Trait variation in yeast is defined by population history

PLoS Genetics

Volumn 7, Issue 6, 2011, Pages

  Warringer, Jonas ^a,b   Zörgö, Enikö ^b   Cubillos, Francisco A ^c   Zia, Amin ^d   Gjuvsland, Arne ^b   Simpson, Jared T ^e   Forsmark, Annabelle ^a   Durbin, Richard ^e   Omholt, Stig W ^b   Louis, Edward J ^c   Liti, Gianni ^c   Moses, Alan ^d   Blomberg, Anders ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

^c UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^d UNIVERSITY OF TORONTO   (Canada)

^e WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL PROTEIN; GALACTOSE; PROTEIN GAL3; UNCLASSIFIED DRUG;

ALLELE; ARTICLE; CONTROLLED STUDY; FUNGAL GENE; FUNGAL GENETICS; FUNGAL STRAIN; GAL3 GENE; GENE MAPPING; GENETIC DRIFT; GENETIC SELECTION; GENETIC TRAIT; GENETIC VARIABILITY; GEOGRAPHICAL VARIATION (SPECIES); NONHUMAN; PHENOTYPE; SACCHAROMYCES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES PARADOXUS; SIGNAL TRANSDUCTION; SPECIES DIFFERENCE; YEAST; AFRICA; CELL PROLIFERATION; CYTOLOGY; ECOLOGY; EVOLUTION; GENETICS; METABOLISM; QUANTITATIVE TRAIT LOCUS;

SACCHAROMYCES CEREVISIAE; SACCHAROMYCETALES;

AFRICA, WESTERN; ALLELES; BIOLOGICAL EVOLUTION; CELL PROLIFERATION; ECOLOGY; FUNGAL PROTEINS; GALACTOSE; GENETIC VARIATION; METABOLIC NETWORKS AND PATHWAYS; PHENOTYPE; QUANTITATIVE TRAIT LOCI; SACCHAROMYCES; SACCHAROMYCES CEREVISIAE; SELECTION, GENETIC; SPECIES SPECIFICITY;

EID: 79959847334     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002111     Document Type: Article

References (54)

1. Dujon B, (2010) Yeast evolutionary genomics. Nat Rev Genet 11: 512-524.
2. Costanzo M, Baryshnikova A, Bellay J, Kim Y, Spear ED, et al. (2010) The genetic landscape of a cell. Science 327: 425-431.
3. Giaever G, Chu AM, Ni L, Connelly C, Riles L, et al. (2002) Functional profiling of the Saccharomyces cerevisiae genome. Nature 418: 387-391.
4. Li Z, Vizeacoumar FJ, Bahr S, Li J, Warringer J, et al. (2011) Systematic exploration of essential yeast gene function with temperature-sensitive mutants. Nat Biotechnol.
5. Mnaimneh S, Davierwala AP, Haynes J, Moffat J, Peng WT, et al. (2004) Exploration of essential gene functions via titratable promoter alleles. Cell 118: 31-44.
6. Schuldiner M, Collins SR, Thompson NJ, Denic V, Bhamidipati A, et al. (2005) Exploration of the function and organization of the yeast early secretory pathway through an epistatic miniarray profile. Cell 123: 507-519.
7. Sopko R, Huang D, Preston N, Chua G, Papp B, et al. (2006) Mapping pathways and phenotypes by systematic gene overexpression. Mol Cell 21: 319-330.
8. Brem RB, Kruglyak L, (2005) The landscape of genetic complexity across 5,700 gene expression traits in yeast. Proc Natl Acad Sci U S A 102: 1572-1577.
9. Brem RB, Storey JD, Whittle J, Kruglyak L, (2005) Genetic interactions between polymorphisms that affect gene expression in yeast. Nature 436: 701-703.
10. Gerke JP, Chen CT, Cohen BA, (2006) Natural isolates of Saccharomyces cerevisiae display complex genetic variation in sporulation efficiency. Genetics 174: 985-997.
11. Liti G, Haricharan S, Cubillos FA, Tierney AL, Sharp S, et al. (2009) Segregating YKU80 and TLC1 alleles underlying natural variation in telomere properties in wild yeast. PLoS Genet 5: e1000659 doi:10.1371/journal.pgen.1000659.
12. Perlstein EO, Ruderfer DM, Roberts DC, Schreiber SL, Kruglyak L, (2007) Genetic basis of individual differences in the response to small-molecule drugs in yeast. Nat Genet 39: 496-502.
13. Steinmetz LM, Sinha H, Richards DR, Spiegelman JI, Oefner PJ, et al. (2002) Dissecting the architecture of a quantitative trait locus in yeast. Nature 416: 326-330.
14. Ruderfer DM, Pratt SC, Seidel HS, Kruglyak L, (2006) Population genomic analysis of outcrossing and recombination in yeast. Nat Genet 38: 1077-1081.
15. Tsai IJ, Bensasson D, Burt A, Koufopanou V, (2008) Population genomics of the wild yeast Saccharomyces paradoxus: Quantifying the life cycle. Proc Natl Acad Sci U S A 105: 4957-4962.
16. Liti G, Carter DM, Moses AM, Warringer J, Parts L, et al. (2009) Population genomics of domestic and wild yeasts. Nature 458: 337-341.
17. Wang S, Bai F, (2008) Saccharomyces arboricolus sp. nov., a yeast species from tree bark. Int J Syst Evol Microbiol 58: 510-514.
18. Warringer J, Anevski D, Liu B, Blomberg A, (2008) Chemogenetic fingerprinting by analysis of cellular growth dynamics. BMC Chem Biol 8: 3.
19. Warringer J, Ericson E, Fernandez L, Nerman O, Blomberg A, (2003) High-resolution yeast phenomics resolves different physiological features in the saline response. Proc Natl Acad Sci U S A 100: 15724-15729.
20. Novak M, Pfeiffer T, Lenski RE, Sauer U, Bonhoeffer S, (2006) Experimental tests for an evolutionary trade-off between growth rate and yield in E. coli. Am Nat 168: 242-251.
21. Bell G, (2010) Experimental genomics of fitness in yeast. Proc Biol Sci 277: 1459-1467.
22. Wong WW, Tran LM, Liao JC, (2009) A hidden square-root boundary between growth rate and biomass yield. Biotechnol Bioeng 102: 73-80.
23. Kellis M, Patterson N, Endrizzi M, Birren B, Lander ES, (2003) Sequencing and comparison of yeast species to identify genes and regulatory elements. Nature 423: 241-254.
24. Replansky T, Koufopanou V, Greig D, Bell G, (2008) Saccharomyces sensu stricto as a model system for evolution and ecology. Trends Ecol Evol 23: 494-501.
25. Barnett JA, Payne RW, Yarrow D, (2000) Yeasts: Characteristics and identification Cambridge, UK Cambridge University Press.
26. Cubillos FA, Billi E, Zorgo E, Parts L, Fargier P, et al. (2011) Assessing the complex architecture of polygenic traits in diverged yeast populations. Mol Ecol 20: 1401-1413.
27. Fay JC, McCullough HL, Sniegowski PD, Eisen MB, (2004) Population genetic variation in gene expression is associated with phenotypic variation in Saccharomyces cerevisiae. Genome Biol 5: R26.
28. Naumov GI, Serpova EV, Naumova ES, (2006) [A genetically isolated population of Saccharomyces cerevisiae in Malaysia]. Mikrobiologiia 75: 245-249.
29. Wu H, Ito K, Shimoi H, (2005) Identification and characterization of a novel biotin biosynthesis gene in Saccharomyces cerevisiae. Appl Environ Microbiol 71: 6845-6855.
30. Lohr D, Venkov P, Zlatanova J, (1995) Transcriptional regulation in the yeast GAL gene family: a complex genetic network. Faseb J 9: 777-787.
31. Hittinger CT, Goncalves P, Sampaio JP, Dover J, Johnston M, et al. (2010) Remarkably ancient balanced polymorphisms in a multi-locus gene network. Nature.
32. Hittinger CT, Rokas A, Carroll SB, (2004) Parallel inactivation of multiple GAL pathway genes and ecological diversification in yeasts. Proceedings of the National Academy of Sciences of the United States of America 101: 14144-14149.
33. Winston F, Dollard C, Ricupero-Hovasse SL, (1995) Construction of a set of convenient Saccharomyces cerevisiae strains that are isogenic to S288C. Yeast 11: 53-55.
34. Johnston M, Davis RW, (1984) Sequences that regulate the divergent GAL1-GAL10 promoter in Saccharomyces cerevisiae. Mol Cell Biol 4: 1440-1448.
35. Fogel S, Welch JW, (1982) Tandem gene amplification mediates copper resistance in yeast. Proc Natl Acad Sci U S A 79: 5342-5346.
36. Kim HS, Fay JC, (2007) Genetic variation in the cysteine biosynthesis pathway causes sensitivity to pharmacological compounds. Proc Natl Acad Sci U S A 104: 19387-19391.
37. Daran-Lapujade P, Daran JM, Luttik MA, Almering MJ, Pronk JT, et al. (2009) An atypical PMR2 locus is responsible for hypersensitivity to sodium and lithium cations in the laboratory strain Saccharomyces cerevisiae CEN.PK113-7D. FEMS Yeast Res 9: 789-792.
38. Doniger SW, Kim HS, Swain D, Corcuera D, Williams M, et al. (2008) A catalog of neutral and deleterious polymorphism in yeast. PLoS Genet 4: e1000183 doi:10.1371/journal.pgen.1000183.
39. Stern DL, Orgogozo V, (2009) Is genetic evolution predictable? Science 323: 746-751.
40. Zewail A, Xie MW, Xing Y, Lin L, Zhang PF, et al. (2003) Novel functions of the phosphatidylinositol metabolic pathway discovered by a chemical genomics screen with wortmannin. Proc Natl Acad Sci U S A 100: 3345-3350.
41. Wayne RK, Ostrander EA, (2007) Lessons learned from the dog genome. Trends Genet 23: 557-567.
42. Sampaio JP, Goncalves 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.
43. 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 Res 1: 299-306.
44. Kvitek DJ, Will JL, Gasch AP, (2008) Variations in stress sensitivity and genomic expression in diverse S. cerevisiae isolates. PLoS Genet 4: e1000223 doi:10.1371/journal.pgen.1000223.
45. Landry CR, Townsend JP, Hartl DL, Cavalieri D, (2006) Ecological and evolutionary genomics of Saccharomyces cerevisiae. Mol Ecol 15: 575-591.
46. Schacherer J, Shapiro JA, Ruderfer DM, Kruglyak L, (2009) Comprehensive polymorphism survey elucidates population structure of Saccharomyces cerevisiae. Nature 458: 342-345.
47. Ehrenreich IM, Torabi N, Jia Y, Kent J, Martis S, et al. (2010) Dissection of genetically complex traits with extremely large pools of yeast segregants. Nature 464: 1039-1042.
48. Dowell RD, Ryan O, Jansen A, Cheung D, Agarwala S, et al. (2010) Genotype to phenotype: a complex problem. Science 328: 469.
49. Deutschbauer AM, Davis RW, (2005) Quantitative trait loci mapped to single-nucleotide resolution in yeast. Nat Genet 37: 1333-1340.
50. Mortimer RK, Johnston JR, (1986) Genealogy of principal strains of the yeast genetic stock center. Genetics 113: 35-43.
51. Benjamini Y, Hochberg Y, (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society 57: 289-300.
52. Eisen MB, Spellman PT, Brown PO, Botstein D, (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A 95: 14863-14868.
53. Naumova ES, Turakainen H, Naumov GI, Korhola M, (1996) Superfamily of alpha-galactosidase MEL genes of the Saccharomyces sensu stricto species complex. Mol Gen Genet 253: 111-117.
54. Simpson JT, Durbin R, (2010) Efficient construction of an assembly string graph using the FM-index. Bioinformatics 26: i367-373.