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Histone chaperone ASF1 mediates H3.3-H4 deposition in Arabidopsis

Author

Listed:
  • Zhenhui Zhong

    (University of California)

  • Yafei Wang

    (Northwest A&F University)

  • Ming Wang

    (University of California)

  • Fan Yang

    (Northwest A&F University)

  • Quentin Angelo Thomas

    (University of Copenhagen)

  • Yan Xue

    (University of California)

  • Yaxin Zhang

    (Fujian Agriculture and Forestry University)

  • Wanlu Liu

    (Zhejiang University-University of Edinburgh Institute (ZJU-UoE Institute), Zhejiang University School of Medicine, International Campus, Zhejiang University)

  • Yasaman Jami-Alahmadi

    (University of California)

  • Linhao Xu

    (Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), OT Gatersleben)

  • Suhua Feng

    (University of California
    University of California)

  • Sebastian Marquardt

    (University of Copenhagen)

  • James A. Wohlschlegel

    (University of California)

  • Israel Ausin

    (Northwest A&F University)

  • Steven E. Jacobsen

    (University of California
    University of California)

Abstract

Histone chaperones and chromatin remodelers control nucleosome dynamics, which are essential for transcription, replication, and DNA repair. The histone chaperone Anti-Silencing Factor 1 (ASF1) plays a central role in facilitating CAF-1-mediated replication-dependent H3.1 deposition and HIRA-mediated replication-independent H3.3 deposition in yeast and metazoans. Whether ASF1 function is evolutionarily conserved in plants is unknown. Here, we show that Arabidopsis ASF1 proteins display a preference for the HIRA complex. Simultaneous mutation of both Arabidopsis ASF1 genes caused a decrease in chromatin density and ectopic H3.1 occupancy at loci typically enriched with H3.3. Genetic, transcriptomic, and proteomic data indicate that ASF1 proteins strongly prefers the HIRA complex over CAF-1. asf1 mutants also displayed an increase in spurious Pol II transcriptional initiation and showed defects in the maintenance of gene body CG DNA methylation and in the distribution of histone modifications. Furthermore, ectopic targeting of ASF1 caused excessive histone deposition, less accessible chromatin, and gene silencing. These findings reveal the importance of ASF1-mediated histone deposition for proper epigenetic regulation of the genome.

Suggested Citation

  • Zhenhui Zhong & Yafei Wang & Ming Wang & Fan Yang & Quentin Angelo Thomas & Yan Xue & Yaxin Zhang & Wanlu Liu & Yasaman Jami-Alahmadi & Linhao Xu & Suhua Feng & Sebastian Marquardt & James A. Wohlschl, 2022. "Histone chaperone ASF1 mediates H3.3-H4 deposition in Arabidopsis," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-34648-0
    DOI: 10.1038/s41467-022-34648-0
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    References listed on IDEAS

    as
    1. Qikun Liu & Sylvain Bischof & C. Jake Harris & Zhenhui Zhong & Lingyu Zhan & Calvin Nguyen & Andrew Rashoff & William D. Barshop & Fei Sun & Suhua Feng & Magdalena Potok & Javier Gallego-Bartolome & J, 2020. "The characterization of Mediator 12 and 13 as conditional positive gene regulators in Arabidopsis," Nature Communications, Nature, vol. 11(1), pages 1-13, December.
    2. Ilnaz M. Klimovskaia & Clifford Young & Caroline B. Strømme & Patrice Menard & Zuzana Jasencakova & Jakob Mejlvang & Katrine Ask & Michael Ploug & Michael L. Nielsen & Ole N. Jensen & Anja Groth, 2014. "Tousled-like kinases phosphorylate Asf1 to promote histone supply during DNA replication," Nature Communications, Nature, vol. 5(1), pages 1-13, May.
    3. Quentin Angelo Thomas & Ryan Ard & Jinghan Liu & Bingnan Li & Jingwen Wang & Vicent Pelechano & Sebastian Marquardt, 2020. "Transcript isoform sequencing reveals widespread promoter-proximal transcriptional termination in Arabidopsis," Nature Communications, Nature, vol. 11(1), pages 1-15, December.
    4. Magdalena E. Potok & Yafei Wang & Linhao Xu & Zhenhui Zhong & Wanlu Liu & Suhua Feng & Bilguudei Naranbaatar & Shima Rayatpisheh & Zonghua Wang & James A. Wohlschlegel & Israel Ausin & Steven E. Jacob, 2019. "Arabidopsis SWR1-associated protein methyl-CpG-binding domain 9 is required for histone H2A.Z deposition," Nature Communications, Nature, vol. 10(1), pages 1-14, December.
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