Arabidopsis TRB proteins function in H3K4me3 demethylation by recruiting JMJ14

Ming Wang; Zhenhui Zhong; Javier Gallego-Bartolomé; Suhua Feng; Yuan-Hsin Shih; Mukun Liu; Jessica Zhou; John Curtis Richey; Charmaine Ng; Yasaman Jami-Alahmadi; James Wohlschlegel; Keqiang Wu; Steven E Jacobsen

doi:10.1038/s41467-023-37263-9

Arabidopsis TRB proteins function in H3K4me3 demethylation by recruiting JMJ14

Nat Commun. 2023 Mar 28;14(1):1736. doi: 10.1038/s41467-023-37263-9.

Authors

Ming Wang^#¹, Zhenhui Zhong^#¹, Javier Gallego-Bartolomé^{1

2}, Suhua Feng^{1

3}, Yuan-Hsin Shih^{1

4}, Mukun Liu¹, Jessica Zhou¹, John Curtis Richey¹, Charmaine Ng¹, Yasaman Jami-Alahmadi⁵, James Wohlschlegel⁵, Keqiang Wu⁴, Steven E Jacobsen^{6

7

8

9}

Affiliations

¹ Department of Molecular, Cell and Developmental Biology, University of California at Los Angeles, Los Angeles, CA, 90095, USA.
² Instituto de Biología Molecular y Celular de Plantas (IBMCP), CSIC-Universitat Politècnica de València, 46022, Valencia, Spain.
³ Eli & Edythe Broad Center of Regenerative Medicine & Stem Cell Research, University of California at Los Angeles, Los Angeles, CA, 90095, USA.
⁴ Institute of Plant Biology, National Taiwan University, Taipei, 10617, Taiwan.
⁵ Department of Biological Chemistry, University of California at Los Angeles, Los Angeles, CA, 90095, USA.
⁶ Department of Molecular, Cell and Developmental Biology, University of California at Los Angeles, Los Angeles, CA, 90095, USA. jacobsen@ucla.edu.
⁷ Eli & Edythe Broad Center of Regenerative Medicine & Stem Cell Research, University of California at Los Angeles, Los Angeles, CA, 90095, USA. jacobsen@ucla.edu.
⁸ Department of Biological Chemistry, University of California at Los Angeles, Los Angeles, CA, 90095, USA. jacobsen@ucla.edu.
⁹ Howard Hughes Medical Institute (HHMI), University of California at Los Angeles, Los Angeles, CA, 90095, USA. jacobsen@ucla.edu.

^# Contributed equally.

Abstract

Arabidopsis telomeric repeat binding factors (TRBs) can bind telomeric DNA sequences to protect telomeres from degradation. TRBs can also recruit Polycomb Repressive Complex 2 (PRC2) to deposit tri-methylation of H3 lysine 27 (H3K27me3) over certain target loci. Here, we demonstrate that TRBs also associate and colocalize with JUMONJI14 (JMJ14) and trigger H3K4me3 demethylation at some loci. The trb1/2/3 triple mutant and the jmj14-1 mutant show an increased level of H3K4me3 over TRB and JMJ14 binding sites, resulting in up-regulation of their target genes. Furthermore, tethering TRBs to the promoter region of genes with an artificial zinc finger (TRB-ZF) successfully triggers target gene silencing, as well as H3K27me3 deposition, and H3K4me3 removal. Interestingly, JMJ14 is predominantly recruited to ZF off-target sites with low levels of H3K4me3, which is accompanied with TRB-ZFs triggered H3K4me3 removal at these loci. These results suggest that TRB proteins coordinate PRC2 and JMJ14 activities to repress target genes via H3K27me3 deposition and H3K4me3 removal.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Arabidopsis Proteins* / genetics
Arabidopsis Proteins* / metabolism
Arabidopsis* / genetics
Arabidopsis* / metabolism
Demethylation
Gene Expression Regulation, Plant
Histones / genetics
Histones / metabolism
Jumonji Domain-Containing Histone Demethylases / genetics
Jumonji Domain-Containing Histone Demethylases / metabolism
Polycomb Repressive Complex 2 / genetics
Polycomb Repressive Complex 2 / metabolism
Polycomb-Group Proteins / genetics
Polycomb-Group Proteins / metabolism
Telomere-Binding Proteins / metabolism

Substances

histone H3 trimethyl Lys4
Histones
Arabidopsis Proteins
Polycomb Repressive Complex 2
Telomere-Binding Proteins
Polycomb-Group Proteins
JMJ14 protein, Arabidopsis
Jumonji Domain-Containing Histone Demethylases