Phosphorus limitation enhances plant growth and arsenic accumulation in As-hyperaccumulator Pteris vittata: insights from insoluble calcium phytate and phosphate rock

Phosphorus (P) is an essential macronutrient for plant growth, but its availability in soil is often insufficient to achieve optimum crop yield. The As-hyperaccumulator Pteris vittata thrives under low-P condition, with the underlying mechanisms remaining unclear. To understand the P-scavenging traits of P. vittata, we grew P vittata under three P-limiting conditions, low soluble-P, calcium phytate (insoluble organic P), and phosphate rock (PR; insoluble inorganic P), to quantify plant growth, As and P uptake, root exudates, and the gene expression of P transporters. Plants were grown under hydroponics with 50 ​μM As and 20 ​μM soluble-P, 2000 ​μM phytate-P, or 2000 ​μM PR-P, with 200 ​μM soluble-P as a sufficient P control. P. vittata efficiently acquired P when growing under all three low-P sources, with 76–85% greater P in its biomass compared to the sufficient P control. To acquire P from insoluble source, P. vittata secreted 1.7−2.9 fold more organic acids, including malic acid, succinic acid, oxalic acid, and phytic acid as root exudates under phytate and PR treatments. Further, P. vittata increased phytase activity to hydrolyze phytate, showing 6.5- and 3.3-fold greater phytase activity in P. vittata roots and root exudates under phytate treatment. Besides, the frond As content rose by 275–384% when growing under three low-P conditions, possibly attributing to 1.2−5.6 fold upregulation of P-transporters PvPht1;3/1;4 in P. vittata roots. Overall, this study suggests that the effective P and As accumulation by P. vittata under P-limiting conditions is associated with its increased root exudation of organic acids and phytase, and the upregulation of its P-transporters. These findings help to enhance the effectiveness of P. vittata in phytoremediation of As-contaminated soil and improve soil P utilization by crop plants.