PoSPX1 enhances phosphorus deficiency tolerance by improving root growth in tree peony (Paeonia ostii ‘Fengdan’) with dual medicinal and ornamental value

• PoSPX1 promotes root elongation and anthocyanin accumulation in tree peony under phosphate deficiency. • The organic phosphate transporter PoGlpT is strongly induced by Pi starvation in tree peony roots. • Overexpression of PoSPX1 enhances low-phosphorus tolerance in Arabidopsis by improving root and shoot growth. • These findings may offer preliminary genetic clues for improving phosphorus efficiency in tree peony cultivation. Tree peony ( Paeonia ostii ‘Fengdan’) is an economically important medicinal plant. The bark of its root, which is commonly known as Danpi, is rich in bioactive compounds. Phosphorus is essential for plant growth, and its availability can constrain plant development and metabolism. In this study, we examined the phenotypic, physiological, and molecular responses of ‘Fengdan’ seedlings to a gradient of phosphate (Pi) concentrations: deficiency (P0, 0 mM), sufficiency (P1, 1.25 mM), and high (P2, 2.00 mM). Pi deficiency reduced leaf area and root biomass initially, followed by a significant increase in both total and lateral root lengths and an elevated leaf anthocyanin content at a later stage. Transcriptomic analysis revealed numerous differentially expressed genes (DEGs) associated with Pi starvation response, transport, and metabolism. Five key candidate genes, PoSPX1, PoPHT1;7, PoPAP8, PoPAP22 , and PoGlpT were identified and their expression patterns were validated. PoSPX1 showed the highest overall responsiveness. PoGlpT , an organic phosphorus transporter poorly characterized in plants, was also highly responsive to Pi starvation. Notably, overexpression of PoSPX1 in Arabidopsis promoted root and shoot growth and stimulated anthocyanin accumulation under low-Pi conditions. These results suggest the adaptive mechanisms to phosphate deficiency in tree peony and indicate that PoSPX1 may play an important regulatory role. It may also provide insights for optimizing phosphorus fertilization strategies to improve Danpi yield and quality.