Identification of plant vacuolar transporters mediating phosphate storage

Abstract

Plant vacuoles serve as the primary intracellular compartments for inorganic phosphate (Pi) storage. Passage of Pi across vacuolar membranes plays a critical role in buffering the cytoplasmic Pi level against fluctuations of external Pi and metabolic activities. Here we demonstrate that the SPX-MFS proteins, designated as PHOSPHATE TRANSPORTER 5 family (PHT5), also named Vacuolar Phosphate Transporter (VPT), function as vacuolar Pi transporters. Based on 31P-magnetic resonance spectroscopy analysis, Arabidopsis pht5;1 loss-of-function mutants accumulate less Pi and exhibit a lower vacuolar-to-cytoplasmic Pi ratio than controls. Conversely, overexpression of PHT5 leads to massive Pi sequestration into vacuoles and altered regulation of Pi starvation-responsive genes. Furthermore, we show that heterologous expression of the rice homologue OsSPX-MFS1 mediates Pi influx to yeast vacuoles. Our findings show that a group of Pi transporters in vacuolar membranes regulate cytoplasmic Pi homeostasis and are required for fitness and plant growth.

Eukaryotic Phosphate Homeostasis: The Inositol Pyrophosphate Perspective

“…In A. thaliana there are three members (SPX-MSF1-3). The only characterized member is SPX-MFS1, also known as PHT5, which belongs to the class of vacuolar phosphate transporters [26]. The SPX-MFS1 loss of function mutant has low vacuolar-to-cytoplasm phosphate ratio compared to wild-type plants.…”

“…The SPX-MFS1 loss of function mutant has low vacuolar-to-cytoplasm phosphate ratio compared to wild-type plants. Conversely, SPX-MFS1 overexpression leads to misregulation of phosphate starvation-responsive genes and growth retardation as a consequence of phosphate sequestration into vacuoles [26]. The exact function of the SPX domain in this protein is not fully known.…”

Vacuolar SPX-MFS transporters are essential for phosphate adaptation in plants

“…3 Complementary to our results, 31 P-magnetic resonance spectroscopy analysis revealed that loss-of-function of vpt1 mutants accumulated less Pi and exhibited a lower vacuolar-to-cytoplasmic Pi ratio than the wild types. 4 Taken together, these results indicate that the members of SPX-MFS family are the candidate transporters conducting Pi across the tonoplast.…”

“…During most phases of plant development, Pi concentration is much higher in the vacuole than in the cytosol, indicating that the vacuole has transport proteins responsible for the transport of Pi across tonoplast. 2 Recently, we, 3 Liu et al, 4 and Wang et al 5 independently revealed that SPX-MFS family potentially might function as a new group of vacuolar Pi transporters in plants. SPX-MFS proteins contain an evolutionally conserved SPX domain [named after yeast Syg1 and Pho81 and human xenotropic and polytropic retrovirus receptor 1 (XPR1)] with an MFS (Major Facilitator Superfamily) domain.…”

“…4 The observations in rice and Arabidopsis conclude that SPX-MFS family is localized in the tonoplast in plants.…”