Abstract
Fructose (Fru) is a major storage form of sugars found in vacuoles, yet the molecular regulation of vacuolar Fru transport is poorly studied. Although SWEET17 (for SUGARS WILL EVENTUALLY BE EXPORTED TRANSPORTERS17) has been characterized as a vacuolar Fru exporter in leaves, its expression in leaves is low. Here, RNA analysis and SWEET17-β-glucuronidase/-GREEN FLUORESCENT PROTEIN fusions expressed in Arabidopsis (Arabidopsis thaliana) reveal that SWEET17 is highly expressed in the cortex of roots and localizes to the tonoplast of root cells. Expression of SWEET17 in roots was inducible by Fru and darkness, treatments that activate accumulation and release of vacuolar Fru, respectively. Mutation and ectopic expression of SWEET17 led to increased and decreased root growth in the presence of Fru, respectively. Overexpression of SWEET17 specifically reduced the Fru content in leaves by 80% during cold stress. These results intimate that SWEET17 functions as a Fru-specific uniporter on the root tonoplast. Vacuoles overexpressing SWEET17 showed increased [14C]Fru uptake compared with the wild type. SWEET17-mediated Fru uptake was insensitive to ATP or treatment with NH4Cl or carbonyl cyanide m-chlorophenyl hydrazone, indicating that SWEET17 functions as an energy-independent facilitative carrier. The Arabidopsis genome contains a close paralog of SWEET17 in clade IV, SWEET16. The predominant expression of SWEET16 in root vacuoles and reduced root growth of mutants under Fru excess indicate that SWEET16 also functions as a vacuolar transporter in roots. We propose that in addition to a role in leaves, SWEET17 plays a key role in facilitating bidirectional Fru transport across the tonoplast of roots in response to metabolic demand to maintain cytosolic Fru homeostasis.
Highlights
Fructose (Fru) is a major storage form of sugars found in vacuoles, yet the molecular regulation of vacuolar Fru transport is poorly studied
A quantitative reverse transcription-PCR analysis revealed that SWEET17 mRNA was expressed to high levels in roots of 2-week-old seedlings (Fig. 1)
The expression pattern of SWEET17 proteins was consistent with the expression pattern analyzed by plants expressing the GUS reporter driven by the SWEET17 promoter (Supplemental Fig. S1C)
Summary
Fructose (Fru) is a major storage form of sugars found in vacuoles, yet the molecular regulation of vacuolar Fru transport is poorly studied. Two H+-dependent sugar antiporters, the vacuolar Glc transporter (AtVGT1; Aluri and Büttner, 2007) and AtTMT1 (Wormit et al, 2006), mediate Glc uptake across the tonoplast to promote carbohydrate accumulation in Arabidopsis (Arabidopsis thaliana). The Early Responsive to Dehydration-Like protein has been shown to export vacuolar Glc into the cytosol (Poschet et al, 2011), likely via an energy-independent diffusion mechanism (Yamada et al, 2010) Defects in these vacuolar sugar transporters alter carbohydrate partitioning and allocation and inhibit plant growth and seed yield (Aluri and Büttner, 2007; Wingenter et al, 2010; Eom et al, 2011; Poschet et al, 2011)
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