Abstract
Transposable elements can invade virgin genomes within a few generations, after which the elements are 'tamed' and retain only limited transpositional activity. Introduction of the I element, a transposon similar to mammalian LINE elements, into Drosophila melanogaster genomes devoid of such elements initially results in high-frequency transposition of the incoming transposon, high mutation rate, chromosomal nondisjunction and female sterility, a syndrome referred to as hybrid dysgenesis1 (for review, see refs 2, 3, 4); a related syndrome has also been described in mammals5. High-frequency transposition is transient, as the number of I elements reaches a finite value and transposition ceases after approximately ten generations6,7. It has been proposed that the I elements encode a factor that negatively regulates their own transcription, but evidence for such a mechanism is lacking8. Using the hybrid dysgenesis syndrome in Drosophila 1,2,3,4 as a model, we show here that transpositional activity of the I element can be repressed by prior introduction of transgenes expressing a small internal region of the I element. This autoregulation presents features characteristic of homology-dependent gene silencing, a process known as cosuppression9,10,11,12,13,14,15. Repression does not require any translatable sequence, its severity correlates with transgene copy number and it develops in a generation-dependent manner via germline transmission of a silencing effector in females only. These results demonstrate that transposable elements are prone to and can be tamed by homology-dependent gene silencing, a process that may have emerged during the course of evolution as a specific defense mechanism against these elements.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$209.00 per year
only $17.42 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Picard, G. & L'Héritier, P. A maternally inherited factor inducing sterility in D. melanogaster. Drosophila Information Service. 46, 54 54 (1971).
Bregliano, J.C. et al. Hybrid dysgenesis in Drosophila melanogaster. Science 207, 606–611 ( 1980).
Finnegan, D.J. The I factor and I–R hybrid dysgenesis in Drosophila melanogaster . in Mobile DNA (eds Berg, D.E. & Howe, M.M.) 503 –517 (American Society for Microbiology, Washington D.C., 1989).
Bucheton, A. I transposable elements and I–R hybrid dysgenesis in Drosophila. Trends Genet. 6, 16–21 (1990).
Waugh O'Neill, R.J., O'Neill, M.J. & Marshall Graves, J.A. Undermethylation associated with retroelement activation and chromosome remodelling in an interspecific mammalian hybrid. Nature 393, 68–72 ( 1998).
Pélisson, A. & Bregliano, J.C. Evidence for rapid limitation of the I element copy number in a genome submitted to several generations of I–R hybrid dysgenesis in Drosophila melanogaster. Mol. Gen. Genet. 207, 306– 313 (1987).
Pritchard, M.A., Dura, J.M., Pélisson, A. & Finnegan, D.J. A cloned I–factor is fully functional in Drosophila melanogaster . Mol. Gen. Genet. 214, 533– 540 (1988).
Dawson, A., Hartswood, E., Paterson, T. & Finnegan, D.J. A LINE–like transposable element in Drosophila, the I factor, encodes a protein with properties similar to those of retroviral nucleocapsids. EMBO J. 16, 4448–4455 (1997).
Matzke, M.A. & Matzke, A.J.M. How and why do plants inactivate homologous (trans)genes? Plant Physiol. 107, 679–685 (1995).
Jorgensen, R.A. Cosuppression, flower color patterns, and metastable gene expression states. Science 268, 686–691 (1995).
Vaucheret, H., Palauqui, J.–C., Elmayan, T. & Moffatt, B. Molecular and genetic analysis of nitrite reductase co–suppression in transgenic tobacco plants. Mol. Gen. Genet. 248, 311–317 (1995).
Baulcombe, D.C. RNA as a target and an initiator of post–transcriptional gene silencing in transgenic plants. Plant Mol. Biol. 32, 79–88 (1996).
Meyer, P. & Saedler, H. Homology–dependant gene silencing in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47, 23–48 (1996).
Depicker, A. & Van Montagu, M. Post–transcriptional gene silencing in plants. Curr. Opin. Cell Biol. 9, 373–382 (1997).
Metzlaff, M., O'Dell, M., Cluster, P.D. & Flavell, R.B. RNA–mediated RNA degradation and chalcone synthase A silencing in Petunia. Cell 88, 845–854 (1997).
Dorer, D.R. & Henikoff, S. Expansions of transgene repeats cause heterochromatin formation and gene silencing in Drosophila. Cell 77, 993–1002 ( 1994).
Goodwin, J. et al. Genetic and biochemical dissection of transgenic RNA–mediated virus resistance. Plant Cell 8, 95– 105 (1996).
Bingham, P.M. Cosuppression comes to the animals. Cell 90, 385–387 (1997).
Rossignol, J.–L. & Faugeron, G. Gene inactivation triggered by recognition between DNA repeats. Experientia 50, 307–317 (1994).
Pal–Bhadra, M., Bhadra, U. & Birchler, J.A. Cosuppression in Drosophila: gene silencing of Alcohol dehydrogenase by white–Adh transgenes is Polycomb dependent. Cell 90, 479– 490 (1997).
Jensen, S., Cavarec, L., Gassama, M.P. & Heidmann, T. Defective I elements introduced into Drosophila as transgenes can regulate reactivity and prevent I–R hybrid dysgenesis. Mol. Gen. Genet. 248, 381–390 ( 1995).
English, J.J., Mueller, E. & Baulcombe, D.C. Suppression of virus accumulation in transgenic plants exhibiting silencing of nuclear genes. Plant Cell 8 , 179–188 (1996).
Ratcliff, F., Harrison, B.D. & Baulcombe, D.C. A similarity between viral defense and gene silencing in plants. Science 276, 1558– 1560 (1997).
Assaad, F.F., Tucker, K.L. & Signer, E.R. Epigenetic repeat–induced gene silencing (RIGS) in Arabidopsis. Plant Mol. Biol. 22, 1067–1085 (1993).
Garrick, D., Fiering, S., Martin, D.I.K. & Whitelaw, E. Repeat–induced gene silencing in mammals. Nature Genet. 18, 56–59 (1998).
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. USA 95, 11781– 11785 (1998).
Montgomery, M.K. & Fire, A. Double–stranded RNA as a mediator in sequence–specific genetic silencing and co–suppression. Trends Genet. 14, 255– 258 (1998).
Wassenegger, M., Heimes, S., Riedel, L. & Sänger, H.L. RNA–directed de novo methylation of genomic sequences in plants. Cell 76, 567–576 (1994).
Fawcett, D.H., Lister, C.K., Kellet, E. & Finnegan, D.J. Transposable elements controlling I–R hybrid dysgenesis in D. melanogaster are similar to mammalian LINEs. Cell 47, 1007–1015 (1986).
Jensen, S., Cavarec, L., Dhellin, O. & Heidmann, T. Retrotransposition of a marked Drosophila LINE–like I element in cells in culture. Nucleic Acids Res. 22, 1484– 1488 (1994).
Acknowledgements
We especially thank M. Bartozzi for invaluable technical assistance and M. Ashburner, C. Lavialle and L. Cavarec for critical reading of the manuscript and helpful discussions.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Jensen, S., Gassama, MP. & Heidmann, T. Taming of transposable elements by homology-dependent gene silencing . Nat Genet 21, 209–212 (1999). https://doi.org/10.1038/5997
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1038/5997
This article is cited by
-
Small RNAs, DNA methylation and transposable elements in wheat
BMC Genomics (2010)
-
A synthetic biology approach allows inducible retrotransposition in whole plants
Systems and Synthetic Biology (2010)
-
Molecular characterization of a rice mutator-phenotype derived from an incompatible cross-pollination reveals transgenerational mobilization of multiple transposable elements and extensive epigenetic instability
BMC Plant Biology (2009)
-
Endogenous Retroviruses: Thierry Heidmann wins the 2009 Retrovirologyprize
Retrovirology (2009)
-
Endo-siRNAs depend on a new isoform of loquacious and target artificially introduced, high-copy sequences
The EMBO Journal (2009)