OsPAP10c, a novel secreted acid phosphatase in rice, plays an important role in the utilization of external organic phosphorus

Abstract

Under phosphate (Pi ) starvation, plants increase the secretion of purple acid phosphatases (PAPs) into the rhizosphere to scavenge organic phosphorus (P) for plant use. To date, only a few members of the PAP family have been characterized in crops. In this study, we identified a novel secreted PAP in rice, OsPAP10c, and investigated its role in the utilization of external organic P. OsPAP10c belongs to a monocotyledon-specific subclass of Ia group PAPs and is specifically expressed in the epidermis/exodermis cell layers of roots. Both the transcript and protein levels of OsPAP10c are strongly induced by Pi starvation. OsPAP10c overexpression increased acid phosphatase (APase) activity by more than 10-fold in the culture media and almost fivefold in both roots and leaves under Pi -sufficient and Pi -deficient conditions. This increase in APase activity further improved the plant utilization efficiency of external organic P. Moreover, several APase isoforms corresponding to OsPAP10c were identified using in-gel activity assays. Under field conditions with three different Pi supply levels, OsPAP10c-overexpressing plants had significantly higher tiller numbers and shorter plant heights. This study indicates that OsPAP10c encodes a novel secreted APase that plays an important role in the utilization of external organic P in rice.

The effects of diversified phosphorus nutrition on the growth of oat (Avena sativa L.) and acid phosphatase activity

“…In rice, several APase isoforms corresponding to OsPAP10c, rice novel secreted purple APase, were identified using in-gel activity assays [33]. OsPAP10c overexpression increased the accumulation of four APase isoforms in transgenic rice plants; in addition, the results suggested that OsPAP10c could form different homo-or heteromeric protein complexes [33].…”

“…Activity of AtPAP10, a major Pi starvation-induced APase associated with the root surface in Arabidopsis is probably regulated both through local and systemic signaling under Pi starvation [24]. In a recent study, Lu et al [33] identified a novel secreted purple APase in rice (OsPAP10c) and investigated its role in organic P utilization -OsPAP10c overexpression significantly increased APase activity both in leaves and roots, but especially on the root surface and in culture media. Studies by Wang et al [47] indicated that the quantity of rhizosphere APase had positive correlations with P fractions available to plants and Pi uptake by the plants in low-Pi soils; these authors also stated that both Brassica napus and Avena sativa were good candidates to study P utilization.…”

“…One of Pi starvation-inducible APase isoforms was characterized as AtACP5/AtPAP17 around 34 kDa monomeric protein, in addition the strong expression of BnPAP17-2 and BnPAP17-3 was detected in vascular tissues suggesting their roles in Pi absorption and transport [50]. In rice, several APase isoforms corresponding to OsPAP10c, rice novel secreted purple APase, were identified using in-gel activity assays [33]. OsPAP10c overexpression increased the accumulation of four APase isoforms in transgenic rice plants; in addition, the results suggested that OsPAP10c could form different homo-or heteromeric protein complexes [33].…”

“…Intracellular acid phosphatases are believed to be involved in Pi remobilization from senescing organs, storage tissues, older leaves, or intracellular compartments (mainly vacuoles) to young tissues, especially under Pi deficiency conditions [29,31]. Secreted APases have been purified and well characterized in model plants, such as Arabidopsis, lupin, tobacco, or rice [21,[32][33][34] and most of the results indicate an important role of APases during plant growth in response to Pi starvation. However, a negative correlation between the activity of root APase and Pi uptake was also observed under low P stress [28,35].…”

“…Thus, a comprehensive understanding of metabolic function of APases is difficult, partly due to their heterogeneity, large number, as well as relative nonspecificity. Acid phosphatases (especially purple acid phosphatases) and phytases have been recently intensively studied due to their usefulness for Pi-efficient crop engineering [24,31,33]. Transgenic plants expressing microbial or plant-derived APase genes (or phytase) often show higher enzyme activity and improved plant growth under low Pi nutrition [26,31,36].…”