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      Hydrogen Peroxide: Its Role in Plant Biology and Crosstalk with Signalling Networks

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          Abstract

          Hydrogen peroxide (H 2O 2) is steadily gaining more attention in the field of molecular biology research. It is a major REDOX (reduction–oxidation reaction) metabolite and at high concentrations induces oxidative damage to biomolecules, which can culminate in cell death. However, at concentrations in the low nanomolar range, H 2O 2 acts as a signalling molecule and in many aspects, resembles phytohormones. Though its signalling network in plants is much less well characterized than are those of its counterparts in yeast or mammals, accumulating evidence indicates that the role of H 2O 2-mediated signalling in plant cells is possibly even more indispensable. In this review, we summarize hydrogen peroxide metabolism in plants, the sources and sinks of this compound and its transport via peroxiporins. We outline H 2O 2 perception, its direct and indirect effects and known targets in the transcriptional machinery. We focus on the role of H 2O 2 in plant growth and development and discuss the crosstalk between it and phytohormones. In addition to a literature review, we performed a meta-analysis of available transcriptomics data which provided further evidence for crosstalk between H 2O 2 and light, nutrient signalling, temperature stress, drought stress and hormonal pathways.

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          Most cited references217

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          Reactive oxygen species produced by NADPH oxidase regulate plant cell growth.

          Cell expansion is a central process in plant morphogenesis, and the elongation of roots and root hairs is essential for uptake of minerals and water from the soil. Ca2+ influx from the extracellular store is required for (and sets the rates of) cell elongation in roots. Arabidopsis thaliana rhd2 mutants are defective in Ca2+ uptake and consequently cell expansion is compromised--rhd2 mutants have short root hairs and stunted roots. To determine the regulation of Ca2+ acquisition in growing root cells we show here that RHD2 is an NADPH oxidase, a protein that transfers electrons from NADPH to an electron acceptor leading to the formation of reactive oxygen species (ROS). We show that ROS accumulate in growing wild-type (WT) root hairs but their levels are markedly decreased in rhd2 mutants. Blocking the activity of the NADPH oxidase with diphenylene iodonium (DPI) inhibits ROS formation and phenocopies Rhd2-. Treatment of rhd2 roots with ROS partly suppresses the mutant phenotype and stimulates the activity of plasma membrane hyperpolarization-activated Ca2+ channels, the predominant root Ca2+ acquisition system. This indicates that NADPH oxidases control development by making ROS that regulate plant cell expansion through the activation of Ca2+ channels.
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            Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells.

            Drought is a major threat to agricultural production. Plants synthesize the hormone abscisic acid (ABA) in response to drought, triggering a signalling cascade in guard cells that results in stomatal closure, thus reducing water loss. ABA triggers an increase in cytosolic calcium in guard cells ([Ca2+]cyt) that has been proposed to include Ca2+ influx across the plasma membrane. However, direct recordings of Ca2+ currents have been limited and the upstream activation mechanisms of plasma membrane Ca2+ channels remain unknown. Here we report activation of Ca2+-permeable channels in the plasma membrane of Arabidopsis guard cells by hydrogen peroxide. The H2O2-activated Ca2+ channels mediate both influx of Ca2+ in protoplasts and increases in [Ca2+]cyt in intact guard cells. ABA induces the production of H2O2 in guard cells. If H2O2 production is blocked, ABA-induced closure of stomata is inhibited. Moreover, activation of Ca2+ channels by H2O2 and ABA- and H2O2-induced stomatal closing are disrupted in the recessive ABA-insensitive mutant gca2. These data indicate that ABA-induced H2O2 production and the H2O2-activated Ca2+ channels are important mechanisms for ABA-induced stomatal closing.
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              Specific aquaporins facilitate the diffusion of hydrogen peroxide across membranes.

              The metabolism of aerobic organisms continuously produces reactive oxygen species. Although potentially toxic, these compounds also function in signaling. One important feature of signaling compounds is their ability to move between different compartments, e.g. to cross membranes. Here we present evidence that aquaporins can channel hydrogen peroxide (H2O2). Twenty-four aquaporins from plants and mammals were screened in five yeast strains differing in sensitivity toward oxidative stress. Expression of human AQP8 and plant Arabidopsis TIP1;1 and TIP1;2 in yeast decreased growth and survival in the presence of H2O2. Further evidence for aquaporin-mediated H2O2 diffusion was obtained by a fluorescence assay with intact yeast cells using an intracellular reactive oxygen species-sensitive fluorescent dye. Application of silver ions (Ag+), which block aquaporin-mediated water diffusion in a fast kinetics swelling assay, also reversed both the aquaporin-dependent growth repression and the H2O2-induced fluorescence. Our results present the first molecular genetic evidence for the diffusion of H2O2 through specific members of the aquaporin family.
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                Author and article information

                Journal
                Int J Mol Sci
                Int J Mol Sci
                ijms
                International Journal of Molecular Sciences
                MDPI
                1422-0067
                18 September 2018
                September 2018
                : 19
                : 9
                : 2812
                Affiliations
                [1 ]Department of Molecular Biology and Radiobiology, Faculty of AgriSciences Mendel University in Brno, 613 00 Brno, Czech Republic; habanova.ha@ 123456gmail.com (H.H.); miroslavberka94@ 123456gmail.com (M.B.); luklovam@ 123456gmail.com (M.L.); brzoboha@ 123456ibp.cz (B.B.)
                [2 ]Phytophthora Research Centre, Faculty of AgriSciences, Mendel University in Brno, 613 00 Brno, Czech Republic
                [3 ]CEITEC—Central European Institute of Technology, Faculty of AgriSciences Mendel University in Brno, 613 00 Brno, Czech Republic
                [4 ]Brno Ph.D. Talent, South Moravian Centre for International Mobility, 602 00 Brno, Czech Republic
                [5 ]Institute of Biophysics AS CR, 613 00 Brno, Czech Republic
                Author notes
                [* ]Correspondence: martincerny83@ 123456gmail.com ; Tel.: +420-545-133-374
                [†]

                These authors contributed equally to this work.

                Author information
                https://orcid.org/0000-0002-0651-4219
                https://orcid.org/0000-0002-1552-1314
                Article
                ijms-19-02812
                10.3390/ijms19092812
                6163176
                30231521
                7332edb7-3e09-41ca-988d-a790e86e7705
                © 2018 by the author.

                Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( http://creativecommons.org/licenses/by/4.0/).

                History
                : 24 July 2018
                : 15 September 2018
                Categories
                Review

                Molecular biology
                h2o2,plant hormone,signalling,growth and development,stress
                Molecular biology
                h2o2, plant hormone, signalling, growth and development, stress

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