Identification of RCN1 and RSA3 as ethanol-tolerant genes in Saccharomyces cerevisiae using a high copy barcoded library

FEMS Yeast Research

Volumn 12, Issue 1, 2012, Pages 48-60

  Anderson, Michael J ^a   Barker, Sarah L ^b   Boone, Charlie ^b   Measday, Vivien ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

Calcineurin; Environmental stress; Ethanol tolerance; Ribosome biogenesis; Wine yeast

Indexed keywords

ALCOHOL; CALCINEURIN; FUNGAL PROTEIN; PROTEIN RCN1; PROTEIN RSA3; UNCLASSIFIED DRUG;

ALCOHOL INTOXICATION; ARTICLE; BIODEGRADATION; BIOGENESIS; BIOTRANSFORMATION; CELL MEMBRANE; ENVIRONMENTAL STRESS; FUNGAL GENE; FUNGAL STRAIN; FUNGUS GROWTH; GENE IDENTIFICATION; GENE LOCUS; GROWTH INHIBITION; INHIBITION KINETICS; MOLECULAR LIBRARY; NONHUMAN; OPEN READING FRAME; OSMOTIC STRESS; OXIDATIVE STRESS; PLASMID; POLYMERASE CHAIN REACTION; PROTEIN ASSEMBLY; RIBOSOME; SACCHAROMYCES CEREVISIAE;

DNA BARCODING, TAXONOMIC; ETHANOL; GENE DOSAGE; GENE EXPRESSION; GENE LIBRARY; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; PLASMIDS; RIBOSOMAL PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

SACCHAROMYCES CEREVISIAE;

EID: 84855559160     PISSN: 15671356     EISSN: 15671364     Source Type: Journal    
DOI: 10.1111/j.1567-1364.2011.00762.x     Document Type: Article

References (54)

1. Alexandre H, Ansanay-Galeote V, Dequin S & Blondin B (2001) Global gene expression during short-term ethanol stress in Saccharomyces cerevisiae. FEBS Lett 498: 98-103.
2. Araki Y, Wu H, Kitagaki H, Akao T, Takagi H & Shimoi H (2009) Ethanol stress stimulates the Ca2+-mediated calcineurin/Crz1 pathway in Saccharomyces cerevisiae. J Biosci Bioeng 107: 1-6.
3. Attfield PV (1997) Stress tolerance: the key to effective strains of industrial baker's yeast. Nat Biotechnol 15: 1351-1357.
4. Bakalinsky AT & Snow R (1990) The chromosomal constitution of wine strains of Saccharomyces cerevisiae. Yeast 6: 367-382.
5. Barre P, Vezinhet F, Dequin S & Blondin B (1993) Wine Microbiology and Biotechnology. Harwood Academic Publishers, Chur, Switzerland.
6. Bauer FF & Pretorius IS (2000) Yeast stress response and fermentation efficiency: how to survive the making of wine - a review. S Afr J Enol Vitic 21: 27-51.
7. Borneman AR, Forgan AH, Pretorius IS & Chambers PJ (2008) Comparative genome analysis of a Saccharomyces cerevisiae wine strain. FEMS Yeast Res 8: 1185-1195.
8. Borneman AR, Desany BA, Riches D, Affourtit JP, Forgan AH, Pretorius IS, Egholm M & Chambers PJ (2011) Whole-genome comparison reveals novel genetic elements that characterize the genome of industrial strains of Saccharomyces cerevisiae. PLoS Genet 7: e1001287.
9. Bradbury JE, Richards KD, Niederer HA, Lee SA, Rod Dunbar P & Gardner RC (2006) A homozygous diploid subset of commercial wine yeast strains. Antonie Van Leeuwenhoek 89: 27-37.
10. Butcher RA & Schreiber SL (2006) A microarray-based protocol for monitoring the growth of yeast overexpression strains. Nat Protoc 1: 569-576.
11. Casey GP & Ingledew WM (1986) Ethanol tolerance in yeasts. Crit Rev Microbiol 13: 219-280.
12. Codon AC, Benitez T & Korhola M (1998) Chromosomal polymorphism and adaptation to specific industrial environments of Saccharomyces strains. Appl Microbiol Biotechnol 49: 154-163.
13. Costa V, Amorim MA, Reis E, Quintanilha A & Moradas-Ferreira P (1997) Mitochondrial superoxide dismutase is essential for ethanol tolerance of Saccharomyces cerevisiae in the post-diauxic phase. Microbiology 143(Pt 5): 1649-1656.
14. de la Cruz J, Lacombe T, Deloche O, Linder P & Kressler D (2004) The putative RNA helicase Dbp6p functionally interacts with Rpl3p, Nop8p and the novel trans-acting Factor Rsa3p during biogenesis of 60S ribosomal subunits in Saccharomyces cerevisiae. Genetics 166: 1687-1699.
15. Dinh TN, Nagahisa K, Yoshikawa K, Hirasawa T, Furusawa C & Shimizu H (2009) Analysis of adaptation to high ethanol concentration in Saccharomyces cerevisiae using DNA microarray. Bioprocess Biosyst Eng 32: 681-688.
16. Dunn B, Levine RP & Sherlock G (2005) Microarray karyotyping of commercial wine yeast strains reveals shared, as well as unique, genomic signatures. BMC Genomics 6: 53.
17. Gasch AP, Spellman PT, Kao CM, Carmel-Harel O, Eisen MB, Storz G, Botstein D & Brown PO (2000) Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 11: 4241-4257.
18. Gordon JL, Byrne KP & Wolfe KH (2009) Additions, losses, and rearrangements on the evolutionary route from a reconstructed ancestor to the modern Saccharomyces cerevisiae genome. PLoS Genet 5: e1000485.
19. de Groot PW, Ruiz C, Vazquez de Aldana CR et al. (2001) A genomic approach for the identification and classification of genes involved in cell wall formation and its regulation in Saccharomyces cerevisiae. Comp Funct Genomics 2: 124-142.
20. Guijo S, Mauricio JC, Salmon JM & Ortega JM (1997) Determination of the relative ploidy in different Saccharomyces cerevisiae strains used for fermentation and 'flor' film ageing of dry sherry-type wines. Yeast 13: 101-117.
21. Guthrie C & Fink GR (1991) Guide to Yeast Genetics and Molecular Biology. Academic Press, New York.
22. Hallsworth J (1998) Ethanol-induced water stress in yeast. J Ferment Bioeng 85: 125-137.
23. Hilioti Z, Gallagher DA, Low-Nam ST, Ramaswamy P, Gajer P, Kingsbury TJ, Birchwood CJ, Levchenko A & Cunningham KW (2004) GSK-3 kinases enhance calcineurin signaling by phosphorylation of RCNs. Genes Dev 18: 35-47.
24. Ho CH, Magtanong L, Barker SL et al. (2009) A molecular barcoded yeast ORF library enables mode-of-action analysis of bioactive compounds. Nat Biotechnol 27: 369-377.
25. Huxley C, Green ED & Dunham I (1990) Rapid assessment of S. cerevisiae mating type by PCR. Trends Genet 6: 236.
26. Izawa S, Inoue Y & Kimura A (1995) Oxidative stress response in yeast: effect of glutathione on adaptation to hydrogen peroxide stress in Saccharomyces cerevisiae. FEBS Lett 368: 73-76.
27. Kingsbury TJ & Cunningham KW (2000) A conserved family of calcineurin regulators. Genes Dev 14: 1595-1604.
28. Kressler D, de la Cruz J, Rojo M & Linder P (1998) Dbp6p is an essential putative ATP-dependent RNA helicase required for 60S-ribosomal-subunit assembly in Saccharomyces cerevisiae. Mol Cell Biol 18: 1855-1865.
29. Kressler D, Linder P & de La Cruz J (1999) Protein trans-acting factors involved in ribosome biogenesis in Saccharomyces cerevisiae. Mol Cell Biol 19: 7897-7912.
30. Kubota S, Takeo I, Kume K, Kanai M, Shitamukai A, Mizunuma M, Miyakawa T, Shimoi H, Lefuji H & Hirata D (2004) Effect of ethanol on cell growth of budding yeast: genes that are important for cell growth in the presence of ethanol. Biosci Biotechnol Biochem 68: 968-972.
31. Kumar G, Goyashiki R, Ramakrishnan V, Karpel J & Bisson L (2008) Genes required for ethanol tolerance and utilization in Saccharomyces cerevisiae. Am J Enol Vitic 59: 401-411.
32. Leao C & van Uden N (1982) Effects of ethanol and other alkanols on the glucose transport system of Saccharomyces cerevisiae. Biotechnol Bioeng 24: 2601-2604.
33. Leao C & Van Uden N (1984) Effects of ethanol and other alkanols on passive proton influx in the yeast Saccharomyces cerevisiae. Biochim Biophys Acta 774: 43-48.
34. Li BZ, Cheng JS, Ding MZ & Yuan YJ (2010) Transcriptome analysis of differential responses of diploid and haploid yeast to ethanol stress. J Biotechnol 148: 194-203.
35. Longtine MS, McKenzie A III, Demarini DJ et al. (1998) Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14: 953-961.
36. Magtanong L, Ho CH, Barker SL et al. (2011) Dosage suppression genetic interaction networks enhance functional wiring diagrams of the cell. Nat Biotechnol 29: 505-511.
37. 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: 35-52.
38. McMeekin TA, Olley J, Ratkowsky DA & Ross T (2002) Predictive microbiology: towards the interface and beyond. Int J Food Microbiol 73: 395-407.
39. Mendes-Ferreira A, del Olmo M, Garcia-Martinez J, Jimenez-Marti E, Mendes-Faia A, Perez-Ortin JE & Leao C (2007) Transcriptional response of Saccharomyces cerevisiae to different nitrogen concentrations during alcoholic fermentation. Appl Environ Microbiol 73: 3049-3060.
40. Novo M, Bigey F, Beyne E et al. (2009) Eukaryote-to-eukaryote gene transfer events revealed by the genome sequence of the wine yeast Saccharomyces cerevisiae EC1118. P Natl Acad Sci USA 106: 16333-16338.
41. Ovalle R, Spencer M, Thiwanont M & Lipke PN (1999) The spheroplast lysis assay for yeast in microtiter plate format. Appl Environ Microbiol 65: 3325-3327.
42. Perez-Ortin JE, Querol A, Puig S & Barrio E (2002) Molecular characterization of a chromosomal rearrangement involved in the adaptive evolution of yeast strains. Genome Res 12: 1533-1539.
43. Pierce SE, Fung EL, Jaramillo DF, Chu AM, Davis RW, Nislow C & Giaever G (2006) A unique and universal molecular barcode array. Nat Methods 3: 601-603.
44. Piggott N, Cook MA, Tyers M & Measday V (2011) Genome-wide fitness profiles reveal a requirement for autophagy during yeast fermentation. G3 1: 353-367.
45. Piper PW (1995) The heat shock and ethanol stress responses of yeast exhibit extensive similarity and functional overlap. FEMS Microbiol Lett 134: 121-127.
46. Rep M, Reiser V, Gartner U, Thevelein JM, Hohmann S, Ammerer G & Ruis H (1999) Osmotic stress-induced gene expression in Saccharomyces cerevisiae requires Msn1p and the novel nuclear factor Hot1p. Mol Cell Biol 19: 5474-5485.
47. Rosado IV, Dez C, Lebaron S, Caizergues-Ferrer M, Henry Y & de la Cruz J (2007) Characterization of Saccharomyces cerevisiae Npa2p (Urb2p) reveals a low-molecular-mass complex containing Dbp6p, Npa1p (Urb1p), Nop8p, and Rsa3p involved in early steps of 60S ribosomal subunit biogenesis. Mol Cell Biol 27: 1207-1221.
48. Teixeira MC, Raposo LR, Mira NP, Lourenco AB & Sa-Correia I (2009) Genome-wide identification of Saccharomyces cerevisiae genes required for maximal tolerance to ethanol. Appl Environ Microbiol 75: 5761-5772.
49. Thomson JM, Gaucher EA, Burgan MF, De Kee DW, Li T, Aris JP & Benner SA (2005) Resurrecting ancestral alcohol dehydrogenases from yeast. Nat Genet 37: 630-635.
50. Tong AH, Evangelista M, Parsons AB et al. (2001) Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science 294: 2364-2368.
51. van Voorst F, Houghton-Larsen J, Jonson L, Kielland-Brandt MC & Brandt A (2006) Genome-wide identification of genes required for growth of Saccharomyces cerevisiae under ethanol stress. Yeast 23: 351-359.
52. Warner JR (1999) The economics of ribosome biosynthesis in yeast. Trends Biochem Sci 24: 437-440.
53. Yoshikawa K, Tanaka T, Furusawa C, Nagahisa K, Hirasawa T & Shimizu H (2009) Comprehensive phenotypic analysis for identification of genes affecting growth under ethanol stress in Saccharomyces cerevisiae. FEMS Yeast Res 9: 32-44.
54. Zuzuarregui A & del Olmo M (2004) Analyses of stress resistance under laboratory conditions constitute a suitable criterion for wine yeast selection. Antonie Van Leeuwenhoek 85: 271-280.