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Chloroplast-derived photo-oxidative stress causes changes in H(2)O(2) and E(GSH) in other subcellular compartments
Metabolic fluctuations in chloroplasts and mitochondria can trigger retrograde signals to modify nuclear gene expression. Mobile signals likely to be involved are reactive oxygen species (ROS), which can operate protein redox switches by oxidation of specific cysteine residues. Redox buffers, such a...
Autores principales: | , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Oxford University Press
2021
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8154069/ https://www.ncbi.nlm.nih.gov/pubmed/33793922 http://dx.doi.org/10.1093/plphys/kiaa095 |
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author | Ugalde, José Manuel Fuchs, Philippe Nietzel, Thomas Cutolo, Edoardo A Homagk, Maria Vothknecht, Ute C Holuigue, Loreto Schwarzländer, Markus Müller-Schüssele, Stefanie J Meyer, Andreas J |
author_facet | Ugalde, José Manuel Fuchs, Philippe Nietzel, Thomas Cutolo, Edoardo A Homagk, Maria Vothknecht, Ute C Holuigue, Loreto Schwarzländer, Markus Müller-Schüssele, Stefanie J Meyer, Andreas J |
author_sort | Ugalde, José Manuel |
collection | PubMed |
description | Metabolic fluctuations in chloroplasts and mitochondria can trigger retrograde signals to modify nuclear gene expression. Mobile signals likely to be involved are reactive oxygen species (ROS), which can operate protein redox switches by oxidation of specific cysteine residues. Redox buffers, such as the highly reduced glutathione pool, serve as reservoirs of reducing power for several ROS-scavenging and ROS-induced damage repair pathways. Formation of glutathione disulfide and a shift of the glutathione redox potential (E(GSH)) toward less negative values is considered as hallmark of several stress conditions. Here we used the herbicide methyl viologen (MV) to generate ROS locally in chloroplasts of intact Arabidopsis (Arabidopsis thaliana) seedlings and recorded dynamic changes in E(GSH) and H(2)O(2) levels with the genetically encoded biosensors Grx1-roGFP2 (for E(GSH)) and roGFP2-Orp1 (for H(2)O(2)) targeted to chloroplasts, the cytosol, or mitochondria. Treatment of seedlings with MV caused rapid oxidation in chloroplasts and, subsequently, in the cytosol and mitochondria. MV-induced oxidation was significantly boosted by illumination with actinic light, and largely abolished by inhibitors of photosynthetic electron transport. MV also induced autonomous oxidation in the mitochondrial matrix in an electron transport chain activity-dependent manner that was milder than the oxidation triggered in chloroplasts by the combination of MV and light. In vivo redox biosensing resolves the spatiotemporal dynamics of compartmental responses to local ROS generation and provides a basis for understanding how compartment-specific redox dynamics might operate in retrograde signaling and stress acclimation in plants. |
format | Online Article Text |
id | pubmed-8154069 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | Oxford University Press |
record_format | MEDLINE/PubMed |
spelling | pubmed-81540692021-05-28 Chloroplast-derived photo-oxidative stress causes changes in H(2)O(2) and E(GSH) in other subcellular compartments Ugalde, José Manuel Fuchs, Philippe Nietzel, Thomas Cutolo, Edoardo A Homagk, Maria Vothknecht, Ute C Holuigue, Loreto Schwarzländer, Markus Müller-Schüssele, Stefanie J Meyer, Andreas J Plant Physiol Focus Issue on Plant Redox Biology Metabolic fluctuations in chloroplasts and mitochondria can trigger retrograde signals to modify nuclear gene expression. Mobile signals likely to be involved are reactive oxygen species (ROS), which can operate protein redox switches by oxidation of specific cysteine residues. Redox buffers, such as the highly reduced glutathione pool, serve as reservoirs of reducing power for several ROS-scavenging and ROS-induced damage repair pathways. Formation of glutathione disulfide and a shift of the glutathione redox potential (E(GSH)) toward less negative values is considered as hallmark of several stress conditions. Here we used the herbicide methyl viologen (MV) to generate ROS locally in chloroplasts of intact Arabidopsis (Arabidopsis thaliana) seedlings and recorded dynamic changes in E(GSH) and H(2)O(2) levels with the genetically encoded biosensors Grx1-roGFP2 (for E(GSH)) and roGFP2-Orp1 (for H(2)O(2)) targeted to chloroplasts, the cytosol, or mitochondria. Treatment of seedlings with MV caused rapid oxidation in chloroplasts and, subsequently, in the cytosol and mitochondria. MV-induced oxidation was significantly boosted by illumination with actinic light, and largely abolished by inhibitors of photosynthetic electron transport. MV also induced autonomous oxidation in the mitochondrial matrix in an electron transport chain activity-dependent manner that was milder than the oxidation triggered in chloroplasts by the combination of MV and light. In vivo redox biosensing resolves the spatiotemporal dynamics of compartmental responses to local ROS generation and provides a basis for understanding how compartment-specific redox dynamics might operate in retrograde signaling and stress acclimation in plants. Oxford University Press 2021-01-06 /pmc/articles/PMC8154069/ /pubmed/33793922 http://dx.doi.org/10.1093/plphys/kiaa095 Text en © The Author(s) 2021. Published by Oxford University Press on behalf of American Society of Plant Biologists. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) ), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. |
spellingShingle | Focus Issue on Plant Redox Biology Ugalde, José Manuel Fuchs, Philippe Nietzel, Thomas Cutolo, Edoardo A Homagk, Maria Vothknecht, Ute C Holuigue, Loreto Schwarzländer, Markus Müller-Schüssele, Stefanie J Meyer, Andreas J Chloroplast-derived photo-oxidative stress causes changes in H(2)O(2) and E(GSH) in other subcellular compartments |
title | Chloroplast-derived photo-oxidative stress causes changes in H(2)O(2) and E(GSH) in other subcellular compartments |
title_full | Chloroplast-derived photo-oxidative stress causes changes in H(2)O(2) and E(GSH) in other subcellular compartments |
title_fullStr | Chloroplast-derived photo-oxidative stress causes changes in H(2)O(2) and E(GSH) in other subcellular compartments |
title_full_unstemmed | Chloroplast-derived photo-oxidative stress causes changes in H(2)O(2) and E(GSH) in other subcellular compartments |
title_short | Chloroplast-derived photo-oxidative stress causes changes in H(2)O(2) and E(GSH) in other subcellular compartments |
title_sort | chloroplast-derived photo-oxidative stress causes changes in h(2)o(2) and e(gsh) in other subcellular compartments |
topic | Focus Issue on Plant Redox Biology |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8154069/ https://www.ncbi.nlm.nih.gov/pubmed/33793922 http://dx.doi.org/10.1093/plphys/kiaa095 |
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