scholarly journals Paternal easiRNAs regulate parental genome dosage in Arabidopsis

2017 ◽  
Author(s):  
German Martinez ◽  
Philip Wolff ◽  
Zhenxing Wang ◽  
Jordi Moreno-Romero ◽  
Juan Santos-González ◽  
...  
Keyword(s):  
Dna Methylation ◽  
Chromosome Number ◽  
Genome Stability ◽  
Seed Viability ◽  
Parental Genome ◽  
Seed Abortion ◽  
Small Interfering Rnas ◽  
Hybrid Seeds ◽  
Rna Polymerase Iv ◽  
Triploid Block

The regulation of parental genome dosage is of fundamental importance in animals and plants, exemplified by X chromosome inactivation and dosage compensation. The “triploid block” is a classical example of dosage regulation in plants that establishes a reproductive barrier between species differing in chromosome number 1,2. This barrier acts in the endosperm, an ephemeral tissue that nurtures the developing embryo and induces the abortion of hybrid seeds through a yet unknown mechanism. Interploidy hybridizations involving diploid (2×) maternal parents and tetraploid (4×) pollen donors cause failure in endosperm cellularization, leading to embryo arrest 3. Here we show that paternal epigenetically activated small interfering RNAs (easiRNAs) are responsible for the establishment of the triploid block-associated seed abortion in Arabidopsis thaliana. Paternal loss of the plant-specific RNA polymerase IV suppressed easiRNA formation and rescued triploid seeds by restoring small RNA-directed DNA methylation at transposable elements (TEs), correlating with reduced expression of paternally expressed imprinted genes (PEGs). We propose that excess of paternally derived easiRNAs in diploid pollen prevents establishment of DNA methylation, leading to triploid seed abortion. Our data further suggest that easiRNAs form a quantitative signal for chromosome number and their balanced dosage is required for post-fertilization genome stability and seed viability.

scholarly journals RNA Pol IV has antagonistic parent-of-origin effects on Arabidopsis endosperm

2021 ◽  
Author(s):  
P.R. V. Satyaki ◽  
Mary Gehring
Keyword(s):  
Gene Expression ◽  
Dna Methylation ◽  
Regulatory System ◽  
Small Interfering Rnas ◽  
Pol Iv ◽  
Gene Regulatory System ◽  
Rna Polymerase Iv ◽  
Parent Of Origin ◽  
Origin Effects ◽  
Maternal Resources

Gene expression in endosperm, a seed tissue that mediates transfer of maternal resources to offspring, is under complex epigenetic control. We show here that plant-specific RNA Polymerase IV mediates parental control of endosperm gene expression. Pol IV is required for the production of small interfering RNAs that typically direct DNA methylation. We compared small RNAs, DNA methylation, and mRNAs in A. thaliana endosperm from reciprocal heterozygotes produced by crossing wildtype plants to Pol IV mutants. We find that maternally and paternally acting Pol IV have divergent effects on endosperm with loss of maternal and paternal Pol IV impacting sRNAs and DNA methylation at different genomic sites. Strikingly, maternally and paternally-acting Pol IV have antagonistic impacts on gene expression at some loci, divergently promoting or repressing endosperm gene expression. Antagonistic parent-of13 origin effects have only rarely been described and are consistent with a gene regulatory system evolving under parental conflict.

scholarly journals Arabidopsis RNA Polymerase IV generates 21-22 nucleotide small RNAs that can participate in RNA-directed DNA methylation and may regulate genes

2019 ◽  
Author(s):  
Kaushik Panda ◽  
Andrea D. McCue ◽  
R. Keith Slotkin
Keyword(s):  
Dna Methylation ◽  
Transposable Elements ◽  
Rna Polymerase ◽  
Transcript Abundance ◽  
Gene Transcript ◽  
Small Interfering Rnas ◽  
Pol Iv ◽  
Rna Polymerase Iv ◽  
Plant Life Cycle ◽  
And Function

AbstractThe plant-specific RNA Polymerase IV (Pol IV) transcribes heterochromatic regions, including many transposable elements, with the well-described role of generating 24 nucleotide (nt) small interfering RNAs (siRNAs). These siRNAs target DNA methylation back to transposable elements to reinforce the boundary between heterochromatin and euchromatin. In the male gametophytic phase of the plant life cycle, pollen, Pol IV switches to generating primarily 21-22 nt siRNAs, but the biogenesis and function of these siRNAs has been enigmatic. In contrast to being pollen-specific, we identified that Pol IV generates these 21-22 nt siRNAs in sporophytic tissues, likely from the same transcripts that are processed into the more abundant 24 nt siRNAs. The 21-22 nt forms are specifically generated by the combined activities of DICER proteins DCL2/DCL4 and can participate in RNA-directed DNA methylation. These 21-22 nt siRNAs are also loaded into ARGONAUTE1, which is known to function in post-transcriptional regulation. Like other plant siRNAs and microRNAs incorporated into AGO1, we find a signature of genic mRNA cleavage at the predicted target site of these siRNAs, suggesting that Pol IV-generated 21-22 nt siRNAs may function to regulate gene transcript abundance. Our data provides support for the existing model that in pollen Pol IV functions in gene regulation.

scholarly journals microRNA-triggered transposon small RNAs mediate genome dosage response

2017 ◽  
Author(s):  
Filipe Borges ◽  
Jean-Sébastien Parent ◽  
Frédéric van Ex ◽  
Philip Wolff ◽  
German Martínez ◽  
...  
Keyword(s):  
Small Rna ◽  
Primer Binding Site ◽  
Common Mechanism ◽  
Small Interfering Rnas ◽  
Developing Seed ◽  
Dose Dependent Fashion ◽  
Rna Polymerase Iv ◽  
Triploid Block ◽  
Underlying Mechanisms ◽  
Dose Dependent

Chromosome dosage plays a significant role in reproductive isolation and speciation in both plants and animals, but underlying mechanisms are largely obscure1. Transposable elements can promote hybridity through maternal small RNA2, and have been postulated to regulate dosage response via neighboring imprinted genes3,4. Here, we show that a highly conserved microRNA in plants, miR845, targets the tRNAMet primer-binding site (PBS) of LTR-retrotransposons in Arabidopsis pollen, and triggers the accumulation of 21 to 22-nucleotide small RNA in a dose dependent fashion via RNA polymerase IV. We show that these epigenetically activated small-interfering RNAs (easiRNAs) mediate hybridization barriers between diploid seed parents and tetraploid pollen parents (“the triploid block”), and that natural variation for miR845 may account for “endosperm balance” allowing formation of triploid seeds. Targeting the PBS with small RNA is a common mechanism for transposon control in mammals and plants, and provides a uniquely sensitive means to monitor chromosome dosage and imprinting in the developing seed.

scholarly journals Transgenerational effect of mutants in the RNA-directed DNA methylation pathway on the triploid block

2020 ◽  
Author(s):  
Zhenxing Wang ◽  
Nicolas Butel ◽  
Juan Santos-González ◽  
Lauriane Simon ◽  
Cecilia Wärdig ◽  
...  
Keyword(s):  
Dna Methylation ◽  
De Novo ◽  
Early Stage ◽  
Suppressive Effect ◽  
Transgenerational Effect ◽  
Pol Iv ◽  
Short Rnas ◽  
Methylation Pathway ◽  
Rna Polymerase Iv ◽  
Triploid Block

AbstractHybridization of plants that differ in number of chromosome sets (ploidy) frequently causes endosperm failure and seed arrest, a phenomenon referred to as triploid block. Mutation in NRPD1, encoding the largest subunit of the plant-specific RNA Polymerase IV (Pol IV), can suppress the triploid block. Pol IV generates short RNAs required to guide de novo methylation in the RNA-directed DNA methylation (RdDM) pathway. In this study, we found that the ability of mutants in the RdDM pathway to suppress the triploid block depends on their degree of inbreeding. While nrpd1 is able to suppress in the first homozygous generation, mutants in RDR2, NRPE1, and DRM2 require at least one additional round of inbreeding to exert a suppressive effect. Inbreeding of nrpd1 was connected with a transgenerational loss of non-CG DNA methylation on sites jointly regulated by CHROMOMETHYLASES 2 and 3. Our data thus reveal that loss of RdDM function differs in its effect in early and late generations and that Pol IV acts at an early stage of triploid block establishment.One-sentence summaryInbreeding of mutants impaired in RdDM components transgenerationally enhanced their ability to suppress the triploid block.

scholarly journals Arabidopsis RNA Polymerase IV generates 21–22 nucleotide small RNAs that can participate in RNA-directed DNA methylation and may regulate genes

2020 ◽  
Vol 375 (1795) ◽  
pp. 20190417 ◽  
Author(s):  
Kaushik Panda ◽  
Andrea D. McCue ◽  
R. Keith Slotkin
Keyword(s):  
Dna Methylation ◽  
Gene Regulation ◽  
Rna Polymerase ◽  
Transcript Abundance ◽  
Gene Transcript ◽  
Small Interfering Rnas ◽  
Pol Iv ◽  
Rna Polymerase Iv ◽  
Plant Life Cycle ◽  
And Function

The plant-specific RNA Polymerase IV (Pol IV) transcribes heterochromatic regions, including many transposable elements (TEs), with the well-described role of generating 24 nucleotide (nt) small interfering RNAs (siRNAs). These siRNAs target DNA methylation back to TEs to reinforce the boundary between heterochromatin and euchromatin. In the male gametophytic phase of the plant life cycle, pollen, Pol IV switches to generating primarily 21–22 nt siRNAs, but the biogenesis and function of these siRNAs have been enigmatic. In contrast to being pollen-specific, we identified that Pol IV generates these 21–22 nt siRNAs in sporophytic tissues, likely from the same transcripts that are processed into the more abundant 24 nt siRNAs. The 21–22 nt forms are specifically generated by the combined activities of DICER proteins DCL2/DCL4 and can participate in RNA-directed DNA methylation. These 21–22 nt siRNAs are also loaded into ARGONAUTE1 (AGO1), which is known to function in post-transcriptional gene regulation. Like other plant siRNAs and microRNAs incorporated into AGO1, we find a signature of genic mRNA cleavage at the predicted target site of these siRNAs, suggesting that Pol IV-generated 21–22 nt siRNAs may function to regulate gene transcript abundance. Our data provide support for the existing model that in pollen Pol IV functions in gene regulation. This article is part of a discussion meeting issue ‘Crossroads between transposons and gene regulation’.

scholarly journals Identification of Pol IV and RDR2-dependent precursors of 24 nt siRNAs guiding de novo DNA methylation in Arabidopsis

eLife ◽  
2015 ◽  
Vol 4 ◽  
Author(s):  
Todd Blevins ◽  
Ram Podicheti ◽  
Vibhor Mishra ◽  
Michelle Marasco ◽  
Jing Wang ◽  
...  
Keyword(s):  
Rna Polymerase ◽  
Cytosine Methylation ◽  
De Novo ◽  
Transferase Activity ◽  
Small Interfering Rnas ◽  
Pol Iv ◽  
Nuclear Rna ◽  
Rna Polymerase Iv ◽  
Nuclear Rna Polymerase

In Arabidopsis thaliana, abundant 24 nucleotide small interfering RNAs (24 nt siRNA) guide the cytosine methylation and silencing of transposons and a subset of genes. 24 nt siRNA biogenesis requires nuclear RNA polymerase IV (Pol IV), RNA-dependent RNA polymerase 2 (RDR2) and DICER-like 3 (DCL3). However, siRNA precursors are mostly undefined. We identified Pol IV and RDR2-dependent RNAs (P4R2 RNAs) that accumulate in dcl3 mutants and are diced into 24 nt RNAs by DCL3 in vitro. P4R2 RNAs are mostly 26-45 nt and initiate with a purine adjacent to a pyrimidine, characteristics shared by Pol IV transcripts generated in vitro. RDR2 terminal transferase activity, also demonstrated in vitro, may account for occasional non-templated nucleotides at P4R2 RNA 3’ termini. The 24 nt siRNAs primarily correspond to the 5’ or 3’ ends of P4R2 RNAs, suggesting a model whereby siRNAs are generated from either end of P4R2 duplexes by single dicing events.

scholarly journals Control of the DNA Methylation System Component MBD2 by Protein Arginine Methylation

2006 ◽  
Vol 26 (19) ◽  
pp. 7224-7235 ◽  
Author(s):  
Choon Ping Tan ◽  
Sara Nakielny
Keyword(s):  
Dna Methylation ◽  
Complex Formation ◽  
Histone Deacetylases ◽  
Mammalian Cells ◽  
Genome Stability ◽  
Epigenetic Modification ◽  
Arginine Methylation ◽  
System Component ◽  
Transcription Repression ◽  
Mbd Proteins

ABSTRACT DNA methylation is vital for proper chromatin structure and function in mammalian cells. Genetic removal of the enzymes that catalyze DNA methylation results in defective imprinting, transposon silencing, X chromosome dosage compensation, and genome stability. This epigenetic modification is interpreted by methyl-DNA binding domain (MBD) proteins. MBD proteins respond to methylated DNA by recruiting histone deacetylases (HDAC) and other transcription repression factors to the chromatin. The MBD2 protein is dispensable for animal viability, but it is implicated in the genesis of colon tumors. Here we report that the MBD2 protein is controlled by arginine methylation. We identify the protein arginine methyltransferase enzymes that catalyze this modification and show that arginine methylation inhibits the function of MBD2. Arginine methylation of MBD2 reduces MBD2-methyl-DNA complex formation, reduces MBD2-HDAC repression complex formation, and impairs the transcription repression function of MBD2 in cells. Our report provides a molecular description of a potential regulatory mechanism for an MBD protein family member. It is the first to demonstrate that protein arginine methyltransferases participate in the DNA methylation system of chromatin control.

scholarly journals Dynamic DNA Methylation in Plant Growth and Development

2018 ◽  
Vol 19 (7) ◽  
pp. 2144 ◽  
Author(s):  
Arthur Bartels ◽  
Qiang Han ◽  
Pooja Nair ◽  
Liam Stacey ◽  
Hannah Gaynier ◽  
...  
Keyword(s):  
Dna Methylation ◽  
Plant Growth ◽  
Growth And Development ◽  
Genome Stability ◽  
Epigenetic Modification ◽  
Plant Growth And Development ◽  
Complex Dynamic ◽  
Dynamic Changes ◽  
The Common ◽  
Methylation Patterns

DNA methylation is an epigenetic modification required for transposable element (TE) silencing, genome stability, and genomic imprinting. Although DNA methylation has been intensively studied, the dynamic nature of methylation among different species has just begun to be understood. Here we summarize the recent progress in research on the wide variation of DNA methylation in different plants, organs, tissues, and cells; dynamic changes of methylation are also reported during plant growth and development as well as changes in response to environmental stresses. Overall DNA methylation is quite diverse among species, and it occurs in CG, CHG, and CHH (H = A, C, or T) contexts of genes and TEs in angiosperms. Moderately expressed genes are most likely methylated in gene bodies. Methylation levels decrease significantly just upstream of the transcription start site and around transcription termination sites; its levels in the promoter are inversely correlated with the expression of some genes in plants. Methylation can be altered by different environmental stimuli such as pathogens and abiotic stresses. It is likely that methylation existed in the common eukaryotic ancestor before fungi, plants and animals diverged during evolution. In summary, DNA methylation patterns in angiosperms are complex, dynamic, and an integral part of genome diversity after millions of years of evolution.

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