RNA-directed DNA Methylation and sexual reproduction: expanding beyond the seed

Chow, Hiu Tung; Chakraborty, Tania; Mosher, Rebecca A.

doi:10.1016/j.pbi.2019.11.006

Cited by 25 publications

(26 citation statements)

References 72 publications

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“…This study greatly extends the findings from several other functional studies of Pol IV or RdDM-associated genes in rice, tomato, or Brassica rapa (reviewed in Chow et al, 2020), and provides novel insights into the roles of Pol IV in plant reproductive development that would be otherwise indiscernible in Arabidopsis, reinforcing the importance of investigating diverse plant species in future studies of Pol IV and RdDM.…”

supporting

confidence: 72%

Pol IV Function is Differentially Essential within the Brassicaceae

Zhan¹

2020

Plant Cell

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At least five RNA polymerases (Pol I to Pol V) are known to exist in plant cells. Pol IV produces short transcripts that are converted into double-stranded RNAs by RNA-dependent RNA polymerase 2 (RDR2) and processed into 24-nucleotide (nt) small interfering RNAs (siRNAs) by DICER-LIKE 3 (DCL3). These siRNAs direct ARGONAUTE 4 (AGO4) or AGO6 to sites of Pol V transcription and recruit DNA methyltransferases to initiate RNAdirected DNA methylation (RdDM) (reviewed in Cuerda-Gil and Slotkin, 2016). Information about Pol IV's role in plant reproductive development is limited, in part due to the lack of visible mutant phenotypes in Arabidopsis (Arabidopsis thaliana), although it was recently demonstrated that it is critical for the triploid block in Arabidopsis (Satyaki and Gehring, 2019). To examine the function of Pol IV in Capsella (Capsella rubella), a Brassicaceae species closely related to Arabidopsis, Wang et al. (2020) created a loss-of-function mutant of a major subunit of Capsella Pol IV, NRPD1, using CRISPR-Cas9. The mutant (named Cr nrpd1) exhibited obvious defects in female and male fertility. About 30% of the ovules of the homozygous Cr nrpd1 mutant remained unfertilized after pollination with wild-type pollen. When self-fertilized, the mutant produced seeds significantly reduced in size. These phenotypes resemble those of the recently reported nrpd1 mutant in Brassica rapa (Grover et al., 2019). In addition, pollen development in the homozygous Cr nrpd1 mutant was arrested at the post-meiotic, microspore stage (see figure). To understand the molecular basis of the pollen defect, the authors compared small RNA (sRNA) accumulation and transposable element (TE) expression profiles between wildtype and Cr nrpd1 microspores. The results showed that TE-derived 21-to 24-nt siRNAs are depleted in the Cr nrpd1 mutant, indicating that NRPD1, and thus Pol IV activity, is required for the biogenesis of these siRNAs. The extent of upregulation of TE expression positively correlates with the level of siRNAs associated with them, suggesting that the Pol IVdependent siRNAs silence TEs in wild-type microspores. Moreover, these phenomena were also observed in an Arabidopsis nrpd1 mutant (At nrpd1), suggesting that the function of Pol IV in siRNA biogenesis is conserved between Capsella and Arabidopsis.

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supporting

confidence: 72%

Pol IV Function is Differentially Essential within the Brassicaceae

Zhan¹

2020

Plant Cell

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“…Observations suggest the potential role of ncRNA-directed DNA methylation in the direct exposure F1 generation and transgenerational F3 generation. Previous literature has established a role for RNA-directed DNA methylation in a number of biological and cellular systems [26][27][28]. This involves the ability of the ncRNA to recruit or direct chromatin remodeling proteins and proteins such as DNA methyltransferase to guide the DNA methylation at a chromosomal site, which has been established in a variety of different organisms and developmental processes Fig.…”

Section: Discussionmentioning

confidence: 99%

“…These observations suggest potential interactions between the different epigenetic processes, but this remains to be elucidated during the epigenetic inheritance phenomenon. Previous studies have demonstrated a role for ncRNA in RNA-directed DNA methylation in a number of different systems [26][27][28]. The ncRNA can help localize the DNA methylation site and facilitate subsequent chromatin remodeling processes.…”

Section: Introductionmentioning

confidence: 99%

Integration of sperm ncRNA-directed DNA methylation and DNA methylation-directed histone retention in epigenetic transgenerational inheritance

Beck

Maamar

Skinner

2021

Epigenetics & Chromatin

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Background Environmentally induced epigenetic transgenerational inheritance of pathology and phenotypic variation has been demonstrated in all organisms investigated from plants to humans. This non-genetic form of inheritance is mediated through epigenetic alterations in the sperm and/or egg to subsequent generations. Although the combined regulation of differential DNA methylated regions (DMR), non-coding RNA (ncRNA), and differential histone retention (DHR) have been shown to occur, the integration of these different epigenetic processes remains to be elucidated. The current study was designed to examine the integration of the different epigenetic processes. Results A rat model of transiently exposed F0 generation gestating females to the agricultural fungicide vinclozolin or pesticide DDT (dichloro-diphenyl-trichloroethane) was used to acquire the sperm from adult males in the subsequent F1 generation offspring, F2 generation grand offspring, and F3 generation great-grand offspring. The F1 generation sperm ncRNA had substantial overlap with the F1, F2 and F3 generation DMRs, suggesting a potential role for RNA-directed DNA methylation. The DMRs also had significant overlap with the DHRs, suggesting potential DNA methylation-directed histone retention. In addition, a high percentage of DMRs induced in the F1 generation sperm were maintained in subsequent generations. Conclusions Many of the DMRs, ncRNA, and DHRs were colocalized to the same chromosomal location regions. Observations suggest an integration of DMRs, ncRNA, and DHRs in part involve RNA-directed DNA methylation and DNA methylation-directed histone retention in epigenetic transgenerational inheritance.

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“…With the exception of Arabidopsis, which has only a small reduction in seed size, loss of RdDM in most species results in disruption of reproductive development, indicating that RdDM is necessary for successful sexual reproduction [17][18][19][20][21]. Mature embryos accumulate high levels of CHH methylation in Arabidopsis, soybean, and chickpea, suggesting that RdDM might enable reproduction through hypermethylation of the mature embryo [22][23][24][25][26][27].…”

Section: Introductionmentioning

confidence: 99%

Embryo CHH hypermethylation is mediated by RdDM and is autonomously directed inBrassica rapa

Chakraborty

Kendall

Grover

et al. 2020

Preprint

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Background: RNA directed DNA methylation (RdDM) initiates cytosine methylation in all contexts, and maintains asymmetric CHH methylation (where H is any base other than G). Mature plant embryos show one of the highest levels of CHH methylation, and it has been suggested that RdDM is responsible for this hypermethylation. Because loss of RdDM in Brassica rapa causes seed abortion, embryo methylation might play a role in seed development. RdDM is required in the maternal sporophyte, suggesting that small RNAs from the maternal sporophyte might translocate to the developing embryo, triggering DNA methylation that prevents seed abortion. This raises the question whether embryo hypermethylation is autonomously regulated by the embryo itself or influenced by the maternal sporophyte. Results: Here, we demonstrate that B. rapa embryos are hypermethylated in both euchromatin and heterochromatin and that this process requires RdDM. Contrary to current models, B. rapa embryo hypermethylation is not correlated with demethylation of the endosperm. We also show that maternal somatic RdDM is not sufficient for global embryo hypermethylation, and we find no compelling evidence for maternal somatic influence over embryo methylation at any locus. Decoupling of maternal and zygotic RdDM leads to successful seed development despite loss of embryo CHH hypermethylation. Conclusions: We conclude that embryo CHH hypermethylation is conserved, autonomously controlled, and not required for embryo development. Furthermore, maternal somatic RdDM, while required for seed development, does not directly influence embryo methylation patterns.

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RNA-directed DNA Methylation and sexual reproduction: expanding beyond the seed

Cited by 25 publications

References 72 publications

Pol IV Function is Differentially Essential within the Brassicaceae

Pol IV Function is Differentially Essential within the Brassicaceae

Integration of sperm ncRNA-directed DNA methylation and DNA methylation-directed histone retention in epigenetic transgenerational inheritance

Embryo CHH hypermethylation is mediated by RdDM and is autonomously directed inBrassica rapa

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