RNA N<sup>6</sup>-Methyladenosine Affects Copper-Induced Oxidative Stress Response in <i>Arabidopsis thaliana</i>

Recently, post-transcriptional regulation of mRNA mediated by N<sup>6</sup>-methyladenosine (m<sup>6</sup>A) has been found to have profound effects on transcriptome regulation during plant responses to various abiotic stresses. However, whether this RNA modification can affe...

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Main Authors: Bishwas Sharma, Ganesan Govindan, Yongfang Li, Ramanjulu Sunkar, Brian D. Gregory
Format: Article
Language:English
Published: MDPI AG 2024-01-01
Series:Non-Coding RNA
Subjects:
Online Access:https://www.mdpi.com/2311-553X/10/1/8
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author Bishwas Sharma
Ganesan Govindan
Yongfang Li
Ramanjulu Sunkar
Brian D. Gregory
author_facet Bishwas Sharma
Ganesan Govindan
Yongfang Li
Ramanjulu Sunkar
Brian D. Gregory
author_sort Bishwas Sharma
collection DOAJ
description Recently, post-transcriptional regulation of mRNA mediated by N<sup>6</sup>-methyladenosine (m<sup>6</sup>A) has been found to have profound effects on transcriptome regulation during plant responses to various abiotic stresses. However, whether this RNA modification can affect an oxidative stress response in plants has not been studied. To assess the role of m<sup>6</sup>A modifications during copper-induced oxidative stress responses, m<sup>6</sup>A-IP-seq was performed in Arabidopsis seedlings exposed to high levels of copper sulfate. This analysis revealed large-scale shifts in this modification on the transcripts most relevant for oxidative stress. This altered epitranscriptomic mark is known to influence transcript abundance and translation; therefore we scrutinized these possibilities. We found an increased abundance of copper-enriched m<sup>6</sup>A-containing transcripts. Similarly, we also found increased ribosome occupancy of copper-enriched m<sup>6</sup>A-containing transcripts, specifically those encoding proteins involved with stress responses relevant to oxidative stressors. Furthermore, the significance of the m<sup>6</sup>A epitranscriptome on plant oxidative stress tolerance was uncovered by assessing germination and seedling development of the <i>mta</i> (N<sup>6</sup>-methyladenosine RNA methyltransferase A mutant complemented with <i>ABI3</i>:<i>MTA</i>) mutant exposed to high copper treatment. These analyses suggested hypersensitivity of the <i>mta</i> mutant compared to the wild-type plants in response to copper-induced oxidative stress. Overall, our findings suggest an important role for m<sup>6</sup>A in the oxidative stress response of Arabidopsis.
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spelling doaj.art-0f21ba3beb134674bff4f9bee69195ea2024-02-23T15:29:35ZengMDPI AGNon-Coding RNA2311-553X2024-01-01101810.3390/ncrna10010008RNA N<sup>6</sup>-Methyladenosine Affects Copper-Induced Oxidative Stress Response in <i>Arabidopsis thaliana</i>Bishwas Sharma0Ganesan Govindan1Yongfang Li2Ramanjulu Sunkar3Brian D. Gregory4Department of Biology, University of Pennsylvania, Philadelphia, PA 19104, USADepartment of Biochemistry and Molecular Biology, Oklahoma State University, Stillwater, OK 74078, USADepartment of Biochemistry and Molecular Biology, Oklahoma State University, Stillwater, OK 74078, USADepartment of Biochemistry and Molecular Biology, Oklahoma State University, Stillwater, OK 74078, USADepartment of Biology, University of Pennsylvania, Philadelphia, PA 19104, USARecently, post-transcriptional regulation of mRNA mediated by N<sup>6</sup>-methyladenosine (m<sup>6</sup>A) has been found to have profound effects on transcriptome regulation during plant responses to various abiotic stresses. However, whether this RNA modification can affect an oxidative stress response in plants has not been studied. To assess the role of m<sup>6</sup>A modifications during copper-induced oxidative stress responses, m<sup>6</sup>A-IP-seq was performed in Arabidopsis seedlings exposed to high levels of copper sulfate. This analysis revealed large-scale shifts in this modification on the transcripts most relevant for oxidative stress. This altered epitranscriptomic mark is known to influence transcript abundance and translation; therefore we scrutinized these possibilities. We found an increased abundance of copper-enriched m<sup>6</sup>A-containing transcripts. Similarly, we also found increased ribosome occupancy of copper-enriched m<sup>6</sup>A-containing transcripts, specifically those encoding proteins involved with stress responses relevant to oxidative stressors. Furthermore, the significance of the m<sup>6</sup>A epitranscriptome on plant oxidative stress tolerance was uncovered by assessing germination and seedling development of the <i>mta</i> (N<sup>6</sup>-methyladenosine RNA methyltransferase A mutant complemented with <i>ABI3</i>:<i>MTA</i>) mutant exposed to high copper treatment. These analyses suggested hypersensitivity of the <i>mta</i> mutant compared to the wild-type plants in response to copper-induced oxidative stress. Overall, our findings suggest an important role for m<sup>6</sup>A in the oxidative stress response of Arabidopsis.https://www.mdpi.com/2311-553X/10/1/8epitranscriptomelong non-coding RNAsplant stress responseRNA methylationribosome occupancytranscript stability
spellingShingle Bishwas Sharma
Ganesan Govindan
Yongfang Li
Ramanjulu Sunkar
Brian D. Gregory
RNA N<sup>6</sup>-Methyladenosine Affects Copper-Induced Oxidative Stress Response in <i>Arabidopsis thaliana</i>
Non-Coding RNA
epitranscriptome
long non-coding RNAs
plant stress response
RNA methylation
ribosome occupancy
transcript stability
title RNA N<sup>6</sup>-Methyladenosine Affects Copper-Induced Oxidative Stress Response in <i>Arabidopsis thaliana</i>
title_full RNA N<sup>6</sup>-Methyladenosine Affects Copper-Induced Oxidative Stress Response in <i>Arabidopsis thaliana</i>
title_fullStr RNA N<sup>6</sup>-Methyladenosine Affects Copper-Induced Oxidative Stress Response in <i>Arabidopsis thaliana</i>
title_full_unstemmed RNA N<sup>6</sup>-Methyladenosine Affects Copper-Induced Oxidative Stress Response in <i>Arabidopsis thaliana</i>
title_short RNA N<sup>6</sup>-Methyladenosine Affects Copper-Induced Oxidative Stress Response in <i>Arabidopsis thaliana</i>
title_sort rna n sup 6 sup methyladenosine affects copper induced oxidative stress response in i arabidopsis thaliana i
topic epitranscriptome
long non-coding RNAs
plant stress response
RNA methylation
ribosome occupancy
transcript stability
url https://www.mdpi.com/2311-553X/10/1/8
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