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      Evidence for the Involvement of Electrical, Calcium and ROS Signaling in the Systemic Regulation of Non-Photochemical Quenching and Photosynthesis

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          Abstract

          In contrast to the function of reactive oxygen species, calcium, hormones and small RNAs in systemic signaling, systemic electrical signaling in plants is poorly studied and understood. Pulse amplitude-modulated Chl fluorescence imaging and surface electrical potential measurements accompanied by pharmacological treatments were employed to study stimuli-induced electrical signals in leaves from a broad range of plant species and in Arabidopsis thaliana mutants. Here we report that rapid electrical signals in response to a local heat stimulus regulate systemic changes in non-photochemical quenching (NPQ) and PSII quantum efficiency. Both stimuli-induced systemic changes in NPQ and photosynthetic capacity as well as electrical signaling depended on calcium channel activity. Use of an Arabidopsis respiratory burst oxidase homolog D (RBOHD) mutant ( rbohD) as well as an RBOH inhibitor further suggested a cross-talk between ROS and electrical signaling. Our results suggest that higher plants evolved a complex rapid long-distance calcium-dependent electrical systemic signaling in response to local stimuli that regulates and optimizes the balance between PSII quantum efficiency and excess energy dissipation in the form of heat by means of NPQ.

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          Most cited references39

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          Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response.

          Reactive oxygen intermediates (ROI) are strongly associated with plant defense responses. The origin of these ROI has been controversial. Arabidopsis respiratory burst oxidase homologues (rboh genes) have been proposed to play a role in ROI generation. We analyzed lines carrying dSpm insertions in the highly expressed AtrbohD and AtrbohF genes. Both are required for full ROI production observed during incompatible interactions with the bacterial pathogen Pseudomonas syringae pv. tomato DC3000(avrRpm1) and the oomycete parasite Peronospora parasitica. We also observed reduced cell death, visualized by trypan blue stain and reduced electrolyte leakage, in the Atrboh mutants after DC3000(avrRpm1) inoculation. However, enhanced cell death is observed after infection of mutant lines with P. parasitica. Paradoxically, although atrbohD mutation eliminated the majority of total ROI production, atrbohF mutation exhibited the strongest effect on cell death.
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            The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli.

            Cell-to-cell communication and long-distance signaling play a key role in the response of plants to pests, mechanical wounding, and extreme environmental conditions. Here, we report on a rapid systemic signal in Arabidopsis thaliana that traveled at a rate of 8.4 centimeters per minute and was dependent on the respiratory burst oxidase homolog D (RbohD) gene. Signal propagation was accompanied by the accumulation of reactive oxygen species (ROS) in the extracellular spaces between cells and was inhibited by the suppression of ROS accumulation at locations distant from the initiation site. The rapid systemic signal was triggered by wounding, heat, cold, high-intensity light, and salinity stresses. Our results reveal the profound role that ROS play in mediating rapid, long-distance, cell-to-cell propagating signals in plants.
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              Increase in salicylic Acid at the onset of systemic acquired resistance in cucumber.

              In an effort to identify the signal compound that mediates systemic acquired resistance (SAR), changes in the content of phloem sap were monitored in cucumber plants inoculated with either tobacco necrosis virus or the fungal pathogen Colletotrichum lagenarium. The concentration of a fluorescent metabolite was observed to increase transiently after inoculation, with a peak reached before SAR was detected. The compound was purified and identified by gas chromatography-mass spectrometry as salicylic acid, a known exogenous inducer of resistance. The data suggest that salicylic acid could function as the endogenous signal in the transmission of SAR in cucumber.
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                Author and article information

                Journal
                Plant Cell Physiol
                Plant Cell Physiol
                pcp
                Plant and Cell Physiology
                Oxford University Press
                0032-0781
                1471-9053
                February 2017
                10 February 2017
                10 February 2017
                : 58
                : 2
                : 207-215
                Affiliations
                [1 ]Department of Plant Genetics, Breeding and Biotechnology, Faculty of Horticulture, Biotechnology and Landscape Architecture, Warsaw University of Life Sciences SGGW, Nowoursynowska 159, 02-776 Warsaw
                [2 ]Department of Biological Sciences, College of Arts and Sciences, University of North Texas, Denton, TX 76203-5017, USA
                Author notes
                [* ]Corresponding author: E-mail, stanislaw_karpinski@ 123456sggw.pl ; Fax, +48225932152.
                Article
                pcw232
                10.1093/pcp/pcw232
                5444583
                28184891
                0f39bdaf-4c4c-4d6b-a647-3965de3ef10d
                © The Author 2017. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License ( http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com

                History
                : 9 May 2016
                : 24 December 2016
                Page count
                Pages: 9
                Funding
                Funded by: National Science Centre project
                Award ID: UMO-2012/07/B/NZ3/00228
                Award ID: UMO-2014/14/A/NZ1/00218
                Award ID: POKL.04.03.00-00-042/12-00
                Funded by: European Social Fund
                Funded by: USA National Science Foundation
                Award ID: IOS-1353886, IOS-0639964 and IOS-0743954
                Funded by: University of North Texas, College of Arts
                Categories
                Rapid Papers

                Plant science & Botany
                calcium signaling,chlorophyll fluorescence,electrical signals,photosynthesis,reactive oxygen species,systemic acquired acclimation

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