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      Formation of Complexes at Plasmodesmata for Potyvirus Intercellular Movement Is Mediated by the Viral Protein P3N-PIPO

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          Abstract

          Intercellular transport of viruses through cytoplasmic connections, termed plasmodesmata (PD), is essential for systemic infection in plants by viruses. Previous genetic and ultrastructural data revealed that the potyvirus cyclindrical inclusion (CI) protein is directly involved in cell-to-cell movement, likely through the formation of conical structures anchored to and extended through PD. In this study, we demonstrate that plasmodesmatal localization of CI in N. benthamiana leaf cells is modulated by the recently discovered potyviral protein, P3N-PIPO, in a CI:P3N-PIPO ratio-dependent manner. We show that P3N-PIPO is a PD-located protein that physically interacts with CI in planta. The early secretory pathway, rather than the actomyosin motility system, is required for the delivery of P3N-PIPO and CI to PD. Moreover, CI mutations that disrupt virus cell-to-cell movement compromise PD-localization capacity. These data suggest that the CI and P3N-PIPO complex coordinates the formation of PD-associated structures that facilitate the intercellular movement of potyviruses in infected plants.

          Author Summary

          Plant viral pathogens cause an estimated US$60 billion loss in crop yields worldwide each year. Potyviruses, accounting for ∼30% of known plant viruses, include many agriculturally important viruses. Despite their importance, the cell-to-cell spread of potyviruses remains poorly understood. Previous studies have shown that at early time points of infection, the virus-encoded CI protein, one of 11 known potyviral proteins, is associated with cone-shaped structures at plasmodesmata (PD) and is involved in viral cell-to-cell movement. In this paper, we show that a newly identified potyviral protein, P3N-PIPO, is a PD-located protein and directs the CI protein to PD, facilitating the deposition of the cone-shaped structures of CI at PD by interacting with CI protein. We demonstrate that the mutant of CI, which impairs potyviral cell-to-cell movement, loses its ability to accumulate at PD. We further reveal that P3N-PIPO utilizes the secretory pathway rather than the actomyosin motility system for trafficking to PD. Taken together, the data presented in this study suggest that CI and P3N-PIPO coordinates the formation of conical structure at PD for potyviral cell-to-cell spread.

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          Most cited references 38

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          Modular cloning in plant cells.

          New plant genes are being discovered at a rapid pace. Yet, in most cases, their precise function remains elusive. The recent advent of recombinational cloning techniques has significantly improved our ability to investigate gene functions systematically. For example, proteins fused with diverse fluorescent tags can be expressed at will using versatile cloning cassettes. In addition, novel binary T-DNA vectors are now available to assemble multiple DNA fragments simultaneously, which greatly facilitate plant cell and protein engineering.
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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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              The Big Bang of picorna-like virus evolution antedates the radiation of eukaryotic supergroups.

              The recent discovery of RNA viruses in diverse unicellular eukaryotes and developments in evolutionary genomics have provided the means for addressing the origin of eukaryotic RNA viruses. The phylogenetic analyses of RNA polymerases and helicases presented in this Analysis article reveal close evolutionary relationships between RNA viruses infecting hosts from the Chromalveolate and Excavate supergroups and distinct families of picorna-like viruses of plants and animals. Thus, diversification of picorna-like viruses probably occurred in a 'Big Bang' concomitant with key events of eukaryogenesis. The origins of the conserved genes of picorna-like viruses are traced to likely ancestors including bacterial group II retroelements, the family of HtrA proteases and DNA bacteriophages.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Pathog
                plos
                plospath
                PLoS Pathogens
                Public Library of Science (San Francisco, USA )
                1553-7366
                1553-7374
                June 2010
                June 2010
                24 June 2010
                : 6
                : 6
                Affiliations
                [1 ]Southern Crop Protection and Food Research Centre, Agriculture and Agri-Food Canada, London, Ontario, Canada
                [2 ]Department of Biology, The University of Western Ontario, London, Ontario, Canada
                [3 ]College of Horticulture, Nanjing Agricultural University, Nanjing, People's Republic of China
                [4 ]Center of Analysis and Measurement, Zhejiang University, Hangzhou, People's Republic of China
                [5 ]Center for Genome Research and Biocomputing, Oregon State University, Corvallis, Oregon, United States of America
                [6 ]Institute of Biotechnology, Zhejiang University, Hangzhou, People's Republic of China
                University of California San Diego, United States of America
                Author notes

                Conceived and designed the experiments: TW AW. Performed the experiments: TW CZ JH RX KDK. Analyzed the data: TW CZ JH RX KDK XZ JCC AW. Contributed reagents/materials/analysis tools: TW JCC AW. Wrote the paper: TW JCC AW.

                Article
                10-PLPA-RA-2547R2
                10.1371/journal.ppat.1000962
                2891837
                20585568
                5575b32f-cb35-404b-a357-fc6136d660fa
                Wei et al. 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.
                Page count
                Pages: 12
                Categories
                Research Article
                Virology/Host Invasion and Cell Entry

                Infectious disease & Microbiology

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