Inorganic phosphate (Pi) is an essential component of all life forms. Land plants acquire Pi from the soil through roots and associated symbioses, and it is then transported throughout the plant. When sufficient, excess Pi is stored in vacuoles for remobilization following Pi deficiency. Although Pi release from the vacuoles to the cytoplasm serves as a critical mechanism for plants to adapt to low-Pi stress, the transporters responsible for vacuolar Pi efflux have not been identified. Here, we identified a pair of Oryza sativa vacuolar Pi efflux transporters (OsVPE1 and OsVPE2) that were more abundant in plants grown under Pi-deficient conditions. These OsVPE proteins can transport Pi into yeast cells and Xenopus laevis oocytes. Vacuolar Pi content was higher in the loss-of-function Osvpe1 Osvpe2 double mutant than in wild type, particularly under low-Pi stress. Overexpression of either OsVPE1 or OsVPE2 in transgenic plants reduced vacuolar Pi content, consistent with a role in vacuolar Pi efflux. We demonstrate that these VPE proteins evolved from an ancient plasma membrane glycerol-3-phosphate transporter protein. Together, these data indicate that this transporter was recruited to the vacuolar membrane to catalyse Pi efflux during the course of land plant evolution.
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The data that supports the findings of this study are available within the article and its Supplementary Information files or from the corresponding authors upon reasonable request.
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The authors thank B. Menand for valuable suggestions, J. M. Thevelein for the yeast strains, and L. Jiang and G. Miesenböck for the PEpHluorin and PRpHluorin. This work was supported by the National Key Research and Development Program of China (2017YFD0200204) and the National Natural Science Foundation (31772386, 31801924 and 31670267). K.Y. was supported by the National Program for the Support of Top-notch Young Professionals and the Innovation Program of Chinese Academy of Agricultural Sciences. L.D. is funded by a European Research Council Advanced Grant (EVO-500; contract number 25028). S.L. is funded by a grant from the National Science Foundation.
The authors declare no competing interests.
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