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      Molecular Mechanisms of Tungsten Toxicity Differ for Glycine max Depending on Nitrogen Regime

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          Abstract

          Tungsten (W) finds increasing application in military, aviation and household appliance industry, opening new paths into the environment. Since W shares certain chemical properties with the essential plant micronutrient molybdenum (Mo), it is proposed to inhibit enzymatic activity of molybdoenzymes [e.g., nitrate reductase (NR)] by replacing the Mo-ion bound to the co-factor. Recent studies suggest that W, much like other heavy metals, also exerts toxicity on its own. To create a comprehensive picture of tungsten stress, this study investigated the effects of W on growth and metabolism of soybean ( Glycine max), depending on plant nitrogen regime [nitrate fed (N fed) vs. symbiotic N 2 fixation (N fix)] by combining plant physiological data (biomass production, starch and nutrient content, N 2 fixation, nitrate reductase activity) with root and nodule proteome data. Irrespective of N regime, NR activity and total N decreased with increasing W concentrations. Nodulation and therefore also N 2 fixation strongly declined at high W concentrations, particularly in N fix plants. However, N 2 fixation rate (g N fixed g −1 nodule dwt) remained unaffected by increasing W concentrations. Proteomic analysis revealed a strong decline in leghemoglobin and nitrogenase precursor levels (NifD), as well as an increase in abundance of proteins involved in secondary metabolism in N fix nodules. Taken together this indicates that, in contrast to the reported direct inhibition of NR, N 2 fixation appears to be indirectly inhibited by a decrease in nitrogenase synthesis due to W induced changes in nodule oxygen levels of N fix plants. Besides N metabolism, plants exhibited a strong reduction of shoot (both N regimes) and root (N fed only) biomass, an imbalance in nutrient levels and a failure of carbon metabolic pathways accompanied by an accumulation of starch at high tungsten concentrations, independent of N-regime. Proteomic data (available via ProteomeXchange with identifier PXD010877) demonstrated that the response to high W concentrations was independent of nodule functionality and dominated by several peroxidases and other general stress related proteins. Based on an evaluation of several W responsive proteotypic peptides, we identified a set of protein markers of W stress and possible targets for improved stress tolerance.

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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
                02 April 2019
                2019
                : 10
                : 367
                Affiliations
                [1] 1Division of Molecular Systems Biology, Department of Ecogenomics and Systems Biology, University of Vienna , Vienna, Austria
                [2] 2Department of Forest and Soil Sciences, Institute of Soil Research, University of Natural Resources and Life Sciences Vienna , Tulln, Austria
                [3] 3Division of Terrestrial Ecosystem Research, Department of Microbiology and Ecosystem Science, University of Vienna , Vienna, Austria
                Author notes

                Edited by: Andrew Wood, Southern Illinois University Carbondale, United States

                Reviewed by: Manuel Tejada-Jimenez, Universidad de Córdoba, Spain; Juan Jose Rios, Center for Edaphology and Applied Biology of Segura (CSIC), Spain

                *Correspondence: Stefanie Wienkoop stefanie.wienkoop@ 123456univie.ac.at

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

                Article
                10.3389/fpls.2019.00367
                6454624
                72c7a3b8-3a4f-4baa-9094-752e91534ae9
                Copyright © 2019 Preiner, Wienkoop, Weckwerth and Oburger.

                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(s) 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
                : 02 October 2018
                : 08 March 2019
                Page count
                Figures: 7, Tables: 2, Equations: 2, References: 135, Pages: 23, Words: 17909
                Funding
                Funded by: Austrian Science Fund 10.13039/501100002428
                Award ID: P 25942-N28
                Award ID: W 1257
                Categories
                Plant Science
                Original Research

                Plant science & Botany
                glycine max,tungsten toxicity,n-assimilation,nitrate reductase,15n natural abundance,symbiotic n2 fixation,starch accumulation

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