Moving targets: Mechanisms regulating siRNA production and DNA methylation during plant development - PubMed (original) (raw)
Review
Moving targets: Mechanisms regulating siRNA production and DNA methylation during plant development
Laura M Martins et al. Curr Opin Plant Biol. 2023 Oct.
Abstract
DNA methylation is a conserved modification that must be precisely regulated during development to facilitate its roles in silencing transposable elements and regulating gene expression. In plants, DNA methylation changes during reproduction are widely documented and, in many cases, the underlying mechanisms are well understood. In somatic tissues, the diversity of methylation patterns are only recently emerging but they are often associated with the RNA-directed DNA methylation (RdDM) pathway. Here, we discuss advances in our understanding of how the locus-specific targeting and tissue-specific expression of RdDM proteins regulate methylation patterns, how the targeting of methylation at loci with imperfect homology expands the purview of RdDM, and how natural variation within RdDM factors impacts DNA methylation patterns.
Copyright © 2023 Elsevier Ltd. All rights reserved.
Conflict of interest statement
Declaration of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Figures
Figure 1.
Detailed view of the canonical RdDM pathway, which utilizes two different types of non-coding RNAs to target DNA methylation and silence genes and transposons. Briefly, RdDM is initiated by the Pol-IV polymerase, which interacts with, and is targeted to chromatin by, a number of proteins, including SHH1, all four CLSYs, and ZMP. Pol-IV transcripts are processed co-transcriptionally by RDR2 to generate short double-stranded RNAs (dsRNAs). These RNAs are chopped by DCL3 into 24nt siRNAs, which are loaded into various AGO effector complexes. Pol-V, which is targeted by the DDR complex and two SUVH proteins, generates long non-coding RNAs. AGO effector complexes are recruited to RdDM loci via interactions with the WG/GW motifs present in Pol-V and SPT5L and interactions with the nascent Pol-V transcript. Sliced Pol-V transcripts bound by AGO4 are proposed to promote the association with DRM2 to enable efficient deposition of DNA methylation. Non-canonical RdDM pathways, which generate siRNAs in a Pol-IV independent manner, are reviewed in[43]. The red dots and green octagons represent DNA and histone methylation, respectively.
Figure 2.
Locus- and tissue-specificity of Pol-IV targeting factors. (A) Scaled Venn diagrams adapted from[20] showing the overlaps of reduced siRNA clusters in the indicated genotypes and tissues. Overlaps in ovules are shown on a 3x scale. (B) Cartoon depicting the genomic distributions of loci regulated by the CLSYs and ZMP in flowers, where arrow thicknesses correspond to the relative numbers of siRNA clusters regulated by these factors. An inlay showing two alternative models for the hypermethylation phenotypes observed in clsy mutants, using clsy4 as an example: (Left) Redistribution of Pol-IV in the absence of CLSY4 vs (Right) Direct role for CLSY4 in targeting the DNA demethylase, ROS1.
Figure 3.
Mechanisms employed by Pol-IV targeting factors to generate epigenetic diversity within and between tissues. (A-B) Cartoons depicting the targeting mechanisms employed by CLSY1 and CLSY2 (A), or CLSY3 and CLSY4 (B), in the indicated tissues. In B, the targeting mechanism(s) in several tissues remain open questions (?). (C and D) CLSY expression levels [log2 (fpkm+1)] and genomic distributions (Chr 1) of reduced siRNA clusters in clsy1,2 (C) or clsy3,4 (D) mutants in the indicated tissues[20]. In D, the distributions of siren loci in ovules and HyperTEs in tapetum cells, as well as the overlaps of these loci, are also included. (E) Cartoons portraying the ability of siRNAs from siren loci to target methylation at genes with imperfect homology in ovule cells (Upper) and the ability of siRNAs from HyperTE loci to move from tapetum cells into neighboring meiocytes to target genes with imperfect homology (Lower). In the former, what blocks Pol-IV from generating perfectly matching siRNAs at the targeted genes remains an open question (?) and in the latter, what blocks the targeting of methylation at imperfectly matching targets in tapetum cells remains an open question (?). The background colors in A, B and E correspond to the Pol-IV targeting factors being discussed.
Figure 4.
Examples of genes mis-regulated in RdDM mutants. Cartoons showing the locus-specific misregulation of the indicated genes in RdDM mutants along with their phenotypic consequences. For zmp, the target gene and mechanism of gene silencing remain to be determined as indicated by question marks (?). Root images were adapted from[40].
References
- Matzke MA, Mosher RA: RNA-directed DNA methylation: an epigenetic pathway of increasing complexity. Nature reviews. Genetics 2014, 15:394–408. -PubMed
- Zhang H, Gong Z, Zhu JK: Active DNA demethylation in plants: 20 years of discovery and beyond. J Integr Plant Biol 2022, 64:2217–2239. -PubMed
- Kawashima T, Berger F: Epigenetic reprogramming in plant sexual reproduction. Nat Rev Genet 2014, 15:613–624. -PubMed