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      Network Properties of Robust Immunity in Plants

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          Abstract

          Two modes of plant immunity against biotrophic pathogens, Effector Triggered Immunity (ETI) and Pattern-Triggered Immunity (PTI), are triggered by recognition of pathogen effectors and Microbe-Associated Molecular Patterns (MAMPs), respectively. Although the jasmonic acid (JA)/ethylene (ET) and salicylic acid (SA) signaling sectors are generally antagonistic and important for immunity against necrotrophic and biotrophic pathogens, respectively, their precise roles and interactions in ETI and PTI have not been clear. We constructed an Arabidopsis dde2/ ein2/ pad4/ sid2-quadruple mutant. DDE2, EIN2, and SID2 are essential components of the JA, ET, and SA sectors, respectively. The pad4 mutation affects the SA sector and a poorly characterized sector. Although the ETI triggered by the bacterial effector AvrRpt2 (AvrRpt2-ETI) and the PTI triggered by the bacterial MAMP flg22 (flg22-PTI) were largely intact in plants with mutations in any one of these genes, they were mostly abolished in the quadruple mutant. For the purposes of this study, AvrRpt2-ETI and flg22-PTI were measured as relative growth of Pseudomonas syringae bacteria within leaves. Immunity to the necrotrophic fungal pathogen Alternaria brassicicola was also severely compromised in the quadruple mutant. Quantitative measurements of the immunity levels in all combinatorial mutants and wild type allowed us to estimate the effects of the wild-type genes and their interactions on the immunity by fitting a mixed general linear model. This signaling allocation analysis showed that, contrary to current ideas, each of the JA, ET, and SA signaling sectors can positively contribute to immunity against both biotrophic and necrotrophic pathogens. The analysis also revealed that while flg22-PTI and AvrRpt2-ETI use a highly overlapping signaling network, the way they use the common network is very different: synergistic relationships among the signaling sectors are evident in PTI, which may amplify the signal; compensatory relationships among the sectors dominate in ETI, explaining the robustness of ETI against genetic and pathogenic perturbations.

          Author Summary

          Plants sense molecules originating from pathogens and turn on a battery of immune responses. Activation of immune responses is controlled by a complex network of signaling mechanisms. A traditional approach, knocking out one mechanism at a time, has revealed little about major parts of the signaling network involved in two forms of immunity, Effector-Triggered Immunity (ETI) and Pattern-Triggered Immunity (PTI). ETI and PTI are triggered by different types of pathogen molecules. By simultaneously knocking out four major signaling mechanisms in the network, we demonstrated that a common network comprised of the four signaling mechanisms accounts for most of ETI and PTI triggered by particular molecules. The common network was also important for another form of immunity. We also precisely measured how much each signaling mechanism contributes to ETI and PTI and studied how the signaling mechanisms work together. We found that signaling mechanisms work together synergistically in PTI, which may amplify the signal, while they back up one another in ETI to make the immune signaling highly resistant to pathogen attack (pathogens produce molecules that interfere with immune signaling). Therefore, different forms of plant immunity share the same signaling mechanisms, but they use the same mechanisms in very different ways.

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          Most cited references37

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          JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling.

          Jasmonate and related signalling compounds have a crucial role in both host immunity and development in plants, but the molecular details of the signalling mechanism are poorly understood. Here we identify members of the jasmonate ZIM-domain (JAZ) protein family as key regulators of jasmonate signalling. JAZ1 protein acts to repress transcription of jasmonate-responsive genes. Jasmonate treatment causes JAZ1 degradation and this degradation is dependent on activities of the SCF(COI1) ubiquitin ligase and the 26S proteasome. Furthermore, the jasmonoyl-isoleucine (JA-Ile) conjugate, but not other jasmonate-derivatives such as jasmonate, 12-oxo-phytodienoic acid, or methyl-jasmonate, promotes physical interaction between COI1 and JAZ1 proteins in the absence of other plant proteins. Our results suggest a model in which jasmonate ligands promote the binding of the SCF(COI1) ubiquitin ligase to and subsequent degradation of the JAZ1 repressor protein, and implicate the SCF(COI1)-JAZ1 protein complex as a site of perception of the plant hormone JA-Ile.
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            Isochorismate synthase is required to synthesize salicylic acid for plant defence.

            Salicylic acid (SA) mediates plant defences against pathogens, accumulating in both infected and distal leaves in response to pathogen attack. Pathogenesis-related gene expression and the synthesis of defensive compounds associated with both local and systemic acquired resistance (LAR and SAR) in plants require SA. In Arabidopsis, exogenous application of SA suffices to establish SAR, resulting in enhanced resistance to a variety of pathogens. However, despite its importance in plant defence against pathogens, SA biosynthesis is not well defined. Previous work has suggested that plants synthesize SA from phenylalanine; however, SA could still be produced when this pathway was inhibited, and the specific activity of radiolabelled SA in feeding experiments was often lower than expected. Some bacteria such as Pseudomonas aeruginosa synthesize SA using isochorismate synthase (ICS) and pyruvate lyase. Here we show, by cloning and characterizing an Arabidopsis defence-related gene (SID2) defined by mutation, that SA is synthesized from chorismate by means of ICS, and that SA made by this pathway is required for LAR and SAR responses.
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              Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation.

              Higher eukaryotes sense microbes through the perception of pathogen-associated molecular patterns (PAMPs). Arabidopsis plants detect a variety of PAMPs including conserved domains of bacterial flagellin and of bacterial EF-Tu. Here, we show that flagellin and EF-Tu activate a common set of signaling events and defense responses but without clear synergistic effects. Treatment with either PAMP results in increased binding sites for both PAMPs. We used this finding in a targeted reverse-genetic approach to identify a receptor kinase essential for EF-Tu perception, which we called EFR. Nicotiana benthamiana, a plant unable to perceive EF-Tu, acquires EF-Tu binding sites and responsiveness upon transient expression of EFR. Arabidopsis efr mutants show enhanced susceptibility to the bacterium Agrobacterium tumefaciens, as revealed by a higher efficiency of T-DNA transformation. These results demonstrate that EFR is the EF-Tu receptor and that plant defense responses induced by PAMPs such as EF-Tu reduce transformation by Agrobacterium.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Genet
                plos
                plosgen
                PLoS Genetics
                Public Library of Science (San Francisco, USA )
                1553-7390
                1553-7404
                December 2009
                December 2009
                11 December 2009
                : 5
                : 12
                : e1000772
                Affiliations
                [1 ]Department of Plant Biology, Microbial and Plant Genomics Institute, University of Minnesota, St. Paul, Minnesota, United States of America
                [2 ]Department of Life Sciences, Graduate School of Arts and Sciences, The University of Tokyo, Tokyo, Japan
                The University of North Carolina at Chapel Hill, United States of America
                Author notes

                Conceived and designed the experiments: KT JG FK. Performed the experiments: KT TS. Analyzed the data: KT MS FK. Wrote the paper: KT JG FK.

                Article
                09-PLGE-RA-1692R2
                10.1371/journal.pgen.1000772
                2782137
                20011122
                1e4afc8b-6ef0-4167-9ba8-29cdec0868f4
                Tsuda 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.
                History
                : 24 September 2009
                : 13 November 2009
                Page count
                Pages: 16
                Categories
                Research Article
                Genetics and Genomics/Plant Genetics and Gene Expression
                Mathematics/Statistics
                Plant Biology/Plant-Biotic Interactions

                Genetics
                Genetics

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