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

Isolated thylakoids from halophytic Eutrema salsugineum (Thellungiella salsuginea) produces more H2O2 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 H2O2 levels i...

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Main Authors: Maria Pilarska, Monika Wiciarz, Ivan Jajić, Małgorzata Kozieradzka-Kiszkurno, Petre Dobrev, Radomira Vanková, Ewa Niewiadomska
Format: Article
Language:English
Published: Frontiers Media S.A. 2016-08-01
Series:Frontiers in Plant Science
Subjects:
Online Access:http://journal.frontiersin.org/Journal/10.3389/fpls.2016.01179/full
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spelling doaj-a8084ebd6e294d97ac3e0c94ab622a622020-11-25T00:10:17ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2016-08-01710.3389/fpls.2016.01179207766A 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 signalingMaria Pilarska0Monika Wiciarz1Ivan Jajić2Małgorzata Kozieradzka-Kiszkurno3Petre Dobrev4Radomira Vanková5Ewa Niewiadomska6Institute of Plant Physiology Polish Academy of SciencesFaculty of Biochemistry Biophysics and Biotechnology, Jagiellonian UniversityFaculty of Biochemistry Biophysics and Biotechnology, Jagiellonian UniversityFaculty of Biology, University of GdańskInstitute of Experimental Botany AS CRInstitute of Experimental Botany AS CRInstitute of Plant Physiology Polish Academy of SciencesIsolated thylakoids from halophytic Eutrema salsugineum (Thellungiella salsuginea) produces more H2O2 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 H2O2 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 O2.-/H2O2 in E.s in comparison to A.thaliana as detected by electron paramagnetic resonance (EPR) method. As a next step, we tested how this specific ROS signature of halophytic species affect 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 (GPX), and the presence of thylakoid-bound forms of iron superoxide dismutase (FeSOD) and ascorbate peroxidase (APX) in E.s.. These cues were, however, independent from application of salt stress. The typical H2O2-dependent cellular responses, namely the levels of glucosinolates and stress-related hormones were determined. The total glucosinolate content in E.s water-treated leaves was higher than in A.t. and increased after salinity treatment. Treatment with salinity up-regulated all of tested stress hormones, their precursors and catabolites (abscisic acid, dihydrophaseic acid, phaseic acid, 1-aminocyclopropane-1-carboxylic acid, salicylic acid, jasmonic acid, cis-(+)-12-oxo-phytodienoic acid and jasmonoyl-L-isoleucine) in A.t., whereas in E.s. only a stimulation in ethylene synthesis and abscisic acid catabolism was noted. Obtained results suggest that constitutively enhanced H2O2 generation in chloroplasts of E.s. 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.http://journal.frontiersin.org/Journal/10.3389/fpls.2016.01179/fullGlucosinolatesHydrogen PeroxidechloroplastSalinitystress hormoneshalophyte
collection DOAJ
language English
format Article
sources DOAJ
author Maria Pilarska
Monika Wiciarz
Ivan Jajić
Małgorzata Kozieradzka-Kiszkurno
Petre Dobrev
Radomira Vanková
Ewa Niewiadomska
spellingShingle Maria Pilarska
Monika Wiciarz
Ivan Jajić
Małgorzata Kozieradzka-Kiszkurno
Petre Dobrev
Radomira Vanková
Ewa Niewiadomska
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
Frontiers in Plant Science
Glucosinolates
Hydrogen Peroxide
chloroplast
Salinity
stress hormones
halophyte
author_facet Maria Pilarska
Monika Wiciarz
Ivan Jajić
Małgorzata Kozieradzka-Kiszkurno
Petre Dobrev
Radomira Vanková
Ewa Niewiadomska
author_sort Maria Pilarska
title 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
title_short 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
title_full 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
title_fullStr 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
title_full_unstemmed 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
title_sort 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
publisher Frontiers Media S.A.
series Frontiers in Plant Science
issn 1664-462X
publishDate 2016-08-01
description Isolated thylakoids from halophytic Eutrema salsugineum (Thellungiella salsuginea) produces more H2O2 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 H2O2 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 O2.-/H2O2 in E.s in comparison to A.thaliana as detected by electron paramagnetic resonance (EPR) method. As a next step, we tested how this specific ROS signature of halophytic species affect 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 (GPX), and the presence of thylakoid-bound forms of iron superoxide dismutase (FeSOD) and ascorbate peroxidase (APX) in E.s.. These cues were, however, independent from application of salt stress. The typical H2O2-dependent cellular responses, namely the levels of glucosinolates and stress-related hormones were determined. The total glucosinolate content in E.s water-treated leaves was higher than in A.t. and increased after salinity treatment. Treatment with salinity up-regulated all of tested stress hormones, their precursors and catabolites (abscisic acid, dihydrophaseic acid, phaseic acid, 1-aminocyclopropane-1-carboxylic acid, salicylic acid, jasmonic acid, cis-(+)-12-oxo-phytodienoic acid and jasmonoyl-L-isoleucine) in A.t., whereas in E.s. only a stimulation in ethylene synthesis and abscisic acid catabolism was noted. Obtained results suggest that constitutively enhanced H2O2 generation in chloroplasts of E.s. 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.
topic Glucosinolates
Hydrogen Peroxide
chloroplast
Salinity
stress hormones
halophyte
url http://journal.frontiersin.org/Journal/10.3389/fpls.2016.01179/full
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