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Chemical inhibition of stomatal differentiation by perturbation of the master-regulatory bHLH heterodimer via an ACT-Like domain

Author

Listed:
  • Ayami Nakagawa

    (Nagoya University)

  • Krishna Mohan Sepuru

    (The University of Texas at Austin
    The University of Texas at Austin)

  • Shu Jan Yip

    (Nagoya University)

  • Hyemin Seo

    (The University of Texas at Austin
    The University of Texas at Austin)

  • Calvin M. Coffin

    (The University of Texas at Austin
    The University of Texas at Austin)

  • Kota Hashimoto

    (Kwansei Gakuin University)

  • Zixuan Li

    (Kwansei Gakuin University)

  • Yasutomo Segawa

    (Myodaiji)

  • Rie Iwasaki

    (Nagoya University)

  • Hiroe Kato

    (Nagoya University)

  • Daisuke Kurihara

    (Nagoya University
    Nagoya University)

  • Yusuke Aihara

    (Nagoya University
    Chiyoda)

  • Stephanie Kim

    (The University of Texas at Austin)

  • Toshinori Kinoshita

    (Nagoya University)

  • Kenichiro Itami

    (Nagoya University)

  • Soon-Ki Han

    (Nagoya University
    Nagoya University)

  • Kei Murakami

    (Nagoya University
    Kwansei Gakuin University
    Chiyoda)

  • Keiko U. Torii

    (Nagoya University
    The University of Texas at Austin
    The University of Texas at Austin)

Abstract

Selective perturbation of protein interactions with chemical compounds enables dissection and control of developmental processes. Differentiation of stomata, cellular valves vital for plant growth and survival, is specified by the basic-helix-loop-helix (bHLH) heterodimers. Harnessing a new amination reaction, we here report a synthesis, derivatization, target identification, and mode of action of an atypical doubly-sulfonylated imidazolone, Stomidazolone, which triggers stomatal stem cell arrest. Our forward chemical genetics followed by biophysical analyses elucidates that Stomidazolone directly binds to the C-terminal ACT-Like (ACTL) domain of MUTE, a master regulator of stomatal differentiation, and perturbs its heterodimerization with a partner bHLH, SCREAM in vitro and in plant cells. On the other hand, Stomidazolone analogs that are biologically inactive do not bind to MUTE or disrupt the SCREAM-MUTE heterodimers. Guided by structural docking modeling, we rationally design MUTE with reduced Stomidazolone binding. These engineered MUTE proteins are fully functional and confer Stomidazolone resistance in vivo. Our study identifies doubly-sulfonylated imidazolone as a direct inhibitor of the stomatal master regulator, further expanding the chemical space for perturbing bHLH-ACTL proteins to manipulate plant development.

Suggested Citation

  • Ayami Nakagawa & Krishna Mohan Sepuru & Shu Jan Yip & Hyemin Seo & Calvin M. Coffin & Kota Hashimoto & Zixuan Li & Yasutomo Segawa & Rie Iwasaki & Hiroe Kato & Daisuke Kurihara & Yusuke Aihara & Steph, 2024. "Chemical inhibition of stomatal differentiation by perturbation of the master-regulatory bHLH heterodimer via an ACT-Like domain," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-53214-4
    DOI: 10.1038/s41467-024-53214-4
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    References listed on IDEAS

    as
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    3. Alistair M. Hetherington & F. Ian Woodward, 2003. "The role of stomata in sensing and driving environmental change," Nature, Nature, vol. 424(6951), pages 901-908, August.
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