Abstract
The response of plants to phosphate starvation engages PHR (CC-MYB-PHOSPHATE STARVATION RESPONSE) transcription factors that bind to P1BS (GNATATNC) promoter elements of phosphate-starvation induced (PSI) genes. The encoded proteins include single-domain SPX (SYG1/Pho81/XPR1) proteins. SPX proteins bind PHR proteins. Current models of SPX1: PHR interaction define only a high-phosphate role for SPX1, as an inositol (pyro)phosphate-dependent negative regulator of PHR. Here, by combination of chemical synthesis, orthogonal binding assays and molecular modeling we report that full-length SPX1 binds P1BS promoter elements and inositol (pyro)phosphates with similar affinity. Inositol (pyro)phosphates and DNA are reciprocally competing ligands of SPX1. Structural models of SPX1: inositol (pyrophosphate) and of SPX1: P1BS interaction are provided beside a working hypothesis of SPX1: PHR1 interaction. The results reveal the low-phosphate function of SPX1. These findings proffer a fundamentally different perspective of SPX involvement in the phosphate starvation response (PSR).
Data availability
The Molecular dynamics data generated in this study have been deposited in the MDRepo database under accession codes MDR00004441, MDR00004443, MDR00004444, MDR00004445, MDR00004446, MDR00004447, MDR00004448. The free energy calculation data are available at the University of East Anglia Digital Respository. Source data are provided with this paper.
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Acknowledgements
We thank Hui-Fen Kuo and Tzyy-Jen Chiou, Academia Sinica, Taiwan, for the gift of plasmid encoding SPX. Induced fit docking calculations and SPX1: DNA complex structure predictions were carried out on the High-Performance Computing Cluster supported by the Research and Specialist Computing Support service at the University of East Anglia. The molecular dynamics simulations and MMPBSA calculations needed to complete the second round review corrections were performed by A.M.H. using the high-performance computing facility at the International Center for Food and Health, Shanghai Ocean University. This research was funded in whole, or in part, by the Natural Environment Research Council (Grant number NE/W000350/1) to C.A.B. and the Wellcome Trust [Grant number 101010] to B.V.L.P. as a Wellcome Trust Senior Investigator. For the purpose of open access, the authors have applied a CC BY public copyright licence to any Author Accepted Manuscript version arising from this submission.
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C.A.B.: conceptualization, funding acquisition, project administration, formal analysis, supervision, investigation, methodology, writing—original draft, writing—review and editing. A.M.H.: investigation, methodology, writing—review and editing. M.G.: investigation. B.V.L.P.: funding acquisition, supervision, methodology, writing—review and editing. A.M.R.: investigation, supervision, methodology, writing—review and editing. M.L.S.: investigation, methodology, writing—review and editing. H.L.W.: formal analysis, investigation, methodology, writing—original draft, writing—review and editing.
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Whitfield, H.L., Gilmartin, M., Riley, A.M. et al. The intracellular inositol (pyro)phosphate receptor AtSPX1 reciprocally binds to P1BS DNA. Nat Commun (2026). https://doi.org/10.1038/s41467-026-69810-5
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DOI: https://doi.org/10.1038/s41467-026-69810-5
