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Incipient Balancing Selection through Adaptive Loss of Aquaporins in Natural Populations


A major goal in evolutionary biology is to understand how adaptive evolution has influenced natural variation, but identifying loci subject to positive selection has been a challenge. Here we present the adaptive loss of a pair of paralogous genes in specific Saccharomyces cerevisiae subpopulations. We mapped natural variation in freeze-thaw tolerance to two water transporters, AQY1 and AQY2, previously implicated in freeze-thaw survival. However, whereas freeze-thaw–tolerant strains harbor functional aquaporin genes, the set of sensitive strains lost aquaporin function at least 6 independent times. Several genomic signatures at AQY1 and/or AQY2 reveal low variation surrounding these loci within strains of the same haplotype, but high variation between strain groups. This is consistent with recent adaptive loss of aquaporins in subgroups of strains, leading to incipient balancing selection. We show that, although aquaporins are critical for surviving freeze-thaw stress, loss of both genes provides a major fitness advantage on high-sugar substrates common to many strains' natural niche. Strikingly, strains with non-functional alleles have also lost the ancestral requirement for aquaporins during spore formation. Thus, the antagonistic effect of aquaporin function—providing an advantage in freeze-thaw tolerance but a fitness defect for growth in high-sugar environments—contributes to the maintenance of both functional and nonfunctional alleles in S. cerevisiae. This work also shows that gene loss through multiple missense and nonsense mutations, hallmarks of pseudogenization presumed to emerge after loss of constraint, can arise through positive selection.


Vyšlo v časopise: Incipient Balancing Selection through Adaptive Loss of Aquaporins in Natural Populations. PLoS Genet 6(4): e32767. doi:10.1371/journal.pgen.1000893
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1000893

Souhrn

A major goal in evolutionary biology is to understand how adaptive evolution has influenced natural variation, but identifying loci subject to positive selection has been a challenge. Here we present the adaptive loss of a pair of paralogous genes in specific Saccharomyces cerevisiae subpopulations. We mapped natural variation in freeze-thaw tolerance to two water transporters, AQY1 and AQY2, previously implicated in freeze-thaw survival. However, whereas freeze-thaw–tolerant strains harbor functional aquaporin genes, the set of sensitive strains lost aquaporin function at least 6 independent times. Several genomic signatures at AQY1 and/or AQY2 reveal low variation surrounding these loci within strains of the same haplotype, but high variation between strain groups. This is consistent with recent adaptive loss of aquaporins in subgroups of strains, leading to incipient balancing selection. We show that, although aquaporins are critical for surviving freeze-thaw stress, loss of both genes provides a major fitness advantage on high-sugar substrates common to many strains' natural niche. Strikingly, strains with non-functional alleles have also lost the ancestral requirement for aquaporins during spore formation. Thus, the antagonistic effect of aquaporin function—providing an advantage in freeze-thaw tolerance but a fitness defect for growth in high-sugar environments—contributes to the maintenance of both functional and nonfunctional alleles in S. cerevisiae. This work also shows that gene loss through multiple missense and nonsense mutations, hallmarks of pseudogenization presumed to emerge after loss of constraint, can arise through positive selection.


Zdroje

1. Mitchell-OldsT

WillisJH

GoldsteinDB

2007 Which evolutionary processes influence natural genetic variation for phenotypic traits? Nat Rev Genet 8 845 856

2. AkeyJM

ZhangG

ZhangK

JinL

ShriverMD

2002 Interrogating a high-density SNP map for signatures of natural selection. Genome Res 12 1805 1814

3. ClarkAG

GlanowskiS

NielsenR

ThomasPD

KejariwalA

2003 Inferring nonneutral evolution from human-chimp-mouse orthologous gene trios. Science 302 1960 1963

4. NielsenR

BustamanteC

ClarkAG

GlanowskiS

SacktonTB

2005 A scan for positively selected genes in the genomes of humans and chimpanzees. PLoS Biol 3 e170 doi:10.1371/journal.pbio.0030170

5. SabetiPC

ReichDE

HigginsJM

LevineHZ

RichterDJ

2002 Detecting recent positive selection in the human genome from haplotype structure. Nature 419 832 837

6. VoightBF

KudaravalliS

WenX

PritchardJK

2006 A map of recent positive selection in the human genome. PLoS Biol 4 e72 doi:10.1371/journal.pbio.0050147

7. YamasakiM

TenaillonMI

BiIV

SchroederSG

Sanchez-VilledaH

2005 A large-scale screen for artificial selection in maize identifies candidate agronomic loci for domestication and crop improvement. Plant Cell 17 2859 2872

8. MackayTF

StoneEA

AyrolesJF

2009 The genetics of quantitative traits: challenges and prospects. Nat Rev Genet 10 565 577

9. KvitekDJ

WillJL

GaschAP

2008 Variations in stress sensitivity and genomic expression in diverse S. cerevisiae isolates. PLoS Genet 4 e1000223 doi:10.1371/journal.pgen.1000223

10. TangheA

Van DijckP

DumortierF

TeunissenA

HohmannS

2002 Aquaporin expression correlates with freeze tolerance in baker's yeast, and overexpression improves freeze tolerance in industrial strains. Appl Environ Microbiol 68 5981 5989

11. TangheA

Van DijckP

ColavizzaD

TheveleinJM

2004 Aquaporin-mediated improvement of freeze tolerance of Saccharomyces cerevisiae is restricted to rapid freezing conditions. Appl Environ Microbiol 70 3377 3382

12. WolfeKH

ShieldsDC

1997 Molecular evidence for an ancient duplication of the entire yeast genome. Nature 387 708 713

13. BonhiversM

CarbreyJM

GouldSJ

AgreP

1998 Aquaporins in Saccharomyces. Genetic and functional distinctions between laboratory and wild-type strains. J Biol Chem 273 27565 27572

14. CarbreyJM

BonhiversM

BoekeJD

AgreP

2001 Aquaporins in Saccharomyces: Characterization of a second functional water channel protein. Proc Natl Acad Sci U S A 98 1000 1005

15. LaizeV

GobinR

RousseletG

BadierC

HohmannS

1999 Molecular and functional study of AQY1 from Saccharomyces cerevisiae: role of the C-terminal domain. Biochem Biophys Res Commun 257 139 144

16. LaizeV

TacnetF

RipocheP

HohmannS

2000 Polymorphism of Saccharomyces cerevisiae aquaporins. Yeast 16 897 903

17. SniegowskiPD

DombrowskiPG

FingermanE

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

18. KimHS

FayJC

2007 Genetic variation in the cysteine biosynthesis pathway causes sensitivity to pharmacological compounds. Proc Natl Acad Sci U S A 104 19387 19391

19. TangheA

Van DijckP

TheveleinJM

2006 Why do microorganisms have aquaporins? Trends Microbiol 14 78 85

20. FayJC

BenavidesJA

2005 Evidence for domesticated and wild populations of Saccharomyces cerevisiae. PLoS Genet 1 e5 doi:10.1371/journal.pgen.0010005

21. LitiG

CarterDM

MosesAM

WarringerJ

PartsL

2009 Population genomics of domestic and wild yeasts. Nature 458 337 341

22. McDonaldJH

KreitmanM

1991 Adaptive protein evolution at the Adh locus in Drosophila. Nature 351 652 654

23. WrightSI

CharlesworthB

2004 The HKA test revisited: a maximum-likelihood-ratio test of the standard neutral model. Genetics 168 1071 1076

24. KreitmanM

2000 Methods to detect selection in populations with applications to the human. Annu Rev Genomics Hum Genet 1 539 559

25. CharlesworthD

2006 Balancing selection and its effects on sequences in nearby genome regions. PLoS Genet 2 e64 doi:10.1371/journal.pgen.0020064

26. LegrasJL

MerdinogluD

CornuetJM

KarstF

2007 Bread, beer and wine: Saccharomyces cerevisiae diversity reflects human history. Mol Ecol 16 2091 2102

27. ReplanskyT

KoufopanouV

GreigD

BellG

2008 Saccharomyces sensu stricto as a model system for evolution and ecology. Trends Ecol Evol 23 494 501

28. RuderferDM

PrattSC

SeidelHS

KruglyakL

2006 Population genomic analysis of outcrossing and recombination in yeast. Nat Genet 38 1077 1081

29. SchachererJ

ShapiroJA

RuderferDM

KruglyakL

2009 Comprehensive polymorphism survey elucidates population structure of Saccharomyces cerevisiae. Nature 458 342 345

30. TeshimaK

CoopG

PrzeworskiM

2006 How reliable are empirical genomic scans for selective sweeps? Genome Res 6 702 712

31. CatharinoRR

CunhaIB

FogacaAO

FaccoEM

GodoyHT

2006 Characterization of must and wine of six varieties of grapes by direct infusion electrospray ionization mass spectrometry. J Mass Spectrom 41 185 190

32. Sidoux-WalterF

PetterssonN

HohmannS

2004 The Saccharomyces cerevisiae aquaporin Aqy1 is involved in sporulation. Proc Natl Acad Sci U S A 101 17422 17427

33. GerkeJP

ChenCT

CohenBA

2006 Natural isolates of Saccharomyces cerevisiae display complex genetic variation in sporulation efficiency. Genetics 174 985 997

34. KarpelJE

BissonLF

2006 Aquaporins in Saccharomyces cerevisiae wine yeast. FEMS Microbiol Lett 257 117 123

35. DonigerSW

KimHS

SwainD

CorcueraD

WilliamsM

2008 A catalog of neutral and deleterious polymorphism in yeast. PLoS Genet 4 e1000183 doi:10.1371/journal.pgen.1000183

36. NaumovGI

JamesSA

NaumovaES

LouisEJ

RobertsIN

2000 Three new species in the Saccharomyces sensu stricto complex: Saccharomyces cariocanus, Saccharomyces kudriavzevii and Saccharomyces mikatae. Int J Syst Evol Microbiol 50 Pt 5 1931 1942

37. FayJC

McCulloughHL

SniegowskiPD

EisenMB

2004 Population genetic variation in gene expression is associated with phenotypic variation in Saccharomyces cerevisiae. Genome Biol 5 R26

38. SampaioJP

GoncalvesP

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

39. XuZ

LeiningerT

LeeAW

TainterF

2001 Chemical properties associated with bacterial wetwood in red oaks. Wood Fiber Sci 33 76 83

40. AaE

TownsendJP

AdamsRI

NielsenKM

TaylorJW

2006 Population structure and gene evolution in Saccharomyces cerevisiae. FEMS Yeast Res 6 702 715

41. SchluterD

2009 Evidence for ecological speciation and its alternative. Science 323 737 741

42. DiezmannS

DietrichFS

2009 Saccharomyces cerevisiae: population divergence and resistance to oxidative stress in clinical, domesticated and wild isolates. PLoS ONE 4 e5317 doi:10.1371/journal.pone.0005317

43. KainthP

SassiHE

Pena-CastilloL

ChuaG

HughesTR

2009 Comprehensive genetic analysis of transcription factor pathways using a dual reporter gene system in budding yeast. Methods 48 258 264

44. BromanKW

WuH

SenS

ChurchillGA

2003 R/qtl: QTL mapping in experimental crosses. Bioinformatics 19 889 890

45. LibradoP

RozasJ

2009 DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25 1451 1452

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


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