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Mobile small RNAs regulate genome-wide DNA methylation

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posted on 2023-02-16, 22:59 authored by Mathew LewseyMathew Lewsey, TJ Hardcastle, CW Melnyk, A Molnar, A Valli, MA Urich, JR Nery, DC Baulcombe, JR Ecker
RNA silencing at the transcriptional and posttranscriptional levels regulates endogenous gene expression, controls invading transposable elements (TEs), and protects the cell against viruses. Key components of the mechanism are small RNAs (sRNAs) of 21-24 nt that guide the silencing machinery to their nucleic acid targets in a nucleotide sequence-specific manner. Transcriptional gene silencing is associated with 24-nt sRNAs and RNA-directed DNA methylation (RdDM) at cytosine residues in three DNA sequence contexts (CG, CHG, and CHH). We previously demonstrated that 24-nt sRNAs are mobile from shoot to root in Arabidopsis thaliana and confirmed that they mediate DNA methylation at three sites in recipient cells. In this study, we extend this finding by demonstrating that RdDM of thousands of loci in root tissues is dependent upon mobile sRNAs from the shoot and that mobile sRNA-dependent DNA methylation occurs predominantly in non-CG contexts. Mobile sRNA-dependent non-CG methylation is largely dependent on the DOMAINS REARRANGED METHYLTRANSFERASES 1/2 (DRM1/DRM2) RdDM pathway but is independent of the CHROMOMETHYLASE (CMT)2/3 DNA methyltransferases. Specific superfamilies of TEs, including those typically found in gene-rich euchromatic regions, lose DNA methylation in a mutant lacking 22-to 24-nt sRNAs (dicer-like 2, 3, 4 triple mutant). Transcriptome analyses identified a small number of genes whose expression in roots is associated with mobile sRNAs and connected to DNA methylation directly or indirectly. Finally, we demonstrate that sRNAs from shoots of one accession move across a graft union and target DNA methylation de novo at normally unmethylated sites in the genomes of root cells from a different accession.

History

Publication Date

2016-02-09

Journal

Proceedings of the National Academy of Sciences of the United States of America

Volume

113

Issue

6

Pagination

10p. (p. E801-E810)

Publisher

National Academy of Sciences

ISSN

0027-8424

Rights Statement

© The Authors 2016. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). You are free to share - copy and redistribute the material in any medium or format; adapt - remix, transform, and build upon the material, under the following terms: Attribution: you must give appropriate credit, provide a link to the license, and indicate if changes were made. You may do so in any reasonable manner, but not in any way that suggests the licensor endorses you or your use. NonCommercial: you may not use the material for commercial purposes. NonDerivative: you may not use the material for derivative or adaptations purposes No additional restrictions — you may not apply legal terms or technological measures that legally restrict others from doing anything the license permits.

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