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      Autophagy promotes jasmonate-mediated defense against nematodes

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          Abstract

          Autophagy, as an intracellular degradation system, plays a critical role in plant immunity. However, the involvement of autophagy in the plant immune system and its function in plant nematode resistance are largely unknown. Here, we show that root-knot nematode (RKN; Meloidogyne incognita) infection induces autophagy in tomato ( Solanum lycopersicum) and different atg mutants exhibit high sensitivity to RKNs. The jasmonate (JA) signaling negative regulators JASMONATE-ASSOCIATED MYC2-LIKE 1 (JAM1), JAM2 and JAM3 interact with ATG8s via an ATG8-interacting motif (AIM), and JAM1 is degraded by autophagy during RKN infection. JAM1 impairs the formation of a transcriptional activation complex between ETHYLENE RESPONSE FACTOR 1 (ERF1) and MEDIATOR 25 (MED25) and interferes with transcriptional regulation of JA-mediated defense-related genes by ERF1. Furthermore, ERF1 acts in a positive feedback loop and regulates autophagy activity by transcriptionally activating ATG expression in response to RKN infection. Therefore, autophagy promotes JA-mediated defense against RKNs via forming a positive feedback circuit in the degradation of JAMs and transcriptional activation by ERF1.

          Abstract

          Autophagy plays a critical role in plant immunity. Here the authors show that in tomato, autophagy promotes defense against root-knot nematodes by promoting degradation of negative regulators of jasmonic acid signaling.

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          Most cited references71

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          Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method.

          The two most commonly used methods to analyze data from real-time, quantitative PCR experiments are absolute quantification and relative quantification. Absolute quantification determines the input copy number, usually by relating the PCR signal to a standard curve. Relative quantification relates the PCR signal of the target transcript in a treatment group to that of another sample such as an untreated control. The 2(-Delta Delta C(T)) method is a convenient way to analyze the relative changes in gene expression from real-time quantitative PCR experiments. The purpose of this report is to present the derivation, assumptions, and applications of the 2(-Delta Delta C(T)) method. In addition, we present the derivation and applications of two variations of the 2(-Delta Delta C(T)) method that may be useful in the analysis of real-time, quantitative PCR data. Copyright 2001 Elsevier Science (USA).
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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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              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
                jie@zju.edu.cn
                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group UK (London )
                2041-1723
                8 August 2023
                8 August 2023
                2023
                : 14
                : 4769
                Affiliations
                [1 ]GRID grid.13402.34, ISNI 0000 0004 1759 700X, Department of Horticulture, Zhejiang Provincial Key Laboratory of Horticultural Plant Integrative Biology, , Zhejiang University, ; Yuhangtang Road 866, 310058 Hangzhou, China
                [2 ]GRID grid.13402.34, ISNI 0000 0004 1759 700X, Hainan Institute, , Zhejiang University, ; 572000 Sanya, China
                [3 ]GRID grid.13402.34, ISNI 0000 0004 1759 700X, Agricultural Experiment Station, , Zhejiang University, ; 310058 Hangzhou, China
                [4 ]Key Laboratory of Horticultural Plants Growth, Development and Quality Improvement, Ministry of Agriculture and Rural Affairs of China, Yuhangtang Road 866, 310058 Hangzhou, China
                [5 ]GRID grid.13402.34, ISNI 0000 0004 1759 700X, Shandong (Linyi) Institute of Modern Agriculture, , Zhejiang University, ; 276000 Linyi, China
                [6 ]GRID grid.16821.3c, ISNI 0000 0004 0368 8293, Shanghai Collaborative Innovation Center of Agri-Seeds, Joint Center for Single Cell Biology, School of Agriculture and Biology, , Shanghai Jiao Tong University, ; 200240 Shanghai, China
                [7 ]GRID grid.34421.30, ISNI 0000 0004 1936 7312, Department of Genetics, Development and Cell Biology, , Iowa State University, ; Ames, IA 50011 USA
                Author information
                http://orcid.org/0000-0001-7411-9360
                http://orcid.org/0000-0002-7626-1165
                http://orcid.org/0000-0002-8797-7214
                Article
                40472
                10.1038/s41467-023-40472-x
                10409745
                37553319
                4ce8b917-c2e3-4d2b-abdc-e69bd58602b6
                © Springer Nature Limited 2023

                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
                : 23 December 2022
                : 28 July 2023
                Funding
                Funded by: FundRef https://doi.org/10.13039/501100001809, National Natural Science Foundation of China (National Science Foundation of China);
                Award ID: 32272790, 31922078 and 31872089
                Award ID: 32020103013
                Award Recipient :
                Funded by: FundRef https://doi.org/10.13039/100000001, National Science Foundation (NSF);
                Award ID: MCB-2040582
                Award Recipient :
                Categories
                Article
                Custom metadata
                © Springer Nature Limited 2023

                Uncategorized
                biotic,plant signalling,autophagy
                Uncategorized
                biotic, plant signalling, autophagy

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