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The relationship between ethylene-induced autophagy and reactive oxygen species in Arabidopsis root cells during the early stages of waterlogging stress

The response of plants to waterlogging stress is a complex process, with ethylene playing a crucial role as a signaling molecule. However, it remains unclear how ethylene is initially triggered in response to waterlogging stress when plants are continuously waterlogged for less than 12 hours. Here,...

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Autores principales: Zheng, Qiwei, Li, Gege, Wang, Hongyan, Zhou, Zhuqing
Formato: Online Artículo Texto
Lenguaje:English
Publicado: PeerJ Inc. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10226478/
https://www.ncbi.nlm.nih.gov/pubmed/37255589
http://dx.doi.org/10.7717/peerj.15404
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author Zheng, Qiwei
Li, Gege
Wang, Hongyan
Zhou, Zhuqing
author_facet Zheng, Qiwei
Li, Gege
Wang, Hongyan
Zhou, Zhuqing
author_sort Zheng, Qiwei
collection PubMed
description The response of plants to waterlogging stress is a complex process, with ethylene playing a crucial role as a signaling molecule. However, it remains unclear how ethylene is initially triggered in response to waterlogging stress when plants are continuously waterlogged for less than 12 hours. Here, we have shown that ethylene-induced autophagy leads to the degradation of damaged mitochondria (the main organelles producing reactive oxygen species (ROS)) to reduce ROS production during oxidative stress in Arabidopsis thaliana, which improves the survival rate of root cells in the early stages of waterlogging stress. Waterlogging stress activated ethylene-related genes, including ACO2, ACS2, ERF72, ERF73, and EIN3, and ethylene content of plants increased significantly within 24 h of continuous waterlogging. As stress duration increased, increased amounts of ROS accumulated in Arabidopsis thaliana roots, and the activity of antioxidant enzymes initially increased and then decreased. Concurrently, the level of ethylene-induced autophagy, which participates in antioxidant defense, is higher in wild-type plants than in the octuple acs mutant cs16651 (acs2-1/acs4-1/acs5-2/acs6-1/acs7-1/acs9-1/amiRacs8acs11). Exogenous application of 1-aminocyclopropanecarboxylic acid (ACC), resulted in a more pronounced manifestation of autophagy in the stele of Arabidopsis roots. Compared with the waterlogging treatment group or the ACC treatment group, the waterlogging + ACC treatment can induce autophagy to occur earlier and expand the autophagic range to the epidermis of Arabidopsis thaliana roots. Overall, our results provide insight into the important role of ethylene-induced autophagy in enhancing the antioxidative capacity of Arabidopsis thaliana during the early stages of waterlogging stress. Furthermore, we suggest ethylene as a potential candidate for mitigating the deleterious effects caused by waterlogging in Arabidopsis thaliana.
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spelling pubmed-102264782023-05-30 The relationship between ethylene-induced autophagy and reactive oxygen species in Arabidopsis root cells during the early stages of waterlogging stress Zheng, Qiwei Li, Gege Wang, Hongyan Zhou, Zhuqing PeerJ Biochemistry The response of plants to waterlogging stress is a complex process, with ethylene playing a crucial role as a signaling molecule. However, it remains unclear how ethylene is initially triggered in response to waterlogging stress when plants are continuously waterlogged for less than 12 hours. Here, we have shown that ethylene-induced autophagy leads to the degradation of damaged mitochondria (the main organelles producing reactive oxygen species (ROS)) to reduce ROS production during oxidative stress in Arabidopsis thaliana, which improves the survival rate of root cells in the early stages of waterlogging stress. Waterlogging stress activated ethylene-related genes, including ACO2, ACS2, ERF72, ERF73, and EIN3, and ethylene content of plants increased significantly within 24 h of continuous waterlogging. As stress duration increased, increased amounts of ROS accumulated in Arabidopsis thaliana roots, and the activity of antioxidant enzymes initially increased and then decreased. Concurrently, the level of ethylene-induced autophagy, which participates in antioxidant defense, is higher in wild-type plants than in the octuple acs mutant cs16651 (acs2-1/acs4-1/acs5-2/acs6-1/acs7-1/acs9-1/amiRacs8acs11). Exogenous application of 1-aminocyclopropanecarboxylic acid (ACC), resulted in a more pronounced manifestation of autophagy in the stele of Arabidopsis roots. Compared with the waterlogging treatment group or the ACC treatment group, the waterlogging + ACC treatment can induce autophagy to occur earlier and expand the autophagic range to the epidermis of Arabidopsis thaliana roots. Overall, our results provide insight into the important role of ethylene-induced autophagy in enhancing the antioxidative capacity of Arabidopsis thaliana during the early stages of waterlogging stress. Furthermore, we suggest ethylene as a potential candidate for mitigating the deleterious effects caused by waterlogging in Arabidopsis thaliana. PeerJ Inc. 2023-05-26 /pmc/articles/PMC10226478/ /pubmed/37255589 http://dx.doi.org/10.7717/peerj.15404 Text en ©2023 Zheng et al. 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 use, distribution, reproduction and adaptation in any medium and for any purpose provided that it is properly attributed. For attribution, the original author(s), title, publication source (PeerJ) and either DOI or URL of the article must be cited.
spellingShingle Biochemistry
Zheng, Qiwei
Li, Gege
Wang, Hongyan
Zhou, Zhuqing
The relationship between ethylene-induced autophagy and reactive oxygen species in Arabidopsis root cells during the early stages of waterlogging stress
title The relationship between ethylene-induced autophagy and reactive oxygen species in Arabidopsis root cells during the early stages of waterlogging stress
title_full The relationship between ethylene-induced autophagy and reactive oxygen species in Arabidopsis root cells during the early stages of waterlogging stress
title_fullStr The relationship between ethylene-induced autophagy and reactive oxygen species in Arabidopsis root cells during the early stages of waterlogging stress
title_full_unstemmed The relationship between ethylene-induced autophagy and reactive oxygen species in Arabidopsis root cells during the early stages of waterlogging stress
title_short The relationship between ethylene-induced autophagy and reactive oxygen species in Arabidopsis root cells during the early stages of waterlogging stress
title_sort relationship between ethylene-induced autophagy and reactive oxygen species in arabidopsis root cells during the early stages of waterlogging stress
topic Biochemistry
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10226478/
https://www.ncbi.nlm.nih.gov/pubmed/37255589
http://dx.doi.org/10.7717/peerj.15404
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