PHOSPHATE STARVATION RESPONSE1 (PHR1) is a central transcription factor (TF) of plant responses when phosphate (Pi) becomes limiting. We found that PHR1 binds 2,622 sites in the Arabidopsis genome, 664 located nearby Pi-starvation responsive genes. These sites are enriched in two motifs, P1BSI and P1BSII, displaying different binding affinities due to PHR1 acting either as dimer or monomer. A P1BSII- artificial promoter displays Pi starvation responsiveness, but at lower extent than its P1BSI counterpart, in line with the lower PHR1 binding affinity of P1BSII. Pi-starvation induced (PSI) targets with either P1BSI and P1BSII are enriched in different functional classes of genes, with P1BSI associated to core Pi starvation response genes. These binding sites also differ in their evolutionary constraints. In any case, their conservation was higher for binding sites prompting a transcriptional response by PHR1. Remarkably, binding sites nearby non-transcriptionally responsive genes were also conserved, indicative of functionality, e.g., as TF decoys. PSI PHR1 target genes are often also induced by drought and osmotic stress, compatible with the notion that plants reduce water content during Pi-starvation in a PHR1 dependent manner. This finding uncovers the physiological importance of the link between plant water content and Pi homeostasis.