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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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.
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, A., 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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