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Arabidopsis guard cell chloroplasts import cytosolic ATP for starch turnover and stomatal opening

Author

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  • Shey-Li Lim

    (University of Hong Kong)

  • Sabrina Flütsch

    (ETH Zürich)

  • Jinhong Liu

    (University of Hong Kong)

  • Luca Distefano

    (ETH Zürich)

  • Diana Santelia

    (ETH Zürich)

  • Boon Leong Lim

    (University of Hong Kong
    HKU Shenzhen Institute of Research and Innovation
    The Chinese University of Hong Kong)

Abstract

Stomatal opening requires the provision of energy in the form of ATP for proton pumping across the guard cell (GC) plasma membrane and for associated metabolic rearrangements. The source of ATP for GCs is a matter of ongoing debate that is mainly fuelled by controversies around the ability of GC chloroplasts (GCCs) to perform photosynthesis. By imaging compartment-specific fluorescent ATP and NADPH sensor proteins in Arabidopsis, we show that GC photosynthesis is limited and mitochondria are the main source of ATP. Unlike mature mesophyll cell (MC) chloroplasts, which are impermeable to cytosolic ATP, GCCs import cytosolic ATP through NUCLEOTIDE TRANSPORTER (NTT) proteins. GCs from ntt mutants exhibit impaired abilities for starch biosynthesis and stomatal opening. Our work shows that GCs obtain ATP and carbohydrates via different routes from MCs, likely to compensate for the lower chlorophyll contents and limited photosynthesis of GCCs.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-28263-2
    DOI: 10.1038/s41467-022-28263-2
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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. Shey-Li Lim & Chia Pao Voon & Xiaoqian Guan & Yi Yang & Per Gardeström & Boon Leong Lim, 2020. "In planta study of photosynthesis and photorespiration using NADPH and NADH/NAD+ fluorescent protein sensors," Nature Communications, Nature, vol. 11(1), pages 1-12, December.
    3. Nicky Atkinson & Yuwei Mao & Kher Xing Chan & Alistair J. McCormick, 2020. "Condensation of Rubisco into a proto-pyrenoid in higher plant chloroplasts," Nature Communications, Nature, vol. 11(1), pages 1-9, December.
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    Cited by:

    1. Jinhong Liu & Shey-Li Lim & Jia Yi Zhong & Boon Leong Lim, 2022. "Bioenergetics of pollen tube growth in Arabidopsis thaliana revealed by ratiometric genetically encoded biosensors," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    2. 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.

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