Phylogeny, tissue-specific expression, and activities of root-secreted purple acid phosphatases for P uptake from ATP in P starved poplar

Plants secrete purple acid phosphatases (PAPs) under phosphorus (P) shortage but the contribution of plant PAPs to P acquisition is not well understood. The goals of this study were to investigate comprehensively the transcription patterns of PAPs under P shortage in poplar (Populus × canescens), to identify secreted PAPs and to characterize their contribution to mobilize organic P. Phylogenetic analyses of the PAP family revealed 33 putative members. In this study, distinct, tissue-specific P responsive expression patterns could be shown for 23 PAPs in roots and leaves. Root-associated PAP activities were localized on the root surface by in-vivo staining. The activities of root-surface PAPs increased significantly under low P availability, but were suppressed by a PAP inhibitor and corresponded to elevated P uptake from ATP as an organic P source. By proteomic analyses of the root apoplast, we identified three newly secreted proteins under P shortage: PtPAP1 (Potri.005G233400) and two proteins with unknown functions (Potri.013G100800 and Potri.001G209300). Our results, based on the combination of transcriptome and proteome analyses with phosphatase activity assays, support that PtPAP1 plays a central role in enhanced P acquisition from organic sources, when the phosphate concentrations in soil are limited.