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      Epidermal chloroplasts are defense-related motile organelles equipped with plant immune components

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      1 , , 2
      Nature Communications
      Nature Publishing Group UK
      Chloroplasts, Microbe, Biotic

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          Abstract

          In addition to conspicuous large mesophyll chloroplasts, where most photosynthesis occurs, small epidermal chloroplasts have also been observed in plant leaves. However, the functional significance of this small organelle remains unclear. Here, we present evidence that Arabidopsis epidermal chloroplasts control the entry of fungal pathogens. In entry trials, specialized fungal cells called appressoria triggered dynamic movement of epidermal chloroplasts. This movement is controlled by common regulators of mesophyll chloroplast photorelocation movement, designated as the epidermal chloroplast response (ECR). The ECR occurs when the PEN2 myrosinase-related higher-layer antifungal system becomes ineffective, and blockage of the distinct steps of the ECR commonly decreases preinvasive nonhost resistance against fungi. Furthermore, immune components were preferentially localized to epidermal chloroplasts, contributing to antifungal nonhost resistance in the pen2 background. Our findings reveal that atypical small chloroplasts act as defense-related motile organelles by specifically positioning immune components in the plant epidermis, which is the first site of contact between the plant and pathogens. Thus, this work deepens our understanding of the functions of epidermal chloroplasts.

          Abstract

          Leaf epidermal cells contain small chloroplasts which likely contribute little to photosynthesis and whose function is unclear. Here the authors show that these chloroplasts move toward the leaf surface in response to invasion trials by non-adapted fungal pathogens and contribute to non-host resistance.

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          Most cited references74

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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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            Abscisic acid biosynthesis and catabolism.

            The level of abscisic acid (ABA) in any particular tissue in a plant is determined by the rate of biosynthesis and catabolism of the hormone. Therefore, identifying all the genes involved in the metabolism is essential for a complete understanding of how this hormone directs plant growth and development. To date, almost all the biosynthetic genes have been identified through the isolation of auxotrophic mutants. On the other hand, among several ABA catabolic pathways, current genomic approaches revealed that Arabidopsis CYP707A genes encode ABA 8'-hydroxylases, which catalyze the first committed step in the predominant ABA catabolic pathway. Identification of ABA metabolic genes has revealed that multiple metabolic steps are differentially regulated to fine-tune the ABA level at both transcriptional and post-transcriptional levels. Furthermore, recent ongoing studies have given new insights into the regulation and site of ABA metabolism in relation to its physiological roles.
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              A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence.

              Plants sense potential microbial invaders by using pattern-recognition receptors to recognize pathogen-associated molecular patterns (PAMPs). In Arabidopsis thaliana, the leucine-rich repeat receptor kinases flagellin-sensitive 2 (FLS2) (ref. 2) and elongation factor Tu receptor (EFR) (ref. 3) act as pattern-recognition receptors for the bacterial PAMPs flagellin and elongation factor Tu (EF-Tu) (ref. 5) and contribute to resistance against bacterial pathogens. Little is known about the molecular mechanisms that link receptor activation to intracellular signal transduction. Here we show that BAK1 (BRI1-associated receptor kinase 1), a leucine-rich repeat receptor-like kinase that has been reported to regulate the brassinosteroid receptor BRI1 (refs 6,7), is involved in signalling by FLS2 and EFR. Plants carrying bak1 mutations show normal flagellin binding but abnormal early and late flagellin-triggered responses, indicating that BAK1 acts as a positive regulator in signalling. The bak1-mutant plants also show a reduction in early, but not late, EF-Tu-triggered responses. The decrease in responses to PAMPs is not due to reduced sensitivity to brassinosteroids. We provide evidence that FLS2 and BAK1 form a complex in vivo, in a specific ligand-dependent manner, within the first minutes of stimulation with flagellin. Thus, BAK1 is not only associated with developmental regulation through the plant hormone receptor BRI1 (refs 6,7), but also has a functional role in PRR-dependent signalling, which initiates innate immunity.
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                Author and article information

                Contributors
                irieda@shinshu-u.ac.jp
                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group UK (London )
                2041-1723
                20 May 2021
                20 May 2021
                2021
                : 12
                : 2739
                Affiliations
                [1 ]GRID grid.263518.b, ISNI 0000 0001 1507 4692, Academic Assembly, Institute of Agriculture, , Shinshu University, ; Nagano, Japan
                [2 ]GRID grid.258799.8, ISNI 0000 0004 0372 2033, Graduate School of Agriculture, , Kyoto University, ; Kyoto, Japan
                Author information
                http://orcid.org/0000-0002-4545-9187
                Article
                22977
                10.1038/s41467-021-22977-5
                8137707
                34016974
                ea491d91-6b51-43c5-820f-442d06542d8f
                © The Author(s) 2021

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 18 August 2020
                : 6 April 2021
                Funding
                Funded by: FundRef https://doi.org/10.13039/501100001691, MEXT | Japan Society for the Promotion of Science (JSPS);
                Award ID: 15K18648
                Award ID: 18K05643
                Award ID: 18H02204
                Award Recipient :
                Funded by: Leading Initiative for Excellent Young Researchers (LEADER) program of MEXT
                Funded by: FundRef https://doi.org/10.13039/100007684, Asahi Glass Foundation;
                Categories
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                © The Author(s) 2021

                Uncategorized
                chloroplasts,microbe,biotic
                Uncategorized
                chloroplasts, microbe, biotic

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