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      An Ethylene-Protected Achilles’ Heel of Etiolated Seedlings for Arthropod Deterrence

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          Abstract

          A small family of Kunitz protease inhibitors exists in Arabidopsis thaliana, a member of which (encoded by At1g72290) accomplishes highly specific roles during plant development. Arabidopsis Kunitz-protease inhibitor 1 (Kunitz-PI;1), as we dubbed this protein here, is operative as cysteine PI. Activity measurements revealed that despite the presence of the conserved Kunitz-motif the bacterially expressed Kunitz-PI;1 was unable to inhibit serine proteases such as trypsin and chymotrypsin, but very efficiently inhibited the cysteine protease RESPONSIVE TO DESICCATION 21. Western blotting and cytolocalization studies using mono-specific antibodies recalled Kunitz-PI;1 protein expression in flowers, young siliques and etiolated seedlings. In dark-grown seedlings, maximum Kunitz-PI;1 promoter activity was detected in the apical hook region and apical parts of the hypocotyls. Immunolocalization confirmed Kunitz-PI;1 expression in these organs and tissues. No transmitting tract (NTT) and HECATE 1 (HEC1), two transcription factors previously implicated in the formation of the female reproductive tract in flowers of Arabidopsis, were identified to regulate Kunitz-PI;1 expression in the dark and during greening, with NTT acting negatively and HEC1 acting positively. Laboratory feeding experiments with isopod crustaceans such as Porcellio scaber (woodlouse) and Armadillidium vulgare (pillbug) pinpointed the apical hook as ethylene-protected Achilles’ heel of etiolated seedlings. Because exogenous application of the ethylene precursor 1-aminocyclopropane-1-carboxylic acid (ACC) and mechanical stress (wounding) strongly up-regulated HEC1-dependent Kunitz-PI;1 gene expression, our results identify a new circuit controlling herbivore deterrence of etiolated plants in which Kunitz-PI;1 is involved.

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          Most cited references59

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          Genome-wide insertional mutagenesis of Arabidopsis thaliana.

          J Alonso (2003)
          Over 225,000 independent Agrobacterium transferred DNA (T-DNA) insertion events in the genome of the reference plant Arabidopsis thaliana have been created that represent near saturation of the gene space. The precise locations were determined for more than 88,000 T-DNA insertions, which resulted in the identification of mutations in more than 21,700 of the approximately 29,454 predicted Arabidopsis genes. Genome-wide analysis of the distribution of integration events revealed the existence of a large integration site bias at both the chromosome and gene levels. Insertion mutations were identified in genes that are regulated in response to the plant hormone ethylene.
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            Plant responses to ethylene gas are mediated by SCF(EBF1/EBF2)-dependent proteolysis of EIN3 transcription factor.

            Plants use ethylene gas as a signal to regulate myriad developmental processes and stress responses. The Arabidopsis EIN3 protein is a key transcription factor mediating ethylene-regulated gene expression and morphological responses. Here, we report that EIN3 protein levels rapidly increase in response to ethylene and this response requires several ethylene-signaling pathway components including the ethylene receptors (ETR1 and EIN4), CTR1, EIN2, EIN5, and EIN6. In the absence of ethylene, EIN3 is quickly degraded through a ubiquitin/proteasome pathway mediated by two F box proteins, EBF1 and EBF2. Plants containing mutations in either gene show enhanced ethylene response by stabilizing EIN3, whereas efb1 efb2 double mutants show constitutive ethylene phenotypes. Plants overexpressing either F box gene display ethylene insensitivity and destabilization of EIN3 protein. These results reveal that a ubiquitin/proteasome pathway negatively regulates ethylene responses by targeting EIN3 for degradation, and pinpoint EIN3 regulation as the key step in the response to ethylene.
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              Recent advances in ethylene research.

              Ethylene regulates many aspects of the plant life cycle, including seed germination, root initiation, flower development, fruit ripening, senescence, and responses to biotic and abiotic stresses. It thus plays a key role in responses to the environment that have a direct bearing on a plant's fitness for adaptation and reproduction. In recent years, there have been major advances in our understanding of the molecular mechanisms regulating ethylene synthesis and action. Screening for mutants of the triple response phenotype of etiolated Arabidopsis seedlings, together with map-based cloning and candidate gene characterization of natural mutants from other plant species, has led to the identification of many new genes for ethylene biosynthesis, signal transduction, and response pathways. The simple chemical nature of ethylene contrasts with its regulatory complexity. This is illustrated by the multiplicity of genes encoding the key ethylene biosynthesis enzymes 1-aminocyclopropane-1-carboxylic acid (ACC) synthase and ACC oxidase, multiple ethylene receptors and signal transduction components, and the complexity of regulatory steps involving signalling relays and control of mRNA and protein synthesis and turnover. In addition, there are extensive interactions with other hormones. This review integrates knowledge from the model plant Arabidopsis and other plant species and focuses on key aspects of recent research on regulatory networks controlling ethylene synthesis and its role in flower development and fruit ripening.
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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
                30 August 2016
                2016
                : 7
                : 1246
                Affiliations
                [1] 1Laboratoire de Génétique Moléculaire des Plantes and Biologie Environnementale et Systémique, Université Grenoble-Alpes – Laboratoire de Bioénergétique Fondamentale et Appliquée Grenoble, France
                [2] 2Department of Agricultural and Environmental Sciences–Pee Dee Research and Education Center, Clemson University, Florence SC, USA
                [3] 3Department of Crop and Soil Sciences – Center for Reproductive Biology, School of Molecular Biosciences, Washington State University, Pullman WA, USA
                [4] 4Centro de Biotecnología y Genómica de Plantas, Univerdidad Politécnica de Madrid – Instituto Nacional de Investigación y Tecnología Agraria y Alimentación Madrid, Spain
                Author notes

                Edited by: Péter Poór, University of Szeged, Hungary

                Reviewed by: Clay Carter, University of Minnesota, USA; Jorge Alberto Zavala, National Scientific and Technical Research Council, Argentina

                *Correspondence: Steffen Reinbothe sreinbot@ 123456ujf-grenoble.fr Sachin Rustgi rustgiwsu.edu srustgi@ 123456clemson.edu

                Present address: Edouard Boex-Fontvieille, Laboratoire de Biotechnologies Végétales Appliquées aux Plantes Aromatiques et Médicinales, FRE CNRS3727, Université Jean Monnet, 10 Rue Tréfilerie, Saint-Étienne, France

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

                Article
                10.3389/fpls.2016.01246
                5003848
                0200342c-319e-4aa0-b11b-74b125cbc9ce
                Copyright © 2016 Boex-Fontvieille, Rustgi, von Wettstein, Pollmann, Reinbothe and Reinbothe.

                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) or licensor 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
                : 14 April 2016
                : 05 August 2016
                Page count
                Figures: 9, Tables: 0, Equations: 0, References: 68, Pages: 14, Words: 0
                Categories
                Plant Science
                Original Research

                Plant science & Botany
                skotomorphogenesis,apical hook,arabidopsis thaliana,protease inhibitor action,herbivore deterrence

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