Purple acid phosphatase Glyma.12G07500 (GmPAP14) mediated internal and external organic phosphorus utilization in soybean

• Glyma . 12G007500 ( GmPAP14 ) was induced in roots and leaves under organic P (Po) condition. • GmPAP14 overexpression enhanced secreted and intracellular acid phosphatase activities, leading to higher Pi concentrations in cotyledons, functional leaves and roots under Po condition. • GmPAP14 overexpression enhanced internal phosphorus (phosphatidic acid) recycling. Purple acid phosphatases (PAPs) are crucial for plant organic phosphorus (P) utilization. Here, we identified an induced PAP gene, Glyma . 12G007500 ( GmPAP14 ), through transcriptional profiling under long-term organic P (Po) condition. GmPAP14 exhibited significant upregulation across various growth stages in roots and leaves under Po condition. Functional characterization revealed that overexpression of GmPAP14 enhanced secreted and intracellular acid phosphatase activities, resulting in higher phosphate concentrations in cotyledons, functional leaves and roots under Po condition. Subsequent investigations revealed that the transgenic lines (L1 and L2) with GmPAP14 overexpression exhibited marked increase in hundred-grain weight and oil content under Po condition. Lipidomic analysis showed that the contents of phosphatidic acid and non-phosphorus galactolipids and sulfolipids were reduced. These metabolic alterations suggested that GmPAP14 overexpression enhanced internal phosphorus recycling, effectively alleviated phosphorus deficiency symptoms in soybean under Po condition. Overall, these findings demonstrated that GmPAP14 played a pivotal role in coordinating both internal and external Po utilization, providing a promising target for genetic engineering strategies to improve the phosphorus utilization efficiency in soybean.