DNA DAMAGE BINDING PROTEIN2 Shapes the DNA Methylation Landscape

Schalk, Catherine; Drevensek, Stéphanie; Kramdi, Amira; Kassam, Mohamed; Ahmed, Ikhlak; Cognat, Valérie; Graindorge, Stéfanie; Bergdoll, Marc; Baumberger, Nicolas; Heintz, Dimitri; Bowler, Chris; Genschik, Pascal; Barneche, Frédy; Colot, Vincent; Molinier, Jean

doi:10.1105/tpc.16.00474

Cited by 20 publications

(44 citation statements)

References 56 publications

(82 reference statements)

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“…5A). By contrast, a FLAG-tagged, DNA-bindingdeficient point-mutant allele of DDB2 (DDB2 K314E -FLAG) (30,31), which failed to rescue the ddb2-3 UV hypersensitivity (Fig. S5A), coimmunoprecipitated with AGO1 significantly less than the WT DDB2-FLAG allele (Fig.…”

Section: Resultsmentioning

confidence: 99%

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Small RNA-mediated repair of UV-induced DNA lesions by the DNA DAMAGE-BINDING PROTEIN 2 and ARGONAUTE 1

Schalk

Cognat

Graindorge

et al. 2017

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

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As photosynthetic organisms, plants need to prevent irreversible UV-induced DNA lesions. Through an unbiased, genome-wide approach, we have uncovered a previously unrecognized interplay between Global Genome Repair and small interfering RNAs (siRNAs) in the recognition of DNA photoproducts, prevalently in intergenic regions. Genetic and biochemical approaches indicate that, upon UV irradiation, the DNA DAMAGE-BINDING PROTEIN 2 (DDB2) and ARGONAUTE 1 (AGO1) of Arabidopsis thaliana form a chromatin-bound complex together with 21-nt siRNAs, which likely facilitates recognition of DNA damages in an RNA/DNA complementary strand-specific manner. The biogenesis of photoproduct-associated siRNAs involves the noncanonical, concerted action of RNA POLYMERASE IV, RNA-DEPENDENT RNA POLYMERASE-2, and DICER-LIKE-4. Furthermore, the chromatin association/dissociation of the DDB2-AGO1 complex is under the control of siRNA abundance and DNA damage signaling. These findings reveal unexpected nuclear functions for DCL4 and AGO1, and shed light on the interplay between small RNAs and DNA repair recognition factors at damaged sites.

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Section: Resultsmentioning

confidence: 99%

“…The cDNA of Arabidopsis DDB2 and DDB2 K314E were amplified by PCR using primers described in ref. 31. Both cDNA were sequenced and cloned into the pOEX2 vector, between the NcoI and AvrII sites (25).…”

Section: Methodsmentioning

confidence: 99%

Small RNA-mediated repair of UV-induced DNA lesions by the DNA DAMAGE-BINDING PROTEIN 2 and ARGONAUTE 1

Schalk

Cognat

Graindorge

et al. 2017

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

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“…It has been shown that INVOLVED IN DE NOVO2 (IDN2), a dsRNA binding protein (Ausin et al, 2009;Zheng et al, 2010;Schalk et al, 2016), forms a complex with IDN2 paralog 1 (IDP1) and IDP2 that functions at the effector stage of RdDM (Ausin et al, 2012;Xie et al, 2012;Zhang et al, 2012). In this study, we found that IDN2 was involved in HR repair and that its dsRNA binding activity was required for its function in HR repair.…”

Section: Introductionmentioning

confidence: 79%

“…These findings suggest that the RdDM pathway shares components with diRNA-mediated DSB repair. A recent study has also provided a link between the nucleotide excision repair machinery and the RdDM pathway (Schalk et al, 2016). DNA DAMAGE BINDING2, a protein that is involved in nucleotide excision repair, influences de novo DNA methylation through interacting with AGO4 and controlling the local abundance of hc-siRNAs (Schalk et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

IDN2 Interacts with RPA and Facilitates DNA Double-Strand Break Repair by Homologous Recombination in Arabidopsis

Liu

Costa‐Nunes

et al. 2017

Plant Cell

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Repair of DNA double-strand breaks (DSBs) is critical for the maintenance of genome integrity. We previously showed that DSB-induced small RNAs (diRNAs) facilitate homologous recombination-mediated DSB repair in Here, we show that INVOLVED IN DE NOVO2 (IDN2), a double-stranded RNA binding protein involved in small RNA-directed DNA methylation, is required for DSB repair in Arabidopsis. We find that IDN2 interacts with the heterotrimeric replication protein A (RPA) complex. Depletion of IDN2 or the diRNA binding ARGONAUTE2 leads to increased accumulation of RPA at DSB sites and mislocalization of the recombination factor RAD51. These findings support a model in which IDN2 interacts with RPA and facilitates the release of RPA from single-stranded DNA tails and subsequent recruitment of RAD51 at DSB sites to promote DSB repair.

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“…Whether this also occurs in plant cells is not known. A role for the DDB2 DNA damage factor in DNA methylation through both RdDM and regulation of DNA methylcytosine glycosylase has been shown in Arabidopsis (Schalk et al, 2016). Also, interconnections between sRNAs and DNA damage repair have been reported (Schalk et al, 2017;Wei et al, 2012).…”

Section: Discussionmentioning

confidence: 97%

Impact of differential DNA methylation on transgene expression in cotton (Gossypium hirsutum L.) events generated by targeted sequence insertion

Verkest¹,

Bourout²,

Debaveye³

et al. 2019

Plant Biotechnology Journal

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Summary Targeted Genome Optimization ( TGO ) using site‐specific nucleases to introduce a DNA double‐strand break ( DSB ) at a specific target locus has broadened the options available to breeders for generation and combination of multiple traits. The use of targeted DNA cleavage in combination with homologous recombination ( HR )‐mediated repair, enabled the precise targeted insertion of additional trait genes (2m epsps, hppd, axmi115 ) at a pre‐existing transgenic locus in cotton. Here we describe the expression and epigenome analyses of cotton Targeted Sequence Insertion ( TSI ) events over generations. In a subset of events, we observed variability in the level of transgene ( hppd , axmi115 ) expression between independent but genetically identical TSI events. Transgene expression could also be differential within single events and variable over generations. This expression variability and silencing occurred independently of the transgene sequence and could be attributed to DNA methylation that was further linked to different DNA methylation mechanisms. The trigger(s) of transgene DNA methylation remains elusive but we hypothesize that targeted DSB induction and repair could be a potential trigger for DNA methylation.

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DNA DAMAGE BINDING PROTEIN2 Shapes the DNA Methylation Landscape

Cited by 20 publications

References 56 publications

Small RNA-mediated repair of UV-induced DNA lesions by the DNA DAMAGE-BINDING PROTEIN 2 and ARGONAUTE 1

Small RNA-mediated repair of UV-induced DNA lesions by the DNA DAMAGE-BINDING PROTEIN 2 and ARGONAUTE 1

IDN2 Interacts with RPA and Facilitates DNA Double-Strand Break Repair by Homologous Recombination in Arabidopsis

Impact of differential DNA methylation on transgene expression in cotton (Gossypium hirsutum L.) events generated by targeted sequence insertion

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