Chromatin regulates expression of small RNAs to help maintain transposon methylome homeostasis in Arabidopsis
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RESEARCH
Open Access
Chromatin regulates expression of small RNAs to help maintain transposon methylome homeostasis in Arabidopsis Ranjith K. Papareddy, Katalin Páldi†, Subramanian Paulraj†, Ping Kao, Stefan Lutzmayer and Michael D. Nodine* * Correspondence: michael.nodine@ gmi.oeaw.ac.at † Katalin Páldi and Subramanian Paulraj contributed equally to this work. Gregor Mendel Institute (GMI), Austrian Academy of Sciences, Vienna Biocenter (VBC), Dr. Bohr-Gasse 3, 1030 Vienna, Austria
Abstract Background: Eukaryotic genomes are partitioned into euchromatic and heterochromatic domains to regulate gene expression and other fundamental cellular processes. However, chromatin is dynamic during growth and development and must be properly re-established after its decondensation. Small interfering RNAs (siRNAs) promote heterochromatin formation, but little is known about how chromatin regulates siRNA expression. Results: We demonstrate that thousands of transposable elements (TEs) produce exceptionally high levels of siRNAs in Arabidopsis thaliana embryos. TEs generate siRNAs throughout embryogenesis according to two distinct patterns depending on whether they are located in euchromatic or heterochromatic regions of the genome. siRNA precursors are transcribed in embryos, and siRNAs are required to direct the re-establishment of DNA methylation on TEs from which they are derived in the new generation. Decondensed chromatin also permits the production of 24-nt siRNAs from heterochromatic TEs during post-embryogenesis, and siRNA production from bipartite-classified TEs is controlled by their chromatin states. Conclusions: Decondensation of heterochromatin in response to developmental, and perhaps environmental, cues promotes the transcription and function of siRNAs in plants. Our results indicate that chromatin-mediated siRNA transcription provides a cell-autonomous homeostatic control mechanism to help reconstitute pre-existing chromatin states during growth and development including those that ensure silencing of TEs in the future germ line. Keywords: Small RNAs, DNA methylation, Chromatin, Epigenetics, Linker histone H1, Plant embryogenesis, RNAi, Transposable elements
Background Eukaryotic genomes are partitioned into euchromatic and heterochromatic domains [1, 2]. Euchromatic regions are enriched for genes and provide a transcriptionally permissive state. Heterochromatic regions are densely packed, or condensed, regions of the genome that are typically transcriptionally quiescent and characterized by highly © The Author(s). 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwis
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