81
views
0
recommends
+1 Recommend
0 collections
    0
    shares
      • Record: found
      • Abstract: found
      • Article: found
      Is Open Access

      A Different Pattern of Production and Scavenging of Reactive Oxygen Species in Halophytic Eutrema salsugineum (Thellungiella salsuginea) Plants in Comparison to Arabidopsis thaliana and Its Relation to Salt Stress Signaling

      research-article

      Read this article at

      Bookmark
          There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

          Abstract

          Isolated thylakoids from halophytic Eutrema salsugineum ( Thellungiella salsuginea) produces more H 2O 2 in comparison to glycophytic Arabidopsis thaliana. The first objective of this study was to verify whether this feature is relevant also to the intact chloroplasts and leaves. Enhanced H 2O 2 levels in chloroplasts and leaves of E. salsugineum were positively verified with several methods (electron microscopy, staining with Amplex Red and with diaminobenzidine). This effect was associated with a decreased ratio of O•–2 /H 2O 2 in E. salsugineum in comparison to A. thaliana as detected by electron paramagnetic resonance method. As a next step, we tested how this specific ROS signature of halophytic species affects the antioxidant status and down-stream components of ROS signaling. Comparison of enzymatic antioxidants revealed a decreased activity of ascorbate peroxidase (APX), enhanced activity of glutathione peroxidase, and the presence of thylakoid-bound forms of iron superoxide dismutase (FeSOD) and APX in E. salsugineum. These cues were, however, independent from application of salt stress. The typical H 2O 2-dependent cellular responses, namely the levels of glucosinolates and stress-related hormones were determined. The total glucosinolate content in E. salsugineum water-treated leaves was higher than in A. thaliana and increased after salinity treatment. Treatment with salinity up-regulated all of tested stress hormones, their precursors and catabolites [abscisic acid (ABA), dihydrophaseic acid, phaseic acid, 1-aminocyclopropane-1-carboxylic acid, salicylic acid, jasmonic acid, cis-(+)-12-oxo-phytodienoic acid and jasmonoyl- L-isoleucine] in A. thaliana, whereas in E. salsugineum only a stimulation in ethylene synthesis and ABA catabolism was noted. Obtained results suggest that constitutively enhanced H 2O 2 generation in chloroplasts of E. salsugineum might be a crucial component of stress-prepardeness of this halophytic species. It shapes a very efficient antioxidant protection (in which glucosinolates might play a specific role) and a fine tuning of hormonal signaling to suppress the cell death program directed by jasmonate pathway.

          Related collections

          Most cited references49

          • Record: found
          • Abstract: found
          • Article: not found

          ROS homeostasis in halophytes in the context of salinity stress tolerance.

          Halophytes are defined as plants that are adapted to live in soils containing high concentrations of salt and benefiting from it, and thus represent an ideal model to understand complex physiological and genetic mechanisms of salinity stress tolerance. It is also known that oxidative stress signalling and reactive oxygen species (ROS) detoxification are both essential components of salinity stress tolerance mechanisms. This paper comprehensively reviews the differences in ROS homeostasis between halophytes and glycophytes in an attempt to answer the questions of whether stress-induced ROS production is similar between halophytes and glycophytes; is the superior salinity tolerance in halophytes attributed to higher antioxidant activity; and is there something special about the specific 'pool' of enzymatic and non-enzymatic antioxidants in halophytes. We argue that truly salt-tolerant species possessing efficient mechanisms for Na(+) exclusion from the cytosol may not require a high level of antioxidant activity, as they simply do not allow excessive ROS production in the first instance. We also suggest that H2O2 'signatures' may operate in plant signalling networks, in addition to well-known cytosolic calcium 'signatures'. According to the suggested concept, the intrinsically higher superoxide dismutase (SOD) levels in halophytes are required for rapid induction of the H2O2 'signature', and to trigger a cascade of adaptive responses (both genetic and physiological), while the role of other enzymatic antioxidants may be in decreasing the basal levels of H2O2, once the signalling has been processed. Finally, we emphasize the importance of non-enzymatic antioxidants as the only effective means to prevent detrimental effects of hydroxyl radicals on cellular structures.
            Bookmark
            • Record: found
            • Abstract: found
            • Article: not found

            A thiol peroxidase is an H2O2 receptor and redox-transducer in gene activation.

            The Yap1 transcription factor regulates hydroperoxide homeostasis in S. cerevisiae. Yap1 is activated by oxidation when hydroperoxide levels increase. We show that Yap1 is not directly oxidized by hydroperoxide. We identified the glutathione peroxidase (GPx)-like enzyme Gpx3 as a second component of the pathway, serving the role of sensor and transducer of the hydroperoxide signal to Yap1. When oxidized by H2O2, Gpx3 Cys36 bridges Yap1 Cys598 by a disulfide bond. This intermolecular disulfide bond is then resolved into a Yap1 intramolecular disulfide bond, the activated form of the regulator. Thioredoxin turns off the pathway by reducing both sensor and regulator. These data reveal a redox-signaling function for a GPx-like enzyme and elucidate a eukaryotic hydroperoxide-sensing mechanism. Gpx3 is thus a hydroperoxide receptor and redox-transducer.
              Bookmark
              • Record: found
              • Abstract: found
              • Article: not found

              Rapid induction of distinct stress responses after the release of singlet oxygen in Arabidopsis.

              The conditional fluorescent (flu) mutant of Arabidopsis accumulates the photosensitizer protochlorophyllide in the dark. After a dark-to-light shift, the generation of singlet oxygen, a nonradical reactive oxygen species, starts within the first minute of illumination and was shown to be confined to plastids. Immediately after the shift, plants stopped growing and developed necrotic lesions. These early stress responses of the flu mutant do not seem to result merely from physicochemical damage. Peroxidation of chloroplast membrane lipids in these plants started rapidly and led to the transient and selective accumulation of a stereospecific and regiospecific isomer of hydroxyoctadecatrieonic acid, free (13S)-HOTE, that could be attributed almost exclusively to the enzymatic oxidation of linolenic acid. Within the first 15 min of reillumination, distinct sets of genes were activated that were different from those induced by superoxide/hydrogen peroxide. Collectively, these results demonstrate that singlet oxygen does not act primarily as a toxin but rather as a signal that activates several stress-response pathways. Its biological activity in Arabidopsis exhibits a high degree of specificity that seems to be derived from the chemical identity of this reactive oxygen species and/or the intracellular location at which it is generated.
                Bookmark

                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
                04 August 2016
                2016
                : 7
                : 1179
                Affiliations
                [1] 1The Franciszek Górski Institute of Plant Physiology – Polish Academy of Sciences Kraków, Poland
                [2] 2Department of Plant Physiology and Biochemistry, Faculty of Biochemistry Biophysics and Biotechnology, Jagiellonian University Kraków, Poland
                [3] 3Department of Plant Cytology and Embryology, University of Gdańsk Gdańsk, Poland
                [4] 4Institute of Experimental Botany AS CR Prague, Czech Republic
                Author notes

                Edited by: Mirza Hasanuzzaman, Sher-e-Bangla Agricultural University, Bangladesh

                Reviewed by: Sergey Shabala, University of Tasmania, Australia; Kamrun Nahar, Kagawa University, Japan

                *Correspondence: Ewa Niewiadomska, e.niewiadomska@ 123456ifr-pan.edu.pl

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

                Article
                10.3389/fpls.2016.01179
                4972836
                27540390
                584f3927-7367-48b6-ac3c-9432b66f06e8
                Copyright © 2016 Pilarska, Wiciarz, Jajić, Kozieradzka-Kiszkurno, Dobrev, Vanková and Niewiadomska.

                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
                : 30 April 2016
                : 22 July 2016
                Page count
                Figures: 8, Tables: 0, Equations: 0, References: 60, Pages: 12, Words: 0
                Funding
                Funded by: Narodowe Centrum Nauki 10.13039/501100004281
                Award ID: 2011/03/B/NZ9/01619
                Categories
                Plant Science
                Original Research

                Plant science & Botany
                chloroplast,glucosinolates,halophyte,hydrogen peroxide,salinity,stress hormones
                Plant science & Botany
                chloroplast, glucosinolates, halophyte, hydrogen peroxide, salinity, stress hormones

                Comments

                Comment on this article

                scite_
                0
                0
                0
                0
                Smart Citations
                0
                0
                0
                0
                Citing PublicationsSupportingMentioningContrasting
                View Citations

                See how this article has been cited at scite.ai

                scite shows how a scientific paper has been cited by providing the context of the citation, a classification describing whether it supports, mentions, or contrasts the cited claim, and a label indicating in which section the citation was made.

                Similar content458

                Cited by12

                Most referenced authors659