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      Apoplastic invasion patterns triggering plant immunity: plasma membrane sensing at the frontline

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          Summary

          Plants are able to effectively cope with invading pathogens by activating an immune response based on the detection of invasion patterns (IPs) originating from the pathogen or released by the plant after infection. At a first level, this perception takes place at the plasma membrane through cell surface immune receptors and although the involvement of proteinaceous pattern recognition receptors (PRRs) is well established, increasing data are also pointing out the role of membrane lipids in the sensing of IPs. In this review, we discuss the evolution of various conceptual models describing plant immunity and present an overview of well‐characterized IPs from different natures and origins. We summarize the current knowledge on how they are perceived by plants at the plasma membrane, highlighting the increasingly apparent diversity of sentinel‐related systems in plants.

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          Most cited references134

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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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            Regulation of pattern recognition receptor signalling in plants.

            Recognition of pathogen-derived molecules by pattern recognition receptors (PRRs) is a common feature of both animal and plant innate immune systems. In plants, PRR signalling is initiated at the cell surface by kinase complexes, resulting in the activation of immune responses that ward off microorganisms. However, the activation and amplitude of innate immune responses must be tightly controlled. In this Review, we summarize our knowledge of the early signalling events that follow PRR activation and describe the mechanisms that fine-tune immune signalling to maintain immune homeostasis. We also illustrate the mechanisms used by pathogens to inhibit innate immune signalling and discuss how the innate ability of plant cells to monitor the integrity of key immune components can lead to autoimmune phenotypes following genetic or pathogen-induced perturbations of these components.
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              CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis.

              Chitin is a major component of fungal cell walls and serves as a microbe-associated molecular pattern (MAMP) for the detection of various potential pathogens in innate immune systems of both plants and animals. We recently showed that chitin elicitor-binding protein (CEBiP), plasma membrane glycoprotein with LysM motifs, functions as a cell surface receptor for chitin elicitor in rice. The predicted structure of CEBiP does not contain any intracellular domains, suggesting that an additional component(s) is required for signaling through the plasma membrane into the cytoplasm. Here, we identified a receptor-like kinase, designated CERK1, which is essential for chitin elicitor signaling in Arabidopsis. The KO mutants for CERK1 completely lost the ability to respond to the chitin elicitor, including MAPK activation, reactive oxygen species generation, and gene expression. Disease resistance of the KO mutant against an incompatible fungus, Alternaria brassicicola, was partly impaired. Complementation with the WT CERK1 gene showed cerk1 mutations were responsible for the mutant phenotypes. CERK1 is a plasma membrane protein containing three LysM motifs in the extracellular domain and an intracellular Ser/Thr kinase domain with autophosphorylation/myelin basic protein kinase activity, suggesting that CERK1 plays a critical role in fungal MAMP perception in plants.
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                Author and article information

                Contributors
                stephan.dorey@univ-reims.fr
                Journal
                Mol Plant Pathol
                Mol. Plant Pathol
                10.1111/(ISSN)1364-3703
                MPP
                Molecular Plant Pathology
                John Wiley and Sons Inc. (Hoboken )
                1464-6722
                1364-3703
                28 July 2019
                November 2019
                : 20
                : 11 ( doiID: 10.1111/mpp.v20.11 )
                : 1602-1616
                Affiliations
                [ 1 ] University of Reims Champagne‐Ardenne RIBP EA 4707, SFR Condorcet FR CNRS 3417 Reims 51100 France
                Author notes
                [*] [* ] Correspondence: Email: stephan.dorey@ 123456univ-reims.fr

                [†]

                These authors contributed equally to this work.

                Author information
                https://orcid.org/0000-0002-9583-2824
                Article
                MPP12857
                10.1111/mpp.12857
                6804340
                31353775
                d060a443-28a7-4343-880d-9d584eec6fe8
                © 2019 The Authors. Molecular Plant Pathology published by British Society for Plant Pathology and John Wiley & Sons Ltd

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                Page count
                Figures: 1, Tables: 1, Pages: 15, Words: 41174
                Categories
                Microreview
                Microreview
                Custom metadata
                2.0
                mpp12857
                November 2019
                Converter:WILEY_ML3GV2_TO_NLMPMC version:5.7.0 mode:remove_FC converted:22.10.2019

                Plant science & Botany
                invasion patterns,lipids,pattern‐triggered immunity,plasma membrane,prr
                Plant science & Botany
                invasion patterns, lipids, pattern‐triggered immunity, plasma membrane, prr

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