Photosynthetic Physiological, Phosphorus-Biochemical and Integrated Transcriptomic–Metabolomic Analyses Uncover the Function of GmPHF1 Overexpression in Soybean Tolerance to Low Phosphate Stress

Phosphorus is an essential macronutrient for the growth and development of soybeans. PHF1, an endoplasmic reticulum-localized SEC12-like protein mediating intracellular trafficking of phosphate transporters, plays a crucial role in plant responses to low-phosphorus stress. In this study, we analyzed the changes in photosynthetic physiology, transcriptome, and metabolome of soybean plants overexpressing GmPHF1 under low-phosphorus stress conditions. Compared with wild-type plants under low-phosphorus stress conditions, GmPHF1-overexpressing plants exhibited higher photosynthetic capacity, phosphorus content, and acid phosphatase activity. Transcriptome and metabolome analyses revealed that GmPHF1-overexpressing plants exhibited greater numbers of differentially expressed genes (DEGs) and differentially accumulated metabolites (DAMs) involved in low-phosphorus response. Overexpression of GmPHF1 significantly upregulated key DEGs involved in amino acid and phosphorus transport/metabolic pathways under low-phosphorus stress, and also increased the consumption of amino acid and lipid metabolites, which helped sustain soybean growth under phosphorus-limited conditions. Weighted gene co-expression network analysis (WGCNA) indicated that genes involved in the phosphate transport pathway were significantly upregulated in GmPHF1-overexpressing plants, which may explain the marked increases in phosphorus content and acid phosphatase activity under low-phosphorus stress. Collectively, our findings indicate that GmPHF1 overexpression may confer improved low-phosphorus tolerance in soybean, which is linked to preserved photosynthetic efficiency, elevated leaf phosphorus concentration and acid phosphatase activity, as well as modulated transcript and metabolic profiles associated with phosphate transport, amino acid turnover and phosphorus homeostasis.