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      The exodomain of the impaired oomycete susceptibility 1 receptor mediates both endoplasmic reticulum stress responses and abscisic acid signalling during downy mildew infection of Arabidopsis

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          Abstract

          The phytohormone abscisic acid (ABA) regulates cell growth and plant development, and contributes to defence responses to pathogens. We previously showed that the Arabidopsis malectin‐like domain leucine‐rich repeat receptor‐like kinase (MLD‐LRR‐RLK) impaired oomycete susceptibility 1 (IOS1) attenuates ABA signalling during infection with the oomycete downy mildew pathogen Hyaloperonospora arabidopsidis. The exodomain of IOS1 with its MLD retains the receptor in the endoplasmic reticulum (ER), where it interacts with the ribophorin HAP6 to dampen a pathogen‐induced ER stress response called the unfolded protein response (UPR). The down‐regulation of both ABA and UPR signalling probably provides the pathogen with an advantage for infection. Here, we show that ABA‐related phenotypes of the ios1‐1 mutant, such as up‐regulated expression of ABA‐responsive genes and hypersensitivity to exogenous ABA application, were reverted by expression of the IOS1 exodomain in the mutant background. Furthermore, knockdown mutants for ER‐resident HAP6 showed similarly reduced UPR and ABA signalling, indicating that HAP6 positively regulates both pathways. Our data suggest that the IOS1 exodomain and HAP6 contribute in the ER to the IOS1‐mediated interference with ABA and UPR signalling.

          Abstract

          The extracellular (intra‐endoplasmic reticulum) domain of the Arabidopsis malectin‐like domain leucine‐rich repeat receptor‐like kinase impaired oomycete susceptibility 1 attenuates both abscisic acid and unfolded protein response signalling during downy mildew infection, thereby promoting oomycete establishment in plant tissues.

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          Most cited references41

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          The unfolded protein response: controlling cell fate decisions under ER stress and beyond.

          Protein-folding stress at the endoplasmic reticulum (ER) is a salient feature of specialized secretory cells and is also involved in the pathogenesis of many human diseases. ER stress is buffered by the activation of the unfolded protein response (UPR), a homeostatic signalling network that orchestrates the recovery of ER function, and failure to adapt to ER stress results in apoptosis. Progress in the field has provided insight into the regulatory mechanisms and signalling crosstalk of the three branches of the UPR, which are initiated by the stress sensors protein kinase RNA-like ER kinase (PERK), inositol-requiring protein 1α (IRE1α) and activating transcription factor 6 (ATF6). In addition, novel physiological outcomes of the UPR that are not directly related to protein-folding stress, such as innate immunity, metabolism and cell differentiation, have been revealed.
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            A dehydration-induced NAC protein, RD26, is involved in a novel ABA-dependent stress-signaling pathway.

            Arabidopsis thaliana RD26 cDNA, isolated from dehydrated plants, encodes a NAC protein. Expression of the RD26 gene was induced not only by drought but also by abscisic acid (ABA) and high salinity. The RD26 protein is localized in the nucleus and its C terminal has transcriptional activity. Transgenic plants overexpressing RD26 were highly sensitive to ABA, while RD26-repressed plants were insensitive. The results of microarray analysis showed that ABA- and stress-inducible genes are upregulated in the RD26-overexpressed plants and repressed in the RD26-repressed plants. Furthermore, RD26 activated a promoter of its target gene in Arabidopsis protoplasts. These results indicate that RD26 functions as a transcriptional activator in ABA-inducible gene expression under abiotic stress in plants.
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              Plant stomata function in innate immunity against bacterial invasion.

              Microbial entry into host tissue is a critical first step in causing infection in animals and plants. In plants, it has been assumed that microscopic surface openings, such as stomata, serve as passive ports of bacterial entry during infection. Surprisingly, we found that stomatal closure is part of a plant innate immune response to restrict bacterial invasion. Stomatal guard cells of Arabidopsis perceive bacterial surface molecules, which requires the FLS2 receptor, production of nitric oxide, and the guard-cell-specific OST1 kinase. To circumvent this innate immune response, plant pathogenic bacteria have evolved specific virulence factors to effectively cause stomatal reopening as an important pathogenesis strategy. We provide evidence that supports a model in which stomata, as part of an integral innate immune system, act as a barrier against bacterial infection.
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                Author and article information

                Contributors
                harald.keller@inrae.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
                14 September 2022
                December 2022
                : 23
                : 12 ( doiID: 10.1111/mpp.v23.12 )
                : 1783-1791
                Affiliations
                [ 1 ] Université Côte d'Azur, INRAE, CNRS, UMR1355‐7254, ISA Sophia Antipolis France
                Author notes
                [*] [* ] Correspondence

                Harald Keller, Université Côte d'Azur, INRAE, CNRS, UMR1355‐7254, ISA, 400 route des Chappes, 06903 Sophia Antipolis, France.

                Email: harald.keller@ 123456inrae.fr

                Author information
                https://orcid.org/0000-0003-1243-8467
                Article
                MPP13265 MPP-OA-22-148.R1
                10.1111/mpp.13265
                9644275
                36103373
                9a4df8fc-cbea-4259-8fdc-5d359c1d4983
                © 2022 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-nc-nd/4.0/ License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non‐commercial and no modifications or adaptations are made.

                History
                : 13 July 2022
                : 18 May 2022
                : 18 August 2022
                Page count
                Figures: 5, Tables: 0, Pages: 9, Words: 5707
                Funding
                Funded by: Agence Nationale de la Recherche , doi 10.13039/501100001665;
                Award ID: ANR‐11‐LABX‐0028‐01
                Categories
                Original Article
                Original Articles
                Custom metadata
                2.0
                December 2022
                Converter:WILEY_ML3GV2_TO_JATSPMC version:6.2.0 mode:remove_FC converted:09.11.2022

                Plant science & Botany
                abscisic acid,biotrophy,malectin‐like domain leucine‐rich repeat receptor‐like kinase (mld‐lrr‐rlk),unfolded protein response

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