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      Active photosynthetic inhibition mediated by MPK3/MPK6 is critical to effector-triggered immunity

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          Abstract

          Extensive research revealed tremendous details about how plants sense pathogen effectors during effector-triggered immunity (ETI). However, less is known about downstream signaling events. In this report, we demonstrate that prolonged activation of MPK3 and MPK6, two Arabidopsis pathogen-responsive mitogen-activated protein kinases (MPKs), is essential to ETI mediated by both coiled coil-nucleotide binding site-leucine rich repeats (CNLs) and toll/interleukin-1 receptor nucleotide binding site-leucine rich repeats (TNLs) types of R proteins. MPK3/MPK6 activation rapidly alters the expression of photosynthesis-related genes and inhibits photosynthesis, which promotes the accumulation of superoxide (

          ) and hydrogen peroxide (H 2O 2), two major reactive oxygen species (ROS), in chloroplasts under light. In the chemical-genetically rescued mpk3 mpk6 double mutants, ETI-induced photosynthetic inhibition and chloroplastic ROS accumulation are compromised, which correlates with delayed hypersensitive response (HR) cell death and compromised resistance. Furthermore, protection of chloroplasts by expressing a plastid-targeted cyanobacterial flavodoxin (pFLD) delays photosynthetic inhibition and compromises ETI. Collectively, this study highlights a critical role of MPK3/MPK6 in manipulating plant photosynthetic activities to promote ROS accumulation in chloroplasts and HR cell death, which contributes to the robustness of ETI. Furthermore, the dual functionality of MPK3/MPK6 cascade in promoting defense and inhibiting photosynthesis potentially allow it to orchestrate the trade-off between plant growth and defense in plant immunity.

          Author summary

          Plants follow different strategies to defend themselves against pathogens and activate their immune systems once the pathogens have been detected. One of the responses observed is the inhibition of photosynthesis and the global down-regulation of genes that regulate this process, similar to what is frequently observed in plants under various biotic stress conditions. However, the mechanisms underlying the turning off of the photosynthetic activity and whether this process contributes to plants’ defense against pathogens remain to be determined. In this study, we analyze these mechanisms in Arabidopsis plants and show that prolonged activation of MPK3 and MPK6, two kinases critical for pathogen resistance, results in the inhibition of photosynthesis and accumulation of reactive oxygen species (ROS) in the chloroplasts. We find that this response is similar to that observed during pathogen effector-triggered immunity (ETI). Correspondingly, plants that carry mutant versions of MPK3 and MPK6 result in compromised ETI-induced photosynthetic inhibition and chloroplastic ROS accumulation; thus, these two kinases seem to be essential for ETI. Our results suggest that MPK3/MPK6 activation induces a global down-regulation of photosynthesis along with an up-regulation of defense-related genes, and coordinates the growth and defense trade-off in plants.

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          Most cited references66

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          Growth-defense tradeoffs in plants: a balancing act to optimize fitness.

          Growth-defense tradeoffs are thought to occur in plants due to resource restrictions, which demand prioritization towards either growth or defense, depending on external and internal factors. These tradeoffs have profound implications in agriculture and natural ecosystems, as both processes are vital for plant survival, reproduction, and, ultimately, plant fitness. While many of the molecular mechanisms underlying growth and defense tradeoffs remain to be elucidated, hormone crosstalk has emerged as a major player in regulating tradeoffs needed to achieve a balance. In this review, we cover recent advances in understanding growth-defense tradeoffs in plants as well as what is known regarding the underlying molecular mechanisms. Specifically, we address evidence supporting the growth-defense tradeoff concept, as well as known interactions between defense signaling and growth signaling. Understanding the molecular basis of these tradeoffs in plants should provide a foundation for the development of breeding strategies that optimize the growth-defense balance to maximize crop yield to meet rising global food and biofuel demands. © The Author 2014. Published by the Molecular Plant Shanghai Editorial Office in association with Oxford University Press on behalf of CSPB and IPPE, SIBS, CAS.
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            Pivoting the plant immune system from dissection to deployment.

            Diverse and rapidly evolving pathogens cause plant diseases and epidemics that threaten crop yield and food security around the world. Research over the last 25 years has led to an increasingly clear conceptual understanding of the molecular components of the plant immune system. Combined with ever-cheaper DNA-sequencing technology and the rich diversity of germ plasm manipulated for over a century by plant breeders, we now have the means to begin development of durable (long-lasting) disease resistance beyond the limits imposed by conventional breeding and in a manner that will replace costly and unsustainable chemical controls.
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              Regulation of pattern recognition receptor signalling in plants.

              Recognition of pathogen-derived molecules by pattern recognition receptors (PRRs) is a common feature of both animal and plant innate immune systems. In plants, PRR signalling is initiated at the cell surface by kinase complexes, resulting in the activation of immune responses that ward off microorganisms. However, the activation and amplitude of innate immune responses must be tightly controlled. In this Review, we summarize our knowledge of the early signalling events that follow PRR activation and describe the mechanisms that fine-tune immune signalling to maintain immune homeostasis. We also illustrate the mechanisms used by pathogens to inhibit innate immune signalling and discuss how the innate ability of plant cells to monitor the integrity of key immune components can lead to autoimmune phenotypes following genetic or pathogen-induced perturbations of these components.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: ValidationRole: Writing – original draft
                Role: Data curationRole: InvestigationRole: Methodology
                Role: Data curationRole: Investigation
                Role: Data curationRole: Investigation
                Role: Data curationRole: Investigation
                Role: Data curationRole: Investigation
                Role: Data curationRole: Validation
                Role: Resources
                Role: ConceptualizationRole: Project administrationRole: ResourcesRole: SupervisionRole: Writing – original draftRole: Writing – review & editing
                Role: Academic Editor
                Journal
                PLoS Biol
                PLoS Biol
                plos
                plosbiol
                PLoS Biology
                Public Library of Science (San Francisco, CA USA )
                1544-9173
                1545-7885
                3 May 2018
                May 2018
                3 May 2018
                : 16
                : 5
                : e2004122
                Affiliations
                [1 ] Key Laboratory of Plant Physiology and Biochemistry, College of Life Sciences, Zhejiang University, Hangzhou, Zhejiang, China
                [2 ] Division of Biochemistry, Interdisciplinary Plant Group, and Bond Life Sciences Center, University of Missouri, Columbia, Missouri, United States of America
                The Sainsbury Laboratory, United Kingdom of Great Britain and Northern Ireland
                Author notes

                The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0003-2959-6461
                Article
                pbio.2004122
                10.1371/journal.pbio.2004122
                5953503
                29723186
                a26852ae-3b33-4591-8cc5-08fa891b98d0
                © 2018 Su et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 1 September 2017
                : 6 April 2018
                Page count
                Figures: 8, Tables: 0, Pages: 29
                Funding
                111 Project (grant number B14027). Received by SZ. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. NSFC (grant number 31570297). Received by JX. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. NSFC (grant number 31670268). Received by SZ. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Biochemistry
                Plant Biochemistry
                Photosynthesis
                Biology and Life Sciences
                Plant Science
                Plant Biochemistry
                Photosynthesis
                Biology and Life Sciences
                Cell Biology
                Cellular Structures and Organelles
                Chloroplasts
                Biology and Life Sciences
                Cell Biology
                Plant Cell Biology
                Chloroplasts
                Biology and Life Sciences
                Plant Science
                Plant Cell Biology
                Chloroplasts
                Biology and Life Sciences
                Cell Biology
                Cellular Types
                Plant Cells
                Chloroplasts
                Biology and Life Sciences
                Cell Biology
                Plant Cell Biology
                Plant Cells
                Chloroplasts
                Biology and Life Sciences
                Plant Science
                Plant Cell Biology
                Plant Cells
                Chloroplasts
                Biology and Life Sciences
                Cell Biology
                Cellular Structures and Organelles
                Chloroplasts
                Chlorophyll
                Biology and Life Sciences
                Cell Biology
                Plant Cell Biology
                Chloroplasts
                Chlorophyll
                Biology and Life Sciences
                Plant Science
                Plant Cell Biology
                Chloroplasts
                Chlorophyll
                Biology and Life Sciences
                Cell Biology
                Cellular Types
                Plant Cells
                Chloroplasts
                Chlorophyll
                Biology and Life Sciences
                Cell Biology
                Plant Cell Biology
                Plant Cells
                Chloroplasts
                Chlorophyll
                Biology and Life Sciences
                Plant Science
                Plant Cell Biology
                Plant Cells
                Chloroplasts
                Chlorophyll
                Physical Sciences
                Materials Science
                Materials by Attribute
                Pigments
                Organic Pigments
                Chlorophyll
                Research and Analysis Methods
                Electrophoretic Techniques
                Gel Electrophoresis
                Polyacrylamide Gel Electrophoresis
                Blue Native Polyacrylamide Gel Electrophoresis
                Research and Analysis Methods
                Experimental Organism Systems
                Model Organisms
                Arabidopsis Thaliana
                Research and Analysis Methods
                Model Organisms
                Arabidopsis Thaliana
                Biology and Life Sciences
                Organisms
                Eukaryota
                Plants
                Brassica
                Arabidopsis Thaliana
                Research and Analysis Methods
                Experimental Organism Systems
                Plant and Algal Models
                Arabidopsis Thaliana
                Biology and Life Sciences
                Cell Biology
                Cell Processes
                Cell Death
                Biology and Life Sciences
                Biochemistry
                Oxidative Damage
                Reactive Oxygen Species
                Biology and Life Sciences
                Plant Science
                Plant Anatomy
                Leaves
                Custom metadata
                vor-update-to-uncorrected-proof
                2018-05-15
                All relevant data are within the paper and its Supporting information files, with the exception of the raw Illumina reads generated from RNA-seq experiments, which were deposited at NCBI Sequence Read Archive (SRP111959).

                Life sciences
                Life sciences

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