The genetics of non-conventional wine yeasts: Current knowledge and future challenges

Frontiers in Microbiology

Volumn 6, Issue JAN, 2016, Pages

  Masneuf Pomarede, Isabelle ^a,b   Bely, Marina ^a   Marullo, Philippe ^a,c   Albertin, Warren ^a,d  

^a UNIVERSITÉ DE BORDEAUX   (France)

^b BORDEAUX SCIENCES AGRO   (France)

^c Research Subsidiary of the Laffort Group   (France)

^d BORDEAUX INP   (France)

Author keywords

Enology; Microsatellite; Non conventional yeast; Non Saccharomyces; Oenology; Wine

Indexed keywords

BIODIVERSITY; DIFFERENTIATION; GENETIC IMPROVEMENT; GENETICS; GENOMICS; NEXT GENERATION SEQUENCING; POPULATION STRUCTURE; SPECIES; WINE; WINE INDUSTRY; YEAST;

EID: 84957989597     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.01563     Document Type: Short Survey

References (169)

1. Aa, E., Townsend, J. P., Adams, R. I., Nielsen, K. M., and Taylor, J. W. (2006). Population structure and gene evolution in Saccharomyces cerevisiae. FEMS Yeast Res. 6, 702-715. doi: 10.1111/j.1567-1364.2006.00059.x.
2. Albergaria, H., Francisco, D., Gori, K., Arneborg, N., and Gírio, F. (2010). Saccharomyces cerevisiae CCMI 885 secretes peptides that inhibit the growth of some non-Saccharomyces wine-related strains. Appl. Microbiol. Biotechnol. 86, 965-972. doi: 10.1007/s00253-009-2409-6.
3. Albertin, W., Chasseriaud, L., Comte, G., Panfili, A., Delcamp, A., Salin, F., et al. (2014a). Winemaking and bioprocesses strongly shaped the genetic diversity of the ubiquitous yeast Torulaspora delbrueckii. PLoS ONE 9:e94246. doi: 10.1371/journal.pone.0094246.
4. Albertin, W., Marullo, P., Aigle, M., Bourgais, A., Bely, M., Dillmann, C., et al. (2009). Evidence for autotetraploidy associated with reproductive isolation in Saccharomyces cerevisiae: towards a new domesticated species. J. Evol. Biol. 22, 2157-2170. doi: 10.1111/j.1420-9101.2009.01828.x.
5. Albertin, W., Marullo, P., Peltier, E., Windholtz, S., Bely, M., and Masneuf-Pomarede, I. (2015). Biodiversity of Wine Yeasts: New Insights from Population Genetics. Oeno2015.
6. Albertin, W., Miot-Sertier, C., Bely, M., Marullo, P., Coulon, J., Moine, V., et al. (2014b). Oenological prefermentation practices strongly impact yeast population dynamics and alcoholic fermentation kinetics in Chardonnay grape must. Int. J. Food Microbiol. 178, 87-97. doi: 10.1016/j.ijfoodmicro.2014.03.009.
7. Albertin, W., Miot-Sertier, C., Bely, M., Mostert, T. T., Colonna-Ceccaldi, B., Coulon, J., et al. (2016). Hanseniaspora uvarum from winemaking environments show spatial and temporal genetic clustering. Front. Microbiol. 6:1569. doi: 10.3389/fmicb.2015.01569.
8. Albertin, W., Panfili, A., Miot-Sertier, C., Goulielmakis, A., Delcamp, A., Salin, F., et al. (2014c). Development of microsatellite markers for the rapid and reliable genotyping of Brettanomyces bruxellensis at strain level. Food Microbiol. 42, 188-195. doi: 10.1016/j.fm.2014.03.012.
9. Almeida, P., Barbosa, R., Zalar, P., Imanishi, Y., Shimizu, K., Turchetti, B., et al. (2015). A population genomics insight into the mediterranean origins of wine yeast domestication. Mol. Ecol. 24, 5412-5427. doi: 10.1111/mec.13341.
10. Almeida, P., Gonçalves, C., Teixeira, S., Libkind, D., Bontrager, M., Masneuf-Pomarède, I., et al. (2014). A Gondwanan imprint on global diversity and domestication of wine and cider yeast Saccharomyces uvarum. Nat. Commun. 5:4044. doi: 10.1038/ncomms5044.
11. Al Safadi, R., Weiss-Gayet, M., Briolay, J., and Aigle, M. (2010). A polyploid population of Saccharomyces cerevisiae with separate sexes (dioecy). FEMS Yeast Res. 10, 757-768. doi: 10.1111/j.1567-1364.2010.00660.x.
12. Ambroset, C., Petit, M., Brion, C., Sanchez, I., Delobel, P., Guérin, C., et al. (2011). Deciphering the molecular basis of wine yeast fermentation traits using a combined genetic and genomic approach. G3 1, 263-281. doi: 10.1534/g3.111.000422.
13. Andorrà, I., Berradre, M., Mas, A., Esteve-Zarzoso, B., and Guillamón, J. M. (2012). Effect of mixed culture fermentations on yeast populations and aroma profile. LWT Food Sci. Technol. 49, 8-13. doi: 10.1016/j.lwt.2012.04.008.
14. Anfang, N., Brajkovich, M., and Goddard, M. R. (2009). Co-fermentation with Pichia kluyveri increases varietal thiol concentrations in Sauvignon Blanc. Aust. J. Grape Wine Res. 15, 1-8. doi: 10.1111/j.1755-0238.2008.00031.x.
15. Azzolini, M., Fedrizzi, B., Tosi, E., Finato, F., Vagnoli, P., Scrinzi, C., et al. (2012). Effects of Torulaspora delbrueckii and Saccharomyces cerevisiae mixed cultures on fermentation and aroma of Amarone wine. Eur. Food Res. Technol. 235, 303-313. doi: 10.1007/s00217-012-1762-3.
16. Ball, C. (1984). Genetics and Breeding of Industrial Microorganisms. Seattle, WA: CRC Press.
17. Barnett, J. A., Payne, R. W., and Yarrow, D. (2000). Yeasts: Characteritics and Identification. Cambridge, UK: Cambridge University Press.
18. Barquet, M., Martín, V., Medina, K., Pérez, G., Carrau, F., and Gaggero, C. (2012). Tandem repeat-tRNA (TRtRNA) PCR method for the molecular typing of non-Saccharomyces subspecies. Appl. Microbiol. Biotechnol. 93, 807-814. doi: 10.1007/s00253-011-3714-4.
19. Barrio, E., Gonzalez, S., Arias, A., Belloch, C., and Querol, A. (2006). "Molecular mechanisms involved in the adaptive evolution of industrial yeasts," in Yeasts in Food and Beverages, eds A. Querol and G. Fleet (Berlin; Heildeberg: Springer-Verlag), 153-174.
20. Bely, M., Renault, P., da Silva, T., Masneuf-Pomarede, I., Albertin, W., Moine, V., et al. (2013). "Non-conventional yeasts and alcohol level reduction," in Alcohol Level Reduction in Wine (Vigne et Vin Publications Internationales), 33-37.
21. Bely, M., Stoeckle, P., Masneuf-Pomarède, I., and Dubourdieu, D. (2008). Impact of mixed Torulaspora delbrueckii-Saccharomyces cerevisiae culture on high-sugar fermentation. Int. J. Food Microbiol. 122, 312-320. doi: 10.1016/j.ijfoodmicro.2007.12.023.
22. Blein-Nicolas, M., Albertin, W., da Silva, T., Valot, B., Balliau, T., Masneuf-Pomarede, I., et al. (2015). A systems approach to elucidate heterosis of protein abundances in yeast. Mol. Cell. Proteomics 14, 2056-2071. doi: 10.1074/mcp.M115.048058.
23. Borneman, A. R., Desany, B. A., Riches, D., Affourtit, J. P., Forgan, A. H., Pretorius, I. S., et al. (2012). The genome sequence of the wine yeast VIN7 reveals an allotriploid hybrid genome with Saccharomyces cerevisiae and Saccharomyces kudriavzevii origins. FEMS Yeast Res. 12, 88-96. doi: 10.1111/j.1567-1364.2011.00773.x.
24. Borneman, A. R., Forgan, A. H., Pretorius, I. S., and Chambers, P. J. (2008). Comparative genome analysis of a Saccharomyces cerevisiae wine strain. FEMS Yeast Res. 8, 1185-1195. doi: 10.1111/j.1567-1364.2008.00434.x.
25. Branco, P., Viana, T., Albergaria, H., and Arneborg, N. (2015). Antimicrobial peptides (AMPs) produced by Saccharomyces cerevisiae induce alterations in the intracellular pH, membrane permeability and culturability of Hanseniaspora guilliermondii cells. Int. J. Food Microbiol. 205, 112-118. doi: 10.1016/j.ijfoodmicro.2015.04.015.
26. Breuer, U., and Harms, H. (2006). Debaryomyces hansenii-an extremophilic yeast with biotechnological potential. Yeast 23, 415-437. doi: 10.1002/yea.1374.
27. Chan, G. F., Gan, H. M., Ling, H. L., and Rashid, N. A. (2012). Genome sequence of Pichia kudriavzevii M12, a potential producer of bioethanol and phytase. Eukaryot. Cell 11, 1300-1301. doi: 10.1128/EC.00229-12.
28. Ciani, M., Beco, L., and Comitini, F. (2006). Fermentation behaviour and metabolic interactions of multistarter wine yeast fermentations. Int. J. Food Microbiol. 108, 239-245. doi: 10.1016/j.ijfoodmicro.2005.11.012.
29. Ciani, M., Canonico, L., Oro, L., and Comitini, F. (2014). Sequential fermentation using non-Saccharomyces yeasts for the reduction of alcohol content in wine. BIO Web Conf. 3:02015. doi: 10.1051/bioconf/20140302015.
30. Ciani, M., and Comitini, F. (2015). Yeast interactions in multi-starter wine fermentation. Curr. Opin. Food Sci. 1, 1-6. doi: 10.1016/j.cofs.2014.07.001.
31. Ciani, M., Comitini, F., Mannazzu, I., and Domizio, P. (2010). Controlled mixed culture fermentation: a new perspective on the use of non-Saccharomyces yeasts in winemaking. FEMS Yeast Res. 10, 123-133. doi: 10.1111/j.1567-1364.2009.00579.x.
32. Ciani, M., and Maccarelli, F. (1998). Oenological properties of non-Saccharomyces yeasts associated with wine-making. World J. Microbiol. Biotechnol. 14, 199-203. doi: 10.1023/A:1008825928354.
33. Clemente-Jimenez, J. M., Mingorance-Cazorla, L., Martiìnez-Rodriìguez, S., Heras-Vázquez, F. J. L., and Rodriìguez-Vico, F. (2004). Molecular characterization and oenological properties of wine yeasts isolated during spontaneous fermentation of six varieties of grape must. Food Microbiol. 21, 149-155. doi: 10.1016/S0740-0020(03)00063-7.
34. Clemente-Jimenez, J. M., Mingorance-Cazorla, L., Martínez-Rodríguez, S., Las Heras-Vázquez, F. J., and Rodríguez-Vico, F. (2005). Influence of sequential yeast mixtures on wine fermentation. Int. J. Food Microbiol. 98, 301-308. doi: 10.1016/j.ijfoodmicro.2004.06.007.
35. Cliften, P., Sudarsanam, P., Desikan, A., Fulton, L., Fulton, B., Majors, J., et al. (2003). Finding functional features in Saccharomyces genomes by phylogenetic footprinting. Science 301, 71-76. doi: 10.1126/science.1084337.
36. Comitini, F., Gobbi, M., Domizio, P., Romani, C., Lencioni, L., Mannazzu, I., et al. (2011). Selected non-Saccharomyces wine yeasts in controlled multistarter fermentations with Saccharomyces cerevisiae. Food Microbiol. 28, 873-882. doi: 10.1016/j.fm.2010.12.001.
37. Comitini, F., De Ingeniis, J., Pepe, L., Mannazzu, I., and Ciani, M. (2004). Pichia anomala and Kluyveromyces wickerhamii killer toxins as new tools against Dekkera/Brettanomyces spoilage yeasts. FEMS Microbiol. Lett. 238, 235-240. doi: 10.1111/j.1574-6968.2004.tb09761.x.
38. Csoma, H., and Sipiczki, M. (2008). Taxonomic reclassification of Candida stellata strains reveals frequent occurrence of Candida zemplinina in wine fermentation. FEMS Yeast Res. 8, 328-336. doi: 10.1111/j.1567-1364.2007.00339.x.
39. Cubillos, F. A., Vásquez, C., Faugeron, S., Ganga, A., and Martínez, C. (2009). Self-fertilization is the main sexual reproduction mechanism in native wine yeast populations. FEMS Microbiol. Ecol. 67, 162-170. doi: 10.1111/j.1574-6941.2008.00600.x.
40. da Silva, T., Albertin, W., Dillmann, C., Bely, M., la Guerche, S., Giraud, C., et al. (2015). Hybridization within Saccharomyces Genus Results in Homoeostasis and Phenotypic Novelty in Winemaking Conditions. PLoS ONE 10:e0123834. doi: 10.1371/journal.pone.0123834.
41. Diezmann, S., and Dietrich, F. S. (2009). Saccharomyces cerevisiae: population Divergence and Resistance to Oxidative Stress in Clinical, Domesticated and Wild Isolates. PLoS ONE 4:e5317. doi: 10.1371/journal.pone.0005317.
42. Di Maio, S., Genna, G., Gandolfo, V., Amore, G., Ciaccio, M., and Oliva, D. (2012). Presence of Candida zemplinina in sicilian musts and selection of a strain for wine mixed fermentations. S. Afr. J. Enol. Viticult. 33, 80-87.
43. Divol, B., du Toit, M., and Duckitt, E. (2012). Surviving in the presence of sulphur dioxide: strategies developed by wine yeasts. Appl. Microbiol. Biotechnol. 95, 601-613. doi: 10.1007/s00253-012-4186-x.
44. Domizio, P., Liu, Y., Bisson, L. F., and Barile, D. (2014). Use of non-Saccharomyces wine yeasts as novel sources of mannoproteins in wine. Food Microbiol. 43, 5-15. doi: 10.1016/j.fm.2014.04.005.
45. Domizio, P., Romani, C., Comitini, F., Gobbi, M., Lencioni, L., Mannazzu, I., et al. (2011a). Potential spoilage non-Saccharomyces yeasts in mixed cultures with Saccharomyces cerevisiae. Ann. Microbiol. 61, 137-144. doi: 10.1007/s13213-010-0125-1.
46. Domizio, P., Romani, C., Lencioni, L., Comitini, F., Gobbi, M., Mannazzu, I., et al. (2011b). Outlining a future for non-Saccharomyces yeasts: Selection of putative spoilage wine strains to be used in association with Saccharomyces cerevisiae for grape juice fermentation. Int. J. Food Microbiol. 147, 170-180. doi: 10.1016/j.ijfoodmicro.2011.03.020.
47. Dujon, B., Sherman, D., Fischer, G., Durrens, P., Casaregola, S., Lafontaine, I., et al. (2004). Genome evolution in yeasts. Nature 430, 35-44. doi: 10.1038/nature02579.
48. Egli, C. M., Edinger, W. D., Mitrakul, C. M., and Henick-Kling, T. (1998). Dynamics of indigenous and inoculated yeast populations and their effect on the sensory character of Riesling and Chardonnay wines. J. Appl. Microbiol. 85, 779-789. doi: 10.1046/j.1365-2672.1998.00521.x.
49. Ehrenreich, I. M., Torabi, N., Jia, Y., Kent, J., Martis, S., Shapiro, J. A., et al. (2010). Dissection of genetically complex traits with extremely large pools of yeast segregants. Nature 464, 1039-1042. doi: 10.1038/nature08923.
50. Englezos, V., Rantsiou, K., Torchio, F., Rolle, L., Gerbi, V., and Cocolin, L. (2015). Exploitation of the non-Saccharomyces yeast Starmerella bacillaris (synonym Candida zemplinina) in wine fermentation: physiological and molecular characterizations. Int. J. Food Microbiol. 199, 33-40. doi: 10.1016/j.ijfoodmicro.2015.01.009.
51. Erny, C., Raoult, P., Alais, A., Butterlin, G., Delobel, P., Matei-Radoi, F., et al. (2012). Ecological success of a group of Saccharomyces cerevisiae/Saccharomyces kudriavzevii hybrids in the Northern European wine making environment. Appl. Environ. Microbiol. 8, 3256-3265. doi: 10.1128/AEM.06752-11.
52. Esteve-Zarzoso, B., Peris-Torán, M., Ramón, D., and Querol, A. (2001). Molecular characterisation of Hanseniaspora species. Antonie van Leeuwenhoek 80, 85-92. doi: 10.1023/A:1012268931569.
53. Fay, J. C., and Benavides, J. A. (2005). Evidence for domesticated and wild populations of Saccharomyces cerevisiae. PLoS Genet. 1, 66-71. doi: 10.1371/journal.pgen.0010005.
54. Fleet, G. H. (2003). Yeast interactions and wine flavour. Int. J. Food Microbiol. 86, 11-22. doi: 10.1016/S0168-1605(03)00245-9.
55. Foury, F., Roganti, T., Lecrenier, N., and Purnelle, B. (1998). The complete sequence of the mitochondrial genome of Saccharomyces cerevisiae. FEBS Lett. 440, 325-331. doi: 10.1016/S0014-5793(98)01467-7.
56. Freel, K. C., Friedrich, A., Hou, J., and Schacherer, J. (2014). Population genomic analysis reveals highly conserved mitochondrial genomes in the yeast species Lachancea thermotolerans. Genome Biol. Evol. 6, 2586-2594. doi: 10.1093/gbe/evu203.
57. Friel, D., Vandenbol, M., and Jijakli, M. H. (2005). Genetic characterization of the yeast Pichia anomala (strain K), an antagonist of postharvest diseases of apple. J. Appl. Microbiol. 98, 783-788. doi: 10.1111/j.1365-2672.2004.02520.x.
58. García-Ríos, E., Gutiérrez, A., Salvadó, Z., Arroyo-López, F. N., and Guillamon, J. M. (2014). The fitness advantage of commercial wine yeasts in relation to the nitrogen concentration, temperature, and ethanol content under microvinification conditions. Appl. Environ. Microbiol. 80, 704-713. doi: 10.1128/AEM.03405-13.
59. Giaramida, P., Ponticello, G., Di Maio, S., Squadrito, M., Genna, G., Barone, E., et al. (2013). Candida zemplinina for production of wines with less alcohol and more glycerol. S. Afr. J. Enol. Viticult. 34, 204-211. doi: 10.1128/AEM.06768-11.
60. Giorello, F. M., Berna, L., Greif, G., Camesasca, L., Salzman, V., Medina, K., et al. (2014). Genome sequence of the native apiculate wine yeast Hanseniaspora vineae T02/19AF. Genome Announc 2, e00530-e00614. doi: 10.1128/genomeA.00530-14.
61. Giudici, P., Solieri, L., Pulvirenti, A. M., and Cassanelli, S. (2005). Strategies and perspectives for genetic improvement of wine yeasts. Appl. Microbiol. Biotechnol. 66, 622-628. doi: 10.1007/s00253-004-1784-2.
62. Goddard, M. R. (2008). Quantifying the complexities of Saccharomyces cerevisiae's ecosystem engineering via fermentation. Ecology 89, 2077-2082. doi: 10.1890/07-2060.1.
63. Goddard, M. R., Anfang, N., Tang, R., Gardner, R. C., and Jun, C. (2010). A distinct population of Saccharomyces cerevisiae in New Zealand: evidence for local dispersal by insects and human-aided global dispersal in oak barrels. Environ. Microbiol. 12, 63-73. doi: 10.1111/j.1462-2920.2009.02035.x.
64. Goffeau, A., Barrell, B. G., Bussey, H., Davis, R. W., Dujon, B., Feldmann, H., et al. (1996). Life with 6000 genes. Science 274, 546; 563-547. doi: 10.1126/science.274.5287.546.
65. Gomez-Angulo, J., Vega-Alvarado, L., Escalante-García, Z., Grande, R., Gschaedler-Mathis, A., Amaya-Delgado, L., et al. (2015). Genome sequence of Torulaspora delbrueckii NRRL Y-50541, isolated from mezcal fermentation. Genome Announc. 3, e00438-e00515. doi: 10.1128/genomeA.00438-15.
66. Gordon, J. L., Armisén, D., Proux-Wéra, E., Óhéigeartaigh, S. S., Byrne, K. P., and Wolfe, K. H. (2011). Evolutionary erosion of yeast sex chromosomes by mating-type switching accidents. Proc. Natl. Acad. Sci. U.S.A. 108, 20024-20029. doi: 10.1073/pnas.1112808108.
67. Grangeteau, C., Gerhards, D., Rousseaux, S., von Wallbrunn, C., Alexandre, H., and Guilloux-Benatier, M. (2015). Diversity of yeast strains of the genus Hanseniaspora in the winery environment: what is their involvement in grape must fermentation? Food Microbiol. 50, 70-77. doi: 10.1016/j.fm.2015.03.009.
68. Hall, B., Durall, D. M., and Stanley, G. (2011). Population dynamics of Saccharomyces cerevisiae during spontaneous fermentation at a British Columbia Winery. Am. J. Enol. Vitic. 62, 66-72. doi: 10.5344/ajev.2010.10054.
69. Hong, Y.-A., and Park, H.-D. (2013). Role of non-Saccharomyces yeasts in Korean wines produced from campbell early grapes: potential use of Hanseniaspora uvarum as a starter culture. Food Microbiol. 34, 207-214. doi: 10.1016/j.fm.2012.12.011.
70. Howell, K. S., Cozzolino, D., Bartowsky, E. J., Fleet, G. H., and Henschke, P. A. (2006). Metabolic profiling as a tool for revealing Saccharomyces interactions during wine fermentation. FEMS Yeast Res. 6, 91-101. doi: 10.1111/j.1567-1364.2005.00010.x.
71. Jara, M., Cubillos, F. A., García, V., Salinas, F., Aguilera, O., Liti, G., et al. (2014). Mapping genetic variants underlying differences in the central nitrogen metabolism in fermenter yeasts. PLoS ONE 9:e86533. doi: 10.1371/journal.pone.0086533.
72. Jarosz, D. F., Brown, J. C., Walker, G. A., Datta, M. S., Ung, W. L., Lancaster, A. K., et al. (2014). Cross-kingdom chemical communication drives a heritable, mutually beneficial prion-based transformation of metabolism. Cell 158, 1083-1093. doi: 10.1016/j.cell.2014.07.025.
73. Johnson, L. J., Koufopanou, V., Goddard, M. R., Hetherington, R., Schäfer, S. M., and Burt, A. (2004). Population genetics of the wild yeast Saccharomyces paradoxus. Genetics 166, 43-52. doi: 10.1534/genetics.166.1.43.
74. Jolly, N. P., Augustyn, O. P. H., and Pretorius, I. S. (2006). The role and use of non-Saccharomyces yeasts in wine production. S. Afr. J. Enol. Viticult. 27, 15-39.
75. Jung, P. P., Friedrich, A., Reisser, C., Hou, J., and Schacherer, J. (2012). Mitochondrial genome evolution in a single protoploid yeast species. G3 2, 1103-1111. doi: 10.1534/g3.112.003152.
76. Kemsawasd, V., Branco, P., Almeida, M. G., Caldeira, J., Albergaria, H., and Arneborg, N. (2015). Cell-to-cell contact and antimicrobial peptides play a combined role in the death of Lachanchea thermotolerans during mixed-culture alcoholic fermentation with Saccharomyces cerevisiae. FEMS Microbiol. Lett. 362:fnv103. doi: 10.1093/femsle/fnv103.
77. Kimura, M. (1980). A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16, 111-120. doi: 10.1007/BF01731581.
78. King, E. S., Swiegers, J. H., Travis, B., Francis, I. L., Bastian, S. E. P., and Pretorius, I. S. (2008). Coinoculated fermentations using Saccharomyces yeasts affect the volatile composition and sensory properties of Vitis vinifera L. cv. Sauvignon Blanc Wines. J. Agric. Food Chem. 56, 10829-10837. doi: 10.1021/jf801695h.
79. Knop, M. (2006). Evolution of the hemiascomycete yeasts: on life styles and the importance of inbreeding. Bioessays 28, 696-708. doi: 10.1002/bies.20435.
80. Kreger-van Rij, N. J. W. (1977). Ultrastructure of Hanseniaspora ascospores. Antonie Van Leeuwenhoek 43, 225-232. doi: 10.1007/BF00395677.
81. Kumar, S., Randhawa, A., Ganesan, K., Raghava, G. P. S., and Mondal, A. K. (2012). Draft genome sequence of salt-tolerant yeast Debaryomyces hansenii var. hansenii MTCC 234. Eukaryotic Cell 11, 961-962. doi: 10.1128/EC.00137-12.
82. Kurtzman, C. P., Fell, J. W., and Boekhout, T. (2011). The Yeasts: A Taxonomic Study. Amsterdam: Elsevier.
83. Kvitek, D. J., Will, J. L., and Gasch, A. P. (2008). Variations in Stress Sensitivity and Genomic Expression in Diverse, S. cerevisiae Isolates. PLoS Genet. 4:e1000223. doi: 10.1371/journal.pgen.1000223.
84. Landry, C. R., Oh, J., Hartl, D. L., and Cavalieri, D. (2006). Genome-wide scan reveals that genetic variation for transcriptional plasticity in yeast is biased towards multi-copy and dispensable genes. Gene 366, 343-351. doi: 10.1016/j.gene.2005.10.042.
85. Legras, J. L., Merdinoglu, D., Cornuet, J. M., and Karst, F. (2007). Bread, beer and wine: Saccharomyces cerevisiae diversity reflects human history. Mol. Ecol. 16, 2091-2102. doi: 10.1111/j.1365-294X.2007.03266.x.
86. Legras, J. L., Ruh, O., Merdinoglu, D., and Karst, F. (2005). Selection of hypervariable microsatellite loci for the characterization of Saccharomyces cerevisiae strains. Int. J. Food Microbiol. 102, 73-83. doi: 10.1016/j.ijfoodmicro.2004.12.007.
87. Liti, G., Carter, D. M., Moses, A. M., Warringer, J., Parts, L., James, S. A., et al. (2009). Population genomics of domestic and wild yeasts. Nature 458, 337-341. doi: 10.1038/nature07743.
88. Liti, G., and Louis, E. J. (2005). Yeast evolution and comparative genomics. Annu. Rev. Microbiol. 59, 135-153. doi: 10.1146/annurev.micro.59.030804.121400.
89. Liti, G., Peruffo, A., James, S. A., Roberts, I. N., and Louis, E. J. (2005). Inferences of evolutionary relationships from a population survey of LTR-retrotransposons and telomeric-associated sequences in the Saccharomyces sensu stricto complex. Yeast 22, 177-192. doi: 10.1002/yea.1200.
90. Magyar, I., Nyitrai-Sárdy, D., Leskó, A., Pomázi, A., and Kállay, M. (2014). Anaerobic organic acid metabolism of Candida zemplinina in comparison with Saccharomyces wine yeasts. Int. J. Food Microbiol. 178, 1-6. doi: 10.1016/j.ijfoodmicro.2014.03.002.
91. Magyar, I., and Tóth, T. (2011). Comparative evaluation of some oenological properties in wine strains of Candida stellata, Candida zemplinina, Saccharomyces uvarum and Saccharomyces cerevisiae. Food Microbiol. 28, 94-100. doi: 10.1016/j.fm.2010.08.011.
92. Malpertuy, A., Llorente, B., Blandin, G., Artiguenave, F., Wincker, P., and Dujon, B. (2000). Genomic exploration of the hemiascomycetous yeasts: 10. Kluyveromyces thermotolerans. FEBS Lett. 487, 61-65. doi: 10.1016/S0014-5793(00)02281-X.
93. Mangani, S., Buscioni, G., Collina, L., Bocci, E., and Vincenzini, M. (2011). Effects of microbial populations on anthocyanin profile of sangiovese wines produced in Tuscany, Italy. Am. J. Enol. Vitic. 62, 487-494. doi: 10.5344/ajev.2011.11047.
94. Marsit, S., Mena, A., Bigey, F., Sauvage, F. X., Couloux, A., Guy, J., et al. (2015). Evolutionary advantage conferred by an eukaryote-to-eukaryote gene transfer event in wine yeasts. Mol. Biol. Evol. 32, 1695-1707. doi: 10.1093/molbev/msv057.
95. Marullo, P., Aigle, M., Bely, M., Masneuf-Pomarède, I., Durrens, P., Dubourdieu, D., et al. (2007). Single QTL mapping and nucleotide-level resolution of a physiologic trait in wine Saccharomyces cerevisiae strains. FEMS Yeast Res. 7, 941-952. doi: 10.1111/j.1567-1364.2007.00252.x.
96. Marullo, P., Bely, M., Masneuf-Pomarède, I., Pons, M., Aigle, M., and Dubourdieu, D. (2006). Breeding strategies for combining fermentative qualities and reducing off-flavor production in a wine yeast model. FEMS Yeast Res. 6, 268-279. doi: 10.1111/j.1567-1364.2006.00034.x.
97. Marullo, P., and Dubourdieu, D. (2010). "Yeast selection for wine flavour modulation," in Managing Wine Quality, Vol. 2, ed A. G. Reynolds (Cambridge: Woodhead Publishing), 293-345.
98. Masneuf-Pomarede, I., Bely, M., Marullo, P., Lonvaud-Funel, A., and Dubourdieu, D. (2010). Reassessment of phenotypic traits for Saccharomyces bayanus var. uvarum wine yeast strains. Int. J. Food Microbiol. 139, 79-86. doi: 10.1016/j.ijfoodmicro.2010.01.038.
99. Masneuf-Pomarede, I., Juquin, E., Miot-Sertier, C., Renault, P., Laizet, Y. H., Salin, F., et al. (2015). The yeast Starmerella bacillaris (synonym Candida zemplinina) shows high genetic diversity in winemaking environments. 15:fov045. FEMS Yeast Res. doi: 10.1093/femsyr/fov045.
100. Masneuf-Pomarede, I., Le Jeune, C., Durrens, P., Lollier, M., Aigle, M., and Dubourdieu, D. (2007). Molecular typing of wine yeast strains Saccharomyces bayanus var. uvarum using microsatellite markers. Syst. Appl. Microbiol. 30, 75-82. doi: 10.1016/j.syapm.2006.02.006.
101. Masneuf-Pomarede, I., Salin, F., Coton, E., Coton, M., Le Jeune, C., Lonvaud-Funel, A., et al. (2009). "First insight into the genetic structure of S. bayanus var. uvarum revealed by microsatellite markers analysis," in 27th ISSY (Paris).
102. Maturano, Y. P., Mestre, M. V., Esteve-Zarzoso, B., Nally, M. C., Lerena, M. C., Toro, M. E., et al. (2015). Yeast population dynamics during prefermentative cold soak of Cabernet Sauvignon and Malbec wines. Int. J. Food Microbiol. 199, 23-32. doi: 10.1016/j.ijfoodmicro.2015.01.005.
103. Miller, M., Kock, J. L. F., Pretorius, G. H. J., and Coetzee, D. J. (1989). The value of orthogonal-field-alternation gel electrophoresis and other criteria in the taxonomy of the Genus Pichia Hansen emend. Kurtzman. Syst. Appl. Microbiol. 12, 191-202. doi: 10.1016/S0723-2020(89)80014-1.
104. Mira, N. P., Münsterkötter, M., Dias-Valada, F., Santos, J., Palma, M., Roque, F. C., et al. (2014). The genome sequence of the highly acetic acid-tolerant Zygosaccharomyces bailii-derived interspecies hybrid strain ISA1307, isolated from a sparkling wine plant. DNA Res. 21, 299-313. doi: 10.1093/dnares/dst058.
105. Moreira, N., Mendes, F., Guedes de Pinho, P., Hogg, T., and Vasconcelos, I. (2008). Heavy sulphur compounds, higher alcohols and esters production profile of Hanseniaspora uvarum and Hanseniaspora guilliermondii grown as pure and mixed cultures in grape must. Int. J. Food Microbiol. 124, 231-238. doi: 10.1016/j.ijfoodmicro.2008.03.025.
106. Muller, L. A. H., and McCusker, J. H. (2009). Microsatellite analysis of genetic diversity among clinical and nonclinical Saccharomyces cerevisiae isolates suggests heterozygote advantage in clinical environments. Mol. Ecol. 18, 2779-2786. doi: 10.1111/j.1365-294X.2009.04234.x.
107. Murphy, H. A., and Zeyl, C. W. (2010). Yeast sex: surprisingly high rates of outcrossing between asci. PLoS ONE 5:e10461. doi: 10.1371/journal.pone.0010461.
108. Naumov, G. I., Masneuf, I., Naumova, E. S., Aigle, M., and Dubourdieu, D. (2000). Association of Saccharomyces bayanus var. uvarum with some French wines: genetic analysis of yeast populations. Res. Microbiol. 151, 683-691. doi: 10.1016/S0923-2508(00)90131-1.
109. Naumov, G. I., and Naumova, E. S. (2009). Chromosomal differentiation of the sibling species Pichia membranifaciens and Pichia manshurica. Microbiology 78, 214-217. doi: 10.1134/S002626170902012X.
110. Nissen, P., and Arneborg, N. (2003). Characterization of early deaths of non-Saccharomyces yeasts in mixed cultures with Saccharomyces cerevisiae. Arch. Microbiol. 180, 257-263. doi: 10.1007/s00203-003-0585-9.
111. Nissen, P., Nielsen, D., and Arneborg, N. (2003). Viable Saccharomyces cerevisiae cells at high concentrations cause early growth arrest of non-Saccharomyces yeasts in mixed cultures by a cell-cell contact-mediated mechanism. Yeast 20, 331-341. doi: 10.1002/yea.965.
112. Novo, M., Bigey, F., Beyne, E., Galeote, V., Gavory, F., Mallet, S., et al. (2009). 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. 106, 16333-16338. doi: 10.1073/pnas.0904673106.
113. Pacheco, A., Almeida, M. J., and Sousa, M. J. (2009). Improved gene disruption method for Torulaspora delbrueckii. FEMS Yeast Res. 9, 158-160. doi: 10.1111/j.1567-1364.2008.00452.x.
114. Palanca, L., Gaskett, A. C., Günther, C. S., Newcomb, R. D., and Goddard, M. R. (2013). Quantifying variation in the ability of yeasts to attract Drosophila melanogaster. PLoS ONE 8:e75332. doi: 10.1371/journal.pone.0075332.
115. Paradis, E., Claude, J., and Strimmer, K. (2004). APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289-290. doi: 10.1093/bioinformatics/btg412.
116. Parapouli, M., Hatziloukas, E., Drainas, C., and Perisynakis, A. (2010). The effect of Debina grapevine indigenous yeast strains of Metschnikowia and Saccharomyces on wine flavour. J. Indust. Microbiol. Biotechnol. 37, 85-93. doi: 10.1007/s10295-009-0651-7.
117. Parle, J. N., and Di Menna, M. E. (1966). The source of yeasts in New Zealand wines. N.Z. J. Agric. Res. 9, 98-107. doi: 10.1080/00288233.1966.10418122.
118. Pérez-Nevado, F., Albergaria, H., Hogg, T., and Girio, F. (2006). Cellular death of two non-Saccharomyces wine-related yeasts during mixed fermentations with Saccharomyces cerevisiae. Int. J. Food Microbiol. 108, 336-345. doi: 10.1016/j.ijfoodmicro.2005.12.012.
119. Pfliegler, W. P., Horváth, E., Kallai, Z., and Sipiczki, M. (2014). Diversity of Candida zemplinina isolates inferred from RAPD, micro/minisatellite and physiological analysis. Microbiol. Res. 169, 402-410. doi: 10.1016/j.micres.2013.09.006.
120. Picazo, C., Gamero-Sandemetrio, E., Orozco, H., Albertin, W., Marullo, P., Matallana, E., et al. (2015). Mitochondria inheritance is a key factor for tolerance to dehydration in wine yeast production. Lett. Appl. Microbiol. 60, 217-222. doi: 10.1111/lam.12369.
121. Pina, A., Calderón, I. L., and Benítez, T. (1986). Intergeneric hybrids of Saccharomyces cerevisiae and Zygosaccharomyces fermentati obtained by protoplast fusion. Appl. Environ. Microbiol. 51, 995-1003.
122. Plech, M., de Visser, J. A., and Korona, R. (2014). Heterosis is prevalent among domesticated but not wild strains of Saccharomyces cerevisiae. G3 4, 315-323. doi: 10.1534/g3.113.009381.
123. Pramateftaki, P. V., Kouvelis, V. N., Lanaridis, P., and Typas, M. A. (2006). The mitochondrial genome of the wine yeast Hanseniaspora uvarum: a unique genome organization among yeast/fungal counterparts. FEMS Yeast Res. 6, 77-90. doi: 10.1111/j.1567-1364.2005.00018.x.
124. Pramateftaki, P. V., Kouvelis, V. N., Lanaridis, P., and Typas, M. A. (2008). Complete mitochondrial genome sequence of the wine yeast Candida zemplinina: intraspecies distribution of a novel group-IIB1 intron with eubacterial affiliations. FEMS Yeast Res. 8, 311-327. doi: 10.1111/j.1567-1364.2007.00332.x.
125. Pretorius, I. S. (2000). Tailoring wine yeast for the new millennium: novel approaches to the ancient art of winemaking. Yeast 16, 675-729. doi: 10.1002/1097-0061(20000615)16:8<675::AID-YEA585>3.0.CO;2-B.
126. Ramírez, M., Velázquez, R., Maqueda, M., López-Piñeiro, A., and Ribas, J. C. (2015). A new wine Torulaspora delbrueckii killer strain with broad antifungal activity and its toxin-encoding double-stranded RNA virus. Front. Microbiol. 6:983. doi: 10.3389/fmicb.2015.00983.
127. Renault, P. E., Albertin, W., and Bely, M. (2013). An innovative tool reveals interaction mechanisms among yeast populations under oenological conditions. Appl. Microbiol. Biotechnol. 97, 4105-4119. doi: 10.1007/s00253-012-4660-5.
128. Renault, P., Miot-Sertier, C., Marullo, P., Hernández-Orte, P., Lagarrigue, L., Lonvaud-Funel, A., et al. (2009). Genetic characterization and phenotypic variability in Torulaspora delbrueckii species: potential applications in the wine industry. Int. J. Food Microbiol. 134, 201-210. doi: 10.1016/j.ijfoodmicro.2009.06.008.
129. Richards, K. D., Goddard, M. R., and Gardner, R. C. (2009). A database of microsatellite genotypes for Saccharomyces cerevisiae. Antonie Van Leeuwenhoek 96, 355-359. doi: 10.1007/s10482-009-9346-3.
130. Roberts, I. N., and Oliver, S. G. (2011). The yin and yang of yeast: biodiversity research and systems biology as complementary forces driving innovation in biotechnology. Biotechnol. Lett. 33, 477-487. doi: 10.1007/s10529-010-0482-7.
131. Rodrigues, F., Ludovico, P., Sousa, M. J., Steensma, H. Y., Côrte-Real, M., and Leão, C. (2003). The spoilage yeast Zygosaccharomyces bailii forms mitotic spores: a screening method for haploidization. Appl. Environ. Microbiol. 69, 649-653. doi: 10.1128/AEM.69.1.649-653.2003.
132. Rojas, V., Gil, J. V., Piñaga, F., and Manzanares, P. (2001). Studies on acetate ester production by non-Saccharomyces wine yeasts. Int. J. Food Microbiol. 70, 283-289. doi: 10.1016/S0168-1605(01)00552-9.
133. Ruderfer, D. M., Pratt, S. C., Seidel, H. S., and Kruglyak, L. (2006). Population genomic analysis of outcrossing and recombination in yeast. Nat. Genet. 38, 1077-1081. doi: 10.1038/ng1859.
134. Sadoudi, M., Tourdot-Maréchal, R., Rousseaux, S., Steyer, D., Gallardo-Chacón, J. J., Ballester, J., et al. (2012). Yeast-yeast interactions revealed by aromatic profile analysis of Sauvignon Blanc wine fermented by single or co-culture of non-Saccharomyces and Saccharomyces yeasts. Food Microbiol. 32, 243-253. doi: 10.1016/j.fm.2012.06.006.
135. Salinas, F., Cubillos, F. A., Soto, D., Garcia, V., Bergström, A., Warringer, J., et al. (2012). The genetic basis of natural variation in oenological traits in Saccharomyces cerevisiae. PLoS ONE 7:e49640. doi: 10.1371/journal.pone.0049640.
136. Salvadó, Z., Arroyo-López, F. N., Barrio, E., Querol, A., and Guillamón, J. M. (2011). Quantifying the individual effects of ethanol and temperature on the fitness advantage of Saccharomyces cerevisiae. Food Microbiol. 28, 1155-1161. doi: 10.1016/j.fm.2011.03.008.
137. Sarilar, V., Bleykasten-Grosshans, C., and Neuvéglise, C. (2015). Evolutionary dynamics of hAT DNA transposon families in Saccharomycetaceae. Genome Biol. Evol. 7, 172-190. doi: 10.1093/gbe/evu273.
138. Scannell, D. R., Butler, G., and Wolfe, K. H. (2007). Yeast genome evolution-the origin of the species. Yeast 24, 929-942. doi: 10.1002/yea.1515.
139. Schacherer, J., Shapiro, J. A., Ruderfer, D. M., and Kruglyak, L. (2009). Comprehensive polymorphism survey elucidates population structure of Saccharomyces cerevisiae. Nature 458, 342-345. doi: 10.1038/nature07670.
140. Schuller, D., Cardoso, F., Sousa, S., Gomes, P., Gomes, A. C., Santos, M. A., et al. (2012). Genetic diversity and population structure of Saccharomyces cerevisiae strains isolated from different grape varieties and winemaking regions. PLoS ONE 7:e32507. doi: 10.1371/journal.pone.0032507.
141. Sicard, D., and Legras, J. L. (2011). Bread, beer and wine: yeast domestication in the Saccharomyces sensu stricto complex. C. R. Biol. 334, 229-236. doi: 10.1016/j.crvi.2010.12.016.
142. Sipiczki, M. (2004). Species identification and comparative molecular and physiological analysis of Candida zemplinina and Candida stellata. J. Basic Microbiol. 44, 471-479. doi: 10.1002/jobm.200410449.
143. Sniegowski, P. D., Dombrowski, P. G., and Fingerman, E. (2002). Saccharomyces cerevisiae and Saccharomyces paradoxus coexist in a natural woodland site in North America and display different levels of reproductive isolation from European conspecifics. FEMS Yeast Res. 1, 299-306. doi: 10.1111/j.1567-1364.2002.tb00048.x.
144. Solieri, L., Dakal, T., and Giudici, P. (2013). Next-generation sequencing and its potential impact on food microbial genomics. Ann. Microbiol. 63, 21-37. doi: 10.1007/s13213-012-0478-8.
145. Souciet, J. L., Dujon, B., Gaillardin, C., Johnston, M., Baret, P. V., Cliften, P., et al. (2009). Comparative genomics of protoploid Saccharomycetaceae. Genome Res. 19, 1696-1709. doi: 10.1101/gr.091546.109.
146. Starmer, W. T., Ganter, P. F., and Aberdeen, V. (1992). Geographic distribution and genetics of killer phenotypes for the yeast Pichia kluyveri across the United States. Appl. Environ. Microbiol. 58, 990-997.
147. Steensels, J., Snoek, T., Meersman, E., Picca Nicolino, M., Voordeckers, K., and Verstrepen, K. J. (2014). Improving industrial yeast strains: exploiting natural and artificial diversity. FEMS Microbiol. Rev. 38, 947-995. doi: 10.1111/1574-6976.12073.
148. Steensels, J., and Verstrepen, K. J. (2014). Taming wild yeast: potential of conventional and nonconventional yeasts in industrial fermentations. Annu. Rev. Microbiol. 68, 61-80. doi: 10.1146/annurev-micro-091213-113025.
149. Stefanini, I., Dapporto, L., Legras, J. L., Calabretta, A., Di Paola, M., De Filippo, C., et al. (2012). Role of social wasps in Saccharomyces cerevisiae ecology and evolution. Proc. Natl. Acad. Sci. U.S.A. 109, 13398-13403. doi: 10.1073/pnas.1208362109.
150. Strope, P. K., Skelly, D. A., Kozmin, S. G., Mahadevan, G., Stone, E. A., Magwene, P. M., et al. (2015). The 100-genomes strains, an S. cerevisiae resource that illuminates its natural phenotypic and genotypic variation and emergence as an opportunistic pathogen. Genome Res. 25, 762-774. doi: 10.1101/gr.185538.114.
151. Sutterlin, K. A. (2010). Fructophilic Yeasts to Cure Stuck Fermentations in Alcoholic Beverages. Ph.D. thesis, University of Stellenbosch.
152. Talla, E., Anthouard, V., Bouchier, C., Frangeul, L., and Dujon, B. (2005). The complete mitochondrial genome of the yeast Kluyveromyces thermotolerans. FEBS Lett. 579, 30-40. doi: 10.1016/j.febslet.2004.10.106.
153. Timberlake, W. E., Frizzell, M. A., Richards, K. D., and Gardner, R. C. (2011). A new yeast genetic resource for analysis and breeding. Yeast 28, 63-80. doi: 10.1002/yea.1821.
154. Tofalo, R., Perpetuini, G., Fasoli, G., Schirone, M., Corsetti, A., and Suzzi, G. (2014). Biodiversity study of wine yeasts belonging to the "terroir" of Montepulciano d'Abruzzo "Colline Teramane" revealed Saccharomyces cerevisiae strains exhibiting atypical and unique 5.8S-ITS restriction patterns. Food Microbiol. 39, 7-12. doi: 10.1016/j.fm.2013.10.001.
155. Tofalo, R., Perpetuini, G., Schirone, M., Fasoli, G., Aguzzi, I., Corsetti, A., et al. (2013). Biogeographical characterization of Saccharomyces cerevisiae wine yeast by molecular methods. Front. Microbiol. 4:166. doi: 10.3389/fmicb.2013.00166.
156. Tofalo, R., Schirone, M., Torriani, S., Rantsiou, K., Cocolin, L., Perpetuini, G., et al. (2012). Diversity of Candida zemplinina strains from grapes and Italian wines. Food Microbiol. 29, 18-26. doi: 10.1016/j.fm.2011.08.014.
157. Viana, F., Belloch, C., Vallés, S., and Manzanares, P. (2011). Monitoring a mixed starter of Hanseniaspora vineae-Saccharomyces cerevisiae in natural must: impact on 2-phenylethyl acetate production. Int. J. Food Microbiol. 151, 235-240. doi: 10.1016/j.ijfoodmicro.2011.09.005.
158. Viana, F., Gil, J. V., Genovés, S., Vallés, S., and Manzanares, P. (2008). Rational selection of non-Saccharomyces wine yeasts for mixed starters based on ester formation and enological traits. Food Microbiol. 25, 778-785. doi: 10.1016/j.fm.2008.04.015.
159. Wang, C., and Liu, Y. (2013). Dynamic study of yeast species and Saccharomyces cerevisiae strains during the spontaneous fermentations of Muscat blanc in Jingyang, China. Food Microbiol. 33, 172-177. doi: 10.1016/j.fm.2012.09.014.
160. Wang, C., Mas, A., and Esteve-Zarzoso, B. (2015). Interaction between Hanseniaspora uvarum and Saccharomyces cerevisiae during alcoholic fermentation. Int. J. Food Microbiol. 206, 67-74. doi: 10.1016/j.ijfoodmicro.2015.04.022.
161. Wang, Q.-M., Liu, W.-Q., Liti, G., Wang, S.-A., and Bai, F.-Y. (2012). Surprisingly diverged populations of Saccharomyces cerevisiae in natural environments remote from human activity. Mol. Ecol. 21, 5404-5417. doi: 10.1111/j.1365-294X.2012.05732.x.
162. Warringer, J., Zörgö, E., Cubillos, F. A., Zia, A., Gjuvsland, A., Simpson, J. T., et al. (2011). Trait variation in yeast is defined by population history. PLoS Genet. 7:e1002111. doi: 10.1371/journal.pgen.1002111.
163. Wrent, P., Rivas, E. M., Peinado, J. M., and de Silóniz, M. I. (2015). Development of an affordable typing method for Meyerozyma guilliermondii using microsatellite markers. Int. J. Food Microbiol. 217, 1-6. doi: 10.1016/j.ijfoodmicro.2015.10.008.
164. Wu, B., Buljic, A., and Hao, W. (2015). Extensive horizontal transfer and homologous recombination generate highly chimeric mitochondrial genomes in yeast. Mol. Biol. Evol. 32, 2559-2570. doi: 10.1093/molbev/msv127.
165. Yanai, T., and Sato, M. (1999). Isolation and properties of β-glucosidase produced by Debaryomyces hansenii and its application in winemaking. Am. J. Enol. Vitic. 50, 231-235.
166. Zara, G., Mannazzu, I., Del Caro, A., Budroni, M., Pinna, M. B., Murru, M., et al. (2014). Wine quality improvement through the combined utilisation of yeast hulls and Candida zemplinina/Saccharomyces cerevisiae mixed starter cultures. Aust. J. Grape Wine Res. 20, 199-207. doi: 10.1111/ajgw.12078.
167. Zeyl, C. (2004). Capturing the adaptive mutation in yeast. Res. Microbiol. 155, 217-223. doi: 10.1016/j.resmic.2003.12.006.
168. Zimmer, A., Durand, C., Loira, N., Durrens, P., Sherman, D. J., and Marullo, P. (2014). QTL dissection of lag phase in wine fermentation reveals a new translocation responsible for Saccharomyces cerevisiae adaptation to sulfite. PLoS ONE 9:e86298. doi: 10.1371/journal.pone.0086298.
169. Zott, K., Thibon, C., Bely, M., Lonvaud-Funel, A., Dubourdieu, D., and Masneuf-Pomarede, I. (2011). The grape must non-Saccharomyces microbial community: impact on volatile thiol release. Int. J. Food Microbiol. 151, 210-215. doi: 10.1016/j.ijfoodmicro.2011.08.026.