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Reductive stress triggers ANAC017-mediated retrograde signaling to safeguard the endoplasmic reticulum by boosting mitochondrial respiratory capacity

Redox processes are at the heart of universal life processes, such as metabolism, signaling, or folding of secreted proteins. Redox landscapes differ between cell compartments and are strictly controlled to tolerate changing conditions and to avoid cell dysfunction. While a sophisticated antioxidant...

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Autores principales: Fuchs, Philippe, Bohle, Finja, Lichtenauer, Sophie, Ugalde, José Manuel, Feitosa Araujo, Elias, Mansuroglu, Berivan, Ruberti, Cristina, Wagner, Stephan, Müller-Schüssele, Stefanie J, Meyer, Andreas J, Schwarzländer, Markus
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9125394/
https://www.ncbi.nlm.nih.gov/pubmed/35078237
http://dx.doi.org/10.1093/plcell/koac017
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author Fuchs, Philippe
Bohle, Finja
Lichtenauer, Sophie
Ugalde, José Manuel
Feitosa Araujo, Elias
Mansuroglu, Berivan
Ruberti, Cristina
Wagner, Stephan
Müller-Schüssele, Stefanie J
Meyer, Andreas J
Schwarzländer, Markus
author_facet Fuchs, Philippe
Bohle, Finja
Lichtenauer, Sophie
Ugalde, José Manuel
Feitosa Araujo, Elias
Mansuroglu, Berivan
Ruberti, Cristina
Wagner, Stephan
Müller-Schüssele, Stefanie J
Meyer, Andreas J
Schwarzländer, Markus
author_sort Fuchs, Philippe
collection PubMed
description Redox processes are at the heart of universal life processes, such as metabolism, signaling, or folding of secreted proteins. Redox landscapes differ between cell compartments and are strictly controlled to tolerate changing conditions and to avoid cell dysfunction. While a sophisticated antioxidant network counteracts oxidative stress, our understanding of reductive stress responses remains fragmentary. Here, we observed root growth impairment in Arabidopsis thaliana mutants of mitochondrial alternative oxidase 1a (aox1a) in response to the model thiol reductant dithiothreitol (DTT). Mutants of mitochondrial uncoupling protein 1 (ucp1) displayed a similar phenotype indicating that impaired respiratory flexibility led to hypersensitivity. Endoplasmic reticulum (ER) stress was enhanced in the mitochondrial mutants and limiting ER oxidoreductin capacity in the aox1a background led to synergistic root growth impairment by DTT, indicating that mitochondrial respiration alleviates reductive ER stress. The observations that DTT triggered nicotinamide adenine dinucleotide (NAD) reduction in vivo and that the presence of thiols led to electron transport chain activity in isolated mitochondria offer a biochemical framework of mitochondrion-mediated alleviation of thiol-mediated reductive stress. Ablation of transcription factor Arabidopsis NAC domain-containing protein17 (ANAC017) impaired the induction of AOX1a expression by DTT and led to DTT hypersensitivity, revealing that reductive stress tolerance is achieved by adjusting mitochondrial respiratory capacity via retrograde signaling. Our data reveal an unexpected role for mitochondrial respiratory flexibility and retrograde signaling in reductive stress tolerance involving inter-organelle redox crosstalk.
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spelling pubmed-91253942022-05-24 Reductive stress triggers ANAC017-mediated retrograde signaling to safeguard the endoplasmic reticulum by boosting mitochondrial respiratory capacity Fuchs, Philippe Bohle, Finja Lichtenauer, Sophie Ugalde, José Manuel Feitosa Araujo, Elias Mansuroglu, Berivan Ruberti, Cristina Wagner, Stephan Müller-Schüssele, Stefanie J Meyer, Andreas J Schwarzländer, Markus Plant Cell Research Articles Redox processes are at the heart of universal life processes, such as metabolism, signaling, or folding of secreted proteins. Redox landscapes differ between cell compartments and are strictly controlled to tolerate changing conditions and to avoid cell dysfunction. While a sophisticated antioxidant network counteracts oxidative stress, our understanding of reductive stress responses remains fragmentary. Here, we observed root growth impairment in Arabidopsis thaliana mutants of mitochondrial alternative oxidase 1a (aox1a) in response to the model thiol reductant dithiothreitol (DTT). Mutants of mitochondrial uncoupling protein 1 (ucp1) displayed a similar phenotype indicating that impaired respiratory flexibility led to hypersensitivity. Endoplasmic reticulum (ER) stress was enhanced in the mitochondrial mutants and limiting ER oxidoreductin capacity in the aox1a background led to synergistic root growth impairment by DTT, indicating that mitochondrial respiration alleviates reductive ER stress. The observations that DTT triggered nicotinamide adenine dinucleotide (NAD) reduction in vivo and that the presence of thiols led to electron transport chain activity in isolated mitochondria offer a biochemical framework of mitochondrion-mediated alleviation of thiol-mediated reductive stress. Ablation of transcription factor Arabidopsis NAC domain-containing protein17 (ANAC017) impaired the induction of AOX1a expression by DTT and led to DTT hypersensitivity, revealing that reductive stress tolerance is achieved by adjusting mitochondrial respiratory capacity via retrograde signaling. Our data reveal an unexpected role for mitochondrial respiratory flexibility and retrograde signaling in reductive stress tolerance involving inter-organelle redox crosstalk. Oxford University Press 2022-01-25 /pmc/articles/PMC9125394/ /pubmed/35078237 http://dx.doi.org/10.1093/plcell/koac017 Text en © The Author(s) 2022. 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 (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 Research Articles
Fuchs, Philippe
Bohle, Finja
Lichtenauer, Sophie
Ugalde, José Manuel
Feitosa Araujo, Elias
Mansuroglu, Berivan
Ruberti, Cristina
Wagner, Stephan
Müller-Schüssele, Stefanie J
Meyer, Andreas J
Schwarzländer, Markus
Reductive stress triggers ANAC017-mediated retrograde signaling to safeguard the endoplasmic reticulum by boosting mitochondrial respiratory capacity
title Reductive stress triggers ANAC017-mediated retrograde signaling to safeguard the endoplasmic reticulum by boosting mitochondrial respiratory capacity
title_full Reductive stress triggers ANAC017-mediated retrograde signaling to safeguard the endoplasmic reticulum by boosting mitochondrial respiratory capacity
title_fullStr Reductive stress triggers ANAC017-mediated retrograde signaling to safeguard the endoplasmic reticulum by boosting mitochondrial respiratory capacity
title_full_unstemmed Reductive stress triggers ANAC017-mediated retrograde signaling to safeguard the endoplasmic reticulum by boosting mitochondrial respiratory capacity
title_short Reductive stress triggers ANAC017-mediated retrograde signaling to safeguard the endoplasmic reticulum by boosting mitochondrial respiratory capacity
title_sort reductive stress triggers anac017-mediated retrograde signaling to safeguard the endoplasmic reticulum by boosting mitochondrial respiratory capacity
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9125394/
https://www.ncbi.nlm.nih.gov/pubmed/35078237
http://dx.doi.org/10.1093/plcell/koac017
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