The secreted purple acid phosphatase isozymes AtPAP12 and AtPAP26 play a pivotal role in extracellular phosphate-scavenging by Arabidopsis thaliana

Orthophosphate (P(i)) is an essential but limiting macronutrient for plant growth. Extensive soil P reserves exist in the form of organic P (P(o)), which is unavailable for root uptake until hydrolysed by secretory acid phosphatases (APases). The predominant purple APase (PAP) isozymes secreted by roots of P(i)-deficient (–P(i)) Arabidopsis thaliana were recently identified as AtPAP12 (At2g27190) and AtPAP26 (At5g34850). The present study demonstrated that exogenous P(o) compounds such as glycerol-3-phosphate or herring sperm DNA: (i) effectively substituted for P(i) in supporting the P nutrition of Arabidopsis seedlings, and (ii) caused upregulation and secretion of AtPAP12 and AtPAP26 into the growth medium. When cultivated under –P(i) conditions or supplied with P(o) as its sole source of P nutrition, an atpap26/atpap12 T-DNA double insertion mutant exhibited impaired growth coupled with >60 and >30% decreases in root secretory APase activity and rosette total P(i) concentration, respectively. Development of the atpap12/atpap26 mutant was unaffected during growth on P(i)-replete medium but was completely arrested when 7-day-old P(i)-sufficient seedlings were transplanted into a –P(i), P(o)-containing soil mix. Both PAPs were also strongly upregulated on root surfaces and in shoot cell-wall extracts of –P(i) seedlings. It is hypothesized that secreted AtPAP12 and AtPAP26 facilitate the acclimation of Arabidopsis to nutritional Pi deficiency by: (i) functioning in the rhizosphere to scavenge P(i) from the soil’s accessible P(o) pool, while (ii) recycling P(i) from endogenous phosphomonoesters that have been leaked into cell walls from the cytoplasm. Thus, AtPAP12 and AtPAP26 are promising targets for improving crop P-use efficiency.