#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

The and Hybrid Incompatibility Genes Suppress a Broad Range of Heterochromatic Repeats


Sister species capable of mating often produce hybrids that are sterile or die during development. This reproductive isolation is caused by incompatibilities between the two sister species' genomes. Some hybrid incompatibilities involve genes that encode rapidly evolving proteins that localize to heterochromatin. Heterochromatin is largely made up of highly repetitive transposable elements and satellite DNAs. It has been hypothesized that rapid changes in heterochromatic DNA drives the changes in these HI genes and thus the evolution of reproductive isolation. In support of this model, we show that two rapidly evolving HI proteins, Lhr and Hmr, which reproductively isolate the fruit fly sister species D. melanogaster and D. simulans, repress transposable elements and satellite DNAs. These proteins also help regulate the length of the atypical Drosophila telomeres, which are themselves made of domesticated transposable elements. Our data suggest that these proteins are part of the adaptive machinery that allows the host to respond to changes and increases in heterochromatin and to maintain the activity of genes located within or adjacent to heterochromatin.


Vyšlo v časopise: The and Hybrid Incompatibility Genes Suppress a Broad Range of Heterochromatic Repeats. PLoS Genet 10(3): e32767. doi:10.1371/journal.pgen.1004240
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004240

Souhrn

Sister species capable of mating often produce hybrids that are sterile or die during development. This reproductive isolation is caused by incompatibilities between the two sister species' genomes. Some hybrid incompatibilities involve genes that encode rapidly evolving proteins that localize to heterochromatin. Heterochromatin is largely made up of highly repetitive transposable elements and satellite DNAs. It has been hypothesized that rapid changes in heterochromatic DNA drives the changes in these HI genes and thus the evolution of reproductive isolation. In support of this model, we show that two rapidly evolving HI proteins, Lhr and Hmr, which reproductively isolate the fruit fly sister species D. melanogaster and D. simulans, repress transposable elements and satellite DNAs. These proteins also help regulate the length of the atypical Drosophila telomeres, which are themselves made of domesticated transposable elements. Our data suggest that these proteins are part of the adaptive machinery that allows the host to respond to changes and increases in heterochromatin and to maintain the activity of genes located within or adjacent to heterochromatin.


Zdroje

1. MaheshwariS, BarbashDA (2011) The genetics of hybrid incompatibilities. Annu Rev Genet 45: 331–355.

2. PresgravesDC (2010) The molecular evolutionary basis of species formation. Nat Rev Genet 11: 175–180.

3. BarbashDA, SiinoDF, TaroneAM, RooteJ (2003) A rapidly evolving MYB-related protein causes species isolation in Drosophila. Proc Natl Acad Sci U S A 100: 5302–5307.

4. ArunaS, FloresHA, BarbashDA (2009) Reduced fertility of Drosophila melanogaster Hybrid male rescue (Hmr) mutant females is partially complemented by Hmr orthologs from sibling species. Genetics 181: 1437–1450.

5. TangS, PresgravesDC (2009) Evolution of the Drosophila nuclear pore complex results in multiple hybrid incompatibilities. Science 323: 779–782.

6. BrideauNJ, FloresHA, WangJ, MaheshwariS, WangX, BarbashDA (2006) Two Dobzhansky-Muller genes interact to cause hybrid lethality in Drosophila. Science 314: 1292–1295.

7. BarbashDA, AwadallaP, TaroneAM (2004) Functional divergence caused by ancient positive selection of a Drosophila hybrid incompatibility locus. PLoS Biol 2: e142.

8. MaheshwariS, BarbashDA (2012) Cis-by-Trans regulatory divergence causes the asymmetric lethal effects of an ancestral hybrid incompatibility gene. PLoS Genet 8: e1002597.

9. BrideauNJ, BarbashDA (2011) Functional conservation of the Drosophila hybrid incompatibility gene Lhr. BMC Evol Biol 11: 57.

10. WatanabeTK (1979) A gene that rescues the lethal hybrids between Drosophila melanogaster and D. simulans. Jpn J Genet 54: 325–331.

11. HutterP, AshburnerM (1987) Genetic rescue of inviable hybrids between Drosophila melanogaster and its sibling species. Nature 327: 331–333.

12. GreilF, de WitE, BussemakerHJ, van SteenselB (2007) HP1 controls genomic targeting of four novel heterochromatin proteins in Drosophila. EMBO J 26: 741–751.

13. Lohe A, Roberts P (1988) Evolution of satellite DNA sequences in Drosophila. In: Verma RS, editors. Heterochromatin, Molecular and Structural Aspects. Cambridge: Cambridge Univ. Press. pp. 148–186.

14. BoscoG, CampbellP, Leiva-NetoJT, MarkowTA (2007) Analysis of Drosophila species genome size and satellite DNA content reveals significant differences among strains as well as between species. Genetics 177: 1277–1290.

15. GregoryTR (2005) Synergy between sequence and size in large-scale genomics. Nat Rev Genet 6: 699–708.

16. CharlesworthB, SniegowskiP, StephanW (1994) The evolutionary dynamics of repetitive DNA in eukaryotes. Nature 371: 215–220.

17. HickeyDA (1982) Selfish DNA: a sexually-transmitted nuclear parasite. Genetics 101: 519–531.

18. WalkerPM (1971) Origin of satellite DNA. Nature 229: 306–308.

19. BlumenstielJP (2011) Evolutionary dynamics of transposable elements in a small RNA world. Trends Genet 27: 23–31.

20. KhuranaJS, TheurkaufW (2010) piRNAs, transposon silencing, and Drosophila germline development. J Cell Biol 191: 905–913.

21. UsakinL, AbadJ, VaginVV, de PablosB, VillasanteA, GvozdevVA (2007) Transcription of the 1.688 satellite DNA family is under the control of RNA interference machinery in Drosophila melanogaster ovaries. Genetics 176: 1343–1349.

22. LeeYCG, LangleyCH (2012) Long-term and short-term evolutionary impacts of transposable elements on Drosophila. Genetics 192: 1411–1432.

23. JohnsonNA (2010) Hybrid incompatibility genes: remnants of a genomic battlefield? Trends Genet 26: 317–325.

24. LeratE, BurletN, BiémontC, VieiraC (2011) Comparative analysis of transposable elements in the melanogaster subgroup sequenced genomes. Gene 473: 100–109.

25. AndreyevaEN, BelyaevaES, SemeshinVF, PokholkovaGV, ZhimulevIF (2005) Three distinct chromatin domains in telomere ends of polytene chromosomes in Drosophila melanogaster Tel mutants. J Cell Sci 118: 5465–5477.

26. MeffordHC, TraskBJ (2002) The complex structure and dynamic evolution of human subtelomeres. Nat Rev Genet 3: 91–102.

27. AndersonJA, GillilandWD, LangleyCH (2009) Molecular population genetics and evolution of Drosophila meiosis genes. Genetics 181: 177–185.

28. RaffaGD, CiapponiL, CenciG, GattiM (2011) Terminin: a protein complex that mediates epigenetic maintenance of Drosophila telomeres. Nucleus 2: 383–391.

29. ZwickME, SalstromJL, LangleyCH (1999) Genetic variation in rates of nondisjunction: association of two naturally occurring polymorphisms in the chromokinesin nod with increased rates of nondisjunction in Drosophila melanogaster. Genetics 152: 1605–1614.

30. GiotL, BaderJS, BrouwerC, ChaudhuriA, KuangB, et al. (2003) A protein interaction map of Drosophila melanogaster. Science 302: 1727–1736.

31. BhaskarV, CoureyAJ (2002) The MADF-BESS domain factor Dip3 potentiates synergistic activation by Dorsal and Twist. Gene 299: 173–184.

32. PerratPN, DasGuptaS, WangJ, TheurkaufW, WengZ, et al. (2013) Transposition-driven genomic heterogeneity in the Drosophila brain. Science 340: 91–95.

33. PardueM-L, DebarysheP (2011) Adapting to life at the end of the line: How Drosophila telomeric retrotransposons cope with their job. Mob Genet Elements 1: 128–134.

34. LoheAR, HillikerAJ, RobertsPA (1993) Mapping simple repeated DNA sequences in heterochromatin of Drosophila melanogaster. Genetics 134: 1149–1174.

35. PlateroJS, CsinkAK, QuintanillaA, HenikoffS (1998) Changes in chromosomal localization of heterochromatin-binding proteins during the cell cycle in Drosophila. J Cell Biol 140: 1297–1306.

36. BarichevaEA, BerriosM, BogachevSS, BorisevichIV, LapikER, et al. (1996) DNA from Drosophila melanogaster beta-heterochromatin binds specifically to nuclear lamins in vitro and the nuclear envelope in situ. Gene 171: 171–176.

37. VaginVV, SigovaA, LiC, SeitzH, GvozdevV, ZamorePD (2006) A distinct small RNA pathway silences selfish genetic elements in the germline. Science 313: 320–324.

38. LiC, VaginVV, LeeS, XuJ, MaS, et al. (2009) Collapse of germline piRNAs in the absence of Argonaute3 reveals somatic piRNAs in flies. Cell 137: 509–521.

39. MaloneCD, BrenneckeJ, DusM, StarkA, McCombieWR, et al. (2009) Specialized piRNA pathways act in germline and somatic tissues of the Drosophila ovary. Cell 137: 522–535.

40. DönertasD, SienskiG, BrenneckeJ (2013) Drosophila Gtsf1 is an essential component of the Piwi-mediated transcriptional silencing complex. Genes Dev 27: 1693–1705.

41. BrenneckeJ, AravinAA, StarkA, DusM, KellisM, et al. (2007) Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 128: 1089–1103.

42. BlumenstielJP, HartlDL (2005) Evidence for maternally transmitted small interfering RNA in the repression of transposition in Drosophila virilis. Proc Natl Acad Sci U S A 102: 15965–15970.

43. CzechB, MaloneCD, ZhouR, StarkA, SchlingeheydeC, et al. (2008) An endogenous small interfering RNA pathway in Drosophila. Nature 453: 798–802.

44. RozhkovNV, AravinAA, ZelentsovaES, SchostakNG, SachidanandamR, et al. (2010) Small RNA-based silencing strategies for transposons in the process of invading Drosophila species. RNA 16: 1634–1645.

45. KoflerR, BetancourtAJ, SchlöttererC (2012) Sequencing of pooled DNA samples (Pool-Seq) uncovers complex dynamics of transposable element insertions in Drosophila melanogaster. PLoS Genet 8: e1002487.

46. BergmanCM, BensassonD (2007) Recent LTR retrotransposon insertion contrasts with waves of non-LTR insertion since speciation in Drosophila melanogaster. Proc Natl Acad Sci U S A 104: 11340–11345.

47. RebolloR, LeratE, KleineLL, BiémontC, VieiraC (2008) Losing helena: the extinction of a drosophila line-like element. BMC Genomics 9: 149.

48. KelleherES, EdelmanNB, BarbashDA (2012) Drosophila interspecific hybrids phenocopy piRNA-pathway mutants. PLoS Biol 10: e1001428.

49. EissenbergJC, ElginSC (2000) The HP1 protein family: getting a grip on chromatin. Curr Opin Genet Dev 10: 204–210.

50. SavitskyM, KravchukO, MelnikovaL, GeorgievP (2002) Heterochromatin protein 1 is involved in control of telomere elongation in Drosophila melanogaster. Mol Cell Biol 22: 3204–3218.

51. WangSH, ElginSCR (2011) Drosophila Piwi functions downstream of piRNA production mediating a chromatin-based transposon silencing mechanism in female germ line. Proc Natl Acad Sci U S A 108: 21164–21169.

52. EissenbergJC, JamesTC, Foster-HartnettDM, HartnettT, NganV, et al. (1990) Mutation in a heterochromatin-specific chromosomal protein is associated with suppression of position-effect variegation in Drosophila melanogaster. Proc Natl Acad Sci U S A 87: 9923–9927.

53. ThomaeAW, SchadeGOM, PadekenJ, BorathM, VetterI, et al. (2013) A Pair of Centromeric Proteins Mediates Reproductive Isolation in Drosophila Species. Dev Cell 27 (4) 412–24.

54. ZhangY, MaloneJH, PowellSK, PeriwalV, SpanaE, et al. (2010) Expression in aneuploid Drosophila S2 cells. PLoS Biol 8: e1000320.

55. SawamuraK (2012) Chromatin evolution and molecular drive in speciation. Int J Evol Biol 2012: 301894.

56. DoolittleWF (2013) Is junk DNA bunk? A critique of ENCODE. Proc Natl Acad Sci U S A 110: 5294–5300.

57. PetrovDA (2002) Mutational equilibrium model of genome size evolution. Theor Popul Biol 61: 531–544.

58. ShepelevVA, AlexandrovAA, YurovYB, AlexandrovIA (2009) The evolutionary origin of man can be traced in the layers of defunct ancestral alpha satellites flanking the active centromeres of human chromosomes. PLoS Genet 5: e1000641.

59. WerrenJH (2011) Selfish genetic elements, genetic conflict, and evolutionary innovation. Proc Natl Acad Sci U S A 108 Suppl 2: 10863–10870.

60. Bregliano J-C, Kidwell MG (1983) Hybrid dysgenesis determinants. In: Mob Genet Elements. Academic Press, New York.

61. FishmanL, SaundersA (2008) Centromere-associated female meiotic drive entails male fitness costs in monkeyflowers. Science 322: 1559–1562.

62. GonzálezJ, PetrovDA (2012) Evolution of genome content: population dynamics of transposable elements in flies and humans. Methods Mol Biol 855: 361–383.

63. LeeYCG, LangleyCH (2010) Transposable elements in natural populations of Drosophila melanogaster. Philos Trans R Soc Lond B Biol Sci 365: 1219–1228.

64. KlenovMS, SokolovaOA, YakushevEY, StolyarenkoAD, MikhalevaEA, et al. (2011) Separation of stem cell maintenance and transposon silencing functions of Piwi protein. Proc Natl Acad Sci U S A 108: 18760–18765.

65. YamanakaS, MehtaS, Reyes-TurcuFE, ZhuangF, FuchsRT, et al. (2013) RNAi triggered by specialized machinery silences developmental genes and retrotransposons. Nature 493: 557–560.

66. VillasanteA, AbadJP, PlanellóR, Méndez-LagoM, CelnikerSE, de PablosB (2007) Drosophila telomeric retrotransposons derived from an ancestral element that was recruited to replace telomerase. Genome Res 17: 1909–1918.

67. Shpiz S, Kalmykova A (2012) Control of Telomere Length in Drosophila. In: Li, B, editor. Review of Selected Topic of Telomere Biology. Rijeka: InTech. pp. 33–56.

68. RanganP, MaloneCD, NavarroC, NewboldSP, HayesPS, et al. (2011) piRNA Production Requires Heterochromatin Formation in Drosophila. Curr Biol 21 (16) 1373–9.

69. SageBT, CsinkAK (2003) Heterochromatic self-association, a determinant of nuclear organization, does not require sequence homology in Drosophila. Genetics 165: 1183–1193.

70. FerreePM, PrasadS (2012) How can satellite DNA divergence cause reproductive isolation? Let us count the chromosomal ways. Genet Res Int 2012: 430136.

71. BonaccorsiS, GattiM, PisanoC, LoheA (1990) Transcription of a satellite DNA on two Y chromosome loops of Drosophila melanogaster. Chromosoma 99: 260–266.

72. HeB, CaudyA, ParsonsL, RosebrockA, PaneA, et al. (2012) Mapping the pericentric heterochromatin by comparative genomic hybridization analysis and chromosome deletions in Drosophila melanogaster. Genome Res

73. GranzottoA, LopesFR, VieiraC, CararetoCMA (2011) Vertical inheritance and bursts of transposition have shaped the evolution of the BS non-LTR retrotransposon in Drosophila. Mol Genet Genomics 286: 57–66.

74. CsinkAK, McDonaldJF (1995) Analysis of copia sequence variation within and between Drosophila species. Mol Biol Evol 12: 83–93.

75. DowsettAP, YoungMW (1982) Differing levels of dispersed repetitive DNA among closely related species of Drosophila. Proc Natl Acad Sci U S A 79: 4570–4574.

76. YasuharaJC, WakimotoBT (2006) Oxymoron no more: the expanding world of heterochromatic genes. Trends Genet 22: 330–338.

77. CastilloDM, MoyleLC (2012) Evolutionary Implications of Mechanistic Models of TE-Mediated Hybrid Incompatibility. Int J Evol Biol 2012: 698198.

78. KerkisJ (1933) Development of gonads in hybrids between Drosophila melanogaster and Drosophila simulans. J Exper Zool 66: 477–509.

79. KawamuraY, SaitoK, KinT, OnoY, AsaiK, et al. (2008) Drosophila endogenous small RNAs bind to Argonaute 2 in somatic cells. Nature 453: 793–797.

80. GhildiyalM, SeitzH, HorwichMD, LiC, DuT, et al. (2008) Endogenous siRNAs derived from transposons and mRNAs in Drosophila somatic cells. Science 320: 1077–1081.

81. BarbashDA, RooteJ, AshburnerM (2000) The Drosophila melanogaster Hybrid male rescue gene causes inviability in male and female species hybrids. Genetics 154: 1747–1771.

82. OrrHA, IrvingS (2000) Genetic analysis of the Hybrid male rescue locus of Drosophila. Genetics 155: 225–231.

83. FerreePM, BarbashDA (2009) Species-specific heterochromatin prevents mitotic chromosome segregation to cause hybrid lethality in Drosophila. PLoS Biol 7: e1000234.

84. GongWJ, GolicKG (2004) Genomic deletions of the Drosophila melanogaster Hsp70 genes. Genetics 168: 1467–1476.

85. HernanR, HeuermannK, BrizzardB (2000) Multiple epitope tagging of expressed proteins for enhanced detection. Biotechniques 28: 789–793.

86. GrothAC, FishM, NusseR, CalosMP (2004) Construction of transgenic Drosophila by using the site-specific integrase from phage phiC31. Genetics 166: 1775–1782.

87. VenkenKJT, HeY, HoskinsRA, BellenHJ (2006) P[acman]: a BAC transgenic platform for targeted insertion of large DNA fragments in D. melanogaster. Science 314: 1747–1751.

88. BarbashDA, LoriganJG (2007) Lethality in Drosophila melanogaster/Drosophila simulans species hybrids is not associated with substantial transcriptional misregulation. J Exp Zool B Mol Dev Evol 308: 74–84.

89. PaneA, WehrK, SchüpbachT (2007) zucchini and squash encode two putative nucleases required for rasiRNA production in the Drosophila germline. Dev Cell 12: 851–862.

90. KlenovMS, LavrovSA, StolyarenkoAD, RyazanskySS, AravinAA, et al. (2007) Repeat-associated siRNAs cause chromatin silencing of retrotransposons in the Drosophila melanogaster germline. Nucleic Acids Res 35: 5430–5438.

91. LangmeadB, TrapnellC, PopM, SalzbergSL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25.

92. TrapnellC, PachterL, SalzbergSL (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25: 1105–1111.

93. TrapnellC, WilliamsBA, PerteaG, MortazaviA, KwanG, et al. (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28: 511–515.

94. GeorgeJA, DeBaryshePG, TraverseKL, CelnikerSE, PardueM-L (2006) Genomic organization of the Drosophila telomere retrotransposable elements. Genome Res 16: 1231–1240.

95. WangL, FengZ, WangX, WangX, ZhangX (2010) DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26: 136–138.

96. JurkaJ, KapitonovVV, PavlicekA, KlonowskiP, KohanyO, WalichiewiczJ (2005) Repbase Update, a database of eukaryotic repetitive elements. Cytogenet Genome Res 110: 462–467.

97. Dernburg AF (2000) In situ hybridization to somatic chromosomes. In: Drosophila protocols. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. pp. 22–55.

98. SmithCD, EdgarRC, YandellMD, SmithDR, CelnikerSE, et al. (2007) Improved repeat identification and masking in Dipterans. Gene 389: 1–9.

99. KaminkerJS, BergmanCM, KronmillerB, CarlsonJ, SvirskasR, et al. (2002) The transposable elements of the Drosophila melanogaster euchromatin: a genomics perspective. Genome Biol 3: RESEARCH0084.

100. RiddleNC, MinodaA, KharchenkoPV, AlekseyenkoAA, SchwartzYB, et al. (2011) Plasticity in patterns of histone modifications and chromosomal proteins in Drosophila heterochromatin. Genome Res 21: 147–163.

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2014 Číslo 3
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
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#