Proton-driven sucrose symport and antiport are provided by the vacuolar transporters SUC4 and TMT1/2

Authors

  • Alexander Schulz,

    1. University of Wuerzburg, Institute for Molecular Plant Physiology and Biophysics, Julius von Sachs Platz 2, D-97082 Wuerzburg, Germany
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  • Diana Beyhl,

    1. University of Wuerzburg, Institute for Molecular Plant Physiology and Biophysics, Julius von Sachs Platz 2, D-97082 Wuerzburg, Germany
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  • Irene Marten,

    1. University of Wuerzburg, Institute for Molecular Plant Physiology and Biophysics, Julius von Sachs Platz 2, D-97082 Wuerzburg, Germany
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  • Alexandra Wormit,

    1. University of Kaiserslautern, Plant Physiology, Erwin Schrödinger Straße, D-67653 Kaiserslautern, Germany
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  • Ekkehard Neuhaus,

    1. University of Kaiserslautern, Plant Physiology, Erwin Schrödinger Straße, D-67653 Kaiserslautern, Germany
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  • Gernot Poschet,

    1. University of Heidelberg, Heidelberg Institute for Plant Sciences, Im Neuenheimer Feld 360, D-69120 Heidelberg, Germany
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  • Michael Büttner,

    1. University of Heidelberg, Heidelberg Institute for Plant Sciences, Im Neuenheimer Feld 360, D-69120 Heidelberg, Germany
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  • Sabine Schneider,

    1. Friedrich Alexander University of Erlangen-Nürnberg, Molecular Plant Physiology, Staudtstraße 5, D-91058 Erlangen, Germany
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  • Norbert Sauer,

    Corresponding author
    1. Friedrich Alexander University of Erlangen-Nürnberg, Molecular Plant Physiology, Staudtstraße 5, D-91058 Erlangen, Germany
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  • Rainer Hedrich

    Corresponding author
    1. University of Wuerzburg, Institute for Molecular Plant Physiology and Biophysics, Julius von Sachs Platz 2, D-97082 Wuerzburg, Germany
    2. King Saud University, Riyadh, Saudi Arabia
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(fax +49 9131 85 28751; e-mail nsauer@biologie.uni-erlangen.de or fax +49 931 31-86157; e-mail hedrich@botanik.uni-wuerzburg.de).

Summary

The vacuolar membrane is involved in solute uptake into and release from the vacuole, which is the largest plant organelle. In addition to inorganic ions and metabolites, large quantities of protons and sugars are shuttled across this membrane. Current models suggest that the proton gradient across the membrane drives the accumulation and/or release of sugars. Recent studies have associated AtSUC4 with the vacuolar membrane. Some members of the SUC family are plasma membrane proton/sucrose symporters. In addition, the sugar transporters TMT1 and TMT2, which are localized to the vacuolar membrane, have been suggested to function in proton-driven glucose antiport. Here we used the patch-clamp technique to monitor carrier-mediated sucrose transport by AtSUC4 and AtTMTs in intact Arabidopsis thaliana mesophyll vacuoles. In the whole-vacuole configuration with wild-type material, cytosolic sucrose-induced proton currents were associated with a proton/sucrose antiport mechanism. To identify the related transporter on one hand, and to enable the recording of symporter-mediated currents on the other hand, we electrophysiologically characterized vacuolar proteins recognized by Arabidopsis mutants of partially impaired sugar compartmentation. To our surprise, the intrinsic sucrose/proton antiporter activity was greatly reduced when vacuoles were isolated from plants lacking the monosaccharide transporter AtTMT1/TMT2. Transient expression of AtSUC4 in this mutant background resulted in proton/sucrose symport activity. From these studies, we conclude that, in the natural environment within the Arabidopsis cell, AtSUC4 most likely catalyses proton-coupled sucrose export from the vacuole. However, TMT1/2 probably represents a proton-coupled antiporter capable of high-capacity loading of glucose and sucrose into the vacuole.

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