Skip to main content
Genetics logoLink to Genetics
. 2003 Jun;164(2):521–531. doi: 10.1093/genetics/164.2.521

Gene silencing triggered by non-LTR retrotransposons in the female germline of Drosophila melanogaster.

Stéphanie Robin 1, Séverine Chambeyron 1, Alain Bucheton 1, Isabelle Busseau 1
PMCID: PMC1462600  PMID: 12807773

Abstract

Several studies have recently shown that the activity of some eukaryotic transposable elements is sensitive to the presence of homologous transgenes, suggesting the involvement of homology-dependent gene-silencing mechanisms in their regulation. Here we provide data indicating that two non-LTR retrotransposons of Drosophila melanogaster are themselves natural triggers of homology-dependent gene silencing. We show that, in the female germline of D. melanogaster, fragments from the R1 or from the I retrotransposons can mediate silencing of chimeric transcription units into which they are inserted. This silencing is probably mediated by sequence identity with endogenous copies of the retrotransposons because it does not occur with a fragment from the divergent R1 elements of Bombyx mori, and, when a fragment of I is used, it occurs only in females containing functional copies of the I element. This silencing is not accompanied by cosuppression of the endogenous gene homologous to the chimeric transcription unit, which contrasts to some other silencing mechanisms in Drosophila. These observations suggest that in the female germline of D. melanogaster the R1 and I retrotransposons may self-regulate their own activity and their copy number by triggering homology-dependent gene silencing.

Full Text

The Full Text of this article is available as a PDF (277.7 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abad P., Vaury C., Pélisson A., Chaboissier M. C., Busseau I., Bucheton A. A long interspersed repetitive element--the I factor of Drosophila teissieri--is able to transpose in different Drosophila species. Proc Natl Acad Sci U S A. 1989 Nov;86(22):8887–8891. doi: 10.1073/pnas.86.22.8887. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Aravin A. A., Naumova N. M., Tulin A. V., Vagin V. V., Rozovsky Y. M., Gvozdev V. A. Double-stranded RNA-mediated silencing of genomic tandem repeats and transposable elements in the D. melanogaster germline. Curr Biol. 2001 Jul 10;11(13):1017–1027. doi: 10.1016/s0960-9822(01)00299-8. [DOI] [PubMed] [Google Scholar]
  3. Aït-Ahmed O., Bellon B., Capri M., Joblet C., Thomas-Delaage M. The yemanuclein-alpha: a new Drosophila DNA binding protein specific for the oocyte nucleus. Mech Dev. 1992 Mar;37(1-2):69–80. doi: 10.1016/0925-4773(92)90016-d. [DOI] [PubMed] [Google Scholar]
  4. Bingham P. M. Cosuppression comes to the animals. Cell. 1997 Aug 8;90(3):385–387. doi: 10.1016/s0092-8674(00)80496-1. [DOI] [PubMed] [Google Scholar]
  5. Bird Adrian. DNA methylation patterns and epigenetic memory. Genes Dev. 2002 Jan 1;16(1):6–21. doi: 10.1101/gad.947102. [DOI] [PubMed] [Google Scholar]
  6. Blackman R. K., Grimaila R., Koehler M. M., Gelbart W. M. Mobilization of hobo elements residing within the decapentaplegic gene complex: suggestion of a new hybrid dysgenesis system in Drosophila melanogaster. Cell. 1987 May 22;49(4):497–505. doi: 10.1016/0092-8674(87)90452-1. [DOI] [PubMed] [Google Scholar]
  7. Bouhidel K., Terzian C., Pinon H. The full-length transcript of the I factor, a LINE element of Drosophila melanogaster, is a potential bicistronic RNA messenger. Nucleic Acids Res. 1994 Jun 25;22(12):2370–2374. doi: 10.1093/nar/22.12.2370. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bucheton A., Vaury C., Chaboissier M. C., Abad P., Pélisson A., Simonelig M. I elements and the Drosophila genome. Genetica. 1992;86(1-3):175–190. doi: 10.1007/BF00133719. [DOI] [PubMed] [Google Scholar]
  9. Busseau I., Malinsky S., Balakireva M., Chaboissier M. C., Teninges D., Bucheton A. A genetically marked I element in Drosophila melanogaster can be mobilized when ORF2 is provided in trans. Genetics. 1998 Jan;148(1):267–275. doi: 10.1093/genetics/148.1.267. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Capri M., Santoni M. J., Thomas-Delaage M., Aït-Ahmed O. Implication of a 5' coding sequence in targeting maternal mRNA to the Drosophila oocyte. Mech Dev. 1997 Nov;68(1-2):91–100. doi: 10.1016/s0925-4773(97)00130-5. [DOI] [PubMed] [Google Scholar]
  11. Chaboissier M. C., Bucheton A., Finnegan D. J. Copy number control of a transposable element, the I factor, a LINE-like element in Drosophila. Proc Natl Acad Sci U S A. 1998 Sep 29;95(20):11781–11785. doi: 10.1073/pnas.95.20.11781. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Chaboissier M. C., Busseau I., Prosser J., Finnegan D. J., Bucheton A. Identification of a potential RNA intermediate for transposition of the LINE-like element I factor in Drosophila melanogaster. EMBO J. 1990 Nov;9(11):3557–3563. doi: 10.1002/j.1460-2075.1990.tb07566.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Chaboissier M. C., Finnegan D., Bucheton A. Retrotransposition of the I factor, a non-long terminal repeat retrotransposon of Drosophila, generates tandem repeats at the 3' end. Nucleic Acids Res. 2000 Jul 1;28(13):2467–2472. doi: 10.1093/nar/28.13.2467. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Chambeyron Séverine, Brun Christine, Robin Stéphanie, Bucheton Alain, Busseau Isabelle. Chimeric RNA transposition intermediates of the I factor produce precise retrotransposed copies. Nucleic Acids Res. 2002 Aug 1;30(15):3387–3394. doi: 10.1093/nar/gkf456. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Chambeyron Séverine, Bucheton Alain, Busseau Isabelle. Tandem UAA repeats at the 3'-end of the transcript are essential for the precise initiation of reverse transcription of the I factor in Drosophila melanogaster. J Biol Chem. 2002 Mar 6;277(20):17877–17882. doi: 10.1074/jbc.M200996200. [DOI] [PubMed] [Google Scholar]
  16. Dernburg A. F., Zalevsky J., Colaiácovo M. P., Villeneuve A. M. Transgene-mediated cosuppression in the C. elegans germ line. Genes Dev. 2000 Jul 1;14(13):1578–1583. [PMC free article] [PubMed] [Google Scholar]
  17. Feng Q., Moran J. V., Kazazian H. H., Jr, Boeke J. D. Human L1 retrotransposon encodes a conserved endonuclease required for retrotransposition. Cell. 1996 Nov 29;87(5):905–916. doi: 10.1016/s0092-8674(00)81997-2. [DOI] [PubMed] [Google Scholar]
  18. Feng Q., Schumann G., Boeke J. D. Retrotransposon R1Bm endonuclease cleaves the target sequence. Proc Natl Acad Sci U S A. 1998 Mar 3;95(5):2083–2088. doi: 10.1073/pnas.95.5.2083. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Gauthier E., Tatout C., Pinon H. Artificial and epigenetic regulation of the I factor, a nonviral retrotransposon of Drosophila melanogaster. Genetics. 2000 Dec;156(4):1867–1878. doi: 10.1093/genetics/156.4.1867. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Grishok A., Tabara H., Mello C. C. Genetic requirements for inheritance of RNAi in C. elegans. Science. 2000 Mar 31;287(5462):2494–2497. doi: 10.1126/science.287.5462.2494. [DOI] [PubMed] [Google Scholar]
  21. Hirochika H., Okamoto H., Kakutani T. Silencing of retrotransposons in arabidopsis and reactivation by the ddm1 mutation. Plant Cell. 2000 Mar;12(3):357–369. doi: 10.1105/tpc.12.3.357. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Hsieh J., Fire A. Recognition and silencing of repeated DNA. Annu Rev Genet. 2000;34:187–204. doi: 10.1146/annurev.genet.34.1.187. [DOI] [PubMed] [Google Scholar]
  23. Jackson James P., Lindroth Anders M., Cao Xiaofeng, Jacobsen Steven E. Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase. Nature. 2002 Mar 17;416(6880):556–560. doi: 10.1038/nature731. [DOI] [PubMed] [Google Scholar]
  24. Jakubczak J. L., Xiong Y., Eickbush T. H. Type I (R1) and type II (R2) ribosomal DNA insertions of Drosophila melanogaster are retrotransposable elements closely related to those of Bombyx mori. J Mol Biol. 1990 Mar 5;212(1):37–52. doi: 10.1016/0022-2836(90)90303-4. [DOI] [PubMed] [Google Scholar]
  25. Jakubczak J. L., Zenni M. K., Woodruff R. C., Eickbush T. H. Turnover of R1 (type I) and R2 (type II) retrotransposable elements in the ribosomal DNA of Drosophila melanogaster. Genetics. 1992 May;131(1):129–142. doi: 10.1093/genetics/131.1.129. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Jamrich M., Miller O. L., Jr The rare transcripts of interrupted rRNA genes in Drosophila melanogaster are processed or degraded during synthesis. EMBO J. 1984 Jul;3(7):1541–1545. doi: 10.1002/j.1460-2075.1984.tb02008.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Jensen S., Gassama M. P., Heidmann T. Taming of transposable elements by homology-dependent gene silencing. Nat Genet. 1999 Feb;21(2):209–212. doi: 10.1038/5997. [DOI] [PubMed] [Google Scholar]
  28. Jensen Silke, Gassama Marie-Pierre, Dramard Xavier, Heidmann Thierry. Regulation of I-transposon activity in Drosophila: evidence for cosuppression of nonhomologous transgenes and possible role of ancestral I-related pericentromeric elements. Genetics. 2002 Nov;162(3):1197–1209. doi: 10.1093/genetics/162.3.1197. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Ketting R. F., Haverkamp T. H., van Luenen H. G., Plasterk R. H. Mut-7 of C. elegans, required for transposon silencing and RNA interference, is a homolog of Werner syndrome helicase and RNaseD. Cell. 1999 Oct 15;99(2):133–141. doi: 10.1016/s0092-8674(00)81645-1. [DOI] [PubMed] [Google Scholar]
  30. Ketting R. F., Plasterk R. H. A genetic link between co-suppression and RNA interference in C. elegans. Nature. 2000 Mar 16;404(6775):296–298. doi: 10.1038/35005113. [DOI] [PubMed] [Google Scholar]
  31. Lindroth A. M., Cao X., Jackson J. P., Zilberman D., McCallum C. M., Henikoff S., Jacobsen S. E. Requirement of CHROMOMETHYLASE3 for maintenance of CpXpG methylation. Science. 2001 May 10;292(5524):2077–2080. doi: 10.1126/science.1059745. [DOI] [PubMed] [Google Scholar]
  32. Long E. O., Collins M., Kiefer B. I., Dawid I. B. Expression of the ribosomal DNA insertions in bobbed mutants of Drosophila melanogaster. Mol Gen Genet. 1981;182(3):377–384. doi: 10.1007/BF00293925. [DOI] [PubMed] [Google Scholar]
  33. Malinsky S., Bucheton A., Busseau I. New insights on homology-dependent silencing of I factor activity by transgenes containing ORF1 in Drosophila melanogaster. Genetics. 2000 Nov;156(3):1147–1155. doi: 10.1093/genetics/156.3.1147. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Marin L., Lehmann M., Nouaud D., Izaabel H., Anxolabéhère D., Ronsseray S. P-Element repression in Drosophila melanogaster by a naturally occurring defective telomeric P copy. Genetics. 2000 Aug;155(4):1841–1854. doi: 10.1093/genetics/155.4.1841. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Martín F., Olivares M., López M. C., Alonso C. Do non-long terminal repeat retrotransposons have nuclease activity? Trends Biochem Sci. 1996 Aug;21(8):283–285. [PubMed] [Google Scholar]
  36. Pal-Bhadra M., Bhadra U., Birchler J. A. Cosuppression in Drosophila: gene silencing of Alcohol dehydrogenase by white-Adh transgenes is Polycomb dependent. Cell. 1997 Aug 8;90(3):479–490. doi: 10.1016/s0092-8674(00)80508-5. [DOI] [PubMed] [Google Scholar]
  37. Pal-Bhadra M., Bhadra U., Birchler J. A. Cosuppression of nonhomologous transgenes in Drosophila involves mutually related endogenous sequences. Cell. 1999 Oct 1;99(1):35–46. doi: 10.1016/s0092-8674(00)80060-4. [DOI] [PubMed] [Google Scholar]
  38. Pal-Bhadra Manika, Bhadra Utpal, Birchler James A. RNAi related mechanisms affect both transcriptional and posttranscriptional transgene silencing in Drosophila. Mol Cell. 2002 Feb;9(2):315–327. doi: 10.1016/s1097-2765(02)00440-9. [DOI] [PubMed] [Google Scholar]
  39. Pritchard M. A., Dura J. M., Pélisson A., Bucheton A., Finnegan D. J. A cloned I-factor is fully functional in Drosophila melanogaster. Mol Gen Genet. 1988 Nov;214(3):533–540. doi: 10.1007/BF00330491. [DOI] [PubMed] [Google Scholar]
  40. Pritchard M. A., Dura J. M., Pélisson A., Bucheton A., Finnegan D. J. A cloned I-factor is fully functional in Drosophila melanogaster. Mol Gen Genet. 1988 Nov;214(3):533–540. doi: 10.1007/BF00330491. [DOI] [PubMed] [Google Scholar]
  41. Pérez-González César E., Eickbush Thomas H. Rates of R1 and R2 retrotransposition and elimination from the rDNA locus of Drosophila melanogaster. Genetics. 2002 Oct;162(2):799–811. doi: 10.1093/genetics/162.2.799. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Ronsseray S., Boivin A., Anxolabéhère D. P-Element repression in Drosophila melanogaster by variegating clusters of P-lacZ-white transgenes. Genetics. 2001 Dec;159(4):1631–1642. doi: 10.1093/genetics/159.4.1631. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Spradling A. C., Rubin G. M. Transposition of cloned P elements into Drosophila germ line chromosomes. Science. 1982 Oct 22;218(4570):341–347. doi: 10.1126/science.6289435. [DOI] [PubMed] [Google Scholar]
  44. Stapleton W., Das S., McKee B. D. A role of the Drosophila homeless gene in repression of Stellate in male meiosis. Chromosoma. 2001 Jul;110(3):228–240. doi: 10.1007/s004120100136. [DOI] [PubMed] [Google Scholar]
  45. Tabara H., Sarkissian M., Kelly W. G., Fleenor J., Grishok A., Timmons L., Fire A., Mello C. C. The rde-1 gene, RNA interference, and transposon silencing in C. elegans. Cell. 1999 Oct 15;99(2):123–132. doi: 10.1016/s0092-8674(00)81644-x. [DOI] [PubMed] [Google Scholar]
  46. Tijsterman Marcel, Okihara Kristy L., Thijssen Karen, Plasterk Ronald H. A. PPW-1, a PAZ/PIWI protein required for efficient germline RNAi, is defective in a natural isolate of C. elegans. Curr Biol. 2002 Sep 3;12(17):1535–1540. doi: 10.1016/s0960-9822(02)01110-7. [DOI] [PubMed] [Google Scholar]
  47. Tompa Rachel, McCallum Claire M., Delrow Jeffrey, Henikoff Jorja G., van Steensel Bas, Henikoff Steven. Genome-wide profiling of DNA methylation reveals transposon targets of CHROMOMETHYLASE3. Curr Biol. 2002 Jan 8;12(1):65–68. doi: 10.1016/s0960-9822(01)00622-4. [DOI] [PubMed] [Google Scholar]
  48. Vaury C., Pélisson A., Abad P., Bucheton A. Properties of transgenic strains of Drosophila melanogaster containing I transposable elements from Drosophila teissieri. Genet Res. 1993 Apr;61(2):81–90. doi: 10.1017/s0016672300031177. [DOI] [PubMed] [Google Scholar]
  49. Yoder J. A., Walsh C. P., Bestor T. H. Cytosine methylation and the ecology of intragenomic parasites. Trends Genet. 1997 Aug;13(8):335–340. doi: 10.1016/s0168-9525(97)01181-5. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES