GWAS unravels acid phosphatase ACP2 as a photosynthesis regulator under phosphate starvation conditions through modulating serine metabolism in rice.

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 A_sat^Pi- to A_sat^Pi+. 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 ACP2^v8G-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.