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.