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NODULIN HOMEOBOX is required for heterochromatin homeostasis in Arabidopsis

Author

Listed:
  • Zsolt Karányi

    (University of Debrecen
    University of Debrecen)

  • Ágnes Mosolygó-L

    (University of Debrecen)

  • Orsolya Feró

    (University of Debrecen)

  • Adrienn Horváth

    (University of Debrecen)

  • Beáta Boros-Oláh

    (University of Debrecen
    University of Debrecen
    University of Debrecen)

  • Éva Nagy

    (University of Debrecen)

  • Szabolcs Hetey

    (University of Debrecen)

  • Imre Holb

    (University of Debrecen)

  • Henrik Mihály Szaker

    (MATE University, Genetics and Biotechnology Institute
    Biological Research Centre)

  • Márton Miskei

    (University of Debrecen)

  • Tibor Csorba

    (MATE University, Genetics and Biotechnology Institute)

  • Lóránt Székvölgyi

    (University of Debrecen
    University of Debrecen)

Abstract

Arabidopsis NODULIN HOMEOBOX (NDX) is a nuclear protein described as a regulator of specific euchromatic genes within transcriptionally active chromosome arms. Here we show that NDX is primarily a heterochromatin regulator that functions in pericentromeric regions to control siRNA production and non-CG methylation. Most NDX binding sites coincide with pericentromeric het-siRNA loci that mediate transposon silencing, and are antagonistic with R-loop structures that are prevalent in euchromatic chromosomal arms. Inactivation of NDX leads to differential siRNA accumulation and DNA methylation, of which CHH/CHG hypomethylation colocalizes with NDX binding sites. Hi-C analysis shows significant chromatin structural changes in the ndx mutant, with decreased intrachromosomal interactions at pericentromeres where NDX is enriched in wild-type plants, and increased interchromosomal contacts between KNOT-forming regions, similar to those observed in DNA methylation mutants. We conclude that NDX is a key regulator of heterochromatin that is functionally coupled to het-siRNA loci and non-CG DNA methylation pathways.

Suggested Citation

  • Zsolt Karányi & Ágnes Mosolygó-L & Orsolya Feró & Adrienn Horváth & Beáta Boros-Oláh & Éva Nagy & Szabolcs Hetey & Imre Holb & Henrik Mihály Szaker & Márton Miskei & Tibor Csorba & Lóránt Székvölgyi, 2022. "NODULIN HOMEOBOX is required for heterochromatin homeostasis in Arabidopsis," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-32709-y
    DOI: 10.1038/s41467-022-32709-y
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    References listed on IDEAS

    as
    1. Zhihuan Gao & Hai-Liang Liu & Lucia Daxinger & Olga Pontes & Xinjian He & Weiqiang Qian & Huixin Lin & Mingtang Xie & Zdravko J. Lorkovic & Shoudong Zhang & Daisuke Miki & Xiangqiang Zhan & Dominique , 2010. "An RNA polymerase II- and AGO4-associated protein acts in RNA-directed DNA methylation," Nature, Nature, vol. 465(7294), pages 106-109, May.
    2. Congyao Xu & Zhe Wu & Hong-Chao Duan & Xiaofeng Fang & Guifang Jia & Caroline Dean, 2021. "R-loop resolution promotes co-transcriptional chromatin silencing," Nature Communications, Nature, vol. 12(1), pages 1-9, December.
    3. Charles Bou-Nader & Ankur Bothra & David N. Garboczi & Stephen H. Leppla & Jinwei Zhang, 2022. "Structural basis of R-loop recognition by the S9.6 monoclonal antibody," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    4. Cuijun Zhang & Xuan Du & Kai Tang & Zhenlin Yang & Li Pan & Peipei Zhu & Jinyan Luo & Yuwei Jiang & Hui Zhang & Huafang Wan & Xingang Wang & Fengkai Wu & W. Andy Tao & Xin-Jian He & Heng Zhang & Ray A, 2018. "Arabidopsis AGDP1 links H3K9me2 to DNA methylation in heterochromatin," Nature Communications, Nature, vol. 9(1), pages 1-14, December.
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