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Hydrogen peroxide is required for light-induced stomatal opening across different plant species

Author

Listed:
  • Wen Shi

    (Shandong University)

  • Yue Liu

    (Shandong University
    Shanghai Jiao Tong University)

  • Na Zhao

    (Shandong University)

  • Lianmei Yao

    (Shandong University)

  • Jinge Li

    (Shandong Normal University)

  • Min Fan

    (Shandong University)

  • Bojian Zhong

    (Nanjing Normal University)

  • Ming-Yi Bai

    (Shandong University)

  • Chao Han

    (Shandong University)

Abstract

Stomatal movement is vital for plants to exchange gases and adaption to terrestrial habitats, which is regulated by environmental and phytohormonal signals. Here, we demonstrate that hydrogen peroxide (H2O2) is required for light-induced stomatal opening. H2O2 accumulates specifically in guard cells even when plants are under unstressed conditions. Reducing H2O2 content through chemical treatments or genetic manipulations results in impaired stomatal opening in response to light. This phenomenon is observed across different plant species, including lycopodium, fern, and monocotyledonous wheat. Additionally, we show that H2O2 induces the nuclear localization of KIN10 protein, the catalytic subunit of plant energy sensor SnRK1. The nuclear-localized KIN10 interacts with and phosphorylates the bZIP transcription factor bZIP30, leading to the formation of a heterodimer between bZIP30 and BRASSINAZOLE-RESISTANT1 (BZR1), the master regulator of brassinosteroid signaling. This heterodimer complex activates the expression of amylase, which enables guard cell starch degradation and promotes stomatal opening. Overall, these findings suggest that H2O2 plays a critical role in light-induced stomatal opening across different plant species.

Suggested Citation

  • Wen Shi & Yue Liu & Na Zhao & Lianmei Yao & Jinge Li & Min Fan & Bojian Zhong & Ming-Yi Bai & Chao Han, 2024. "Hydrogen peroxide is required for light-induced stomatal opening across different plant species," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-49377-9
    DOI: 10.1038/s41467-024-49377-9
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    References listed on IDEAS

    as
    1. Chao Han & Yue Liu & Wen Shi & Yan Qiao & Lingyan Wang & Yanchen Tian & Min Fan & Zhiping Deng & On Sun Lau & Geert De Jaeger & Ming-Yi Bai, 2020. "KIN10 promotes stomatal development through stabilization of the SPEECHLESS transcription factor," Nature Communications, Nature, vol. 11(1), pages 1-10, December.
    2. Zhen-Ming Pei & Yoshiyuki Murata & Gregor Benning & Sébastien Thomine & Birgit Klüsener & Gethyn J. Allen & Erwin Grill & Julian I. Schroeder, 2000. "Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells," Nature, Nature, vol. 406(6797), pages 731-734, August.
    3. Elena Baena-González & Filip Rolland & Johan M. Thevelein & Jen Sheen, 2007. "A central integrator of transcription networks in plant stress and energy signalling," Nature, Nature, vol. 448(7156), pages 938-942, August.
    4. Yanchen Tian & Min Fan & Zhaoxia Qin & Hongjun Lv & Minmin Wang & Zhe Zhang & Wenying Zhou & Na Zhao & Xiaohui Li & Chao Han & Zhaojun Ding & Wenfei Wang & Zhi-Yong Wang & Ming-Yi Bai, 2018. "Hydrogen peroxide positively regulates brassinosteroid signaling through oxidation of the BRASSINAZOLE-RESISTANT1 transcription factor," Nature Communications, Nature, vol. 9(1), pages 1-13, December.
    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. Shey-Li Lim & Sabrina Flütsch & Jinhong Liu & Luca Distefano & Diana Santelia & Boon Leong Lim, 2022. "Arabidopsis guard cell chloroplasts import cytosolic ATP for starch turnover and stomatal opening," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
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