The Dual-Targeted Purple Acid Phosphatase Isozyme AtPAP26 Is Essential for Efficient Acclimation of Arabidopsis to Nutritional Phosphate Deprivation      

Abstract

Induction of intracellular and secreted acid phosphatases (APases) is a widespread response of orthophosphate (Pi)-starved (2Pi) plants. APases catalyze Pi hydrolysis from a broad range of phosphomonoesters at an acidic pH. The largest class of nonspecific plant APases is comprised of the purple APases (PAPs). Although the biochemical properties, subcellular location, and expression of several plant PAPs have been described, their physiological functions have not been fully resolved. Recent biochemical studies indicated that AtPAP26, one of 29 PAPs encoded by the Arabidopsis (Arabidopsis thaliana) genome, is the predominant intracellular APase, as well as a major secreted APase isozyme up-regulated by 2Pi Arabidopsis. An atpap26 T-DNA insertion mutant lacking AtPAP26 transcripts and 55-kD immunoreactive AtPAP26 polypeptides exhibited: (1) 9-and 5-fold lower shoot and root APase activity, respectively, which did not change in response to Pi starvation, (2) a 40% decrease in secreted APase activity during Pi deprivation, (3) 35% and 50% reductions in free and total Pi concentration, respectively, as well as 5-fold higher anthocyanin levels in shoots of soil-grown 2Pi plants, and (4) impaired shoot and root development when subjected to Pi deficiency. By contrast, no deleterious influence of AtPAP26 loss of function occurred under Pi-replete conditions, or during nitrogen or potassium-limited growth, or oxidative stress. Transient expression of AtPAP26-mCherry in Arabidopsis suspension cells verified that AtPAP26 is targeted to the cell vacuole. Our results confirm that AtPAP26 is a principal contributor to Pi stress-inducible APase activity, and that it plays an important role in the Pi metabolism of 2Pi Arabidopsis.Orthophosphate (Pi) is an essential plant macronutrient required for many pivotal metabolic processes such as photosynthesis and respiration. However, the massive use of Pi fertilizers in agriculture demonstrates how the free Pi level of many soils is suboptimal for plant growth. The world's reserves of rock phosphate, our major source of Pi fertilizers, are projected to be depleted by the end of this century (Vance et al., 2003). Furthermore, Pi runoff from fertilized fields into nearby surface waters results in environmentally destructive processes such as aquatic eutrophication and blooms of toxic cyanobacteria. Effective biotechnological strategies are needed to engineer Pi-efficient transgenic crops to ensure agricultural sustainability and a reduction in Pi fertilizer overuse. This necessitates a detailed understanding of Pi-starvation-inducible (PSI) gene expression and the complex morphological, physiological, and biochemical adaptations of Pi-deficient (2Pi) plants.A well-documented component of the plant Pi stress response is the up-regulation of intracellular and secreted acid phosphatases (APases; E.C. 3.1.3.2) that catalyze the hydrolysis of Pi from various phosphate monoesters and anhydrides in the acidic pH range (Tran et al., 2010a). APase induction by 2Pi plants has been correlated wit...

Metabolic Adaptations of Phosphate-Starved Plants

“…Recent biochemical and functional genomic studies have established the dual-targeted AtPAP26 as the predominant intracellular (vacuolar) APase, as well as a major secreted APase isozyme up-regulated by 2Pi Arabidopsis (Veljanovski et al, 2006;Hurley et al, 2010;Tran et al, 2010b). Transient expression of an AtPAP26-GFP fusion construct coupled with imaging via epifuorescence microscopy confirmed AtPAP26's vacuolar localization (Hurley et al, 2010).…”

Phosphorus Dynamics: From Soil to Plant

“…Releasing Pi from organic sources, such as phosphomonoesters and nucleic acids, is also an important step for internal P-recycling processes. Phosphatases are needed to release Pi from phosphomonoesters, and a dual-targeted purple acid phosphatase isozyme AtPAP26 (intracellular and secreted APase) is essential for efficient acclimation of Arabidopsis to P deprivation (Hurley et al, 2010). Ribonucleases are responsible for P mobilization from RNA, and two genes (AtRNS1 and AtRNS2) are up-regulated by P starvation (Bariola et al, 1999).…”

The THO/TREX Complex Active in miRNA Biogenesis Negatively Regulates Root-Associated Acid Phosphatase Activity Induced by Phosphate Starvation

“…Induction and secretion of acid phosphatases (APase) is a universal response of plants to Pi starvation and is regarded as an important way by which plants scavenge Pi from external organophosphates (Tran et al, 2010a). Indeed, knockout or overexpression of some APase genes significantly affects plant utilization of external organic P (Hurley et al, 2010;Robinson et al, 2012;Wang et al, 2009Wang et al, , 2011Wang et al, , 2014.…”