Abstract
Inorganic phosphorus (Pi) deficiency significantly impacts plant growth, development, and photosynthetic efficiency. This study evaluated 206 rice accessions from a MiniCore population under both Pi-sufficient (Pi+) and Pi-starvation (Pi-) conditions in the field to assess photosynthetic phosphorus use efficiency (PPUE), defined as the ratio of AsatPi- to AsatPi+. A genome-wide association study and differential gene expression analyses identified an acid phosphatase gene (ACP2) that responds strongly to phosphate availability. Overexpression and knockout of ACP2 led to a 67% increase and 32% decrease in PPUE, respectively, compared with wild type. Introduction of an elite allele A, by substituting the v5 SNP G with A, resulted in an 18% increase in PPUE in gene-edited ACP2 rice lines. The phosphate-responsive gene PHR2 was found to transcriptionally activate ACP2 in parallel with PHR2 overexpression, resulting in an 11% increase in PPUE. Biochemical assays indicated that ACP2 primarily catalyzes the hydrolysis of phosphoethanolamine and phospho-L-serine. In addition, serine levels increased significantly in the ACP2v8G-overexpression line, along with a concomitant decrease in the expression of all nine genes involved in the photorespiratory pathway. Application of serine enhanced PPUE and reduced photorespiration rates in ACP2 mutants under Pi-starvation conditions. We deduce that ACP2 plays a crucial role in promoting photosynthesis adaptation to Pi starvation by regulating serine metabolism in rice.