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E2Fs co-participate in cadmium stress response through activation of MSHs during the cell cycle

Cadmium is one of the most common heavy metal contaminants found in agricultural fields. MutSα, MutSβ, and MutSγ are three different MutS-associated protein heterodimer complexes consisting of MSH2/MSH6, MSH2/MSH3, and MSH2/MSH7, respectively. These complexes have different mismatch recognition prop...

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Autores principales: Zheng, Wen-Jie, Li, Wang-Qing, Peng, Yan, Shao, Ye, Tang, Li, Liu, Ci-Tao, Zhang, Dan, Zhang, Lan-Jing, Li, Ji-Huan, Luo, Wu-Zhong, Yuan, Zhi-Cheng, Zhao, Bing-Ran, Mao, Bi-Gang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9749859/
https://www.ncbi.nlm.nih.gov/pubmed/36531377
http://dx.doi.org/10.3389/fpls.2022.1068769
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author Zheng, Wen-Jie
Li, Wang-Qing
Peng, Yan
Shao, Ye
Tang, Li
Liu, Ci-Tao
Zhang, Dan
Zhang, Lan-Jing
Li, Ji-Huan
Luo, Wu-Zhong
Yuan, Zhi-Cheng
Zhao, Bing-Ran
Mao, Bi-Gang
author_facet Zheng, Wen-Jie
Li, Wang-Qing
Peng, Yan
Shao, Ye
Tang, Li
Liu, Ci-Tao
Zhang, Dan
Zhang, Lan-Jing
Li, Ji-Huan
Luo, Wu-Zhong
Yuan, Zhi-Cheng
Zhao, Bing-Ran
Mao, Bi-Gang
author_sort Zheng, Wen-Jie
collection PubMed
description Cadmium is one of the most common heavy metal contaminants found in agricultural fields. MutSα, MutSβ, and MutSγ are three different MutS-associated protein heterodimer complexes consisting of MSH2/MSH6, MSH2/MSH3, and MSH2/MSH7, respectively. These complexes have different mismatch recognition properties and abilities to support MMR. However, changes in mismatch repair genes (OsMSH2, OsMSH3, OsMSH6, and OsMSH7) of the MutS system in rice, one of the most important food crops, under cadmium stress and their association with E2Fs, the key transcription factors affecting cell cycles, are poorly evaluated. In this study, we systematically categorized six rice E2Fs and confirmed that OsMSHs were the downstream target genes of E2F using dual-luciferase reporter assays. In addition, we constructed four msh mutant rice varieties (msh2, msh3, msh6, and msh7) using the CRISPR-Cas9 technology, exposed these mutant rice seedlings to different concentrations of cadmium (0, 2, and 4 mg/L) and observed changes in their phenotype and transcriptomic profiles using RNA-Seq and qRT-PCR. We found that the difference in plant height before and after cadmium stress was more significant in mutant rice seedlings than in wild-type rice seedlings. Transcriptomic profiling and qRT-PCR quantification showed that cadmium stress specifically mobilized cell cycle-related genes ATR, CDKB2;1, MAD2, CycD5;2, CDKA;1, and OsRBR1. Furthermore, we expressed OsE2Fs in yeasts and found that heterologous E2F expression in yeast strains regulated cadmium tolerance by regulating MSHs expression. Further exploration of the underlying mechanisms revealed that cadmium stress may activate the CDKA/CYCD complex, which phosphorylates RBR proteins to release E2F, to regulate downstream MSHs expression and subsequent DNA damage repairment, thereby enhancing the response to cadmium stress.
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spelling pubmed-97498592022-12-15 E2Fs co-participate in cadmium stress response through activation of MSHs during the cell cycle Zheng, Wen-Jie Li, Wang-Qing Peng, Yan Shao, Ye Tang, Li Liu, Ci-Tao Zhang, Dan Zhang, Lan-Jing Li, Ji-Huan Luo, Wu-Zhong Yuan, Zhi-Cheng Zhao, Bing-Ran Mao, Bi-Gang Front Plant Sci Plant Science Cadmium is one of the most common heavy metal contaminants found in agricultural fields. MutSα, MutSβ, and MutSγ are three different MutS-associated protein heterodimer complexes consisting of MSH2/MSH6, MSH2/MSH3, and MSH2/MSH7, respectively. These complexes have different mismatch recognition properties and abilities to support MMR. However, changes in mismatch repair genes (OsMSH2, OsMSH3, OsMSH6, and OsMSH7) of the MutS system in rice, one of the most important food crops, under cadmium stress and their association with E2Fs, the key transcription factors affecting cell cycles, are poorly evaluated. In this study, we systematically categorized six rice E2Fs and confirmed that OsMSHs were the downstream target genes of E2F using dual-luciferase reporter assays. In addition, we constructed four msh mutant rice varieties (msh2, msh3, msh6, and msh7) using the CRISPR-Cas9 technology, exposed these mutant rice seedlings to different concentrations of cadmium (0, 2, and 4 mg/L) and observed changes in their phenotype and transcriptomic profiles using RNA-Seq and qRT-PCR. We found that the difference in plant height before and after cadmium stress was more significant in mutant rice seedlings than in wild-type rice seedlings. Transcriptomic profiling and qRT-PCR quantification showed that cadmium stress specifically mobilized cell cycle-related genes ATR, CDKB2;1, MAD2, CycD5;2, CDKA;1, and OsRBR1. Furthermore, we expressed OsE2Fs in yeasts and found that heterologous E2F expression in yeast strains regulated cadmium tolerance by regulating MSHs expression. Further exploration of the underlying mechanisms revealed that cadmium stress may activate the CDKA/CYCD complex, which phosphorylates RBR proteins to release E2F, to regulate downstream MSHs expression and subsequent DNA damage repairment, thereby enhancing the response to cadmium stress. Frontiers Media S.A. 2022-11-29 /pmc/articles/PMC9749859/ /pubmed/36531377 http://dx.doi.org/10.3389/fpls.2022.1068769 Text en Copyright © 2022 Zheng, Li, Peng, Shao, Tang, Liu, Zhang, Zhang, Li, Luo, Yuan, Zhao and Mao 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
Zheng, Wen-Jie
Li, Wang-Qing
Peng, Yan
Shao, Ye
Tang, Li
Liu, Ci-Tao
Zhang, Dan
Zhang, Lan-Jing
Li, Ji-Huan
Luo, Wu-Zhong
Yuan, Zhi-Cheng
Zhao, Bing-Ran
Mao, Bi-Gang
E2Fs co-participate in cadmium stress response through activation of MSHs during the cell cycle
title E2Fs co-participate in cadmium stress response through activation of MSHs during the cell cycle
title_full E2Fs co-participate in cadmium stress response through activation of MSHs during the cell cycle
title_fullStr E2Fs co-participate in cadmium stress response through activation of MSHs during the cell cycle
title_full_unstemmed E2Fs co-participate in cadmium stress response through activation of MSHs during the cell cycle
title_short E2Fs co-participate in cadmium stress response through activation of MSHs during the cell cycle
title_sort e2fs co-participate in cadmium stress response through activation of mshs during the cell cycle
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9749859/
https://www.ncbi.nlm.nih.gov/pubmed/36531377
http://dx.doi.org/10.3389/fpls.2022.1068769
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