Heterosis is prevalent among domesticated but not wild strains of Saccharomyces cerevisiae

G3: Genes, Genomes, Genetics

Volumn 4, Issue 2, 2014, Pages 315-323

  Plech, Marcin ^a,b   de Visser, J Arjan G M ^b   Korona, Ryszard ^a  

^a JAGIELLONIAN UNIVERSITY   (Poland)

^b WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

Genetic load; Heterosis; Sequence divergence

Indexed keywords

ARTICLE; DELETION MUTANT; DOMESTICATION; FUNGAL GENOME; FUNGAL STRAIN; GENE SEQUENCE; HABITAT; HETEROSIS; HETEROZYGOTE; HOMOZYGOTE; HYBRID; NONHUMAN; SACCHAROMYCES CEREVISIAE;

GENETIC LOAD; HETEROSIS; SEQUENCE DIVERGENCE;

GENETIC LOAD; GENOME, FUNGAL; HYBRID VIGOR; HYBRIDIZATION, GENETIC; MUTATION; PHYLOGENY; SACCHAROMYCES CEREVISIAE; SELECTION, GENETIC;

EID: 84894574236     PISSN: None     EISSN: 21601836     Source Type: Journal    
DOI: 10.1534/g3.113.009381     Document Type: Article

References (51)

1. Agrawal, A. F., and M. C. Whitlock, 2010 Environmental duress and epistasis: how does stress affect the strength of selection on new mutations? Trends Ecol. Evol. 25: 450-458.
2. Bataillon, T., and M. Kirkpatrick, 2000 Inbreeding depression due to mildly deleterious mutations in finite populations: size does matter. Genet. Res. 75: 75-81.
3. Charlesworth, D., and B. Charlesworth, 1987 Inbreeding depression and its evolutionary consequences. Annu. Rev. Ecol. Syst. 18: 237-268.
4. Charlesworth, D., and J. H. Willis, 2009 The genetics of inbreeding depression. Nat. Rev. Genet. 10: 783-796.
5. Cruz, F., C. Vila, and M. T. Webster, 2008 The legacy of domestication: accumulation of deleterious mutations in the dog genome. Mol. Biol. Evol. 25: 2331-2336.
6. Cubillos, F. A., E. J. Louis, and G. Liti, 2009 Generation of a large set of genetically tractable haploid and diploid Saccharomyces strains. FEMS Yeast Res. 9: 1217-1225.
7. Cubillos, F. A., E. Billi, E. Zorgo, L. Parts, P. Fargier et al., 2011 Assessing the complex architecture of polygenic traits in diverged yeast populations. Mol. Ecol. 20: 1401-1413.
8. de Visser, J. A., J. Hermisson, G. P. Wagner, L. Ancel Meyers, H. Bagheri-Chaichian et al., 2003 Perspective: Evolution and detection of genetic robustness. Evolution Int J Org Evolution 57: 1959-1972.
9. Dettman, J. R., C. Sirjusingh, L. M. Kohn, and J. B. Anderson, 2007 Incipient speciation by divergent adaptation and antagonistic epistasis in yeast. Nature 447: 585-588.
10. Diamond, J., 2002 Evolution, consequences and future of plant and animal domestication. Nature 418: 700-707.
11. Diezmann, S., and F. S. Dietrich, 2009 Saccharomyces cerevisiae: population divergence and resistance to oxidative stress in clinical, domesticated and wild isolates. PLoS ONE 4: e5317.
12. Doebley, J. F., B. S. Gaut, and B. D. Smith, 2006 The molecular genetics of crop domestication. Cell 127: 1309-1321.
13. Dowell, R. D., O. Ryan, A. Jansen, D. Cheung, S. Agarwala et al., 2010 Genotype to phenotype: a complex problem. Science 328: 469.
14. Eyre-Walker, A., R. L. Gaut, H. Hilton, D. L. Feldman, and B. S. Gaut, 1998 Investigation of the bottleneck leading to the domestication of maize. Proc. Natl. Acad. Sci. USA 95: 4441-4446.
15. Fay, J. C., and J. A. Benavides, 2005 Evidence for domesticated and wild populations of Saccharomyces cerevisiae. PLoS Genet. 1: 66-71.
16. Frankham, R., J. D. Ballou, M. D. Eldridge, R. C. Lacy, K. Ralls et al., 2011 Predicting the probability of outbreeding depression. Conserv. Biol. 25: 465-475.
17. Glemin, S., J. Ronfort, and T. Bataillon, 2003 Patterns of inbreeding depression and architecture of the load in subdivided populations. Genetics 165: 2193-2212.
18. Gu, Z., L. David, D. Petrov, T. Jones, R. W. Davis et al., 2005 Elevated evolutionary rates in the laboratory strain of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 102: 1092-1097.
19. Haag, C. R., and D. Roze, 2007 Genetic load in sexual and asexual diploids: segregation, dominance and genetic drift. Genetics 176: 1663-1678.
20. Haldane, J. B. S., 1937 The effect of variation on fitness. Am. Nat. 71: 337-349.
21. Hampsey, M., 1997 A review of phenotypes in Saccharomyces cerevisiae. Yeast 13: 1099-1133.
22. Hedrick, P. W., 2012 What is the evidence for heterozygote advantage selection? Trends Ecol. Evol. 27: 698-704.
23. Hill, W., and A. Robertson, 1966 The effect of linkage on limits to artificial selection. Genet. Res. 8: 269-294.
24. Hoffmann, A. A., and P. A. Parsons, 1991 Evolutionary genetics and environmental stress, Oxford University Press, Oxford.
25. Hyma, K. E., S. M. Saerens, K. J. Verstrepen, and J. C. Fay, 2011 Divergence in wine characteristics produced by wild and domesticated strains of Saccharomyces cerevisiae. FEMS Yeast Res. 11: 540-551.
26. Johnston, J. R., 1994 Molecular genetics of yeast, Oxford University Press, Oxford.
27. Johnston, S. E., J. Gratten, C. Berenos, J. G. Pilkington, T. H. Clutton-Brock et al., 2013 Life history trade-offs at a single locus maintain sexually selected genetic variation. Nature 502: 93-95.
28. Kacser, H., and J. A. Burns, 1981 The molecular basis of dominance. Genetics 97: 639-666.
29. Kawecki, T. J., N. H. Barton, and J. D. Fry, 1997 Mutational collapse of fitness in marginal habitats and the evolution of ecological specialisation. J. Evol. Biol. 10: 407-429.
30. Krieger, U., Z. B. Lippman, and D. Zamir, 2010 The flowering gene SINGLE FLOWER TRUSS drives heterosis for yield in tomato. Nat. Genet. 42: 459-463.
31. Lawless, C., D. J. Wilkinson, A. Young, S. G. Addinall, and D. A. Lydall, 2010 Colonyzer: automated quantification of micro-organism growth characteristics on solid agar. BMC Bioinformatics 11: 287.
32. Legras, J. L., D. Merdinoglu, J. M. Cornuet, and F. Karst, 2007 Bread, beer and wine: Saccharomyces cerevisiae diversity reflects human history. Mol. Ecol. 16: 2091-2102.
33. Libkind, D., C. T. Hittinger, E. Valerio, C. Goncalves, J. Dover et al., 2011 Microbe domestication and the identification of the wild genetic stock of lager-brewing yeast. Proc. Natl. Acad. Sci. USA 108: 14539-14544.
34. Liti, G.,D.M.Carter, A. M. Moses, J. Warringer, L. Parts et al., 2009 Population genomics of domestic and wild yeasts. Nature 458: 337-341.
35. Lu, J., T. Tang, H. Tang, J. Huang, S. Shi et al., 2006 The accumulation of deleterious mutations in rice genomes: a hypothesis on the cost of domestication. Trends Genet. 22: 126-131.
36. Lynch, M., 1991 The genetic interpretation of inbreeding depression and outbreeding depression. Evolution 45: 622-629.
37. Magwene, P. M., O. Kayikci, J. A. Granek, J. M. Reininga, Z. Scholl et al., 2011 Outcrossing, mitotic recombination, and life-history trade-offs shape genome evolution in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 108: 1987-1992.
38. Masel, J., and D. N. Lyttle, 2011 The consequences of rare sexual reproduction by means of selfing in an otherwise clonally reproducing species. Theor. Popul. Biol. 80: 317-322.
39. McGuigan, K., and C. M. Sgro, 2009 Evolutionary consequences of cryptic genetic variation. Trends Ecol. Evol. 24: 305-311.
40. Mortimer, R. K., 2000 Evolution and variation of the yeast (Saccharomyces) genome. Genome Res. 10: 403-409.
41. Ruderfer, D. M., S. C. Pratt, H. S. Seidel, and L. Kruglyak, 2006 Population genomic analysis of outcrossing and recombination in yeast. Nat. Genet. 38: 1077-1081.
42. Schacherer, J., J. A. Shapiro, D. M. Ruderfer, and L. Kruglyak, 2009 Comprehensive polymorphism survey elucidates population structure of Saccharomyces cerevisiae. Nature 458: 342-345.
43. Timberlake, W. E., M. A. Frizzell, K. D. Richards, and R. C. Gardner, 2011 A new yeast genetic resource for analysis and breeding. Yeast 28: 63-80.
44. Tsai, I. J., D. Bensasson, A. Burt, and V. Koufopanou, 2008 Population genomics of the wild yeast Saccharomyces paradoxus: Quantifying the life cycle. Proc. Natl. Acad. Sci. USA 105: 4957-4962.
45. Wang, J., W. G. Hill, D. Charlesworth, and B. Charlesworth, 1999 Dynamics of inbreeding depression due to deleterious mutations in small populations: mutation parameters and inbreeding rate. Genet. Res. 74: 165-178.
46. Wang, Q. M.,W. Q. Liu, G. Liti, S. A.Wang, and F. Y. Bai, 2012 Surprisingly diverged populations of Saccharomyces cerevisiae in natural environments remote from human activity. Mol. Ecol. 21: 5404-5417.
47. Warringer, J., E. Zorgo, F. A. Cubillos, A. Zia, A. Gjuvsland et al., 2011 Trait variation in yeast is defined by population history. PLoS Genet. 7: e1002111.
48. Whitlock, M. C., 2002 Selection, load and inbreeding depression in a large metapopulation. Genetics 160: 1191-1202.
49. Whitlock, M. C., P. K. Ingvarsson, and T. Hatfield, 2000 Local drift load and the heterosis of interconnected populations. Heredity (Edinb) 84(Pt 4): 452-457.
50. Zeyl, C., 2009 The role of sex in fungal evolution. Curr. Opin. Microbiol. 12: 592-598.
51. Zorgo, E., A. Gjuvsland, F. A. Cubillos, E. J. Louis, G. Liti et al., 2012 Life history shapes trait heredity by accumulation of loss-of-function alleles in yeast. Mol. Biol. Evol. 29: 1781-1789.