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      Verticillium dahliae secreted protein Vd424Y is required for full virulence, targets the nucleus of plant cells, and induces cell death

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          Abstract

          Fungal pathogens secrete effector proteins that regulate host immunity and can suppress basal defence mechanisms against colonization in plants. Verticillium dahliae is a widespread and destructive soilborne fungus that can cause vascular wilt disease and reduces plant yields. However, little is currently known about how the effectors secreted by Vdahliae function. In this study, we analysed and identified 34 candidate effectors in the Vdahliae secretome and found that Vd424Y, a glycoside hydrolase family 11 protein, was highly upregulated during the early stages of Vdahliae infection in cotton plants. This protein was located in the nucleus and its deletion compromised the virulence of the fungus. The transient expression of Vd424Y in Nicotiana benthamiana induced BAK1‐ and SOBIR1‐dependent cell death and activated both salicylic acid and jasmonic acid signalling. This enhanced its resistance to the oomycetes Phytophthora capsici in a way that depended on its nuclear localization signal and signal peptides. Our results demonstrate that Vd424Y is an important effector protein targeting the host nucleus to regulate and activate effector‐triggered immunity in plants.

          Abstract

          Vd424Y is an important effector protein targeting the host nucleus to regulate and activate effector‐triggered immunity in plants.

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          Most cited references57

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          Pathogen recognition and innate immunity.

          Microorganisms that invade a vertebrate host are initially recognized by the innate immune system through germline-encoded pattern-recognition receptors (PRRs). Several classes of PRRs, including Toll-like receptors and cytoplasmic receptors, recognize distinct microbial components and directly activate immune cells. Exposure of immune cells to the ligands of these receptors activates intracellular signaling cascades that rapidly induce the expression of a variety of overlapping and unique genes involved in the inflammatory and immune responses. New insights into innate immunity are changing the way we think about pathogenesis and the treatment of infectious diseases, allergy, and autoimmunity.
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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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              The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants.

              In pathogen-associated molecular pattern (PAMP)-triggered immunity (PTI), plant cell surface receptors sense potential microbial pathogens by recognizing elicitors called PAMPs. Although diverse PAMPs trigger PTI through distinct receptors, the resulting intracellular responses overlap extensively. Despite this, a common component(s) linking signal perception with transduction remains unknown. In this study, we identify SOMATIC EMBRYOGENESIS RECEPTOR KINASE (SERK)3/brassinosteroid-associated kinase (BAK)1, a receptor-like kinase previously implicated in hormone signaling, as a component of plant PTI. In Arabidopsis thaliana, AtSERK3/BAK1 rapidly enters an elicitor-dependent complex with FLAGELLIN SENSING 2 (FLS2), the receptor for the bacterial PAMP flagellin and its peptide derivative flg22. In the absence of AtSERK3/BAK1, early flg22-dependent responses are greatly reduced in both A. thaliana and Nicotiana benthamiana. Furthermore, N. benthamiana Serk3/Bak1 is required for full responses to unrelated PAMPs and, importantly, for restriction of bacterial and oomycete infections. Thus, SERK3/BAK1 appears to integrate diverse perception events into downstream PAMP responses, leading to immunity against a range of invading microbes.
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                Author and article information

                Contributors
                yongjunlin@mail.hzau.edu.cn
                aylifug@caas.cn
                gexiaoyang@caas.cn
                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
                07 July 2021
                September 2021
                : 22
                : 9 ( doiID: 10.1002/mpp.v22.9 )
                : 1109-1120
                Affiliations
                [ 1 ] Institute of Cotton Research Henan Normal University Research Base of State Key Laboratory of Cotton Biology Henan China
                [ 2 ] National Key Laboratory of Crop Genetic Improvement Huazhong Agricultural University Wuhan China
                [ 3 ] Zhengzhou Research Base, State Key Laboratory of Cotton Biology, School of Agricultural Sciences Zhengzhou University Zhengzhou China
                Author notes
                [*] [* ] Correspondence

                Xiaoyang Ge, Institute of Cotton Research, Henan Normal University Research Base of State Key Laboratory of Cotton Biology, Henan, China.

                Emails: gexiaoyang@ 123456caas.cn

                (X.G.); aylifug@ 123456caas.cn (F.L.); yongjunlin@ 123456mail.hzau.edu.cn (Y.L.)

                Author information
                https://orcid.org/0000-0003-3428-2942
                Article
                MPP13100
                10.1111/mpp.13100
                8358993
                34233072
                8bd9bc52-683f-4d02-ad7c-fd8b3373c3e7
                © 2021 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
                : 09 May 2021
                : 12 November 2020
                : 27 May 2021
                Page count
                Figures: 8, Tables: 0, Pages: 12, Words: 8059
                Funding
                Funded by: 'Seven Crop Breeding' National Major Project
                Award ID: 2016YFD0101006
                Funded by: Agricultural Science and Technology Innovation Program of Chinese Academy of Agricultural Science
                Funded by: Agriculture Research System of MOF and MARA
                Award ID: CARS‐15‐02
                Categories
                Original Article
                Original Articles
                Custom metadata
                2.0
                September 2021
                Converter:WILEY_ML3GV2_TO_JATSPMC version:6.0.5 mode:remove_FC converted:12.08.2021

                Plant science & Botany
                cell death,effector,nuclear localization signal,verticillium dahliae,virulence

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