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      A cyclic GMP-dependent signalling pathway regulates bacterial phytopathogenesis

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          Abstract

          Cyclic guanosine 3′,5′-monophosphate (cyclic GMP) is a second messenger whose role in bacterial signalling is poorly understood. A genetic screen in the plant pathogen Xanthomonas campestris ( Xcc) identified that XC_0250, which encodes a protein with a class III nucleotidyl cyclase domain, is required for cyclic GMP synthesis. Purified XC_0250 was active in cyclic GMP synthesis in vitro. The linked gene XC_0249 encodes a protein with a cyclic mononucleotide-binding (cNMP) domain and a GGDEF diguanylate cyclase domain. The activity of XC_0249 in cyclic di-GMP synthesis was enhanced by addition of cyclic GMP. The isolated cNMP domain of XC_0249 bound cyclic GMP and a structure–function analysis, directed by determination of the crystal structure of the holo-complex, demonstrated the site of cyclic GMP binding that modulates cyclic di-GMP synthesis. Mutation of either XC_0250 or XC_0249 led to a reduced virulence to plants and reduced biofilm formation in vitro. These findings describe a regulatory pathway in which cyclic GMP regulates virulence and biofilm formation through interaction with a novel effector that directly links cyclic GMP and cyclic di-GMP signalling.

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          Most cited references15

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          Pathogenomics of Xanthomonas: understanding bacterium-plant interactions.

          Xanthomonas is a large genus of Gram-negative bacteria that cause disease in hundreds of plant hosts, including many economically important crops. Pathogenic species and pathovars within species show a high degree of host plant specificity and many exhibit tissue specificity, invading either the vascular system or the mesophyll tissue of the host. In this Review, we discuss the insights that functional and comparative genomic studies are providing into the adaptation of this group of bacteria to exploit the extraordinary diversity of plant hosts and different host tissues.
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            Biofilm dispersal in Xanthomonas campestris is controlled by cell-cell signaling and is required for full virulence to plants.

            The rpf gene cluster of Xanthomonas campestris pathovar campestris (Xcc) is required for the pathogenesis of this bacterium to plants. Several rpf genes are involved in the coordinate positive regulation of the production of virulence factors mediated by the small diffusible molecule DSF (for diffusible signal factor). RpfF directs the synthesis of DSF, and a two-component sensory transduction system comprising RpfC and RpfG has been implicated in the perception of the DSF signal and signal transduction. In L medium, rpfF, rpfG, rpfC, and rpfGHC mutants grew as matrix-enclosed aggregates, whereas the wild type grew in a dispersed planktonic fashion. Synthesis of the extracellular polysaccharide xanthan was required for aggregate formation. Addition of DSF triggered dispersion of the aggregates formed by the rpfF strain, but not those of rpf strains defective in DSF signal transduction. An extracellular enzyme from Xcc whose synthesis was positively controlled by the DSF/rpf system could disperse the aggregates produced by all rpf strains. The enzyme was identified as the single endo-beta-1,4-mannanase encoded by the Xcc genome. This enzyme had no detectable activity against soluble xanthan. The endo-beta-1,4-mannanase was required for the full virulence of Xcc to plants. On the basis of this model system, we propose that one role of the beta-mannanase during disease is to promote transitions from an aggregated or biofilm lifestyle to a planktonic lifestyle in response to the DSF signal.
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              You've come a long way: c-di-GMP signaling.

              Cyclic dimeric guanosine monophosphate (c-di-GMP) is a common, bacterial second messenger that regulates diverse cellular processes in bacteria. Opposing activities of diguanylate cyclases (DGCs) and phosphodiesterases (PDEs) control c-di-GMP homeostasis in the cell. Many microbes have a large number of genes encoding DGCs and PDEs that are predicted to be part of c-di-GMP signaling networks. Other building blocks of these networks are c-di-GMP receptors which sense the cellular levels of the dinucleotide. C-di-GMP receptors form a more diverse family, including various transcription factors, PilZ domains, degenerate DGCs or PDEs, and riboswitches. Recent studies revealing the molecular basis of c-di-GMP signaling mechanisms enhanced our understanding of how this molecule controls downstream biological processes and how c-di-GMP signaling specificity is achieved. Copyright © 2012 Elsevier Ltd. All rights reserved.
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                Author and article information

                Journal
                EMBO J
                EMBO J
                The EMBO Journal
                Nature Publishing Group
                0261-4189
                1460-2075
                11 September 2013
                23 July 2013
                23 July 2013
                : 32
                : 18
                : 2430-2438
                Affiliations
                [1 ]Division of Molecular Microbiology, College of Life Sciences, University of Dundee , Dundee, UK
                [2 ]Agricultural Biotechnology Center, Institute of Biochemistry, National Chung Hsing University , Taichung, Taiwan, ROC
                [3 ]Division of Molecular Medicine, Colleges of Life Sciences, University of Dundee , Dundee, UK
                [4 ]Department of Microbiology, Biosciences Institute, University College Cork , Cork, Ireland
                [5 ]The Genome Analysis Centre , Norwich, UK
                Author notes
                [a ]Agricultural Biotechnology Center, Institute of Biochemistry, National Chung Hsing University , Taichung, Taiwan, ROC. Tel.:+886 422840468; E-mail: shchou@ 123456nchu.edu.tw
                [b ]Division of Molecular Microbiology, College of Life Sciences, University of Dundee , Dundee DD1 4JU, UK. Tel.:+44 (0)1382384272; Fax:+44 (0)1382388216; E-mail: rpryan@ 123456dundee.ac.uk
                [*]

                These authors contributed equally to this work.

                Article
                emboj2013165
                10.1038/emboj.2013.165
                3770947
                23881098
                ccbb61ff-6c80-44a6-84e7-cf216195c732
                Copyright © 2013, European Molecular Biology Organization

                This article is licensed under a Creative Commons Attribution 3.0 Unported Licence. To view a copy of this licence visit http://creativecommons.org/licenses/by/3.0/.

                History
                : 13 May 2013
                : 04 July 2013
                Categories
                Article

                Molecular biology
                biofilm,cyclic di-gmp,signal transduction,virulence,xanthomonas campestris
                Molecular biology
                biofilm, cyclic di-gmp, signal transduction, virulence, xanthomonas campestris

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