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

Inorganic phosphorus (Pi) deficiency significantly impacts plant growth, development and photosynthetic efficiency (Asat). 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 (GWAS) and differential gene expression analyses identified an acid phosphatase (ACP2) gene that responds strongly to phosphate availability. Overexpress and knock out ACP2 led to 67% increase and 32% decrease in PPUE, respectively, compared to WT. Introduction of an elite allele A, by substituting v5 SNP from G to A, resulted in 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 11% increase in PPUE. Biochemical assays indicated that ACP2 primarily catalyzes the hydrolysis of phosphoethanolamine and phospho-L-serine. Additionally, serine levels were found to increase significantly in ACP2v8G OE line, along with a concomitant decrease in the expression of all nine genes involved in the photorespiratory pathway. Application of serine was shown to enhance PPUE and reduce photorespiration rates (PR) in ACP2 mutant under Pi-starvation conditions. In deduction, ACP2 plays a crucial role in promoting photosynthesis adaptation to Pi starvation by regulating serine metabolism in rice.