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Abstract Vanadium (V) pollution potentially threatens human health. Here, it is found thatnsp1andnsp2,Rhizobiumsymbiosis defective mutants ofMedicago truncatula, are sensitive to V. Concentrations of phosphorus (P), iron (Fe), and sulfur (S) with V are negatively correlated in the shoots of wild‐type R108, but not in mutantnsp1andnsp2shoots. Mutations in the P transporterPHT1,PHO1, andVPTfamilies, Fe transporterIRT1, and S transporterSULTR1/3/4family confer varying degrees of V tolerance on plants. Among these gene families,MtPT1,MtZIP6,MtZIP9, andMtSULTR1; 1in R108 roots are significantly inhibited by V stress, whileMtPHO1; 2,MtVPT2, andMtVPT3are significantly induced. Overexpression ofArabidopsis thaliana VPT1orM. truncatula MtVPT3increases plant V tolerance. However, the response of these genes to V is weakened innsp1ornsp2and influenced by soil microorganisms. Mutations inNSPsreduce rhizobacterial diversity under V stress and simplify the V‐responsive operational taxonomic unit modules in co‐occurrence networks. Furthermore, R108 recruits more beneficial rhizobacteria related to V, P, Fe, and S than doesnsp1ornsp2. Thus, NSPs can modulate the accumulation and tolerance of legumes to V through P, Fe, and S transporters, ion homeostasis, and rhizobacterial community responses. 

SUMMARY Although vacuolar phosphate transporters (VPTs) are essential for plant phosphorus adaptation, their role inRhizobium–legume symbiosis is unclear. In this study, homologous genes ofVPT1(MtVPTs)were identified inMedicago truncatulato assess their roles inRhizobium–legume symbiosis and phosphorus adaptation.MtVPT2andMtVPT3mainly positively responded to low and high phosphate, respectively. However, bothmtvpt2andmtvpt3mutants displayed shoot phenotypes with high phosphate sensitivity and low phosphate tolerance. The root‐to‐shoot phosphate transfer efficiency was significantly enhanced inmtvpt3but weakened inmtvpt2, accompanied by lower and higher root cytosolic inorganic phosphate (Pi) concentration, respectively. Low phosphate inducedMtVPT2andMtVPT3expressions in nodules.MtVPT2andMtVPT3mutations markedly reduced the nodule number and nitrogenase activity under different phosphate conditions. Cytosolic Pi concentration in nodules was significantly lower inmtvpt2andmtvpt3than in the wildtype, especially in tissues near the base of nodules, probably due to inhibition of long‐distance Pi transport and cytosolic Pi supply. Also,mtvpt2andmtvpt3could not maintain a stable cytosolic Pi level in the nodule fixation zone as the wildtype under low phosphate stress. These findings show thatMtVPT2and MtVPT3modulate phosphorus adaptation and rhizobia–legume symbiosis, possibly by regulating long‐distance Pi transport.