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.
Highlights
Plant vacuoles serve as the primary intracellular compartments for inorganic phosphate (Pi) storage
When external Pi is in scarce supply, the level of cytoplasmic Pi is kept relatively constant at the expense of vacuolar Pi, whereas when Pi is resupplied to Pi-starved plants, rapid and massive Pi uptake to the plasma membrane is accompanied by the efficient sequestration of Pi inside the vacuole[17,18]
Despite the critical role of vacuolar Pi (vac-Pi) in buffering the cytoplasmic Pi (cyt-Pi) against fluctuations caused by variable Pi availability and metabolic activities, the molecular identity of the vac-Pi transporter as well as the regulatory mechanism by which Pi is translocated across vacuolar membranes remain elusive
Summary
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. Our findings show that a group of Pi transporters in vacuolar membranes regulate cytoplasmic Pi homeostasis and are required for fitness and plant growth. When external Pi is in scarce supply, the level of cytoplasmic Pi (cyt-Pi; the sum of Pi in the cytosol and the non-vacuole organelles) is kept relatively constant at the expense of vacuolar Pi (vac-Pi) (refs 15,16), whereas when Pi is resupplied to Pi-starved plants, rapid and massive Pi uptake to the plasma membrane is accompanied by the efficient sequestration of Pi inside the vacuole[17,18]. We envisaged that the plant SPX-MFS family potentially functions as a new group of Pi transporters in plants
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