A population genomics insight into the Mediterranean origins of wine yeast domestication

Molecular Ecology

Volumn 24, Issue 21, 2015, Pages 5412-5427

  Almeida, Pedro ^a   Barbosa, Raquel ^a   Zalar, Polona ^b   Imanishi, Yumi ^c   Shimizu, Kiminori ^d   Turchetti, Benedetta ^e   Legras, Jean Luc ^f   Serra, Marta ^a   Dequin, Sylvie ^f   Couloux, Arnaud ^g   Guy, Julie ^g   Bensasson, Douda ^h   Gonçalves, Paula ^a   Sampaio, José Paulo ^a  

^a UNIVERSIDADE NOVA DE LISBOA   (Portugal)

^b UNIVERSITY OF LJUBLJANA   (Slovenia)

^c KANTO GAKUIN UNIVERSITY   (Japan)

^d CHIBA UNIVERSITY   (Japan)

^e UNIVERSITY OF PERUGIA   (Italy)

^f SPO   (France)

^g DIF   (France)

^h UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

comparative genomics; domestication fingerprints; microbe domestication; microbe population genomics; yeast molecular ecology

Indexed keywords

FUNGAL DNA; MICROSATELLITE DNA; RIBOSOMAL SPACER DNA;

BIOLOGICAL MODEL; DNA SEQUENCE; EUROPE; FUNGAL GENOME; GENETIC VARIATION; GENETICS; MICROBIOLOGY; MOLECULAR EVOLUTION; OAK; PHYLOGENY; POPULATION GENETICS; SACCHAROMYCES CEREVISIAE; SINGLE NUCLEOTIDE POLYMORPHISM; SOUTHERN EUROPE; WINE;

DNA, FUNGAL; DNA, RIBOSOMAL SPACER; EUROPE; EVOLUTION, MOLECULAR; GENETIC VARIATION; GENETICS, POPULATION; GENOME, FUNGAL; MEDITERRANEAN REGION; MICROSATELLITE REPEATS; MODELS, GENETIC; PHYLOGENY; POLYMORPHISM, SINGLE NUCLEOTIDE; QUERCUS; SACCHAROMYCES CEREVISIAE; SEQUENCE ANALYSIS, DNA; WINE;

EID: 84945452256     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/mec.13341     Document Type: Article

References (63)

1. Almeida P, Gonçalves C, Teixeira S, et al,. (2014) A Gondwanan imprint on global diversity and domestication of wine and cider yeast Saccharomyces uvarum. Nature Communications, 5, 4044.
2. Bergström A, Simpson JT, Salinas F, et al,. (2014) A high-definition view of functional genetic variation from natural yeast genomes. Molecular Biology and Evolution, 31, 872-888.
3. Bing J, Han P-J, Liu W-Q, Wang Q-M, Bai F-Y, (2014) Evidence for a Far East Asian origin of lager beer yeast. Current Biology, 24, R380-R381.
4. Bradley RK, Roberts A, Smoot M, et al,. (2009) Fast statistical alignment. PLoS Computational Biology, 5, e1000392.
5. Cavalieri D, McGovern PE, Hartl DL, Mortimer R, Polsinelli M, (2003) Evidence for S. cerevisiae fermentation in ancient wine. Journal of Molecular Evolution, 57 (Suppl 1), S226-S232.
6. Charron G, Leducq J-B, Bertin C, Dubé AK, Landry CR, (2014) Exploring the northern limit of the distribution of Saccharomyces cerevisiae and Saccharomyces paradoxus in North America. FEMS Yeast Research, 14, 281-288.
7. Cheeseman K, Ropars J, Renault P, et al,. (2014) Multiple recent horizontal transfers of a large genomic region in cheese making fungi. Nature Communications, 5, 2876.
8. Cornille A, Gladieux P, Smulders MJM, et al,. (2012) New insight into the history of domesticated apple: secondary contribution of the European wild apple to the genome of cultivated varieties. PLoS Genetics, 8, e1002703.
9. Cromie GA, Hyma KE, Ludlow CL, et al,. (2013) Genomic sequence diversity and population structure of Saccharomyces cerevisiae assessed by RAD-seq. G3 (Bethesda, Md.), 3, 2163-2171.
10. Doebley JF, Gaut BS, Smith BD, (2006) The molecular genetics of crop domestication. Cell, 127, 1309-1321.
11. Douglas GL, Klaenhammer TR, (2010) Genomic evolution of domesticated microorganisms. Annual Review of Food Science and Technology, 1, 397-414.
12. Evanno G, Regnaut S, Goudet J, (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology, 14, 2611-2620.
13. Falush D, Stephens M, Pritchard JK, (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics, 164, 1567-1587.
14. Fay JC, Benavides JA, (2005) Evidence for domesticated and wild populations of Saccharomyces cerevisiae. PLoS Genetics, 1, 66-71.
15. Galeote V, Novo M, Salema-Oom M, et al,. (2010) FSY1, a horizontally transferred gene in the Saccharomyces cerevisiae EC1118 wine yeast strain, encodes a high-affinity fructose/H+ symporter. Microbiology, 156, 3754-3761.
16. Galeote V, Bigey F, Beyne E, et al,. (2011) Amplification of a Zygosaccharomyces bailii DNA Segment in wine yeast genomes by extrachromosomal circular DNA formation (N Nikolaidis, Ed,). PLoS One, 6, e17872.
17. Gibbons JG, Salichos L, Slot JC, et al,. (2012) The evolutionary imprint of domestication on genome variation and function of the filamentous fungus Aspergillus oryzae. Current Biology, 22, 1403-1409.
18. Gutenkunst RN, Hernandez RD, Williamson SH, Bustamante CD, (2009) Inferring the joint demographic history of multiple populations from multidimensional SNP frequency data (G McVean, Ed,). PLoS Genetics, 5, e1000695.
19. Hewitt GM, (2004) The structure of biodiversity-insights from molecular phylogeography. Frontiers in Zoology, 1, 4.
20. Hornsey IS, (2003) A History of Beer and Brewing. Royal Society of Chemistry paperbacks, Cambridge, UK.
21. Hornsey IS, (2007) The Chemistry and Biology of Winemaking. Royal Society of Chemistry, Cambridge, UK.
22. Hudson RR, (2002) Generating samples under a Wright-Fisher neutral model of genetic variation. Bioinformatics, 18, 337-338.
23. Huson DH, Bryant D, (2006) Application of phylogenetic networks in evolutionary studies. Molecular Biology and Evolution, 23, 254-267.
24. Hutter S, Vilella AJ, Rozas J, (2006) Genome-wide DNA polymorphism analyses using VariScan. BMC Bioinformatics, 7, 409.
25. Hyma KE, Fay JC, (2013) Mixing of vineyard and oak-tree ecotypes of Saccharomyces cerevisiae in North American vineyards. Molecular Ecology, 22, 2917-2930.
26. Hyma KE, Saerens SM, Verstrepen KJ, Fay JC, (2011) Divergence in wine characteristics produced by wild and domesticated strains of Saccharomyces cerevisiae. FEMS Yeast Research, 11, 540-551.
27. Joffe AH, (1998) Alcohol and social complexity in ancient Western Asia. Current Anthropology, 39, 297-322.
28. Johnson LJ, Koufopanou V, Goddard MR, et al,. (2004) Population genetics of the wild yeast Saccharomyces paradoxus. Genetics, 166, 43-52.
29. Kamvar ZN, Tabima JF, Grünwald NJ, (2014) Poppr: an R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ, 2, e281.
30. Lawson DJ, Hellenthal G, Myers S, Falush D, (2012) Inference of population structure using dense haplotype data. PLoS Genetics, 8, e1002453.
31. Leducq J-B, Charron G, Samani P, et al,. (2014) Local climatic adaptation in a widespread microorganism. Proceedings Biological Sciences/The Royal Society, 281, 20132472.
32. Legras J-L, Merdinoglu D, Cornuet J-M, Karst F, (2007) Bread, beer and wine: Saccharomyces cerevisiae diversity reflects human history. Molecular Ecology, 16, 2091-2102.
33. Li H, Durbin R, (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics (Oxford, England), 25, 1754-1760.
34. Li H, Handsaker B, Wysoker A, et al,. (2009) The sequence alignment/map format and SAMtools. Bioinformatics (Oxford, England), 25, 2078-2079.
35. Libkind D, Hittinger CT, Valerio E, et al,. (2011) Microbe domestication and the identification of the wild genetic stock of lager-brewing yeast. Proceedings of the National Academy of Sciences, 108, 14539-14544.
36. Liti G, Barton DBH, Louis EJ, (2006) Sequence diversity, reproductive isolation and species concepts in saccharomyces. Genetics, 174, 839-850.
37. Liti G, Carter DM, Moses AM, et al,. (2009) Population genomics of domestic and wild yeasts. Nature, 458, 337-341.
38. Lynch M, Sung W, Morris K, et al,. (2008) A genome-wide view of the spectrum of spontaneous mutations in yeast. Proceedings of the National Academy of Sciences, 105, 9272-9277.
39. Marsit S, Mena A, Bigey F, et al,. (2015) Evolutionary advantage conferred by an Eukaryote-to-Eukaryote gene transfer event in wine yeasts. Molecular Biology and Evolution, 32, 1695-1707.
40. McGovern PE, (2003) Ancient Wine: the Search for the Origins of Viniculture. Princeton University Press, Princeton, New Jersey.
41. McGovern PE, (2009) Uncorking the Past: the Quest for Wine, Beer, and Other Alcoholic Beverages. University of California Press, Berkeley, California.
42. McGovern PE, Glusker DL, Exner LJ, Voigt MM, (1996) Neolithic resinated wine. Nature, 381, 480-481.
43. McGovern PE, Zhang J, Tang J, et al,. (2004) Fermented beverages of pre- and proto-historic China. Proceedings of the National Academy of Sciences of the United States of America, 101, 17593-17598.
44. McGovern PE, Luley BP, Rovira N, et al,. (2013) Beginning of viniculture in France. Proceedings of the National Academy of Sciences of the United States of America, 110, 10147-10152.
45. Michel RH, McGovern PE, Badler VR, (1992) Chemical evidence for ancient beer. Nature, 360, 24.
46. Naumov GI, Naumova ES, Sniegowski PD, (1998) Saccharomyces paradoxus and Saccharomyces cerevisiae are associated with exudates of North American oaks. Canadian Journal of Microbiology, 44, 1045-1050.
47. 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. Proceedings of the National Academy of Sciences of the United States of America, 106, 16333-16338.
48. Pretorius IS, (2000) Tailoring wine yeast for the new millennium: novel approaches to the ancient art of winemaking. Yeast (Chichester, England), 16, 675-729.
49. Pritchard JK, Stephens M, Donnelly P, (2000) Inference of population structure using multilocus genotype data. Genetics, 155, 945-959.
50. R Core Team (2013) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
51. Salzberg SL, Phillippy AM, Zimin A, et al,. (2012) GAGE: a critical evaluation of genome assemblies and assembly algorithms. Genome Research, 22, 557-567.
52. 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. Applied and Environmental Microbiology, 74, 2144-2152.
53. Samuel D, (1996) Investigation of ancient Egyptian baking and brewing methods by correlative microscopy. Science, 273, 488-490.
54. Samuel D, (2000) Brewing and baking. In: Ancient Egyptian Materials and Technology, pp. 537-576. Cambridge University Press, Cambridge, New York.
55. Schacherer J, Shapiro JA, Ruderfer DM, Kruglyak L, (2009) Comprehensive polymorphism survey elucidates population structure of Saccharomyces cerevisiae. Nature, 458, 342-345.
56. Sniegowski PD, Dombrowski PG, 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 Research, 1, 299-306.
57. Stamatakis A, (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics (Oxford, England), 22, 2688-2690.
58. Strope PK, Skelly DA, Kozmin SG, 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 Research, 25, 762-774.
59. Tamura K, Peterson D, Peterson N, et al,. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28, 2731-2739.
60. Thornton K, (2003) Libsequence: a C++ class library for evolutionary genetic analysis. Bioinformatics (Oxford, England), 19, 2325-2327.
61. Valamoti SM, Mangafa M, Koukouli-Chrysanthaki C, Malamidou D, (2007) Grape-pressings from northern Greece: the earliest wine in the Aegean? Antiquity, 81, 54-61.
62. Wang Q-M, Liu W-Q, Liti G, Wang S-A, Bai F-Y, (2012) Surprisingly diverged populations of Saccharomyces cerevisiae in natural environments remote from human activity. Molecular Ecology, 21, 5404-5417.
63. Zerbino DR, Birney E, (2008) Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Research, 18, 821-829.