Coupling of H3K27me3 recognition with transcriptional repression through the BAH-PHD-CPL2 complex in Arabidopsis

Yi-Zhe Zhang, Jianlong Yuan, Lingrui Zhang, Chunxiang Chen, Yuhua Wang, Guiping Zhang, Li Peng, Si-Si Xie, Jing Jiang, Jian-Kang Zhu (), Jiamu Du () and Cheng-Guo Duan ()
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Yi-Zhe Zhang: Shanghai Center for Plant Stress Biology and CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences
Jianlong Yuan: Shanghai Center for Plant Stress Biology and CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences
Lingrui Zhang: Purdue University
Chunxiang Chen: Shanghai Center for Plant Stress Biology and CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences
Yuhua Wang: Shanghai Center for Plant Stress Biology and CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences
Guiping Zhang: Shanghai Center for Plant Stress Biology and CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences
Li Peng: Shanghai Center for Plant Stress Biology and CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences
Si-Si Xie: Shanghai Center for Plant Stress Biology and CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences
Jing Jiang: State Key Laboratory of Crop Stress Adaptation and Improvement, School of Life Sciences, Henan University
Jian-Kang Zhu: Shanghai Center for Plant Stress Biology and CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences
Jiamu Du: 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
Cheng-Guo Duan: Shanghai Center for Plant Stress Biology and CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences

Nature Communications, 2020, vol. 11, issue 1, 1-16

Abstract: Abstract Histone 3 Lys 27 trimethylation (H3K27me3)-mediated epigenetic silencing plays a critical role in multiple biological processes. However, the H3K27me3 recognition and transcriptional repression mechanisms are only partially understood. Here, we report a mechanism for H3K27me3 recognition and transcriptional repression. Our structural and biochemical data showed that the BAH domain protein AIPP3 and the PHD proteins AIPP2 and PAIPP2 cooperate to read H3K27me3 and unmodified H3K4 histone marks, respectively, in Arabidopsis. The BAH-PHD bivalent histone reader complex silences a substantial subset of H3K27me3-enriched loci, including a number of development and stress response-related genes such as the RNA silencing effector gene ARGONAUTE 5 (AGO5). We found that the BAH-PHD module associates with CPL2, a plant-specific Pol II carboxyl terminal domain (CTD) phosphatase, to form the BAH-PHD-CPL2 complex (BPC) for transcriptional repression. The BPC complex represses transcription through CPL2-mediated CTD dephosphorylation, thereby causing inhibition of Pol II release from the transcriptional start site. Our work reveals a mechanism coupling H3K27me3 recognition with transcriptional repression through the alteration of Pol II phosphorylation states, thereby contributing to our understanding of the mechanism of H3K27me3-dependent silencing.

Date: 2020
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DOI: 10.1038/s41467-020-20089-0

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