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      The molecular dialogue between Arabidopsis thaliana and the necrotrophic fungus Botrytis cinerea leads to major changes in host carbon metabolism

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          Abstract

          Photoassimilates play crucial roles during plant-pathogen interactions, as colonizing pathogens rely on the supply of sugars from hosts. The competition for sugar acquisition at the plant-pathogen interface involves different strategies from both partners which are critical for the outcome of the interaction. Here, we dissect individual mechanisms of sugar uptake during the interaction of Arabidopsis thaliana with the necrotrophic fungus Botrytis cinerea using millicell culture insert, that enables molecular communication without physical contact. We demonstrate that B. cinerea is able to actively absorb glucose and fructose with equal capacities. Challenged Arabidopsis cells compete for extracellular monosaccharides through transcriptional reprogramming of host sugar transporter genes and activation of a complex sugar uptake system which displays differential specificity and affinity for hexoses. We provide evidence that the molecular dialogue between Arabidopsis cells and B. cinerea triggers major changes in host metabolism, including apoplastic sucrose degradation and consumption of carbohydrates and oxygen, suggesting an enhanced activity of the glycolysis and the cellular respiration. We conclude that beside a role in sugar deprivation of the pathogen by competing for sugar availability in the apoplast, the enhanced uptake of hexoses also contributes to sustain the increased activity of respiratory metabolism to fuel plant defences.

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          Most cited references 37

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          Sugar transporters for intercellular exchange and nutrition of pathogens.

          Sugar efflux transporters are essential for the maintenance of animal blood glucose levels, plant nectar production, and plant seed and pollen development. Despite broad biological importance, the identity of sugar efflux transporters has remained elusive. Using optical glucose sensors, we identified a new class of sugar transporters, named SWEETs, and show that at least six out of seventeen Arabidopsis, two out of over twenty rice and two out of seven homologues in Caenorhabditis elegans, and the single copy human protein, mediate glucose transport. Arabidopsis SWEET8 is essential for pollen viability, and the rice homologues SWEET11 and SWEET14 are specifically exploited by bacterial pathogens for virulence by means of direct binding of a bacterial effector to the SWEET promoter. Bacterial symbionts and fungal and bacterial pathogens induce the expression of different SWEET genes, indicating that the sugar efflux function of SWEET transporters is probably targeted by pathogens and symbionts for nutritional gain. The metazoan homologues may be involved in sugar efflux from intestinal, liver, epididymis and mammary cells.
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            Primary metabolism and plant defense--fuel for the fire.

             D. Bolton (2009)
            Plants have the ability to recognize and respond to a multitude of microorganisms. Recognition of pathogens results in a massive reprogramming of the plant cell to activate and deploy defense responses to halt pathogen growth. Such responses are associated with increased demands for energy, reducing equivalents, and carbon skeletons that are provided by primary metabolic pathways. Although pathogen recognition and downstream resistance responses have been the focus of major study, an intriguing and comparatively understudied phenomenon is how plants are able to recruit energy for the defense response. To that end, this review will summarize current research on energy-producing primary metabolism pathways and their role in fueling the resistance response.
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              Plant pattern recognition receptor complexes at the plasma membrane.

              A key feature of innate immunity is the ability to recognize and respond to potential pathogens in a highly sensitive and specific manner. In plants, the activation of pattern recognition receptors (PRRs) by pathogen-associated molecular patterns (PAMPs) elicits a defense programme known as PAMP-triggered immunity (PTI). Although only a handful of PAMP-PRR pairs have been defined, all known PRRs are modular transmembrane proteins containing ligand-binding ectodomains. It is becoming clear that PRRs do not act alone but rather function as part of multi-protein complexes at the plasma membrane. Recent studies describing the molecular interactions and protein modifications that occur between PRRs and their regulatory proteins have provided important mechanistic insight into how plants avoid infection and achieve immunity. Copyright © 2012 Elsevier Ltd. All rights reserved.
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                Author and article information

                Contributors
                sylvain.la.camera@univ-poitiers.fr
                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group UK (London )
                2045-2322
                7 December 2017
                7 December 2017
                2017
                : 7
                Affiliations
                [1 ]ISNI 0000 0001 2160 6368, GRID grid.11166.31, Laboratoire Ecologie et Biologie des Interactions, , Equipe “SEVE-Sucres et Echanges Végétaux-Environnement”, Université de Poitiers, UMR CNRS 7267, ; F-86073 Poitiers, France
                [2 ]ISNI 0000 0004 1936 9991, GRID grid.35403.31, Present Address: Department of Plant Biology and Institute for Genomic Biology, , University of Illinois at Urbana-Champaign, ; Urbana, Illinois 61801 USA
                Article
                17413
                10.1038/s41598-017-17413-y
                5719352
                29215097
                © The Author(s) 2017

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

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