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      Ethylene response pathway modulates attractiveness of plant roots to soybean cyst nematode Heterodera glycines

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          Abstract

          Plant parasitic nematodes respond to root exudates to locate their host roots. In our studies second stage juveniles of Heterodera glycines, the soybean cyst nematode (SCN), quickly migrated to soybean roots in Pluronic F-127 gel. Roots of soybean and non-host Arabidopsis treated with the ethylene (ET)-synthesis inhibitor aminoethoxyvinylglycine (AVG) were more attractive to SCN than untreated roots, and significantly more nematodes penetrated into roots. Moreover, Arabidopsis ET insensitive mutants ( ein2, ein2-1, ein2-5, ein3-1, ein5-1, and ein6) were more attractive than wild-type plants. Conversely, the constitutive triple-response mutant ctr1-1, was less attractive to SCN. While ET receptor gain-of-function mutant ein4-1 attracted more SCN than the wild-type, there were no significant differences in attractiveness between another gain-of-function ET receptor mutant, etr1-3, or the loss-of-function mutants etr1-7 and ers1-3 and the wild type. Expression of the reporter construct EBS: β-glucuronidase ( GUS) was detected in Arabidopsis root tips as early as 6 h post infection, indicating that ET signaling was activated in Arabidopsis early by SCN infection. These results suggest that an active ET signaling pathway reduces root attractiveness to SCN in a way similar to that reported for root-knot nematodes, but opposite to that suggested for the sugar beet cyst nematode Heterodera schachtii.

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          CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the raf family of protein kinases.

          We isolated a recessive Arabidopsis mutant, ctr1, that constitutively exhibits seedling and adult phenotypes observed in plants treated with the plant hormone ethylene. The ctr1 adult morphology can be phenocopied by treatment of wild-type plants with exogenous ethylene and is due, at least in part, to inhibition of cell elongation. Seedlings and adult ctr1 plants show constitutive expression of ethylene-regulated genes. The epistasis of ctr1 and other ethylene response mutants has defined the position of CTR1 in the ethylene signal transduction pathway. The CTR1 gene has been cloned, and the DNA sequences of four mutant alleles were determined. The gene encodes a putative serine/threonine protein kinase that is most closely related to the Raf protein kinase family.
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            EIN2, a bifunctional transducer of ethylene and stress responses in Arabidopsis.

            Ethylene regulates plant growth, development, and responsiveness to a variety of stresses. Cloning of the Arabidopsis EIN2 gene identifies a central component of the ethylene signaling pathway. The amino-terminal integral membrane domain of EIN2 shows similarity to the disease-related Nramp family of metal-ion transporters. Expression of the EIN2 CEND is sufficient to constitutively activate ethylene responses and restores responsiveness to jasmonic acid and paraquat-induced oxygen radicals to mutant plants. EIN2 is thus recognized as a molecular link between previously distinct hormone response pathways. Plants may use a combinatorial mechanism for assessing various stresses by enlisting a common set of signaling molecules.
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              Activation of the ethylene gas response pathway in Arabidopsis by the nuclear protein ETHYLENE-INSENSITIVE3 and related proteins.

              Mutations in the Arabidopsis ETHYLENE-INSENSITIVE3 (EIN3) gene severely limit a plant's response to the gaseous hormone ethylene. ein3 mutants show a loss of ethylene-mediated effects including gene expression, the triple response, cell growth inhibition, and accelerated senescence. EIN3 acts downstream of the histidine kinase ethylene receptor, ETR1, and the Raf-like kinase, CTR1. The EIN3 gene encodes a novel nuclear-localized protein that shares sequence similarity, structural features, and genetic function with three EIN3-LIKE (EIL) proteins. In addition to EIN3, EIL1 orEIL2 were able to complement ein3, suggesting their participation in the ethylene signaling pathway. Overexpression of EIN3 or EIL1 in wild-type or ethylene-insensitive2 plants conferred constitutive ethylene phenotypes, indicating their sufficiency for activation of the pathway in the absence of ethylene.
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                Author and article information

                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group
                2045-2322
                23 January 2017
                2017
                : 7
                : 41282
                Affiliations
                [1 ]Key Laboratory of Mollisols Agroecology, Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences , Harbin 150081 China
                [2 ]Department of Plant Pathology, University of California , Davis, CA 95616 USA
                Author notes
                Article
                srep41282
                10.1038/srep41282
                5256374
                28112257
                a1836871-0942-4767-8794-f6129c6d5d2a
                Copyright © 2017, The Author(s)

                This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

                History
                : 13 July 2016
                : 19 December 2016
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