Novel brewing yeast hybrids: creation and application

Applied Microbiology and Biotechnology

Volumn 101, Issue 1, 2017, Pages 65-78

  Krogerus, Kristoffer ^a,b   Magalhães, Frederico ^a,b   Vidgren, Virve ^a   Gibson, Brian ^a  

^a VTT TECHNICAL RESEARCH CENTRE OF FINLAND   (Finland)

^b AALTO UNIVERSITY   (Finland)

Author keywords

Aroma; Brewing; Heterosis; Lager; Mating; S. eubayanus; Stability; Stress tolerance

Indexed keywords

BEER; CONVERGENCE OF NUMERICAL METHODS; FERMENTATION; MICROORGANISMS; ODORS; TEMPERATURE; YEAST;

AROMA; HETEROSIS; LAGER; MATING; S. EUBAYANUS; STRESS TOLERANCE;

BREWING;

MALTOTRIOSE; SUGAR;

ALCOHOL; BREWING INDUSTRY; EVOLUTIONARY BIOLOGY; FEASIBILITY STUDY; GENOME; HETEROSIS; HYBRID; HYBRIDIZATION; INDUSTRIAL ECOLOGY; ODOR; TOLERANCE; YEAST;

AROMA; ARTIFICIAL HYBRIDIZATION; BREWING; FERMENTATION; GENOME; GENOMIC INSTABILITY; HYBRIDIZATION; NONHUMAN; PHENOTYPE; REVIEW; SACCHAROMYCES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES EUBAYANUS; STRESS; TEMPERATURE; ALCOHOLIC BEVERAGE; CROSS BREEDING; GENETICS; METABOLIC ENGINEERING; METABOLISM; MICROBIOLOGY;

SACCHAROMYCES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES PASTORIANUS;

ALCOHOLIC BEVERAGES; CROSSES, GENETIC; FERMENTATION; INDUSTRIAL MICROBIOLOGY; METABOLIC ENGINEERING; SACCHAROMYCES;

EID: 84996844888     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-016-8007-5     Document Type: Review

References (135)

1. Aguilera J, Randez-Gil F, Prieto JA (2007) Cold response in Saccharomyces cerevisiae: new functions for old mechanisms. FEMS Microbiol Rev 31:327–341
2. Alexander W, Peris D, Pfannenstiel B, Opulente D, Kuang M, Hittinger C (2016) Efficient engineering of marker-free synthetic allotetraploids of Saccharomyces. Fungal Genet Biol 89:10–17
3. Almeida P, Gonçalves C, Teixeira S, Libkind D, Bontrager M, Masneuf-Pomarède I, Allbertin W, Durrens P, Sherman DJ, Marullo P, Hittinger CT, Gonçalves P, Sampaio JP (2014) A Gondwanan imprint on global diversity and domestication of wine and cider yeast Saccharomyces uvarum. Nat Commun 5:4044
4. Alves S Jr, Herberts R, Hollatz C (2007) Maltose and maltotriose active transport and fermentation by Saccharomyces cerevisiae. J Am Soc Brew Chem 65:99–104
5. Antunovics Z, Nguyen H-V, Gaillardin C, Sipiczki M (2005) Gradual genome stabilisation by progressive reduction of the Saccharomyces uvarum genome in an interspecific hybrid with Saccharomyces cerevisiae. FEMS Yeast Res 5:1141–1150
6. Baker E, Wang B, Bellora N, Peris D, Hulfachor A, Koshalek J, Adams M, Libkind D, Hittinger C (2015) The genome sequence of Saccharomyces eubayanus and the domestication of lager-brewing yeasts. Mol Biol Evol 32:2818–2831
7. Basso R, Alcarde A, Portugal C (2016) Could non-Saccharomyces yeasts contribute on innovative brewing fermentations? Food Res Int 86:112–120
8. Bellon J, Eglinton J, Siebert T, Pollnitz A, Rose L, de Barros LM, Chambers P (2011) Newly generated interspecific wine yeast hybrids introduce flavour and aroma diversity to wines. Appl Microbiol Biotechnol 91:603–612
9. Bellon J, Schmid F, Capone D, Dunn B, Chambers P (2013) Introducing a new breed of wine yeast: interspecific hybridisation between a commercial Saccharomyces cerevisiae wine yeast and Saccharomyces mikatae. PLoS One 8:e62053. doi:10.1371/journal.pone.0062053
10. Bellon J, Yang F, Day M, Inglis D, Chambers P (2015) Designing and creating Saccharomyces interspecific hybrids for improved, industry relevant, phenotypes. Appl Microbiol Biotechnol 99:8597–8609
11. Bilinski C, Russell I, Stewart G (1986) Analysis of sporulation in brewer’s yeast: induction of tetrad formation. J Inst Brew 92:594–598
12. Bing J, Han P, Liu W, Wang Q, Bai F (2014) Evidence for a far east Asian origin of lager beer yeast. Curr Biol 24:R380–R381
13. Bizaj E, Cordente A, Bellon J, Raspor P, Curtin C, Pretorius I (2012) A breeding strategy to harness flavour diversity of Saccharomyces interspecific hybrids and minimize hydrogen sulphide production. FEMS Yeast Res 12:456–465
14. Blieck L, Toye G, Dumortier F, Verstrepen K, Delvaux F, Thevelein J, Van Dijck P (2007) Isolation and characterization of brewer’s yeast variants with improved fermentation performance under high-gravity conditions. Appl Environ Microbiol 73:815–824
15. Bolat I, Romagnoli G, Zhu F, Pronk J, Daran J (2013) Functional analysis and transcriptional regulation of two orthologs of ARO10, encoding broad-substrate-specificity 2-oxo-acid decarboxylases, in the brewing yeast Saccharomyces pastorianus CBS1483. FEMS Yeast Res 13:505–517
16. Caesar R, Palmfeldt J, Gustafsson JS, Pettersson E, Hossein Hashemi S, Blomberg A (2007) Comparative proteomics of industrial lager yeast reveals differential expression of the cerevisiae and non-cerevisiae parts of their genomes. Proteomics 7:4135–4147
17. Canonico L, Agarbati A, Comitini F, Ciani M (2016) Torulaspora delbrueckii in the brewing process: a new approach to enhance bioflavour and to reduce ethanol content. Food Microbiol 56:45–51
18. Chen Z (2013) Genomic and epigenetic insights into the molecular bases of heterosis. Nat Rev Genet 14:471–482
19. Choi B, Jang K, Kim K (2002) Fermentation characteristics of brewing yeast HCS with glucoamylase expression by rare mating and beer analysis. Food Sci Biotechnol 11:34–39
20. Codón A, Gasent-Ramírez J, Benítez T (1995) Factors which affect the frequency of sporulation and tetrad formation in Saccharomyces cerevisiae baker’s yeast. Appl Environ Microbiol 61:630–638
21. da Silva T, Albertin W, Dillmann C, Bely M, la Guerche S, Giraud C, Huet S, Sicard D, Masneuf-Pomarède I, de Vienne D, Marullo P (2015) Hybridization within Saccharomyces genus results in homoeostasis and phenotypic novelty in winemaking conditions. PLoS One 10:e0123834. doi:10.1371/journal.pone.0123834
22. de Barros LM, Bellon J, Shirley N, Ganter P (2002) Evidence for multiple interspecific hybridization in Saccharomyces sensu stricto species. FEMS Yeast Res 1:323–331
23. Dornbusch H (1997) Prost! The story of German beer. Brewers Publications, Boulder
24. Dunn B, Sherlock G (2008) Reconstruction of the genome origins and evolution of the hybrid lager yeast Saccharomyces pastorianus. Genome Res 18:1610–1623
25. Dunn B, Paulish T, Stanbery A, Piotrowski J, Koniges G, Kroll E, Louis E, Liti G, Sherlock G, Rosenzweig F (2013) Recurrent rearrangement during adaptive evolution in an interspecific yeast hybrid suggests a model for rapid introgression. PLoS Genet 9(3):e1003366. doi:10.1371/journal.pgen.1003366
26. Ekberg J, Rautio J, Mattinen L, Vidgren V, Londesborough J, Gibson B (2013) Adaptive evolution of the lager brewing yeast Saccharomyces pastorianus for improved growth under hyperosmotic conditions and its influence on fermentation performance. FEMS Yeast Res 13:335–349
27. Fernández-Espinar M, Esteve-Zarzoso B, Querol A, Barrio E (2000) RFLP analysis of the ribosomal internal transcribed spacers and the 5.8S rRNA gene region of the genus Saccharomyces: a fast method for species identification and the differentiation of flor yeasts. Antonie Van Leeuwenhoek 78:87–97
28. Fu D, Xiao M, Hayward A, Jiang G, Zhu L, Zhou Q, Li J, Zhang M (2015) What is crop heterosis: new insights into an old topic. J Appl Genet 56:1–13
29. Fukuda N, Kaishima M, Ishii J, Kondo A, Honda S (2016) Continuous crossbreeding of sake yeasts using growth selection systems for a-type and α-type cells. AMB Expr 6:45. doi:10.1186/s13568-016-0216-x
30. Gallone B, Steensels J, Prahl T, Soriaga L, Saels V, Herrera-Malaver B, Merlevede A, Roncoroni M, Voordeckers K, Miraglia L, Teiling C, Steffy B, Taylor M, Schwartz A, Richardson T, White C, Baele G, Maere S, Verstrepen K (2016) Domestication and divergence of Saccharomyces cerevisiae beer yeasts. Cell 166:1397–1410
31. Gamero A, Tronchoni J, Querol A, Belloch C (2013) Production of aroma compounds by cryotolerant Saccharomyces species and hybrids at low and moderate fermentation temperatures. J Appl Microbiol 114:1405–1414
32. García-Ríos E, Querol A, Guillamón JM (2016) iTRAQ-based proteome profiling of Saccharomyces cerevisiae and cryotolerant species Saccharomyces uvarum and Saccharomyces kudriavzevii during low-temperature wine fermentation. J Proteome 146:70–79
33. Garcia Sanchez R, Solodovnikova N, Wendland J (2012) Breeding of lager yeast with Saccharomyces cerevisiae improves stress resistance and fermentation performance. Yeast 29:343–355
34. Gayevskiy V, Goddard M (2016) Saccharomyces eubayanus and Saccharomyces arboricola reside in North Island native New Zealand forests. Environ Microbiol 18:1137–1147
35. Gibson B, Storgårds E, Krogerus K, Vidgren V (2013) Comparative physiology and fermentation performance of Saaz and Frohberg lager yeast strains and the parental species Saccharomyces eubayanus. Yeast 30:255–266
36. Gibson B, Liti G (2015) Saccharomyces pastorianus: genomic insights inspiring innovation for industry. Yeast 32:17–27
37. Gibson B, Krogerus K, Ekberg J, Monroux A, Mattinen L, Rautio J, Vidgren V (2015) Variation in α-acetolactate production within the hybrid lager yeast group Saccharomyces pastorianus and the affirmation of the central role of the ILV6 gene. Yeast 32:301–316
38. Gjermansen C, Sigsgaard P (1981) Construction of a hybrid brewing strain of Saccharomyces carlsbergensis by mating of meiotic segregants. Carlsb Res Commun 46:1–11
39. Glendinning T (1899) Some practical aspects of the fermentable matter in beer. J Fed Inst Brew 5:20–34
40. Goddard MR, Greig D (2015) Saccharomyces cerevisiae: a nomadic yeast with no niche? FEMS Yeast Res 15. doi:10.1093/femsyr/fov009
41. Gonçalves P, Valério E, Correia C, de Almedia J, Sampaio J (2011) Evidence for divergent evolution of growth temperature preference in sympatric Saccharomyces species. PLoS One 6:e20739
42. Gonçalves M, Pontes A, Almeida P, Barbosa R, Serra M, Libkind D, Hutzler M, Gonçalves P, Sampaio J (2016) Distinct domestication trajectories in top-fermenting beer yeasts and wine yeasts. Curr Biol 26:2750–2761
43. González S, Barrio E, Gafner J, Querol A (2006) Natural hybrids from Saccharomyces cerevisiae, Saccharomyces bayanus and Saccharomyces kudriavzevii in wine fermentations. FEMS Yeast Res 6:1221–1234
44. González S, Barrio E, Querol A (2008) Molecular characterization of new natural hybrids of Saccharomyces cerevisiae and S. kudriavzevii in brewing. Appl Environ Microbiol 74:2314–2320
45. Greig D, Louis E, Borts R, Travisano M (2002) Hybrid speciation in experimental populations of yeast. Science 298:1773–1775
46. Hammond J, Eckersley K (1984) Fermentation properties of brewing yeast with killer character. J Inst Brew 90:167–177
47. Hansen J, Cherest H, Kielland-Brandt MC (1994) Two divergent MET10 genes, one from Saccharomyces cerevisiae and one from Saccharomyces carlsbergensis, encode the alpha subunit of sulfite reductase and specify potential binding sites for FAD and NADPH. J Bacteriol 176:6050–6058
48. He Y, Dong J, Yin H, Chen P, Lin H, Chen L (2014) Monitoring of the production of flavour compounds by analysis of the gene transcription involved in higher alcohol and ester formation by the brewer’s yeast Saccharomyces pastorianus using a multiplex RT-qPCR assay. J Inst Brew 120:119–126
49. Hebly M, Brickwedde A, Bolat I, Driessen M, de Hulster E, van den Broek M, Pronk J, Geertman J, Daran J, Daran-Lapujade P (2015) S. cerevisiae × S. eubayanus interspecific hybrid, best of both worlds and beyond. FEMS Yeast Res 15. doi:10.1093/femsyr/fov005
50. Hiraoka M, Watanabe K, Umezu K, Maki H (2000) Spontaneous loss of heterozygosity in diploid Saccharomyces cerevisiae cells. Genetics 156:1531–1548
51. Horinouchi T, Yoshikawa K, Kawaide R, Furusawa C, Nakao Y, Hirasawa T, Shimizu H (2010) Genome-wide expression analysis of Saccharomyces pastorianus orthologous genes using oligonucleotide microarrays. J Biosci Bioeng 110:602–607
52. Hornsey I (2003) A history of beer and brewing. Royal Society of Chemistry, Cambridge, p. 720
53. Hornsey IS (2012) Alcohol and its role in the evolution of human society. RSC Publishing, Cambridge
54. Huuskonen A, Markkula T, Vidgren V, Lima L, Mulder L, Geurts W, Walsh M, Londesborough J (2010) Selection from industrial lager yeast strains of variants with improved fermentation performance in very-high-gravity worts. Appl Environ Microbiol 76:1563–1573
55. Iijima K, Ogata T (2010) Construction and evaluation of self-cloning bottom-fermenting yeast with high SSU1 expression. J Appl Microbiol 109:1906–1913
56. James TC, Usher J, Campbell S, Bond U (2008) Lager yeasts possess dynamic genomes that undergo rearrangements and gene amplification in response to stress. Curr Genet 53:139–152
57. Janderová B, Cvrcková F, Bendová O (1990) Construction of the dextrin-degrading pof brewing yeast by protoplast fusion. J Basic Microbiol 30:499–505
58. Johnston J (1965) Breeding yeasts for brewing: II. Production of hybrid strains J Inst Brew 71:135–137
59. Krogerus K, Gibson B (2013) 125th anniversary review: diacetyl and its control during brewery fermentation. J Inst Brew 119:86–97
60. Krogerus K, Magalhães F, Vidgren V, Gibson B (2015) New lager yeast strains generated by interspecific hybridization. J Ind Microbiol Biotechnol 42:769–778
61. Krogerus K, Arvas M, De Chiara M, Magalhães F, Mattinen L, Oja M, Vidgren V, Yue J, Liti G, Gibson B (2016) Ploidy influences the functional attributes of de novo lager yeast hybrids. Appl Microbiol Biotechnol 100:7203–7222
62. Kumaran R, Yang S-Y, Leu J-Y (2013) Characterization of chromosome stability in diploid, polyploid and hybrid yeast cells. PLoS One 8:e68094
63. Landaud S, Helinck S, Bonnarme P (2008) Formation of volatile sulfur compounds and metabolism of methionine and other sulfur compounds in fermented food. Appl Microbiol Biotechnol 77:1191–1205
64. Landry CR, Hartl DL, Ranz JM (2007) Genome clashes in hybrids: insights from gene expression. Heredity 99:483–493
65. Le Jeune C, Lollier M, Demuyter C, Erny C, Legras J, Aigle M, Masneuf-Pomaréde I (2007) Characterization of natural hybrids of Saccharomyces cerevisiae and Saccharomyces bayanus var. uvarum. FEMS Yeast Res 7:540–549
66. Legras J, Karst F (2003) Optimisation of interdelta analysis for Saccharomyces cerevisiae strain characterisation. FEMS Microbiol Lett 221:249–255
67. Legras J, Merdinoglu D, Cornuet J, Karst F (2007) Bread, beer and wine: Saccharomyces cerevisiae diversity reflects human history. Mol Ecol 16:2091–2102
68. Libkind D, Hittinger C, Valerio E, Gonçalves C, Dover J, Johnston M, Gonçalves P, Sampaio J (2011) Microbe domestication and the identification of the wild genetic stock of lager-brewing yeast. Proc Natl Acad Sci U S A 108:14539–14544
69. Liti G, Peruffo A, James S, Roberts I, Louis E (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
70. Lopandic K, Pfliegler W, Tiefenbrunner W, Gangl H, Sipiczki M, Sterflinger K (2016) Genotypic and phenotypic evolution of yeast interspecies hybrids during high-sugar fermentation. Appl Microbiol Biotechnol 100:6331–6343
71. Lopes CA, Barrio E, Querol A (2010) Natural hybrids of S. cerevisiae x S. kudriavzevii share alleles with European wild populations of Saccharomyces kudriavzevii. FEMS Yeast Res 10:412–421
72. López-Malo M, Querol A, Guillamon J (2013) Metabolomic comparison of Saccharomyces cerevisiae and the cryotolerant species S. bayanus var. uvarum and S. kudriavzevii during wine fermentation at low temperature. PLoS One 8:e60135
73. Lucca M, Spencer J, de Figueroa L (2002) Glycerol and arabitol production by an intergeneric hybrid, PB2, obtained by protoplast fusion between Saccharomyces cerevisiae and Torulaspora delbrueckii. Appl Microbiol Biotechnol 59:472–476
74. Magalhães F, Vidgren V, Ruohonen L, Gibson B (2016) Maltose and maltotriose utilisation by group I strains of the hybrid lager yeast Saccharomyces pastorianus. FEMS Yeast Res 16. doi:10.1093/femsyr/fow053
75. Masneuf-Pomarède I, Bely M, Marullo P, Lonvaud-Funel A, Dubourdieu D (2010) Reassessment of phenotypic traits for Saccharomyces bayanus var. uvarum wine yeast strains. Int J Food Microbiol 139:79–86
76. Masneuf-Pomarède I, Le Jeune C, Durrens P, Lollier M, Aigle M, Dubourdieu D (2007) Molecular typing of wine strains Saccharomyces bayanus var. uvarum using microsatellite markers. Systems Appl Microbiol 30:345–354
77. Merlini L, Dudin O, Martin S (2013) Mate and fuse: how yeast cells do it. Open Biol 3:130008. doi:10.1098/rsob.130008
78. Mertens S, Steensels J, Saels V, de Rouck G, Aerts G, Verstrepen K (2015) A large set of newly created interspecific yeast hybrids increases aromatic diversity in lager beers. Appl Environ Microbiol 81:8202–8214
79. Michel M, Kopecka J, Meier-Dörnberg T, Zarnkow M, Jacob F, Hutzler M (2016) Screening for new brewing yeasts in the non-Saccharomyces sector with Torulaspora delbrueckii as model. Yeast 33:129–144
80. Mikkelsen JD, Sigsgaard P, Olsen A, Erdal K, Kielland-Brandt MC, Petersen JGL (1979) Thiaisoleucine resistant mutants in Saccharomyces carlsbergensis increase the content of D-amyl alcohol in beer. Carlsb Res Commun 44:219
81. Minato T, Yoshida S, Ishiguro T, Shimada E, Mizutani S, Kobayashi O, Yoshimoto H (2009) Expression profiling of the bottom fermenting yeast Saccharomyces pastorianus orthologous genes using oligonucleotide microarrays. Yeast 26:147–165
82. Monerawela C, James T, Wolfe K, Bond U (2015) Loss of lager specific genes and subtelomeric regions define two different Saccharomyces cerevisiae lineages for Saccharomyces pastorianus group I and II strains. FEMS Yeast Res 15. doi:10.1093/femsyr/fou008
83. Muir A, Harrison E, Wheals A (2011) A multiplex set of species-specific primers for rapid identification of members of the genus Saccharomyces. FEMS Yeast Res 11:552–563
84. Mukai N, Nishimori C, Fujishige I, Mizuno A, Takahashi T, Sato K (2001) Beer brewing using a fusant between a sake yeast and a brewer’s yeast. J Biosci Bioeng 91:482–486
85. Mukai N, Masaki K, Fujii T, Iefuhi H (2014) Single nucleotide polymorphisms of PAD1 and FDC1 show a positive relationship with ferulic acid decarboxylation ability among industrial yeasts used in alcoholic beverage production. J Biosci Bioeng 118:50–55
86. Nakao Y, Kanamori T, Itoh T, Kodama Y, Rainieri S, Nakamura N, Shimonaga T, Hattori M, Ashikari T (2009) Genome sequence of the lager brewing yeast, an interspecies hybrid. DNA Res 16:115–129
87. Naumov GI, James SA, Naumova E, Louis E, Roberts IN (2000) Three new species in the Saccharomyces sensu stricto complex: Saccharomyces cariocanus, Saccharomyces kudriavzevii, and Saccharomyces mikatae. Int J Syst Evol Microbiol 50:1931–1942
88. Naumov GI, Nguyen HV, Naumova ES, Michel A, Aigle M, Gaillardin C (2001) Genetic identification of Saccharomyces bayanus var. uvarum, a cider-fermenting yeast. Int J Food Microbiol 65:163–171
89. Nilsson-Tillgren T, Gjermansen C, Kielland-Brandt M, Petersen J, Holmberg S (1981) Genetic differences between Saccharomyces carlsbergensis and S. cerevisiae. Analysis of chromosome III by single chromosome-transfer. Carlsb Res Commun 46:65–76
90. Ogata T, Shikata-Myoshi M, Tadami H, Nakazawa N (2011) Isolation of meiotic segregants from a bottom fermenting yeast. J Inst Brew 117:199–205
91. Ogata T, Kobayashi M, Gibson BR (2013) Pilot scale brewing using self-cloning bottom-fermenting yeast with high SSU1 expression. J Inst Brew 119:17–22
92. Okuno M, Kajitani R, Ryusui R, Morimoto H, Kodama Y, Itoh T (2016) Next-generation sequencing analysis of lager brewing strains reveals the evolutionary history of interspecies hybridization. DNA Res 23:67–80
93. Paget C, Schwartz J, Delneri D (2014) Environmental systems biology of cold-tolerant phenotype in Saccharomyces species adapted to grow at different temperatures. Mol Ecol 23:5241–5257
94. Pedersen MB (1985) DNA sequence polymorphisms in the genus Saccharomyces. II. Analaysis of the gees RDN1, HIS4, LEU2 and Ty transposable elements in Carlsberg, Tuborg, and 22 Bavarian brewing strains. Carlsb Res Commun 50:262–272
95. Pérez-Través L, Lopes C, Barrio E, Querol A (2012) Evaluation of different genetic procedures for the generation of artificial hybrids in Saccharomyces genus for winemaking. Int J Food Microbiol 156:102–111
96. Peris D, Belloch C, Lopandić K, Álvarez-Pérez JM, Querol A, Barrio E (2012) The molecular characterization of new types of Saccharomyces cerevisiae x S. kudriavzevii hybrid yeasts unveils a high genetic diversity. Yeast 29:81–91
97. Peris D, Sylvester K, Libkind D, Gonçalves P, Sampaio J, Alexander W, Hittinger C (2014) Population structure and reticulate evolution of Saccharomyces eubayanus and its lager-brewing hybrids. Mol Ecol 23:2031–2045
98. Peris D, Langdon Q, Moriarty R, Sylvester K, Bontrager M, Charron G, Leducq J, Landry C, Libkind D, Hittinger C (2016) Complex ancestries of lager-brewing hybrids were shaped by standing variation in the wild yeast Saccharomyces eubayanus. PLoS Genet 12(7):e1006155. doi:10.1371/journal.pgen.1006155
99. Pfliegler W, Antunovics Z, Sipiczki M (2012) Double sterility barrier between Saccharomyces species and its breakdown in allopolyploid hybrids by chromosome loss. FEMS Yeast Res 12:703–718
100. Piotrowski J, Nagarajan S, Kroll E, Stanbery A, Chiotti K, Kruckeberg A, Dunn B, Sherlock G, Rosenzweig F (2012) Different selective pressures lead to different genomic outcomes as newly-formed hybrid yeasts evolve. BMC Evol Biol 12:46. doi:10.1186/1471-2148-12-46
101. Pires E, Teixeira J, Branyik T, Vicente A (2014) Yeast: the soul of beer’s aroma—a review of flavour-active esters and higher alcohols produced by the brewing yeast. Appl Microbiol Biotechnol 98:1937–1949
102. Plech M, de Visser J, Korona R (2014) Heterosis is prevalent among domesticated but not wild strains of Saccharomyces cerevisiae. G3 4:315–323
103. Rautio J, Londesborough J (2003) Maltose transport by brewer’s yeasts in brewer’s wort. J Inst Brew 109:251–261
104. Russell I, Hancock I, Stewart G (1983) Construction of dextrin fermentative yeast strains that do not produce phenolic off-flavours in beer. J Am Soc Brew Chem 41:45–51
105. Sahara T, Goda T, Ohgiya S (2002) Comprehensive expression analysis of time-dependent genetic responses in yeast cells to low temperature. J Biol Chem 277:50015–50021
106. Salvadó Z, Arroyo-López FN, Guillamón JM, Salazar G, Querol A, Barrio E (2011) Temperature adaptation markedly determines evolution within the genus Saccharomyces. Appl Environ Microbiol 77:2292–2302
107. Salvadó Z, Ramos-Alonso L, Tronchoni J, Penacho V, García-Ríos E, Morales P, Gonzalez R, Guillamón JM (2016) Genome-wide identification of genes involved in growth and fermentation activity at low temperature in Sacchaomyces cerevisiae. Int J Food Microbiol 236:38–46
108. Sampaio JP, Gonçalves P (2008) Natural populations of Saccharomyces kudriavzevii in Portugal are associated with oak bark and are sympatric with S. cerevisiae and S. paradoxus. Appl Environ Microbiol 74:2144–2152
109. Sato M, Kishimoto M, Watari J, Takashio M (2002) Breeding of brewer’s yeast by hybridization between a top-fermenting yeast Saccharomyces cerevisiae and a cryophilic yeast Saccharomyces bayanus. J Biosci Bioeng 93:509–511
110. Schade B, Jansen G, Whiteway M, Entian KD, Thomas DY (2004) Cold adaptation in budding yeast. Mol Biol Cell 15:5492–5502
111. Schnable P, Springer N (2013) Progress toward understanding heterosis in crop plants. Annu Rev Plant Biol 64:71–88
112. Sebastiani F, Barberio C, Casalone E, Cavalieri D, Polsinelli M (2002) Crosses between Saccharomyces cerevisiae and Saccharomyces bayanus generate fertile hybrids. Res Microbiol 153:53–58
113. Selmecki A, Maruvka Y, Richmond P, Guillet M, Shoresh N, Sorenson A, De S, Kishony R, Michor F, Dowell R, Pellman D (2015) Polyploidy can drive rapid adaptation in yeast. Nature 519:349–352
114. Shapira R, Levy T, Shaked S, Fridman E, David L (2014) Extensive heterosis in growth of yeast hybrids is explained by a combination of genetic models. Heredity 113:316–326
115. Snoek T, Picca Nicolino M, Van den Bremt S, Mertens S, Saels V, Verplaetse A, Steensels J, Verstrepen K (2015) Large-scale robot-assisted genome shuffling yields industrial Saccharomyces cerevisiae yeasts with increased ethanol tolerance. Biotechnol Biofuels 8:32
116. Spencer J, Spencer D (1977) Hybridization of non-sporulating and weakly sporulating strains of brewer’s and distiller’s yeasts. J Inst Brew 83:287–289
117. Spencer J, Spencer D, Whittington-Vaughan P, Miller R (1983) Use of mitochondrial mutants in the isolation of hybrids involving industrial yeast strains: IV. Characterization of an intergeneric hybrid, Saccharomyces diastaticus x Hansenula capsulata, obtained by protoplast fusion. Curr Genet 7:159–164
118. Steensels J, Meersman E, Snoek T, Saels V, Verstrepen K (2014) Large-scale selection and breeding to generate industrial yeasts with superior aroma production. Appl Environ Microbiol 80:6965–6975
119. Strejc J, Siříštova L, Karabín M, Almeida e Silva JB, Brányik B (2013) Production of alcohol-free beer with elevated amounts of flavouring compounds using lager yeast mutants. J Inst Brew 119:149–155
120. Stribny J, Querol A, Pérez-Torrado R (2016) Differences in enzymatic properties of the Saccharomyces kudriavzevii and Saccharomyces uvarum alcohol acetyltransferases and their impact on aroma-active compounds production. Front Microbiol 7:00897. doi:10.3389/fmicb.2016.00897
121. Tai SL, Daran-Lapujade P, Walsh MC, Pronk JT, Daran JM (2007) Acclimation of Saccharomyces cerevisiae to low temperature: a chemostat-based transcriptome analysis. Mol Biol Cell 18(12):5100–5112
122. Tamai Y, Momma T, Yoshimoto H, Kaneko Y (1998) Co-existence of two types of chromosome in the bottom fermenting yeast, Saccharomyces pastorianus. Yeast 14:923–933
123. Tirosh I, Reikhav S, Levy A, Barkai N (2009) A yeast hybrid provides insight into the evolution of gene expression regulation. Science 324:659–662
124. Tubb R, Searle B, Goodey A, Brown A (1981) Rare mating and transformation for construction of novel brewing yeasts. Proc 18th Congr Eur Brew Conv pp. 487–496
125. Twardowski T, Malyska A (2015) Uninformed and disinformed society and the GMO market. Trends Biotechnol 33:1–3
126. Urano N, Sahara H, Koshino S (1993) Conversion of a non-flocculent brewer’s yeast to flocculent ones by electrofusion: 1. Identification and characterization of the fusants by pulsed field gel electrophoresis J Biotechnol 28:237–247
127. Van den Broek M, Bolat I, Nijkamp J, Ramos E, Luttik M, Koopman F, Geertman J, de Ridder D, Pronk J, Daran J (2015) Chromosomal copy number variation in Saccharomyces pastorianus evidence for extensive genome dynamics in industrial lager brewing strains. Appl Environ Microbiol 81:6253–6267
128. van Solingen P, van der Plaat J (1977) Fusion of yeast spheroplasts. J Bacteriol 130:946–947
129. Vanderhaegen B, Nevin H, Verachtert H, Derdelinckx G (2006) The chemistry of beer aging—a critical review. Food Chem 95:357–381
130. Vidgren V, Multanen J, Ruohonen L, Londesborough J (2010) The temperature dependence of maltose transport in ale and lager strains of brewer’s yeast. FEMS Yeast Res 10:402–411
131. Vidgren V, Viljanen K, Mattinen L, Rautio J, Londesborough J (2014) Three Agt1 transporters from brewer’s yeasts exhibit different temperature dependencies for maltose transport over the range of brewery temperatures (0–20 °C). FEMS Yeast Res 14:601–613
132. Walther A, Hesselbart A, Wendland J (2014) Genome sequence of Saccharomyces carlsbergensis, the world’s first pure culture lager yeast. G3 4:783–793
133. Wendland J (2014) Lager yeast comes of age. Eukaryot Cell 13:1256–1265
134. Winge O (1944) On segregation and mutation in yeast. Compt Rend Trav Lab Carlsberg 24:79–96
135. Yoshida S, Hashimoto K, Shimada E, Ishiguro T, Minato T, Mizutani S, Yoshimoto H, Tashiro K, Kuhara S, Kobayashi O (2007) Identification of bottom-fermenting yeast genes expressed during lager beer fermentation. Yeast 24:599–606