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A clade of receptor-like cytoplasmic kinases and 14-3-3 proteins coordinate inositol hexaphosphate accumulation

Author

Listed:
  • Li Lin Xu

    (Zhejiang University
    South China Agricultural University)

  • Meng Qi Cui

    (Zhejiang University
    South China Agricultural University)

  • Chen Xu

    (Zhejiang University
    South China Agricultural University)

  • Miao Jing Zhang

    (Zhejiang University)

  • Gui Xin Li

    (Zhejiang University)

  • Ji Ming Xu

    (Zhejiang University)

  • Xiao Dan Wu

    (Zhejiang University)

  • Chuan Zao Mao

    (Zhejiang University)

  • Wo Na Ding

    (Ningbo University)

  • Moussa Benhamed

    (Institute of Plant Sciences Paris-Saclay (IPS2))

  • Zhong Jie Ding

    (Zhejiang University)

  • Shao Jian Zheng

    (Zhejiang University
    South China Agricultural University)

Abstract

Inositol hexaphosphate (InsP6) is the major storage form of phosphorus in seeds. Reducing seed InsP6 content is a breeding objective in agriculture, as InsP6 negatively impacts animal nutrition and the environment. Nevertheless, how InsP6 accumulation is regulated remains largely unknown. Here, we identify a clade of receptor-like cytoplasmic kinases (RLCKs), named Inositol Polyphosphate-related Cytoplasmic Kinases 1-6 (IPCK1-IPCK6), deeply involved in InsP6 accumulation. The InsP6 concentration is dramatically reduced in seeds of ipck quadruple (T-4m/C-4m) and quintuple (C-5m) mutants, accompanied with the obviously increase of phosphate (Pi) concentration. The plasma membrane-localized IPCKs recruit IPK1 involved in InsP6 synthesis, and facilitate its binding and activity via phosphorylation of GRF 14-3-3 proteins. IPCKs also recruit IPK2s and PI-PLCs required for InsP4/InsP5 and InsP3 biosynthesis respectively, to form a potential IPCK-GRF-PLC-IPK2-IPK1 complex. Our findings therefore uncover a regulatory mechanism of InsP6 accumulation governed by IPCKs, shedding light on the mechanisms of InsP biosynthesis in eukaryotes.

Suggested Citation

  • Li Lin Xu & Meng Qi Cui & Chen Xu & Miao Jing Zhang & Gui Xin Li & Ji Ming Xu & Xiao Dan Wu & Chuan Zao Mao & Wo Na Ding & Moussa Benhamed & Zhong Jie Ding & Shao Jian Zheng, 2024. "A clade of receptor-like cytoplasmic kinases and 14-3-3 proteins coordinate inositol hexaphosphate accumulation," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-49102-6
    DOI: 10.1038/s41467-024-49102-6
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    References listed on IDEAS

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    1. Naoki Yamaji & Yuma Takemoto & Takaaki Miyaji & Namiki Mitani-Ueno & Kaoru T. Yoshida & Jian Feng Ma, 2017. "Erratum: Reducing phosphorus accumulation in rice grains with an impaired transporter in the node," Nature, Nature, vol. 543(7643), pages 136-136, March.
    2. Martina K. Ried & Rebekka Wild & Jinsheng Zhu & Joka Pipercevic & Kristina Sturm & Larissa Broger & Robert K. Harmel & Luciano A. Abriata & Ludwig A. Hothorn & Dorothea Fiedler & Sebastian Hiller & Mi, 2021. "Inositol pyrophosphates promote the interaction of SPX domains with the coiled-coil motif of PHR transcription factors to regulate plant phosphate homeostasis," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    3. Naoki Yamaji & Yuma Takemoto & Takaaki Miyaji & Namiki Mitani-Ueno & Kaoru T. Yoshida & Jian Feng Ma, 2017. "Reducing phosphorus accumulation in rice grains with an impaired transporter in the node," Nature, Nature, vol. 541(7635), pages 92-95, January.
    4. Jia Zhou & Qinli Hu & Xinlong Xiao & Deqiang Yao & Shenghong Ge & Jin Ye & Haojie Li & Rujie Cai & Renyang Liu & Fangang Meng & Chao Wang & Jian-Kang Zhu & Mingguang Lei & Weiman Xing, 2021. "Mechanism of phosphate sensing and signaling revealed by rice SPX1-PHR2 complex structure," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
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