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Nitric oxide controls shoot meristem activity via regulation of DNA methylation

Author

Listed:
  • Jian Zeng

    (Heidelberg University)

  • Xin’Ai Zhao

    (Heidelberg University)

  • Zhe Liang

    (Heidelberg University
    Biotechnology Research Institute, Chinese Academy of Agricultural Sciences)

  • Inés Hidalgo

    (Heidelberg University)

  • Michael Gebert

    (Heidelberg University
    CureVac)

  • Pengfei Fan

    (Heidelberg University)

  • Christian Wenzl

    (Heidelberg University)

  • Sebastian G. Gornik

    (Heidelberg University)

  • Jan U. Lohmann

    (Heidelberg University)

Abstract

Despite the importance of Nitric Oxide (NO) as signaling molecule in both plant and animal development, the regulatory mechanisms downstream of NO remain largely unclear. Here, we show that NO is involved in Arabidopsis shoot stem cell control via modifying expression and activity of ARGONAUTE 4 (AGO4), a core component of the RNA-directed DNA Methylation (RdDM) pathway. Mutations in components of the RdDM pathway cause meristematic defects, and reduce responses of the stem cell system to NO signaling. Importantly, we find that the stem cell inducing WUSCHEL transcription factor directly interacts with AGO4 in a NO dependent manner, explaining how these two signaling systems may converge to modify DNA methylation patterns. Taken together, our results reveal that NO signaling plays an important role in controlling plant stem cell homeostasis via the regulation of de novo DNA methylation.

Suggested Citation

  • Jian Zeng & Xin’Ai Zhao & Zhe Liang & Inés Hidalgo & Michael Gebert & Pengfei Fan & Christian Wenzl & Sebastian G. Gornik & Jan U. Lohmann, 2023. "Nitric oxide controls shoot meristem activity via regulation of DNA methylation," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43705-1
    DOI: 10.1038/s41467-023-43705-1
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    1. Kathryn Tunyasuvunakool & Jonas Adler & Zachary Wu & Tim Green & Michal Zielinski & Augustin Žídek & Alex Bridgland & Andrew Cowie & Clemens Meyer & Agata Laydon & Sameer Velankar & Gerard J. Kleywegt, 2021. "Highly accurate protein structure prediction for the human proteome," Nature, Nature, vol. 596(7873), pages 590-596, August.
    2. Caihuan Tian & Ying Wang & Haopeng Yu & Jun He & Jin Wang & Bihai Shi & Qingwei Du & Nicholas J. Provart & Elliot M. Meyerowitz & Yuling Jiao, 2019. "A gene expression map of shoot domains reveals regulatory mechanisms," Nature Communications, Nature, vol. 10(1), pages 1-12, December.
    3. Yanfei Ma & Andrej Miotk & Zoran Šutiković & Olga Ermakova & Christian Wenzl & Anna Medzihradszky & Christophe Gaillochet & Joachim Forner & Gözde Utan & Klaus Brackmann & Carlos S. Galván-Ampudia & T, 2019. "WUSCHEL acts as an auxin response rheostat to maintain apical stem cells in Arabidopsis," Nature Communications, Nature, vol. 10(1), pages 1-11, December.
    4. John Jumper & Richard Evans & Alexander Pritzel & Tim Green & Michael Figurnov & Olaf Ronneberger & Kathryn Tunyasuvunakool & Russ Bates & Augustin Žídek & Anna Potapenko & Alex Bridgland & Clemens Me, 2021. "Highly accurate protein structure prediction with AlphaFold," Nature, Nature, vol. 596(7873), pages 583-589, August.
    5. Sjon Hartman & Zeguang Liu & Hans Veen & Jorge Vicente & Emilie Reinen & Shanice Martopawiro & Hongtao Zhang & Nienke Dongen & Femke Bosman & George W. Bassel & Eric J. W. Visser & Julia Bailey-Serres, 2019. "Ethylene-mediated nitric oxide depletion pre-adapts plants to hypoxia stress," Nature Communications, Nature, vol. 10(1), pages 1-9, December.
    6. Yun Zhou & Xing Liu & Eric M. Engstrom & Zachary L. Nimchuk & Jose L. Pruneda-Paz & Paul T. Tarr & An Yan & Steve A. Kay & Elliot M. Meyerowitz, 2015. "Control of plant stem cell function by conserved interacting transcriptional regulators," Nature, Nature, vol. 517(7534), pages 377-380, January.
    7. Zhong Zhao & Stig U. Andersen & Karin Ljung & Karel Dolezal & Andrej Miotk & Sebastian J. Schultheiss & Jan U. Lohmann, 2010. "Hormonal control of the shoot stem-cell niche," Nature, Nature, vol. 465(7301), pages 1089-1092, June.
    8. Jian Feng & Chun Wang & Qingguo Chen & Hui Chen & Bo Ren & Xiaoming Li & Jianru Zuo, 2013. "S-nitrosylation of phosphotransfer proteins represses cytokinin signaling," Nature Communications, Nature, vol. 4(1), pages 1-9, June.
    9. Asuka Higo & Noriko Saihara & Fumihito Miura & Yoko Higashi & Megumi Yamada & Shojiro Tamaki & Tasuku Ito & Yoshiaki Tarutani & Tomoaki Sakamoto & Masayuki Fujiwara & Tetsuya Kurata & Yoichiro Fukao &, 2020. "DNA methylation is reconfigured at the onset of reproduction in rice shoot apical meristem," Nature Communications, Nature, vol. 11(1), pages 1-12, December.
    10. Andrea Leibfried & Jennifer P. C. To & Wolfgang Busch & Sandra Stehling & Andreas Kehle & Monika Demar & Joseph J. Kieber & Jan U. Lohmann, 2005. "WUSCHEL controls meristem function by direct regulation of cytokinin-inducible response regulators," Nature, Nature, vol. 438(7071), pages 1172-1175, December.
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