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ROS Homeostasis Involved in Dose-Dependent Responses of Arabidopsis Seedlings to Copper Toxicity
As an essential element in plant nutrition, copper (Cu) can promote or inhibit plant growth depending on its concentration. However, the dose-dependent effects of copper, particularly on DNA damage associated with reactive oxygen species (ROS) homeostasis, are much less understood. In this work, we...
Autores principales: | , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
MDPI
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9858908/ https://www.ncbi.nlm.nih.gov/pubmed/36672752 http://dx.doi.org/10.3390/genes14010011 |
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author | Wang, Jiehua Moeen-ud-din, Muhammad Yin, Rong Yang, Shaohui |
author_facet | Wang, Jiehua Moeen-ud-din, Muhammad Yin, Rong Yang, Shaohui |
author_sort | Wang, Jiehua |
collection | PubMed |
description | As an essential element in plant nutrition, copper (Cu) can promote or inhibit plant growth depending on its concentration. However, the dose-dependent effects of copper, particularly on DNA damage associated with reactive oxygen species (ROS) homeostasis, are much less understood. In this work, we analyzed the dual effect of Cu (5, 20, and 60 μM) on the reproductive performance of Arabidopsis plants. Whereas Cu5 promoted inflorescence initiation and increased kilo seed weight, two higher concentrations, Cu20 and Cu60, delayed inflorescence initiation and negatively affected silique size. Excess Cu also induced changes in cellular redox homeostasis, which was examined by in situ visualization and measurements of ROS, including superoxide (O(2)(•−)), hydrogen peroxide (H(2)O(2)), malonyldialdehyde (MDA), and plasma membrane damage. The most dramatic increases in the production of O(2)(•−) and H(2)O(2) along with increased activity of superoxide dismutase (SOD) and glutathione peroxidase (GPX) and decreased activity of catalase (CAT) and ascorbate peroxidase (APX) were observed in roots with Cu60. Oxidative stress also modulated the expression levels of a number of genes involved in the DNA damage response (DDR), particularly those related to DNA repair. The Cu-induced chlorosis of Arabidopsis seedlings could be alleviated by exogenous addition of glutathione (GSH) and ascorbate (Asc), as the chlorophyll content was significantly increased. Overall, internal homeostasis ROS and the associated DDR pathway and the corresponding scavenging mechanisms play a central role in the response of Arabidopsis to oxidative stress induced by inhibitory Cu concentrations. Our results have shown, for the first time, that the biphasic responses of Arabidopsis seedlings to increasing Cu concentrations involve different DNA damage responses and oxidative reactions. They provide the basis for elucidating the network of Cu-induced DDR-related genes and the regulatory mechanism of the complex ROS production and scavenging system. |
format | Online Article Text |
id | pubmed-9858908 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | MDPI |
record_format | MEDLINE/PubMed |
spelling | pubmed-98589082023-01-21 ROS Homeostasis Involved in Dose-Dependent Responses of Arabidopsis Seedlings to Copper Toxicity Wang, Jiehua Moeen-ud-din, Muhammad Yin, Rong Yang, Shaohui Genes (Basel) Article As an essential element in plant nutrition, copper (Cu) can promote or inhibit plant growth depending on its concentration. However, the dose-dependent effects of copper, particularly on DNA damage associated with reactive oxygen species (ROS) homeostasis, are much less understood. In this work, we analyzed the dual effect of Cu (5, 20, and 60 μM) on the reproductive performance of Arabidopsis plants. Whereas Cu5 promoted inflorescence initiation and increased kilo seed weight, two higher concentrations, Cu20 and Cu60, delayed inflorescence initiation and negatively affected silique size. Excess Cu also induced changes in cellular redox homeostasis, which was examined by in situ visualization and measurements of ROS, including superoxide (O(2)(•−)), hydrogen peroxide (H(2)O(2)), malonyldialdehyde (MDA), and plasma membrane damage. The most dramatic increases in the production of O(2)(•−) and H(2)O(2) along with increased activity of superoxide dismutase (SOD) and glutathione peroxidase (GPX) and decreased activity of catalase (CAT) and ascorbate peroxidase (APX) were observed in roots with Cu60. Oxidative stress also modulated the expression levels of a number of genes involved in the DNA damage response (DDR), particularly those related to DNA repair. The Cu-induced chlorosis of Arabidopsis seedlings could be alleviated by exogenous addition of glutathione (GSH) and ascorbate (Asc), as the chlorophyll content was significantly increased. Overall, internal homeostasis ROS and the associated DDR pathway and the corresponding scavenging mechanisms play a central role in the response of Arabidopsis to oxidative stress induced by inhibitory Cu concentrations. Our results have shown, for the first time, that the biphasic responses of Arabidopsis seedlings to increasing Cu concentrations involve different DNA damage responses and oxidative reactions. They provide the basis for elucidating the network of Cu-induced DDR-related genes and the regulatory mechanism of the complex ROS production and scavenging system. MDPI 2022-12-21 /pmc/articles/PMC9858908/ /pubmed/36672752 http://dx.doi.org/10.3390/genes14010011 Text en © 2022 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/). |
spellingShingle | Article Wang, Jiehua Moeen-ud-din, Muhammad Yin, Rong Yang, Shaohui ROS Homeostasis Involved in Dose-Dependent Responses of Arabidopsis Seedlings to Copper Toxicity |
title | ROS Homeostasis Involved in Dose-Dependent Responses of Arabidopsis Seedlings to Copper Toxicity |
title_full | ROS Homeostasis Involved in Dose-Dependent Responses of Arabidopsis Seedlings to Copper Toxicity |
title_fullStr | ROS Homeostasis Involved in Dose-Dependent Responses of Arabidopsis Seedlings to Copper Toxicity |
title_full_unstemmed | ROS Homeostasis Involved in Dose-Dependent Responses of Arabidopsis Seedlings to Copper Toxicity |
title_short | ROS Homeostasis Involved in Dose-Dependent Responses of Arabidopsis Seedlings to Copper Toxicity |
title_sort | ros homeostasis involved in dose-dependent responses of arabidopsis seedlings to copper toxicity |
topic | Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9858908/ https://www.ncbi.nlm.nih.gov/pubmed/36672752 http://dx.doi.org/10.3390/genes14010011 |
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