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      Dual impact of elevated temperature on plant defence and bacterial virulence in Arabidopsis

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          Abstract

          Environmental conditions profoundly affect plant disease development; however, the underlying molecular bases are not well understood. Here we show that elevated temperature significantly increases the susceptibility of Arabidopsis to Pseudomonas syringae pv. tomato ( Pst) DC3000 independently of the phyB/PIF thermosensing pathway. Instead, elevated temperature promotes translocation of bacterial effector proteins into plant cells and causes a loss of ICS1-mediated salicylic acid (SA) biosynthesis. Global transcriptome analysis reveals a major temperature-sensitive node of SA signalling, impacting ~60% of benzothiadiazole (BTH)-regulated genes, including ICS1 and the canonical SA marker gene, PR1. Remarkably, BTH can effectively protect Arabidopsis against Pst DC3000 infection at elevated temperature despite the lack of ICS1 and PR1 expression. Our results highlight the broad impact of a major climate condition on the enigmatic molecular interplay between temperature, SA defence and function of a central bacterial virulence system in the context of a widely studied susceptible plant–pathogen interaction.

          Abstract

          Temperature is known to influence plant disease development. Here Huot et al. show that elevated temperature can enhance Pseudomonas syringae effector delivery into plant cells and suppress SA biosynthesis while also finding a temperature-sensitive branch of the SA signaling pathway in Arabidopsis.

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          Most cited references69

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          Isochorismate synthase is required to synthesize salicylic acid for plant defence.

          Salicylic acid (SA) mediates plant defences against pathogens, accumulating in both infected and distal leaves in response to pathogen attack. Pathogenesis-related gene expression and the synthesis of defensive compounds associated with both local and systemic acquired resistance (LAR and SAR) in plants require SA. In Arabidopsis, exogenous application of SA suffices to establish SAR, resulting in enhanced resistance to a variety of pathogens. However, despite its importance in plant defence against pathogens, SA biosynthesis is not well defined. Previous work has suggested that plants synthesize SA from phenylalanine; however, SA could still be produced when this pathway was inhibited, and the specific activity of radiolabelled SA in feeding experiments was often lower than expected. Some bacteria such as Pseudomonas aeruginosa synthesize SA using isochorismate synthase (ICS) and pyruvate lyase. Here we show, by cloning and characterizing an Arabidopsis defence-related gene (SID2) defined by mutation, that SA is synthesized from chorismate by means of ICS, and that SA made by this pathway is required for LAR and SAR responses.
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            Crop losses to pests

            E-C Oerke (2005)
            The Journal of Agricultural Science, 144(1), 31-43 ["Productivity of crops grown for human consumption is at risk due to the incidence of pests, especially weeds, pathogens and animal pests. Crop losses due to these harmful organisms can be substantial and may be prevented, or reduced, by crop protection measures. An overview is given on different types of crop losses as well as on various methods of pest control developed during the last century.", "Estimates on potential and actual losses despite the current crop protection practices are given for wheat, rice, maize, potatoes, soybeans, and cotton for the period 2001–03 on a regional basis (19 regions) as well as for the global total. Among crops, the total global potential loss due to pests varied from about 50% in wheat to more than 80% in cotton production. The responses are estimated as losses of 26–29% for soybean, wheat and cotton, and 31, 37 and 40% for maize, rice and potatoes, respectively. Overall, weeds produced the highest potential loss (34%), with animal pests and pathogens being less important (losses of 18 and 16%). The efficacy of crop protection was higher in cash crops than in food crops. Weed control can be managed mechanically or chemically, therefore worldwide efficacy was considerably higher than for the control of animal pests or diseases, which rely heavily on synthetic chemicals. Regional differences in efficacy are outlined. Despite a clear increase in pesticide use, crop losses have not significantly decreased during the last 40 years. However, pesticide use has enabled farmers to modify production systems and to increase crop productivity without sustaining the higher losses likely to occur from an increased susceptibility to the damaging effect of pests.", "The concept of integrated pest/crop management includes a threshold concept for the application of pest control measures and reduction in the amount/frequency of pesticides applied to an economically and ecologically acceptable level. Often minor crop losses are economically acceptable; however, an increase in crop productivity without adequate crop protection does not make sense, because an increase in attainable yields is often associated with an increased vulnerability to damage inflicted by pests."]
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              Systemic acquired resistance: turning local infection into global defense.

              Systemic acquired resistance (SAR) is an induced immune mechanism in plants. Unlike vertebrate adaptive immunity, SAR is broad spectrum, with no specificity to the initial infection. An avirulent pathogen causing local programmed cell death can induce SAR through generation of mobile signals, accumulation of the defense hormone salicylic acid, and secretion of the antimicrobial PR (pathogenesis-related) proteins. Consequently, the rest of the plant is protected from secondary infection for a period of weeks to months. SAR can even be passed on to progeny through epigenetic regulation. The Arabidopsis NPR1 (nonexpresser of PR genes 1) protein is a master regulator of SAR. Recent study has shown that salicylic acid directly binds to the NPR1 adaptor proteins NPR3 and NPR4, regulates their interactions with NPR1, and controls NPR1 protein stability. However, how NPR1 interacts with TGA transcription factors to activate defense gene expression is still not well understood. In addition, redox regulators, the mediator complex, WRKY transcription factors, endoplasmic reticulum-resident proteins, and DNA repair proteins play critical roles in SAR.
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                Author and article information

                Contributors
                montg133@msu.edu
                hes@msu.edu
                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group UK (London )
                2041-1723
                27 November 2017
                27 November 2017
                2017
                : 8
                : 1808
                Affiliations
                [1 ]ISNI 0000 0001 2150 1785, GRID grid.17088.36, Department of Energy Plant Research Laboratory, , Michigan State University, ; East Lansing, MI 48824 USA
                [2 ]ISNI 0000 0001 2150 1785, GRID grid.17088.36, Cell and Molecular Biology Program, , Michigan State University, ; East Lansing, MI 48824 USA
                [3 ]ISNI 0000 0001 2150 1785, GRID grid.17088.36, Plant Resilience Institute, , Michigan State University, ; East Lansing, MI 48824 USA
                [4 ]ISNI 0000 0001 2150 1785, GRID grid.17088.36, Department of Plant Biology, , Michigan State University, ; East Lansing, MI 48824 USA
                [5 ]ISNI 0000 0001 2150 1785, GRID grid.17088.36, Center for Genomics Enabled Plant Science, , Michigan State University, ; East Lansing, MI 48824 USA
                [6 ]ISNI 0000 0001 0672 1122, GRID grid.268187.2, Department of Biological Sciences, , Western Michigan University, ; Kalamazoo, MI 49008 USA
                [7 ]ISNI 0000 0001 0660 6765, GRID grid.419498.9, Department of Plant-Microbe Interactions, , Max Planck Institute for Plant Breeding Research, ; 50829 Cologne, Germany
                [8 ]ISNI 0000 0001 2150 1785, GRID grid.17088.36, Department of Biochemistry and Molecular Biology, , Michigan State University, ; East Lansing, MI 48824 USA
                [9 ]ISNI 0000 0001 2150 1785, GRID grid.17088.36, Department of Microbiology and Molecular Genetics, , Michigan State University, ; East Lansing, MI 48824 USA
                [10 ]ISNI 0000 0001 2150 1785, GRID grid.17088.36, Howard Hughes Medical Institute, , Michigan State University, ; East Lansing, MI 48933 USA
                Author information
                http://orcid.org/0000-0002-0007-753X
                http://orcid.org/0000-0002-9982-8451
                http://orcid.org/0000-0002-3680-062X
                http://orcid.org/0000-0001-7074-0731
                Article
                1674
                10.1038/s41467-017-01674-2
                5704021
                29180698
                be62686b-3f78-4bdc-a228-e3d6ea95e8d2
                © 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/.

                History
                : 14 January 2017
                : 6 October 2017
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