title: In plants, decapping prevents RDR6-dependent production of small interfering RNAs from endogenous mRNAs.
abstract: Cytoplasmic degradation of endogenous RNAs is an integral part of RNA quality control (RQC) and often relies on the removal of the 5' cap structure and their subsequent 5' to 3' degradation in cytoplasmic processing (P-)bodies. In parallel, many eukaryotes degrade exogenous and selected endogenous RNAs through post-transcriptional gene silencing (PTGS). In plants, PTGS depends on small interfering (si)RNAs produced after the conversion of single-stranded RNAs to double-stranded RNAs by the cellular RNA-dependent RNA polymerase 6 (RDR6) in cytoplasmic siRNA-bodies. PTGS and RQC compete for transgene-derived RNAs, but it is unknown whether this competition also occurs for endogenous transcripts. We show that the lethality of decapping mutants is suppressed by impairing RDR6 activity. We establish that upon decapping impairment hundreds of endogenous mRNAs give rise to a new class of rqc-siRNAs, that over-accumulate when RQC processes are impaired, a subset of which depending on RDR6 for their production. We observe that P- and siRNA-bodies often are dynamically juxtaposed, potentially allowing for cross-talk of the two machineries. Our results suggest that the decapping of endogenous RNA limits their entry into the PTGS pathway. We anticipate that the rqc-siRNAs identified in decapping mutants represent a subset of a larger ensemble of endogenous siRNAs.
authors.affiliation: Institut Jean-Pierre Bourgin UMR 1318, INRA, SPS Saclay Plant Sciences, Versailles, France.
authors.forename: Angel Emilio
authors.initials: AE
authors.lastname: Martínez de Alba
authors.affiliation: Institut des Sciences du Végétal, CNRS UPR 2355, SPS Saclay Plant Sciences, Gif-sur-Yvette, France.
authors.forename: Ana Beatriz
authors.initials: AB
authors.lastname: Moreno
authors.affiliation: Institute for Integrative Biology of the Cell, UMR 9198 - Universite Paris-Sud, Gif-sur-Yvette, France.
authors.forename: Marc
authors.initials: M
authors.lastname: Gabriel
authors.affiliation: Institut Jean-Pierre Bourgin UMR 1318, INRA, SPS Saclay Plant Sciences, Versailles, France.
authors.forename: Allison C
authors.initials: AC
authors.lastname: Mallory
authors.affiliation: Institut des Sciences du Végétal, CNRS UPR 2355, SPS Saclay Plant Sciences, Gif-sur-Yvette, France.
authors.forename: Aurélie
authors.initials: A
authors.lastname: Christ
authors.affiliation: Unité de Recherche en Génomique Végétale, UMR INRA 1165-CNRS 8114-UEVE, Evry, France.
authors.forename: Rémi
authors.initials: R
authors.lastname: Bounon
authors.affiliation: Unité de Recherche en Génomique Végétale, UMR INRA 1165-CNRS 8114-UEVE, Evry, France.
authors.forename: Sandrine
authors.initials: S
authors.lastname: Balzergue
authors.affiliation: Unité de Recherche en Génomique Végétale, UMR INRA 1165-CNRS 8114-UEVE, Evry, France.
authors.forename: Sebastien
authors.initials: S
authors.lastname: Aubourg
authors.affiliation: Institute for Integrative Biology of the Cell, UMR 9198 - Universite Paris-Sud, Gif-sur-Yvette, France.
authors.forename: Daniel
authors.initials: D
authors.lastname: Gautheret
authors.affiliation: Institut des Sciences du Végétal, CNRS UPR 2355, SPS Saclay Plant Sciences, Gif-sur-Yvette, France.
authors.forename: Martin D
authors.initials: MD
authors.lastname: Crespi
authors.affiliation: Institut Jean-Pierre Bourgin UMR 1318, INRA, SPS Saclay Plant Sciences, Versailles, France herve.vaucheret@versailles.inra.fr.
authors.forename: Hervé
authors.initials: H
authors.lastname: Vaucheret
authors.affiliation: Institut des Sciences du Végétal, CNRS UPR 2355, SPS Saclay Plant Sciences, Gif-sur-Yvette, France Center for Organismal Studies, University of Heidelberg, Germany alexis.maizel@cos.uni-heidelberg.de.
authors.forename: Alexis
authors.initials: A
authors.lastname: Maizel
mesh_terms: D017360:Arabidopsis / Q000235:genetics / Q000378:metabolism; D029681:Arabidopsis Proteins / Q000235:genetics* / Q000378:metabolism; D004722:Endoribonucleases / Q000235:genetics / Q000378:metabolism; D018506:Gene Expression Regulation, Plant; D009154:Mutation; D020411:Oligonucleotide Array Sequence Analysis; D030821:Plants, Genetically Modified; D012315:RNA Caps / Q000235:genetics* / Q000378:metabolism; D034622:RNA Interference; D012333:RNA, Messenger / Q000235:genetics* / Q000378:metabolism; D018749:RNA, Plant / Q000235:genetics* / Q000378:metabolism; D034741:RNA, Small Interfering / Q000235:genetics* / Q000378:metabolism; D058727:RNA, Small Untranslated / Q000235:genetics / Q000378:metabolism; D012324:RNA-Dependent RNA Polymerase / Q000235:genetics* / Q000378:metabolism; D059467:Transcriptome
chemical_list: D029681:Arabidopsis Proteins; D012315:RNA Caps; D012333:RNA, Messenger; D018749:RNA, Plant; D034741:RNA, Small Interfering; D058727:RNA, Small Untranslated; C483689:VARICOSE protein, Arabidopsis; C030052:mRNA decapping enzymes; C514575:RDR6 protein, Arabidopsis; D012324:RNA-Dependent RNA Polymerase; D004722:Endoribonucleases; C518493:Dcp1 protein, Arabidopsis; C518494:Dcp2 protein, Arabidopsis