Segregating Variation in the Polycomb Group Gene Alters the Effect of Temperature on Multiple Traits

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The phenotype produced by a given genotype can be strongly modulated by environmental conditions. Therefore, natural populations continuously adapt to environment heterogeneity to maintain optimal phenotypes. It generates a high genetic variation in environment-sensitive gene networks, which is thought to facilitate evolution. Here we analyze the chromatin regulator crm, identified as a candidate for adaptation of Drosophila melanogaster to northern latitudes. We show that crm contributes to environmental canalization. In particular, crm modulates the effect of temperature on a genomic region encoding Hedgehog and Wingless signaling effectors. crm affects this region through both constitutive heterochromatin and Polycomb silencing. Furthermore, we show that crm European and African natural variants shift the reaction norms of plastic traits. Interestingly, traits modulated by crm natural variants can differ markedly between Drosophila species, suggesting that temperature adaptation facilitates their evolution.

Vyšlo v časopise: Segregating Variation in the Polycomb Group Gene Alters the Effect of Temperature on Multiple Traits. PLoS Genet 7(1): e32767. doi:10.1371/journal.pgen.1001280
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1001280

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Zdroje

1. CrickmoreMA

RanadeV

MannRS

2009 Regulation of Ubx expression by epigenetic enhancer silencing in response to Ubx levels and genetic variation. PLoS Genet 5 e1000633 doi:10.1371/journal.pgen.1000633

2. Meireles-FilhoAC

StarkA

2009 Comparative genomics of gene regulation-conservation and divergence of cis-regulatory information. Curr Opin Genet Dev 19 565 570

3. FrankelN

DavisGK

VargasD

WangS

PayreF

2010 Phenotypic robustness conferred by apparently redundant transcriptional enhancers. Nature

4. PerryMW

BoettigerAN

BothmaJP

LevineM

2010 Shadow enhancers foster robustness of Drosophila gastrulation. Curr Biol 20 1562 1567

5. WaddingtonCH

1959 Canalization of development and genetic assimilation of acquired characters. Nature 183 1654 1655

6. GretherGF

2005 Environmental change, phenotypic plasticity, and genetic compensation. Am Nat 166 E115 123

7. ViaS

GomulkieviczR

de JongG

ScheinerSM

SchlichtingCD

1995 Adaptive phenotypic plasticity: consensus and controversy. TREE 10 212 217

8. SuzukiY

NijhoutHF

2006 Evolution of a polyphenism by genetic accommodation. Science 311 650 652

9. GibsonG

HognessDS

1996 Effect of polymorphism in the Drosophila regulatory gene Ultrabithorax on homeotic stability. Science 271 200 203

10. MoczekAP

2007 Developmental capacitance, genetic accommodation, and adaptive evolution. Evol Dev 9 299 305

11. PriceTD

QvarnströmA

IrwinDE

2003 The role of phenotypic plasticity in driving genetic evolution. Proc R Soc Lond B 270 1433 1440

12. West-EberhardMJ

2005 Developmental plasticity and the origin of species differences. Proc Natl Acad Sci U S A 102 Suppl 1 6543 6549

13. TrottaV

CalboliFCF

ZiosiM

GuerraD

PezzoliMC

2006 Thermal plasticity in Drosophila melanogaster: a comparison of geographical population. BMC Evolutionary Biology 6

14. Bouletreau-MerleJ

FouilletP

VaraldiJ

2003 Divergent strategies in low temperature environment for the sibling species Drosophila melanogaster and D. simulans: overwintering in extension borders area of France and comparison with African populations,. Evolutionary Ecology 17 523 548

15. GibertP

CapyP

ImashevaA

MoreteauB

MorinJP

2004 Comparative analysis of morphological traits among Drosophila melanogaster and D. simulans: genetic variability, clines and phenotypic plasticity. Genetica 120 165 179

16. HarrB

KauerM

SchlottererC

2002 Hitchhiking mapping: a population-based fine-mapping strategy for adaptive mutations in Drosophilamelanogaster. Proc Natl Acad Sci U S A 99 12949 12954

17. YamamotoY

GirardF

BelloB

AffolterM

GehringWJ

1997 The cramped gene of Drosophila is a member of the Polycomb-group, and interacts with mus209, the gene encoding Proliferating Cell Nuclear Antigen. Development 124 3385 3394

18. FauvarqueMO

DuraJM

1993 polyhomeotic regulatory sequences induce developmental regulator-dependent variegation and targeted P-element insertions in Drosophila. Genes Dev 7 1508 1520

19. DosztanyiZ

CsizmokV

TompaP

SimonI

2005 IUPred: web server for the prediction of intrinsically unstructured regions of proteins based on estimated energy content. Bioinformatics 21 3433 3434

20. HegyiH

SchadE

TompaP

2007 Structural disorder promotes assembly of protein complexes. BMC Struct Biol 7 65

21. MittagT

KayLE

Forman-KayJD

2009 Protein dynamics and conformational disorder in molecular recognition. J Mol Recognit

22. PattatucciAM

KaufmanTC

1991 The homeotic gene Sex combs reduced of Drosophila melanogaster is differentially regulated in the embryonic and imaginal stages of development. Genetics 129 443 461

23. GibertJM

PeronnetF

SchlottererC

2007 Phenotypic Plasticity in Drosophila Pigmentation Caused by Temperature Sensitivity of a Chromatin Regulator Network. PLoS Genet 3 e30 doi:10.1371/journal.pgen.0030030

24. SchottaG

EbertA

KraussV

FischerA

HoffmannJ

2002 Central role of Drosophila SU(VAR)3-9 in histone H3-K9 methylation and heterochromatic gene silencing. Embo J 21 1121 1131

25. EhsanH

ReichheldJP

DurfeeT

RoeJL

2004 TOUSLED kinase activity oscillates during the cell cycle and interacts with chromatin regulators. Plant Physiol 134 1488 1499

26. ChanasG

LavrovS

IralF

CavalliG

MaschatF

2004 Engrailed and polyhomeotic maintain posterior cell identity through cubitus-interruptus regulation. Dev Biol 272 522 535

27. RyderE

BlowsF

AshburnerM

Bautista-LlacerR

CoulsonD

2004 The DrosDel collection: a set of P-element insertions for generating custom chromosomal aberrations in Drosophila melanogaster. Genetics 167 797 813

28. de WitE

GreilF

van SteenselB

2007 High-resolution mapping reveals links of HP1 with active and inactive chromatin components. PLoS Genet 3 e38 doi:10.1371/journal.pgen.0030038

29. DubininNP

SidorovBN

1934 Relation between the effect of a gene and its position in the system. Am Naturalist 18 377 381

30. DemakovaOV

BelyaevaES

ZhimulevIF

1998 The somatic pairing of homologues of chromosome 4 causes the suppression of the Dubinin effect in Drosophila melanogaster. Russian Journal of Genetics 34 511 516

31. LockeJ

TartofKD

1994 Molecular analysis of cubitus interruptus (ci) mutations suggests an explanation for the unusual ci position effects. Mol Gen Genet 243 234 243

32. WallrathLL

ElginSC

1995 Position effect variegation in Drosophila is associated with an altered chromatin structure. Genes Dev 9 1263 1277

33. MinakuchiC

ZhouX

RiddifordLM

2008 Kruppel homolog 1 (Kr-h1) mediates juvenile hormone action during metamorphosis of Drosophila melanogaster. Mech Dev 125 91 105

34. ParkerDS

JemisonJ

CadiganKM

2002 Pygopus, a nuclear PHD-finger protein required for Wingless signaling in Drosophila. Development 129 2565 2576

35. SvendsenPC

MarshallSD

KybaM

BrookWJ

2000 The combgap locus encodes a zinc-finger protein that regulates cubitus interruptus during limb development in Drosophila melanogaster. Development 127 4083 4093

36. LawrencePA

CasalJ

StruhlG

2002 Towards a model of the organisation of planar polarity and pattern in the Drosophila abdomen. Development 129 2749 2760

37. KoppA

DuncanI

1997 Control of cell fate and polarity in the adult abdominal segments of Drosophila by optomotor-blind. Development 124 3715 3726

38. KoppA

BlackmanRK

DuncanI

1999 Wingless, decapentaplegic and EGF receptor signaling pathways interact to specify dorso-ventral pattern in the adult abdomen of Drosophila. Development 126 3495 3507

39. ScharlooW

1962 The influence of selection and temperature on a mutant character (ciD) in Drosophila melanogaster. Arch Neerl Zool 14 433 511

40. RebeizM

PoolJE

KassnerVA

AquadroCF

CarrollSB

2009 Stepwise modification of a modular enhancer underlies adaptation in a Drosophila population. Science 326 1663 1667

41. GibertP

MoreteauB

DavidJR

2004 Phenotypic plasticity of body pigmentation in Drosophila melanogaster: genetic repeatability of quantitative parameters in two successive generations. Heredity 92 499 507

42. PoolJE

AquadroCF

2007 The genetic basis of adaptive pigmentation variation in Drosophila melanogaster. Mol Ecol 16 2844 2851

43. GibertP

MoreteauB

MoreteauJ-C

ParkashR

DavidJR

1998 Light body pigmentation in Indian Drosophila melanogaster: a likely adaptation to a hot and arid climate. Journal of Genetics 77 13 20

44. CaracristiG

SchlottererC

2003 Genetic differentiation between American and European Drosophila melanogaster populations could be attributed to admixture of African alleles. Mol Biol Evol 20 792 799

45. YukilevichR

TrueJR

2008 African morphology, behavior and phermones underlie incipient sexual isolation between us and Caribbean Drosophila melanogaster. Evolution 62 2807 2828

46. Prud'hommeB

GompelN

CarrollSB

2007 Emerging principles of regulatory evolution. Proc Natl Acad Sci U S A 104 Suppl 1 8605 8612

47. SawyerSA

ParschJ

ZhangZ

HartlDL

2007 Prevalence of positive selection among nearly neutral amino acid replacements in Drosophila. Proc Natl Acad Sci U S A 104 6504 6510

48. LevineMT

BegunDJ

2008 Evidence of Spatially Varying Selection Acting on Four Chromatin-Remodeling Loci in Drosophila melanogaster. Genetics 179 475 485

49. BeisswangerS

StephanW

2008 Evidence that strong positive selection drives neofunctionalization in the tandemly duplicated polyhomeotic genes in Drosophila. Proc Natl Acad Sci U S A 105 5447 5452

50. KoppA

GrazeRM

XuS

CarrollSB

NuzhdinSV

2003 Quantitative trait loci responsible for variation in sexually dimorphic traits in Drosophila melanogaster. Genetics 163 771 787

51. KoppA

BarminaO

2005 Evolutionary history of the Drosophila bipectinata species complex. Genet Res 85 23 46

52. KoppA

TrueJR

2002 Evolution of male sexual characters in the oriental Drosophila melanogaster species group. Evol Dev 4 278 291

53. WittkoppPJ

CarrollSB

KoppA

2003 Evolution in black and white: genetic control of pigment patterns in Drosophila. Trends Genet 19 495 504

54. RohmerC

DavidJR

MoreteauB

JolyD

2004 Heat induced male sterility in Drosophila melanogaster: adaptive genetic variations among geographic populations and role of the Y chromosome. J Exp Biol 207 2735 2743

55. NgCS

KoppA

2008 Sex Combs are Important for Male Mating Success in Drosophila melanogaster. Behav Genet 38 195 201

56. AdamsMD

CelnikerSE

HoltRA

EvansCA

GocayneJD

2000 The genome sequence of Drosophila melanogaster. Science 287 2185 2195

57. SchmidtHA

StrimmerK

VingronM

von HaeselerA

2002 TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18 502 504

58. RozasJ

Sanchez-DelBarrioJC

MesseguerX

RozasR

2003 DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19 2496 2497

59. ThompsonJD

HigginsDG

GibsonTJ

1994 CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22 4673 4680

60. RocaAI

AlmadaAE

AbajianAC

2008 ProfileGrids as a new visual representation of large multiple sequence alignments: a case study of the RecA protein family. BMC Bioinformatics 9 554

61. NagaiT

IbataK

ParkES

KubotaM

MikoshibaK

2002 A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nat Biotechnol 20 87 90

62. BischofJ

MaedaRK

HedigerM

KarchF

BaslerK

2007 An optimized transgenesis system for Drosophila using germ-line-specific {varphi}C31 integrases. Proc Natl Acad Sci U S A 104 3312 3317