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).