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

Article Article scientifique Article Mechanistic insights into the regulation of plant phosphate homeostasis by the rice SPX2 - PHR2 complex eng 2022-03-24 2022-03-24 author Guan Zeyuan 0000-0002-8909-866X National Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural University, Wuhan, 430070, China. author Zhang Qunxia National Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural University, Wuhan, 430070, China. author Zhang Zhifei National Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural University, Wuhan, 430070, China. author Zuo Jiaqi National Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural University, Wuhan, 430070, China. author Chen Juan National Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural University, Wuhan, 430070, China. author Liu Ruiwen National Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural University, Wuhan, 430070, China. author Savarin Julie 0000-0002-9655-2496 Structural Plant Biology Laboratory, Department of Botany and Plant Biology, University of Geneva, Geneva, 1211, Switzerland. 926485 author Broger Larissa Structural Plant Biology Laboratory, Department of Botany and Plant Biology, University of Geneva, Geneva, 1211, Switzerland. 95643 Département des sciences végétales (BIVEG) author Cheng Peng National Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural University, Wuhan, 430070, China. author Wang Qiang National Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural University, Wuhan, 430070, China. author Pei Kai National Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural University, Wuhan, 430070, China. author Zhang Delin National Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural University, Wuhan, 430070, China. author Zou Tingting 0000-0002-7240-1378 National Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural University, Wuhan, 430070, China. author Yan Junjie National Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural University, Wuhan, 430070, China. author Yin Ping 0000-0001-8001-221X National Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural University, Wuhan, 430070, China. author Hothorn Michael 0000-0002-3597-5698 Structural Plant Biology Laboratory, Department of Botany and Plant Biology, University of Geneva, Geneva, 1211, Switzerland. 826130 Département des sciences végétales (BIVEG) author Liu Zhu 0000-0003-4073-7237 National Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural University, Wuhan, 430070, China. liuzhu@mail.hzau.edu.cn. 1581 10.1038/s41467-022-29275-8 35332155 2041-1723 PMC8948245 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/InsP<sub>6</sub>/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/InsP<sub>6</sub>/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. Gene Expression Regulation, Plant Homeostasis Oryza / genetics Oryza / metabolism Phosphates / metabolism Plant Proteins / genetics Plant Proteins / metabolism Plants / metabolism Transcription Factors / metabolism Dewey 580 European Commission System-wide discovery and analysis of inositol pyrophosphate signaling networks in plants 818696 INSPIRE EU H2020 45 Département des sciences végétales 163 false Nature communications 13 1 75feb16d-7531-4d88-bece-086eed430e0d Appendix Public 41467_2022_29275_MOESM2_ESM.pdf 4657860 application/pdf 9cbbc57719e8e0368fa9ac5ac97f0bb95bc0f21daf75ff1c8f7e4a2882e3e484 9e4c4f14-150e-4eae-8028-8a65d0177e7e Appendix Public 41467_2022_29275_MOESM1_ESM.pdf 3267368 application/pdf 1f21b2e3511b6166b3c3ab23668aabd5d8d398862e9fe7286e1331681716cfdd a6423a19-22cd-4ccb-894a-41c6116b26d7 Appendix Public 41467_2022_29275_MOESM3_ESM.pdf 1029148 application/pdf 9683379c5df0f5f6ac55592a1afc49303a1641685ace4cfca531aedbbc046a1a 305ebd04-7452-4622-b434-e5f9b17afd55 Article (Published version) Public Article-scientifique-from-europePmc.pdf 2702910 application/pdf CC BY 5293dfecb2a45df91d9e4762fac5eef7f6bae86934d77d2b560910b406162304 openAccess Faculté des sciences / Section de biologie / Département des sciences végétales

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Mechanistic insights into the regulation of plant phosphate homeostasis by the rice SPX2 - PHR2 complex	Nature communications			2022	109	91

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Savarin, Julie