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Reactive Oxygen Species Partly Mediate DNA Methylation in Responses to Different Heavy Metals in Pokeweed

DNA methylation is a rapid response strategy promoting plant survival under heavy metal (HM) stress. However, the roles of DNA methylation underlying plant adaptation to HM stress remain largely unknown. Here, we used pokeweed, a hyperaccumulator of manganese (Mn) and cadmium (Cd), to explore respon...

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Autores principales: Jing, Minyu, Zhang, Hanchao, Wei, Mingyue, Tang, Yongwei, Xia, Yan, Chen, Yahua, Shen, Zhenguo, Chen, Chen
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9021841/
https://www.ncbi.nlm.nih.gov/pubmed/35463456
http://dx.doi.org/10.3389/fpls.2022.845108
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author Jing, Minyu
Zhang, Hanchao
Wei, Mingyue
Tang, Yongwei
Xia, Yan
Chen, Yahua
Shen, Zhenguo
Chen, Chen
author_facet Jing, Minyu
Zhang, Hanchao
Wei, Mingyue
Tang, Yongwei
Xia, Yan
Chen, Yahua
Shen, Zhenguo
Chen, Chen
author_sort Jing, Minyu
collection PubMed
description DNA methylation is a rapid response strategy promoting plant survival under heavy metal (HM) stress. However, the roles of DNA methylation underlying plant adaptation to HM stress remain largely unknown. Here, we used pokeweed, a hyperaccumulator of manganese (Mn) and cadmium (Cd), to explore responses of plant to HM stress at phenotypic, transcriptional and DNA methylation levels. Mn- and Cd-specific response patterns were detected in pokeweed. The growth of pokeweed was both inhibited with exposure to excess Mn/Cd, but pokeweed distinguished Mn and Cd with different subcellular distributions, ROS scavenging systems, transcriptional patterns including genes involved in DNA methylation, and differentially methylated loci (DML). The number of DML between Mn/Cd treated and untreated samples increased with increased Mn/Cd concentrations. Meanwhile, pretreatment with NADPH oxidase inhibitors prior to HM exposure markedly reduced HM-induced reactive oxygen species (ROS), which caused reductions in expressions of DNA methylase and demethylase in pretreated samples. The increased levels of HM-induced demethylation were suppressed with alleviated ROS stress, and a series of HM-related methylated loci were also ROS-related. Taken together, our study demonstrates that different HMs affect different DNA methylation sites in a dose-dependent manner and changes in DNA methylation under Mn/Cd stress are partly mediated by HM-induced ROS.
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spelling pubmed-90218412022-04-22 Reactive Oxygen Species Partly Mediate DNA Methylation in Responses to Different Heavy Metals in Pokeweed Jing, Minyu Zhang, Hanchao Wei, Mingyue Tang, Yongwei Xia, Yan Chen, Yahua Shen, Zhenguo Chen, Chen Front Plant Sci Plant Science DNA methylation is a rapid response strategy promoting plant survival under heavy metal (HM) stress. However, the roles of DNA methylation underlying plant adaptation to HM stress remain largely unknown. Here, we used pokeweed, a hyperaccumulator of manganese (Mn) and cadmium (Cd), to explore responses of plant to HM stress at phenotypic, transcriptional and DNA methylation levels. Mn- and Cd-specific response patterns were detected in pokeweed. The growth of pokeweed was both inhibited with exposure to excess Mn/Cd, but pokeweed distinguished Mn and Cd with different subcellular distributions, ROS scavenging systems, transcriptional patterns including genes involved in DNA methylation, and differentially methylated loci (DML). The number of DML between Mn/Cd treated and untreated samples increased with increased Mn/Cd concentrations. Meanwhile, pretreatment with NADPH oxidase inhibitors prior to HM exposure markedly reduced HM-induced reactive oxygen species (ROS), which caused reductions in expressions of DNA methylase and demethylase in pretreated samples. The increased levels of HM-induced demethylation were suppressed with alleviated ROS stress, and a series of HM-related methylated loci were also ROS-related. Taken together, our study demonstrates that different HMs affect different DNA methylation sites in a dose-dependent manner and changes in DNA methylation under Mn/Cd stress are partly mediated by HM-induced ROS. Frontiers Media S.A. 2022-04-07 /pmc/articles/PMC9021841/ /pubmed/35463456 http://dx.doi.org/10.3389/fpls.2022.845108 Text en Copyright © 2022 Jing, Zhang, Wei, Tang, Xia, Chen, Shen and Chen. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Jing, Minyu
Zhang, Hanchao
Wei, Mingyue
Tang, Yongwei
Xia, Yan
Chen, Yahua
Shen, Zhenguo
Chen, Chen
Reactive Oxygen Species Partly Mediate DNA Methylation in Responses to Different Heavy Metals in Pokeweed
title Reactive Oxygen Species Partly Mediate DNA Methylation in Responses to Different Heavy Metals in Pokeweed
title_full Reactive Oxygen Species Partly Mediate DNA Methylation in Responses to Different Heavy Metals in Pokeweed
title_fullStr Reactive Oxygen Species Partly Mediate DNA Methylation in Responses to Different Heavy Metals in Pokeweed
title_full_unstemmed Reactive Oxygen Species Partly Mediate DNA Methylation in Responses to Different Heavy Metals in Pokeweed
title_short Reactive Oxygen Species Partly Mediate DNA Methylation in Responses to Different Heavy Metals in Pokeweed
title_sort reactive oxygen species partly mediate dna methylation in responses to different heavy metals in pokeweed
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9021841/
https://www.ncbi.nlm.nih.gov/pubmed/35463456
http://dx.doi.org/10.3389/fpls.2022.845108
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