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

Schalk, Catherine; Cognat, Valérie; Graindorge, Stéfanie; Vincent, Timothée; Voinnet, Olivier; Molinier, Jean

doi:10.1073/pnas.1618834114

Cited by 61 publications

(91 citation statements)

References 57 publications

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“…AGO1, as the main component of the miRNA effector complex, also responds to the environment, rendering its activity variable. In this sense, AGO1 was shown to participate in the response to several stresses, including UV‐induced DNA damage, salt stress and hormone responses (Dolata et al ., ; Schalk et al ., ; Liu et al ., ). In addition, some of the few proteins known to interact with AGO1 in plants are also heavily regulated by stress.…”

Section: Environmental Regulation Of the Mirna Biogenesis Machinerymentioning

confidence: 99%

Keep calm and carry on: miRNA biogenesis under stress

2019

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Summary MicroRNAs (miRNAs) are major post‐transcriptional regulators of gene expression. Their biogenesis relies on the cleavage of longer precursors by a nuclear localized processing machinery. The evolutionary preference of plant miRNAs to silence transcription factors turned these small molecules into key actors during growth and adaptive responses. Furthermore, during their life cycle plants are subject to changes in the environmental conditions surrounding them. In order to face these changes, plants display unique adaptive capacities based on an enormous developmental plasticity, where miRNAs play central roles. Many individual miRNAs have been shown to modulate the plant response to different environmental cues and stresses. In the last few years, increasing evidence has shown that not only individual genes encoding miRNAs but also the miRNA pathway as a whole is subject to regulation in response to external stimulus. In this review, we discuss the current knowledge about the miRNA pathway. We dissect the pathway to analyze the events leading to the generation of these small RNAs and emphasize the regulation of core components of the miRNA biogenesis machinery.

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Section: Environmental Regulation Of the Mirna Biogenesis Machinerymentioning

confidence: 99%

Keep calm and carry on: miRNA biogenesis under stress

2019

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“…Therefore, in such plants, the NER pathway (TCR and GGR) would be expected to be the main process used to remove DNA photolesions. We also used ddb2, dcl4 and ago1 mutant plants that are defective in GGR (ddb2; Molinier et al, 2008; and/or in small RNA-mediated GGR (ddb2, dcl4 and ago1; Schalk et al, 2017). Thus, the DR would be expected to be predominantly used to repair photolesions as well as other pathways (i.e.…”

Section: Photodamage Dna Repair Pathways Prevent Excessive Changes Ofmentioning

confidence: 99%

“…In order to determine a genome-wide map of photolesions, genomic DNA was prepared from the same UV-C treated plants (WT, uvr3 phrI, ddb2, dcl4 and ago1; see methods for details) used for the methylome analyses. Genomic DNA was subjected to immunoprecipitation using anti-CPD and anti-6,4 PPs antibodies and high throughput sequencing was performed on the immunoprecipitated DNA (Schalk et al, 2017). The resulting sequences were mapped on the nuclear arabidopsis genome and the enriched genomic regions (IP/input) containing photolesions were identified using bioinformatic workflow (Schalk et al, 2017; see methods for details).…”

Section: Genome Wide Mapping Of Uv-c-induced Photolesionsmentioning

confidence: 99%

“…Interestingly, DDB2 also associates with the silencing factor ARGONAUTE 1 (AGO1) to form a chromatin-bound complex with 21-nt small RNA (siRNAs; Schalk et al, 2017). This class of small RNAs, called UV-induced siRNA (uviRNAs), originates from the photo-damaged regions (mainly TE and intergenic regions) and involves a non-canonical biogenesis pathway requiring the plant specific RNA POLYMERASE IV (RNA POL IV), RNA-DEPENDENT RNA POLYMERASE 2 (RDR2) and DICER-LIKE 4 (DCL4; Schalk et al, 2017). The DDB2-AGO1-uviRNA complex loads on chromatin upon UV irradiation and likely facilitates photodamage recognition in an RNA/DNA complementary manner (Schalk et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

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Photodamage repair pathways contribute to the accurate maintenance of the DNA methylome landscape upon UV exposure

Graindorge

Cognat

Berens

et al. 2019

Preprint

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Plants are exposed to the damaging effect of sunlight that induces DNA photolesions. In order to maintain genome integrity, specific DNA repair pathways are mobilized. Upon removal of UV-induced DNA lesions, the accurate re-establishment of epigenome landscape is expected to be a prominent step of these DNA repair pathways. However, it remains poorly documented whether DNA methylation is accurately maintained at photodamaged sites and how photodamage repair pathways contribute to the maintenance of genome/methylome integrities.Using genome wide approaches, we report that UV-C irradiation leads to asymmetric DNA methylation changes. We identified that the specific DNA repair pathways involved in the repair of UV-induced DNA lesions, Direct Repair (DR) and Global Genome Repair (GGR), prevent the excessive alterations of DNA methylation landscape. Moreover, we identified that UV-C irradiation induced chromocenter reorganization and that photodamage repair factors control this dynamics. The methylome changes rely on misregulation of maintenance, de novo and active DNA demethylation pathways highlighting that molecular processes related to genome and methylome integrities are closely interconnected. Importantly, we identified that photolesions are sources of DNA methylation changes in both, constitutive and facultative heterochromatin. This study unveils that DNA repair factors, together with small RNA, act to accurately maintain both genome and methylome integrities at photodamaged silent genomic regions, strengthening the idea that plants have evolved sophisticated interplays between DNA methylation dynamics and DNA repair. Availability of data and materialsWGBS, DNA-seq and small RNA-seq raw data generated in this work are publicly accessible through the GEO registration number : GSE132750. Authors' contributionsSG and VC performed bioinformatics. PJtoB performed cytogenetics, developed the automated image analysis program with JMu and analyzed the data. SG, VC, PJtoB and JMu wrote the methods section. JM designed experiments, prepared the biological samples, analyzed the data and wrote the manuscript. All authors read and approved the final manuscript.

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“…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). DSBs were shown to trigger the induction of sRNAs required for mediating RdDM independent DSB repair (Wei et al, 2012).…”

Section: Discussionmentioning

confidence: 99%

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

Cited by 61 publications

References 57 publications

Keep calm and carry on: miRNA biogenesis under stress

Keep calm and carry on: miRNA biogenesis under stress

Photodamage repair pathways contribute to the accurate maintenance of the DNA methylome landscape upon UV exposure

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

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