IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-45236-9.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-45236-9
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-45236-9?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    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. 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.
    5. 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.
    6. 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.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Jiyu Chen & Jing Gao & Qi Wang & Xianming Tan & Shenglan Li & Ping Chen & Taiwen Yong & Xiaochun Wang & Yushan Wu & Feng Yang & Wenyu Yang, 2022. "Blue-Light-Dependent Stomatal Density and Specific Leaf Weight Coordinate to Promote Gas Exchange of Soybean Leaves," Agriculture, MDPI, vol. 13(1), pages 1-13, December.
    2. Xingyun Liang & Defu Wang & Qing Ye & Jinmeng Zhang & Mengyun Liu & Hui Liu & Kailiang Yu & Yujie Wang & Enqing Hou & Buqing Zhong & Long Xu & Tong Lv & Shouzhang Peng & Haibo Lu & Pierre Sicard & Ale, 2023. "Stomatal responses of terrestrial plants to global change," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    3. 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.
    4. Marius Arend & Yizhong Yuan & M. Águila Ruiz-Sola & Nooshin Omranian & Zoran Nikoloski & Dimitris Petroutsos, 2023. "Widening the landscape of transcriptional regulation of green algal photoprotection," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    5. Wang, Lunche & Kisi, Ozgur & Zounemat-Kermani, Mohammad & Hu, Bo & Gong, Wei, 2016. "Modeling and comparison of hourly photosynthetically active radiation in different ecosystems," Renewable and Sustainable Energy Reviews, Elsevier, vol. 56(C), pages 436-453.
    6. Yeonggeun Song & Sukwoo Kim & Haeun Koo & Hyeonhwa Kim & Kidae Kim & Jaeuk Lee & Sujin Jang & Kyeong Cheol Lee, 2023. "Assessing the Suitability of Sediment Soil to Be Reused by Different Soil Treatments for Forest Agriculture," Sustainability, MDPI, vol. 15(15), pages 1-18, July.
    7. Hou, Jingxiang & Liu, Xuezhi & Zhang, Jiarui & Wei, Zhenhua & Ma, Yingying & Wan, Heng & Liu, Jie & Cui, Bingjing & Zong, Yuzheng & Chen, Yiting & Liang, Kehao & Liu, Fulai, 2023. "Combined application of biochar and partial root-zone drying irrigation improves water relations and water use efficiency of cotton plants under salt stress," Agricultural Water Management, Elsevier, vol. 290(C).
    8. Armando Hernández Pérez & Juana Cruz García Santiago & Valentín Robledo Torres & Alonso Méndez López & Alberto Sandoval Rangel & Neymar Camposeco Montejo, 2021. "Nitrate/ammonium ratio effect on the growth, yield and foliar anatomy of grafted tomato plants," Horticultural Science, Czech Academy of Agricultural Sciences, vol. 48(2), pages 80-89.
    9. Siddhartha Shankar Bhattacharyya & Pedro Mondaca & Oloka Shushupti & Sharjeel Ashfaq, 2023. "Interplay between Plant Functional Traits and Soil Carbon Sequestration under Ambient and Elevated CO 2 Levels," Sustainability, MDPI, vol. 15(9), pages 1-20, May.
    10. Yuki Hayashi & Kohei Fukatsu & Koji Takahashi & Satoru N. Kinoshita & Kyohei Kato & Taku Sakakibara & Keiko Kuwata & Toshinori Kinoshita, 2024. "Phosphorylation of plasma membrane H+-ATPase Thr881 participates in light-induced stomatal opening," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    11. Ki-Hong Jung & Jinwon Lee & Chris Dardick & Young-Su Seo & Peijian Cao & Patrick Canlas & Jirapa Phetsom & Xia Xu & Shu Ouyang & Kyungsook An & Yun-Ja Cho & Geun-Cheol Lee & Yoosook Lee & Gynheung An , 2008. "Identification and Functional Analysis of Light-Responsive Unique Genes and Gene Family Members in Rice," PLOS Genetics, Public Library of Science, vol. 4(8), pages 1-19, August.
    12. Chen, Haodong & Ma, Zhihui & Liu, Xianliang & Qiao, Kaiming & Xie, Longlong & Li, Zhenxing & Shen, Jun & Dai, Wei & Ou, Zhiqiang & Yibole, Hargen & Tegus, Ojiyed & Taskaev, Sergey V. & Chu, Ke & Long,, 2022. "Evaluation of thermomagnetic generation performance of classic magnetocaloric materials for harvesting low-grade waste heat," Applied Energy, Elsevier, vol. 306(PA).
    13. Aicha Nait Douch & Laila Boukhalef & Abdelhafed El Asbahani & Ali A. Al-Namazi & Khadija El Mehrach & Laila Bouqbis & Mourad Touaf & Fatima Ain-Lhout, 2022. "Photosynthetic Behavior of Argania spinosa (L.) Skeels Induced under Grazed and Ungrazed Conditions," Sustainability, MDPI, vol. 14(19), pages 1-12, September.
    14. Hong Il Choi & Sung-Won Hwang & Jongrae Kim & Byeonghyeok Park & EonSeon Jin & In-Geol Choi & Sang Jun Sim, 2021. "Augmented CO2 tolerance by expressing a single H+-pump enables microalgal valorization of industrial flue gas," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    15. T. Bertie Ansell & Wanling Song & Claire E. Coupland & Loic Carrique & Robin A. Corey & Anna L. Duncan & C. Keith Cassidy & Maxwell M. G. Geurts & Tim Rasmussen & Andrew B. Ward & Christian Siebold & , 2023. "LipIDens: simulation assisted interpretation of lipid densities in cryo-EM structures of membrane proteins," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    16. Yusuke Aihara & Bumpei Maeda & Kanna Goto & Koji Takahashi & Mika Nomoto & Shigeo Toh & Wenxiu Ye & Yosuke Toda & Mami Uchida & Eri Asai & Yasuomi Tada & Kenichiro Itami & Ayato Sato & Kei Murakami & , 2023. "Identification and improvement of isothiocyanate-based inhibitors on stomatal opening to act as drought tolerance-conferring agrochemicals," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    17. Yawen Li & Yinan Ding & Lili Qu & Xinru Li & Qinxuan Lai & Pingxia Zhao & Yongxiang Gao & Chengbin Xiang & Chunlei Cang & Xin Liu & Linfeng Sun, 2022. "Structure of the Arabidopsis guard cell anion channel SLAC1 suggests activation mechanism by phosphorylation," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    18. Zongxin Guo & Fredrik Orädd & Viktoria Bågenholm & Christina Grønberg & Jian Feng Ma & Peter Ott & Yong Wang & Magnus Andersson & Per Amstrup Pedersen & Kaituo Wang & Pontus Gourdon, 2024. "Diverse roles of the metal binding domains and transport mechanism of copper transporting P-type ATPases," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    19. Lea Reuter & Tanja Schmidt & Prabha Manishankar & Christian Throm & Jutta Keicher & Andrea Bock & Irina Droste-Borel & Claudia Oecking, 2021. "Light-triggered and phosphorylation-dependent 14-3-3 association with NON-PHOTOTROPIC HYPOCOTYL 3 is required for hypocotyl phototropism," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    20. Silber, Avner & Israeli, Yair & Levi, Menashe & Keinan, Ami & Chudi, George & Golan, Avner & Noy, Michael & Levkovitch, Irit & Narkis, Kfir & Naor, Amos & Assouline, Shmuel, 2013. "The roles of fruit sink in the regulation of gas exchange and water uptake: A case study for avocado," Agricultural Water Management, Elsevier, vol. 116(C), pages 21-28.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-45236-9. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.