Shoot-to-root communication is crucial for plant acclimation to phosphorus (P)-deficiency. Both sugars and miRNAs have been implicated as potential signal molecules transported through phloem from shoot to root for the regulation of gene expression and Pi uptake in the root. By studying the expression patterns of both a serine/threonine phosphatase gene (PvHAD1) and microRNA399 (miR399) in common bean (Phaseolus vulgaris L.), we provide evidence for the interaction between light, phloem transport, and miR399 in the systemic regulation of gene expression under P-deficiency. Especially, miR399 expression in both the shoot and the root requires photosynthetic carbon assimilation during the onset of P-deficiency. In contrast to systemic signaling, local sensing was the primary causal factor for rapid down-regulation of PvHAD1 by Pi prior to the reduction of miR399 level in P-deficient roots. Furthermore, this initial response to Pi in P-deficient root was also mimicked by the Pi analog, phosphonate (Phi). Our current findings suggest that plants have developed a highly coordinated dual regulatory pathway, namely long-distance signaling of P-deficiency from shoot to root versus local sensing of Pi in the root.