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Light-induced stomatal opening requires phosphorylation of the C-terminal autoinhibitory domain of plasma membrane H+-ATPase

Author

Listed:
  • Saashia Fuji

    (Yamaguchi University)

  • Shota Yamauchi

    (Yamaguchi University
    Tokyo University of Science)

  • Naoyuki Sugiyama

    (Kyoto University)

  • Takayuki Kohchi

    (Kyoto University)

  • Ryuichi Nishihama

    (Kyoto University
    Tokyo University of Science)

  • Ken-ichiro Shimazaki

    (Kyushu University)

  • Atsushi Takemiya

    (Yamaguchi University)

Abstract

Plasma membrane H+-ATPase provides the driving force for light-induced stomatal opening. However, the mechanisms underlying the regulation of its activity remain unclear. Here, we show that the phosphorylation of two Thr residues in the C-terminal autoinhibitory domain is crucial for H+-ATPase activation and stomatal opening in Arabidopsis thaliana. Using phosphoproteome analysis, we show that blue light induces the phosphorylation of Thr-881 within the C-terminal region I, in addition to penultimate Thr-948 in AUTOINHIBITED H+-ATPASE 1 (AHA1). Based on site-directed mutagenesis experiments, phosphorylation of both Thr residues is essential for H+ pumping and stomatal opening in response to blue light. Thr-948 phosphorylation is a prerequisite for Thr-881 phosphorylation by blue light. Additionally, red light-driven guard cell photosynthesis induces Thr-881 phosphorylation, possibly contributing to red light-dependent stomatal opening. Our findings provide mechanistic insights into H+-ATPase activation that exploits the ion transport across the plasma membrane and light signalling network in guard cells.

Suggested Citation

  • Saashia Fuji & Shota Yamauchi & Naoyuki Sugiyama & Takayuki Kohchi & Ryuichi Nishihama & Ken-ichiro Shimazaki & Atsushi Takemiya, 2024. "Light-induced stomatal opening requires phosphorylation of the C-terminal autoinhibitory domain of plasma membrane H+-ATPase," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-45236-9
    DOI: 10.1038/s41467-024-45236-9
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    References listed on IDEAS

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    1. Toshinori Kinoshita & Michio Doi & Noriyuki Suetsugu & Takatoshi Kagawa & Masamitsu Wada & Ken-ichiro Shimazaki, 2001. "phot1 and phot2 mediate blue light regulation of stomatal opening," Nature, Nature, vol. 414(6864), pages 656-660, December.
    2. 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.
    3. Bjørn P. Pedersen & Morten J. Buch-Pedersen & J. Preben Morth & Michael G. Palmgren & Poul Nissen, 2007. "Crystal structure of the plasma membrane proton pump," Nature, Nature, vol. 450(7172), pages 1111-1114, December.
    4. Lanxin Li & Inge Verstraeten & Mark Roosjen & Koji Takahashi & Lesia Rodriguez & Jack Merrin & Jian Chen & Lana Shabala & Wouter Smet & Hong Ren & Steffen Vanneste & Sergey Shabala & Bert De Rybel & D, 2021. "Cell surface and intracellular auxin signalling for H+ fluxes in root growth," Nature, Nature, vol. 599(7884), pages 273-277, November.
    5. Asami Hiyama & Atsushi Takemiya & Shintaro Munemasa & Eiji Okuma & Naoyuki Sugiyama & Yasuomi Tada & Yoshiyuki Murata & Ken-ichiro Shimazaki, 2017. "Blue light and CO2 signals converge to regulate light-induced stomatal opening," Nature Communications, Nature, vol. 8(1), pages 1-13, December.
    6. Peng Zhao & Chaoran Zhao & Dandan Chen & Caihong Yun & Huilin Li & Lin Bai, 2021. "Structure and activation mechanism of the hexameric plasma membrane H+-ATPase," Nature Communications, Nature, vol. 12(1), pages 1-11, December.
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