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      Salmonella Heterogeneously Expresses Flagellin during Colonization of Plants

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          Abstract

          Minimally processed or fresh fruits and vegetables are unfortunately linked to an increasing number of food-borne diseases, such as salmonellosis. One of the relevant virulence factors during the initial phases of the infection process is the bacterial flagellum. Although its function is well studied in animal systems, contradictory results have been published regarding its role during plant colonization. In this study, we tested the hypothesis that Salmonella’s flagellin plays a versatile function during the colonization of tomato plants. We have assessed the persistence in plant tissues of a Salmonella enterica wild type strain, and of a strain lacking the two flagellins, FljB and FliC. We detected no differences between these strains concerning their respective abilities to reach distal, non-inoculated parts of the plant. Analysis of flagellin expression inside the plant, at both the population and single cell levels, shows that the majority of bacteria down-regulate flagellin production, however, a small fraction of the population continues to express flagellin at a very high level inside the plant. This heterogeneous expression of flagellin might be an adaptive strategy to the plant environment. In summary, our study provides new insights on Salmonella adaption to the plant environment through the regulation of flagellin expression.

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          Most cited references54

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          The Role of the Bacterial Flagellum in Adhesion and Virulence

          The bacterial flagellum is a complex apparatus assembled of more than 20 different proteins. The flagellar basal body traverses the cell wall, whereas the curved hook connects the basal body to the whip-like flagellar filament that protrudes several µm from the bacterial cell. The flagellum has traditionally been regarded only as a motility organelle, but more recently it has become evident that flagella have a number of other biological functions. The major subunit, flagellin or FliC, of the flagellum plays a well-documented role in innate immunity and as a dominant antigen of the adaptive immune response. Importantly, flagella have also been reported to function as adhesins. Whole flagella have been indicated as significant in bacterial adhesion to and invasion into host cells. In various pathogens, e.g., Escherichia coli, Pseudomonas aeruginosa and Clostridium difficile, flagellin and/or the distally located flagellar cap protein have been reported to function as adhesins. Recently, FliC of Shiga-toxigenic E. coli was shown to be involved in cellular invasion via lipid rafts. Here, we examine the latest or most important findings regarding flagellar adhesive and invasive properties, especially focusing on the flagellum as a potential virulence factor.
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            Role of stomata in plant innate immunity and foliar bacterial diseases.

            Pathogen entry into host tissue is a critical first step in causing infection. For foliar bacterial plant pathogens, natural surface openings, such as stomata, are important entry sites. Historically, these surface openings have been considered as passive portals of entry for plant pathogenic bacteria. However, recent studies have shown that stomata can play an active role in limiting bacterial invasion as part of the plant innate immune system. As a counter-defense, the plant pathogen Pseudomonas syringae pv. tomato DC3000 uses the virulence factor coronatine to actively open stomata. In nature, many foliar bacterial disease outbreaks require high humidity, rain, or storms, which could favor stomatal opening and/or bypass stomatal defense by creating wounds as alternative entry sites. Further studies on microbial and environmental regulation of stomatal closure and opening could fill gaps in our understanding of bacterial pathogenesis, disease epidemiology, and microbiology of the phyllosphere.
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              Reactive oxygen species and their role in plant defence and cell wall metabolism.

              Harnessing the toxic properties of reactive oxygen species (ROS) to fight off invading pathogens can be considered a major evolutionary success story. All aerobic organisms have evolved the ability to regulate the levels of these toxic intermediates, whereas some have evolved elaborate signalling pathways to dramatically increase the levels of ROS and use them as weapons in mounting a defence response, a process commonly referred to as the oxidative burst. The balance between steady state levels of ROS and the exponential increase in these levels during the oxidative burst has begun to shed light on complex signalling networks mediated by these molecules. Here, we discuss the different sources of ROS that are present in plant cells and review their role in the oxidative burst. We further describe two well-studied ROS generating systems, the NADPH oxidase and apoplastic peroxidase proteins, and their role as the primary producers of ROS during pathogen invasion. We then discuss what is known about the metabolic and proteomic fluxes that occur in plant cells during the oxidative burst and after pathogen recognition, and try to highlight underlying biochemical processes that may provide more insight on the complex regulation of ROS in plants.
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                Author and article information

                Journal
                Microorganisms
                Microorganisms
                microorganisms
                Microorganisms
                MDPI
                2076-2607
                29 May 2020
                June 2020
                : 8
                : 6
                : 815
                Affiliations
                [1 ]Julius Kühn-Institut Federal Research Centre for Cultivated Plants (JKI), Institute for Epidemiology and Pathogen Diagnostics, Messeweg 11/12, 38104 Braunschweig, Germany; azhar.zarkani@ 123456julius-kuehn.de (A.A.Z.); maja.grimm@ 123456julius-kuehn.de (M.G.)
                [2 ]Department of Biotechnology, College of Science, University of Baghdad, 10071 Baghdad, Iraq
                [3 ]Instituto de Hortofruticultura Subtropical y Mediterránea, Universidad de Málaga-Consejo Superior de Investigaciones Científicas (IHSM-UMA-CSIC), Dpto. Biología Celular, Genética y Fisiología, Campus de Teatinos, 29071 Malaga, Spain; nieves.lpg@ 123456uma.es (N.L.-P.); javieruizal@ 123456uma.es (J.R.-A.); cbeuzon@ 123456uma.es (C.R.B.)
                [4 ]Departamento de Genética, Facultad de Biología, Universidad de Sevilla, Apartado 1095, 41080 Seville, Spain; mtsanchez@ 123456us.es
                [5 ]Current address: Departamento de Microbiología y Parasitología, Facultad de Farmacia, Universidad de Sevilla, Calle Profesor García González 2, 41012 Seville, Spain
                Author notes
                Author information
                https://orcid.org/0000-0003-3098-1033
                https://orcid.org/0000-0002-6888-3845
                https://orcid.org/0000-0002-0869-6423
                Article
                microorganisms-08-00815
                10.3390/microorganisms8060815
                7355505
                32485895
                3b5a774d-2301-4224-919c-10389a02791c
                © 2020 by the authors.

                Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( http://creativecommons.org/licenses/by/4.0/).

                History
                : 05 May 2020
                : 27 May 2020
                Categories
                Article

                salmonella,flagellin,colonization,crop plants,heterogeneous expression

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