AGO6 Functions in RNA-Mediated Transcriptional Gene Silencing in Shoot and Root Meristems in Arabidopsis thaliana

Eun, Chang-Ho; Lorković, Zdravko J.; Naumann, Ulf; Long, Quan; Havecker, Ericka R.; Simon, Stacey A.; Matzke, A. J. M.; Matzke, Marjori

doi:10.1371/journal.pone.0025730

Cited by 58 publications

(54 citation statements)

References 34 publications

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“…1E). Although the RdDM pathway is known to be required for epigenetic silencing of some transgenes and numerous endogenous loci, including many transposon repeats (22)(23)(24)(25), our forward genetic screen here identified the RdDM as an antisilencing pathway. The notion of the RdDM pathway also having an antisilencing role is consistent with a previous report (17).…”

Section: Rddm Mutations Cause the Silencing Of 35s::suc2 And 2 × 35s:mentioning

confidence: 84%

Regulatory link between DNA methylation and active demethylation in Arabidopsis

Lei

Zhang

Julian

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

216

207

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De novo DNA methylation through the RNA-directed DNA methylation (RdDM) pathway and active DNA demethylation play important roles in controlling genome-wide DNA methylation patterns in plants. Little is known about how cells manage the balance between DNA methylation and active demethylation activities. Here, we report the identification of a unique RdDM target sequence, where DNA methylation is required for maintaining proper active DNA demethylation of the Arabidopsis genome. In a genetic screen for cellular antisilencing factors, we isolated several REPRESSOR OF SILENCING 1 (ros1) mutant alleles, as well as many RdDM mutants, which showed drastically reduced ROS1 gene expression and, consequently, transcriptional silencing of two reporter genes. A helitron transposon element (TE) in the ROS1 gene promoter negatively controls ROS1 expression, whereas DNA methylation of an RdDM target sequence between ROS1 5′ UTR and the promoter TE region antagonizes this helitron TE in regulating ROS1 expression. This RdDM target sequence is also targeted by ROS1, and defective DNA demethylation in loss-of-function ros1 mutant alleles causes DNA hypermethylation of this sequence and concomitantly causes increased ROS1 expression. Our results suggest that this sequence in the ROS1 promoter region serves as a DNA methylation monitoring sequence (MEMS) that senses DNA methylation and active DNA demethylation activities. Therefore, the ROS1 promoter functions like a thermostat (i.e., methylstat) to sense DNA methylation levels and regulates DNA methylation by controlling ROS1 expression.NA methylation is a conserved epigenetic mark important for development and stress responses in plants and many animals (1-4). Genome-wide DNA methylation patterns are dynamically regulated by establishment, maintenance, and removal activities (4, 5). In plants, de novo DNA methylation is controlled by the RNA-directed DNA methylation (RdDM) pathway, in which complementary pairing between long noncoding RNAs and siRNAs mediates cytosine methylation in a sequence-specific manner (2, 4, 6, 7). Best characterized in Arabidopsis, RdDM involves a complex array of regulators and mainly targets heterochromatic regions that are enriched with transposon elements (TEs) and other DNA repeat sequences (8, 9). Once established, Arabidopsis DNA methylation is maintained via different mechanisms depending on the cytosine contexts [i.e., CG, CHG, CHH (H represents A, T, or C)]. CG and CHG methylation is maintained by MET1 and CMT3, respectively (2), whereas CHH methylation within pericentromeric long TEs can be catalyzed by CMT2 and CHH methylation at other loci is established de novo by DRM2 during every cell cycle (2, 10). In contrast to DNA methyltransferases that establish and/or maintain cytosine methylation, plant 5-methylcytosine DNA glycosylases initiate a base excision repair pathway that erases DNA methylation, thereby generating, together with the establishment and maintenance activities, a dynamic landscape of DNA methylation (11, 12).The Arabidopsis ...

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Section: Rddm Mutations Cause the Silencing Of 35s::suc2 And 2 × 35s:mentioning

confidence: 84%

Regulatory link between DNA methylation and active demethylation in Arabidopsis

Lei

Zhang

Julian

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

216

207

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“…Whereas AGO9 encodes an AGO protein that preferentially interacts with a 24-nucleotide sRNA corresponding to transposable elements located in the pericentromeric regions of all Arabidopsis chromosomes Olmedo-Monfil et al, 2010), RDR6 acts in the biogenesis of various types of sRNAs including trans-acting small interfering RNAs and in posttranscriptional transgene silencing mediated by sRNAs (Peragine et al, 2004;Yoshikawa et al, 2005;Chitwood et al, 2009). AGO9 is phylogenetically related to AGO4 and AGO6, proteins that are involved in heterochromatic silencing through the RNA-directed DNA methylation pathway (Zilberman et al, 2003(Zilberman et al, , 2004Vaucheret, 2008;Havecker et al, 2010;Mallory and Vaucheret, 2010;Eun et al, 2011). The introduction of a single dominant loss-of-function ago9 or rdr6 allele in some Arabidopsis ecotypes resulted in a buffering effect that limited the number of ovules showing ectopic configurations, whereas this buffering effect was lost in plants that completely lost AGO9 activity.…”

Section: Discussionmentioning

confidence: 99%

Natural Variation in Epigenetic Pathways Affects the Specification of Female Gamete Precursors in Arabidopsis

et al. 2015

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In angiosperms, the transition to the female gametophytic phase relies on the specification of premeiotic gamete precursors from sporophytic cells in the ovule. In Arabidopsis thaliana, a single diploid cell is specified as the premeiotic female gamete precursor. Here, we show that ecotypes of Arabidopsis exhibit differences in megasporogenesis leading to phenotypes reminiscent of defects in dominant mutations that epigenetically affect the specification of female gamete precursors. Intraspecific hybridization and polyploidy exacerbate these defects, which segregate quantitatively in F2 populations derived from ecotypic hybrids, suggesting that multiple loci control cell specification at the onset of female meiosis. This variation in cell differentiation is influenced by the activity of ARGONAUTE9 (AGO9) and RNA-DEPENDENT RNA POLYMERASE6 (RDR6), two genes involved in epigenetic silencing that control the specification of female gamete precursors. The pattern of transcriptional regulation and localization of AGO9 varies among ecotypes, and abnormal gamete precursors in ovules defective for RDR6 share identity with ectopic gamete precursors found in selected ecotypes. Our results indicate that differences in the epigenetic control of cell specification lead to natural phenotypic variation during megasporogenesis. We propose that this mechanism could be implicated in the emergence and evolution of the reproductive alternatives that prevail in flowering plants.

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“…AGO6 appears to differ from AGO4 in binding preference for siRNAs produced from different loci, which may be attributed to their different spatiotemporal expression and interaction with target loci (Havecker et al, 2010). AGO4 is ubiquitously expressed throughout plant, whereas AGO6 is predominantly expressed in shoot and root apical meristems and in tissues enriched for dividing cells but not in mature leaves (Zheng et al, 2007;Havecker et al, 2010;Eun et al, 2011). A recent study provided additional insights into the nonredundant roles of AGO4 and AGO6 .…”

Section: Ago2/3/7 Cladementioning

confidence: 99%

RNAi in Plants: An Argonaute-Centered View

2016

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Argonaute (AGO) family proteins are effectors of RNAi in eukaryotes. AGOs bind small RNAs and use them as guides to silence target genes or transposable elements at the transcriptional or posttranscriptional level. Eukaryotic AGO proteins share common structural and biochemical properties and function through conserved core mechanisms in RNAi pathways, yet plant AGOs have evolved specialized and diversified functions. This Review covers the general features of AGO proteins and highlights recent progress toward our understanding of the mechanisms and functions of plant AGOs.

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AGO6 Functions in RNA-Mediated Transcriptional Gene Silencing in Shoot and Root Meristems in Arabidopsis thaliana

Cited by 58 publications

References 34 publications

Regulatory link between DNA methylation and active demethylation in Arabidopsis

Regulatory link between DNA methylation and active demethylation in Arabidopsis

Natural Variation in Epigenetic Pathways Affects the Specification of Female Gamete Precursors in Arabidopsis

RNAi in Plants: An Argonaute-Centered View

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