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...
| Main Authors: | , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2022-11-01
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| Series: | Frontiers in Plant Science |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fpls.2022.1068769/full |
| _version_ | 1798015932879077376 |
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| author | Wen-Jie Zheng Wang-Qing Li Yan Peng Ye Shao Li Tang Ci-Tao Liu Dan Zhang Dan Zhang Lan-Jing Zhang Ji-Huan Li Wu-Zhong Luo Zhi-Cheng Yuan Bing-Ran Zhao Bing-Ran Zhao Bing-Ran Zhao Bi-Gang Mao Bi-Gang Mao |
| author_facet | Wen-Jie Zheng Wang-Qing Li Yan Peng Ye Shao Li Tang Ci-Tao Liu Dan Zhang Dan Zhang Lan-Jing Zhang Ji-Huan Li Wu-Zhong Luo Zhi-Cheng Yuan Bing-Ran Zhao Bing-Ran Zhao Bing-Ran Zhao Bi-Gang Mao Bi-Gang Mao |
| author_sort | Wen-Jie Zheng |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-04-11T15:42:38Z |
| format | Article |
| id | doaj.art-73365f62d5e343eab29cac900177a829 |
| institution | Directory Open Access Journal |
| issn | 1664-462X |
| language | English |
| last_indexed | 2024-04-11T15:42:38Z |
| publishDate | 2022-11-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Plant Science |
| spelling | doaj.art-73365f62d5e343eab29cac900177a8292022-12-22T04:15:44ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2022-11-011310.3389/fpls.2022.10687691068769E2Fs co-participate in cadmium stress response through activation of MSHs during the cell cycleWen-Jie Zheng0Wang-Qing Li1Yan Peng2Ye Shao3Li Tang4Ci-Tao Liu5Dan Zhang6Dan Zhang7Lan-Jing Zhang8Ji-Huan Li9Wu-Zhong Luo10Zhi-Cheng Yuan11Bing-Ran Zhao12Bing-Ran Zhao13Bing-Ran Zhao14Bi-Gang Mao15Bi-Gang Mao16Longping Branch, College of Biology, Hunan University, Changsha, ChinaLongping Branch, College of Biology, Hunan University, Changsha, ChinaState Key Laboratory of Hybrid Rice, Hunan Hybrid Rice Research Center, Changsha, ChinaState Key Laboratory of Hybrid Rice, Hunan Hybrid Rice Research Center, Changsha, ChinaState Key Laboratory of Hybrid Rice, Hunan Hybrid Rice Research Center, Changsha, ChinaCollege of Agricultural, Hunan Agricultural University, Changsha, ChinaState Key Laboratory of Hybrid Rice, Hunan Hybrid Rice Research Center, Changsha, ChinaCollege of Agricultural, Hunan Agricultural University, Changsha, ChinaCollege of Agricultural, Hunan Agricultural University, Changsha, ChinaCollege of Agricultural, Hunan Agricultural University, Changsha, ChinaState Key Laboratory of Hybrid Rice, Hunan Hybrid Rice Research Center, Changsha, ChinaState Key Laboratory of Hybrid Rice, Hunan Hybrid Rice Research Center, Changsha, ChinaLongping Branch, College of Biology, Hunan University, Changsha, ChinaState Key Laboratory of Hybrid Rice, Hunan Hybrid Rice Research Center, Changsha, ChinaCollege of Agricultural, Hunan Agricultural University, Changsha, ChinaLongping Branch, College of Biology, Hunan University, Changsha, ChinaState Key Laboratory of Hybrid Rice, Hunan Hybrid Rice Research Center, Changsha, ChinaCadmium 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.https://www.frontiersin.org/articles/10.3389/fpls.2022.1068769/fullcadmiumcell cycleE2FsMSHsDNA damageRNA-seq |
| spellingShingle | Wen-Jie Zheng Wang-Qing Li Yan Peng Ye Shao Li Tang Ci-Tao Liu Dan Zhang Dan Zhang Lan-Jing Zhang Ji-Huan Li Wu-Zhong Luo Zhi-Cheng Yuan Bing-Ran Zhao Bing-Ran Zhao Bing-Ran Zhao Bi-Gang Mao Bi-Gang Mao E2Fs co-participate in cadmium stress response through activation of MSHs during the cell cycle Frontiers in Plant Science cadmium cell cycle E2Fs MSHs DNA damage RNA-seq |
| 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 | cadmium cell cycle E2Fs MSHs DNA damage RNA-seq |
| url | https://www.frontiersin.org/articles/10.3389/fpls.2022.1068769/full |
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