SWEET17, a facilitative transporter, mediates fructose transport across the tonoplast of arabidopsis roots and leaves

Woei-Jiun Guo, Reka Nagy, Hsin Yi Chen, Stefanie Pfrunder, Ya Chi Yu, Diana Santelia, Wolf B. Frommer, Enrico Martinoia

Research output: Contribution to journalArticle

78 Citations (Scopus)

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.

Original languageEnglish
Pages (from-to)777-789
Number of pages13
JournalPlant Physiology
Volume164
Issue number2
DOIs
Publication statusPublished - 2014 Feb 1

Fingerprint

tonoplast
Fructose
Arabidopsis
transporters
fructose
sugars
leaves
Vacuoles
vacuoles
root growth
Carbonyl Cyanide m-Chlorophenyl Hydrazone
uptake mechanisms
Glucuronidase
Darkness
cyanides
cold stress
Growth
homeostasis
cortex
Homeostasis

All Science Journal Classification (ASJC) codes

  • Physiology
  • Genetics
  • Plant Science

Cite this

Guo, Woei-Jiun ; Nagy, Reka ; Chen, Hsin Yi ; Pfrunder, Stefanie ; Yu, Ya Chi ; Santelia, Diana ; Frommer, Wolf B. ; Martinoia, Enrico. / SWEET17, a facilitative transporter, mediates fructose transport across the tonoplast of arabidopsis roots and leaves. In: Plant Physiology. 2014 ; Vol. 164, No. 2. pp. 777-789.
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title = "SWEET17, a facilitative transporter, mediates fructose transport across the tonoplast of arabidopsis roots and leaves",
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.",
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Guo, W-J, Nagy, R, Chen, HY, Pfrunder, S, Yu, YC, Santelia, D, Frommer, WB & Martinoia, E 2014, 'SWEET17, a facilitative transporter, mediates fructose transport across the tonoplast of arabidopsis roots and leaves', Plant Physiology, vol. 164, no. 2, pp. 777-789. https://doi.org/10.1104/pp.113.232751

SWEET17, a facilitative transporter, mediates fructose transport across the tonoplast of arabidopsis roots and leaves. / Guo, Woei-Jiun; Nagy, Reka; Chen, Hsin Yi; Pfrunder, Stefanie; Yu, Ya Chi; Santelia, Diana; Frommer, Wolf B.; Martinoia, Enrico.

In: Plant Physiology, Vol. 164, No. 2, 01.02.2014, p. 777-789.

Research output: Contribution to journalArticle

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T1 - SWEET17, a facilitative transporter, mediates fructose transport across the tonoplast of arabidopsis roots and leaves

AU - Guo, Woei-Jiun

AU - Nagy, Reka

AU - Chen, Hsin Yi

AU - Pfrunder, Stefanie

AU - Yu, Ya Chi

AU - Santelia, Diana

AU - Frommer, Wolf B.

AU - Martinoia, Enrico

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