Phosphate availability switches nitrate-driven phosphorus acquisition strategies in poplar: Arbuscular mycorrhizal symbiosis reshapes emergency foraging and homeostatic maintenance

Nitrogen (N) and phosphorus (P) imbalances constrain plant growth. This study examines how nitrate (NO 3 ⁻) supply affects root phosphate (Pi) uptake in Populus alba × P. glandulosa (84 K poplar) under varying Pi conditions, with a focus on the role of arbuscular mycorrhizal fungi (AMF, Rhizophagus irregularis ). Transcriptomic and physiological analyses reveal that Pi availability modulates NO 3 ⁻ responses and AMF symbiosis. At the hormone–root architecture level, under low Pi conditions, NO 3 ⁻ suppresses jasmonic acid (JA) signaling while activating auxin (IAA) and abscisic acid (ABA) pathways, thereby promoting lateral root proliferation. Under adequate Pi conditions, it primarily mediates SA/IAA/ABA-driven primary root elongation. AMF optimize this developmental response by regulating the expression of MIZ1 and WRKY70 . At the carbon–P interface, under low Pi, NO 3 ⁻ upregulates PEPC and MS to stimulate the secretion of organic acids, which, in concert with phosphatases, facilitate rhizosphere Pi mobilization. AMF further enhance the efficiency of carbon–P exchange, whereas under adequate Pi, carbon flux is redirected toward aboveground growth. Within P metabolism, under low Pi, NO 3 ⁻ activates PHT1 and P recycling through the PHL5 – HHO2 – SPX transcriptional network, albeit at increased energetic cost; under adequate Pi, recycling pathways are downregulated to maintain homeostasis. AMF reduce energy expenditure under low Pi by substituting hyphal-mediated transport for root active transport, and under adequate Pi, convert surplus P into an inositol pyrophosphate (IP 7 ) signaling pool, thereby improving phosphorus-use efficiency. These findings reveal conserved N–P regulatory mechanisms in a woody model under controlled conditions and may provide mechanistic insights relevant to improving nutrient management in plantation forestry and tree cultivation. • NO 3 − reshapes root architecture: Promotes lateral roots for P capture in low-Pi; drives main root elongation in high-Pi. • 2.Phosphate availability switches P strategies: Low-Pi activates PHL5-HHO2 emergency uptake; high-Pi suppresses turnover for homeostasis. • 3.AM symbiosis rewires energy use: Hyphal P uptake replaces root PHT1 under low-Pi; excess P converted to IP 7 signals under high-P. • 4.HHO2 coordinates P homeostasis: Directly upregulates PHT1 transporters and fine-tunes inositol phosphate metabolism.