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      Phytohormone-mediated interkingdom signaling shapes the outcome of rice- Xanthomonas oryzae pv. oryzae interactions

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          Abstract

          Background

          Small-molecule hormones are well known to play key roles in the plant immune signaling network that is activated upon pathogen perception. In contrast, little is known about whether phytohormones also directly influence microbial virulence, similar to what has been reported in animal systems.

          Results

          In this paper, we tested the hypothesis that hormones fulfill dual roles in plant-microbe interactions by orchestrating host immune responses, on the one hand, and modulating microbial virulence traits, on the other. Employing the rice- Xanthomonas oryzae pv. oryzae ( Xoo) interaction as a model system, we show that Xoo uses the classic immune hormone salicylic acid (SA) as a trigger to activate its virulence-associated quorum sensing (QS) machinery. Despite repressing swimming motility, sodium salicylate (NaSA) induced production of the Diffusible Signal Factor (DSF) and Diffusible Factor (DF) QS signals, with resultant accumulation of xanthomonadin and extracellular polysaccharides. In contrast, abscisic acid (ABA), which favors infection by Xoo, had little impact on DF- and DSF-mediated QS, but promoted bacterial swimming via the LuxR solo protein OryR. Moreover, we found both DF and DSF to influence SA- and ABA-responsive gene expression in planta.

          Conclusions

          Together our findings indicate that the rice SA and ABA signaling pathways cross-communicate with the Xoo DF and DSF QS systems and underscore the importance of bidirectional interkingdom signaling in molding plant-microbe interactions.

          Electronic supplementary material

          The online version of this article (doi:10.1186/s12870-014-0411-3) contains supplementary material, which is available to authorized users.

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          Most cited references61

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          Quorum sensing, communication and cross-kingdom signalling in the bacterial world.

          Although unicellular, bacteria are highly interactive and employ a range of cell-to-cell communication or 'quorum sensing (QS)' systems for promoting collective behaviour within a population. QS is generally considered to facilitate gene expression only when the population has reached a sufficient cell density and depends on the synthesis of small molecules that diffuse in and out of bacterial cells. As the bacterial population density increases, so does the synthesis of QS signal molecules and consequently, their concentration in the external environment increases. Once a critical threshold concentration is reached, a target sensor kinase or response regulator is activated, so facilitating the expression of QS-dependent target genes. Several chemically distinct families of QS signal molecules have been described, of which the N-acylhomoserine lactone (AHL) family in Gram-negative bacteria have been the most intensively investigated. QS contributes to environmental adaptation by facilitating the elaboration of virulence determinants in pathogenic species and plant biocontrol characteristics in beneficial species as well as directing biofilm formation and colony escape. QS also crosses the prokaryotic-eukaryotic boundary in that QS signal molecules influence the behaviour of eukaryotic organisms in both the plant and mammalian worlds such that QS signal molecules may directly facilitate bacterial survival by promoting an advantageous lifestyle within a given environmental niche.
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            Regulation and secretion of Xanthomonas virulence factors.

            Plant pathogenic bacteria of the genus Xanthomonas cause a variety of diseases in economically important monocotyledonous and dicotyledonous crop plants worldwide. Successful infection and bacterial multiplication in the host tissue often depend on the virulence factors secreted including adhesins, polysaccharides, LPS and degradative enzymes. One of the key pathogenicity factors is the type III secretion system, which injects effector proteins into the host cell cytosol to manipulate plant cellular processes such as basal defense to the benefit of the pathogen. The coordinated expression of bacterial virulence factors is orchestrated by quorum-sensing pathways, multiple two-component systems and transcriptional regulators such as Clp, Zur, FhrR, HrpX and HpaR. Furthermore, virulence gene expression is post-transcriptionally controlled by the RNA-binding protein RsmA. In this review, we summarize the current knowledge on the infection strategies and regulatory networks controlling secreted virulence factors from Xanthomonas species.
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              Highly sensitive and high-throughput analysis of plant hormones using MS-probe modification and liquid chromatography-tandem mass spectrometry: an application for hormone profiling in Oryza sativa.

              We have developed a highly sensitive and high-throughput method for the simultaneous analysis of 43 molecular species of cytokinins, auxins, ABA and gibberellins. This method consists of an automatic liquid handling system for solid phase extraction and ultra-performance liquid chromatography (UPLC) coupled with a tandem quadrupole mass spectrometer (qMS/MS) equipped with an electrospray interface (ESI; UPLC-ESI-qMS/MS). In order to improve the detection limit of negatively charged compounds, such as gibberellins, we chemically derivatized fractions containing auxin, ABA and gibberellins with bromocholine that has a quaternary ammonium functional group. This modification, that we call 'MS-probe', makes these hormone derivatives have a positive ion charge and permits all compounds to be measured in the positive ion mode with UPLC-ESI-qMS/MS in a single run. Consequently, quantification limits of gibberellins increased up to 50-fold. Our current method needs 180 plant samples simultaneously. Application of this method to plant hormone profiling enabled us to draw organ distribution maps of hormone species in rice and also to identify interactions among the four major hormones in the rice gibberellin signaling mutants, gid1-3, gid2-1 and slr1. Combining the results of hormone profiling data with transcriptome data in the gibberellin signaling mutants allows us to analyze relationships between changes in gene expression and hormone metabolism.
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                Author and article information

                Contributors
                jing.xu@ugent.be
                lianzhou@sjtu.edu.cn
                venturi@icgeb.org
                yawenhe@sjtu.edu.cn
                mikiko@riken.jp
                sakaki@postman.riken.go.jp
                monica.hofte@ugent.be
                david.devleesschauwer@ugent.be
                Journal
                BMC Plant Biol
                BMC Plant Biol
                BMC Plant Biology
                BioMed Central (London )
                1471-2229
                21 January 2015
                21 January 2015
                2015
                : 15
                : 1
                : 10
                Affiliations
                [ ]Lab of Phytopathology, Department of Crop Protection, Ghent University, Coupure Links 653, 9000 Ghent, Belgium
                [ ]State Key Laboratory of Microbial Metabolism, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai, 200240 China
                [ ]International Centre for Genetic Engineering and Biotechnology, Padriciano 99, 34149 Trieste, Italy
                [ ]RIKEN Center for Sustainable Resource Science, Yokohama, 230-0045 Japan
                Article
                411
                10.1186/s12870-014-0411-3
                4307914
                25605284
                e16abafe-f14c-41cd-8d47-e0a70518f96b
                © Xu et al.; licensee BioMed Central. 2015

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 13 September 2014
                : 30 December 2014
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2015

                Plant science & Botany
                plant immunity,oryza sativa,defense,hormone signaling,quorum sensing,pathogenicity

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