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      Nuclear Signaling of Plant MAPKs

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          Abstract

          Mitogen-activated protein kinases (MAPKs) are conserved protein kinases in eukaryotes that establish signaling modules where MAPK kinase kinases (MAPKKKs) activate MAPK kinases (MAPKKs) which in turn activate MAPKs. In plants, they are involved in the signaling of multiple environmental stresses and developmental programs. MAPKs phosphorylate their substrates and this post-translational modification (PTM) contributes to the regulation of proteins. PTMs may indeed modify the activity, subcellular localization, stability or trans-interactions of modified proteins. Plant MAPKs usually localize to the cytosol and/or nucleus, and in some instances they may also translocate from the cytosol to the nucleus. Upon the detection of environmental changes at the cell surface, MAPKs participate in the signal transduction to the nucleus, allowing an adequate transcriptional reprogramming. The identification of plant MAPK substrates largely contributed to a better understanding of the underlying signaling mechanisms. In this review, we highlight the nuclear signaling of plant MAPKs. We discuss the activation, regulation and activity of plant MAPKs, as well as their nuclear re-localization. We also describe and discuss known nuclear substrates of plant MAPKs in the context of biotic stress, abiotic stress and development and consider future research directions in the field of plant MAPKs.

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          Most cited references131

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          Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation.

          Higher eukaryotes sense microbes through the perception of pathogen-associated molecular patterns (PAMPs). Arabidopsis plants detect a variety of PAMPs including conserved domains of bacterial flagellin and of bacterial EF-Tu. Here, we show that flagellin and EF-Tu activate a common set of signaling events and defense responses but without clear synergistic effects. Treatment with either PAMP results in increased binding sites for both PAMPs. We used this finding in a targeted reverse-genetic approach to identify a receptor kinase essential for EF-Tu perception, which we called EFR. Nicotiana benthamiana, a plant unable to perceive EF-Tu, acquires EF-Tu binding sites and responsiveness upon transient expression of EFR. Arabidopsis efr mutants show enhanced susceptibility to the bacterium Agrobacterium tumefaciens, as revealed by a higher efficiency of T-DNA transformation. These results demonstrate that EFR is the EF-Tu receptor and that plant defense responses induced by PAMPs such as EF-Tu reduce transformation by Agrobacterium.
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            Phosphorylation of a WRKY transcription factor by two pathogen-responsive MAPKs drives phytoalexin biosynthesis in Arabidopsis.

            Plant sensing of invading pathogens triggers massive metabolic reprogramming, including the induction of secondary antimicrobial compounds known as phytoalexins. We recently reported that MPK3 and MPK6, two pathogen-responsive mitogen-activated protein kinases, play essential roles in the induction of camalexin, the major phytoalexin in Arabidopsis thaliana. In search of the transcription factors downstream of MPK3/MPK6, we found that WRKY33 is required for MPK3/MPK6-induced camalexin biosynthesis. In wrky33 mutants, both gain-of-function MPK3/MPK6- and pathogen-induced camalexin production are compromised, which is associated with the loss of camalexin biosynthetic gene activation. WRKY33 is a pathogen-inducible transcription factor, whose expression is regulated by the MPK3/MPK6 cascade. Chromatin immunoprecipitation assays reveal that WRKY33 binds to its own promoter in vivo, suggesting a potential positive feedback regulatory loop. Furthermore, WRKY33 is a substrate of MPK3/MPK6. Mutation of MPK3/MPK6 phosphorylation sites in WRKY33 compromises its ability to complement the camalexin induction in the wrky33 mutant. Using a phospho-protein mobility shift assay, we demonstrate that WRKY33 is phosphorylated by MPK3/MPK6 in vivo in response to Botrytis cinerea infection. Based on these data, we conclude that WRKY33 functions downstream of MPK3/MPK6 in reprogramming the expression of camalexin biosynthetic genes, which drives the metabolic flow to camalexin production in Arabidopsis challenged by pathogens.
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              Scaffold proteins: hubs for controlling the flow of cellular information.

              The spatial and temporal organization of molecules within a cell is critical for coordinating the many distinct activities carried out by the cell. In an increasing number of biological signaling processes, scaffold proteins have been found to play a central role in physically assembling the relevant molecular components. Although most scaffolds use a simple tethering mechanism to increase the efficiency of interaction between individual partner molecules, these proteins can also exert complex allosteric control over their partners and are themselves the target of regulation. Scaffold proteins offer a simple, flexible strategy for regulating selectivity in pathways, shaping output behaviors, and achieving new responses from preexisting signaling components. As a result, scaffold proteins have been exploited by evolution, pathogens, and cellular engineers to reshape cellular behavior.
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                Author and article information

                Contributors
                Journal
                Front Plant Sci
                Front Plant Sci
                Front. Plant Sci.
                Frontiers in Plant Science
                Frontiers Media S.A.
                1664-462X
                11 April 2018
                2018
                : 9
                : 469
                Affiliations
                [1] 1Institute of Plant Sciences Paris-Saclay IPS2, Centre National de la Recherche Scientifique, Institut National de la Recherche Agronomique, Université Paris-Sud, Université Evry, Université Paris-Saclay , Orsay, France
                [2] 2Institute of Plant Sciences Paris-Saclay IPS2, Paris Diderot, Sorbonne Paris-Cité , Orsay, France
                [3] 3Center for Desert Agriculture, King Abdullah University of Science and Technology , Thuwal, Saudi Arabia
                Author notes

                Edited by: Stéphane Bourque, Université de Bourgogne, France

                Reviewed by: Alok Krishna Sinha, National Institute of Plant Genome Research, India; Olivier Lamotte, INRA UMR1347 Agroécologie, France

                *Correspondence: Heribert Hirt heribert.hirt@ 123456kaust.edu.sa

                This article was submitted to Plant Physiology, a section of the journal Frontiers in Plant Science

                Article
                10.3389/fpls.2018.00469
                5905223
                29696029
                5e9c77b0-cee0-4b08-9c77-34b2ac62cc18
                Copyright © 2018 Bigeard and Hirt.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 06 December 2017
                : 26 March 2018
                Page count
                Figures: 1, Tables: 1, Equations: 0, References: 171, Pages: 18, Words: 15550
                Funding
                Funded by: Global Collaborative Research, King Abdullah University of Science and Technology 10.13039/501100003422
                Award ID: BAS/1/1062–01-0
                Award ID: URF/1/2574-01-01
                Award ID: URF/1/2965-01-01
                Funded by: LabEx Saclay Plant Sciences-SPS
                Award ID: ANR-10-LABX-0040-SPS
                Categories
                Plant Science
                Review

                Plant science & Botany
                nucleus,mitogen-activated protein kinase,phosphorylation,signaling,biotic stress,abiotic stress,development

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