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Nucleic Acids Research 2005 33(19):6405-6417; doi:10.1093/nar/gki952
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Published online 10 November 2005

© The Author 2005. Published by Oxford University Press. All rights reserved
The online version of this article has been published under an open access model. Users are entitled to use, reproduce, disseminate, or display the open access version of this article for non-commercial purposes provided that: the original authorship is properly and fully attributed; the Journal and Oxford University Press are attributed as the original place of publication with the correct citation details given; if an article is subsequently reproduced or disseminated not in its entirety but only in part or as a derivative work this must be clearly indicated. For commercial re-use, please contact journals.permissions{at}oxfordjournals.org

Article

Silencing of retrotransposons in Dictyostelium by DNA methylation and RNAi

Markus Kuhlmann, Branimira E. Borisova, Markus Kaller, Pontus Larsson1, Dirk Stach2, Jianbo Na3, Ludwig Eichinger3, Frank Lyko2, Victor Ambros4, Fredrik Söderbom5, Christian Hammann and Wolfgang Nellen*

Abt. Genetik, Universität Kassel Heinrich-Plett-Str. 40, 34132 Kassel, Germany 1Department of Cell and Molecular Biology, Biomedical Center, Uppsala University Box 596, S-751 24 Uppsala, Sweden 2Arbeitsgruppe Epigenetik, Deutsches Krebsforschungszentrum Im Neuenheimer Feld 280, 69120 Heidelberg, Germany 3Institut fuer Biochemie I, Medizinische Einrichtungen der Universitaet zu Koeln Joseph-Stelzmann-Str. 52, 50931 Koeln, Germany 4Department of Genetics, Dartmouth Medical School Hanover, NH 03755, USA 5Department of Molecular Biology, Biomedical Center, Swedish University of Agricultural Sciences Box 590, S-75124 Uppsala, Sweden

*To whom correspondence should be addressed. Tel: +49 561 8044805; Fax: +49 561 8044800; Email: nellen{at}uni-kassel.de

Received September 13, 2005. Revised October 8, 2005. Accepted October 18, 2005.

We have identified a DNA methyltransferase of the Dnmt2 family in Dictyostelium that was denominated DnmA. Expression of the dnmA gene is downregulated during the developmental cycle. Overall DNA methylation in Dictyostelium is ~0.2% of the cytosine residues, which indicates its restriction to a limited set of genomic loci. Bisulfite sequencing of specific sites revealed that DnmA is responsible for methylation of mostly asymmetric C-residues in the retrotransposons DIRS-1 and Skipper. Disruption of the gene resulted in a loss of methylation and in increased transcription and mobilization of Skipper. Skipper transcription was also upregulated in strains that had genes encoding components of the RNA interference pathway disrupted. In contrast, DIRS-1 expression was not affected by a loss of DnmA but was strongly increased in strains that had the RNA-directed RNA polymerase gene rrpC disrupted. A large number of siRNAs were found that corresponded to the DIRS-1 sequence, suggesting concerted regulation of DIRS-1 expression by RNAi and DNA modification. No siRNAs corresponding to the standard Skipper element were found. The data show that DNA methylation plays a crucial role in epigenetic gene silencing in Dictyostelium but that different, partially overlapping mechanisms control transposon silencing.

The authors wish it to be known that, in their opinion, the first two authors should be regarded as joint First Authors


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