RNA-directed DNA methylation (RdDM) is the major small RNA-mediated epigenetic pathway in plants. RdDM requires a specialized transcriptional machinery that comprises two plant-specific RNA polymerases - Pol IV and Pol V - and a growing number of accessory proteins, the functions of which in the RdDM mechanism are only partially understood. Recent work has revealed variations in the canonical RdDM pathway and identified factors that recruit Pol IV and Pol V to specific target sequences. RdDM, which transcriptionally represses a subset of transposons and genes, is implicated in pathogen defence, stress responses and reproduction, as well as in interallelic and intercellular communication.

RNA-directed DNA methylation: an epigenetic pathway of increasing complexity

DNA methylation is a conserved epigenetic modification that is important for gene regulation and genome stability. Aberrant patterns of DNA methylation can lead to plant developmental abnormalities. A specific DNA methylation state is an outcome of dynamic regulation by de novo methylation, maintenance of methylation and active demethylation, which are catalysed by various enzymes that are targeted by distinct regulatory pathways. In this Review, we discuss DNA methylation in plants, including methylating and demethylating enzymes and regulatory factors, and the coordination of methylation and demethylation activities by a so-called methylstat mechanism; the functions of DNA methylation in regulating transposon silencing, gene expression and chromosome interactions; the roles of DNA methylation in plant development; and the involvement of DNA methylation in plant responses to biotic and abiotic stress conditions.

Dynamics and function of DNA methylation in plants.

Methylation of DNA and of histone 3 at Lys 9 (H3K9) are highly correlated with gene silencing in eukaryotes from fungi to humans. Both of these epigenetic marks need to be established at specific regions of the genome and then maintained at these sites through cell division. Protein structural domains that specifically recognize methylated DNA and methylated histones are key for targeting enzymes that catalyse these marks to appropriate genome sites. Genetic, genomic, structural and biochemical data reveal connections between these two epigenetic marks, and these domains mediate much of the crosstalk.

/pdf/dna-methylation-pathways-and-their-crosstalk-with-histone-4offoscn9k.pdf

DNA methylation pathways and their crosstalk with histone methylation.

RNA-directed DNA methylation (RdDM) is an epigenetic process in plants that involves both short and long noncoding RNAs. The generation of these RNAs and the induction of RdDM rely on complex transcriptional machineries comprising two plant-specific, RNA polymerase II (Pol II)–related RNA polymerases known as Pol IV and Pol V, as well as a host of auxiliary factors that include both novel and refashioned proteins. We present current views on the mechanism of RdDM with a focus on evolutionary innovations that occurred during the transition from a Pol II transcriptional pathway, which produces mRNA precursors and numerous noncoding RNAs, to the Pol IV and Pol V pathways, which are specialized for RdDM and gene silencing. We describe recently recognized deviations from the canonical RdDM pathway, discuss unresolved issues, and speculate on the biological significance of RdDM for flowering plants, which have a highly developed Pol V pathway.

RNA-Directed DNA Methylation: The Evolution of a Complex Epigenetic Pathway in Flowering Plants.

IDN2/RDM12 has been previously identified as a component of the RNA–directed DNA methylation (RdDM) machinery in Arabidopsis thaliana, but how it functions in RdDM remains unknown. By affinity purification of IDN2, we co-purified two IDN2 paralogs IDP1 and IDP2 (IDN2 PARALOG 1 and 2). The coiled-coil domain between the XS and XH domains of IDN2 is essential for IDN2 homodimerization, whereas the IDN2 C-terminal XH domain but not the coiled-coil domain is required for IDN2 interaction with IDP1 and IDP2. By introducing the wild-type IDN2 sequence and its mutated derivatives into the idn2 mutant for complementation testing, we demonstrated that the previously uncharacterized IDN2 XH domain is required for the IDN2-IDP1/IDP2 complex formation as well as for IDN2 function. IDP1 is required for de novo DNA methylation, siRNA accumulation, and transcriptional gene silencing, whereas IDP2 has partially overlapping roles with IDP1. Unlike IDN2, IDP1 and IDP2 are incapable of binding double-stranded RNA, suggesting that the roles of IDP1 and IDP2 are different from those of IDN2 in the IDN2-IDP1/IDP2 complex and that IDP1 and IDP2 are essential for the functioning of the complex in RdDM.

/pdf/idn2-and-its-paralogs-form-a-complex-required-for-rna-535ruyds0k.pdf

IDN2 and its paralogs form a complex required for RNA-directed DNA methylation.

The chromodomain helicase DNA-binding family of ATP-dependent chromatin remodeling factors play essential roles during eukaryote growth and development They are recruited by specific transcription factors and regulate the expression of developmentally important genes Here, we describe an unexpected role in non-coding RNA-directed DNA methylation in Arabidopsis thaliana Through forward genetic screens we identified PKL, a gene required for developmental regulation in plants, as a factor promoting transcriptional silencing at the transgenic RD29A promoter Mutation of PKL results in DNA methylation changes at more than half of the loci that are targeted by RNA-directed DNA methylation (RdDM) A small number of transposable elements and genes had reduced DNA methylation correlated with derepression in the pkl mutant, though for the majority, decreases in DNA methylation are not sufficient to cause release of silencing The changes in DNA methylation in the pkl mutant are positively correlated with changes in 24-nt siRNA levels In addition, PKL is required for the accumulation of Pol V-dependent transcripts and for the positioning of Pol V-stabilized nucleosomes at several tested loci, indicating that RNA polymerase V-related functions are impaired in the pkl mutant PKL is required for transcriptional silencing and has significant effects on RdDM in plants The changes in DNA methylation in the pkl mutant are correlated with changes in the non-coding RNAs produced by Pol IV and Pol V We propose that at RdDM target regions, PKL may be required to create a chromatin environment that influences non-coding RNA production, DNA methylation, and transcriptional silencing

/pdf/the-developmental-regulator-pkl-is-required-to-maintain-5ao3146khj.pdf

The developmental regulator PKL is required to maintain correct DNA methylation patterns at RNA-directed DNA methylation loci

RNA-directed DNA methylation (RdDM) is an important de novo DNA methylation pathway in plants. RdDM mediates the transcriptional silencing of many endogenous genomic loci, most of which are transposon related. A forward genetics screen identified DTF1 (DNA-binding transcription factor 1) as a new component for RdDM in Arabidopsis. Loss-of-function mutations in DTF1 release the transcriptional silencing of RdDM target loci and reduce the accumulation of 24-nt small interfering RNAs (siRNAs) from some of the targets. Interestingly, in the dtf1 mutant plants, the release of transcriptional gene silencing at solo-LTR is accompanied by decreased siRNA accumulation but not by reduced DNA methylation. These results suggest that DTF1 is an atypical component of RdDM and has both DNA methylation-dependent and -independent roles in transcriptional gene silencing. We suggest that besides DNA methylation, siRNAs may cause some other uncharacterized epigenetic modifications that lead to transcriptional gene silencing.

/pdf/an-atypical-component-of-rna-directed-dna-methylation-58o7tcjx4h.pdf

An atypical component of RNA-directed DNA methylation machinery has both DNA methylation-dependent and -independent roles in locus-specific transcriptional gene silencing

Chromatin modifications are known to affect flowering time in plants, but little is known about how these modifications regulate flowering time in response to environmental signals like photoperiod. In Arabidopsis thaliana, HDC1, a conserved subunit of the RPD3-like histone deacetylase (HDAC) complex, was previously reported to regulate flowering time via the same mechanism as does the HDAC HDA6. Here, we demonstrate that HDC1, SNLs and MSI1 are shared subunits of the HDA6 and HDA19 HDAC complexes. While the late-flowering phenotype of the hda6 mutant is independent of photoperiod, the hda19, hdc1 and snl2/3/4 mutants flower later than or at a similar time to the wild-type in long-day conditions but flower earlier than the wild-type in short-day conditions. Our genome-wide analyses indicate that the effect of hdc1 on histone acetylation and transcription is comparable with that of hda19 but is different from that of hda6. Especially, we demonstrate that the HDA19 complex directly regulates the expression of two flowering repressor genes related to the gibberellin signaling pathway. Thus, the study reveals a photoperiod-dependent role of the HDA19 HDAC complex in the regulation of flowering time.

The HDA19 histone deacetylase complex is involved in the regulation of flowering time in a photoperiod-dependent manner.

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IDN2 and its paralogs form a complex required for RNA-directed DNA methylation.

The developmental regulator PKL is required to maintain correct DNA methylation patterns at RNA-directed DNA methylation loci

An atypical component of RNA-directed DNA methylation machinery has both DNA methylation-dependent and -independent roles in locus-specific transcriptional gene silencing

The HDA19 histone deacetylase complex is involved in the regulation of flowering time in a photoperiod-dependent manner.