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      Nucleotide‐binding leucine‐rich repeat network underlies nonhost resistance of pepper against the Irish potato famine pathogen Phytophthora infestans

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          Summary

          Nonhost resistance (NHR) is a robust plant immune response against non‐adapted pathogens. A number of nucleotide‐binding leucine‐rich repeat (NLR) proteins that recognize non‐adapted pathogens have been identified, although the underlying molecular mechanisms driving robustness of NHR are still unknown. Here, we screened 57 effectors of the potato late blight pathogen Phytophthora infestans in nonhost pepper ( Capsicum annuum) to identify avirulence effector candidates. Selected effectors were tested against 436 genome‐wide cloned pepper NLRs, and we identified multiple functional NLRs that recognize P. infestans effectors and confer disease resistance in the Nicotiana benthamiana as a surrogate system. The identified NLRs were homologous to known NLRs derived from wild potatoes that recognize P. infestans effectors such as Avr2, Avrblb1, Avrblb2, and Avrvnt1. The identified Ca Rpi‐blb2 is a homologue of Rpi‐blb2, recognizes Avrblb2 family effectors, exhibits feature of lineage‐specifically evolved gene in microsynteny and phylogenetic analyses, and requires pepper‐specific NRC (NLR required for cell death)‐type helper NLR for proper function. Moreover, CaRpi‐blb2–mediated hypersensitive response and blight resistance were more tolerant to suppression by the PITG_15 278 than those mediated by Rpi‐blb2. Combined results indicate that pepper has stacked multiple NLRs recognizing effectors of non‐adapted P. infestans, and these NLRs could be more tolerant to pathogen‐mediated immune suppression than NLRs derived from the host plants. Our study suggests that NLRs derived from nonhost plants have potential as untapped resources to develop crops with durable resistance against fast‐evolving pathogens by stacking the network of nonhost NLRs into susceptible host plants.

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          Most cited references65

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          MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets.

          We present the latest version of the Molecular Evolutionary Genetics Analysis (Mega) software, which contains many sophisticated methods and tools for phylogenomics and phylomedicine. In this major upgrade, Mega has been optimized for use on 64-bit computing systems for analyzing larger datasets. Researchers can now explore and analyze tens of thousands of sequences in Mega The new version also provides an advanced wizard for building timetrees and includes a new functionality to automatically predict gene duplication events in gene family trees. The 64-bit Mega is made available in two interfaces: graphical and command line. The graphical user interface (GUI) is a native Microsoft Windows application that can also be used on Mac OS X. The command line Mega is available as native applications for Windows, Linux, and Mac OS X. They are intended for use in high-throughput and scripted analysis. Both versions are available from www.megasoftware.net free of charge.
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            Plant immunity: towards an integrated view of plant-pathogen interactions.

            Plants are engaged in a continuous co-evolutionary struggle for dominance with their pathogens. The outcomes of these interactions are of particular importance to human activities, as they can have dramatic effects on agricultural systems. The recent convergence of molecular studies of plant immunity and pathogen infection strategies is revealing an integrated picture of the plant-pathogen interaction from the perspective of both organisms. Plants have an amazing capacity to recognize pathogens through strategies involving both conserved and variable pathogen elicitors, and pathogens manipulate the defence response through secretion of virulence effector molecules. These insights suggest novel biotechnological approaches to crop protection.
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              Effector-triggered immunity: from pathogen perception to robust defense.

              In plant innate immunity, individual cells have the capacity to sense and respond to pathogen attack. Intracellular recognition mechanisms have evolved to intercept perturbations by pathogen virulence factors (effectors) early in host infection and convert it to rapid defense. One key to resistance success is a polymorphic family of intracellular nucleotide-binding/leucine-rich-repeat (NLR) receptors that detect effector interference in different parts of the cell. Effector-activated NLRs connect, in various ways, to a conserved basal resistance network in order to transcriptionally boost defense programs. Effector-triggered immunity displays remarkable robustness against pathogen disturbance, in part by employing compensatory mechanisms within the defense network. Also, the mobility of some NLRs and coordination of resistance pathways across cell compartments provides flexibility to fine-tune immune outputs. Furthermore, a number of NLRs function close to the nuclear chromatin by balancing actions of defense-repressing and defense-activating transcription factors to program cells dynamically for effective disease resistance.
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                Author and article information

                Contributors
                doil@snu.ac.kr
                Journal
                Plant Biotechnol J
                Plant Biotechnol J
                10.1111/(ISSN)1467-7652
                PBI
                Plant Biotechnology Journal
                John Wiley and Sons Inc. (Hoboken )
                1467-7644
                1467-7652
                13 March 2023
                July 2023
                : 21
                : 7 ( doiID: 10.1111/pbi.v21.7 )
                : 1361-1372
                Affiliations
                [ 1 ] Plant Immunity Research Center, College of Agriculture and Life Sciences Seoul National University Seoul South Korea
                [ 2 ] Department of Agriculture, Forestry and Bioresources, Plant Genomics and Breeding Institute, College of Agriculture and Life Sciences Seoul National University Seoul South Korea
                [ 3 ] The Sainsbury Laboratory University of East Anglia, Norwich Research Park Norwich UK
                [ 4 ] Department of Horticulture, Division of Smart Horticulture Yonam University Cheonan South Korea
                [ 5 ] Korean Research Institute of Bioscience & Biotechnology (KRIBB) Daejeon South Korea
                [ 6 ]Present address: Institute of Plant and Microbial Biology, Academia Sinica Taipei Taiwan
                Author notes
                [*] [* ] Correspondence (Tel +82 2‐880‐4568; fax +82 2‐877‐4634; email doil@ 123456snu.ac.kr )
                Author information
                https://orcid.org/0000-0003-0003-588X
                https://orcid.org/0000-0002-4366-3627
                Article
                PBI14039 PBI-01096-2022.R2
                10.1111/pbi.14039
                10281606
                36912620
                9f31d885-31ea-4453-a25f-8afed527dc37
                © 2023 The Authors. Plant Biotechnology Journal published by Society for Experimental Biology and The Association of Applied Biologists 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
                : 20 February 2023
                : 17 September 2022
                : 28 February 2023
                Page count
                Figures: 6, Tables: 0, Pages: 1372, Words: 11395
                Funding
                Funded by: National Research Foundation of Korea , doi 10.13039/501100003725;
                Award ID: 2018R1A5A1023599
                Award ID: 2021R1A2B5B03001613
                Categories
                Research Article
                Research Articles
                Custom metadata
                2.0
                July 2023
                Converter:WILEY_ML3GV2_TO_JATSPMC version:6.2.9 mode:remove_FC converted:20.06.2023

                Biotechnology
                nonhost resistance,solanaceae,potato late blight,nucleotide‐binding leucine‐rich repeats network,robustness

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