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Photosynthesis pp 703-729 | Cite as

Sucrose Transport in Higher Plants: From Source to Sink

  • Naohiro Aoki
  • Tatsuro Hirose
  • Robert T. Furbank
Chapter
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 34)

Summary

Sucrose transport in plants has been as area of intense interest for many years, particularly following the cloning of the first sucrose/proton symporter, or sucrose transporter, from spinach more than 15 years ago. Much debate and research has focused on phloem loading, particularly the issue of apoplasmic versus symplasmic pathways of loading and in the apoplasmic loaders, on the location of the sucrose transporter protein and mRNA. This chapter focuses on pointing out the remaining unanswered questions in phloem loading and sucrose transport in general rather than extensively reviewing the literature. We discuss in more detail the long-distance transport pathway from source to sink and post-phloem unloading in sink tissue such as dicot seed, cereal grain, sink leaves, roots and tubers.

Keywords

Sieve Tube Minor Vein Hexose Transporter Sucrose Transport Sink Tissue 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Abbreviations:

CC –

Companion cell;

CF –

Carboxyfluorescein;

GFP –

Green fluorescent protein;

PCMBS –

Para-chloromercuribenzylsulphonic acid;

RFO –

Raffinose-family oligosaccharide;

SE –

Sieve element;

SUT –

Sucrose transporter

Notes

Acknowledgements

We wish to acknowledge the help and encouragement of all our colleagues in sugar transport research, particularly those that made data available to us pre-publication.

References

  1. Ageorges A, Issaly N, Picaud S, Delrot S and Romieu C (2000) Identification and functional expression in yeast of a grape berry sucrose carrier. Plant Physiol Biochem 38: 177–185CrossRefGoogle Scholar
  2. Aoki N, Hirose T, Takahashi S, Ono K, Ishimaru K and Ohsugi R (1999) Molecular cloning and expression analysis of a gene for a sucrose transporter in maize (Zea mays L.). Plant Cell Physiol 40: 1072–1078PubMedCrossRefGoogle Scholar
  3. Aoki N, Whitfeld P, Hoeren F, Scofield G, Newell K, Patrick J, Offler C, Clarke B, Rahman S and Furbank RT (2002) Three sucrose transporter genes are expressed in the developing grain of hexaploid wheat. Plant Mol Biol 50: 453–462PubMedCrossRefGoogle Scholar
  4. Aoki N, Hirose T, Scofield GN, Whitfeld PR and Furbank RT (2003) The sucrose transporter gene family in rice. Plant Cell Physiol 44: 223–232PubMedCrossRefGoogle Scholar
  5. Aoki N, Scofield GN, Wang X-D, Patrick JW, Offler CE and Furbank RT (2004) Expression and localization analysis of the wheat sucrose transporter TaSUT1 in vegetative tissues. Planta 219: 176–184PubMedCrossRefGoogle Scholar
  6. Aoki N, Scofield GN, Wang, X-D Offler, CE, Patrick JW and Furbank RT (2006) Expression studies indicate sugar transporters play key roles in germinating wheat seeds. Plant Physiol 141: 1255–1263PubMedCrossRefGoogle Scholar
  7. Ayre BG, Keller F and Turgeon R (2003) Symplastic continuity between companion cells and the translocation stream: long-distance transport is controlled by retention and retrieval mechanisms in the phloem. Plant Physiol 131: 1518–1528PubMedCrossRefGoogle Scholar
  8. Bagnall N, Wang X-D, Scofield GN, Furbank RT, Offler CE and Patrick JW (2000) Sucrose transport-related genes are expressed in both maternal and filial tissues of developing wheat grains. Aust J Plant Physiol 27: 1009–1020Google Scholar
  9. Barker L, Kühn C, Weise A, Schulz A, Gebhardt C, Hirner B, Hellmann H, Schulze W, Ward JM and Frommer WB (2000) SUT2, a putative sucrose sensor in sieve elements. Plant Cell 12: 1153–1164PubMedGoogle Scholar
  10. Baroja-Fernandez E, Etxeberria E, Muñoz FJ, Morán-Zorzano MT, Alonso-Casajús N, Gonzalez P and Pozueta-Romero J (2006) An important pool of sucrose linked to starch biosynthesis is taken up by endocytosis in heterotrophic cells. Plant Cell Physiol 47: 447–456PubMedCrossRefGoogle Scholar
  11. Barth I, Meyer S and Sauer N (2003) PmSUC3: characterization of a SUT2/SUC3-type sucrose transporter from Plantago major. Plant Cell 15: 1375–1385PubMedCrossRefGoogle Scholar
  12. Baud S, Wuillème S, Lemoine R, Kronenberger J, Caboche M, Lepiniec L and Rochat C (2005) The AtSUC5 sucrose transporter specifically expressed in the endosperm is involved in early seed development in Arabidopsis. Plant J 43: 824–836PubMedCrossRefGoogle Scholar
  13. Beebe DU and Russin WA (1999) Plasmodesmata in the phloem-loading pathway. In: Van Bel AJE and Van Kesteren WJP (eds) Plasmodesmata: Structure, Function, Role in Cell Communication, pp 261–294. Springer-Verlag, BerlinGoogle Scholar
  14. Beebe DU and Turgeon R (1992) Localization of galactinol, raffinose, and stachyose synthesis in Cucrbita pepo leaves. Planta 188: 354–361CrossRefGoogle Scholar
  15. Bell CI and Leigh RA (1996) Differential effects of turgor on sucrose and potassium transport at the tonoplast and plasma membrane of sugarbeet storage root tissue. Plant Cell Environ 19: 191–200CrossRefGoogle Scholar
  16. Bewley (1997) Seed germination and dormancy. Plant Cell 9: 1055–1066PubMedCrossRefGoogle Scholar
  17. Bick J-A, Neelam A, Smith E, Nelson SJ, Hall JL and Williams LE (1998) Expression analysis of a sucrose carrier in the germinating seedling of Ricinus communis. Plant Mol Biol 38: 425–435PubMedCrossRefGoogle Scholar
  18. Boorer KJ, Loo DDF, Frommer WB and Wright EM (1996) Transport mechanism of the cloned potato H+/sucrose cotransporter StSUT1. J Biol Chem 271: 25139–25144PubMedCrossRefGoogle Scholar
  19. Borisjuk L, Walenta S, Weber H, Muller-Klieser W and Wobus U (1998) High-resolution histographical mapping of glucose concentrations in developing cotyledons of Vicia faba in relation to mitotic activity and storage processes: glucose as a possible developmental trigger. Plant J 15: 583–591CrossRefGoogle Scholar
  20. Borisjuk L, Walenta S, Rolletschek H, Muller-Klieser W, Wobus U and Weber H (2002) Spatial analysis of plant metabolism: sucrose imaging within Vicia faba cotyledons reveals specific developmental patterns. Plant J 29: 521–530PubMedCrossRefGoogle Scholar
  21. Borstlap AC and Shuurmans JAMJ (2004) Sucrose transport into plasma membrane vesicles from tobacco leaves by H+ symport or counter exchange does not display a linear component. J Membrane Biol 198: 31–42CrossRefGoogle Scholar
  22. Botha CEJ and Cross RHM (1997) Plasmodesmatal frequency in relation to short-distance transport and phloem loading in leaves of barley (Hordeum vulgare). Phloem is not loaded directly from the symplast. Physiol Plant 99: 355–362CrossRefGoogle Scholar
  23. Botha CEJ, Cross RHM, Van Bel AJE and Peter CI (2000) Phloem loading in the sucrose-export-defective (SXD-1) mutant maize is limited by callose deposition at plasmodesmata in bundle sheath-vascular parenchyma interface. Protoplasma 214: 65–72CrossRefGoogle Scholar
  24. Braun DM and Slewinski TL (2009) Genetic control of carbon partitioning in grasses: roles of sucrose transporters and tie-dyed loci in phloem loading. Plant Physiol 149: 71–81PubMedCrossRefGoogle Scholar
  25. Braun DM, Ma Y, Inada N, Muszynski MG and Baker RF (2006) tie-dyed1 regulates carbohydrate accumulation in maize leaves. Plant Physiol 142: 1511–1522PubMedCrossRefGoogle Scholar
  26. Bürkle L, Hibberd JM, Quick WPK, Kühn C, Hirner B and Frommer WB (1998) The H+-sucrose cotransporter NtSUT1 is essential for sugar export from tobacco leaves. Plant Physiol 118: 59–68PubMedCrossRefGoogle Scholar
  27. Bush DR (1993) Proton-coupled sugar and amino acid transporters in plants. Annu Rev Plant Physiol Plant Mol Biol 44: 513–542CrossRefGoogle Scholar
  28. Carpaneto A, Geiger D, Bamberg E, Sauer N, Fromm J and Hedrich R (2005) Phloem-localized, proton-coupled sucrose carrier ZmSUT1 mediates sucrose efflux under control of sucrose gradient and pmf. J Biol Chem 280: 21437–21443PubMedCrossRefGoogle Scholar
  29. Casu RE, Grof CPL, Rae AL, McIntyre CL, Dimmock CM and Manners JM (2003) Identification of a novel sugar transporter homologue strongly expressed in mature stem vascular tissues of sugarcane by expressed sequence tag and microarray analysis. Plant Mol Biol 52: 371–386PubMedCrossRefGoogle Scholar
  30. Chiou TJ and Bush DR (1998) Sucrose is a signal molecule in assimilate partitioning. Proc Natl Acad Sci USA 95: 4784–4788PubMedCrossRefGoogle Scholar
  31. Chourey PS, Taliercio EW, Carlson SJ and Ruan YL (1998) Genetic evidence that the two isozymes of sucrose synthase present in developing maize endosperm are critical, one for cell wall integrity and the other for starch biosynthesis. Mol Gen Genet 259: 88–96PubMedCrossRefGoogle Scholar
  32. Cock JH and Yoshida S (1972) Accumulation of 14C-labelled carbohydrate before flowering and its subsequent redistribution and respiration in the rice plant. Proc Crop Sci Soc Jpn 41: 226–234CrossRefGoogle Scholar
  33. Coombe BG (1992) Research on development and ripening of the grape berry. Am J Enol Vitic 43: 101–110Google Scholar
  34. Davies C and Robinson SP (1996) Sugar accumulation in grape berries: cloning of two putative vacuolar invertase cDNAs and their expression in grapevine tissue. Plant Physiol 111: 275–283PubMedCrossRefGoogle Scholar
  35. Decourteix M, Alves G, Brunel N, Améglio T, Guilliot A, Lemoine R, Pétel G and Sakr (2006) JrSUT1, a putative xylem sucrose transporter, could mediate sucrose influx into xylem parenchyma cells and be up-regulated by freeze-thaw cycles over the autumn-winter period in walnut tree (Juglans regia L.). Plant Cell Environ 29: 36–47PubMedCrossRefGoogle Scholar
  36. Dorion S, Lalonde S and Saini HS (1996) Induction of male sterility in wheat by meiotic-stage water deficit is preceded by a decline in invertase activity and changes in carbohydrate metabolism in anthers. Plant Physiol 111: 137–145PubMedGoogle Scholar
  37. Echeverría E (2000) Vesicle-mediated solute transport between the vacuole and the plasma membrane. Plant Physiol 123: 1217–1226PubMedCrossRefGoogle Scholar
  38. Edelman J, Shibko SI and Keys AJ (1959) The role of the scutellum of cereal seedlings in the synthesis and transport of sucrose. J Exp Bot 10: 178–189CrossRefGoogle Scholar
  39. Endler A, Meyer S, Schelbert S, Schneider T, Weschke W, Peters SW, Keller F, Baginsky S, Martinoia E and Schmidt UG (2006) Identification of a vacuolar sucrose transporter in barley and Arabidopsis mesophyll cells by a tonoplast proteomic approach. Plant Physiol 141: 196–207PubMedCrossRefGoogle Scholar
  40. Etxeberria E, Baroja-Fernandez E, Muños FJ and Pozueta-Romero J (2005) Sucrose-inducible endocytosis as a mechanism for nutrient uptake in heterotrophic plant cell. Plant Cell Physiol 46: 474–481PubMedCrossRefGoogle Scholar
  41. Evert RF, Eschrich W and Heyser W (1978) Leaf structure in relation to solute transport and phloem loading in Zea mays L. Planta 138: 279–294CrossRefGoogle Scholar
  42. Evert RF, Russin WA and Botha CEJ (1996) Distribution and frequency of plasmodesmata in relation to photoassimilate pathways and phloem loading in the barley leaf. Planta 198: 572–579CrossRefGoogle Scholar
  43. Fallahi H, Scofield GN, Badger MR, Chow WS, Furbank RT and Ruan YL (2008) Localization of sucrose synthase in developing seed and siliques of Arabidopsis thaliana reveals diverse roles for SUS during development. J Ex Bot 59: 3283–3295CrossRefGoogle Scholar
  44. Fillion L, Ageorges A, Picaud S, Coutos-Thévenot P, Lemoine R, Romieu C and Derlot S (1999) Cloning and expression of a hexose transporter gene expressed during the ripening of grape berry. Plant Physiol 120: 1083–1093PubMedCrossRefGoogle Scholar
  45. Fisher DG (1986) Ultrastructure, plasmodesmatal frequency and solute concentration in green areas of variegated Coleus blumei Benth. leaves. Planta 169: 141–152CrossRefGoogle Scholar
  46. Fukumorita T and Chino M (1982) Sugar, amino acid and inorganic contents in rice phloem sap. Plant Cell Physiol 23: 273–283Google Scholar
  47. Furbank RT, Scofield GN, Hirose T, Wang X-D, Patrick JW and Offler CE (2001) Cellular localisation and function of a sucrose transporter OsSUT1 in developing rice grains. Aust J Plant Physiol 28: 1187–1196Google Scholar
  48. Gahrtz M, Stolz J and Sauer N (1994) A phloem specific sucrose-H+ symporter from Plantago major L. supports the model of apoplastic phloem loading. Plant J 6: 697–706PubMedCrossRefGoogle Scholar
  49. Gahrtz M, Schmelzer E, Stolz J and Sauer N (1996) Expression of the PmSUC1 sucrose carrier gene from Plantago major L. is induced during seed development. Plant J 9: 93–100PubMedCrossRefGoogle Scholar
  50. Gamalei YV (1989) Structure and function of leaf minor veins in trees and herbs. A taxonomic review. Trees 3: 96–110CrossRefGoogle Scholar
  51. Gamalei YV (1991) Phloem loading and its development related to plant evolution from trees to herbs. Trees 5: 50–64CrossRefGoogle Scholar
  52. Giaquinta RT (1983) Phloem loading of sucrose. Ann Rev Plant Physiol 34: 347–387CrossRefGoogle Scholar
  53. Gottwald JR, Krysan PJ, Young JC, Evert RF and Sussman MR (2000) Genetic evidence for the in planta role of phloem-specific plasma membrane sucrose transporters. Proc Natl Acad Sci USA 97: 13979–13984PubMedCrossRefGoogle Scholar
  54. Grimm E, Bernhardt G, Rothe K and Jacob F (1990) Mechanism of sucrose retrieval along the phloem path: a kinetic approach. Planta 182: 480–485CrossRefGoogle Scholar
  55. Hackel A, Schauer N, Carrari F, Fernie AR, Grimm B and Kühn C (2006) Sucrose transporter LeSUT1 and LeSUT2 inhibition affects tomato fruit development in different ways. Plant J 45: 180–192PubMedCrossRefGoogle Scholar
  56. Haupt S, Duncan GH, Holzberg S and Oparka KJ (2001) Evidence for symplastic phloem unloading in sink leaves of barley. Plant Physiol 125: 209–218PubMedCrossRefGoogle Scholar
  57. Haritatos E, Keller F and Turgeon R (1996) Raffinose oligosaccharide concentrations measured in individual cell and tissue types in Cucumis melo L. leaves: implications for phloem loading. Planta 198: 614–622CrossRefGoogle Scholar
  58. Hayashi H and Chino M (1986) Collection of pure phloem sap from wheat and its chemical composition. Plant Cell Physiol 27: 1387–1393Google Scholar
  59. Hirose T and Terao T (2004) A comprehensive expression analysis of the starch synthase gene family in rice (Oryza sativa L.). Planta 220: 9–16PubMedCrossRefGoogle Scholar
  60. Hirose T, Imaizumi N, Scofield GN, Furbank RT and Ohsugi R (1997) cDNA cloning and tissue specific expression of a gene for sucrose transporter from rice (Oryza sativa L.). Plant Cell Physiol 38: 1389–1396PubMedCrossRefGoogle Scholar
  61. Hirose T, Endler A and Ohsugi R (1999) Gene expression of enzymes for starch and sucrose metabolism and transport in leaf sheaths of rice (Oryza sativa L.) during the heading period in relation to the sink to source transition. Plant Prod Sci 2: 178–183CrossRefGoogle Scholar
  62. Hirose T, Takano M and Terao T (2002) Cell wall invertase in developing rice caryopsis: molecular cloning of OsCIN1 and analysis of its expression in relation to its role in grain filling. Plant Cell Physiol 43: 452–459PubMedCrossRefGoogle Scholar
  63. Hirose T, Ohdan T, Nakamura Y, Terao T (2006) Expression profiling of genes related to starch synthesis in rice leaf sheaths during the heading period. Physiol Plant 128: 425–435CrossRefGoogle Scholar
  64. Hofius D, Hajirezaei M-R, Geiger M, Tschiersch H and Melzer M (2004) RNAi-mediated tocopherol deficiency impairs photoassimilate export in transgenic potato plants. Plant Physiol 135: 1256–1268PubMedCrossRefGoogle Scholar
  65. Imlau A, Truernit E and Sauer N (1999) Cell-to-cell and long-distance trafficking of the green fluorescent protein in the phloem and symplastic unloading of the protein into sink tissues. Plant Cell 11: 309–322PubMedGoogle Scholar
  66. Ishimaru K, Hirose T, Aoki N, Takahashi S, Ono K, Yamamoto S, Wu J, Saji S, Baba T, Ugaki M, Matsumoto T and Ohsugi R (2001) Antisense expression of a rice sucrose transporter OsSUT1 in rice (Oryza sativa L.). Plant Cell Physiol 42: 1181–1185PubMedCrossRefGoogle Scholar
  67. Jacobsen KR, Fisher DG, Maretzki A and Moore PH (1992) Developmental changes in the anatomy of the sugarcane stem in relation to phloem unloading and sucrose storage. Bot Acta 105: 70–80Google Scholar
  68. Juchaux-Cachau M, Landouar-Arsivaud L, Pichaut J-P, Campion C, Porcheron B, Jeauffre J, Noiraud-Romy N, Simoneau P, Maurousset L and Lemoine R (2007) Characterization of AgMaT2, a plasma membrane mannitol transporter from celery, expressing in phloem cells, including phloem parenchyma cells. Plant Physiol 145: 62–74PubMedCrossRefGoogle Scholar
  69. Kaneko M, Chonan N and Matsuda T (1980) Ultrastructure of the small vascular bundles and transfer pathways for photosynthate in the leaves of rice plant. Japan J Crop Sci 49: 42–50 (In Japanese with English summary)CrossRefGoogle Scholar
  70. King SP, Lunn JE and Furbank RT (1997) Carbohydrate content and enzyme metabolism in developing canola siliques. Plant Physiol 114: 153–160PubMedGoogle Scholar
  71. Knop C, Voitsekhovskaja O and Lohaus G (2001) Sucrose transporters in two members of the Scrophulariaceae with different types of transport sugar. Planta 213: 80–91PubMedCrossRefGoogle Scholar
  72. Knop C, Stadler R, Sauer N and Lohaus G (2004) AmSUT1, a sucrose transporter in collection and transport phloem of the putative symplastic phloem loader Alonsoa meridionalis. Plant Physiol 134: 204–214PubMedCrossRefGoogle Scholar
  73. Koonjul PK, Minhas JS, Nunes C, Sheoran IS and Saini HS (2005) Selective transcriptional down-regulation of anther invertases precedes the failure of pollen development in water-stressed wheat. J Exp Bot 56: 179–190PubMedGoogle Scholar
  74. Krügel U, Veenhoff LM, Langbin J, Wiederhold E, Liesche J, Friedrich T, Grimm B, Martinoia E, Poolman B and Kühn C (2008) Transport and sorting of the Solanum tuberosum sucrose transporter SUT1 is affected by posttranscriptional modification. Plant Cell 20: 2497–2513PubMedCrossRefGoogle Scholar
  75. Kühn C (2003) A comparison of the sucrose trnasporter systems of different plant species. Plant Biol 5: 215–232CrossRefGoogle Scholar
  76. Kühn C, Quick WP, Schulz A Riesmeier JW, Sonnewald U and Frommer WB (1996) Companion cell-specific inhibition of the potato sucrose transporter SUT1. Plant Cell Environ 19: 1115–1123CrossRefGoogle Scholar
  77. Kühn C, Franceschi VR, Schulz A, Lemoine R and Frommer WB (1997) Macromolecular trafficking indicated by localization and turnover of sucrose transporters in enucleate sieve elements. Science 275: 1298–1300PubMedCrossRefGoogle Scholar
  78. Kühn C, Hajirezaei M-R, Fernie AR, Roessner-Tunali U, Czechowski T, Hirner B and Frommer WB (2003) The sucrose transporter StSUT1 localizes to sieve elements in potato tuber phloem and influences tuber physiology and development. Plant Physiol 131: 102–113PubMedCrossRefGoogle Scholar
  79. Lalonde S, Boles E, Hellmann H, Barker L, Patrick JW, Frommer WB and Ward JM (1999) A dual function of sugar carriers in transport and sugar sensing. Plant Cell 11: 707–726PubMedGoogle Scholar
  80. Lalonde S, Tegeder M, Throne-Holst M, Frommer WB and Patrick JW (2003) Phloem loading and unloading of sugars and amino acids. Plant Cell Environ 26: 37–56CrossRefGoogle Scholar
  81. Lalonde S, Wipf D and Frommer WB (2004) Transport mechanism for organic forms of carbon and nitrogen between source and sink. Annu Rev Plant Biol 55: 341–372PubMedCrossRefGoogle Scholar
  82. Lauterbach C, Niedermeier M, Besenbeck R, Stadler R and Sauer N (2007) Immunolocalization of the PmSUC1 sucrose transporter in Plantago major flowers and reporter-gene analyses of the PmSUC1 promoter suggest a role in sucrose release from the inner integument. Plant Biol 9: 357–365PubMedCrossRefGoogle Scholar
  83. Lemoine R (2000) Sucrose transporters in plants: update on function and structure. Biochim Biophys Acta 1465: 246–262PubMedCrossRefGoogle Scholar
  84. Lemoine R, Delrot S, Gallet O and Larsson C (1989) The sucrose carrier of the plant plasma membrane. II. Immunological characterization. Biochim Biophys Acta 978: 65–71CrossRefGoogle Scholar
  85. Lemoine R, Kühn C, Thiele N, Delrot S and Frommer WB (1996) Antisense inhibition of the sucrose transporter in potato: effects on amount and activity. Plant Cell Environ 19: 1124–1131CrossRefGoogle Scholar
  86. Frommer WB (1999) Identification of a pollen-specific sucrose transporter-like protein NtSUT3 from tobacco. FEBS Lett 454: 325–330PubMedCrossRefGoogle Scholar
  87. Lu JM-Y and Bush DR (1998) His-65 in the proton--sucrose symporter is an essential amino acid whose modification with site-directed mutagenesis increase transport activity. Proc Natl Acad Sci USA 95: 9025–9030PubMedCrossRefGoogle Scholar
  88. Ludwig A, Stolz J and Sauer N (2000) Plant sucrose-H+ symporters mediate the transport of vitamin H. Plant J 24: 503–509PubMedCrossRefGoogle Scholar
  89. Ma Y, Baker F, Magallanes-Lundback M, DellaPenna D and Braun DM (2008) Tie-dyed1 and Sucrose export defevtive1 act independently to promote carbohydrate export from maize leaves. Planta 227: 527–538PubMedCrossRefGoogle Scholar
  90. Ma Y, Slewinski TL, Baker RF and Braun DM (2009) Tie-dyed1 encodes a novel phloem-expressed transmembrane protein that functions in carbohydrate partitioning. Plant Physiol 149: 181–194PubMedCrossRefGoogle Scholar
  91. Marger MD and Saier MH Jr (1993) A major superfamily of trans-membrane facilitators that catalyze uniport, symport and antiport. Trends Biochem Sci 18: 13–20PubMedCrossRefGoogle Scholar
  92. Matsukura C, Saitoh T, Hirose T, Ohsugi R, Perata P and Yamaguchi J (2000) Sugar uptake and transport in rice embryo. Expression of companion cell-specific sucrose transporter (OsSUT1) induced by sugar and light. Plant Physiol 124: 85–93PubMedCrossRefGoogle Scholar
  93. M’Batchi B and Delrot S (1988) Stimulation of sugar exit from leaf tissues of Vicia faba L. Planta 174: 340–348CrossRefGoogle Scholar
  94. McCaskill A and Turgeon R (2007) Phloem loading in Verbascum phoeniceum L. depends on the synthesis of raffinose-family oligosaccharides. Proc Natl Acad Sci USA 104: 19619–19624PubMedCrossRefGoogle Scholar
  95. Meyer S, Melzer M, Truernit E, Hümmer C, Besenbeck, Stadler R and Sauer N (2000) AtSUC3, a gene encoding a new Arabidopsis sucrose transporter, is expressed in cells adjacent to the vascular tissue and in a carpel cell layer. Plant J 24: 869–882PubMedCrossRefGoogle Scholar
  96. Meyer S, Lauterbach C, Niedermeier M, Barth I, Sjolund RD and Sauer N (2004) Wounding enhances expression of AtSUC3, a sucrose transporter from Arabidopsis sieve elements and sink tissues. Plant Physiol 134: 684–693PubMedCrossRefGoogle Scholar
  97. Minchin PEH and Lacointe A (2005) New understanding on phloem physiology and possible consequences for modeling long-distance carbon transport. New Phytol 166: 771–779PubMedCrossRefGoogle Scholar
  98. Neubohn B, Gubatz S, Wobus U and Weber H (2000) Sugar levels altered by ectopic expression of a yeast-derived invertase affect cellular differentiation of developing cotyledons of Vicia narbonensis L. Planta 211: 325–334PubMedCrossRefGoogle Scholar
  99. Noiraud N, Delrot S and Lemoine R (2000) The sucrose transporter of celery. Identification and expression during salt stress. Plant Physiol 122: 1447–1455PubMedCrossRefGoogle Scholar
  100. Noiraud N, Maurousset L and Lemoine R (2001) Transport of polyols in higher plants. Plant Physiol Biochem 39: 717–728CrossRefGoogle Scholar
  101. Ohshima T, Hayashi H and Chino M (1990) Collection and chemical composition of pure phloem sap from Zea mays L.. Plant Cell Physiol 31: 735–737Google Scholar
  102. Oliver SN, Van Dongen J, Alfred SC, Mamun EA, Zhao X, Saini HS, Fernandes SF, Blanchard CL, Sutton BG, Geigenberger P, Dennis ES and Dolferus R (2005) Cold-induced repression of the rice anther-specific cell wall invertase gene OsINV4 is correlated with sucrose accumulation and pollen sterility. Plant Cell Environ 28:1534–1541CrossRefGoogle Scholar
  103. Oparka KJ and Roberts AG (2001) Plasmodesmata: a not so open-and-shut case. Plant Physiol 125: 123–126PubMedCrossRefGoogle Scholar
  104. Oparka KJ, Duckett CM, Prior DAM and Fisher DB (1994) Real-time imaging of phloem unloading in the root tip of Arabidopsis. Plant J 6: 759–766CrossRefGoogle Scholar
  105. Oparka, K.J., Prior, D.A.M. and Wright, K.M. (1995) Symplastic communication between primary and developing lateral roots of Arabidopsis thaliana. J Exp Bot 46: 187–198CrossRefGoogle Scholar
  106. Oparka KJ, Roberts AG, Boevink P, Santa Cruz S, Roberts I, Pradel KS, Imlau A, Kotlizky G, Sauer N and Epel B (1999) Simple, but not branched, plasmodesmata allow the nonspecific trafficking of proteins in developing tobacco leaves. Cell 97: 743–754PubMedCrossRefGoogle Scholar
  107. Patrick JW and Offler CE (1995) Post-sieve element transport of sucrose in developing seeds. Aust J Plant Physiol 22: 681–702CrossRefGoogle Scholar
  108. Patrick JW and Offler CE (1996) Post-sieve element transport of photoassimilate in sink regions. J Exp Bot 47: 1165–1177PubMedCrossRefGoogle Scholar
  109. Porfirova S, Bergmüller E, Tropf S, Lemke R and Dörmann P (2002) Isolation of an Arabidopsis mutant lacking vitamin E and identification of a cyclase essential for all tocopherol biosynthesis. Proc Natl Acad Sci USA 99: 12495–12500PubMedCrossRefGoogle Scholar
  110. Provencher LM, Miao L, Sinha N and Lucas WJ (2001) Sucrose export defective1 encodes a novel protein implicated in chloroplast-to-nucleus signaling. Plant Cell 13: 1127–1141PubMedGoogle Scholar
  111. Rae AL, Perroux JM and Grof CPL (2005) Sucrose partitioning between vascular bundles and storage parenchyma in the sugarcane stem: a potential role for the ShSUT1 sucrose transporter. Planta 220: 817–825PubMedCrossRefGoogle Scholar
  112. Reinders A, Schulze W, Kuhn C, Barker L, Schulz A, Ward JM and Frommer WB (2002) Protein-protein interactions between sucrose transporters of different affinities colocalized in the same enucleate sieve element. Plant Cell 14: 1567–1577PubMedCrossRefGoogle Scholar
  113. Reinders A, Sivitz AB, His A, Grof CP, Perroux JM and Ward JM (2006) Sugarcane ShSUT1: analysis of sucrose transport activity and inhibition by sucralose. Plant Cell Environ 29: 1871–1880PubMedCrossRefGoogle Scholar
  114. Reinders A, Sivitz A, Starker CG, Gantt JS and Ward JM (2008) Functional analysis of LjSUT4, a vacuolar sucrose transporter from Lotus japonicus. Plant Mol Biol 68: 289–299PubMedCrossRefGoogle Scholar
  115. Riesmeier JW, Willmitzer L and Frommer WB (1992) Isolation and characterization of sucrose carrier cDNA from spinach by functional expression in yeast. EMBO J 11: 4705–4713PubMedGoogle Scholar
  116. Riesmeier JW, Hirner B and Frommer WB (1993) Potato sucrose transporter expression in minor veins indicates a role in phloem loading. Plant Cell 5: 1591–1598PubMedGoogle Scholar
  117. Riesmeier JW, Willmitzer L and Frommer WB (1994) Evidence for an essential role of the sucrose transporter in phloem loading and assimilate partitioning. EMBO J 13: 1–7PubMedGoogle Scholar
  118. Roberts AG and Oparka KJ (2003) Plasmodesmata and the control of symplastic transport. Plant Cell Environ 26: 103–124CrossRefGoogle Scholar
  119. Roblin G, Sakr S, Bonmort J and Delrot S (1998) Regulation of a plasma membrane sucrose transporter by phosphorylation. FEBS Lett 424: 165–168PubMedCrossRefGoogle Scholar
  120. Roitsch T and Tanner W (1996) Cell wall invertase: bridging the gap. Bot Acta 109: 90–93Google Scholar
  121. Roitsch T, Balibrea ME, Hofmann M, Proels R and Sinha AK (2003) Extracellular invertase: key metabolic enzyme and PR protein. J Exp Bot 54: 513–524PubMedCrossRefGoogle Scholar
  122. Ruan Y-L and Patrick JW (1995) The cellular pathway of postphloem sugar transport in developing tomato fruit. Planta 196: 434–444CrossRefGoogle Scholar
  123. Ruan Y-L, Llewellyn DJ and Furbank RT (2000) Pathway and control of sucrose import into initiating cotton fibre cells. Aust J Plant Physiol 27: 795–800Google Scholar
  124. Ruan Y-L, Llewellyn DJ and Furbank RT (2001) The control of single-celled cotton fibre elongation by developmentally reversible gating of plasmodesmata and coordinated expression of sucrose and K+ transporters and expansin. Plant Cell 13: 47–60PubMedGoogle Scholar
  125. Ruan Y-L, Xu S-M, White R and Furbank RT (2004) Genotypic and developmental evidence for the role of plasmodesmatal regulation in cotton fiber elongation mediated by callose turnover. Plant Physiol 136: 4104–4113PubMedCrossRefGoogle Scholar
  126. Ruan YL, Llewellyn DJ, Furbank RT and Chourey PS (2005) The delayed initiation and slow elongation of fuzz-like short fibre cells in relation to altered pattern of sucrose synthase expression and plasmodesmata gating in a lintless mutant of cotton, J Ex Bot 56: 977–984CrossRefGoogle Scholar
  127. Russin WA, Evert RF, Vanderveer PJ, Sharkey TD and Briggs SP (1996) Modification of a specific class of plasmodesmata and loss of sucrose export ability in the sucrose export defective1 maize mutant. Plant Cell 8: 645–658PubMedGoogle Scholar
  128. Ruuska SA, Girke T, Benning C and Ohlrogge JB (2002) Contrapuntal networks of gene expression during Arabidopsis seed filling. Plant Cell 14: 1191–1206PubMedCrossRefGoogle Scholar
  129. Saier MH Jr (2000) Families of transmembrane sugar transport proteins. Mol Microbiol 35: 699–710PubMedCrossRefGoogle Scholar
  130. Sattler SE, Cahoon EB, Coughlan SJ and DellaPenna D (2003) Characterization of tocopherol cyclases from higher plants and cyanobacteria. Evolutionary implications for tocopherol synthesis and function. Plant Physiol 132: 2184–2195PubMedCrossRefGoogle Scholar
  131. Sauer N (2007) Molecular physiology of higher plant sucrose transporter. FEBS Lett. 581: 2309–2317PubMedCrossRefGoogle Scholar
  132. Sauer N and Stolz J (1994) SUC1 and SUC2: two sucrose transporters from Arabidopsis thaliana; expression and characterization in baker’s yeast and identification of the histidine-tagged protein. Plant J 6: 67–77PubMedCrossRefGoogle Scholar
  133. Sauer N, Ludwig A, Knoblauch A, Rothe P, Gahrtz M and Klebl F (2004) AtSUC8 and AtSUC9 encode functional sucrose transporters, but the closely related AtSUC6 and AtSUC7 genes encode aberrant proteins in different Arabidopsis ecotypes. Plant J 40: 120–130PubMedCrossRefGoogle Scholar
  134. Schnyder H (1993) The role of carbohydrate storage and redistribution in the source-sink relations of wheat and barley during grain filling - a review. New Phytol 123: 233–245CrossRefGoogle Scholar
  135. Schobert C, Lucas WJ, Franceschi VR and Frommer WB (2000) Intercellular transport and phloem loading of sucrose, oligosaccharides and amino acids. In: Leegood RC, Sharkey TD and von Caemmerer S (eds) Photosynthesis: Physiology and Metabolism, Advances in Photosynthesis, Vol 9, pp 249–274. Kluwer Academic Publishers, DordrechtCrossRefGoogle Scholar
  136. Schulze W, Weise A, Frommer WB and Ward JM (2000) Function of the cytosolic N-terminus of sucrose transporter AtSUT2 in substrate affinity. FEBS Lett 485: 189–194PubMedCrossRefGoogle Scholar
  137. Schulze WX, Reinders A, Ward J, Lalonde S and Frommer WB (2003) Interactions between co-expressed Arabidopsis sucrose transporters in the split-ubiquitin system. BMC Biochem 4: 3PubMedCrossRefGoogle Scholar
  138. Scofield GN, Hirose T, Gaudron JA, Upadhyaya NM, Ohsugi R and Furbank RT (2002) Antisense suppression of the rice sucrose transporter gene, OsSUT1, leads to impaired grain filling and germination but does not affect photosynthesis. Funct Plant Biol 29: 815–826CrossRefGoogle Scholar
  139. Scofield GN, Aoki N, Hirose T, Takano M, Jenkins CLD and Furbank RT (2007a) The role of the sucrose transporter, OsSUT1, in germination and early seedling growth and development of rice plants. J Exp Bot 58: 483–495PubMedCrossRefGoogle Scholar
  140. Scofield GN, Hirose T, Aoki N and Furbank RT (2007b) Involvement of the sucrose transporter, OsSUT1, in the long-distance pathway for assimilate transport in rice. J Exp Bot 58: 3155–3169PubMedCrossRefGoogle Scholar
  141. Scofield GN, Ruuska SA, Aoki N, Lewis DC, Tabe LM and Jenkins CLD (2009) Starch storage in the stems of wheat plants: localization and temporal changes. Ann Bot 103: 859–868Google Scholar
  142. Sheoran IS and Saini HS (1996) Drought-induced male sterility in rice: changes in carbohydrate levels and enzyme activities associated with the inhibition of starch accumulation in pollen. Sex Plant Reprod 9: 161–169CrossRefGoogle Scholar
  143. Sivitz AB, Reinders A and Ward JM (2005) Analysis of the transport activity of barley sucrose transporter HvSUT1. Plant Cell Physiol 46: 1666–1673PubMedCrossRefGoogle Scholar
  144. Sivitz AB, Reinders A and Ward JM (2008) Arabidopsis sucrose transporter AtSUC1 is important for pollen germination and sucrose induced anthocyanin accumulation. Plant Physiol 147: 92–100CrossRefGoogle Scholar
  145. Slewinski TL, Meeley R and Braun DM (2009) Sucrose transpoter1 functions in phloem loading in maize leaves. J Exp Bot 60: 881–892Google Scholar
  146. Slewinski TL, Ma Y, Baker F, Huang M, Meeley R and Braun DM (2008) Determining the role of Tie-dyed1 in starch metabolism: epistasis analysis with maize ADP-Glucose pyrophosphorylase mutant lacking leaf starch. J Hered 99: 661–666PubMedCrossRefGoogle Scholar
  147. Sonnewald U, Brauer M, von Schaewen A, Stitt M and Willmitzer L (1991) Transgenic tobacco plants expressing yeast-derived invertase in either the cytosol, vacuole or apoplast: a powerful tool for studying sucrose metabolism and sink/source interactions. Plant J 1: 95–106PubMedCrossRefGoogle Scholar
  148. Sonnewald U, Hajirezaei MR, Kossmann J, Heyer A, Trethewey RN and Willmitzer L (1997) Increased potato tuber size resulting from expression of a yeast invertase. Nat Biotechnol 15: 794–797PubMedCrossRefGoogle Scholar
  149. Sreenivasulu N, Altschmied L, Radchuk V, Gubatz S, Wobus U and Weschke W (2004) Transcript profiles and deduced changes of metabolic pathways in maternal and filial tissues of developing barley grains. Plant J 37: 539–553PubMedCrossRefGoogle Scholar
  150. Stadler R, Brandner J, Schulz A, Gahrtz M and Sauer N (1995) Phloem loading by the PmSUC2 sucrose carrier from Plantago major occurs into companion cells. Plant Cell 7: 1545–1554PubMedGoogle Scholar
  151. Stadler R, Truernit E, Gahrtz M and Sauer N (1999) The AtSUC1 sucrose carrier may represent the osmotic driving force for anther dehiscence and pollen tube growth in Arabodopsis. Plant J 19: 269–278PubMedCrossRefGoogle Scholar
  152. Takahashi S, Ishimaru K, Yazaki J, Fujii F, Shimbo K, Yamamoto K, Sakata K, Sasaki T, Kishimoto N and Kikuchi S (2005) Microarray analysis of sink-source transition in rice leaf sheaths. Breed Sci 55: 153–162CrossRefGoogle Scholar
  153. Takeda T, Toyofuku K, Matsukura C and Yamaguchi J (2001) Sugar transporters involved in flowering and grain development of rice. J Plant Physiol 158: 465–470CrossRefGoogle Scholar
  154. Tegeder M, Wang X-D, Frommer WB, Offler CE and Patrick JW (1999) Sucrose transport into developing seeds of Pisum sativum L. Plant J 18: 151–161PubMedCrossRefGoogle Scholar
  155. Thompson RG and Dale JE (1981) Export of 14C- and 11C-labelled assimilate from wheat and maize leaves: effects of parachloromercuribenzylsulphonic acid and fusicoccin and of potassium deficiency. Can J Bot 59: 2439–2444CrossRefGoogle Scholar
  156. Thorpe MR and Minchin PEH (1996) Mechanism of long and short distance transport from sources to sinks. In: Zamski E and Schaffer AA (eds) Photoassimilate Distribution in Plants and Crops: Source and Sink Relations, pp 261–282. Marcel Dekker, New YorkGoogle Scholar
  157. Tomlinson KL, McHugh S, Labbe H, Grainger JL, James LE, Pomeroy KM, Mullin JW, Miller SS, Dennis DT and Miki BL (2004) Evidence that the hexose-to-sucrose ratio does not control the switch to storage product accumulation in oilseeds: analysis of tobacco seed development and effects of overexpressing apoplastic invertase. J Exp Bot 55: 2291–2303PubMedCrossRefGoogle Scholar
  158. Turgeon R (1991) Symplastic phloem loading and the sink-source transition in leaves: A model. In: Bonnemain J-L, Delrot S, Lucas WJ and Dainty J (eds) Recent Advances in Phloem Transport and Assimilate Compartmentation, pp 18–22. Ouest Editions, NantesGoogle Scholar
  159. Turgeon R and Gowan E (1990) Phloem loading in Coleus blumei in the absence of carrier-mediated uptake of export sugar from apoplast. Plant Physiol 94: 1244–1249PubMedCrossRefGoogle Scholar
  160. Turgeon R and Medville (1998) The absence of phloem loading in willow leaves. Proc Natl Acad Sci USA 95: 12055–12060PubMedCrossRefGoogle Scholar
  161. Turgeon R and Medville R (2004) Phloem loading. A reevaluation of the relationship between plasmodesmatal frequencies and loading strategies. Plant Physiol 136: 3795–3803PubMedCrossRefGoogle Scholar
  162. Turgeon R and Wolf S (2008) Phloem transport: cellular pathway and molecular trafficking. Ann Rev Plant Biol 60: 207–221CrossRefGoogle Scholar
  163. Van Bel AJE (1993) Strategies of phloem loading. Ann Rev Plant Physiol Plant Mol Biol 44: 253–281CrossRefGoogle Scholar
  164. Van Bel AJE (1995) The low-profile directors of carbon and nitrogen economy in plants: parenchyma cells associated with translocation channels. In: Gartner BL (ed) Plant Stems: Physiology and Functional Morphology, pp 205–222. Academic Press, San DiegoGoogle Scholar
  165. Van Bel AJE (2003) The phloem, a miracle of ingenuity. Plant Cell Environ 26: 125–149CrossRefGoogle Scholar
  166. Van Bel AJE and Hess PH (2008) Hexoses as phloem transport sugars: the end of dogma? J Exp Bot 59: 261–272PubMedCrossRefGoogle Scholar
  167. Van Bel AJE, Gamalei YV, Ammerlaan A and Bik LPM (1992) Dissimilar phloem loading in leaves with symplasmic or apoplasmic minor-vein configurations. Planta 186: 518–525CrossRefGoogle Scholar
  168. Van Bel AJE, Ammerlaan A and Van Dijk AA (1994) A three-step screening procedure to identify the mode of phloem loading in intact leaves. Planta 192: 31–39Google Scholar
  169. Van den Ende W, Clerens S, Vergauwen R, Van Riet L, Van Laere A Yoshida M and Kawakami A (2003) Fructan 1-exohydrolases. β-(2,1)-Trimmers during graminan biosynthesis in stems of wheat? Purification, characterization, mass mapping and cloning of two fructan 1-exohydrolase isoforms. Plant Physiol 131: 621–631CrossRefGoogle Scholar
  170. Vilhar B, Kladnik A, Blejec A, Chourey PS and Dermastia M (2002) Cytometrical evidence that the loss of seed weight in the miniature1 seed mutant of maize is associated with reduced mitotic activity in the developing endosperm. Plant Physiol 129: 23–30PubMedCrossRefGoogle Scholar
  171. Viola R, Roberts AG, Haupt S, Gazzani S, Hancock RD, Marmiroli N, Marchray N and Oparka KJ (2001) Tuberization in potato involves a switch from apoplastic to symplastic phloem unloading. Plant Cell 13: 385–398PubMedGoogle Scholar
  172. Walsh KB, Sky C and Brown SM (1996) Pathway of sucrose unloading from the phloem in sugarcane stalk. In: Wilson JR, Hogarth DM, Campbell JA and Garside AL (eds) Sugarcane: Research Towards Efficient and Sustainable Production, pp 105–107. CSIRO Division of Tropical Crops and Pastures, BrisbaneGoogle Scholar
  173. Wardlaw IF and Willenbrink J (2000) Mobilization of fructan reserves and changes in enzyme activities in wheat stems correlate with water stress during kernel filling. New Phytol 148: 413–422CrossRefGoogle Scholar
  174. Weber H, Borisjuk L, Sauer N and Wobus U (1997) A role for sucrose transporters during seed development: molecular characterization of a hexose and a sucrose carrier in Faba bean seeds. Plant Cell 9: 895–908PubMedCrossRefGoogle Scholar
  175. Weber H, Heim U, Golombek S, Borisjuk L, Manteuffel R and Wobus U (1998) Expression of a yeast-derived invertase in developing cotyledons of Vicia narbonensis alters the carbohydrate state and affects storage functions. Plant J 16: 163–172PubMedCrossRefGoogle Scholar
  176. Weise A, Barker L, Kühn C, Lalonde S, Buschmann H, Frommer WB and Ward JM (2000) A new subfamily of sucrose transporters, SUT4, with low affinity/high capacity localized in enucleate sieve elements of plants. Plant Cell 12: 1345–1355PubMedGoogle Scholar
  177. Weschke W, Panitz R, Sauer N, Wang Q, Neubohn B, Weber H and Wobus U (2000) Sucrose transport into barley seeds: molecular characterization of two transporters and implications for seed development and starch accumulation. Plant J 21: 455–467PubMedCrossRefGoogle Scholar
  178. Weschke W, Panitz R, Gubatz S, Wang Q, Radchuk R, Weber H and Wobus U (2003) The role of invertases and hexose transporters in controlling sugar ratios in maternal and filial tissues of barley caryopses during early development. Plant J 33: 395–411PubMedCrossRefGoogle Scholar
  179. Willenbrink J (2002) Assimilate transport in phloem: regulation and mechanism. Russ J Plant Physiol 49: 8–15CrossRefGoogle Scholar
  180. Williams LE, Lemoine R and Sauer N (2000) Sugar transporters in higher plants - a diversity of roles and complex regulation. Trends Plant Sci 5: 283–290PubMedCrossRefGoogle Scholar
  181. Winter H, Lohaus G and Heldt HW (1992) Phloem transport of amino acids in relation to cytosolic levels in barley leaves. Plant Physiol 99: 996–1004PubMedCrossRefGoogle Scholar
  182. Zhou Y, Qu H, Dibley KE, Offler CE and Patrick JW (2007) A suite of sucrose transporters expressed in coats of developing legume seeds includes novel pH-independent facilitators. Plant J 49: 750–764PubMedCrossRefGoogle Scholar
  183. Zimmermann MH and Ziegler H (1975) List of sugars and sugar alcohols in sieve-tube exudates. In: Zimmermann MH and Milburn JA (eds) Encyclopedia of Plant Physiology, New Series Vol 1, Transport in Plants 1, Phloem Transport, pp 480–503. Springer, New YorkGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Naohiro Aoki
    • 1
    • 2
  • Tatsuro Hirose
    • 3
  • Robert T. Furbank
    • 1
  1. 1.CSIRO Plant IndustryCanberraAustralia
  2. 2.Graduate School of Agricultural and Life SciencesThe University of TokyoTokyoJapan
  3. 3.National Agricultural Research CenterJoetsuJapan

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