Cargando…

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 H(2)O(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(2)O(2)...

Descripción completa

Detalles Bibliográficos
Autores principales: Pilarska, Maria, Wiciarz, Monika, Jajić, Ivan, Kozieradzka-Kiszkurno, Małgorzata, Dobrev, Petre, Vanková, Radomíra, Niewiadomska, Ewa
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4972836/
https://www.ncbi.nlm.nih.gov/pubmed/27540390
http://dx.doi.org/10.3389/fpls.2016.01179
_version_ 1782446300469395456
author Pilarska, Maria
Wiciarz, Monika
Jajić, Ivan
Kozieradzka-Kiszkurno, Małgorzata
Dobrev, Petre
Vanková, Radomíra
Niewiadomska, Ewa
author_facet Pilarska, Maria
Wiciarz, Monika
Jajić, Ivan
Kozieradzka-Kiszkurno, Małgorzata
Dobrev, Petre
Vanková, Radomíra
Niewiadomska, Ewa
author_sort Pilarska, Maria
collection PubMed
description Isolated thylakoids from halophytic Eutrema salsugineum (Thellungiella salsuginea) produces more H(2)O(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(2)O(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 [Formula: see text] /H(2)O(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(2)O(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(2)O(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.
format Online
Article
Text
id pubmed-4972836
institution National Center for Biotechnology Information
language English
publishDate 2016
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-49728362016-08-18 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 Pilarska, Maria Wiciarz, Monika Jajić, Ivan Kozieradzka-Kiszkurno, Małgorzata Dobrev, Petre Vanková, Radomíra Niewiadomska, Ewa Front Plant Sci Plant Science Isolated thylakoids from halophytic Eutrema salsugineum (Thellungiella salsuginea) produces more H(2)O(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(2)O(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 [Formula: see text] /H(2)O(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(2)O(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(2)O(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. Frontiers Media S.A. 2016-08-04 /pmc/articles/PMC4972836/ /pubmed/27540390 http://dx.doi.org/10.3389/fpls.2016.01179 Text en Copyright © 2016 Pilarska, Wiciarz, Jajić, Kozieradzka-Kiszkurno, Dobrev, Vanková and Niewiadomska. http://creativecommons.org/licenses/by/4.0/ 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.
spellingShingle Plant Science
Pilarska, Maria
Wiciarz, Monika
Jajić, Ivan
Kozieradzka-Kiszkurno, Małgorzata
Dobrev, Petre
Vanková, Radomíra
Niewiadomska, Ewa
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 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_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_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
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4972836/
https://www.ncbi.nlm.nih.gov/pubmed/27540390
http://dx.doi.org/10.3389/fpls.2016.01179
work_keys_str_mv AT pilarskamaria adifferentpatternofproductionandscavengingofreactiveoxygenspeciesinhalophyticeutremasalsugineumthellungiellasalsugineaplantsincomparisontoarabidopsisthalianaanditsrelationtosaltstresssignaling
AT wiciarzmonika adifferentpatternofproductionandscavengingofreactiveoxygenspeciesinhalophyticeutremasalsugineumthellungiellasalsugineaplantsincomparisontoarabidopsisthalianaanditsrelationtosaltstresssignaling
AT jajicivan adifferentpatternofproductionandscavengingofreactiveoxygenspeciesinhalophyticeutremasalsugineumthellungiellasalsugineaplantsincomparisontoarabidopsisthalianaanditsrelationtosaltstresssignaling
AT kozieradzkakiszkurnomałgorzata adifferentpatternofproductionandscavengingofreactiveoxygenspeciesinhalophyticeutremasalsugineumthellungiellasalsugineaplantsincomparisontoarabidopsisthalianaanditsrelationtosaltstresssignaling
AT dobrevpetre adifferentpatternofproductionandscavengingofreactiveoxygenspeciesinhalophyticeutremasalsugineumthellungiellasalsugineaplantsincomparisontoarabidopsisthalianaanditsrelationtosaltstresssignaling
AT vankovaradomira adifferentpatternofproductionandscavengingofreactiveoxygenspeciesinhalophyticeutremasalsugineumthellungiellasalsugineaplantsincomparisontoarabidopsisthalianaanditsrelationtosaltstresssignaling
AT niewiadomskaewa adifferentpatternofproductionandscavengingofreactiveoxygenspeciesinhalophyticeutremasalsugineumthellungiellasalsugineaplantsincomparisontoarabidopsisthalianaanditsrelationtosaltstresssignaling
AT pilarskamaria differentpatternofproductionandscavengingofreactiveoxygenspeciesinhalophyticeutremasalsugineumthellungiellasalsugineaplantsincomparisontoarabidopsisthalianaanditsrelationtosaltstresssignaling
AT wiciarzmonika differentpatternofproductionandscavengingofreactiveoxygenspeciesinhalophyticeutremasalsugineumthellungiellasalsugineaplantsincomparisontoarabidopsisthalianaanditsrelationtosaltstresssignaling
AT jajicivan differentpatternofproductionandscavengingofreactiveoxygenspeciesinhalophyticeutremasalsugineumthellungiellasalsugineaplantsincomparisontoarabidopsisthalianaanditsrelationtosaltstresssignaling
AT kozieradzkakiszkurnomałgorzata differentpatternofproductionandscavengingofreactiveoxygenspeciesinhalophyticeutremasalsugineumthellungiellasalsugineaplantsincomparisontoarabidopsisthalianaanditsrelationtosaltstresssignaling
AT dobrevpetre differentpatternofproductionandscavengingofreactiveoxygenspeciesinhalophyticeutremasalsugineumthellungiellasalsugineaplantsincomparisontoarabidopsisthalianaanditsrelationtosaltstresssignaling
AT vankovaradomira differentpatternofproductionandscavengingofreactiveoxygenspeciesinhalophyticeutremasalsugineumthellungiellasalsugineaplantsincomparisontoarabidopsisthalianaanditsrelationtosaltstresssignaling
AT niewiadomskaewa differentpatternofproductionandscavengingofreactiveoxygenspeciesinhalophyticeutremasalsugineumthellungiellasalsugineaplantsincomparisontoarabidopsisthalianaanditsrelationtosaltstresssignaling