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The core autophagy machinery is not required for chloroplast singlet oxygen-mediated cell death in the Arabidopsis thaliana plastid ferrochelatase two mutant

BACKGROUND: Chloroplasts respond to stress and changes in the environment by producing reactive oxygen species (ROS) that have specific signaling abilities. The ROS singlet oxygen ((1)O(2)) is unique in that it can signal to initiate cellular degradation including the selective degradation of damage...

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Autores principales: Lemke, Matthew D., Fisher, Karen E., Kozlowska, Marta A., Tano, David W., Woodson, Jesse D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8290626/
https://www.ncbi.nlm.nih.gov/pubmed/34281507
http://dx.doi.org/10.1186/s12870-021-03119-x
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author Lemke, Matthew D.
Fisher, Karen E.
Kozlowska, Marta A.
Tano, David W.
Woodson, Jesse D.
author_facet Lemke, Matthew D.
Fisher, Karen E.
Kozlowska, Marta A.
Tano, David W.
Woodson, Jesse D.
author_sort Lemke, Matthew D.
collection PubMed
description BACKGROUND: Chloroplasts respond to stress and changes in the environment by producing reactive oxygen species (ROS) that have specific signaling abilities. The ROS singlet oxygen ((1)O(2)) is unique in that it can signal to initiate cellular degradation including the selective degradation of damaged chloroplasts. This chloroplast quality control pathway can be monitored in the Arabidopsis thaliana mutant plastid ferrochelatase two (fc2) that conditionally accumulates chloroplast (1)O(2) under diurnal light cycling conditions leading to rapid chloroplast degradation and eventual cell death. The cellular machinery involved in such degradation, however, remains unknown. Recently, it was demonstrated that whole damaged chloroplasts can be transported to the central vacuole via a process requiring autophagosomes and core components of the autophagy machinery. The relationship between this process, referred to as chlorophagy, and the degradation of (1)O(2)-stressed chloroplasts and cells has remained unexplored. RESULTS: To further understand (1)O(2)-induced cellular degradation and determine what role autophagy may play, the expression of autophagy-related genes was monitored in (1)O(2)-stressed fc2 seedlings and found to be induced. Although autophagosomes were present in fc2 cells, they did not associate with chloroplasts during (1)O(2) stress. Mutations affecting the core autophagy machinery (atg5, atg7, and atg10) were unable to suppress (1)O(2)-induced cell death or chloroplast protrusion into the central vacuole, suggesting autophagosome formation is dispensable for such (1)O(2)–mediated cellular degradation. However, both atg5 and atg7 led to specific defects in chloroplast ultrastructure and photosynthetic efficiencies, suggesting core autophagy machinery is involved in protecting chloroplasts from photo-oxidative damage. Finally, genes predicted to be involved in microautophagy were shown to be induced in stressed fc2 seedlings, indicating a possible role for an alternate form of autophagy in the dismantling of (1)O(2)-damaged chloroplasts. CONCLUSIONS: Our results support the hypothesis that (1)O(2)-dependent cell death is independent from autophagosome formation, canonical autophagy, and chlorophagy. Furthermore, autophagosome-independent microautophagy may be involved in degrading (1)O(2)-damaged chloroplasts. At the same time, canonical autophagy may still play a role in protecting chloroplasts from (1)O(2)-induced photo-oxidative stress. Together, this suggests chloroplast function and degradation is a complex process utilizing multiple autophagy and degradation machineries, possibly depending on the type of stress or damage incurred. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-021-03119-x.
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spelling pubmed-82906262021-07-21 The core autophagy machinery is not required for chloroplast singlet oxygen-mediated cell death in the Arabidopsis thaliana plastid ferrochelatase two mutant Lemke, Matthew D. Fisher, Karen E. Kozlowska, Marta A. Tano, David W. Woodson, Jesse D. BMC Plant Biol Research BACKGROUND: Chloroplasts respond to stress and changes in the environment by producing reactive oxygen species (ROS) that have specific signaling abilities. The ROS singlet oxygen ((1)O(2)) is unique in that it can signal to initiate cellular degradation including the selective degradation of damaged chloroplasts. This chloroplast quality control pathway can be monitored in the Arabidopsis thaliana mutant plastid ferrochelatase two (fc2) that conditionally accumulates chloroplast (1)O(2) under diurnal light cycling conditions leading to rapid chloroplast degradation and eventual cell death. The cellular machinery involved in such degradation, however, remains unknown. Recently, it was demonstrated that whole damaged chloroplasts can be transported to the central vacuole via a process requiring autophagosomes and core components of the autophagy machinery. The relationship between this process, referred to as chlorophagy, and the degradation of (1)O(2)-stressed chloroplasts and cells has remained unexplored. RESULTS: To further understand (1)O(2)-induced cellular degradation and determine what role autophagy may play, the expression of autophagy-related genes was monitored in (1)O(2)-stressed fc2 seedlings and found to be induced. Although autophagosomes were present in fc2 cells, they did not associate with chloroplasts during (1)O(2) stress. Mutations affecting the core autophagy machinery (atg5, atg7, and atg10) were unable to suppress (1)O(2)-induced cell death or chloroplast protrusion into the central vacuole, suggesting autophagosome formation is dispensable for such (1)O(2)–mediated cellular degradation. However, both atg5 and atg7 led to specific defects in chloroplast ultrastructure and photosynthetic efficiencies, suggesting core autophagy machinery is involved in protecting chloroplasts from photo-oxidative damage. Finally, genes predicted to be involved in microautophagy were shown to be induced in stressed fc2 seedlings, indicating a possible role for an alternate form of autophagy in the dismantling of (1)O(2)-damaged chloroplasts. CONCLUSIONS: Our results support the hypothesis that (1)O(2)-dependent cell death is independent from autophagosome formation, canonical autophagy, and chlorophagy. Furthermore, autophagosome-independent microautophagy may be involved in degrading (1)O(2)-damaged chloroplasts. At the same time, canonical autophagy may still play a role in protecting chloroplasts from (1)O(2)-induced photo-oxidative stress. Together, this suggests chloroplast function and degradation is a complex process utilizing multiple autophagy and degradation machineries, possibly depending on the type of stress or damage incurred. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-021-03119-x. BioMed Central 2021-07-19 /pmc/articles/PMC8290626/ /pubmed/34281507 http://dx.doi.org/10.1186/s12870-021-03119-x Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Lemke, Matthew D.
Fisher, Karen E.
Kozlowska, Marta A.
Tano, David W.
Woodson, Jesse D.
The core autophagy machinery is not required for chloroplast singlet oxygen-mediated cell death in the Arabidopsis thaliana plastid ferrochelatase two mutant
title The core autophagy machinery is not required for chloroplast singlet oxygen-mediated cell death in the Arabidopsis thaliana plastid ferrochelatase two mutant
title_full The core autophagy machinery is not required for chloroplast singlet oxygen-mediated cell death in the Arabidopsis thaliana plastid ferrochelatase two mutant
title_fullStr The core autophagy machinery is not required for chloroplast singlet oxygen-mediated cell death in the Arabidopsis thaliana plastid ferrochelatase two mutant
title_full_unstemmed The core autophagy machinery is not required for chloroplast singlet oxygen-mediated cell death in the Arabidopsis thaliana plastid ferrochelatase two mutant
title_short The core autophagy machinery is not required for chloroplast singlet oxygen-mediated cell death in the Arabidopsis thaliana plastid ferrochelatase two mutant
title_sort core autophagy machinery is not required for chloroplast singlet oxygen-mediated cell death in the arabidopsis thaliana plastid ferrochelatase two mutant
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8290626/
https://www.ncbi.nlm.nih.gov/pubmed/34281507
http://dx.doi.org/10.1186/s12870-021-03119-x
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