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ENVIRONMENTAL STRESS AND ADAPTATION

Characterization of Anion Channels in the Plasma Membrane of Arabidopsis Epidermal Root Cells and the Identification of a Citrate-Permeable Channel Induced by Phosphate Starvation¹

Department of Biological Sciences, Lancaster Environment Centre, Lancaster University, Lancaster LA1 4YQ, United Kingdom (E.D., M.R., S.K.R.); and Biology Department, University of York, York YO10 5YW, United Kingdom (D.S.)

Organic-acid secretion from higher plant roots into the rhizosphere plays an important role in nutrient acquisition and metal detoxification. In this study we report the electrophysiological characterization of anion channels in Arabidopsis (Arabidopsis thaliana) root epidermal cells and show that anion channels represent a pathway for citrate efflux to the soil solution. Plants were grown in nutrient-replete conditions and the patch clamp technique was applied to protoplasts isolated from the root epidermal cells of the elongation zone and young root hairs. Using SO₄^2– as the dominant anion in the pipette, voltage-dependent whole-cell inward currents were activated at membrane potentials positive of –180 mV exhibiting a maximum peak inward current (I_peak) at approximately –130 mV. These currents reversed at potentials close to the equilibrium potential for SO₄^2–, indicating that the inward currents represented SO₄^2– efflux. Replacing intracellular SO₄^2– with Cl^– or NO₃^– resulted in inward currents exhibiting similar properties to the SO₄^2– efflux currents, suggesting that these channels were also permeable to a range of inorganic anions; however when intracellular SO₄^2– was replaced with citrate or malate, no inward currents were ever observed. Outside-out patches were used to characterize a 12.4-picoSiemens channel responsible for these whole-cell currents. Citrate efflux from Arabidopsis roots is induced by phosphate starvation. Thus, we investigated anion channel activity from root epidermal protoplasts isolated from Arabidopsis plants deprived of phosphate for up to 7 d after being grown for 10 d on phosphate-replete media (1.25 mM). In contrast to phosphate-replete plants, protoplasts from phosphate-starved roots exhibited depolarization-activated voltage-dependent citrate and malate efflux currents. Furthermore, phosphate starvation did not regulate inorganic anion efflux, suggesting that citrate efflux is probably mediated by novel anion channel activity, which could have a role in phosphate acquisition.