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      Myosins VIII and XI Play Distinct Roles in Reproduction and Transport of Tobacco Mosaic Virus

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          Abstract

          Viruses are obligatory parasites that depend on host cellular factors for their replication as well as for their local and systemic movement to establish infection. Although myosin motors are thought to contribute to plant virus infection, their exact roles in the specific infection steps have not been addressed. Here we investigated the replication, cell-to-cell and systemic spread of Tobacco mosaic virus (TMV) using dominant negative inhibition of myosin activity. We found that interference with the functions of three class VIII myosins and two class XI myosins significantly reduced the local and long-distance transport of the virus. We further determined that the inactivation of myosins XI-2 and XI-K affected the structure and dynamic behavior of the ER leading to aggregation of the viral movement protein (MP) and to a delay in the MP accumulation in plasmodesmata (PD). The inactivation of myosin XI-2 but not of myosin XI-K affected the localization pattern of the 126k replicase subunit and the level of TMV accumulation. The inhibition of myosins VIII-1, VIII-2 and VIII-B abolished MP localization to PD and caused its retention at the plasma membrane. These results suggest that class XI myosins contribute to the viral propagation and intracellular trafficking, whereas myosins VIII are specifically required for the MP targeting to and virus movement through the PD. Thus, TMV appears to recruit distinct myosins for different steps in the cell-to-cell spread of the infection.

          Author Summary

          Viruses are parasites that require the host cell machinery for their propagation within and between cells. Myosins are molecular motors involved in the trafficking of cargos along actin filaments. Plant viruses have evolved to borrow this transport mechanism to aid their infection and spread within the plant. However, little is known about which of the many plant myosins are essential and at which specific steps they act to support virus infection. Here we investigated the role of different N. benthamiana myosins during the infection by Tobacco mosaic virus (TMV). Our results show that class XI myosins play specific roles in the reproduction and intracellular movement of TMV in association with the dynamic endoplasmic reticulum network, whereas class VIII myosins support the specific targeting of the viral movement protein to plasmodesmata and thus the cell-to-cell movement of the virus. Together these results indicate that TMV interacts with distinct myosins during specific infection steps.

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          Most cited references57

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          Initiation and maintenance of virus-induced gene silencing

          The phytoene desaturase (PDS) gene of Nicotiana benthamiana was silenced in plants infected with potato virus X (PVX) vectors carrying PDS inserts, and a green fluorescent protein (GFP) transgene was silenced in plants infected with PVX-GFP. This virus-induced gene silencing (VIGS) is post-transcriptional and cytoplasmic because it is targeted against exons rather than introns of PDS RNA and against viral RNAs. Although PDS and GFP RNAs are most likely targeted through the same mechanism, the VIGS phenotypes differed in two respects. PDS mRNA was targeted by VIGS in all green tissue of the PVX-PDS-infected plant, whereas PVX-PDS was not affected. In contrast, VIGS of the GFP was targeted against PVX-GFP. Initially, VIGS of the GFP was initiated in all green tissues, as occurred with PDS VIGS. However, after 30 days of infection, the GFP VIGS was no longer initiated in newly emerging leaves, although it was maintained in tissue in which it had already been initiated. Based on these analyses, we propose a model for VIGS in which the initiation of VIGS is dependent on the virus and maintenance of it is virus independent.
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            Remorin, a solanaceae protein resident in membrane rafts and plasmodesmata, impairs potato virus X movement.

            Remorins (REMs) are proteins of unknown function specific to vascular plants. We have used imaging and biochemical approaches and in situ labeling to demonstrate that REM clusters at plasmodesmata and in approximately 70-nm membrane domains, similar to lipid rafts, in the cytosolic leaflet of the plasma membrane. From a manipulation of REM levels in transgenic tomato (Solanum lycopersicum) plants, we show that Potato virus X (PVX) movement is inversely related to REM accumulation. We show that REM can interact physically with the movement protein TRIPLE GENE BLOCK PROTEIN1 from PVX. Based on the localization of REM and its impact on virus macromolecular trafficking, we discuss the potential for lipid rafts to act as functional components in plasmodesmata and the plasma membrane.
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              Myosin-dependent endoplasmic reticulum motility and F-actin organization in plant cells.

              Plants exhibit an ultimate case of the intracellular motility involving rapid organelle trafficking and continuous streaming of the endoplasmic reticulum (ER). Although it was long assumed that the ER dynamics is actomyosin-driven, the responsible myosins were not identified, and the ER streaming was not characterized quantitatively. Here we developed software to generate a detailed velocity-distribution map for the GFP-labeled ER. This map revealed that the ER in the most peripheral plane was relatively static, whereas the ER in the inner plane was rapidly streaming with the velocities of up to approximately 3.5 microm/sec. Similar patterns were observed when the cytosolic GFP was used to evaluate the cytoplasmic streaming. Using gene knockouts, we demonstrate that the ER dynamics is driven primarily by the ER-associated myosin XI-K, a member of a plant-specific myosin class XI. Furthermore, we show that the myosin XI deficiency affects organization of the ER network and orientation of the actin filament bundles. Collectively, our findings suggest a model whereby dynamic three-way interactions between ER, F-actin, and myosins determine the architecture and movement patterns of the ER strands, and cause cytosol hauling traditionally defined as cytoplasmic streaming.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Pathog
                PLoS Pathog
                plos
                plospath
                PLoS Pathogens
                Public Library of Science (San Francisco, USA )
                1553-7366
                1553-7374
                October 2014
                16 October 2014
                : 10
                : 10
                : e1004448
                Affiliations
                [1 ]Zürich-Basel Plant Science Center, Botany, Department of Environmental Sciences, University of Basel, Basel, Switzerland
                [2 ]Department of Botany and Plant Pathology and Center for Genome Research and Biocomputing, Oregon State University, Corvallis, Oregon, United States of America
                [3 ]Institut de Biologie Moléculaire des Plantes du CNRS, Université de Strasbourg, Strasbourg, France
                University of Kentucky, United States of America
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: KA MH. Performed the experiments: KA MDD. Analyzed the data: KA MDD. Contributed reagents/materials/analysis tools: KA MDD VVD MH. Wrote the paper: KA VVD MH.

                [¤a]

                Current address: Institut de Biologie Moléculaire des Plantes du CNRS, Université de Strasbourg, Strasbourg, France

                [¤b]

                Current address: Department of Biology-Plant Biology, University of Fribourg, Fribourg, Switzerland

                Article
                PPATHOGENS-D-14-00792
                10.1371/journal.ppat.1004448
                4199776
                25329993
                5f520e05-bdf9-42a4-9f87-d457dfe03b3f
                Copyright @ 2014

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 2 April 2014
                : 4 September 2014
                Page count
                Pages: 15
                Funding
                Work of KA was supported through a grant of the Swiss National Science Foundation ( www.snf.ch; grant 310031A_140694) to MH. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Cell Biology
                Plant Cell Biology
                Plant Science
                Plant Pathology
                Plant Pathogens
                Plant Viral Pathogens
                Custom metadata
                The authors confirm that all data underlying the findings are fully available without restriction. All relevant data are within the paper and its Supporting Information files

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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