#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Tempo and Mode in Evolution of Transcriptional Regulation


Perennial questions of evolutionary biology can be applied to gene regulatory systems using the abundance of experimental data addressing gene regulation in a comparative context. What is the tempo (frequency, rate) and mode (way, mechanism) of transcriptional regulatory evolution? Here we synthesize the results of 230 experiments performed on insects and nematodes in which regulatory DNA from one species was used to drive gene expression in another species. General principles of regulatory evolution emerge. Gene regulatory evolution is widespread and accumulates with genetic divergence in both insects and nematodes. Divergence in cis is more common than divergence in trans. Coevolution between cis and trans shows a particular increase over greater evolutionary timespans, especially in sex-specific gene regulation. Despite these generalities, the evolution of gene regulation is gene- and taxon-specific. The congruence of these conclusions with evidence from other types of experiments suggests that general principles are discoverable, and a unified view of the tempo and mode of regulatory evolution may be achievable.


Vyšlo v časopise: Tempo and Mode in Evolution of Transcriptional Regulation. PLoS Genet 8(1): e32767. doi:10.1371/journal.pgen.1002432
Kategorie: Review
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002432

Souhrn

Perennial questions of evolutionary biology can be applied to gene regulatory systems using the abundance of experimental data addressing gene regulation in a comparative context. What is the tempo (frequency, rate) and mode (way, mechanism) of transcriptional regulatory evolution? Here we synthesize the results of 230 experiments performed on insects and nematodes in which regulatory DNA from one species was used to drive gene expression in another species. General principles of regulatory evolution emerge. Gene regulatory evolution is widespread and accumulates with genetic divergence in both insects and nematodes. Divergence in cis is more common than divergence in trans. Coevolution between cis and trans shows a particular increase over greater evolutionary timespans, especially in sex-specific gene regulation. Despite these generalities, the evolution of gene regulation is gene- and taxon-specific. The congruence of these conclusions with evidence from other types of experiments suggests that general principles are discoverable, and a unified view of the tempo and mode of regulatory evolution may be achievable.


Zdroje

1. SimpsonGG 1944 Tempo and mode in evolution New York Columbia University Press

2. DarwinC 1859 On the origin of species London John Murray

3. DavidsonEH 2001 Genomic regulatory systems: Development and evolution San Diego (CA) Academic Press

4. SternDL 2010 Evolution, development, and the predictable genome Greenwood Village (CO) Roberts & Company Publishers

5. CarrollSBGrenierJKWeatherbeeSD 2001 From DNA to diversity: Molecular genetics and the evolution of animal design Malden (MA) Blackwell Scientific

6. KingMCWilsonAC 1975 Evolution at 2 levels in humans and chimpanzees. Science 188 4184 107 116

7. AkamM 1989 Hox and hom - homologous gene clusters in insects and vertebrates. Cell 57 3 347 349

8. PanganibanGIrvineSMLoweCRoehlHCorleyLS 1997 The origin and evolution of animal appendages. Proc Natl Acad Sci U S A 94 10 5162 5166

9. QuiringRWalldorfUKloterUGehringWJ 1994 Homology of the eyeless gene of Drosophila to the small eye gene in mice and aniridia in humans. Science 265 5173 785 789

10. AparicioSMorrisonAGouldAGilthorpeJChaudhuriC 1995 Detecting conserved regulatory elements with the model genome of the japanese puffer fish, Fugu rubripes. Proc Natl Acad Sci U S A 92 5 1684 1688

11. CooperGMBrownCD 2008 Qualifying the relationship between sequence conservation and molecular function. Genome Res 18 2 201 205

12. WeirauchMTHughesTR 2010 Conserved expression without conserved regulatory sequence: The more things change, the more they stay the same. Trends in Genetics 26 2 66 74

13. WrayGAHahnMWAbouheifEBalhoffJPPizerM 2003 The evolution of transcriptional regulation in eukaryotes. Mol Biol Evol 20 9 1377 1419

14. FrankelNDavisGKVargasDWangSPayreF 2010 Phenotypic robustness conferred by apparently redundant transcriptional enhancers. Nature 466 7305 490 493

15. HareEEPetersonBKIyerVNMeierREisenMB 2008 Sepsid even-skipped enhancers are functionally conserved in Drosophila despite lack of sequence conservation. PLoS Genet 4 6 e1000106 doi:10.1371/journal.pgen.1000106

16. BarriereAGordonKLRuvinskyI 2011 Distinct functional constraints partition sequence conservation in a cis-regulatory element. PLoS Genet 7 6 e1002095 doi:10.1371/journal.pgen.1002095

17. SwansonCIEvansNCBaroloS 2010 Structural rules and complex regulatory circuitry constrain expression of a notch- and EGFR-regulated eye enhancer. Dev Cell 18 3 359 370

18. SternDLOrgogozoV 2008 The loci of evolution: How predictable is genetic evolution? Evolution 62 9 2155 2177

19. CarrollSB 2005 Evolution at two levels: on genes and form. PLoS Biol 3 7 e245 doi:10.1371/journal.pbio.0030245

20. PriceMDLaiZC 1999 The yan gene is highly conserved in Drosophila and its expression suggests a complex role throughout development. Dev Genes Evol 209 4 207 217

21. KuwabaraPE 1996 Interspecies comparison reveals evolution of control regions in the nematode sex-determining gene tra-2. Genetics 144 2 597 607

22. ChangYLiuFRYuNSungHYangP 2008 Roles of cis- and trans-changes in the regulatory evolution of genes in the gluconeogenic pathway in yeast. Mol Biol Evol 25 9 1863 1875

23. GiladYOshlackASmythGKSpeedTPWhiteKP 2006 Expression profiling in primates reveals a rapid evolution of human transcription factors. Nature 440 7081 242 245

24. ParikhAMirandaERKatoh-KurasawaMFullerDRotG 2010 Conserved developmental transcriptomes in evolutionarily divergent species. Genome Biol 11 3 R35

25. NegreNBrownCDMaLBristowCAMillerSW 2011 A cis-regulatory map of the Drosophila genome. Nature 471 7339 527 531

26. GersteinMBLuZJVan NostrandELChengCArshinoffBI 2010 Integrative analysis of the Caenorhabditis elegans genome by the modENCODE project. Science 330(6012): 1775–1787. Erratum in Science 2011 Jan 7; 331 6013 30

27. BradleyRKLiXTrapnellCDavidsonSPachterL 2010 Binding site turnover produces pervasive quantitative changes in transcription factor binding between closely related Drosophila species. PLoS Biol 8 3 e1000343 doi:10.1371/journal.pbio.1000343

28. WittkoppPJHaerumBKClarkAG 2008 Regulatory changes underlying expression differences within and between Drosophila species. Nat Genet 40 3 346 350

29. TuchBBGalgoczyDJHerndayADLiHJohnsonAD 2008 The evolution of combinatorial gene regulation in fungi. PLoS Biol 6 2 e38 doi:10.1371/journal.pbio.0060038

30. TsongAETuchBBLiHJohnsonAD 2006 Evolution of alternative transcriptional circuits with identical logic. Nature 443 7110 415 420

31. HinmanVFDavidsonEH 2007 Evolutionary plasticity of developmental gene regulatory network architecture. Proc Natl Acad Sci U S A 104 49 19404 19409

32. HillRCde CarvalhoCESalogiannisJSchlagerBPilgrimD 2006 Genetic flexibility in the convergent evolution of hermaphroditism in Caenorhabditis nematodes. Dev Cell 10 4 531 538

33. WangXSommerRJ 2011 Antagonism of LIN-17/Frizzled and LIN-18/Ryk in nematode vulva induction reveals evolutionary alterations in core developmental pathways. PLoS Biol 9 7 e1001110 doi:10.1371/journal.pbio.1001110

34. PickrellJKMarioniJCPaiAADegnerJFEngelhardtBE 2010 Understanding mechanisms underlying human gene expression variation with RNA sequencing. Nature 464 7289 768 772

35. Dori-BachashMShemaETiroshI 2011 Coupled evolution of transcription and mRNA degradation. PLoS Biol 9 7 e1001106 doi:10.1371/journal.pbio.1001106

36. LeMTShyh-ChangNKhawSLChinLTehC 2011 Conserved regulation of p53 network dosage by microRNA–125b occurs through evolving miRNA–target gene pairs. PLoS Genet 7 9 e1002242 doi:10.1371/journal.pgen.1002242

37. NirenbergMMatthaeiJH 1961 The dependence of cell-free protein synthesis in E. coli upon naturally occurring or synthetic polyribonucleotides. Proc Natl Acad Sci U S A 47 10 1588 1602

38. GauntMWMilesMA 2002 An insect molecular clock dates the origin of the insects and accords with palaeontological and biogeographic landmarks. Mol Biol Evol 19 5 748 761

39. McGregorAPOrgogozoVDelonIZanetJSrinivasanDG 2007 Morphological evolution through multiple cis-regulatory mutations at a single gene. Nature 448 7153 587-U6

40. FrankelNErezyilmazDMcGregorAPWangSPayreF 2011 Morphological evolution caused by many subtle-effect substitutions in regulatory DNA. Nature 474 598 598-603

41. BickelRDKoppANuzhdinSV 2011 Composite effects of polymorphisms near multiple regulatory elements create a major-effect QTL. PLoS Genet 7 1 e1001275 doi:10.1371/journal.pgen.1001275

42. LudwigMZPalssonAAlekseevaEBergmanCMNathanJ 2005 Functional evolution of a cis-regulatory module. PLoS Biol 3 4 e93 doi:10.1371/journal.pbio.0030093

43. MolinLMounseyAAslamSBauerPYoungJ 2000 Evolutionary conservation of redundancy between a diverged pair of forkhead transcription factor homologues. Development 127 22 4825 4835

44. EmersonJJHsiehLSungHWangTHuangC 2010 Natural selection on cis and trans regulation in yeasts. Genome Res 20 6 826 836

45. GibsonGRiley-BergerRHarshmanLKoppAVachaS 2004 Extensive sex-specific nonadditivity of gene expression in Drosophila melanogaster. Genetics 167 4 1791 1799

46. McManusCJCoolonJDDuffMOEipper-MainsJGraveleyBR 2010 Regulatory divergence in Drosophila revealed by mRNA-seq. Genome Res 20 6 816 825

47. PennacchioLAAhituvNMosesAMPrabhakarSNobregaMA 2006 In vivo enhancer analysis of human conserved non-coding sequences. Nature 444 7118 499 502

48. BlowMJMcCulleyDJLiZZhangTAkiyamaJA 2010 ChIP-seq identification of weakly conserved heart enhancers. Nat Genet 42 9 806 810

49. KiontkeKGavinNPRaynesYRoehrigCPianoF 2004 Caenorhabditis phylogeny predicts convergence of hermaphroditism and extensive intron loss. Proc Natl Acad Sci U S A 101 24 9003 9008

50. KalinkaATVargaKMGerrardDTPreibischSCorcoranDL 2010 Gene expression divergence recapitulates the developmental hourglass model. Nature 468 7325 811 814

51. RifkinSAKimJWhiteKP 2003 Evolution of gene expression in the Drosophila melanogaster subgroup. Nat Genet 33 2 138 144

52. WittkoppPJVaccaroKCarrollSB 2002 Evolution of yellow gene regulation and pigmentation in Drosophila. Current Biology: CB 12 18 1547 1556

53. Prud'hommeBGompelNRokasAKassnerVaWilliamsTM 2006 Repeated morphological evolution through cis-regulatory changes in a pleiotropic gene. Nature 440 7087 1050 1053

54. KalayGWittkoppPJ 2010 Nomadic enhancers: Tissue-specific cis-regulatory elements of yellow have divergent genomic positions among Drosophila species. PLoS Genet 6 11 e1001222 doi:10.1371/journal.pgen.1001222

55. JeongSRokasACarrollSB 2006 Regulation of body pigmentation by the abdominal-B hox protein and its gain and loss in Drosophila evolution. Cell 125 7 1387 1399

56. GompelNPrud'hommeBWittkoppPJKassnerVaCarrollSB 2005 Chance caught on the wing: Cis-regulatory evolution and the origin of pigment patterns in Drosophila. Nature 433 7025 481 487

57. WernerTKoshikawaSWilliamsTMCarrollSB 2010 Generation of a novel wing colour pattern by the wingless morphogen. Nature 464 7292 1143 1148

58. WittkoppPJStewartEEArnoldLLNeidertAHHaerumBK 2009 Intraspecific polymorphism to interspecific divergence: Genetics of pigmentation in Drosophila. Science (New York, N.Y.) 326 5952 540 544

59. LemkeSStauberMShawPJRafiqiAMPrellA 2008 bicoid occurrence and Bicoid-dependent hunchback regulation in lower cyclorrhaphan flies. Evol Dev 10 4 413 420

60. CavenerDR 1992 Transgenic animal studies on the evolution of genetic regulatory circuitries. Bioessays 14 4 237 244

61. BremRBYvertGClintonRKruglyakL 2002 Genetic dissection of transcriptional regulation in budding yeast. Science 296 5568 752 755

62. TiroshIReikhavSLevyAABarkaiN 2009 A yeast hybrid provides insight into the evolution of gene expression regulation. Science 324 5927 659 662

63. LemosBAraripeLOFontanillasPHartlDL 2008 Dominance and the evolutionary accumulation of cis- and trans-effects on gene expression. Proc Natl Acad Sci U S A 105 38 14471 14476

64. WittkoppPJHaerumBKClarkAG 2004 Evolutionary changes in cis and trans gene regulation. Nature 430 6995 85 88

65. VeyrierasJKudaravalliSKimSYDermitzakisETGiladY 2008 High-resolution mapping of expression-QTLs yields insight into human gene regulation. PLoS Genet 4 10 e1000214 doi:10.1371/journal.pgen.1000214

66. SternDL 2000 Perspective: Evolutionary developmental biology and the problem of variation. Evolution 54 4 1079 1091

67. TakahasiKRMatsuoTTakano-Shimizu-KounoT 2011 Two types of cis-trans compensation in the evolution of transcriptional regulation. Proc Natl Acad Sci U S A 108 37 15276 15281

68. LandryCRWittkoppPJTaubesCHRanzJMClarkAG 2005 Compensatory cis-trans evolution and the dysregulation of gene expression in interspecific hybrids of Drosophila. Genetics 171 4 1813 1822

69. RanzJMNamgyalKGibsonGHartlDL 2004 Anomalies in the expression profile of interspecific hybrids of Drosophila melanogaster and Drosophila simulans. Genome Res 14 3 373 379

70. BremRBKruglyakL 2005 The landscape of genetic complexity across 5,700 gene expression traits in yeast. Proc Natl Acad Sci U S A 102 5 1572 1577

71. ChanYFMarksMEJonesFCVillarrealGJrShapiroMD 2010 Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer. Science 327 5963 302 305

72. LoweCWrayG 1997 Radical alterations in the roles of homeobox genes during echinoderm evolution. Nature 389 6652 718 721

73. KeysDLewisDSelegueJPearsonBGoodrichL 1999 Recruitment of a hedgehog regulatory circuit in butterfly eyespot evolution. Science 283 5401 532 534

74. SungHWangTWangDHuangYWuJ 2009 Roles of trans and cis variation in yeast intraspecies evolution of gene expression. Mol Biol Evol 26 11 2533 2538

75. RebeizMPoolJEKassnerVAAquadroCFCarrollSB 2009 Stepwise modification of a modular enhancer underlies adaptation in a Drosophila population. Science 326 5960 1663 1667

76. JeongSRebeizMAndolfattoPWernerTTrueJ 2008 The evolution of gene regulation underlies a morphological difference between two Drosophila sister species. Cell 132 5 783 93

77. LudwigMZPatelNHKreitmanM 1998 Functional analysis of eve stripe 2 enhancer evolution in Drosophila: Rules governing conservation and change. Development 125 5 949 958

78. HittingerCTGoncalvesPSampaioJPDoverJJohnstonM 2010 Remarkably ancient balanced polymorphisms in a multi-locus gene network. Nature 464 7285 54-U61

79. OrrHATurelliM 2001 The evolution of postzygotic isolation: Accumulating Dobzhansky-Muller Incompatibilities. Evolution 55 6 1085 1094

80. MatuteDRButlerIATurissiniDACoyneJA 2010 A test of the snowball theory for the rate of evolution of hybrid incompatibilities. Science 329 5998 1518 1521

81. MoyleLCNakazatoT 2010 Hybrid incompatibility “snowballs” between Solanum species. Science 329 5998 1521 1523

82. CrockerJTamoriYErivesA 2008 Evolution acts on enhancer organization to fine-tune gradient threshold readouts. PLoS Biol 6 11 e263 doi:10.1371/journal.pbio.0060263

83. GregorTMcGregorAPWieschausEF 2008 Shape and function of the bicoid morphogen gradient in dipteran species with different sized embryos. Dev Biol 316 2 350 358

84. LinnenCRKingsleyEPJensenJDHoekstraHE 2009 On the origin and spread of an adaptive allele in deer mice. Science 325 5944 1095 1098

85. ShirangiTRDufourHDWilliamsTMCarrollSB 2009 Rapid evolution of sex pheromone-producing enzyme expression in Drosophila. PLoS Biol 7 8 e1000168 doi:10.1371/journal.pbio.1000168

86. EllegrenHParschJ 2007 The evolution of sex-biased genes and sex-biased gene expression. Nat Rev Genet 8 9 689 698

87. GilleardJS 2004 The use of Caenorhabditis elegans in parasitic nematode research. Parasitology 128 S49 S70

88. HeZEichelKRuvinskyI 2011 Functional conservation of cis-regulatory elements of heat-shock genes over long evolutionary distances. PLoS ONE 6 7 e22677 doi:10.1371/journal.pone.0022677

89. SkavdisGSidenKiamosIMullerHMCrisantiALouisC 1996 Conserved function of Anopheles gambiae midgut-specific promoters in the fruitfly. EMBO J 15 2 344 350

90. LottSEVillaltaJESchrothGPLuoSTonkinLA 2011 Noncanonical compensation of zygotic X transcription in early Drosophila melanogaster development revealed through single-embryo RNA-seq. PLoS Biol 9 2 e1000590 doi:10.1371/journal.pbio.1000590

91. WilliamsTMCarrollSB 2009 Genetic and molecular insights into the development and evolution of sexual dimorphism. Nat Rev Genet 10 11 797 804

92. Pires-daSilvaA 2007 Evolution of the control of sexual identity in nematodes. Semin Cell Dev Biol 18 3 362 370

93. MitsialisSaKafatosFC 1985 Regulatory elements controlling chorion gene expression are conserved between flies and moths. Nature 317 6036 453 456

94. MarriSGuptaBP 2009 Dissection of lin-11 enhancer regions in caenorhabditis elegans and other nematodes. Dev Biol 325 2 402 11

95. HoMCWJohnsenHGoetzSESchillerBJBaeE 2009 Functional evolution of cis-regulatory modules at a homeotic gene in Drosophila. PLoS Genet 5 11 e1000709 doi:10.1371/journal.pgen.1000709

96. ZinzenRPCandeJRonshaugenMPapatsenkoDLevineM 2006 Evolution of the ventral midline in insect embryos. Developmental Cell 11 6 895 902

97. LibermanLMStathopoulosA 2009 Design flexibility in cis-regulatory control of gene expression: Synthetic and comparative evidence. Dev Biol 327 2 578 589

98. DowellRD 2010 Transcription factor binding variation in the evolution of gene regulation. Trends in Genetics 26 11 468 475

99. HaddrillPRBachtrogDAndolfattoP 2008 Positive and negative selection on noncoding DNA in Drosophila simulans. Mol Biol Evol 25 9 1825 1834

100. HeBZHollowayAKMaerklSJKreitmanM 2011 Does positive selection drive transcription factor binding site turnover? A test with Drosophila cis-regulatory modules. PLoS Genet 7 4 e1002053 doi:10.1371/journal.pgen.10002053

101. BullaugheyK 2011 Changes in selective effects over time facilitate turnover of enhancer sequences. Genetics 187 2 567-U328

102. TrueJRHaagES 2001 Developmental system drift and flexibility in evolutionary trajectories. Evol Dev 3 2 109 119

103. SwansonCISchwimmerDBBaroloS 2011 Rapid evolutionary rewiring of a structurally constrained eye enhancer. Current Biology 21 14 1186 1196

104. RosenthalR 1979 The file drawer problem and tolerance for null results. Psychol Bull 86 3 638 641

105. RuvinskyIRuvkunG 2003 Functional tests of enhancer conservation between distantly related species. Development 130 21 5133 5142

106. LocascioAAnielloFAmorosoAManzanaresMKrumlaufR 1999 Patterning the ascidian nervous system: Structure, expression and transgenic analysis of the CiHox3 gene. Development 126 21 4737 4748

107. BrennanMDWuCYBerryAJ 1988 Tissue-specific regulatory differences for the alcohol-dehydrogenase genes of hawaiian Drosophila are conserved in Drosophila melanogaster transformants. Proc Natl Acad Sci U S A 85 18 6866 6869

108. WangXDChamberlinHM 2004 Evolutionary innovation of the excretory system in Caenorhabditis elegans. Nat Genet 36 3 231 232

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2012 Číslo 1
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#