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Mechanistic insights into the regulation of plant phosphate homeostasis by the rice SPX2 – PHR2 complex

Author

Listed:
  • Zeyuan Guan

    (Huazhong Agricultural University)

  • Qunxia Zhang

    (Huazhong Agricultural University)

  • Zhifei Zhang

    (Huazhong Agricultural University)

  • Jiaqi Zuo

    (Huazhong Agricultural University)

  • Juan Chen

    (Huazhong Agricultural University)

  • Ruiwen Liu

    (Huazhong Agricultural University)

  • Julie Savarin

    (University of Geneva)

  • Larissa Broger

    (University of Geneva)

  • Peng Cheng

    (Huazhong Agricultural University)

  • Qiang Wang

    (Huazhong Agricultural University)

  • Kai Pei

    (Huazhong Agricultural University)

  • Delin Zhang

    (Huazhong Agricultural University)

  • Tingting Zou

    (Huazhong Agricultural University)

  • Junjie Yan

    (Huazhong Agricultural University)

  • Ping Yin

    (Huazhong Agricultural University)

  • Michael Hothorn

    (University of Geneva)

  • Zhu Liu

    (Huazhong Agricultural University)

Abstract

Phosphate (Pi) starvation response (PHR) transcription factors play key roles in plant Pi homeostasis maintenance. They are negatively regulated by stand-alone SPX proteins, cellular receptors for inositol pyrophosphate (PP-InsP) nutrient messengers. How PP-InsP-bound SPX interacts with PHRs is poorly understood. Here, we report crystal structures of the rice SPX2/InsP6/PHR2 complex and of the PHR2 DNA binding (MYB) domain in complex with target DNA at resolutions of 3.1 Å and 2.7 Å, respectively. In the SPX2/InsP6/PHR2 complex, the signalling-active SPX2 assembles into a domain-swapped dimer conformation and binds two copies of PHR2, targeting both its coiled-coil (CC) oligomerisation domain and MYB domain. Our results reveal that the SPX2 senses PP-InsPs to inactivate PHR2 by establishing severe steric clashes with the PHR2 MYB domain, preventing DNA binding, and by disrupting oligomerisation of the PHR2 CC domain, attenuating promoter binding. Our findings rationalize how PP-InsPs activate SPX receptor proteins to target PHR family transcription factors.

Suggested Citation

  • Zeyuan Guan & Qunxia Zhang & Zhifei Zhang & Jiaqi Zuo & Juan Chen & Ruiwen Liu & Julie Savarin & Larissa Broger & Peng Cheng & Qiang Wang & Kai Pei & Delin Zhang & Tingting Zou & Junjie Yan & Ping Yin, 2022. "Mechanistic insights into the regulation of plant phosphate homeostasis by the rice SPX2 – PHR2 complex," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-29275-8
    DOI: 10.1038/s41467-022-29275-8
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    References listed on IDEAS

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    1. 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.
    2. 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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    Cited by:

    1. Zeyuan Guan & Juan Chen & Ruiwen Liu & Yanke Chen & Qiong Xing & Zhangmeng Du & Meng Cheng & Jianjian Hu & Wenhui Zhang & Wencong Mei & Beijing Wan & Qiang Wang & Jie Zhang & Peng Cheng & Huanyu Cai &, 2023. "The cytoplasmic synthesis and coupled membrane translocation of eukaryotic polyphosphate by signal-activated VTC complex," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    2. Yukari Nagatoshi & Kenta Ikazaki & Yasufumi Kobayashi & Nobuyuki Mizuno & Ryohei Sugita & Yumiko Takebayashi & Mikiko Kojima & Hitoshi Sakakibara & Natsuko I. Kobayashi & Keitaro Tanoi & Kenichiro Fuj, 2023. "Phosphate starvation response precedes abscisic acid response under progressive mild drought in plants," Nature Communications, Nature, vol. 14(1), pages 1-16, December.

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