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      Nonsense-Mediated Decay Serves as a General Viral Restriction Mechanism in Plants

      1 , , 1 , 1 , 2 , ∗∗

      Cell Host & Microbe

      Elsevier Inc.

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          Summary

          (+)strand RNA viruses have to overcome various points of restriction in the host to establish successful infection. In plants, this includes RNA silencing. To uncover additional bottlenecks to RNA virus infection, we genetically attenuated the impact of RNA silencing on transgenically expressed Potato virus X (PVX), a (+)strand RNA virus that replicates in Arabidopsis. A genetic screen in this sensitized background uncovered how nonsense-mediated decay (NMD), a host RNA quality control mechanism, recognizes and eliminates PVX RNAs with internal termination codons and long 3′ UTRs. NMD also operates in natural infection contexts, and while some viruses have evolved genome expression strategies to overcome this process altogether, the virulence of NMD-activating viruses entails their ability to directly suppress NMD or to promote an NMD-unfavorable cellular state. These principles of induction, evasion, and suppression define NMD as a general viral restriction mechanism in plants that also likely operates in animals.

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          Highlights

          • A sensitized genetic screen for modifiers of (+)strand RNA virus accumulation in Arabidopsis

          • The host nonsense-mediated decay (NMD) pathway restricts PVX during natural infection

          • NMD targets viral RNAs containing internal termination codons and long 3′ UTRs

          • Some viruses have evolved to evade NMD altogether, while others may suppress NMD actively

          Abstract

          Garcia et al. identify the nonsense-mediated decay (NMD) pathway, an endogenous RNA quality control mechanism, as a general bottleneck to RNA virus infection in plants. They elucidate intrinsic features of RNA virus biology that trigger NMD during authentic infection and show that viruses have evolved to evade or suppress this process in order to thrive in their hosts.

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          Most cited references 30

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          An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus.

          Transient gene expression is a fast, flexible and reproducible approach to high-level expression of useful proteins. In plants, recombinant strains of Agrobacterium tumefaciens can be used for transient expression of genes that have been inserted into the T-DNA region of the bacterial Ti plasmid. A bacterial culture is vacuum-infiltrated into leaves, and upon T-DNA transfer, there is ectopic expression of the gene of interest in the plant cells. However, the utility of the system is limited because the ectopic protein expression ceases after 2-3 days. Here, we show that post-transcriptional gene silencing (PTGS) is a major cause for this lack of efficiency. We describe a system based on co-expression of a viral-encoded suppressor of gene silencing, the p19 protein of tomato bushy stunt virus (TBSV), that prevents the onset of PTGS in the infiltrated tissues and allows high level of transient expression. Expression of a range of proteins was enhanced 50-folds or more in the presence of p19 so that protein purification could be achieved from as little as 100 mg of infiltrated leaf material. The effect of p19 was not saturated in cells that had received up to four individual T-DNAs and persisted until leaf senescence. Because of its simplicity and rapidity, we anticipate that the p19-enhanced expression system will have value in industrial production as well as a research tool for isolation and biochemical characterisation of a broad range of proteins without the need for the time-consuming regeneration of stably transformed plants.
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            A microRNA superfamily regulates nucleotide binding site-leucine-rich repeats and other mRNAs.

            Analysis of tomato (Solanum lycopersicum) small RNA data sets revealed the presence of a regulatory cascade affecting disease resistance. The initiators of the cascade are microRNA members of an unusually diverse superfamily in which miR482 and miR2118 are prominent members. Members of this superfamily are variable in sequence and abundance in different species, but all variants target the coding sequence for the P-loop motif in the mRNA sequences for disease resistance proteins with nucleotide binding site (NBS) and leucine-rich repeat (LRR) motifs. We confirm, using transient expression in Nicotiana benthamiana, that miR482 targets mRNAs for NBS-LRR disease resistance proteins with coiled-coil domains at their N terminus. The targeting causes mRNA decay and production of secondary siRNAs in a manner that depends on RNA-dependent RNA polymerase 6. At least one of these secondary siRNAs targets other mRNAs of a defense-related protein. The miR482-mediated silencing cascade is suppressed in plants infected with viruses or bacteria so that expression of mRNAs with miR482 or secondary siRNA target sequences is increased. We propose that this process allows pathogen-inducible expression of NBS-LRR proteins and that it contributes to a novel layer of defense against pathogen attack.
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              NMD: a multifaceted response to premature translational termination.

              Although most mRNA molecules derived from protein-coding genes are destined to be translated into functional polypeptides, some are eliminated by cellular quality control pathways that collectively perform the task of mRNA surveillance. In the nonsense-mediated decay (NMD) pathway premature translation termination promotes the recruitment of a set of factors that destabilize a targeted mRNA. The same factors also seem to have key roles in repressing the translation of the mRNA, dissociating its terminating ribosome and messenger ribonucleoproteins (mRNPs), promoting the degradation of its truncated polypeptide product and possibly even feeding back to the site of transcription to interfere with splicing of the primary transcript.
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                Author and article information

                Contributors
                Journal
                Cell Host Microbe
                Cell Host Microbe
                Cell Host & Microbe
                Elsevier Inc.
                1931-3128
                1934-6069
                21 August 2014
                10 September 2014
                21 August 2014
                : 16
                : 3
                : 391-402
                Affiliations
                [1 ]Institut de Biologie Moléculaire des Plantes (IBMP), Centre National de la Recherche Scientifique, UPR 2357, 67084 Strasbourg, France
                [2 ]Swiss Federal Institute of Technology Zurich, Department of Biology, Universitätstrasse 2, 8092 Zürich, Switzerland
                Author notes
                []Corresponding author damien.garcia@ 123456ibmp-cnrs.unistra.fr
                [∗∗ ]Corresponding author voinneto@ 123456ethz.ch
                Article
                S1931-3128(14)00270-4
                10.1016/j.chom.2014.08.001
                7185767
                25155460
                Copyright © 2014 Elsevier Inc. All rights reserved.

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                Microbiology & Virology

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