Integrated Transcriptomic and Metabolomic Analyses Reveal Trade-Off Mechanisms Underlying Phosphorus Acquisition Strategies in Soybean Roots

Under phosphorus (P) deficiency, soybean ( Glycine max ) adapts by modifying root architecture, increasing the release of organic exudates, enhancing arbuscular mycorrhizal (AM) colonization, and reshaping rhizosphere microbial communities; however, how these strategies trade off across a phosphorus gradient remains unclear. In this study, we integrated transcriptomic and metabolomic analyses to examine five soybean cultivars under soil P supplies of 0 mg P kg⁻¹ (severe deficiency, P0), 30 mg P kg⁻¹ (moderate deficiency, P30), 60 mg P kg⁻¹ (mild deficiency, P60), 90 mg P kg⁻¹ (adequate), and 120 mg P kg⁻¹ (excess). Our results indicate that the gradient of plant-available P drives dynamic switching among soybean P-acquisition strategies. Under moderately low P, soybean upregulated PPDK , accC , and FabI , which is consistent with a shift in carbon use that could support arbuscular mycorrhizal fungi, and AMF colonization increased by 30–50%. Under severe deficiency P, soybean primarily relied on root-driven strategies: pckA , MDH , aceB , and CS (genes associated with the PEPC shunt) were upregulated, the concentration of low-molecular-weight organic acids increased by 17– to 24–fold, and fine-root length increased by approximately 35%, thereby optimizing root system architecture. Cultivars differed in their adaptive preferences: AM-dependent types were better suited to temperate soils with moderate P limitation, whereas fine-rooted cultivars were advantageous in tropical and subtropical soils with severe P depletion. Overall, our findings reveal the regulatory networks underlying soybean P-acquisition strategies and highlight their breeding and management significance. This study provides a foundation for developing P-efficient soybean cultivars and for precision P management in sustainable agriculture.