ABSTRACT
Phosphorus is indispensable in agricultural production. An increasing food supply requires more efficient use of phosphate due to limited phosphate resources. However, how crops regulate phosphate efficiency remains largely unknown. Here, we identified a major quantitative trait locus, qPE19, that controls 7 low-phosphate (LP)-related traits in soybean (Glycine max) through linkage mapping and genome-wide association studies. We identified the gene responsible for qPE19 as GLYCEROPHOSPHORYL DIESTER PHOSPHODIESTERASE2 (GmGDPD2), and haplotype 5 represents the optimal allele favoring LP tolerance. Overexpression of GmGDPD2 significantly affects hormone signaling and improves root architecture, phosphate efficiency and yield-related traits; conversely, CRISPR/Cas9-edited plants show decreases in these traits. GmMyb73 negatively regulates GmGDPD2 by directly binding to its promoter; thus, GmMyb73 negatively regulates LP tolerance. GmGDPD2 physically interacts with GA 2-oxidase 1 (GmGA2ox1) in the plasma membrane, and overexpressing GmGA2ox1 enhances LP-associated traits, similar to GmGDPD2 overexpression. Analysis of double mutants for GmGDPD2 and GmGA2ox1 demonstrated that GmGDPD2 regulates LP tolerance likely by influencing auxin and gibberellin dose-associated cell division in the root. These results reveal a regulatory module that plays a major role in regulating LP tolerance in soybeans and is expected to be utilized to develop phosphate-efficient varieties to enhance soybean production, particularly in phosphate-deficient soils.