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      The secreted FoAPY1 peptidase promotes Fusarium oxysporum invasion

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          Abstract

          The secretion of peptidases from several pathogens has been reported, but the biological function of these proteins in plant-pathogen interactions is poorly understood. Fusarium oxysporum, a soil-borne plant pathogenic fungus that causes Fusarium wilt in its host, can secrete proteins into host plant cells during the infection process to interfere with the host plant defense response and promote disease occurrence. In this study, we identified a peptidase, FoAPY1, that could be secreted from F. oxysporum depending on the N-terminal signal peptide of the protein. FoAPY1 belongs to the peptidase M28 family and exerts peptidase activity in vitro. Furthermore, the FoAYP1 gene knockout strain (∆FoAYP1) presented reduced virulence to tomato plants, but its mycelial growth and conidiation were unchanged. Moreover, FoAYP1 overexpression tomato seedlings exhibited enhanced susceptibility to F. oxysporum and Botrytis cinerea strains. These data demonstrated that FoAYP1 contributes to the virulence of F. oxysporum may through peptidase activity against host plant proteins.

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          The plant immune system.

          Many plant-associated microbes are pathogens that impair plant growth and reproduction. Plants respond to infection using a two-branched innate immune system. The first branch recognizes and responds to molecules common to many classes of microbes, including non-pathogens. The second responds to pathogen virulence factors, either directly or through their effects on host targets. These plant immune systems, and the pathogen molecules to which they respond, provide extraordinary insights into molecular recognition, cell biology and evolution across biological kingdoms. A detailed understanding of plant immune function will underpin crop improvement for food, fibre and biofuels production.
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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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              Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium.

              Fusarium species are among the most important phytopathogenic and toxigenic fungi. To understand the molecular underpinnings of pathogenicity in the genus Fusarium, we compared the genomes of three phenotypically diverse species: Fusarium graminearum, Fusarium verticillioides and Fusarium oxysporum f. sp. lycopersici. Our analysis revealed lineage-specific (LS) genomic regions in F. oxysporum that include four entire chromosomes and account for more than one-quarter of the genome. LS regions are rich in transposons and genes with distinct evolutionary profiles but related to pathogenicity, indicative of horizontal acquisition. Experimentally, we demonstrate the transfer of two LS chromosomes between strains of F. oxysporum, converting a non-pathogenic strain into a pathogen. Transfer of LS chromosomes between otherwise genetically isolated strains explains the polyphyletic origin of host specificity and the emergence of new pathogenic lineages in F. oxysporum. These findings put the evolution of fungal pathogenicity into a new perspective.
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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                19 October 2022
                2022
                : 13
                : 1040302
                Affiliations
                [1] 1College of Life Sciences, Shandong Normal University , Jinan, China
                [2] 2Key Lab of Integrated Crop Pest Management of Shandong Province, College of Plant Health and Medicine, Qingdao Agricultural University , Qingdao, China
                Author notes

                Edited by: Jinliang Liu, Jilin University, China

                Reviewed by: Jie-Yin Chen, Chinese Academy of Agricultural Sciences, China; Yong-Hwan Lee, Seoul National University, South Korea; Shou-qiang Ouyang, Yangzhou University, China

                *Correspondence: Wenxing Liang, wliang1@ 123456qau.edu.cn

                This article was submitted to Microbe and Virus Interactions With Plants, a section of the journal Frontiers in Microbiology

                Article
                10.3389/fmicb.2022.1040302
                9626516
                91a14964-6839-4162-9cba-01480566f724
                Copyright © 2022 Qian, Song, Wang, Wang and Liang.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 09 September 2022
                : 06 October 2022
                Page count
                Figures: 7, Tables: 0, Equations: 0, References: 54, Pages: 14, Words: 9223
                Funding
                Funded by: National Natural Science Foundation of China , doi 10.13039/501100001809;
                Award ID: 31972213
                Funded by: Natural Science Foundation of Shandong Province , doi 10.13039/501100007129;
                Award ID: ZR2020KC003
                Funded by: Shandong Province
                Award ID: WST2018008
                Funded by: Shandong Province
                Award ID: 2019YQ017
                Award ID: tshw20130963
                Funded by: Research and Development , doi 10.13039/100006190;
                Funded by: Shandong Province
                Categories
                Microbiology
                Original Research

                Microbiology & Virology
                fusarium oxysporum,secretion,peptidase,virulence,proteomics
                Microbiology & Virology
                fusarium oxysporum, secretion, peptidase, virulence, proteomics

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