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A host factor supports retrotransposition of the TRE5-A population in Dictyostelium cells by suppressing an Argonaute protein
BACKGROUND: In the compact and haploid genome of Dictyostelium discoideum control of transposon activity is of particular importance to maintain viability. The non-long terminal repeat retrotransposon TRE5-A amplifies continuously in D. discoideum cells even though it produces considerable amounts o...
Autores principales: | , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
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BioMed Central
2015
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4559204/ https://www.ncbi.nlm.nih.gov/pubmed/26339297 http://dx.doi.org/10.1186/s13100-015-0045-5 |
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author | Schmith, Anika Spaller, Thomas Gaube, Friedemann Fransson, Åsa Boesler, Benjamin Ojha, Sandeep Nellen, Wolfgang Hammann, Christian Söderbom, Fredrik Winckler, Thomas |
author_facet | Schmith, Anika Spaller, Thomas Gaube, Friedemann Fransson, Åsa Boesler, Benjamin Ojha, Sandeep Nellen, Wolfgang Hammann, Christian Söderbom, Fredrik Winckler, Thomas |
author_sort | Schmith, Anika |
collection | PubMed |
description | BACKGROUND: In the compact and haploid genome of Dictyostelium discoideum control of transposon activity is of particular importance to maintain viability. The non-long terminal repeat retrotransposon TRE5-A amplifies continuously in D. discoideum cells even though it produces considerable amounts of minus-strand (antisense) RNA in the presence of an active RNA interference machinery. Removal of the host-encoded C-module-binding factor (CbfA) from D. discoideum cells resulted in a more than 90 % reduction of both plus- and minus-strand RNA of TRE5-A and a strong decrease of the retrotransposition activity of the cellular TRE5-A population. Transcriptome analysis revealed an approximately 230-fold overexpression of the gene coding for the Argonaute-like protein AgnC in a CbfA-depleted mutant. RESULTS: The D. discoideum genome contains orthologs of RNA-dependent RNA polymerases, Dicer-like proteins, and Argonaute proteins that are supposed to represent RNA interference pathways. We analyzed available mutants in these genes for altered expression of TRE5-A. We found that the retrotransposon was overexpressed in mutants lacking the Argonaute proteins AgnC and AgnE. Because the agnC gene is barely expressed in wild-type cells, probably due to repression by CbfA, we employed a new method of promoter-swapping to overexpress agnC in a CbfA-independent manner. In these strains we established an in vivo retrotransposition assay that determines the retrotransposition frequency of the cellular TRE5-A population. We observed that both the TRE5-A steady-state RNA level and retrotransposition rate dropped to less than 10 % of wild-type in the agnC overexpressor strains. CONCLUSIONS: The data suggest that TRE5-A amplification is controlled by a distinct pathway of the Dictyostelium RNA interference machinery that does not require RNA-dependent RNA polymerases but involves AgnC. This control is at least partially overcome by the activity of CbfA, a factor derived from the retrotransposon’s host. This unusual regulation of mobile element activity most likely had a profound effect on genome evolution in D. discoideum. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13100-015-0045-5) contains supplementary material, which is available to authorized users. |
format | Online Article Text |
id | pubmed-4559204 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2015 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-45592042015-09-04 A host factor supports retrotransposition of the TRE5-A population in Dictyostelium cells by suppressing an Argonaute protein Schmith, Anika Spaller, Thomas Gaube, Friedemann Fransson, Åsa Boesler, Benjamin Ojha, Sandeep Nellen, Wolfgang Hammann, Christian Söderbom, Fredrik Winckler, Thomas Mob DNA Research BACKGROUND: In the compact and haploid genome of Dictyostelium discoideum control of transposon activity is of particular importance to maintain viability. The non-long terminal repeat retrotransposon TRE5-A amplifies continuously in D. discoideum cells even though it produces considerable amounts of minus-strand (antisense) RNA in the presence of an active RNA interference machinery. Removal of the host-encoded C-module-binding factor (CbfA) from D. discoideum cells resulted in a more than 90 % reduction of both plus- and minus-strand RNA of TRE5-A and a strong decrease of the retrotransposition activity of the cellular TRE5-A population. Transcriptome analysis revealed an approximately 230-fold overexpression of the gene coding for the Argonaute-like protein AgnC in a CbfA-depleted mutant. RESULTS: The D. discoideum genome contains orthologs of RNA-dependent RNA polymerases, Dicer-like proteins, and Argonaute proteins that are supposed to represent RNA interference pathways. We analyzed available mutants in these genes for altered expression of TRE5-A. We found that the retrotransposon was overexpressed in mutants lacking the Argonaute proteins AgnC and AgnE. Because the agnC gene is barely expressed in wild-type cells, probably due to repression by CbfA, we employed a new method of promoter-swapping to overexpress agnC in a CbfA-independent manner. In these strains we established an in vivo retrotransposition assay that determines the retrotransposition frequency of the cellular TRE5-A population. We observed that both the TRE5-A steady-state RNA level and retrotransposition rate dropped to less than 10 % of wild-type in the agnC overexpressor strains. CONCLUSIONS: The data suggest that TRE5-A amplification is controlled by a distinct pathway of the Dictyostelium RNA interference machinery that does not require RNA-dependent RNA polymerases but involves AgnC. This control is at least partially overcome by the activity of CbfA, a factor derived from the retrotransposon’s host. This unusual regulation of mobile element activity most likely had a profound effect on genome evolution in D. discoideum. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13100-015-0045-5) contains supplementary material, which is available to authorized users. BioMed Central 2015-09-03 /pmc/articles/PMC4559204/ /pubmed/26339297 http://dx.doi.org/10.1186/s13100-015-0045-5 Text en © Schmith et al. 2015 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. |
spellingShingle | Research Schmith, Anika Spaller, Thomas Gaube, Friedemann Fransson, Åsa Boesler, Benjamin Ojha, Sandeep Nellen, Wolfgang Hammann, Christian Söderbom, Fredrik Winckler, Thomas A host factor supports retrotransposition of the TRE5-A population in Dictyostelium cells by suppressing an Argonaute protein |
title | A host factor supports retrotransposition of the TRE5-A population in Dictyostelium cells by suppressing an Argonaute protein |
title_full | A host factor supports retrotransposition of the TRE5-A population in Dictyostelium cells by suppressing an Argonaute protein |
title_fullStr | A host factor supports retrotransposition of the TRE5-A population in Dictyostelium cells by suppressing an Argonaute protein |
title_full_unstemmed | A host factor supports retrotransposition of the TRE5-A population in Dictyostelium cells by suppressing an Argonaute protein |
title_short | A host factor supports retrotransposition of the TRE5-A population in Dictyostelium cells by suppressing an Argonaute protein |
title_sort | host factor supports retrotransposition of the tre5-a population in dictyostelium cells by suppressing an argonaute protein |
topic | Research |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4559204/ https://www.ncbi.nlm.nih.gov/pubmed/26339297 http://dx.doi.org/10.1186/s13100-015-0045-5 |
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