Comparative Analysis of PvPAP Gene Family and Their Functions in Response to Phosphorus Deficiency in Common Bean

Abstract

BackgroundPurple acid phosphatases (PAPs) play a vital role in adaptive strategies of plants to phosphorus (P) deficiency. However, their functions in relation to P efficiency are fragmentary in common bean.Principal FindingsFive PvPAPs were isolated and sequenced in common bean. Phylogenetic analysis showed that PvPAPs could be classified into two groups, including a small group with low molecular mass, and a large group with high molecular mass. Among them, PvPAP3, PvPAP4 and PvPAP5 belong to the small group, while the other two belong to the large group. Transient expression of 35S:PvPAPs-GFP on onion epidermal cells verified the variations of subcellular localization among PvPAPs, suggesting functional diversities of PvPAPs in common bean. Quantitative PCR results showed that most PvPAPs were up-regulated by phosphate (Pi) starvation. Among them, the expression of the small group PvPAPs responded more to Pi starvation, especially in the roots of G19833, the P-efficient genotype. However, only overexpressing PvPAP1 and PvPAP3 could result in significantly increased utilization of extracellular dNTPs in the transgenic bean hairy roots. Furthermore, overexpressing PvPAP3 in Arabidopsis enhanced both plant growth and total P content when dNTPs were supplied as the sole external P source.ConclusionsThe results suggest that PvPAPs in bean varied in protein structure, response to P deficiency and subcellular localization. Among them, both PvPAP1 and PvPAP3 might function as utilization of extracellular dNTPs.

Molecular characterization of a tomato purple acid phosphatase during seed germination and seedling growth under phosphate stress

“…Purple acid phosphatases (PAPs) form a unique group among the APases, characterized by the purple color of the purified protein in aqueous solution and an iron (III)-containing dimetal center in the catalytic site (Olczak et al 2003;Strater et al 1995). PAPs have been found in, and characterized from, many plant species, including Arabidopsis, rice, tobacco, sweet potato, kidney bean and soybean, as well as other crop plants (Dionisio et al 2011;Durmus et al 1999;Hur et al 2007;Kaida et al 2003;Li et al 2002;Liang et al 2012;Liang 1998;Schenk et al 1999). PAPs contain five conserved amino acid motifs required for metal binding: DXG/GDXXY/GNH[D/E]/VXXH/ GHXH (bold letters represent the metal-binding residues) (Li et al 2002;Schenk et al 2000;Strater et al 1995).…”

Lectin AtGAL1 interacts with high‐mannose glycoform of the purple acid phosphatase AtPAP26 secreted by phosphate‐starved Arabidopsis

“…Thus, AtPAP26 has become an attractive candidate for biotechnological strategies aimed at improving crop Pi acquisition from the abundant organic‐P sources prevalent in agricultural soils. Indeed, overexpression of AtPAP26, or its closest orthologue from other dicot or monocot species (i.e., rice, stylo, and common bean) has been reported to improve biomass and Pi accumulation of −Pi plants (Gao et al, ; Liang et al, ; Liu et al, ; Wang et al, ). It will be of considerable interest to examine the Pi metabolism and growth characteristics of combined AtGAL1 and AtPAP26 overexpressors during their cultivation on unfertilized soils and/or with various Pi‐monoesters as their sole source of exogenous P.…”

“…In contrast to the abundance of plant PAP genomic and transcriptomic data, comparatively little information is available on the identity and detailed biochemical characteristics of specific PAP isozymes that mediate intracellular versus extracellular Pi scavenging and remobilization. However, integrated biochemical and functional genomic studies have established the Arabidopsis PAP AtPAP26 (and its orthologue from rice, common bean, and stylo): (a) as a principal contributor to intracellular and extracellular PSI APase activity and (b) to play a central role in Pi‐scavenging and recycling during Pi deprivation or leaf senescence (Gao, Lu, Qiu, Wang, & Shou, ; Hurley et al, ; Liang, Sun, Yao, Liao, & Tian, ; Liu, Xue, Chen, Liu, & Tian, ; Robinson, Carson, Ying, Ellis, & Plaxton, ; Robinson, Park, et al, ; Shane, Stigter, Fedosejevs, & Plaxton, ; Tran et al, ; Veljanovski, Vanderbeld, Knowles, Snedden, & Plaxton, ; Wang & Liu, ; Wang et al, ). Native enzyme purification and characterization led to the discovery that AtPAP26 is secreted as a pair of distinct glycoforms (AtPAP26‐S1 and AtPAP26‐S2) by −Pi Arabidopsis (Del Vecchio et al, ; Ghahremani et al, ; Tran, Qian, et al, ).…”

A purple acid phosphatase plays a role in nodule formation and nitrogen fixation in Astragalus sinicus

“…In Arabidopsis, among the 29 PAPs, the members induced or up-regulated by LP treatment are related to Pi acquisition (Hurley et al 2010;Robinson et al 2012). Several PAPs have been reported in legumes (Liang et al 2012;Olczak and Olczak 2002) including 35 PAP genes in soybean (Li et al 2012), 23 of which were induced under LP condition, indicating that they could play roles in Pi acquisition and assimilation. However, the constitutive expression of four PAP genes (including the AsPPD1 homolog Gmpap17) and Slides with no primary antibodies added were used as the control.…”

“…Most known PAPs, such as PPD1 from L. luteus, are secreted proteins (Olczak et al 2003), although mitochondrial (Liao et al 2003), cytosolic (Liang et al 2012), cellmembrane-bound (Liang et al 2012), and dual-targeted variants have been reported for PAPs. We have demonstrated that AsPPD1 localized to the plasma membrane in hairy root cells and to symbiosome membranes in infected nodule cells.…”