DNA methylation underpins the epigenomic landscape regulating genome transcription in Arabidopsis

Zhao, Lun1,2; Zhou, Qiangwei1; He, Li2; Deng, Li1; Lozano-Duran, Rosa2,3; Li, Guoliang1,4,5; Zhu, Jian-Kang2,6,7,8

2022-09-20

10.1186/s13059-022-02768-x

GENOME BIOLOGY   Impact Factor & Quartile

1474-760X

Background It is challenging to determine the effect of DNA methylation on the epigenetic landscape and the function in higher organisms due to the lack of DNA methylation-free mutants. Results Here, the analysis of a recently generated Arabidopsis mutant completely devoid of DNA methylation reveals that DNA methylation underpins the genome-wide landscape of histone modifications. Complete loss of DNA methylation causes an upheaval of the histone modification landscape, including complete loss of H3K9me2 and widespread redistribution of active and H3K27me3 histone marks, mostly owing to the role of DNA methylation in initiating H3K9me2 deposition and excluding active marks and repressive mark H3K27me3; CG and non-CG methylation can act independently at some genomic regions while they act cooperatively at many other regions. The transcriptional reprogramming upon loss of all DNA methylation correlates with the extensive redistribution or switches of the examined histone modifications. Histone modifications retained or gained in the DNA methylation-free mutant serve as DNA methylation-independent transcriptional regulatory signals: active marks promote genome transcription, whereas the repressive mark H3K27me3 compensates for the lack of DNA hypermethylation/H3K9me2 at multiple transposon families. Conclusions Our results show that an intact DNA methylome constitutes the scaffolding of the epigenomic landscape in Arabidopsis and is critical for controlled genome transcription and ultimately for proper growth and development.

DNA methylation-free plant Histone modification Chromatin state

SCI

English

Corresponding

National Natural Science Foundation of China["32222063","32100458","32188102"] ; National Key Research and Development Program of China["2021YFF1000100","2021YFA1300404"] ; Fundamental Research Funds for the Central Universities[2662021PY005] ; International Postdoctoral Exchange Fellowship Program 2020 by the Office of China Postdoctoral Council[PC2020034] ; First Class Discipline Construction Funds of College of Plant Science and Technology of Huazhong Agricultural University[2022ZKPY004]

Biotechnology & Applied Microbiology ; Genetics & Heredity

Biotechnology & Applied Microbiology ; Genetics & Heredity

WOS:000855784200001

BMC

MOLECULAR BIOLOGY & GENETICS

Web of Science

1.Huazhong Agr Univ, Natl Engn Res Ctr Rapeseed, Natl Key Lab Crop Genet Improvement, Hubei Hongshan Lab, Wuhan 430070, Peoples R China
2.Chinese Acad Sci, Shanghai Ctr Plant Stress Biol, Ctr Excellence Mol Plant Sci, Shanghai 201602, Peoples R China
3.Eberhard Karls Univ Tubingen, Ctr Plant Mol Biol ZMBP, Dept Plant Biochem, D-72076 Tubingen, Germany
4.Huazhong Agr Univ, Hubei Key Lab Agr Bioinformat, Wuhan 430070, Peoples R China
5.Huazhong Agr Univ, Hubei Engn Technol Res Ctr Agr Big Data, Wuhan 430070, Peoples R China
6.Southern Univ Sci & Technol, Inst Adv Biotechnol, Shenzhen 518055, Peoples R China
7.Southern Univ Sci & Technol, Sch Life Sci, Shenzhen 518055, Peoples R China
8.Chinese Acad Agr Sci, Ctr Adv Bioind Technol, Beijing 100081, Peoples R China

Zhao, Lun,Zhou, Qiangwei,He, Li,et al. DNA methylation underpins the epigenomic landscape regulating genome transcription in Arabidopsis[J]. GENOME BIOLOGY,2022,23(1).

Zhao, Lun.,Zhou, Qiangwei.,He, Li.,Deng, Li.,Lozano-Duran, Rosa.,...&Zhu, Jian-Kang.(2022).DNA methylation underpins the epigenomic landscape regulating genome transcription in Arabidopsis.GENOME BIOLOGY,23(1).

Zhao, Lun,et al."DNA methylation underpins the epigenomic landscape regulating genome transcription in Arabidopsis".GENOME BIOLOGY 23.1(2022).