4:e1000223.
  • [25]Harbison CT, Gordon DB, Lee TI, Rinaldi NJ, Macisaac KD, Danford TW, Hannett NM, Tagne J-B, Reynolds DB, Yoo J, Jennings EG, Zeitlinger J, Pokholok DK, Kellis M, Rolfe PA, Takusagawa KT, Lander ES, Gifford DK, Fraenkel E, Young RA: Transcriptional regulatory code of a eukaryotic genome. Nature 2004, 431:99-104.
  • [26]Treu L, Toniolo C, Nadai C, Sardu A, Giacomini A, Corich V, Campanaro S: The impact of genomic variability on gene expression in environmental Saccharomyces cerevisiae strains. Environ Microbiol 2014, 16:1378-1397.
  • [27]Hohmann S, Meacock PA: Thiamin metabolism and thiamin diphosphate-dependent enzymes in the yeast Saccharomyces cerevisiae: genetic regulation. Biochim Biophys Acta 1998, 1385:201-219.
  • [28]Bely M, Sablayrolles J-M, Barre P: Automatic detection of assimilable nitrogen deficiencies during alcoholic fermentation in oenological conditions. J Ferment Bioeng 1990, 70:246-252.
  • [29]Güldener U, Heck S, Fielder T, Beinhauer J, Hegemann JH: A new efficient gene disruption cassette for repeated use in budding yeast. Nucleic Acids Res 1996, 24:2519-2524.
  • [30]Novo M, Bigey F, Beyne E, Galeote V, Gavory F, Mallet S, Cambon B, Legras J-L, Wincker P, Casaregola S, Dequin S: Eukaryote-to-eukaryote gene transfer events revealed by the genome sequence of the wine yeast Saccharomyces cerevisiae EC1118. Proc Natl Acad Sci U S A 2009, 106:16333-16338.
  • [31]R Development Core Team:: R: A Language and Environment for Statistical Computing. Austria: Vienna; 2011. ISBN 3-900051-07-0, URL http://www.R-project.org/ webcite
  • [32]Smyth GK, Speed T: Normalization of cDNA microarray data. Methods 2003, 31:265-273.
  • [33]Smyth GK: Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 2004, 3:Article3.
  • [34]Smyth G: limma: Linear Models for Microarray Data. In Bioinformatics and Computational Biology Solutions Using R and Bioconductor. Edited by Gentleman R, Carey VJ, Huber W, Irizarry RA, Dudoit S. New York: Springer New York; 2005:397-420. [Statistics for Biology and Health]
  • [35]Broman KW, Wu H, Sen S, Churchill GA: R/qtl: QTL mapping in experimental crosses. Bioinformatics 2003, 19:889-890.
  • [36]Tesnière C, Delobel P, Pradal M, Blondin B: Impact of Nutrient Imbalance on Wine Alcoholic Fermentations: Nitrogen Excess Enhances Yeast Cell Death in Lipid-Limited Must. PLoS ONE 2013, 8:e61645.
  文献评价指标  
  下载次数:91次 浏览次数:34次