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Quaternary ammonium iminofullerenes improve root growth of oxidative-stress maize through ASA-GSH cycle modulating redox homeostasis of roots and ROS-mediated root-hair elongation

BACKGROUND: Various environmental factors are capable of oxidative stress to result in limiting plant development and agricultural production. Fullerene-based carbon nanomaterials can enable radical scavenging and positively regulate plant growth. Even so, to date, our knowledge about the mechanism...

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Autores principales: Tai, Fuju, Wang, Shuai, Liang, Benshuai, Li, Yue, Wu, Jiakai, Fan, Chenjie, Hu, Xiuli, Wang, Hezhong, He, Rui, Wang, Wei
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8725307/
https://www.ncbi.nlm.nih.gov/pubmed/34983547
http://dx.doi.org/10.1186/s12951-021-01222-7
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author Tai, Fuju
Wang, Shuai
Liang, Benshuai
Li, Yue
Wu, Jiakai
Fan, Chenjie
Hu, Xiuli
Wang, Hezhong
He, Rui
Wang, Wei
author_facet Tai, Fuju
Wang, Shuai
Liang, Benshuai
Li, Yue
Wu, Jiakai
Fan, Chenjie
Hu, Xiuli
Wang, Hezhong
He, Rui
Wang, Wei
author_sort Tai, Fuju
collection PubMed
description BACKGROUND: Various environmental factors are capable of oxidative stress to result in limiting plant development and agricultural production. Fullerene-based carbon nanomaterials can enable radical scavenging and positively regulate plant growth. Even so, to date, our knowledge about the mechanism of fullerene-based carbon nanomaterials on plant growth and response to oxidative stress is still unclear. RESULTS: 20 or 50 mg/L quaternary ammonium iminofullerenes (IFQA) rescued the reduction in root lengths and root-hair densities and lengths of Arabidopsis and maize induced by accumulation of endogenous hydrogen peroxide (H(2)O(2)) under 3-amino-1,2,4-triazole or exogenous H(2)O(2) treatment, as well as the root active absorption area and root activity under exogenous H(2)O(2) treatment. Meanwhile, the downregulated contents of ascorbate acid (ASA) and glutathione (GSH) and the upregulated contents of dehydroascorbic acid (DHA), oxidized glutathione (GSSG), malondialdehyde (MDA), and H(2)O(2) indicated that the exogenous H(2)O(2) treatment induced oxidative stress of maize. Nonetheless, application of IFQA can increase the ratios of ASA/DHA and GSH/GSSG, as well as the activities of glutathione reductase, and ascorbate peroxidase, and decrease the contents of H(2)O(2) and MDA. Moreover, the root lengths were inhibited by buthionine sulfoximine, a specific inhibitor of GSH biosynthesis, and subsequently rescued after addition of IFQA. The results suggested that IFQA could alleviate exogenous-H(2)O(2)-induced oxidative stress on maize by regulating the ASA-GSH cycle. Furthermore, IFQA reduced the excess accumulation of ROS in root hairs, as well as the NADPH oxidase activity under H(2)O(2) treatment. The transcript levels of genes affecting ROS-mediated root-hair development, such as RBOH B, RBOH C, PFT1, and PRX59, were significantly induced by H(2)O(2) treatment and then decreased after addition of IFQA. CONCLUSION: The positive effect of fullerene-based carbon nanomaterials on maize-root-hair growth under the induced oxidative stress was discovered. Application IFQA can ameliorate oxidative stress to promote maize-root growth through decreasing NADPH-oxidase activity, improving the scavenging of ROS by ASA-GSH cycle, and regulating the expressions of genes affecting maize-root-hair development. It will enrich more understanding the actual mechanism of fullerene-based nanoelicitors responsible for plant growth promotion and protection from oxidative stress. GRAPHICAL ABSTRACT: [Image: see text]
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spelling pubmed-87253072022-01-06 Quaternary ammonium iminofullerenes improve root growth of oxidative-stress maize through ASA-GSH cycle modulating redox homeostasis of roots and ROS-mediated root-hair elongation Tai, Fuju Wang, Shuai Liang, Benshuai Li, Yue Wu, Jiakai Fan, Chenjie Hu, Xiuli Wang, Hezhong He, Rui Wang, Wei J Nanobiotechnology Research BACKGROUND: Various environmental factors are capable of oxidative stress to result in limiting plant development and agricultural production. Fullerene-based carbon nanomaterials can enable radical scavenging and positively regulate plant growth. Even so, to date, our knowledge about the mechanism of fullerene-based carbon nanomaterials on plant growth and response to oxidative stress is still unclear. RESULTS: 20 or 50 mg/L quaternary ammonium iminofullerenes (IFQA) rescued the reduction in root lengths and root-hair densities and lengths of Arabidopsis and maize induced by accumulation of endogenous hydrogen peroxide (H(2)O(2)) under 3-amino-1,2,4-triazole or exogenous H(2)O(2) treatment, as well as the root active absorption area and root activity under exogenous H(2)O(2) treatment. Meanwhile, the downregulated contents of ascorbate acid (ASA) and glutathione (GSH) and the upregulated contents of dehydroascorbic acid (DHA), oxidized glutathione (GSSG), malondialdehyde (MDA), and H(2)O(2) indicated that the exogenous H(2)O(2) treatment induced oxidative stress of maize. Nonetheless, application of IFQA can increase the ratios of ASA/DHA and GSH/GSSG, as well as the activities of glutathione reductase, and ascorbate peroxidase, and decrease the contents of H(2)O(2) and MDA. Moreover, the root lengths were inhibited by buthionine sulfoximine, a specific inhibitor of GSH biosynthesis, and subsequently rescued after addition of IFQA. The results suggested that IFQA could alleviate exogenous-H(2)O(2)-induced oxidative stress on maize by regulating the ASA-GSH cycle. Furthermore, IFQA reduced the excess accumulation of ROS in root hairs, as well as the NADPH oxidase activity under H(2)O(2) treatment. The transcript levels of genes affecting ROS-mediated root-hair development, such as RBOH B, RBOH C, PFT1, and PRX59, were significantly induced by H(2)O(2) treatment and then decreased after addition of IFQA. CONCLUSION: The positive effect of fullerene-based carbon nanomaterials on maize-root-hair growth under the induced oxidative stress was discovered. Application IFQA can ameliorate oxidative stress to promote maize-root growth through decreasing NADPH-oxidase activity, improving the scavenging of ROS by ASA-GSH cycle, and regulating the expressions of genes affecting maize-root-hair development. It will enrich more understanding the actual mechanism of fullerene-based nanoelicitors responsible for plant growth promotion and protection from oxidative stress. GRAPHICAL ABSTRACT: [Image: see text] BioMed Central 2022-01-04 /pmc/articles/PMC8725307/ /pubmed/34983547 http://dx.doi.org/10.1186/s12951-021-01222-7 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
Tai, Fuju
Wang, Shuai
Liang, Benshuai
Li, Yue
Wu, Jiakai
Fan, Chenjie
Hu, Xiuli
Wang, Hezhong
He, Rui
Wang, Wei
Quaternary ammonium iminofullerenes improve root growth of oxidative-stress maize through ASA-GSH cycle modulating redox homeostasis of roots and ROS-mediated root-hair elongation
title Quaternary ammonium iminofullerenes improve root growth of oxidative-stress maize through ASA-GSH cycle modulating redox homeostasis of roots and ROS-mediated root-hair elongation
title_full Quaternary ammonium iminofullerenes improve root growth of oxidative-stress maize through ASA-GSH cycle modulating redox homeostasis of roots and ROS-mediated root-hair elongation
title_fullStr Quaternary ammonium iminofullerenes improve root growth of oxidative-stress maize through ASA-GSH cycle modulating redox homeostasis of roots and ROS-mediated root-hair elongation
title_full_unstemmed Quaternary ammonium iminofullerenes improve root growth of oxidative-stress maize through ASA-GSH cycle modulating redox homeostasis of roots and ROS-mediated root-hair elongation
title_short Quaternary ammonium iminofullerenes improve root growth of oxidative-stress maize through ASA-GSH cycle modulating redox homeostasis of roots and ROS-mediated root-hair elongation
title_sort quaternary ammonium iminofullerenes improve root growth of oxidative-stress maize through asa-gsh cycle modulating redox homeostasis of roots and ros-mediated root-hair elongation
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8725307/
https://www.ncbi.nlm.nih.gov/pubmed/34983547
http://dx.doi.org/10.1186/s12951-021-01222-7
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