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

SPX receptors regulate plant phosphate response via PHR transcription factors. Here, based on crystal structure analysis of rice PHR2 complexes, the authors propose that SPX2 regulates PHR2 by preventing DNA binding and oligomerisation of the PHR2 CC domain. 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(6)/PHR2 complex and of the PHR2 DNA binding (MYB) domain in complex with target DNA at resolutions of 3.1 angstrom and 2.7 angstrom, respectively. In the SPX2/InsP(6)/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.

Automated summary

In this study, the authors investigate the regulation of PHR2 by SPX2 based on crystal structure analysis. They propose that SPX2 prevents the DNA binding and oligomerisation of PHR2 to inactivate it. These findings provide insights into how PP-InsPs activate SPX receptor proteins to target PHR family transcription factors.