Overexpression of the vacuolar sugar carrier AtSWEET16 modifies germination, growth, and stress tolerance in Arabidopsis

Plant Physiology

Volumn 163, Issue 3, 2013, Pages 1338-1352

  Klemens, Patrick A W ^a   Patzke, Kathrin ^a   Deitmer, Joachim ^a   Spinner, Lara ^b,c   Le Hir, Rozenn ^b   Bellini, Catherine ^b,c   Bedu, Magali ^b   Chardon, Fabien ^b   Krapp, Anne ^b   Ekkehard Neuhaus, H ^a  

^a Rheinland Pfälzische Technische Universität Kaiserslautern Landau   (Germany)

^b INSTITUT JEAN PIERRE BOURGIN   (France)

^c UMEÅ UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; XENOPUS LAEVIS;

ARABIDOPSIS PROTEIN; CARRIER PROTEIN; FRUCTOSE; GLUCOSE; GLUCOSE TRANSPORTER; GREEN FLUORESCENT PROTEIN; NITROGEN; SUCROSE; SWEET16 PROTEIN, ARABIDOPSIS;

ADAPTATION; ARABIDOPSIS; ARTICLE; BIOMASS; CELL VACUOLE; COLD; CONFOCAL MICROSCOPY; DOWN REGULATION; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; GERMINATION; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUTATION; NORTHERN BLOTTING; OSMOTIC PRESSURE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSGENIC PLANT;

ADAPTATION, PHYSIOLOGICAL; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BIOMASS; BLOTTING, NORTHERN; CARRIER PROTEINS; COLD TEMPERATURE; DOWN-REGULATION; FRUCTOSE; GENE EXPRESSION REGULATION, PLANT; GERMINATION; GLUCOSE; GREEN FLUORESCENT PROTEINS; MICROSCOPY, CONFOCAL; MONOSACCHARIDE TRANSPORT PROTEINS; MUTATION; NITROGEN; OSMOTIC PRESSURE; PLANTS, GENETICALLY MODIFIED; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SUCROSE; VACUOLES;

EID: 84886799091     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.113.224972     Document Type: Article

References (69)

1. Alberdi M, Corcuera LJ (1991) Cold-acclimation in plants. Phytochemistry 30: 3177-3184
2. 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
3. Arenas-Huertero F, Arroyo A, Zhou L, Sheen J, León P (2000) Analysis of Arabidopsis glucose insensitive mutants, gin5 and gin6, reveals a central role of the plant hormone ABA in the regulation of plant vegetative development by sugar. Genes Dev 14: 2085-2096
4. Bröer S, Bröer A, Schneider HP, Stegen C, Halestrap AP, Deitmer JW (1999) Characterization of the high-affinity monocarboxylate transporter MCT2 in Xenopus laevis oocytes. Biochem J 341: 529-535
5. Büttner M, Sauer N (2000) Monosaccharide transporters in plants: structure, function and physiology. Biochim Biophys Acta 1465: 263-274
6. Chardon F, Barthélémy J, Daniel-Vedele F, Masclaux-Daubresse C (2010) Natural variation of nitrate uptake and nitrogen use efficiency in Arabidopsis thaliana cultivated with limiting and ample nitrogen supply. J Exp Bot 61: 2293-2302
7. Chardon F, Bedu M, Calenge F, Klemens PA, 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
8. 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
9. 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
10. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacteriummediated transformation of Arabidopsis thaliana. Plant J 16: 735-743
11. Coruzzi G, Bush DR (2001) Nitrogen and carbon nutrient and metabolite signaling in plants. Plant Physiol 125: 61-64
12. Coruzzi GM, Zhou L (2001) Carbon and nitrogen sensing and signaling in plants: emerging 'matrix effects.' Curr Opin Plant Biol 4: 247-253
13. Cox SE, Stushnoff C (2001) Temperature-related shifts in soluble carbohydrate content during dormancy and cold acclimation in Populus tremuloides. Can J Res 31: 730-737
14. Czechowski T, Stitt M, Altmann T, Udvardi MK, Scheible WR (2005) Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol 139: 5-17
15. Dekkers BJ, Schuurmans JA, Smeekens SC (2004) Glucose delays seed germination in Arabidopsis thaliana. Planta 218: 579-588
16. Dekkers BJ, Schuurmans JA, Smeekens SC (2008) Interaction between sugar and abscisic acid signalling during early seedling development in Arabidopsis. Plant Mol Biol 67: 151-167
17. Desbrosses-Fonrouge AG, Voigt K, Schröder A, Arrivault S, Thomine S, Krämer U (2005) Arabidopsis thaliana MTP1 is a Zn transporter in the vacuolar membrane which mediates Zn detoxification and drives leaf Zn accumulation. FEBS Lett 579: 4165-4174
18. Endler A, Meyer S, Schelbert S, Schneider T, Weschke W, Peters SW, Keller F, Baginsky S, Martinoia E, Schmidt UG (2006) Identification of a vacuolar sucrose transporter in barley and Arabidopsis mesophyll cells by a tonoplast proteomic approach. Plant Physiol 141: 196-207
19. 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 tonoplastlocalized sucrose transporter in rice, OsSUT2, limits the transport of vacuolar reserve sucrose and affects plant growth. Plant Physiol 157: 109-119
20. Fettke J, Eckermann N, Tiessen A, Geigenberger P, Steup M (2005) Identification, subcellular localization and biochemical characterization of water-soluble heteroglycans (SHG) in leaves of Arabidopsis thaliana L.: distinct SHG reside in the cytosol and in the apoplast. Plant J 43: 568-585
21. Flinn CL, Ashworth EN (1995) The relationship between carbohydrates and flower bud hardiness among three forsythia taxa. J Am Soc Hortic Sci 120: 607-613
22. Gerhardt R, Stitt MN, Heldt HW (1987) Subcellular metabolite levels in spinach leaves: regulation of sucrose synthesis during diurnal alterations in photosynthesis. Plant Physiol 83: 339-407
23. Getz HP (1987) Accumulation of sucrose into vacuoles released from isolated sugar beet root protoplasts by both, direct sucrose uptake and UDP-glucose-dependent group translocation. Plant Physiol Biochem 25: 573-580
24. 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
25. Granot D, David-Schwartz R, Kelly G (2013) Hexose kinases and their role in sugar-sensing and plant development. Front Plant Sci 4: 44
26. Hannah MA, Heyer AG, Hincha DK (2005) A global survey of gene regulation during cold acclimation in Arabidopsis thaliana. PLoS Genet 1: e26
27. Hirel B, Le Gouis J, Ney B, Gallais A (2007) The challenge of improving nitrogen use efficiency in crop plants: towards a more central role for genetic variability and quantitative genetics within integrated approaches. J Exp Bot 58: 2369-2387
28. Jang JC, León P, Zhou L, Sheen J (1997) Hexokinase as a sugar sensor in higher plants. Plant Cell 9: 5-19
29. John P (1992) Biosynthesis of the Major Crop Products. John Wiley & Sons, Chichester, UK
30. Kaiser G, Heber U (1984) Sucrose transport into vacuoles isolated from barley mesophyll protoplasts. Planta 161: 562-568
31. Karimi M, Inzé D, Depicker A (2002) Gateway vectors for Agrobacteriummediated plant transformation. Trends Plant Sci 7: 193-195
32. Koch KE (1996) Carbohydrate-modulated gene expression in plants. Annu Rev Plant Physiol Plant Mol Biol 47: 509-540
33. Kovermann P, Meyer S, Hörtensteiner S, Picco C, Scholz-Starke J, Ravera S, Lee Y, Martinoia E (2007) The Arabidopsis vacuolar malate channel is a member of the ALMT family. Plant J 52: 1169-1180
34. Krapp A, Berthomé R, Orsel M, Mercey-Boutet S, Yu A, Castaings L, Elftieh S, Major H, Renou JP, Daniel-Vedele F (2011) Arabidopsis roots and shoots show distinct temporal adaptation patterns toward nitrogen starvation. Plant Physiol 157: 1255-1282
35. Krapp A, Truong HN (2005) Regulation of C/N interaction in model plant species. In S Goyal, R Tischner, A Basra, eds, Enhancing the Efficiency of Nitrogen Utilization in Plants. Haworth, New York, pp 127-173
36. Lalonde S, Wipf D, Frommer WB (2004) Transport mechanisms for organic forms of carbon and nitrogen between source and sink. Annu Rev Plant Biol 55: 341-372
37. Marger MD, Saier MH Jr (1993) A major superfamily of transmembrane facilitators that catalyse uniport, symport and antiport. Trends Biochem Sci 18: 13-20
38. Martinoia E, Maeshima M, Neuhaus HE (2007) Vacuolar transporters and their essential role in plant metabolism. J Exp Bot 58: 83-102
39. Martinoia E, Meyer S, De Angeli A, Nagy R (2012) Vacuolar transporters in their physiological context. Annu Rev Plant Biol 63: 183-213
40. McAllister CH, Beatty PH, Good AG (2012) Engineering nitrogen use efficient crop plants: the current status. Plant Biotechnol J 10: 1011-1025
41. Nägele T, Henkel S, Hörmiller I, Sauter T, Sawodny O, Ederer M, Heyer AG (2010) Mathematical modeling of the central carbohydrate metabolism in Arabidopsis reveals a substantial regulatory influence of vacuolar invertase on whole plant carbon metabolism. Plant Physiol 153: 260-272
42. Nägele T, Heyer AG (2013) Approximating subcellular organisation of carbohydrate metabolism during cold acclimation in different natural accessions of Arabidopsis thaliana. New Phytol 198: 777-787
43. Neuhaus HE (2007) Transport of primary metabolites across the plant vacuolar membrane. FEBS Lett 581: 2223-2226
44. 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
45. 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
46. Quick WP, Siegl G, Neuhaus HE, Feil R, Stitt M (1989) Short-term water stress leads to a stimulation of sucrose synthesis by activating sucrosephosphate synthase. Planta 177: 535-546
47. Reinders A, Sivitz AB, Starker CG, Gantt JS, Ward JM (2008) Functional analysis of LjSUT4, a vacuolar sucrose transporter from Lotus japonicus. Plant Mol Biol 68: 289-299
48. Ristic Z, Ashworth EN (1993) Ultrastructural evidence that intracellular ice formation and possibly cavitation are the sources of freezing injury in supercooling wood tissue of Cornus florida L. Plant Physiol 103: 753-761
49. Roitsch T, González MC (2004) Function and regulation of plant invertases: sweet sensations. Trends Plant Sci 9: 606-613
50. Rolland F, Moore B, Sheen J (2002) Sugar sensing and signaling in plants. Plant Cell (Suppl) 14: S185-S205
51. Scheible WR, Morcuende R, Czechowski T, Fritz C, Osuna D, Palacios-Rojas N, Schindelasch D, Thimm O, Udvardi MK, Stitt M (2004) Genome-wide reprogramming of primary and secondary metabolism, protein synthesis, cellular growth processes, and the regulatory infrastructure of Arabidopsis in response to nitrogen. Plant Physiol 136: 2483-2499
52. Schneider S, Hulpke S, Schulz A, Yaron I, Höll J, Imlau A, Schmitt B, Batz S, Wolf S, Hedrich R, et al (2012) Vacuoles release sucrose via tonoplast-localised SUC4-type transporters. Plant Biol (Stuttg) 14: 325-336
53. 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
54. Schulze W, Schneider T, Starck S, Martinoia E, Trentmann O (2012) Cold acclimation induces changes in Arabidopsis tonoplast protein abundance and activity and alters phosphorylation of tonoplast monosaccharide transporters. Plant J 69: 529-541
55. Schumacher K, Krebs M (2010) The V-ATPase: small cargo, large effects. Curr Opin Plant Biol 13: 724-730
56. Shan X, Yan J, Xie D (2012) Comparison of phytohormone signaling mechanisms. Curr Opin Plant Biol 15: 84-91
57. Smeekens S, Rook F (1997) Sugar sensing and sugar-mediated signal transduction in plants. Plant Physiol 115: 7-13
58. Szecowka M, Heise R, Tohge T, Nunes-Nesi A, Vosloh D, Huege J, Feil R, Lunn J, Nikoloski Z, Stitt M, et al (2013) Metabolic fluxes in an illuminated Arabidopsis rosette. Plant Cell 25: 694-714
59. Turgeon R, Wolf S (2009) Phloem transport: cellular pathways and molecular trafficking. Annu Rev Plant Biol 60: 207-221
60. Willenbrink J, Doll S (1979) Characteristics of the sucrose uptake system of vacuoles isolated from red beet tissue: kinetics and specificity of the sucrose uptake system. Planta 157: 159-162
61. 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
62. Wingenter K, Trentmann O, Winschuh I, Hörmiller II, Heyer AG, Reinders J, Schulz A, Geiger D, Hedrich R, Neuhaus HE (2011) A member of the mitogen-activated protein 3-kinase family is involved in the regulation of plant vacuolar glucose uptake. Plant J 68: 890-900
63. Winter H, Robinson DG, Heldt HW (1993) Subcellular volumes and metabolite concentrations in barley leaves. Planta 191: 180-190
64. Winter H, Robinson DG, Heldt HW (1994) Subcellular volumes and metabolite concentrations in spinach leaves. Planta 193: 530-535
65. 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
66. 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
67. Yoo SD, Cho YH, Sheen J (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc 2: 1565-1572
68. Zuther E, Büchel K, Hundertmark M, Stitt M, Hincha DK, Heyer AG (2004) The role of raffinose in the cold acclimation response of Arabidopsis thaliana. FEBS Lett 576: 169-173
69. Zwieniecki MA, Holbrook NM (2009) Confronting Maxwell's demon: biophysics of xylem embolism repair. Trends Plant Sci 14: 530-534