#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

piRNAs Are Associated with Diverse Transgenerational Effects on Gene and Transposon Expression in a Hybrid Dysgenic Syndrome of .


Transposable elements (TEs) are selfish elements that copy themselves. More than half of the human genome is comprised of such elements. Studies in the fruit flies Drosophila melanogaster and D. virilis have been important in demonstrating a role for RNA silencing by PIWI-interacting RNAs (piRNAs) in protecting the genome against these harmful elements. These small RNAs are capable of recognizing TE mRNAs and mediating their destruction. They are also transmitted by the female germline to offspring in order to maintain a stable genome across generations. When males carrying a particular TE family are crossed with females lacking the element, the mother is unable to provide genome defense via complementary piRNAs that target the element. This leads to excess TE activation in the germline and sterility, a phenomenon known as hybrid dysgenesis. In this article we characterize the genomic landscape of TE destabilization that occurs in dysgenic crosses of D. virilis. We demonstrate that this mobilization is associated with an increased level of germline TE expression that persists through adulthood. In addition, we find that TE activation is associated with diverse effects on normal gene expression that are also mediated by piRNAs.


Vyšlo v časopise: piRNAs Are Associated with Diverse Transgenerational Effects on Gene and Transposon Expression in a Hybrid Dysgenic Syndrome of .. PLoS Genet 11(8): e32767. doi:10.1371/journal.pgen.1005332
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005332

Souhrn

Transposable elements (TEs) are selfish elements that copy themselves. More than half of the human genome is comprised of such elements. Studies in the fruit flies Drosophila melanogaster and D. virilis have been important in demonstrating a role for RNA silencing by PIWI-interacting RNAs (piRNAs) in protecting the genome against these harmful elements. These small RNAs are capable of recognizing TE mRNAs and mediating their destruction. They are also transmitted by the female germline to offspring in order to maintain a stable genome across generations. When males carrying a particular TE family are crossed with females lacking the element, the mother is unable to provide genome defense via complementary piRNAs that target the element. This leads to excess TE activation in the germline and sterility, a phenomenon known as hybrid dysgenesis. In this article we characterize the genomic landscape of TE destabilization that occurs in dysgenic crosses of D. virilis. We demonstrate that this mobilization is associated with an increased level of germline TE expression that persists through adulthood. In addition, we find that TE activation is associated with diverse effects on normal gene expression that are also mediated by piRNAs.


Zdroje

1. Hickey DA (1982) Selfish DNA: A sexually-transmitted nuclear parasite. Genetics 101: 519–531. 6293914

2. Charlesworth B, Charlesworth D (1983) The population dynamics of transposable elements. Genetical Research 42: 1–27.

3. Charlesworth B, Langley CH (1989) The population genetics of Drosophila transposable elements. Annual Review of Genetics 23: 251–287. 2559652

4. Daniels SB, Peterson KR, Strausbaugh LD, Kidwell MG, Chovnick A (1990) Evidence for Horizontal Transmission of the P-Transposable Element between Drosophila Species. Genetics 124: 339–355. 2155157

5. Anxolabehere D, Kidwell MG, Periquet G (1988) Molecular characteristics of diverse populations are consistent with the hypothesis of a recent invasion of Drosophila melanogaster by mobile P elements. Mol Biol Evol 5: 252–269. 2838720

6. Coyne JA (1986) Meiotic segregation and male recombination in interspecific hybrids of Drosophila Genetics 114: 485–494.

7. Coyne JA (1989) Mutation rates in hybrids between sibling species of Drosophila. Heredity (Edinb) 63 (Pt 2): 155–162.

8. Dion-Cote AM, Renaut S, Normandeau E, Bernatchez L (2014) RNA-seq reveals transcriptomic shock involving transposable elements reactivation in hybrids of young lake whitefish species. Mol Biol Evol 31: 1188–1199. doi: 10.1093/molbev/msu069 24505119

9. Josefsson C, Dilkes B, Comai L (2006) Parent-dependent loss of gene silencing during interspecies hybridization. Current Biology 16: 1322–1328. 16824920

10. O'Neill RJ, O'Neill MJ, Graves JA (1998) Undermethylation associated with retroelement activation and chromosome remodelling in an interspecific mammalian hybrid. Nature 393: 68–72. 9590690

11. O'Neill RJ, O'Neill MJ, Graves JA (2002) Corrigendum:Undermethylation associated with retroelement activation and chromosome remodelling in an interspecific mammalian hybrid. Nature 420: 106.

12. Hey J (1989) Speciation via hybrid dysgenesis: negative evidence from the Drosophila affinis subgroup. Genetica 78: 97–104.

13. Vela D, Fontdevila A, Vieira C, Garcia Guerreiro MP (2014) A genome-wide survey of genetic instability by transposition in Drosophila hybrids. PLoS One 9: e88992. doi: 10.1371/journal.pone.0088992 24586475

14. Labrador M, Farre M, Utzet F, Fontdevila A (1999) Interspecific hybridization increases transposition rates of Osvaldo. Mol Biol Evol 16: 931–937. 10406110

15. Kelleher ES, Edelman NB, Barbash DA (2012) Drosophila interspecific hybrids phenocopy piRNA-pathway mutants. PLoS Biol 10: e1001428. doi: 10.1371/journal.pbio.1001428 23189033

16. Kidwell MG, Novy JB (1979) Hybrid dysgenesis in Drosophila melanogaster—Sterility resulting from gonadal-dysgenesis in the P-M system. Genetics 92: 1127–1140. 17248943

17. Kidwell MG, Kidwell JF, Sved JA (1977) Hybrid Dysgenesis in Drosophila melanogaster: A Syndrome of Aberrant Traits Including Mutation, Sterility and Male Recombination. Genetics 86: 813–833. 17248751

18. Bingham PM, Kidwell MG, Rubin GM (1982) The molecular basis of P-M dysgenesis—The role of the P-element, a P-Strain-Specific Transposon Family. Cell 29: 995–1004. 6295641

19. Bucheton A, Paro R, Sang HM, Pelisson A, Finnegan DJ (1984) The molecular basis of the I-R hybrid dysgenesis syndreom in Drosophila melanogaster—Identification, cloning and properties of the I-Factor. Cell 38: 153–163. 6088060

20. Yannopoulos G, Stamatis N, Monastirioti M, Hatzopoulos P, Louis C (1987) hobo is responsible for the induction of hybrid dysgenesis by strains of Drosophila melanogater bearing the male recombination factor 23.5MRF. Cell 49: 487–495. 3032457

21. Aravin AA, Lagos-Quintana M, Yalcin A, Zavolan M, Marks D, et al. (2003) The small RNA profile during Drosophila melanogaster development. Developmental Cell 5: 337–350. 12919683

22. Aravin AA, Hannon GJ, Brennecke J (2007) The Piwi-piRNA pathway provides an adaptive defense in the transposon arms race. Science 318: 761–764. 17975059

23. Brennecke J, Aravin AA, Stark A, Dus M, Kellis M, et al. (2007) Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 128: 1089–1103. 17346786

24. Brennecke J, Malone CD, Aravin AA, Sachidanandam R, Stark A, et al. (2008) An Epigenetic Role for Maternally Inherited piRNAs in Transposon Silencing. Science 322: 1387–1392. doi: 10.1126/science.1165171 19039138

25. Gunawardane LS, Saito K, Nishida KM, Miyoshi K, Kawamura Y, et al. (2007) A slicer-mediated mechanism for repeat-associated siRNA 5 ' end formation in Drosophila. Science 315: 1587–1590. 17322028

26. Grentzinger T, Armenise C, Brun C, Mugat B, Serrano V, et al. (2012) piRNA-mediated transgenerational inheritance of an acquired trait. Genome Res 22: 1877–1888. doi: 10.1101/gr.136614.111 22555593

27. Chambeyron S, Popkova A, Payen-Groschene G, Brun C, Laouini D, et al. (2008) piRNA-mediated nuclear accumulation of retrotransposon transcripts in the Drosophila female germline. Proc Natl Acad Sci U S A 105: 14964–14969. doi: 10.1073/pnas.0805943105 18809914

28. Khurana JS, Wang J, Xu J, Koppetsch BS, Thomson TC, et al. (2011) Adaptation to P Element Transposon Invasion in Drosophila melanogaster. Cell 147: 1551–1563. doi: 10.1016/j.cell.2011.11.042 22196730

29. Evgen'ev MB, Arkhipova IR (2005) Penelope-like elements—a new class of retroelements: distribution, function and possible evolutionary significance. Cytogenet Genome Res 110: 510–521. 16093704

30. Lyozin GT, Makarova KS, Velikodvorskaja VV, Zelentsova HS, Khechumian RR, et al. (2001) The structure and evolution of Penelope in the virilis species group of Drosophila: an ancient lineage of retroelements. Journal of Molecular Evolution 52: 445–456. 11443348

31. Evgenev MB, Zelentsova H, Shostak N, Kozitsina M, Barskyi V, et al. (1997) Penelope, a new family of transposable elements and its possible role in hybrid dysgenesis in Drosophila virilis. Proceedings of the National Academy of Sciences of the United States of America 94: 196–201. 8990185

32. Vieira J, Vieira CP, Hartl DL, Lozovskaya ER (1998) Factors contributing to the hybrid dysgenesis syndrome in Drosophila virilis. Genetical Research 71: 109–117. 9717433

33. Blumenstiel JP (2014) Whole genome sequencing in Drosophila virilis identifies Polyphemus, a recently activated Tc1-like transposon with a possible role in hybrid dysgenesis. Mob DNA 5: 6. doi: 10.1186/1759-8753-5-6 24555450

34. Rozhkov NV, Schostak NG, Zelentsova ES, Yushenova IA, Zatsepina OG, et al. (2013) Evolution and dynamics of small RNA response to a retroelement invasion in Drosophila. Mol Biol Evol 30: 397–408. doi: 10.1093/molbev/mss241 23079419

35. Rozhkov NV, Aravin AA, Zelentsova ES, Schostak NG, Sachidanandam R, et al. (2010) Small RNA-based silencing strategies for transposons in the process of invading Drosophila species. Rna-a Publication of the Rna Society 16: 1634–1645.

36. Gerasimova T, Mizrokhi L, Georgiev G (1984) Transposition bursts in genetically unstable Drosophila melanogaster. Nature 309: 714–716.

37. Eggleston WB, Johnson-Schlitz DM, Engels WR (1988) P-M hybrid dysgenesis does not mobilize other transposable element families in D. melanogaster. Nature 331: 368–370. 2829026

38. Petrov DA, Schutzman JL, Hartl DL, Lozovskaya ER (1995) Diverse transposable elements are mobilized in hybrid dysgenesis in Drosophila virilis Proceedings of the National Academy of Sciences of the United States of America 92: 8050–8054. 7644536

39. Rozhkov NV, Zelentsova ES, Shostak NG, Evgen'ev MB (2011) Expression of Drosophila virilis retroelements and role of small RNAs in their intrastrain transposition. PLoS One 6: e21883. doi: 10.1371/journal.pone.0021883 21779346

40. Scheinker VS, Lozovskaya ER, Bishop JG, Corces VG, Evgenev MB (1990) A long terminal repeat-containing retrotransposon in mobilized during hybrid dysgenesis in Drosophila virilis. Proceedings of the National Academy of Sciences of the United States of America 87: 9615–9619. 2175908

41. Casacuberta E, Pardue ML (2003) Transposon telomeres are widely distributed in the Drosophila genus: TART elements in the virilis group. Proc Natl Acad Sci U S A 100: 3363–3368. 12626755

42. Savitsky M, Kwon D, Georgiev P, Kalmykova A, Gvozdev V (2006) Telomere elongation is under the control of the RNAi-based mechanism in the Drosophila germline. Genes & Development 20: 345–354.

43. Shpiz S, Olovnikov I, Sergeeva A, Lavrov S, Abramov Y, et al. (2011) Mechanism of the piRNA-mediated silencing of Drosophila telomeric retrotransposons. Nucleic Acids Res 39: 8703–8711. doi: 10.1093/nar/gkr552 21764773

44. Khurana JS, Xu J, Weng Z, Theurkauf WE (2010) Distinct functions for the Drosophila piRNA pathway in genome maintenance and telomere protection. PLoS Genet 6: e1001246. doi: 10.1371/journal.pgen.1001246 21179579

45. Evgen'ev MB (2013) What happens when Penelope comes?: An unusual retroelement invades a host species genome exploring different strategies. Mob Genet Elements 3: e24542. 23914310

46. Daniels SB, Peterson KR, Strausbaugh LD, Kidwell MG, Chovnick A (1990) Evidence for horizontal transmission of the P transposable element between Drosophila species. Genetics 124: 339–355. 2155157

47. Morales-Hojas R, Vieira CP, Vieira J (2006) The evolutionary history of the transposable element Penelope in the Drosophila virilis group of species. J Mol Evol 63: 262–273. 16830099

48. Chambeyron S, Popkova A, Payen-Groschene G, Brun C, Laouini D, et al. (2008) piRNA-mediated nuclear accumulation of retrotransposon transcripts in the Drosophila female germline. Proceedings of the National Academy of Sciences of the United States of America 105: 14964–14969. doi: 10.1073/pnas.0805943105 18809914

49. Blumenstiel JP, Hartl DL (2005) Evidence for maternally transmitted small interfering RNA in the repression of transposition in Drosophila virilis. Proceedings of the National Academy of Sciences of the United States of America 102: 15965–15970. 16247000

50. Eden E, Navon R, Steinfeld I, Lipson D, Yakhini Z (2009) GOrilla: a tool for discovery and visualization of enriched GO terms in ranked gene lists. BMC Bioinformatics 10: 48. doi: 10.1186/1471-2105-10-48 19192299

51. Pavlidis P, Jensen JD, Stephan W, Stamatakis A (2012) A critical assessment of storytelling: gene ontology categories and the importance of validating genomic scans. Mol Biol Evol 29: 3237–3248. 22617950

52. Gu T, Elgin SC (2013) Maternal depletion of Piwi, a component of the RNAi system, impacts heterochromatin formation in Drosophila. PLoS Genet 9: e1003780. doi: 10.1371/journal.pgen.1003780 24068954

53. Haynes KA, Caudy AA, Collins L, Elgin SCR (2006) Element 1360 and RNAi components contribute to HP1-dependent silencing of a pericentric reporter. Current Biology 16: 2222–2227. 17113386

54. Sentmanat MF, Elgin SC (2012) Ectopic assembly of heterochromatin in Drosophila melanogaster triggered by transposable elements. Proc Natl Acad Sci U S A 109: 14104–14109. doi: 10.1073/pnas.1207036109 22891327

55. Sienski G, Donertas D, Brennecke J (2012) Transcriptional silencing of transposons by Piwi and maelstrom and its impact on chromatin state and gene expression. Cell 151: 964–980. doi: 10.1016/j.cell.2012.10.040 23159368

56. Olovnikov I, Ryazansky S, Shpiz S, Lavrov S, Abramov Y, et al. (2013) De novo piRNA cluster formation in the Drosophila germ line triggered by transgenes containing a transcribed transposon fragment. Nucleic Acids Res 41: 5757–5768. doi: 10.1093/nar/gkt310 23620285

57. Shpiz S, Ryazansky S, Olovnikov I, Abramov Y, Kalmykova A (2014) Euchromatic transposon insertions trigger production of novel Pi- and endo-siRNAs at the target sites in the drosophila germline. PLoS Genet 10: e1004138. doi: 10.1371/journal.pgen.1004138 24516406

58. Czech B, Preall JB, McGinn J, Hannon GJ (2013) A transcriptome-wide RNAi screen in the Drosophila ovary reveals factors of the germline piRNA pathway. Mol Cell 50: 749–761. doi: 10.1016/j.molcel.2013.04.007 23665227

59. Ronsseray S, Josse T, Boivin A, Anxolabehere D (2003) Telomeric transgenes and trans-silencing in Drosophila. Genetica 117: 327–335. 12723712

60. Ronsseray S, Marin L, Lehmann M, Anxolabehere D (1998) Repression of hybrid dysgenesis in Drosophila melanogaster by combinations of telomeric P-element reporters and naturally occurring P elements. Genetics 149: 1857–1866. 9691042

61. Marin L, Lehmann M, Nouaud D, Izaabel H, Anxolabehere D, et al. (2000) P-element repression in Drosophila melanogaster by a naturally occurring defective telomeric P copy. Genetics 155: 1841–1854. 10924479

62. Simmons MJ, Ragatz LM, Sinclair IR, Thorp MW, Buschette JT, et al. (2012) Maternal enhancement of cytotype regulation in Drosophila melanogaster by genetic interactions between telomeric P elements and non-telomeric transgenic P elements. Genet Res (Camb) 94: 339–351.

63. Niemi JB, Raymond JD, Patrek R, Simmons MJ (2004) Establishment and maintenance of the P cytotype associated with telomeric P elements in Drosophila melanogaster. Genetics 166: 255–264. 15020423

64. Rozhkov NV, Aravin AA, Zelentsova ES, Schostak NG, Sachidanandam R, et al. (2010) Small RNA-based silencing strategies for transposons in the process of invading Drosophila species. RNA 16: 1634–1645. doi: 10.1261/rna.2217810 20581131

65. Le Thomas A, Stuwe E, Li S, Du J, Marinov G, et al. (2014) Transgenerationally inherited piRNAs trigger piRNA biogenesis by changing the chromatin of piRNA clusters and inducing precursor processing. Genes Dev 28: 1667–1680. doi: 10.1101/gad.245514.114 25085419

66. de Vanssay A, Bouge AL, Boivin A, Hermant C, Teysset L, et al. (2012) Paramutation in Drosophila linked to emergence of a piRNA-producing locus. Nature 490: 112–115. doi: 10.1038/nature11416 22922650

67. Le Thomas A, Marinov GK, Aravin AA (2014) A transgenerational process defines piRNA biogenesis in Drosophila virilis. Cell Rep 8: 1617–1623. doi: 10.1016/j.celrep.2014.08.013 25199836

68. Obbard DJ, Gordon KHJ, Buck AH, Jiggins FM (2009) The evolution of RNAi as a defence against viruses and transposable elements. Philosophical Transactions of the Royal Society B-Biological Sciences 364: 99–115.

69. Kolaczkowski B, Hupalo DN, Kern AD (2010) Recurrent Adaptation in RNA Interference Genes Across the Drosophila Phylogeny. Molecular Biology and Evolution 28: 1033–1042. doi: 10.1093/molbev/msq284 20971974

70. Simkin A, Wong A, Poh YP, Theurkauf WE, Jensen JD (2013) Recurrent and recent selective sweeps in the piRNA pathway. Evolution 67: 1081–1090. doi: 10.1111/evo.12011 23550757

71. Zhang F, Wang J, Xu J, Zhang Z, Koppetsch BS, et al. (2012) UAP56 couples piRNA clusters to the perinuclear transposon silencing machinery. Cell 151: 871–884. doi: 10.1016/j.cell.2012.09.040 23141543

72. Arteaga-Vazquez M, Sidorenko L, Rabanal FA, Shrivistava R, Nobuta K, et al. (2010) RNA-mediated trans-communication can establish paramutation at the b1 locus in maize. Proc Natl Acad Sci U S A 107: 12986–12991. doi: 10.1073/pnas.1007972107 20616013

73. Alleman M, Sidorenko L, McGinnis K, Seshadri V, Dorweiler JE, et al. (2006) An RNA-dependent RNA polymerase is required for paramutation in maize. Nature 442: 295–298. 16855589

74. Chandler VL (2007) Paramutation: from maize to mice. Cell 128: 641–645. 17320501

75. Mott R, Yuan W, Kaisaki P, Gan X, Cleak J, et al. (2014) The architecture of parent-of-origin effects in mice. Cell 156: 332–342. doi: 10.1016/j.cell.2013.11.043 24439386

76. Gibson G, Riley-Berger R, Harshman L, Kopp A, Vacha S, et al. (2004) Extensive sex-specific nonadditivity of gene expression in Drosophila melanogaster. Genetics 167: 1791–1799. 15342517

77. Wittkopp PJ, Haerum BK, Clark AG (2006) Parent-of-origin effects on mRNA expression in Drosophila melanogaster not caused by genomic imprinting. Genetics 173: 1817–1821. 16702434

78. Bergman CM, Quesneville H, Anxolabehere D, Ashburner M (2006) Recurrent insertion and duplication generate networks of transposable element sequences in the Drosophila melanogaster genome. Genome Biol 7: R112. 17134480

79. Malone CD, Brennecke J, Dus M, Stark A, McCombie WR, et al. (2009) Specialized piRNA Pathways Act in Germline and Somatic Tissues of the Drosophila Ovary. Cell 137: 522–535. doi: 10.1016/j.cell.2009.03.040 19395010

80. Komili S, Farny NG, Roth FP, Silver PA (2007) Functional specificity among ribosomal proteins regulates gene expression. Cell 131: 557–571. 17981122

81. Vastenhouw NL, Fischer SE, Robert VJ, Thijssen KL, Fraser AG, et al. (2003) A genome-wide screen identifies 27 genes involved in transposon silencing in C. elegans. Curr Biol 13: 1311–1316. 12906791

82. Zhang Y, Lu H (2009) Signaling to p53: ribosomal proteins find their way. Cancer Cell 16: 369–377. doi: 10.1016/j.ccr.2009.09.024 19878869

83. Smith CD, Edgar RC, Yandell MD, Smith DR, Celniker SE, et al. (2007) Improved repeat identification and masking in Dipterans. Gene 389: 1–9. 17137733

84. Li R, Ye J, Li S, Wang J, Han Y, et al. (2005) ReAS: Recovery of ancestral sequences for transposable elements from the unassembled reads of a whole genome shotgun. PLoS Comput Biol 1: e43. 16184192

85. Clark AG, Eisen MB, Smith DR, Bergman CM, Oliver B, et al. (2007) Evolution of genes and genomes on the Drosophila phylogeny. Nature 450: 203–218. 17994087

86. Bosco G, Campbell P, Leiva-Neto JT, Markow TA (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. 18039867

87. Blumenstiel JP, Noll AC, Griffiths JA, Perera AG, Walton KN, et al. (2009) Identification of EMS-Induced Mutations in Drosophila melanogaster by Whole-Genome Sequencing. Genetics 182: 25–32. doi: 10.1534/genetics.109.101998 19307605

88. LI H (2013) Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXivorg arXiv:1303.3997v2.

89. Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15: 550. 25516281

90. Vigneault F, Ter-Ovanesyan D, Alon S, Eminaga S, D CC, et al. (2012) High-throughput multiplex sequencing of miRNA. Curr Protoc Hum Genet Chapter 11: Unit 11 12 11–10.

91. Li CJ, Vagin VV, Lee SH, Xu J, Ma SM, et al. (2009) Collapse of Germline piRNAs in the Absence of Argonaute3 Reveals Somatic piRNAs in Flies. Cell 137: 509–521. doi: 10.1016/j.cell.2009.04.027 19395009

92. Li H, Durbin R (2010) Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics 26: 589–595. doi: 10.1093/bioinformatics/btp698 20080505

93. Quinlan AR, Hall IM BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26: 841–842. doi: 10.1093/bioinformatics/btq033 20110278

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2015 Číslo 8
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#