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      The Ustilago maydis Effector Pep1 Suppresses Plant Immunity by Inhibition of Host Peroxidase Activity

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          Abstract

          The corn smut Ustilago maydis establishes a biotrophic interaction with its host plant maize. This interaction requires efficient suppression of plant immune responses, which is attributed to secreted effector proteins. Previously we identified Pep1 (Protein essential during penetration-1) as a secreted effector with an essential role for U. maydis virulence. pep1 deletion mutants induce strong defense responses leading to an early block in pathogenic development of the fungus. Using cytological and functional assays we show that Pep1 functions as an inhibitor of plant peroxidases. At sites of Δ pep1 mutant penetrations, H 2O 2 strongly accumulated in the cell walls, coinciding with a transcriptional induction of the secreted maize peroxidase POX12. Pep1 protein effectively inhibited the peroxidase driven oxidative burst and thereby suppresses the early immune responses of maize. Moreover, Pep1 directly inhibits peroxidases in vitro in a concentration-dependent manner. Using fluorescence complementation assays, we observed a direct interaction of Pep1 and the maize peroxidase POX12 in vivo. Functional relevance of this interaction was demonstrated by partial complementation of the Δ pep1 mutant defect by virus induced gene silencing of maize POX12. We conclude that Pep1 acts as a potent suppressor of early plant defenses by inhibition of peroxidase activity. Thus, it represents a novel strategy for establishing a biotrophic interaction.

          Author Summary

          The maize pathogen U. maydis establishes a biotrophic interaction with its host plant and causes the formation of plant tumors. The U. maydis infection is initiated by a direct penetration of the plant epidermis and relies on living plant tissue. Therefore, suppression of the host immune system is essential for successful infection. Previously we identified the secreted effector Pep1, which is essential for U. maydis pathogenicity. pep1 deletion mutants are blocked by host defense responses immediately upon penetration. In the present study we identified the molecular function of Pep1 and explain its crucial role for fungal virulence. We found that Pep1 inhibits the plant oxidative burst, which is characterized by the accumulation of reactive oxygen species (ROS) such as hydrogen peroxide. A conserved component of the plant ROS generating system are peroxidases. We could show that Pep1 directly inhibits plant peroxidases. One specific maize peroxidase (POX12), which was strongly induced by infection of the pep1 deletion, directly interacts with POX12 in vivo. Moreover, POX12 silenced plants are penetrated by the pep1 deletion mutant, indicating functional relevance of the Pep1-POX12 interaction. Together, these findings show that Pep1 directly interferes with the ROS-generating system of the host plant to suppress immune responses.

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          Most cited references 69

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          THE OXIDATIVE BURST IN PLANT DISEASE RESISTANCE.

          Rapid generation of superoxide and accumulation of H2O2 is a characteristic early feature of the hypersensitive response following perception of pathogen avirulence signals. Emerging data indicate that the oxidative burst reflects activation of a membrane-bound NADPH oxidase closely resembling that operating in activated neutrophils. The oxidants are not only direct protective agents, but H2O2 also functions as a substrate for oxidative cross-linking in the cell wall, as a threshold trigger for hypersensitive cell death, and as a diffusible signal for induction of cellular protectant genes in surrounding cells. Activation of the oxidative burst is a central component of a highly amplified and integrated signal system, also involving salicylic acid and perturbations of cytosolic Ca2+, which underlies the expression of disease-resistance mechanisms.
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            Reactive oxygen species produced by NADPH oxidase regulate plant cell growth.

            Cell expansion is a central process in plant morphogenesis, and the elongation of roots and root hairs is essential for uptake of minerals and water from the soil. Ca2+ influx from the extracellular store is required for (and sets the rates of) cell elongation in roots. Arabidopsis thaliana rhd2 mutants are defective in Ca2+ uptake and consequently cell expansion is compromised--rhd2 mutants have short root hairs and stunted roots. To determine the regulation of Ca2+ acquisition in growing root cells we show here that RHD2 is an NADPH oxidase, a protein that transfers electrons from NADPH to an electron acceptor leading to the formation of reactive oxygen species (ROS). We show that ROS accumulate in growing wild-type (WT) root hairs but their levels are markedly decreased in rhd2 mutants. Blocking the activity of the NADPH oxidase with diphenylene iodonium (DPI) inhibits ROS formation and phenocopies Rhd2-. Treatment of rhd2 roots with ROS partly suppresses the mutant phenotype and stimulates the activity of plasma membrane hyperpolarization-activated Ca2+ channels, the predominant root Ca2+ acquisition system. This indicates that NADPH oxidases control development by making ROS that regulate plant cell expansion through the activation of Ca2+ channels.
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              Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis.

              Ustilago maydis is a ubiquitous pathogen of maize and a well-established model organism for the study of plant-microbe interactions. This basidiomycete fungus does not use aggressive virulence strategies to kill its host. U. maydis belongs to the group of biotrophic parasites (the smuts) that depend on living tissue for proliferation and development. Here we report the genome sequence for a member of this economically important group of biotrophic fungi. The 20.5-million-base U. maydis genome assembly contains 6,902 predicted protein-encoding genes and lacks pathogenicity signatures found in the genomes of aggressive pathogenic fungi, for example a battery of cell-wall-degrading enzymes. However, we detected unexpected genomic features responsible for the pathogenicity of this organism. Specifically, we found 12 clusters of genes encoding small secreted proteins with unknown function. A significant fraction of these genes exists in small gene families. Expression analysis showed that most of the genes contained in these clusters are regulated together and induced in infected tissue. Deletion of individual clusters altered the virulence of U. maydis in five cases, ranging from a complete lack of symptoms to hypervirulence. Despite years of research into the mechanism of pathogenicity in U. maydis, no 'true' virulence factors had been previously identified. Thus, the discovery of the secreted protein gene clusters and the functional demonstration of their decisive role in the infection process illuminate previously unknown mechanisms of pathogenicity operating in biotrophic fungi. Genomic analysis is, similarly, likely to open up new avenues for the discovery of virulence determinants in other pathogens.
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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
                May 2012
                May 2012
                10 May 2012
                : 8
                : 5
                Affiliations
                [1 ]Max Planck Institute for Terrestrial Microbiology, Marburg, Germany
                [2 ]Institute of Plant Sciences, Karl-Franzens University of Graz, Graz, Austria
                Purdue University, United States of America
                Author notes

                Conceived and designed the experiments: C. Hemetsberger C. Herrberger G. Doehlemann. Performed the experiments: C. Hemetsberger C. Herrberger B. Zechmann M. Hillmer. Analyzed the data: C. Hemetsberger C. Herrberger B. Zechmann G. Doehlemann. Wrote the paper: C. Hemetsberger C. Herrberger G. Doehlemann.

                Article
                PPATHOGENS-D-11-02600
                10.1371/journal.ppat.1002684
                3349748
                22589719
                Hemetsberger 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: 14
                Categories
                Research Article
                Biology
                Microbiology
                Host-Pathogen Interaction
                Microbial Pathogens
                Pathogenesis
                Plant Science
                Plant Pathology
                Plant Pathogens

                Infectious disease & Microbiology

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