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      TOR-autophagy branch signaling via Imp1 dictates plant-microbe biotrophic interface longevity

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          There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

          Abstract

          Like other intracellular eukaryotic phytopathogens, the devastating rice blast fungus Magnaporthe ( Pyricularia) oryzae first infects living host cells by elaborating invasive hyphae (IH) surrounded by a plant-derived membrane. This forms an extended biotrophic interface enclosing an apoplastic compartment into which fungal effectors can be deployed to evade host detection. M. oryzae also forms a focal, plant membrane-rich structure, the biotrophic interfacial complex (BIC), that accumulates cytoplasmic effectors for translocation into host cells. Molecular decision-making processes integrating fungal growth and metabolism in host cells with interface function and dynamics are unknown. Here, we report unanticipated roles for the M. oryzae Target-of-Rapamycin (TOR) nutrient-signaling pathway in mediating plant-fungal biotrophic interface membrane integrity. Through a forward genetics screen for M. oryzae mutant strains resistant to the specific TOR kinase inhibitor rapamycin, we discovered IMP1 encoding a novel vacuolar protein required for membrane trafficking, V-ATPase assembly, organelle acidification and autophagy induction. During infection, Δ imp1 deletants developed intracellular IH in the first infected rice cell following cuticle penetration. However, fluorescently labeled effector probes revealed that interface membrane integrity became compromised as biotrophy progressed, abolishing the BIC and releasing apoplastic effectors into host cytoplasm. Growth between rice cells was restricted. TOR-independent autophagy activation in Δ imp1 deletants (following infection) remediated interface function and cell-to-cell growth. Autophagy inhibition in wild type (following infection) recapitulated Δ imp1. In addition to vacuoles, Imp1 GFP localized to IH membranes in an autophagy-dependent manner. Collectively, our results suggest TOR-Imp1-autophagy branch signaling mediates membrane homeostasis to prevent catastrophic erosion of the biotrophic interface, thus facilitating fungal growth in living rice cells. The significance of this work lays in elaborating a novel molecular mechanism of infection stressing the dominance of fungal metabolism and metabolic control in sustaining long-term plant-microbe interactions. This work also has implications for understanding the enigmatic biotrophy to necrotrophy transition.

          Author summary

          Plant-associated fungi can form intimate connections with living host cells. Clarifying the molecular drivers of these interactions, and which partner is dominant, might be important in understanding how beneficial plant-fungal relationships can be enhanced to improve crop yields while pathogenic interactions that threaten crop health are disrupted. In common with other symbionts and phytopathogens, the devastating rice blast fungus Magnaporthe oryzae elaborates invasive hyphae in living host cells surrounded by plant-derived membranes. Nothing is known at the molecular signaling level about how such plant-microbe biotrophic interfacial zones are maintained as the fungus grows in and between host cells. Here, we report that fungal membrane trafficking processes controlled by nutrient signaling pathways are critical for maintaining biotrophic interface integrity during M. oryzae growth in rice cells. Impairing these processes resulted in erosion of the plant-microbe interface and failure of the fungus to thrive. To our knowledge, this work presents the first evidence indicating that the fungal partner is dominant in propagating the plant-microbe boundary. This suggests that the biotrophic interface is a fungal construct and provides clues on how such interfaces might be modulated to benefit the host plant.

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          Most cited references 76

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          Autophagy: process and function.

          Autophagy is an intracellular degradation system that delivers cytoplasmic constituents to the lysosome. Despite its simplicity, recent progress has demonstrated that autophagy plays a wide variety of physiological and pathophysiological roles, which are sometimes complex. Autophagy consists of several sequential steps--sequestration, transport to lysosomes, degradation, and utilization of degradation products--and each step may exert different function. In this review, the process of autophagy is summarized, and the role of autophagy is discussed in a process-based manner.
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            Molecular mechanisms of mTOR-mediated translational control.

             John Blenis,  X Ma (2009)
            The process of translation requires substantial cellular resources. Cells have therefore evolved complex mechanisms to control overall protein synthesis as well as the translation of specific mRNAs that are crucial for cell growth and proliferation. At the heart of this process is the mammalian target of rapamycin (mTOR) signalling pathway, which senses and responds to nutrient availability, energy sufficiency, stress, hormones and mitogens to modulate protein synthesis. Here, we highlight recent findings on the regulators and effectors of mTOR and discuss specific cases that serve as paradigms for the different modes of mTOR regulation and its control of translation.
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              The genome sequence of the rice blast fungus Magnaporthe grisea.

              Magnaporthe grisea is the most destructive pathogen of rice worldwide and the principal model organism for elucidating the molecular basis of fungal disease of plants. Here, we report the draft sequence of the M. grisea genome. Analysis of the gene set provides an insight into the adaptations required by a fungus to cause disease. The genome encodes a large and diverse set of secreted proteins, including those defined by unusual carbohydrate-binding domains. This fungus also possesses an expanded family of G-protein-coupled receptors, several new virulence-associated genes and large suites of enzymes involved in secondary metabolism. Consistent with a role in fungal pathogenesis, the expression of several of these genes is upregulated during the early stages of infection-related development. The M. grisea genome has been subject to invasion and proliferation of active transposable elements, reflecting the clonal nature of this fungus imposed by widespread rice cultivation.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: MethodologyRole: SoftwareRole: VisualizationRole: Writing – review & editing
                Role: Data curationRole: InvestigationRole: MethodologyRole: ResourcesRole: SoftwareRole: ValidationRole: Visualization
                Role: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: ValidationRole: Writing – original draftRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS Genet
                PLoS Genet
                plos
                plosgen
                PLoS Genetics
                Public Library of Science (San Francisco, CA USA )
                1553-7390
                1553-7404
                21 November 2018
                November 2018
                : 14
                : 11
                Affiliations
                [1 ] Department of Plant Pathology, University of Nebraska-Lincoln, Lincoln, Nebraska, United States of America
                [2 ] Department of Agronomy and Horticulture, University of Nebraska-Lincoln, Lincoln, Nebraska, United States of America
                Max-Planck-Institut fur Evolutionsbiologie, GERMANY
                Author notes

                The authors have declared that no competing interests exist.

                Article
                PGENETICS-D-18-00696
                10.1371/journal.pgen.1007814
                6281275
                30462633
                © 2018 Sun 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
                Figures: 11, Tables: 0, Pages: 45
                Product
                Funding
                This work was supported by funding from the National Science Foundation (IOS-1557943) to RAW. The Chinese Scholarship Council supported GS. 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
                Cell Processes
                Cell Death
                Autophagic Cell Death
                Biology and Life Sciences
                Organisms
                Eukaryota
                Plants
                Grasses
                Rice
                Research and Analysis Methods
                Animal Studies
                Experimental Organism Systems
                Plant and Algal Models
                Rice
                Biology and Life Sciences
                Cell Biology
                Cellular Structures and Organelles
                Vacuoles
                Biology and Life Sciences
                Cell Biology
                Cellular Structures and Organelles
                Cell Membranes
                Biology and life sciences
                Cell biology
                Signal transduction
                Cell signaling
                TOR signaling
                Biology and Life Sciences
                Cell Biology
                Plant Cell Biology
                Plant Vacuoles
                Biology and Life Sciences
                Plant Science
                Plant Cell Biology
                Plant Vacuoles
                Biology and Life Sciences
                Cell Biology
                Cellular Structures and Organelles
                Vacuoles
                Plant Vacuoles
                Biology and Life Sciences
                Plant Science
                Plant Anatomy
                Leaves
                Biology and Life Sciences
                Cell Biology
                Cell Physiology
                Membrane Trafficking
                Custom metadata
                vor-update-to-uncorrected-proof
                2018-12-05
                All relevant data are within the paper and its Supporting Information files.

                Genetics

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