Role of transposable elements in heterochromatin and epigenetic control (original) (raw)

• Letter
• Published: 22 July 2004
• Anne-Valérie Gendrel2 na1,
• Michael Black3 nAff6,
• Matthew W. Vaughn1,
• Neilay Dedhia1,
• W. Richard McCombie1,
• Kimberly Lavine1,
• Vivek Mittal1,
• Bruce May1,
• Kristin D. Kasschau4,
• James C. Carrington4,
• Rebecca W. Doerge3,
• Vincent Colot2 &
• …
• Rob Martienssen1

Nature volume 430, pages 471–476 (2004)Cite this article

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Abstract

Heterochromatin has been defined as deeply staining chromosomal material that remains condensed in interphase, whereas euchromatin undergoes de-condensation1. Heterochromatin is found near centromeres and telomeres, but interstitial sites of heterochromatin (knobs) are common in plant genomes and were first described in maize2. These regions are repetitive and late-replicating3. In Drosophila, heterochromatin influences gene expression, a heterochromatin phenomenon called position effect variegation4. Similarities between position effect variegation in Drosophila and gene silencing in maize mediated by “controlling elements” (that is, transposable elements) led in part to the proposal that heterochromatin is composed of transposable elements, and that such elements scattered throughout the genome might regulate development2. Using microarray analysis, we show that heterochromatin in Arabidopsis is determined by transposable elements and related tandem repeats, under the control of the chromatin remodelling ATPase DDM1 (Decrease in DNA Methylation 1). Small interfering RNAs (siRNAs) correspond to these sequences, suggesting a role in guiding DDM1. We also show that transposable elements can regulate genes epigenetically, but only when inserted within or very close to them. This probably accounts for the regulation by DDM1 and the DNA methyltransferase MET1 of the euchromatic, imprinted gene FWA, as its promoter is provided by transposable-element-derived tandem repeats that are associated with siRNAs.

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Acknowledgements

We thank E. Richards and our colleagues T. Osborn, L. Comai, J. Chen and J. Birchler for their comments and advice. We also thank P. Rabinowicz for advice on ChIP microarray experiments. V.C. thanks M. Caboche for laboratory space and continuous support. Z.L. is an Arnold and Mabel Beckman graduate fellow in the Watson School of Biological Sciences. A.V.G. is supported by a graduate studentship from the French Ministry of Research. M.V. is a National Science Foundation Bioinformatics postdoctoral fellow. This work was supported by a grant from the NSF Plant Genome Program (to R.W.D. and R.M.), as well as grants from Genopole and the CNRS (to V.C.), grants from NSF and NIH to J. C., and NIH to R.M.

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Author notes

1. Michael Black
   Present address: Department of Statistics, The University of Auckland, Private Bag 92019, Auckland, New Zealand
2. Zachary Lippman and Anne-Valérie Gendrel: These authors contributed equally to this work

Authors and Affiliations

1. Watson School of Biological Sciences and Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, 11724, USA
   Zachary Lippman, Matthew W. Vaughn, Neilay Dedhia, W. Richard McCombie, Kimberly Lavine, Vivek Mittal, Bruce May & Rob Martienssen
2. Unité de Recherche en Génomique Végétale (URGV), INRA/CNRS/UEVE, 2 Rue Gaston Crémieux, 91057, Evry Cedex, France
   Anne-Valérie Gendrel & Vincent Colot
3. Department of Statistics, Purdue University, West Lafayette, Indiana, 47907, USA
   Michael Black & Rebecca W. Doerge
4. Center for Gene Research and Biotechnology, Oregon State University, Corvallis, Oregon, 97330, USA
   Kristin D. Kasschau & James C. Carrington

Authors

1. Zachary Lippman
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2. Anne-Valérie Gendrel
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3. Michael Black
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4. Matthew W. Vaughn
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5. Neilay Dedhia
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6. W. Richard McCombie
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9. Bruce May
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10. Kristin D. Kasschau
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12. Rebecca W. Doerge
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13. Vincent Colot
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Corresponding authors

Correspondence toVincent Colot or Rob Martienssen.

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Competing interests

R. Martienssen and W. R. McCombie have financial interests in Orion Genomics LLC, a biotechnology company that has commercialized the DNA methylation profiling method under the trademark MethylScope.

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Lippman, Z., Gendrel, AV., Black, M. et al. Role of transposable elements in heterochromatin and epigenetic control.Nature 430, 471–476 (2004). https://doi.org/10.1038/nature02651

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• Received: 02 January 2004
• Accepted: 07 May 2004
• Issue Date: 22 July 2004
• DOI: https://doi.org/10.1038/nature02651

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