Orthophosphate (Pi) is an essential but limiting macronutrient for plant growth. Extensive soil P reserves exist in the form of organic P (Po), which is unavailable for root uptake until hydrolysed by secretory acid phosphatases (APases). The predominant purple APase (PAP) isozymes secreted by roots of Pi-deficient (–Pi) Arabidopsis thaliana were recently identified as AtPAP12 (At2g27190) and AtPAP26 (At5g34850). The present study demonstrated that exogenous Po compounds such as glycerol-3-phosphate or herring sperm DNA: (i) effectively substituted for Pi 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 –Pi conditions or supplied with Po 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 Pi concentration, respectively. Development of the atpap12/atpap26 mutant was unaffected during growth on Pi-replete medium but was completely arrested when 7-day-old Pi-sufficient seedlings were transplanted into a –Pi, Po-containing soil mix. Both PAPs were also strongly upregulated on root surfaces and in shoot cell-wall extracts of –Pi 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 Pi from the soil’s accessible Po pool, while (ii) recycling Pi 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.

SummaryLimitation of crop productivity by suboptimal phosphorus (P) nutrition is a widespread concern. Enhanced crop P-use efficiency could be achieved by improving P remobilization from senescing leaves to developing tissues and seeds. Transcriptomic studies indicate that hundreds of Arabidopsis thaliana genes are up-regulated during leaf senescence, including that encoding the purple acid phosphatase (PAP) AtPAP26 (At5g34850).In this study, biochemical and functional genomic tools were integrated to test the hypothesis that AtPAP26 participates in P remobilization during leaf senescence.An eightfold increase in acid phosphatase activity of senescing leaves was correlated with the accumulation of AtPAP26 transcripts and immunoreactive AtPAP26 polypeptides. Senescing leaves of an atpap26 T-DNA insertion mutant displayed a > 90% decrease in acid phosphatase activity, markedly impaired P remobilization efficiency and delayed senescence. This was paralleled by reduced seed total P concentrations and germination rates.These results demonstrate that AtPAP26 loss of function causes dramatic effects that cannot be compensated for by any other PAP isozyme, even though Arabidopsis contains 29 different PAP genes. Our current and earlier studies establish that AtPAP26 not only helps to scavenge P from organic P sources when Arabidopsis is cultivated in inorganic orthophosphate (Pi)-deficient soils, but also has an important P remobilization function during leaf senescence.