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

Plant Physiology

Volumn 164, Issue 2, 2014, Pages 777-789

  Guo, Woei Jiun ^a,b   Nagy, Reka ^c   Chen, Hsin Yi ^a   Pfrunder, Stefanie ^c   Yu, Ya Chi ^a   Santelia, Diana ^c   Frommer, Wolf B ^b   Martinoia, Enrico ^c  

^a NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^b GEOPHYSICAL LABORATORY   (United States)

^c UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS PROTEIN; CARRIER PROTEIN; FRUCTOSE; GREEN FLUORESCENT PROTEIN; MESSENGER RNA; SWEET17 PROTEIN, ARABIDOPSIS;

ADAPTATION; ARABIDOPSIS; ARTICLE; CELL VACUOLE; COLD; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PLANT GENE; PLANT LEAF; PLANT ROOT; TRANSPORT AT THE CELLULAR LEVEL;

ADAPTATION, PHYSIOLOGICAL; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BIOLOGICAL TRANSPORT; COLD TEMPERATURE; FRUCTOSE; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GREEN FLUORESCENT PROTEINS; MEMBRANE TRANSPORT PROTEINS; PLANT LEAVES; PLANT ROOTS; RNA, MESSENGER; VACUOLES;

EID: 84893450535     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.113.232751     Document Type: Article

References (66)

1. Aluri S, Büttner M (2007) Identification and functional expression of the Arabidopsis thaliana vacuolar glucose transporter 1 and its role in seed germination and flowering. Proc Natl Acad Sci USA 104: 2537-2542
2. Ayre BG (2011) Membrane-transport systems for sucrose in relation to whole-plant carbon partitioning. Mol Plant 4: 377-394
3. Bhagyalakshmi N, Thimmaraju R, Narayan MS (2004) Various hexoses and di-hexoses differently influence growth, morphology and pigment synthesis in transformed root cultures of red beet (Beta vulgaris). Plant Cell Tissue Organ Cult 78: 183-195
4. Bogdanovič J, Mojovič M, Milosavič N, Mitrovič A, Vucinič Z, Spasojevič I (2008) Role of fructose in the adaptation of plants to cold-induced oxidative stress. Eur Biophys J 37: 1241-1246
5. Braun DM, Slewinski TL (2009) Genetic control of carbon partitioning in grasses: roles of sucrose transporters and tie-dyed loci in phloem loading. Plant Physiol 149: 71-81
6. Chardon F, Bedu M, Calenge F, Klemens PAW, Spinner L, Clement G, Chietera G, Léran S, Ferrand M, Lacombe B, et al (2013) Leaf fructose content is controlled by the vacuolar transporter SWEET17 in Arabidopsis. Curr Biol 23: 697-702
7. Chen LQ, Hou BH, Lalonde S, Takanaga H, Hartung ML, Qu XQ, Guo WJ, Kim JG, Underwood W, Chaudhuri B, et al (2010) Sugar transporters for intercellular exchange and nutrition of pathogens. Nature 468: 527-532
8. Chen LQ, Qu XQ, Hou BH, Sosso D, Osorio S, Fernie AR, Frommer WB (2012) Sucrose efflux mediated by SWEET proteins as a key step for phloem transport. Science 335: 207-211
9. Cho YH, Yoo SD (2011) Signaling role of fructose mediated by FINS1/FBP in Arabidopsis thaliana. PLoS Genet 7: e1001263
10. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacteriummediated transformation of Arabidopsis thaliana. Plant J 16: 735-743
11. Curtis MD, Grossniklaus U (2003) A gateway cloning vector set for highthroughput functional analysis of genes in planta. Plant Physiol 133: 462-469
12. Czajkowski R, de Boer WJ, Velvis H, van der Wolf JM (2010) Systemic colonization of potato plants by a soilborne, green fluorescent proteintagged strain of Dickeya sp. biovar 3. Phytopathology 100: 134-142
13. Dekkers BJ, Schuurmans JA, Smeekens SC (2004) Glucose delays seed germination in Arabidopsis thaliana. Planta 218: 579-588
14. Echeverria E, Valich J (1988) Carbohydrate and enzyme distribution in protoplasts from valencia orange juice sacs. Phytochemistry 27: 73-76
15. Eom JS, Cho JI, Reinders A, Lee SW, Yoo Y, Tuan PQ, Choi SB, Bang G, Park YI, Cho MH, et al (2011) Impaired function of the tonoplast-localized sucrose transporter in rice, OsSUT2, limits the transport of vacuolar reserve sucrose and affects plant growth. Plant Physiol 157: 109-119
16. Etxeberria E, Pozueta-Romero J, Gonzalez P (2012) In and out of the plant storage vacuole. Plant Sci 190: 52-61
17. Frommer WB, Sosso D, Chen LQ (2013) SWEET glucoside transporter superfamily. In CK Gordon, ed, Encyclopedia of Biophysics. Springer, New York, pp 2556-2558
18. Ge YX, Angenent GC, Dahlhaus E, Franken J, Peters J, Wullems GJ, Creemers-Molenaar J (2001) Partial silencing of the NEC1 gene results in early opening of anthers in Petunia hybrida. Mol Genet Genomics 265: 414-423
19. Getz HP, Klein M (1995) Characteristics of sucrose transport and sucroseinduced H+ transport on the tonoplast of red beet (Beta vulgaris L.) storage tissue. Plant Physiol 107: 459-467
20. Grennan AK, Gragg J (2009) How sweet it is: identification of vacuolar sucrose transporters. Plant Physiol 150: 1109-1110
21. Guan YF, Huang XY, Zhu J, Gao JF, Zhang HX, Yang ZN (2008) RUPTURED POLLEN GRAIN1, a member of the MtN3/saliva gene family, is crucial for exine pattern formation and cell integrity of microspores in Arabidopsis. Plant Physiol 147: 852-863
22. Hassan S, Mathesius U (2012) The role of flavonoids in root-rhizosphere signalling: opportunities and challenges for improving plant-microbe interactions. J Exp Bot 63: 3429-3444
23. Jones DL, Darrah PR (1996) Re-sorption of organic compounds by roots of Zea mays L. and its consequences in the rhizosphere III. Characteristics of sugar influx and efflux. Plant Soil 178: 153-160
24. Kaiser G, Heber U (1984) Sucrose transport into vacuoles isolated from barley mesophyll protoplasts. Planta 161: 562-568
25. Kang J, Park J, Choi H, Burla B, Kretzschmar T, Lee Y, Martinoia E (2011) Plant ABC transporters. The Arabidopsis Book 9: e0153, doi/10.1199/tab.0153
26. Kaplan F, Kopka J, Haskell DW, Zhao W, Schiller KC, Gatzke N, Sung DY, Guy CL (2004) Exploring the temperature-stress metabolome of Arabidopsis. Plant Physiol 136: 4159-4168
27. Keller F (1988) A large-scale isolation of vacuoles from protoplasts of mature carrot taproots. J Plant Physiol 132: 199-203
28. Klemens PA, Patzke K, Deitmer JW, Spinner L, Le Hir R, Bellini C, Bedu M, Chardon F, Krapp A, Neuhaus HE (2013) Overexpression of the vacuolar sugar carrier AtSWEET16 modifies germination, growth, and stress tolerance in Arabidopsis. Plant Physiol 163: 1338-1352
29. Krügel U, Kühn C (2013) Post-translational regulation of sucrose transporters by direct protein-protein interactions. Front Plant Sci 4: 237
30. Kühn C, Grof CP (2010) Sucrose transporters of higher plants. Curr Opin Plant Biol 13: 288-298
31. Laugier E, Bouguyon E, Mauriès A, Tillard P, Gojon A, Lejay L (2012) Regulation of high-affinity nitrate uptake in roots of Arabidopsis depends predominantly on posttranscriptional control of the NRT2.1/NAR2.1 transport system. Plant Physiol 158: 1067-1078
32. Leigh R (1984) The role of the vacuole in the accumulation and mobilization of sucrose. Plant Growth Regul 2: 339-346
33. Li P, Wind JJ, Shi X, Zhang H, Hanson J, Smeekens SC, Teng S (2011) Fructose sensitivity is suppressed in Arabidopsis by the transcription factor ANAC089 lacking the membrane-bound domain. Proc Natl Acad Sci USA 108: 3436-3441
34. Martinoia E, Kaiser G, Schramm MJ, Heber U (1987) Sugar transport across the plasmalemma and the tonoplast of barley mesophyll protoplasts. Evidence for different transport systems. J Plant Physiol 131: 467-478
35. Martinoia E, Maeshima M, Neuhaus HE (2007) Vacuolar transporters and their essential role in plant metabolism. J Exp Bot 58: 83-102
36. Martinoia E, Massonneau A, Frangne N (2000) Transport processes of solutes across the vacuolar membrane of higher plants. Plant Cell Physiol 41: 1175-1186
37. Martinoia E, Meyer S, De Angeli A, Nagy R (2012) Vacuolar transporters in their physiological context. Annu Rev Plant Biol 63: 183-213
38. Mustroph A, Zanetti ME, Jang CJ, Holtan HE, Repetti PP, Galbraith DW, Girke T, Bailey-Serres J (2009) Profiling translatomes of discrete cell populations resolves altered cellular priorities during hypoxia in Arabidopsis. Proc Natl Acad Sci USA 106: 18843-18848
39. Neuhaus HE (2007) Transport of primary metabolites across the plant vacuolar membrane. FEBS Lett 581: 2223-2226
40. Payyavula RS, Tay KH, Tsai CJ, Harding SA (2011) The sucrose transporter family in Populus: the importance of a tonoplast PtaSUT4 to biomass and carbon partitioning. Plant J 65: 757-770
41. Pego JV, Smeekens SCM (2000) Plant fructokinases: a sweet family gettogether. Trends Plant Sci 5: 531-536
42. Pontis HG (1989) Fructans and cold stress. J Plant Physiol 134: 148-150
43. Poschet G, Hannich B, Raab S, Jungkunz I, Klemens PA, Krueger S, Wic S, Neuhaus HE, Büttner M (2011) A novel Arabidopsis vacuolar glucose exporter is involved in cellular sugar homeostasis and affects the composition of seed storage compounds. Plant Physiol 157: 1664-1676
44. Riesmeier JW, Willmitzer L, Frommer WB (1992) Isolation and characterization of a sucrose carrier cDNA from spinach by functional expression in yeast. EMBO J 11: 4705-4713
45. Rolland F, Baena-Gonzalez E, Sheen J (2006) Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu Rev Plant Biol 57: 675-709
46. Sanghera GS, Wani SH, Hussain W, Singh NB (2011) Engineering cold stress tolerance in crop plants. Curr Genomics 12: 30-43
47. Sauer N (2007) Molecular physiology of higher plant sucrose transporters. FEBS Lett 581: 2309-2317
48. Sauer N, Friedländer K, Gräml-Wicke U (1990) Primary structure, genomic organization and heterologous expression of a glucose transporter from Arabidopsis thaliana. EMBO J 9: 3045-3050
49. Schulz A, Beyhl D, Marten I, Wormit A, Neuhaus E, Poschet G, Büttner M, Schneider S, Sauer N, Hedrich R (2011) Proton-driven sucrose symport and antiport are provided by the vacuolar transporters SUC4 and TMT1/2. Plant J 68: 129-136
50. Sherson SM, Alford HL, Forbes SM, Wallace G, Smith SM (2003) Roles of cell-wall invertases and monosaccharide transporters in the growth and development of Arabidopsis. J Exp Bot 54: 525-531
51. Sivitz AB, Reinders A, Johnson ME, Krentz AD, Grof CPL, Perroux JM, Ward JM (2007) Arabidopsis sucrose transporter AtSUC9: high-affinity transport activity, intragenic control of expression, and early flowering mutant phenotype. Plant Physiol 143: 188-198
52. Song WY, Park J, Mendoza-Cózatl DG, Suter-Grotemeyer M, Shim D, Hörtensteiner S, Geisler M, Weder B, Rea PA, Rentsch D, et al (2010) Arsenic tolerance in Arabidopsis is mediated by two ABCC-type phytochelatin transporters. Proc Natl Acad Sci USA 107: 21187-21192
53. Thom M, Komor E, Maretzki A (1982) Vacuoles from sugarcane suspension cultures. II. Characterization of sugar uptake. Plant Physiol 69: 1320-1325
54. Tohge T, Ramos MS, Nunes-Nesi A, Mutwil M, Giavalisco P, Steinhauser D, Schellenberg M, Willmitzer L, Persson S, Martinoia E, et al (2011) Toward the storage metabolome: profiling the barley vacuole. Plant Physiol 157: 1469-1482
55. Usadel B, Bläsing OE, Gibon Y, Retzlaff K, Höhne M, Günther M, Stitt M (2008) Global transcript levels respond to small changes of the carbon status during progressive exhaustion of carbohydrates in Arabidopsis rosettes. Plant Physiol 146: 1834-1861
56. Voitsekhovskaja OV, Koroleva OA, Batashev DR, Knop C, Tomos AD, Gamalei YV, Heldt HW, Lohaus G (2006) Phloem loading in two Scrophulariaceae species. What can drive symplastic flow via plasmodesmata? Plant Physiol 140: 383-395
57. Wayne RO (2009) The vacuole. In Plant Cell Biology: From Astronomy to Zoology. Elsevier, Atlanta, pp 101-118
58. Williams LE, Lemoine R, Sauer N (2000) Sugar transporters in higher plants-a diversity of roles and complex regulation. Trends Plant Sci 5: 283-290
59. Wingenter K, Schulz A, Wormit A, Wic S, Trentmann O, Hoermiller II, Heyer AG, Marten I, Hedrich R, Neuhaus HE (2010) Increased activity of the vacuolar monosaccharide transporter TMT1 alters cellular sugar partitioning, sugar signaling, and seed yield in Arabidopsis. Plant Physiol 154: 665-677
60. Winter D, Vinegar B, Nahal H, Ammar R, Wilson GV, Provart NJ (2007) An "Electronic Fluorescent Pictograph" browser for exploring and analyzing large-scale biological data sets. PLoS ONE 2: e718
61. Winter H, Robinson DG, Heldt HW (1993) Subcellular volumes and metabolite concentrations in barley leaves. Planta 191: 180-190
62. Wormit A, Trentmann O, Feifer I, Lohr C, Tjaden J, Meyer S, Schmidt U, Martinoia E, Neuhaus HE (2006) Molecular identification and physiological characterization of a novel monosaccharide transporter from Arabidopsis involved in vacuolar sugar transport. Plant Cell 18: 3476-3490
63. Xuan YH, Hu YB, Chen LQ, Sosso D, Ducat DC, Hou BH, Frommer WB (2013) Functional role of oligomerization for bacterial and plant SWEET sugar transporter family. Proc Natl Acad Sci USA 110: E3685-E3694
64. Yamada K, Osakabe Y, Mizoi J, Nakashima K, Fujita Y, Shinozaki K, Yamaguchi-Shinozaki K (2010) Functional analysis of an Arabidopsis thaliana abiotic stress-inducible facilitated diffusion transporter for monosaccharides. J Biol Chem 285: 1138-1146
65. Yang B, Sugio A, White FF (2006) Os8N3 is a host disease-susceptibility gene for bacterial blight of rice. Proc Natl Acad Sci USA 103: 10503-10508
66. Yuan L, Loqué D, Ye F, Frommer WB, von Wirén N (2007) Nitrogendependent posttranscriptional regulation of the ammonium transporter AtAMT1;1. Plant Physiol 143: 732-744