ABSTRACT: Phosphate (P) fertilization induces a myriad of plant rhizosphere processes, required for a better P plant use. However, extended knowledge about plant responses to polyphosphates (PolyP) is still scarce, particularly transcriptomic and functional traits of root-induced rhizosphere processes. The present study aims to investigate belowground traits related to root transcriptomic changes, rhizosphere acidification, root growth, and P acquisition of durum wheat under PolyPs (PolyB and PolyC) supply. Root molecular traits were differentially expressed in response to PolyPs types, with 2481 and 184 genes were differentially expressed (compared to OrthoP) under PolyB (445 up- and 2036 down-regulated) and PolyC (71 up- and 113 down-regulated), respectively. Specifically, PolyB significantly influenced the expression of genes encoding the key enzymes in glycolysis, citrate cycle and acid phosphatases, OGDH, MDH, and ENO, PAP21 genes were upregulated, while TPI, PFK and LDH genes were downregulated. The modulated expression of TCA cycle and PAP genes can presumably explain the induced rhizosphere acidification (pH decreased from 8 to 6.3) and acid phosphatases activity (in root, rhizosphere soil and rhizosphere soil solution) under PolyPs, which consequently increased rhizosphere soil P availability (145% compared to OrthoP). This increase in P availability was concomitant with the modulation of root morphological traits and the upregulation of the AUX1 and ABA transporters genes, indicating PolyPs regulatory role in root growth for efficient P uptake. Moreover, PolyB significantly upregulated the expression of SPX3, which is indispensable for the absorption and transport of inorganic P to both roots and shoots. This was physiologically reflected by the increased shoot (36%) and root (61%) Pi contents in response to PolyB compared to OrthoP. Taken together, our findings provide novel and consistent evidence that enhanced P acquisition from PolyPs entails coordinated regulation of the expression of genes related to root-rhizosphere processes (rhizosphere acidification and phosphatases exudation) and root morphology, which consequently induces physiological adaptive traits enabling enhanced availability, acquisition of P, and wheat growth performance.