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Taming of transposable elements by homology-dependent gene silencing

Nature Genetics volume 21, pages 209–212 (1999)Cite this article

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.

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Figure 1: Constructs and rationale of the assay for measurement of the level of I-element activity in transgenic strains.
Figure 2: Regulation of I-element activity by transgenic strains is transgene copy-number dependent.
Figure 3: Kinetics of the repression process in different hsp[i2Δ]pA and hsp[i2Δ*]pA transgenic strains.
Figure 4: The repressed phenotype is maternally transmitted.
Figure 5: Regulation of I-element activity is not dependent on specific I sequences within the transgenes, but requires their transcription.

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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.

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  1. Unité des Rétrovirus Endogènes et Eléments Rétroïdes des Eucaryotes Supérieurs, CNRS UMR 1573, Institut Gustave Roussy, 39 rue Camille Desmoulins , Villejuif Cedex, 94805, France

    Silke Jensen, Marie-Pierre Gassama & Thierry Heidmann

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  1. Silke Jensen
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Correspondence to Thierry Heidmann.

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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

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