Integrative Biology Journals
JIPB

J Integr Plant Biol. ›› 2022, Vol. 64 ›› Issue (12): 2385-2395.DOI: 10.1111/jipb.13369

• Research Articles • Previous Articles     Next Articles

The H3K9me2-binding protein AGDP3 limits DNA methylation and transcriptional gene silencing in Arabidopsis

Xuelin Zhou1,2†, Mengwei Wei1,2†, Wenfeng Nie1,3†, Yue Xi1,2, Li Peng1, Qijie Zheng1, Kai Tang4, Viswanathan Satheesh1, Yuhua Wang5, Jinyan Luo1, Xuan Du5, Rui Liu5, Zhenlin Yang5, Honggui La1, Yingli Zhong1,6, Yu Yang1, Jian‐Kang Zhu1,4, Jiamu Du5* and Mingguang Lei1*   

  1. 1 Shanghai Center for Plant Stress Biology, CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences, Shanghai 201602, China
    2 University of Chinese Academy of Sciences, Beijing 100049, China
    3 Department of Horticulture, College of Horticulture and Plant Protection, Yangzhou University, Yangzhou 225009, China
    4 Department of Horticulture & Landscape Architecture, Purdue University, West Lafayette, Idiana, 47906, USA
    5 Key Laboratory of Molecular Design for Plant Cell Factory of Guangdong Higher Education Institutes, Institute of Plant and Food Science, School of Life Sciences, Southern University of Science and Technology, Shenzhen 518055, China
    6 College of Bioscience and Biotechnology, Hunan Agricultural University, Changsha 410128, China

    †These authors contributed equally to this work.
    *Correspondences: Jiamu Du (dujm@sustech.edu.cn); Mingguang Lei (mglei@psc.ac.cn, Dr. Lei is fully responsible for the distribution of the materials associated with this article)
  • Received:2022-05-30 Accepted:2022-09-20 Online:2022-09-23 Published:2022-12-01

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Abstract:

DNA methylation, a conserved epigenetic mark, is critical for tuning temporal and spatial gene expression. The Arabidopsis thaliana DNA glycosylase/lyase REPRESSOR OF SILENCING 1 (ROS1) initiates active DNA demethylation and is required to prevent DNA hypermethylation at thousands of genomic loci. However, how ROS1 is recruited to specific loci is not well understood. Here, we report the discovery of Arabidopsis AGENET Domain Containing Protein 3 (AGDP3) as a cellular factor that is required to prevent gene silencing and DNA hypermethylation. AGDP3 binds to H3K9me2 marks in its target DNA via its AGD12 cassette. Analysis of the crystal structure of the AGD12 cassette of AGDP3 in complex with an H3K9me2 peptide revealed that dimethylated H3K9 and unmodified H3K4 are specifically anchored into two different surface pockets. A histidine residue located in the methyllysine binding aromatic cage provides AGDP3 with pH-dependent H3K9me2 binding capacity. Our results uncover a molecular mechanism for the regulation of DNA demethylation by the gene silencing mark H3K9me2.

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