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 seven 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 root. These results reveal a regulatory module that plays a major role in regulating LP tolerance in soybean and is expected to be utilized to develop phosphate-efficient varieties to enhance soybean production, particularly in phosphate-deficient soils.

Phosphorus (P) plays a pivotal role in plant growth and development. Low P stress can greatly hamper plant growth. Here, we identified a QTL (named QPH-9-1), which is associated with P efficiency across multiple environments through linkage analysis and genome-wide association study (GWAS). Furthermore, we successfully cloned the underlying soybean (Glycine max) gene GmRR1 (a soybean type-B Response Regulator 1) that encodes a type-B response regulator protein. Knockout of GmRR1 resulted in a substantial increase in plant height, biomass, P uptake efficiency, and yield-related traits due to the modification of root structure. In contrast, overexpression of GmRR1 in plants resulted in a decrease in these phenotypes. Further analysis revealed that knockout of GmRR1 substantially increased the levels of auxin and ethylene in roots, thereby promoting root hair formation and growth by promoting the formation of root hair primordium and lengthening the root apical meristem. Yeast two-hybrid, bimolecular fluorescence complementation, and dual-luciferase assays demonstrated an interaction between GmRR1 and Histidine-containing Phosphotransmitter protein 1 (GmHP1). Expression analysis suggested that these proteins co-participated in response to low P stress. Analysis of genomic sequences showed that GmRR1 underwent a selection during soybean domestication. Taken together, this study provides further insights into how plants respond to low P stress by modifying root architecture through phytohormone pathways.

Phytocyanins (PCs), plant-specific blue copper proteins, are crucial for various biological processes during plant development. However, a comprehensive characterization of the soybean PC gene family (GmPC) is lacking. In this study, we performed genome-wide screening of soybean PC genes, and 90 PC genes were identified in the soybean genome. Further analysis revealed that the GmPC family was categorized into four subfamilies (stellacyanins, GmSCs; uclacyanins, GmUCs; plantacyanins, GmPLCs; and early nodulin-like proteins, GmENODLs). In-depth analysis revealed that each specific GmPC subfamily exhibited similar characteristics, with segmental duplications playing a major role in expanding the members of GmPC. Additionally, synteny and evolutionary constraint analyses suggested that GmPCs have undergone strong selective pressure for purification during the evolution of soybeans. The promoter cis-regulatory elements analysis of GmPCs suggested that GmPCs might play a crucial role in various stress responses. The expression patterns of GmPCs exhibited tissue-specific variations. Moreover, 23 of the GmPCs may be involved in soybean’s response to salt stress. In all, our study presents a systematic overview of GmPC, which not only provides a valuable foundation for further functional investigations of GmPCs, but also offers new insights into the mechanism of soybean salt tolerance.