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Identification of the transporter responsible for sucrose accumulation in sugar beet taproots


Sugar beet provides around one third of the sugar consumed worldwide and serves as a significant source of bioenergy in the form of ethanol. Sucrose accounts for up to 18% of plant fresh weight in sugar beet. Most of the sucrose is concentrated in the taproot, where it accumulates in the vacuoles. Despite 30 years of intensive research, the transporter that facilitates taproot sucrose accumulation has escaped identification. Here, we combine proteomic analyses of the taproot vacuolar membrane, the tonoplast, with electrophysiological analyses to show that the transporter BvTST2.1 is responsible for vacuolar sucrose uptake in sugar beet taproots. We show that BvTST2.1 is a sucrose-specific transporter, and present evidence to suggest that it operates as a proton antiporter, coupling the import of sucrose into the vacuole to the export of protons. BvTST2.1 exhibits a high amino acid sequence similarity to members of the tonoplast monosaccharide transporter family in Arabidopsis, prompting us to rename this group of proteins ‘tonoplast sugar transporters’. The identification of BvTST2.1 could help to increase sugar yields from sugar beet and other sugar-storing plants in future breeding programs.

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Figure 1: Vacuole preparations and identification of BvTST proteins in B. vulgaris.
Figure 2: Relationship between sucrose content and mRNA levels of all four BvTST paralogues.
Figure 3: Characterization of BvTST2.1 and BvTST1 properties using both electrophysiological assays and transgenic Arabidopsis mutants.


  1. 1

    Giaquinta, R. T. Sucrose translocation and storage in the sugar beet. Plant Physiol. 63, 828–832 (1979).

    CAS  Article  Google Scholar 

  2. 2

    Hawker, J. S. & Hatch, M. D. Mechanisms of sugar storage by mature stem tissue of sugarcane. Physiol. Plant 18, 444–453 (1965).

    Article  Google Scholar 

  3. 3

    Chen, L. Q. et al. Sugar transporters for intercellular exchange and nutrition of pathogens. Nature 468, 527–532 (2010).

    CAS  Article  Google Scholar 

  4. 4

    Lalonde, S., Wipf, D. & Frommer, W. B. Transport mechanisms for organic forms of carbon and nitrogen between source and sink. Ann. Rev. Plant Biol. 55, 341–372 (2004).

    CAS  Article  Google Scholar 

  5. 5

    Williams, L. E., Lemoine, R. & Sauer, N. Sugar transporter in higher plants - a diversity of roles and complex regulation. Trends Plant Sci. 5, 283–289 (2000).

    CAS  Article  Google Scholar 

  6. 6

    Moghaddam, M. R. B. & Van den Ende, W. Sweet immunity in the plant circadian regulatory network. J. Exp. Bot. 64, 1439–1449 (2013).

    Article  Google Scholar 

  7. 7

    Winter, H., Robinson, D. G. & Heldt, H. W. Subcellular volumes and metabolite concentrations in barley leaves. Planta 191, 180–190 (1993).

    CAS  Article  Google Scholar 

  8. 8

    Martinoia, E., Maeshima, M. & Neuhaus, H. E. Vacuolar transporters and their essential role in plant metabolism. J. Exp. Bot. 58, 83–102 (2007).

    CAS  Article  Google Scholar 

  9. 9

    Neuhaus, H. E. Transport of primary metabolites across the plant vacuolar membrane. FEBS Lett. 581, 2223–2226 (2007).

    CAS  Article  Google Scholar 

  10. 10

    Martinoia, E. & Ratajczak, R. in Advances in Botanical Research: The Plant Vacuole Vol. 25 (eds Leigh, A. & Sanders, D.) 365–400 (Academic, 1997).

  11. 11

    Willenbrink, J. & Doll, S. Characteristics of the sucrose uptake system of vacuoles isolated from red beet tissue. Kinetics and specifity of the sucrose uptake system. Planta 157, 159–162 (1979).

    Article  Google Scholar 

  12. 12

    Martinoia, E., Meyer, S., De Angeli, A. & Nagy, R. Vacuolar transporters in their physiological context. Ann. Rev. Plant Biol. 63, 163–213 (2012).

    Article  Google Scholar 

  13. 13

    Aluri, S. & Büttner M. 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 (2007).

    CAS  Article  Google Scholar 

  14. 14

    Wormit, A. et al. Molecular identification and physiological characterization of a novel monosaccharide transporter from Arabidopsis involved in vacuolar sugar transport. Plant Cell 18, 3476–3490 (2006).

    CAS  Article  Google Scholar 

  15. 15

    Klemens, P. A. et al. Overexpression of a proton-coupled vacuolar glucose exporter impairs freezing tolerance and seed germination. New Phytol. 202, 115–121 (2014).

    Article  Google Scholar 

  16. 16

    Wingenter, K. et al. 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 (2011).

    CAS  Article  Google Scholar 

  17. 17

    Poschet G. et al. 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 (2011).

    CAS  Article  Google Scholar 

  18. 18

    Schneider, S. et al. Vacuoles release sucrose via tonoplast-localised SUC4-type transporters. Plant Biol. 14, 325–336 (2012).

    CAS  Article  Google Scholar 

  19. 19

    Schulz, A. et al. Proton-driven sucrose symport and antiport are provided by the vacuolar transporters SUC4 and TMT1/2. Plant J. 68, 129–136 (2011).

    CAS  Article  Google Scholar 

  20. 20

    Eom J. S. et al. 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 (2011).

    CAS  PubMed  Google Scholar 

  21. 21

    Schmidt U. G. et al. Novel tonoplast transporters identified using a proteomic approach with vacuoles isolated from cauliflower buds. Plant Physiol. 145, 216–229 (2007).

    CAS  Article  Google Scholar 

  22. 22

    Chardon, F. et al. Leaf fructose content is controlled by the vacuolar transporter SWEET17 in Arabidopsis. Curr. Biol. 23, 697–702 (2013).

    CAS  Article  Google Scholar 

  23. 23

    Klemens P. A. et al. Overexpression of the vacuolar sugar carrier AtSWEET16 modifies germination, growth, and stress tolerance in Arabidopsis. Plant Physiol. 163, 1338–1352 (2013).

    CAS  Article  Google Scholar 

  24. 24

    Marggraf, A. S. Zuckerrübe (Arnold Wever, Berlin 1767).

  25. 25

    Casdorph, M. 2012 crop year review. Sugarbeet Grower 52, (1), 4–10 (2013).

    Google Scholar 

  26. 26

    Maung, T. A. & Gustafson, C. R. The economic feasibility of sugar beet biofuel production in central North Dakota. Biomass Bioenergy 35, 3737–3747 (2011).

    Google Scholar 

  27. 27

    Dohm, J. C. et al. The genome of the recently domesticated crop plant sugar beet (Beta vulgaris). Nature 505, 546–549 (2014).

    CAS  Article  Google Scholar 

  28. 28

    Wingenter, K. et al. Increased activity of the vacuolar monosaccharide transporter TMT1 alters cellular sugar partitioning, sugar signalling and seed yield in Arabidopsis. Plant Physiol. 154, 665–677 (2010).

    CAS  Article  Google Scholar 

  29. 29

    Zemek. J., Hricovà, D., Stremen, J. & Bauer, S. Effect of 2-deoxy-d-glucose on tissue culture of Nicotiana tabacum L. (cv. Virginia Bright Italia). Z. Pflanzenphysiol. 76, 114–119 (1975).

    CAS  Article  Google Scholar 

  30. 30

    Kunze, H. et al. 2-Deoxyglucose resistance: a novel selection marker for plant transformation. Mol. Breed. 7, 221–227 (2001).

    CAS  Article  Google Scholar 

  31. 31

    Carter, C. et al. The vegetative vacuole proteome of Arabidopsis thaliana reveals predicted and unpredicted proteins. Plant Cell 16, 3285–3303 (2004).

    CAS  Article  Google Scholar 

  32. 32

    Schulze, W. X., Schneider, T., Starck, S., Martinoia, E. & Trentmann, O. Cold acclimation induces changes in Arabidopsis tonoplast protein abundance and activity and alters phosphorylation of tonoplast monosaccharide transporters. Plant. J. 69, 529–541 (2012).

    CAS  Article  Google Scholar 

  33. 33

    Szponarski, W., Sommerer, N., Boyer, J. C., Rossignol, M. & Gibrat, R. Large-scale characterization of integral proteins from Arabidopsis vacuolar membrane by two-dimensional liquid chromatography. Proteomics 4, 397–406 (2004).

    CAS  Article  Google Scholar 

  34. 34

    Endler, A. et al. In vivo phosphorylation sites of barley tonoplast proteins identified by a phosphoproteomic approach. Proteomics 9, 310–321 (2009).

    CAS  Article  Google Scholar 

  35. 35

    Oldemeyer, R. K. Introgressive hybridization as a breeding method in Beta vulgaris. J. Am. Soc. Sugar Beet Technol. 18, 269–273 (1975).

    Article  Google Scholar 

  36. 36

    Carter, J. N. Sucrose production as affected by root yield and sucrose concentration of sugarbeets. J. Am. Soc. Sugar Beet Technol. 24, 14–31 (1987).

    CAS  Article  Google Scholar 

  37. 37

    Leigh, R. A. & Branton, D. Isolation of vacuoles from root storage tissue of Beta vulgaris L. Plant Physiol. 58, 656–662 (1976).

    CAS  Article  Google Scholar 

  38. 38

    Boller, T. & Kende, H. Hydrolytic enzymes in the central vacuole of plant cells. Plant Physiol. 63, 1123–1132 (1979).

    CAS  Article  Google Scholar 

  39. 39

    Reiser, J., Linka, N., Lemke, L., Jeblick, W. & Neuhaus, H. E. Molecular physiological analysis of the two plastidic ATP/ADP transporters from Arabidopsis thaliana. Plant Physiol. 136, 3524–3536 (2004).

    CAS  Article  Google Scholar 

  40. 40

    Bergmeyer, U. Methoden der Enzymatischen Analyse (Verlag Chemie, 1974).

  41. 41

    Stitt, M., Lilley, R.M., Gerhardt, R. & Heldt, H-W. Metabolite levels in specific cells and subcellular compartments of plant leaves. Method Enzymol. 174, 518–552 (1989).

    CAS  Article  Google Scholar 

  42. 42

    Jung, B., Hoffmann, C. & Möhlmann, T. Arabidopsis nucleoside hydrolases involved in intracellular and extracellular degradation of purines. Plant J. 65, 703–711 (2011).

    CAS  Article  Google Scholar 

  43. 43

    Leroch, M. et al. Identification and characterization of a novel plastidic adenine nucleotide uniporter from Solanum tuberosum. J. Biol. Chem. 280, 17992–18000 (2005).

    CAS  Article  Google Scholar 

  44. 44

    Mühlhaus, T., Weiss, J., Hemme, D., Sommer, F. & Schroda, M. Quantitative shotgun proteomics using a uniform 15N-labeled standard to monitor proteome dynamics in time course experiments reveals new insights into the heat stress response of Chlamydomonas reinhardtii. Mol. Cell Proteomics 10, M110 (2011).

    Article  Google Scholar 

  45. 45

    Cox, J. & Mann, M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nature Biotechnol. 26, 1367–1372 (2008).

    CAS  Article  Google Scholar 

  46. 46

    Stanke, M., Schöffmann, O., Morgenstern, B. & Waack, S. Gene prediction in eukaryotes with a generalized hidden Markov model that uses hints from external sources. BMC Bioinformatics 7, 62 (2006).

    Article  Google Scholar 

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Work in the labs of H.E.N., R.H., U-I.F. and N.S. was financially supported by BMBF (Betamorphosis). Work in the lab of R.H. and H.E.N. was additionally supported by the Deutsche Forschungsgemeinschaft (FOR1061) and the Federal State of Rhineland Palatinate (BioComp). We thank Maike Müller for technical assistance. We are grateful to Karsten Harms for supporting project planning and comments on the manuscript.

Author information




B.J. conceived and conducted vacuole preparation; conceived the cloning of GFP fusion constructs and localization studies; and conducted phylogenetic analyses. B.J. and G.M. conceived, performed and analysed the expression studies. B.J., G.M. and N.W. performed sugar determination, growth experiments and generation of transgenic plants. A.S., I.M., D.G. and T.A.C. conducted electrophysiological measurements. B.P. and P.W. studied subcellular localizations. F.S., T.M. and M.S. conceived and conducted proteomic analyses. W.K. provided access to the B. vulgaris nucleotide sequences. F.L., U-I.F., N.S., I.M., R.H. and H.E.N. designed and conceived the study. H.E.N. wrote the manuscript. All authors discussed the results and commented on the manuscript.

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Correspondence to Rainer Hedrich or H. Ekkehard Neuhaus.

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The authors declare no competing financial interests.

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Jung, B., Ludewig, F., Schulz, A. et al. Identification of the transporter responsible for sucrose accumulation in sugar beet taproots. Nature Plants 1, 14001 (2015).

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