Low-phosphorus stress induces GmSTOP1-3-mediated organic acid exudation to recruit phosphate-solubilizing bacteria for organic phosphorus mineralization in soybean rhizosphere

Root exudates serve a vital function in recruiting beneficial phosphate-solubilizing bacteria (PSB), thereby enhancing plant adaptation to phosphorus (P) deficiency. The C2H2-type zinc finger transcription factor STOP1 (sensitive to proton rhizotoxicity 1) regulates root organic acid (OA) exudation in plants. However, the impact of STOP1-regulated root OA exudation on rhizosphere microbial composition remains unexplored. This study revealed enhanced vegetation properties of soybean with higher P content in P-rich soils, while rhizosphere organic acid concentrations were elevated in P-poor soils. The soybean genotype YC03-3 in P-deficient soils specifically recruited three PSB in acid soils: Gammaproteobacteria_Incertae_Sedis, KF_JG30_C25, and Solirubrobacterales. These PSB abundances correlated positively with rhizosphere oxalate and citrate concentrations. Under P-sufficient conditions, GmSTOP1-3 overexpression in soybean plants increased oxalate and citrate exudation compared to YCO3-3 wild type (WT), leading to preferential colonization by the same three PSB species naturally present in P-deficient WT rhizosphere. The population dynamics of these PSB demonstrated strong positive correlations with the abundance of key genes involved in P cycling, particularly those governing acid/alkaline phosphatase activities and organic-P mineralization. Given the phosphate starvation-enhanced expression pattern of GmSTOP1-3, the findings indicate that specific PSB recruitment for organic-P remobilization in soybean rhizosphere depends on GmSTOP1-3-mediated oxalate and citrate exudation in P-deficient acid soils. This research establishes GmSTOP1-3 as a crucial regulator of rhizosphere microbiome assembly and P-acquisition efficiency in acid soils.