Accumulation of DNA damage alters microRNA gene transcription in Arabidopsis thaliana
Abstract Background MicroRNAs (miRNAs) and other epigenetic modifications play fundamental roles in all eukaryotic biological processes. DNA damage repair is a key process for maintaining the genomic integrity of different organisms exposed to diverse stresses. However, the reaction of miRNAs in the...
| Main Authors: | , , , , , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2022-12-01
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| Series: | BMC Plant Biology |
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| Online Access: | https://doi.org/10.1186/s12870-022-03951-9 |
| _version_ | 1811292436145635328 |
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| author | Juan Du Yang Liu Lu Lu Jianfei Shi Longqian Xu Qi Li Xiaofei Cheng Jinfeng Chen Xiaoming Zhang |
| author_facet | Juan Du Yang Liu Lu Lu Jianfei Shi Longqian Xu Qi Li Xiaofei Cheng Jinfeng Chen Xiaoming Zhang |
| author_sort | Juan Du |
| collection | DOAJ |
| description | Abstract Background MicroRNAs (miRNAs) and other epigenetic modifications play fundamental roles in all eukaryotic biological processes. DNA damage repair is a key process for maintaining the genomic integrity of different organisms exposed to diverse stresses. However, the reaction of miRNAs in the DNA damage repair process is unclear. Results In this study, we found that the simultaneous mutation of zinc finger DNA 3′-phosphoesterase (ZDP) and AP endonuclease 2 (APE2), two genes that play overlapping roles in active DNA demethylation and base excision repair (BER), led to genome-wide alteration of miRNAs. The transcripts of newly transcribed miRNA-encoding genes (MIRs) decreased significantly in zdp/ape2, indicating that the mutation of ZDP and APE2 affected the accumulation of miRNAs at the transcriptional level. In addition, the introduction of base damage with the DNA-alkylating reagent methyl methanesulfonate (MMS) accelerated the reduction of miRNAs in zdp/ape2. Further mutation of FORMAMIDOPYRIMIDINE DNA GLYCOSYLASE (FPG), a bifunctional DNA glycosylase/lyase, rescued the accumulation of miRNAs in zdp/ape2, suggesting that the accumulation of DNA damage repair intermediates induced the transcriptional repression of miRNAs. Conclusions Our investigation indicates that the accumulation of DNA damage repair intermediates inhibit miRNAs accumulation by inhibiting MIR transcriptions. |
| first_indexed | 2024-04-13T04:45:22Z |
| format | Article |
| id | doaj.art-c2dd0182c3f0433a9a6b0fb41d6c8ff4 |
| institution | Directory Open Access Journal |
| issn | 1471-2229 |
| language | English |
| last_indexed | 2024-04-13T04:45:22Z |
| publishDate | 2022-12-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Plant Biology |
| spelling | doaj.art-c2dd0182c3f0433a9a6b0fb41d6c8ff42022-12-22T03:01:51ZengBMCBMC Plant Biology1471-22292022-12-0122111310.1186/s12870-022-03951-9Accumulation of DNA damage alters microRNA gene transcription in Arabidopsis thalianaJuan Du0Yang Liu1Lu Lu2Jianfei Shi3Longqian Xu4Qi Li5Xiaofei Cheng6Jinfeng Chen7Xiaoming Zhang8State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of SciencesState Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of SciencesState Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of SciencesState Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of SciencesState Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of SciencesState Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of SciencesKey Laboratory of Germplasm Enhancement, Physiology and Ecology of Food Crops in Cold Region of Chinese Education Ministry, College of Agriculture, Northeast Agricultural UniversityState Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of SciencesState Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of SciencesAbstract Background MicroRNAs (miRNAs) and other epigenetic modifications play fundamental roles in all eukaryotic biological processes. DNA damage repair is a key process for maintaining the genomic integrity of different organisms exposed to diverse stresses. However, the reaction of miRNAs in the DNA damage repair process is unclear. Results In this study, we found that the simultaneous mutation of zinc finger DNA 3′-phosphoesterase (ZDP) and AP endonuclease 2 (APE2), two genes that play overlapping roles in active DNA demethylation and base excision repair (BER), led to genome-wide alteration of miRNAs. The transcripts of newly transcribed miRNA-encoding genes (MIRs) decreased significantly in zdp/ape2, indicating that the mutation of ZDP and APE2 affected the accumulation of miRNAs at the transcriptional level. In addition, the introduction of base damage with the DNA-alkylating reagent methyl methanesulfonate (MMS) accelerated the reduction of miRNAs in zdp/ape2. Further mutation of FORMAMIDOPYRIMIDINE DNA GLYCOSYLASE (FPG), a bifunctional DNA glycosylase/lyase, rescued the accumulation of miRNAs in zdp/ape2, suggesting that the accumulation of DNA damage repair intermediates induced the transcriptional repression of miRNAs. Conclusions Our investigation indicates that the accumulation of DNA damage repair intermediates inhibit miRNAs accumulation by inhibiting MIR transcriptions.https://doi.org/10.1186/s12870-022-03951-9DNA damage repairmiRNAZDPAPE2FPG |
| spellingShingle | Juan Du Yang Liu Lu Lu Jianfei Shi Longqian Xu Qi Li Xiaofei Cheng Jinfeng Chen Xiaoming Zhang Accumulation of DNA damage alters microRNA gene transcription in Arabidopsis thaliana BMC Plant Biology DNA damage repair miRNA ZDP APE2 FPG |
| title | Accumulation of DNA damage alters microRNA gene transcription in Arabidopsis thaliana |
| title_full | Accumulation of DNA damage alters microRNA gene transcription in Arabidopsis thaliana |
| title_fullStr | Accumulation of DNA damage alters microRNA gene transcription in Arabidopsis thaliana |
| title_full_unstemmed | Accumulation of DNA damage alters microRNA gene transcription in Arabidopsis thaliana |
| title_short | Accumulation of DNA damage alters microRNA gene transcription in Arabidopsis thaliana |
| title_sort | accumulation of dna damage alters microrna gene transcription in arabidopsis thaliana |
| topic | DNA damage repair miRNA ZDP APE2 FPG |
| url | https://doi.org/10.1186/s12870-022-03951-9 |
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