Differential adaptation to multi-stressed conditions of wine fermentation revealed by variations in yeast regulatory networks

BMC Genomics

Volumn 14, Issue 1, 2013, Pages

  Brion, Christian ^a,b,c   Ambroset, Chloé ^a,b,c   Sanchez, Isabelle ^a,b,c   Legras, Jean Luc ^a,b,c   Blondin, Bruno ^a,b,c  

^a SPO   (France)

^b MONTPELLIER SUPAGRO   (France)

^c UNIV MONTPELLIER   (France)

Author keywords

Detoxification; Fermentation; Partial disomy; QTL; Transcriptome; Wine yeast

Indexed keywords

ERGOSTEROL; OLEIC ACID; TRANSCRIPTION FACTOR; TRANSCRIPTOME;

ARTICLE; CHROMOSOME 16; CLUSTER ANALYSIS; DETOXIFICATION; DISOMY; DNA POLYMORPHISM; FERMENTATION TECHNIQUE; FUNGAL GENETICS; FUNGAL STRAIN; GENE AMPLIFICATION; GENE CLUSTER; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; GENE LOCUS; GENE REGULATORY NETWORK; GENETIC LINKAGE; GENETIC REGULATION; GENOTYPE; HERITABILITY; LINKAGE ANALYSIS; MICROARRAY ANALYSIS; NONHUMAN; PHENOTYPIC VARIATION; PHYLOGENY; PROTEIN FUNCTION; PROTEIN LOCALIZATION; QUANTITATIVE TRAIT LOCUS; QUANTITATIVE TRAIT LOCUS MAPPING; SACCHAROMYCES CEREVISIAE; SINGLE NUCLEOTIDE POLYMORPHISM; TRANSCRIPTOMICS; WINE; ADAPTATION; ALLELE; CHROMOSOME; CHROMOSOME SEGREGATION; COMPARATIVE GENOMIC HYBRIDIZATION; DRUG INACTIVATION; FERMENTATION; FUNGAL GENE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MUTATION; PHENOTYPE; PHYSIOLOGICAL STRESS; PHYSIOLOGY;

SACCHAROMYCES CEREVISIAE;

ADAPTATION, PHYSIOLOGICAL; ALLELES; CHROMOSOME SEGREGATION; CHROMOSOMES, FUNGAL; CLUSTER ANALYSIS; COMPARATIVE GENOMIC HYBRIDIZATION; FERMENTATION; GENE EXPRESSION REGULATION, FUNGAL; GENE REGULATORY NETWORKS; GENES, FUNGAL; GENETIC LINKAGE; GENETIC LOCI; INACTIVATION, METABOLIC; MUTATION; PHENOTYPE; QUANTITATIVE TRAIT LOCI; SACCHAROMYCES CEREVISIAE; STRESS, PHYSIOLOGICAL; TRANSCRIPTION FACTORS; TRANSCRIPTOME; WINE;

EID: 84884933928     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-14-681     Document Type: Article

References (72)

1. 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. 10.1371/journal.pone.0025147, 3174997, 21949874.
2. Divol B, du Toit M, Duckitt E. Surviving in the presence of sulphur dioxide: strategies developed by wine yeasts. Appl Microbiol Biotechnol 2012, 95:601-613. 10.1007/s00253-012-4186-x, 22669635.
3. Legras JL, Erny C, Jeune CL, Lollier M, Adolphe Y, Demuyter C, Delobel P, Blondin B, Karst F. Activation of two different resistance mechanisms in Saccharomyces cerevisiae upon exposure to octanoic and decanoic acids. Appl Environ Microbiol 2010, 76:7526-7535. 10.1128/AEM.01280-10, 2976208, 20851956.
4. 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.
5. Warringer J, Zörgö E, Cubillos FA, Zia A, Gjuvsland A, Simpson JT, Forsmark A, Durbin R, Omholt SW, Louis EJ, Liti G, Moses A, Blomberg A. Trait variation in yeast is defined by population history. PLoS Genet 2011, 7:e1002111. 10.1371/journal.pgen.1002111, 3116910, 21698134.
6. Marullo P, Mansour C, Dufour M, Albertin W, Sicard D, Bely M, Dubourdieu D. Genetic improvement of thermo-tolerance in wine Saccharomyces cerevisiae strains by a backcross approach. FEMS Yeast Res 2009, 9:1148-1160. 10.1111/j.1567-1364.2009.00550.x, 19758333.
7. Dequin S, Casaregola S. The genomes of fermentative Saccharomyces. C R Biol 2011, 334:687-693. 10.1016/j.crvi.2011.05.019, 21819951.
8. Sicard D, Legras J-L. Bread, beer and wine: yeast domestication in the Saccharomyces sensu stricto complex. C R Biol 2011, 334:229-236. 10.1016/j.crvi.2010.12.016, 21377618.
9. Bisson LF. Geographic origin and diversity of wine strains of saccharomyces. Am J Enol Vitic 2012, 63:165-176.
10. Pérez-Ortín JE, Querol A, Puig S, Barrio E. Molecular characterization of a chromosomal rearrangement involved in the adaptive evolution of yeast strains. Genome Res 2002, 12:1533-1539. 10.1101/gr.436602, 187534, 12368245.
11. Dunn B, Levine RP, Sherlock G. Microarray karyotyping of commercial wine yeast strains reveals shared, as well as unique, genomic signatures. BMC Genomics 2005, 6:53. 10.1186/1471-2164-6-53, 1097725, 15833139.
12. Dunn B, Richter C, Kvitek DJ, Pugh T, Sherlock G. Analysis of the Saccharomyces cerevisiae pan-genome reveals a pool of copy number variants distributed in diverse yeast strains from differing industrial environments. Genome Res 2012, 22:908-924. 10.1101/gr.130310.111, 3337436, 22369888.
13. 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 USA 2009, 106:16333-16338. 10.1073/pnas.0904673106, 2740733, 19805302.
14. Galeote V, Bigey F, Beyne E, Novo M, Legras J-L, Casaregola S, Dequin S. Amplification of a Zygosaccharomyces bailii DNA segment in wine yeast genomes by extrachromosomal circular DNA formation. PLoS One 2011, 6:e17872. 10.1371/journal.pone.0017872, 3053389, 21423766.
15. 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 A O, 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. 10.1038/nature07743, 2659681, 19212322.
16. Schacherer J, Shapiro JA, Ruderfer DM, Kruglyak L. Comprehensive polymorphism survey elucidates population structure of S. cerevisiae. Nature 2009, 458:342-345. 10.1038/nature07670, 2782482, 19212320.
17. 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. 10.1038/416326a, 11907579.
18. 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. 1840089, 17194785.
19. 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. 10.1111/j.1365-294X.2011.05005.x, 21261765.
20. Salinas F, Cubillos FA, Soto D, Garcia V, Bergström A, Warringer J, Ganga MA, Louis EJ, Liti G, Martinez C. The genetic basis of natural variation in oenological traits in Saccharomyces cerevisiae. PLoS ONE 2012, 7:e49640. 10.1371/journal.pone.0049640, 3504119, 23185390.
21. Marullo P, Aigle M, Bely M, Masneuf-Pomarède I, Durrens P, Dubourdieu D, Yvert G. Single QTL mapping and nucleotide-level resolution of a physiologic trait in wine Saccharomyces cerevisiae strains. FEMS Yeast Res 2007, 7:941-952. 10.1111/j.1567-1364.2007.00252.x, 17537182.
22. Ehrenreich IM, Gerke JP, Kruglyak L. Genetic dissection of complex traits in yeast: insights from studies of gene expression and other phenotypes in the BYxRM cross. Cold Spring Harb Symp Quant Biol 2009, 74:145-153. 10.1101/sqb.2009.74.013, 2888688, 19734204.
23. Ehrenreich IM, Torabi N, Jia Y, Kent J, Martis S, Shapiro JA, Gresham D, Caudy AA, Kruglyak L. Dissection of genetically complex traits with extremely large pools of yeast segregants. Nature 2010, 464:1039-1042. 10.1038/nature08923, 2862354, 20393561.
24. Brem RB, Yvert G, Clinton R, Kruglyak L. Genetic dissection of transcriptional regulation in budding yeast. Science 2002, 296:752-755. 10.1126/science.1069516, 11923494.
25. Smith EN, Kruglyak L. Gene-environment interaction in yeast gene expression. PLoS Biol 2008, 6:e83. 10.1371/journal.pbio.0060083, 2292755, 18416601.
26. Brem RB, Kruglyak L. The landscape of genetic complexity across 5,700 gene expression traits in yeast. Proc Natl Acad Sci USA 2005, 102:1572-1577. 10.1073/pnas.0408709102, 547855, 15659551.
27. Brown KM, Landry CR, Hartl DL, Cavalieri D. Cascading transcriptional effects of a naturally occurring frameshift mutation in Saccharomyces cerevisiae. Mol Ecol 2008, 17:2985-2997. 10.1111/j.1365-294X.2008.03765.x, 18422925.
28. Zhu J, Sova P, Xu Q, Dombek KM, Xu EY, Vu H, Tu Z, Brem RB, Bumgarner RE, Schadt EE. Stitching together multiple data dimensions reveals interacting metabolomic and transcriptomic networks that modulate cell regulation. PLoS Biol 2012, 10:e1001301. 10.1371/journal.pbio.1001301, 3317911, 22509135.
29. Lee S-I, Dudley AM, Drubin D, Silver PA, Krogan NJ, Pe'er D, Koller D. Learning a prior on regulatory potential from eQTL data. PLoS Genet 2009, 5:e1000358. 10.1371/journal.pgen.1000358, 2627940, 19180192.
30. Williams RBH, Chan EKF, Cowley MJ, Little PFR. The influence of genetic variation on gene expression. Genome Res 2007, 17:1707-1716. 10.1101/gr.6981507, 18063559.
31. Kliebenstein D. Quantitative genomics: analyzing intraspecific variation using global gene expression polymorphisms or eQTLs. Annu Rev Plant Biol 2009, 60:93-114. 10.1146/annurev.arplant.043008.092114, 19012536.
32. Steyer D, Ambroset C, Brion C, Claudel P, Delobel P, Sanchez I, Erny C, Blondin B, Karst F, Legras J-L. QTL mapping of the production of wine aroma compounds by yeast. BMC Genomics 2012, 13:573. 10.1186/1471-2164-13-573, 3575298, 23110365.
33. Robinson MD, Grigull J, Mohammad N, Hughes TR. FunSpec: a web-based cluster interpreter for yeast. BMC Bioinforma 2002, 3:35.
34. Yvert G, Brem RB, Whittle J, Akey JM, Foss E, Smith EN, Mackelprang R, Kruglyak L. Trans-acting regulatory variation in Saccharomyces cerevisiae and the role of transcription factors. Nat Genet 2003, 35:57-64.
35. Brem RB, Storey JD, Whittle J, Kruglyak L. Genetic interactions between polymorphisms that affect gene expression in yeast. Nature 2005, 436:701-703. 10.1038/nature03865, 1409747, 16079846.
36. Iraqui I, Vissers S, Bernard F, de Craene J-O, Boles E, Urrestarazu A, André B. 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 1999, 19:989-1001. 116030, 9891035.
37. Abdulrehman D, Monteiro PT, Teixeira MC, Mira NP, Lourenco AB, dos Santos SC, Cabrito TR, Francisco AP, Madeira SC, Aires RS, Oliveira AL, Sa-Correia I, Freitas AT. YEASTRACT: providing a programmatic access to curated transcriptional regulatory associations in Saccharomyces cerevisiae through a web services interface. Nucleic Acids Res 2010, 39:D136-D140. 3013800, 20972212.
38. Martínez-Moreno R, Morales P, Gonzalez R, Mas A, Beltran G. Biomass production and alcoholic fermentation performance of Saccharomyces cerevisiae as a function of nitrogen source. FEMS Yeast Res 2012, 12:477-485. 10.1111/j.1567-1364.2012.00802.x, 22429249.
39. Byrd C, Turner GC, Varshavsky A. The N-end rule pathway controls the import of peptides through degradation of a transcriptional repressor. EMBO J 1998, 17:269-277. 10.1093/emboj/17.1.269, 1170377, 9427760.
40. Turner GC, Du F, Varshavsky A. Peptides accelerate their uptake by activating a ubiquitin-dependent proteolytic pathway. Nature 2000, 405:579-583. 10.1038/35014629, 10850718.
41. Damon C, Vallon L, Zimmermann S, Haider MZ, Galeote V, Dequin S, Luis P, Fraissinet-Tachet L, Marmeisse R. A novel fungal family of oligopeptide transporters identified by functional metatranscriptomics of soil eukaryotes. ISME J 2011, 5:1871-1880. 10.1038/ismej.2011.67, 3223307, 21654847.
42. Straver MH, Aar PCVD, Smit G, Kijne JW. Determinants of flocculence of brewer's yeast during fermentation in wort. Yeast 1993, 9:527-532. 10.1002/yea.320090509, 8322515.
43. Hikkel I, Lucau-Danila A, Delaveau T, Marc P, Devaux F, Jacq C. A general strategy to uncover transcription factor properties identifies a new regulator of drug resistance in yeast. J Biol Chem 2003, 278:11427-11432. 10.1074/jbc.M208549200, 12529331.
44. Grey M, Pich CT, Haase E, Brendel M. SNG1-a new gene involved in nitrosoguanidine resistance in Saccharomyces cerevisiae. Mutat Res 1995, 346:207-214. 10.1016/0165-7992(95)90037-3, 7753113.
45. Schuller C. Global phenotypic analysis and transcriptional profiling defines the weak acid stress response regulon in saccharomyces cerevisiae. Mol Biol Cell 2003, 15:706-720. 10.1091/mbc.E03-05-0322, 338074, 14617816.
46. Piper P, Mahé Y, Thompson S, Pandjaitan R, Holyoak C, Egner R, Mühlbauer M, Coote P, Kuchler K. The pdr12 ABC transporter is required for the development of weak organic acid resistance in yeast. EMBO J 1998, 17:4257-4265. 10.1093/emboj/17.15.4257, 1170759, 9687494.
47. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011, 28:2731-2739. 10.1093/molbev/msr121, 3203626, 21546353.
48. McDonald JH, Kreitman M. Adaptive protein evolution at the Adh locus in Drosophila. Nature 1991, 351:652-654. 10.1038/351652a0, 1904993.
49. Erny C, Raoult P, Alais A, Butterlin G, Delobel P, Matei-Radoi F, Casaregola S, Legras JL. Ecological success of a group of Saccharomyces cerevisiae/Saccharomyces kudriavzevii hybrids in the northern european wine-making environment. Appl Environ Microbiol 2012, 78:3256-3265. 10.1128/AEM.06752-11, 3346444, 22344648.
50. Alexandre H, Charpentier C. Biochemical aspects of stuck and sluggish fermentation in grape must. J Ind Microbiol Biotechnol 1998, 20:20-27.
51. Vargas RC, Tenreiro S, Teixeira MC, Fernandes AR, Sá-Correia I. Saccharomyces cerevisiae multidrug transporter Qdr2p (Yil121wp): localization and function as a quinidine resistance determinant. Antimicrob Agents Chemother 2004, 48:2531-2537. 10.1128/AAC.48.7.2531-2537.2004, 434225, 15215105.
52. Ríos G, Cabedo M, Rull B, Yenush L, Serrano R, Mulet JM. Role of the yeast multidrug transporter Qdr2 in cation homeostasis and the oxidative stress response. FEMS Yeast Res 2012, 13(1):97-106.
53. Vargas RC, García-Salcedo R, Tenreiro S, Teixeira MC, Fernandes AR, Ramos J, Sá-Correia I. Saccharomyces cerevisiae multidrug resistance transporter Qdr2 is implicated in potassium uptake, providing a physiological advantage to quinidine-stressed Cells. Eukaryot Cell 2007, 6:134-142. 10.1128/EC.00290-06, 1797947, 17189489.
54. Waterhouse AL. Wine Phenolics. Ann N Y Acad Sci 2002, 957:21-36. 10.1111/j.1749-6632.2002.tb02903.x, 12074959.
55. Kim JH, Campbell BC, Mahoney NE, Chan KL, Molyneux RJ. Identification of phenolics for control of Aspergillus flavus using Saccharomyces cerevisiae in a model target-gene bioassay. J Agric Food Chem 2004, 52:7814-7821. 10.1021/jf0487093, 15612761.
56. Pan Z, Agarwal AK, Xu T, Feng Q, Baerson SR, Duke SO, Rimando AM. Identification of molecular pathways affected by pterostilbene, a natural dimethylether analog of resveratrol. BMC Med Genomics 2008, 1:7. 10.1186/1755-8794-1-7, 2330146, 18366703.
57. Jothi R, Balaji S, Wuster A, Grochow JA, Gsponer J, Przytycka TM, Aravind L, Babu MM. Genomic analysis reveals a tight link between transcription factor dynamics and regulatory network architecture. Mol Syst Biol 2009, 5:294. 2736650, 19690563.
58. Galeote V, Novo M, Salema-Oom M, Brion C, Valério E, Gonçalves P, Dequin S. FSY1, a horizontally transferred gene in the Saccharomyces cerevisiae EC1118 wine yeast strain, encodes a high-affinity fructose/H+ symporter. Microbiology (Reading, Engl.) 2010, 156:3754-3761.
59. Marullo P, Bely M, Masneuf-Pomarède I, Pons M, Aigle M, Dubourdieu D. Breeding strategies for combining fermentative qualities and reducing off-flavor production in a wine yeast model. FEMS Yeast Res 2006, 6:268-279. 10.1111/j.1567-1364.2006.00034.x, 16487348.
60. 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.
61. Calull M, Marcé RM, Borrull F. Determination of carboxylic acids, sugars, glycerol and ethanol in wine and grape must by ion-exchange high-performance liquid chromatography with refractive index detection. J Chromatogr, A 1992, 590:215-222.
62. 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. 10.1093/nar/24.13.2519, 145975, 8692690.
63. R Development Core Team R: A Language and Environment for Statistical Computing 2008, Vienna, Austria: R Foundation for Statistical Computing, ISBN 3-900051-07-0, URL http://www.R-project.org, R Development Core Team.
64. Smyth GK, Speed T. Normalization of cDNA microarray data. Methods 2003, 31:265-273. 10.1016/S1046-2023(03)00155-5, 14597310.
65. Smyth GK. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 2004, 3. Article3.
66. Smyth G. limma: linear models for microarray data. Bioinformatics and Computational Biology Solutions Using R and Bioconductor 2005, 397-420. New York: Springer, Gentleman R, Carey VJ, Huber W, Irizarry RA, Dudoit S.
67. Quan H, Shih WJ. Assessing reproducibility by the within-subject coefficient of variation with random effects models. Biometrics 1996, 52:1195-1203. 10.2307/2532835, 8962450.
68. Benjamini Y, Drai D, Elmer G, Kafkafi N, Golani I. Controlling the false discovery rate in behavior genetics research. Behav Brain Res 2001, 125:279-284. 10.1016/S0166-4328(01)00297-2, 11682119.
69. De Hoon MJL, Imoto S, Nolan J, Miyano S. Open source clustering software. Bioinformatics 2004, 20:1453-1454. 10.1093/bioinformatics/bth078, 14871861.
70. Saldanha AJ. Java treeview-extensible visualization of microarray data. Bioinformatics 2004, 20:3246-3248. 10.1093/bioinformatics/bth349, 15180930.
71. Broman KW, Wu H, Sen S, Churchill GA. R/qtl: QTL mapping in experimental crosses. Bioinformatics 2003, 19:889-890. 10.1093/bioinformatics/btg112, 12724300.
72. Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 1980, 16:111-120. 10.1007/BF01731581, 7463489.