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      COI1-dependent jasmonate signalling affects growth, metabolite production and cell wall protein composition in arabidopsis

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          Abstract

          Background and Aims

          Cultured cell suspensions have been the preferred model to study the apoplast as well as to monitor metabolic and cell cycle-related changes. Previous work showed that methyl jasmonate (MeJA) inhibits leaf growth in a CORONATINE INSENSITIVE 1 ( COI1)-dependent manner, with COI1 being the jasmonate (JA) receptor. Here, the effect of COI1 overexpression on the growth of stably transformed arabidopsis cell cultures is described.

          Methods

          Time-course experiments were carried out to analyse gene expression, and protein and metabolite levels.

          Key Results

          Both MeJA treatment and the overexpression of COI1 modify growth, by altering cell proliferation and expansion. DNA content as well as transcript patterns of cell cycle and cell wall remodelling markers were altered. COI1 overexpression also increases the protein levels of OLIGOGALACTURONIDE OXIDASE 1, BETA-GLUCOSIDASE/ENDOGLUCANASES and POLYGALACTURONASE INHIBITING PROTEIN2, reinforcing the role of COI1 in mediating defence responses and highlighting a link between cell wall loosening and growth regulation. Moreover, changes in the levels of the primary metabolites alanine, serine and succinic acid of MeJA-treated Arabidopsis cell cultures were observed. In addition, COI1 overexpression positively affects the availability of metabolites such as β-alanine, threonic acid, putrescine, glucose and myo-inositol, thereby providing a connection between JA-inhibited growth and stress responses.

          Conclusions

          This study contributes to the understanding of the regulation of growth and the production of metabolic resources by JAs and COI1. This will have important implications in dissecting the complex relationships between hormonal and cell wall signalling in plants. The work also provides tools to uncover novel mechanisms co-ordinating cell division and post-mitotic cell expansion in the absence of organ developmental control.

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          Most cited references95

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          For the past 25 years NIH Image and ImageJ software have been pioneers as open tools for the analysis of scientific images. We discuss the origins, challenges and solutions of these two programs, and how their history can serve to advise and inform other software projects.
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            JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling.

            Jasmonate and related signalling compounds have a crucial role in both host immunity and development in plants, but the molecular details of the signalling mechanism are poorly understood. Here we identify members of the jasmonate ZIM-domain (JAZ) protein family as key regulators of jasmonate signalling. JAZ1 protein acts to repress transcription of jasmonate-responsive genes. Jasmonate treatment causes JAZ1 degradation and this degradation is dependent on activities of the SCF(COI1) ubiquitin ligase and the 26S proteasome. Furthermore, the jasmonoyl-isoleucine (JA-Ile) conjugate, but not other jasmonate-derivatives such as jasmonate, 12-oxo-phytodienoic acid, or methyl-jasmonate, promotes physical interaction between COI1 and JAZ1 proteins in the absence of other plant proteins. Our results suggest a model in which jasmonate ligands promote the binding of the SCF(COI1) ubiquitin ligase to and subsequent degradation of the JAZ1 repressor protein, and implicate the SCF(COI1)-JAZ1 protein complex as a site of perception of the plant hormone JA-Ile.
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              Jasmonate perception by inositol phosphate-potentiated COI1-JAZ co-receptor

              Jasmonates (JAs) are a family of plant hormones that regulate plant growth, development, and responses to stress. The F-box protein CORONATINE-INSENSITIVE 1 (COI1) mediates JA signaling by promoting hormone-dependent ubiquitination and degradation of transcriptional repressor JAZ proteins. Despite its importance, the mechanism of JA perception remains unclear. Here we present structural and pharmacological data to show that the true JA receptor is a complex of both COI1 and JAZ. COI1 contains an open pocket that recognizes the bioactive hormone, (3R,7S)-jasmonoyl-L-isoleucine (JA-Ile), with high specificity. High-affinity hormone binding requires a bipartite JAZ degron sequence consisting of a conserved α-helix for COI1 docking and a loop region to trap the hormone in its binding pocket. In addition, we identify a third critical component of the JA co-receptor complex, inositol pentakisphosphate, which interacts with both COI1 and JAZ adjacent to the ligand. Our results unravel the mechanism of JA perception and highlight the ability of F-box proteins to evolve as multi-component signaling hubs.
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                Author and article information

                Journal
                Ann Bot
                Ann. Bot
                annbot
                Annals of Botany
                Oxford University Press (US )
                0305-7364
                1095-8290
                December 2018
                19 June 2018
                19 June 2018
                : 122
                : 7
                : 1117-1129
                Affiliations
                [1 ]Plant Molecular Science and Centre of Systems and Synthetic Biology, School of Biological Sciences, Royal Holloway University of London, Egham, Surrey, UK
                [2 ]Departamento de Genética Molecular y Microbiología, Departamento de Fruticultura y Enología, Pontificia Universidad Católica de Chile, Santiago, Chile
                [3 ]Pasarow Mass Spectrometry Laboratory, Department of Psychiatry and Biobehavioral Sciences, David Geffen School of Medicine, University of California, Los Angeles, CA, USA
                Author notes
                For correspondence. E-mail Alessandra.Devoto@ 123456rhul.ac.uk

                These authors contributed equally to this work.

                Present address: Natural Resources Institute, University of Greenwich, Central Avenue, Chatham Maritime, Kent ME4 4TB, UK.
                Present address: Biometrology, National Physical Laboratory, Hampton Road, Teddington, Middlesex, TW11 0LW, UK.
                Present address: Bio-Protocol LLC, PO Box 2073, Sunnyvale, CA 94087-0073, USA.
                Article
                mcy109
                10.1093/aob/mcy109
                6324744
                29924303
                e41a83fa-395c-4ae8-b95e-4979193e5b77
                © The Author(s) 2018. Published by Oxford University Press on behalf of the Annals of Botany Company.

                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 reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 09 February 2018
                : 27 March 2018
                : 31 May 2018
                Page count
                Pages: 13
                Funding
                Funded by: WestFocus PARK SEED FUND INVESTMENT AWARD
                Award ID: H2020-MSCA-IF-2015 #705427
                Funded by: BBSRC
                Award ID: BB/E021166
                Categories
                Original Articles

                Plant science & Botany
                arabidopsis thaliana,cell suspension culture,coi1,jasmonate,cell cycle,cell wall proteins,primary metabolism,stress signalling

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