EMF1 functions as a 3D chromatin modulator in Arabidopsis

Jiayue Shu; Linhua Sun; Dingyue Wang; Xiaochang Yin; Minqi Yang; Zhijia Yang; Zheng Gao; Yuehui He; Myriam Calonje; Jinsheng Lai; Xing Wang Deng; Hang He; Yue Zhou

doi:10.1016/j.molcel.2024.10.031

EMF1 functions as a 3D chromatin modulator in Arabidopsis

Mol Cell. 2024 Nov 15:S1097-2765(24)00871-2. doi: 10.1016/j.molcel.2024.10.031. Online ahead of print.

Authors

Jiayue Shu¹, Linhua Sun², Dingyue Wang¹, Xiaochang Yin³, Minqi Yang¹, Zhijia Yang⁴, Zheng Gao¹, Yuehui He⁵, Myriam Calonje⁶, Jinsheng Lai⁴, Xing Wang Deng⁵, Hang He⁷, Yue Zhou⁸

Affiliations

¹ State Key Laboratory of Protein and Plant Gene Research, School of Advanced Agricultural Sciences, Peking-Tsinghua Center for Life Sciences, Peking University, Beijing 100871, China.
² College of Life Sciences, Nanjing Normal University, Nanjing 210023, China.
³ School of Breeding and Multiplication (Sanya Institute of Breeding and Multiplication), Hainan University, Sanya 572025, China.
⁴ State Key Laboratory of Plant Physiology and Biochemistry & National Maize Improvement Center, Department of Plant Genetics and Breeding, China Agricultural University, Beijing 100183, China.
⁵ State Key Laboratory of Protein and Plant Gene Research, School of Advanced Agricultural Sciences, Peking-Tsinghua Center for Life Sciences, Peking University, Beijing 100871, China; Peking University Institute of Advanced Agricultural Sciences, Shandong Laboratory of Advanced Agriculture Sciences in Weifang, Weifang 261325, China.
⁶ Institute of Plant Biochemistry and Photosynthesis (IBVF-CSIC), Avenida Américo Vespucio 49, Seville 41092, Spain.
⁷ State Key Laboratory of Protein and Plant Gene Research, School of Advanced Agricultural Sciences, Peking-Tsinghua Center for Life Sciences, Peking University, Beijing 100871, China; Peking University Institute of Advanced Agricultural Sciences, Shandong Laboratory of Advanced Agriculture Sciences in Weifang, Weifang 261325, China. Electronic address: hehang@pku.edu.cn.
⁸ State Key Laboratory of Protein and Plant Gene Research, School of Advanced Agricultural Sciences, Peking-Tsinghua Center for Life Sciences, Peking University, Beijing 100871, China. Electronic address: yue_zhou@pku.edu.cn.

PMID: 39566504
DOI: 10.1016/j.molcel.2024.10.031

Abstract

It is well known that genome organizers, like mammalian CCCTC-binding factor (CTCF) or Drosophila architectural proteins CP190 and BEAF-32, contribute to the three-dimensional (3D) organization of the genome and ensure normal gene transcription. However, bona fide genome organizers have not been identified in plants. Here, we show that EMBRYONIC FLOWER1 (EMF1) functions as a genome modulator in Arabidopsis. EMF1 interacts with the cohesin component SISTER CHROMATIN COHESION3 (SCC3), and both proteins are enriched at compartment domain (CD) boundaries. Accordingly, emf1 and scc3 show a strength decrease at the CD boundary in which these proteins colocalize. EMF1 maintains CD boundary strength, either independently or in cooperation with histone modifications. Moreover, EMF1 is required to maintain gene-resolution interactions and to block long-range aberrant chromatin loops. These data unveil a key role of EMF1 in regulating 3D chromatin structure.

Keywords: 3D chromatin structure; EMF1; cohesin; compartment domain; histone modification; modulator.