Outcrossing, mitotic recombination, and life-history trade-offs shape genome evolution in Saccharomyces cerevisiae.
We carried out a population genomic survey of Saccharomyces cerevisiae diploid isolates and find that many budding yeast strains have high levels of genomic heterozygosity, much of which is likely due to outcrossing. We demonstrate that variation in heterozygosity among strains is correlated with a life-history trade-off that involves how readily yeast switch from asexual to sexual reproduction under nutrient stress. This trade-off is reflected in a negative relationship between sporulation efficiency and pseudohyphal development and correlates with variation in the expression of RME1, a transcription factor with pleiotropic effects on meiosis and filamentous growth. Selection for alternate life-history strategies in natural versus human-associated environments likely contributes to differential maintenance of genomic heterozygosity through its effect on the frequency that yeast lineages experience sexual cycles and hence the opportunity for inbreeding. In addition to elevated levels of heterozygosity, many strains exhibit large genomic regions of loss-of-heterozygosity (LOH), suggesting that mitotic recombination has a significant impact on genetic variation in this species. This study provides new insights into the roles that both outcrossing and mitotic recombination play in shaping the genome architecture of Saccharomyces cerevisiae. This study also provides a unique case where stark differences in the genomic distribution of genetic variation among individuals of the same species can be largely explained by a life-history trade-off.
Department of Biology and Institute for Genome Sciences and Policy Center for Systems Biology, Duke University, Durham, NC 27708, USA. paul.magwene@duke.edu
Paul M
PM
Magwene
Ömür
Ö
Kayıkçı
Joshua A
JA
Granek
Jennifer M
JM
Reininga
Zackary
Z
Scholl
Debra
D
Murray
D019143:Evolution, Molecular; D016681:Genome, Fungal; D019656:Loss of Heterozygosity; D008938:Mitosis; D011995:Recombination, Genetic; D012441:Saccharomyces cerevisiae / Q000235:genetics* / Q000502:physiology; D013172:Spores, Fungal
Cell Cycle. 2008 Apr 1;7(7):859-64
18414031
Mol Ecol. 2009 Jul;18(13):2779-86
19457175
Environ Microbiol. 2010 Jan;12(1):63-73
19691498
Nature. 2005 Mar 31;434(7033):636-40
15800622
Genetics. 2003 Nov;165(3):1045-58
14668363
PLoS One. 2009;4(4):e5317
19390633
Science. 2003 Sep 26;301(5641):1908-11
14512629
Cell. 1988 Mar 25;52(6):853-62
3280136
Mol Microbiol. 2007 Jun;64(6):1587-604
17555440
Cell. 1992 Mar 20;68(6):1077-90
1547504
Genetics. 1986 May;113(1):35-43
3519363
Proc Biol Sci. 2007 May 22;274(1615):1301-7
17360283
Fungal Genet Biol. 2009 Feb;46(2):159-68
19059493
PLoS Pathog. 2009 May;5(5):e1000458
19478871
Genetics. 2004 Jan;166(1):43-52
15020405
Curr Biol. 2007 Feb 6;17(3):R81-3
17276903
Nature. 2010 Apr 15;464(7291):1039-42
20393561
Curr Biol. 2009 Jun 9;19(11):891-9
19446455
Bioinformatics. 2009 Jul 15;25(14):1754-60
19451168
Nature. 2009 Mar 19;458(7236):342-5
19212320
Science. 2010 Jan 22;327(5964):425-31
20093466
Proc Natl Acad Sci U S A. 2008 Mar 25;105(12):4957-62
18344325
Genetics. 1999 Dec;153(4):1535-46
10581264
Eukaryot Cell. 2008 Feb;7(2):286-93
17890371
Philos Trans R Soc Lond B Biol Sci. 2003 Jun 29;358(1434):1051-70
12831472
Science. 2009 Jan 23;323(5913):498-501
19164747
Proc Natl Acad Sci U S A. 2007 Jul 31;104(31):12825-30
17652520
Microbiol Rev. 1994 Mar;58(1):56-70
8177171
PLoS One. 2010 May 05;5(5):e10461
20463964
Ann Hum Genet. 1977 Oct;41(2):225-33
596830
Genetics. 2003 Aug;164(4):1635-44
12930767
Curr Biol. 2006 Sep 5;16(17):R726-35
16950099
Science. 1987 Sep 4;237(4819):1162-70
3306917
Curr Opin Genet Dev. 2001 Dec;11(6):685-90
11682314
FEMS Yeast Res. 2006 Aug;6(5):702-15
16879422
Nature. 2009 Jun 4;459(7247):657-62
19465905
Genome Res. 2008 Nov;18(11):1851-8
18714091
Nature. 2009 Mar 19;458(7236):337-41
19212322
Yeast. 2007 Aug;24(8):625-36
17534867
J Cell Sci. 2003 Jun 1;116(Pt 11):2137-47
12730290
PLoS Genet. 2009 Mar;5(3):e1000410
19282969
Genetics. 2009 Jul;182(3):799-811
19414562
Nat Genet. 2006 Sep;38(9):1077-81
16892060
Genetics. 2000 Dec;156(4):1973-82
11102388
Nat Genet. 2005 Dec;37(12):1333-40
16273108
Trends Ecol Evol. 2005 Apr;20(4):194-201
16701368
Bioinformatics. 2009 Aug 15;25(16):2078-9
19505943
Genetics. 2006 Oct;174(2):985-97
16951083
Mol Cell Biol. 2007 Jan;27(2):568-78
17101800
BMC Evol Biol. 2009 Dec 22;9:296
20028531
Nature. 1986 Feb 27-Mar 5;319(6056):738-42
3513021