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      The Tomato Prf Complex Is a Molecular Trap for Bacterial Effectors Based on Pto Transphosphorylation

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          Abstract

          The major virulence strategy of phytopathogenic bacteria is to secrete effector proteins into the host cell to target the immune machinery. AvrPto and AvrPtoB are two such effectors from Pseudomonas syringae, which disable an overlapping range of kinases in Arabidopsis and Tomato. Both effectors target surface-localized receptor-kinases to avoid bacterial recognition. In turn, tomato has evolved an intracellular effector-recognition complex composed of the NB-LRR protein Prf and the Pto kinase. Structural analyses have shown that the most important interaction surface for AvrPto and AvrPtoB is the Pto P+1 loop. AvrPto is an inhibitor of Pto kinase activity, but paradoxically, this kinase activity is a prerequisite for defense activation by AvrPto. Here using biochemical approaches we show that disruption of Pto P+1 loop stimulates phosphorylation in trans, which is possible because the Pto/Prf complex is oligomeric. Both P+1 loop disruption and transphosphorylation are necessary for signalling. Thus, effector perturbation of one kinase molecule in the complex activates another. Hence, the Pto/Prf complex is a sophisticated molecular trap for effectors that target protein kinases, an essential aspect of the pathogen's virulence strategy. The data presented here give a clear view of why bacterial virulence and host recognition mechanisms are so often related and how the slowly evolving host is able to keep pace with the faster-evolving pathogen.

          Author Summary

          The bacteria Pseudomonas syringae is a pathogen of many crop species and one of the model pathogens for studying plant and bacterial arms race coevolution. In the current model, plants perceive bacteria pathogens via plasma membrane receptors, and recognition leads to the activation of general defenses. In turn, bacteria inject proteins called effectors into the plant cell to prevent the activation of immune responses. AvrPto and AvrPtoB are two such proteins that inhibit multiple plant kinases. The tomato plant has reacted to these effectors by the evolution of a cytoplasmic resistance complex. This complex is compromised of two proteins, Prf and Pto kinase, and is capable of recognizing the effector proteins. How the Pto kinase is able to avoid inhibition by the effector proteins is currently unknown. Our data shows how the tomato plant utilizes dimerization of resistance proteins to gain advantage over the faster evolving bacterial pathogen. Here we illustrate that oligomerisation of Prf brings into proximity two Pto kinases allowing them to avoid inhibition by the effectors by transphosphorylation and to activate immune responses.

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          Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search.

          We present a statistical model to estimate the accuracy of peptide assignments to tandem mass (MS/MS) spectra made by database search applications such as SEQUEST. Employing the expectation maximization algorithm, the analysis learns to distinguish correct from incorrect database search results, computing probabilities that peptide assignments to spectra are correct based upon database search scores and the number of tryptic termini of peptides. Using SEQUEST search results for spectra generated from a sample of known protein components, we demonstrate that the computed probabilities are accurate and have high power to discriminate between correctly and incorrectly assigned peptides. This analysis makes it possible to filter large volumes of MS/MS database search results with predictable false identification error rates and can serve as a common standard by which the results of different research groups are compared.
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            Innate immunity in plants: an arms race between pattern recognition receptors in plants and effectors in microbial pathogens.

            For many years, research on a suite of plant defense responses that begin when plants are exposed to general microbial elicitors was underappreciated, for a good reason: There has been no critical experimental demonstration of their importance in mediating plant resistance during pathogen infection. Today, these microbial elicitors are named pathogen- or microbe-associated molecular patterns (PAMPs or MAMPs) and the plant responses are known as PAMP-triggered immunity (PTI). Recent studies provide an elegant explanation for the difficulty of demonstrating the role of PTI in plant disease resistance. It turns out that the important contribution of PTI to disease resistance is masked by pathogen virulence effectors that have evolved to suppress it.
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              Active and Inactive Protein Kinases: Structural Basis for Regulation

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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
                January 2013
                January 2013
                31 January 2013
                : 9
                : 1
                : e1003123
                Affiliations
                [1 ]School of Life Sciences, University of Warwick, Coventry, United Kingdom
                [2 ]The Sainsbury Laboratory, Norwich Research Park, Colney, United Kingdom
                The University of North Carolina at Chapel Hill, United States of America
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: VN ALB TSM JRG AMEJ JPR. Performed the experiments: VN ALB TSM JRG AMEJ. Analyzed the data: VN AMEJ JPR. Contributed reagents/materials/analysis tools: VN AMEJ JPR. Wrote the paper: VN JPR.

                [¤a]

                Current address: The University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of America.

                [¤b]

                Current address: Research School of Biology, The Australian National University, Acton, Australian Capital Territory, Australia.

                Article
                PPATHOGENS-D-12-01107
                10.1371/journal.ppat.1003123
                3561153
                23382672
                b533f04b-7900-4346-ac41-bf19f4b45573
                Copyright @ 2013

                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
                : 9 May 2012
                : 27 November 2012
                Page count
                Pages: 14
                Funding
                V. Ntoukakis is supported by the Royal Society. J.P. Rathjen was funded by the Biotechnology and Biological Science Research Council (grant number BB/D00456X/1) and the Gatsby Charitable Foundation, and is a Future Fellow of the Australian Research Council (FT0992129). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Agriculture
                Crops
                Crop Diseases
                Biology
                Biochemistry
                Plant Biochemistry
                Microbiology
                Plant Microbiology
                Molecular Cell Biology
                Signal Transduction
                Signaling in Selected Disciplines
                Plant Signaling
                Plant Cell Biology
                Plant Science

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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