Advertisement

Intracellular And Intercellular Transport Of Nitrogen And Carbon

  • Gertrud Lohaus
  • Karsten Fischer
Chapter
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 12)

Summary

Partitioning of carbon (C) and nitrogen (N) assimilates and export of photoassimilates play an essential role in efficient growth and reproductive success of the plant as well as in crop yield. Sink (net importing) organs need to be supplied with energy and fixed C from the source (net exporting) organs of the plant, e.g. green leaves. During the day, the triose phosphate/phosphate translocator located in the inner membrane of chloroplast envelopes catalyzes the export of triose phosphates, the main product of photosynthesis, to the cytosol of the plant cell where they are used in sucrose synthesis. Some sucrose is stored in source tissues, but the bulk is exported. Sucrose is the major form of exported C from leaves. When the rates of sucrose synthesis and export fall behind that of CO2 fixation, fixed C is retained in the chloroplasts and directed into the synthesis of transitory starch. At night, starch is degraded to glucose that is exported from chloroplasts via a glucose transporter. Triose phosphates also provide skeletons for amino acid synthesis. From the source organs organic C and N metabolites are transported via the phloem to sink organs. The most abundant sugar in the phloem sap of several plant species is sucrose, with concentrations being about 1 M. Total amino acid concentrations are between 50 and 500 mM. Two principal routes for the delivery of metabolites into the sieve-element-companion cell complex (SE-CCC) have been proposed. These are (i) transporter-mediated export from mesophyll cells, diffusion through the apoplast, and subsequent transporter-mediated uptake into the SE-CCC, and (ii) direct symplastic cell-to-cell diffusion via plasmodesmata. Several sucrose and amino acid transporters have been cloned which mediate the uptake of the photoassimilates from the apoplast into the symplast. This chapter gives an overview of the current state of knowledge on the functions of intracellular and intercellular metabolite transport in leaves.

Abbreviations

2-PGA — 2-phosphoglycerate 3-PGA — 3-phosphoglycerate ADP-Glc — ADP glucose AGPase — ADP glucose pyrophosphorylase; C3 — three carbon C4 — four carbon CCCP — carbonyl cyanide m-chlorophenyl hydrazone D-Glc — D-glucose DIT1 — oxoglutarate/malate translocator D-Man — D-mannose E4P — erythrose 4-P FBPase — fructose 1,6-bisphosphatase Fru2, 6bP — fructose 2,6-bisphosphate Glc lP — glucose 1-phosphate Glc6P — glucose 6-phosphate GPT — Glc6P/phosphate translocator OAA — oxaloacetate OPPP — oxidative pentose phosphate pathway PCMBS — p-chloromercuribenzenesulfonic acid PEP — phosphoenolpyruvate PGI — phosphoglucoisomerase pGlcT — plastidic glucose translocator PGM — phosphoglucomutase P1 — Inorganic phosphate PPT — PEP/phosphate translocator R5P — ribose 5-P RPP — reductive pentose phosphate (RPP pathway = Calvin cycle) SE-CCC — sieve-element-companion cell complex SEL — size exclusion limit TP — triose phosphate TPT — trioscphosphate/phosphate translocator 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

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: 177–185Google 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: 1072–1078PubMedGoogle Scholar
  3. Bagge P and Larsson C (1986) Biosynthesis of aromatic amino acids by highly purified spinach chloroplasts—Compartmentation and regulation of the reactions. Physiol Plant 68: 641–647Google Scholar
  4. Baldry CW, Bucke C and Walker DA (1966) Incorporation of inorganic phosphate into sugar phosphates during carbon dioxide fixation by illuminated chloroplasts. Nature 210: 793–796Google Scholar
  5. 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: 1153–1164CrossRefPubMedGoogle Scholar
  6. Barker SA (1955) Acyclic sugar alcohols. In: Peach K and Tracey MV (eds) Modern Methods of Plant Analysis, Vol. 2, pp 158–192. Springer Verlag, BerlinGoogle Scholar
  7. Barlow CA and McCully ME (1972) The ruby laser as an instrument for cutting the stylets of feeding aphids. Can J Zool 50: 1497–1499Google Scholar
  8. Bassham JA, Kirk M and Jensen RG (1968) Photosynthesis by isolated chloroplasts. I. Diffusion of labeled photosynthetic intermediates between isolated chloroplasts and suspending medium. Biochim Biophys Acta 153: 211–218PubMedGoogle Scholar
  9. Batz O, Scheibe R and Neuhaus HE (1992) Transport processes and corresponding changes in metabolite levels in relation to starch synthesis in barley etioplasts. Plant Physiol 100: 184–190Google Scholar
  10. Boorer KJ, Frommer WB, Bush DB, Kreman M, Loo DDF and Wright EM (1996a) Kinetics and specificity of a H+/amino acid transporter from Arabidopsis thaliana. J Biol Chem 271: 2213–2220PubMedGoogle Scholar
  11. Boorer KJ, Loo DDF, Frommer WB and Wright EM (1996b) Transport mechanism of the cloned H+/sucrose transporter StSUT 1. J Biol Chem 271: 25139–25144PubMedGoogle Scholar
  12. Borchert S, Grosse H and Heldt HW (1989) Specific transport of inorganic phosphate, glucose 6-P, dihydroxyacetone phosphate and 3-phosphoglycerate into amyloplasts from pea roots. FEBS Lett 253: 183–186CrossRefGoogle Scholar
  13. Borchert S, Harborth J, Schünemann D, Hoferichter P and Heldt HW (1993) Studies of the enzymic capacities and properties of pea root plastids. Plant Physiol 101: 303–312PubMedGoogle Scholar
  14. Bouché-Pillon S, Fleurat-Lessard P, Fromont JC, Serrano R and Bonnemain JL (1994) Immunolocalization of the plasma membrane-ATPase in minor veins of Vicia faba in relation to phloem loading. Plant Physiol 105: 691–697PubMedGoogle Scholar
  15. Bowsher CG, Hucklesby DB and Ernes MJ (1989) Nitrite reduction and carbohydrate metabolism in plastids purified from roots of Pisum sativum. Planta 177: 359–366CrossRefGoogle Scholar
  16. Bowsher CG, Boulton EL, Rose J, Nayagam S and Emes MJ (1992) Reductant for glutamate synthase is generated by the oxidative pentose phosphate pathway in non-photosynthetic root plastids. Plant J 2: 893–898CrossRefGoogle Scholar
  17. Büker M, Schünemann D and Borchert S (1998) Enzymic properties and capacities of developing tomato fruit plastids. J Exp Bot 49: 681–691Google Scholar
  18. Bürkle L, Hibberd JM, Quick WP, Kühn C, Hirner B and Frommer WB (1998) The H+-sucrose co-transporter NtSUT 1 is essential for sugar export from tobacco leaves. Plant Physiol 118: 59–68PubMedGoogle Scholar
  19. Caspar T, Huber SC and Somerville CR (1986) Alterations in growth, photosynthesis and respiration in a starchless mutant of Arabidopsis thaliana deficient in chloroplast phosphoglucomutase. Plant Physiol 79: 11–17Google Scholar
  20. Caspar T, Lin TP, Monroe J, Benbow L, Preiss J and Somerville CR (1991) Mutantsof Arabidopsis with altered regulation of starch degradation. Plant Physiol 95: 1181–1188Google Scholar
  21. Chen BY, Wang Y and Janes HW (1998) ADP-Glucose pyrophosphorylase is localized to both the cytoplasm and plastids in developing pericarp of tomato fruit. Plant Physiol 116: 101–106CrossRefPubMedGoogle Scholar
  22. Chen L and Bush DR (1997) LHT1, a lysine and histidine specific amino acid transporter in Arabidopsis. Plant Physiol 115: 1127–1134CrossRefPubMedGoogle Scholar
  23. Cockburn W, Baldry CW and Walker DA (1967) Some effects of inorganic phosphate on O2 evolution by isolated chloroplasts. Biochim Biophys Acta 143: 614–624PubMedGoogle Scholar
  24. Cognata UL, Willmitzer L and Müller-Röber B (1995) Molecular cloning and characterization of novel isoforms of potato ADP-glucose pyrophosphorylase. Mol Gen Genet 246: 538–548CrossRefPubMedGoogle Scholar
  25. Davies C, Wolf T and Robinson SP (1999) Three putative sucrose transporters are differentially expressed in grapevine tissue. Plant Sci 147: 93–100CrossRefGoogle Scholar
  26. Davis JM and Loescher WH (1990) [4C]-Assimilate translocation in the light and dark in celery (Apium graveolens) leaves of different ages. Physiol Plant 79: 656–662CrossRefGoogle Scholar
  27. Day DA and Hatch MD (1981) Transport of 3-phosphoglyceric acid, phosphoenolpyruvate, and inorganic phosphate in maize mesophyll chloroplasts and the effect of 3-phosphoglyceric acid on malate and phosphoenolpyruvate production. Arch Biochem Biophys 211: 743–749PubMedGoogle Scholar
  28. Denyer K, Dunlap F, Thorbjörnsen T, Keeling P and Smith AM (1996) The major form of ADP-glucose pyrophosphorylase in maize endosperm is extra-plastidial. Plant Physiol 112: 779–785CrossRefPubMedGoogle Scholar
  29. Eastmond PJ and Rawsthorne S (2000) Coordinate changes in carbon partitioning and plastidial metabolism during the development of oilseed rape. Plant Physiol 122: 767–774CrossRefPubMedGoogle Scholar
  30. Eastmond PJ, Dennis DT and Rawsthorne S (1997) Evidence that a malate/phosphate exchange translocator imports carbon across the leucoplast envelope for fatty acid synthesis in developing castor seed endosperm. Plant Physiol 114: 851–856PubMedGoogle Scholar
  31. Emes MJ and Neuhaus HE (1997) Metabolism and transport in non-photosynthetic plastids. J Exp Bot 48: 1995–2005CrossRefGoogle Scholar
  32. Entwistle G and ap Rees T (1988) Enzymatic capacities of amyloplasts from wheat endosperm. Biochem J 255: 391–396PubMedGoogle Scholar
  33. Entwistle G and ap Rees T (1990) Lack of fructose-1,6-bisphosphatase in a range of higher plants that store starch. Biochem J 271: 467–472PubMedGoogle Scholar
  34. Eschrich W, Evert RF and Heyser W (1971) Proteins of the sievetube exudate of Cucurbita maxima. Planta 100: 208–221CrossRefGoogle Scholar
  35. Evert RF, Russin WA and Bosabalidis AM (1996) Anatomical and ultrastructural changes associated with sink-to-source transition in developing maize leaves. Int J Plant Sci 157:247–261CrossRefGoogle Scholar
  36. Fischer K, Arbinger B, Kammerer B, Busch C, Brink S, Wallmeier H, Sauer N, Eckerskorn C and Flügge UI (1994) Cloning and in vivo expression of functional triose phosphate/phosphate translocators from and C3-and C4-plants: Evidence for the putative participation of specific amino acid residues in the recognition of phosphoenolpyruvate. Plant J 5: 215–226CrossRefPubMedGoogle Scholar
  37. Fischer K, Kammerer B, Gutensohn M, Arbinger B, Weber A, Häusler R and Flügge UI (1997) A new class of plastidic phosphate translocators: A putative link between primary and secondary metabolism by phosphoenolpyruvate/phosphate antiporter. Plant Cell 9: 453–462PubMedGoogle Scholar
  38. Fischer W-N, Kwart M, Hummel S and Frommer WB (1995) Substrate specificity and expression profile of amino acid transporters (AAPs) in Arabidopsis. J Biol Chem 270:16315–16320PubMedGoogle Scholar
  39. Fischer W-N, André B, Rentsch D, Krolkiewicz S, Tegeder M, Breitkreuz K and Frommer WB (1998) Amino acid transport in plants. Trends Plant Sci 3: 188–195CrossRefGoogle Scholar
  40. Fisher DB and Frame JM (1984) A guide to the use of the exuding-stylet technique in phloem physiology. Planta 161: 385–393CrossRefGoogle Scholar
  41. Fisher DB, Wu Y and Ku MSB (1992) Turnover of soluble proteins in the wheat sieve tube. Plant Physiol 100: 1433–1441Google Scholar
  42. Fliege R, Flügge UI, Werdan K and Heldt HW (1978) Specific transport of inorganic phosphate, 3-phosphoglycerate and triosephosphates across the inner membrane of the envelope in spinach chloroplasts. Biochim Biophys Acta 502: 232–247PubMedGoogle Scholar
  43. Flora LL and Madore MA (1993) Stachyose and mannitol transport in olive (Olea europaea L.). Planta 189: 484–490CrossRefGoogle Scholar
  44. Flügge UI (1995) Phosphate translocation in the regulation of photosynthesis. J Exp Bot 46: 1317–1323Google Scholar
  45. Flügge UI (2000) Metabolite transport across the chloroplast envelope of C3-plants. In: Leegood RC, Sharkey TD and von Caemmerer S (eds) Photosynthesis: Physiology and Metabolism, pp 137–152. Kluwer Academic Publishers, DordrechtGoogle Scholar
  46. Flügge UI and Heldt HW (1984) The phosphate-triose phosphate-phosphoglycerate translocator of the chloroplasts. Trends Biochem Sci 9: 530–533Google Scholar
  47. Flügge UI, Stitt M and Heldt HW (1985) Light-driven uptake of pyruvate into mesophyll chloroplasts from maize. FEBS Lett 183: 335–339Google Scholar
  48. Flügge UI, Fischer K, Gross A, Sebald W, Lottspeich F and Eckerskorn C (1989) The triose phosphate-3-phosphoglycerate-phosphate translocator from spinach chloroplasts: Nucleotide sequence of a full-length cDNA clone and import of the in vitro synthesized precursor protein into chloroplasts. EMBO J 8: 39–46PubMedGoogle Scholar
  49. Flügge UI, Weber A, Fischer K, Häusler R and Kammerer B (1996) Molecular characterization of plastid transporters. C R Acad Sci Paris 319: 849–852Google Scholar
  50. Frommer WB, Hummel S and Riesmeier JW (1993) Expression cloning in yeast of a cDNA encoding a broad specificity amino acid permease from Arabidopsis thaliana. Proc Natl Acad Sci USA 90: 6160–6164PubMedGoogle Scholar
  51. 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: 697–706CrossRefPubMedGoogle Scholar
  52. Gamalei Y (1989) Structure and function of leaf minor veins in trees and herbs. A taxonomic review. Trees 3: 96–110Google Scholar
  53. Geiger DR, Giaquinta RT, Sovonick SA and Fellows RJ (1973) Solute distribution in sugar beet leaves in relation to phloem loading and translocation. Plant Physiol 52: 585–589Google Scholar
  54. Giaquinta RT (1977) Possible role of pH gradient and membrane ATPase in the loading of sucrose in the sieve tubes. Nature 267: 369–370CrossRefGoogle Scholar
  55. Giroux MJ and Hannah LC (1994) ADP-glucose pyrophos-phorylase in shrunken-2 and brittle-2 mutants of maize. Mol Gen Genet 243: 400–408PubMedGoogle Scholar
  56. Hall SM and Baker DA (1972) The chemical composition of Ricinus phloem exudate. Planta 106: 131–140.CrossRefGoogle Scholar
  57. Hanson KR and McHale NA (1988) A starchless mutant of Nicotiana sylvestris containing a modified plastid phospho-glucomutase. Plant Physiol 88: 838–844Google Scholar
  58. Harrington GN, Franceschi VR, Offler CE, Patrick JW, Harper JF, Frommer WB, Tegeder M and Hitz WD (1997) Cell specific expression of three genes involved in plasma membrane sucrose transport in developing Viciafaba seed. Protoplasma 197:35–50CrossRefGoogle Scholar
  59. Harrison CJ, Hedley CL and Wang TL (1998) Evidence that the rug3 locus of pea encodes plastidial phosphoglucomutase confirms that the imported substrate for starch synthesis in pea amyloplasts is glucose-6-phosphate. Plant J 13: 753–762CrossRefGoogle Scholar
  60. Harrison CJ, Mould RM, Leech MJ, Johnson SA, Turner L, Schreck SL, Baird KM, Jack PL, Rawsthorne S, Hedley CL and Wang TL (2000) The rug3 locus of pea encodes plastidial phosphoglucomutase. Plant Physiol 122: 1187–1192CrossRefPubMedGoogle Scholar
  61. Hatch MD, Dröscher L, Flügge UI and Heldt HW (1984) A specific translocator for oxaloacetate transport in chloroplasts. FEBS Lett 178: 15–19CrossRefGoogle Scholar
  62. Hatzfeld WD and Stitt M (1990) A study of the rate of recycling of triose phosphates in heterotrophic Chenopodium rubrum cells, potato tubers and maize endosperm. Planta 180: 198–204Google Scholar
  63. Häusler RE, Schlieben NH, Schulz B and Flügge UI (1998) Compensation of decreased triose phosphate/phosphate translocator activity by accelerated starch turnover and glucose transport in transgenic tobacco. Planta 204: 366–376PubMedGoogle Scholar
  64. Häusler RE, Schlieben NH, Nicolay P, Fischer K, Fischer KL and Flügge UI (2000) Control of carbon partitioning and photosynthesis by the triose phosphate/phosphate translocator in transgenic tobacco plants. I. Comparative physiological analysis of tobacco plants with antisense repression and overexpression of the triose phosphate/phosphate translocator. Planta 210: 371–382PubMedGoogle Scholar
  65. Hayashi H and Chino M (1985) Nitrate and other anions in the rice phloem sap. Plant Cell Physiol 26: 325–330Google Scholar
  66. Hayashi H and Chino M (1990) Chemical composition of phloem sap from the uppermost internode of the rice plant. Plant Cell Physiol 31: 247–251Google Scholar
  67. Heineke D, Kruse A, Flügge UI, Frommer WB, Riesmeier JW, Willmitzer L and Heldt HW (1994) Effect of antisense repression of the chloroplast triose phosphate translocator on photosynthetic metabolism in transgenic plants. Planta 193: 174–180CrossRefGoogle Scholar
  68. Heldt HW and Rapley L (1970) Specific transport of inorganic phosphate, 3-phospho-glycerate and dihydroxyacetone phosphate and of dicarboxylates across the inner membrane of spinach chloroplasts. FEBS Lett 10: 143–148CrossRefPubMedGoogle Scholar
  69. Hendrix DL and Huber SC (1986) Diurnal fluctuations in cotton leaf carbon export, carbohydrate content, and sucrose synthesizing enzymes. Plant Physiol 81: 584–586Google Scholar
  70. Herrmann KM and Weaver LM (1999) The shikimate pathway. Annu Rev Plant Physiol Plant Mol Biol 50: 473–503CrossRefPubMedGoogle Scholar
  71. Hill GP (1962) Exudation from aphid stylets during the period from dormancy to bud break in Tilia americana (L.). J Exp Bot 13: 144–151Google Scholar
  72. Hill LM and Smith AM (1991) Evidence that glucose 6-P is imported as the substrate for starch biosynthesis by the plastids of developing pea embryos. Planta 185: 91–96Google Scholar
  73. 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: 1389–1396PubMedGoogle Scholar
  74. Holthaus U and Schmitz K (1991) Distribution and immuno-localization of stachyose synthase in Cucumis melo L. Planta 185:4479–186CrossRefGoogle Scholar
  75. Huber SC and Edwards GE (1977a) Transport in C4-mesophyll chloroplasts. Characterization of a pyruvate carrier. Biochim Biophys Acta 462: 583–602PubMedGoogle Scholar
  76. Huber SC and Edwards GE (1977b) Transport in C4 mesophyll chloroplasts. Evidence for an exchange of inorganic phosphate and phosphoenolpyruvate. Biochim Biophys Acta 462: 603–612PubMedGoogle Scholar
  77. Jones TWA, Gottlieb LD and Pichersky E (1986) Reduced enzyme activity and starch level in an induced mutant of chloroplastic phosphoglucose isomerase. Plant Physiol 81: 367–371Google Scholar
  78. Journet EP and Douce R (1985) Enzynaic capacities of purified cauliflower bud plastids for lipid synthesis and carbohydrate metabolism. Plant Physiol 79: 458–467Google Scholar
  79. Kalt-Torres W, Kerr PS, Usuda H and Huber SC (1987) Diurnal changes in maize leaf photosynthesis. Carbon exchange rate, assimilate export rate, and enzyme activities. Plant Physiol 83: 283–288Google Scholar
  80. Kammerer B, Fischer K, Hilpert B, Schubert S, Gutensohn M, Weber A and Flügge UI (1998) Molecular characterization of a carbon transporter in plastids from heterotrophic tissues: The glucose-6-phosphate/phosphateantiporter. Plant Cell 10: 105–117CrossRefPubMedGoogle Scholar
  81. Kang F and Rawsthorne S (1994) Starch and fatty acid synthesis in plastids from developing embryos of oilseed rape. Plant J 6: 795–805CrossRefGoogle Scholar
  82. Keeling PL, Wood JR, Tyson RH and Bridges IG (1988) Starch biosynthesis in developing wheat grain. Plant Physiol 87: 311–319Google Scholar
  83. Kennecke K, Ziegler H and De Fekete MAR (1971) Enzymak-tivitäten im Siebröhrensaft von Robinia pseudoaccacia L. und anderen Baumarten, Planta 98:330–356CrossRefGoogle Scholar
  84. Kennedy JS and Mittler TE (1953) A method for obtaining phloem sap via the mouth-parts of aphids. Nature 171: 528Google Scholar
  85. King RW and Zeevart JAD (1974) Enhancement of phloem exudation from cut petioles by chelating agents. Plant Physiol 53: 96–103Google Scholar
  86. Kirk PR and Leech RM (1972) Amino acid biosynthesis by isolated chloroplasts during photosynthesis. Plant Physiol 50: 228–234Google Scholar
  87. Knop C, Voitsekhovskaja O and Lohaus G (2001) Sucrose transporters in two Scrophulariaceae with different types of transport sugar. Planta 213: 80–91CrossRefPubMedGoogle Scholar
  88. Kofler H, Häusler RE, Schulz B, Gröner F, Flügge UI and Weber A (2000) Molecular characterisation of a new mutant allele of the plastidic phosphoglucomutase and complementation of the mutant with the wild-type cDNA. Mol Gen Genet 263: 978–986PubMedGoogle Scholar
  89. Kühn C, Franceschi VR, Schulz A, Lemoine R and Frommer WB (1997) Localization and turnover of sucrose transporters in enucleate sieve element indicate macromolecular trafficking. Science 275: 1298–1300PubMedGoogle Scholar
  90. Kwart M, Hirner B, Hummel S and Frommer WB (1993) Differential expression of two related amino acid transporters with differing substrate specificity in Arabidopsis thaliana. Plant J 4: 993–1002CrossRefPubMedGoogle Scholar
  91. Li H, Culligan K, Dixon RA and Chory J (1995) CUE1: A mesophyll cell-specific positive regulator of light-controlled gene expression in Arabidopsis. Plant Cell 7: 1599–1610PubMedGoogle Scholar
  92. Loddenkötter B, Kammerer B, Fischer K and Flügge UI (1993) Expression of the functional mature chloroplast triose phosphate translocator in yeast internal membranes and purification of the histidine tagged protein by a single metal affinity chromatography step. Proc Natl Acad Sci USA 90: 2155–2159PubMedGoogle Scholar
  93. Lohaus G and Möllers C (2000) Phloem transport of amino acids in two Brassica napus genotypes and one Brassica carinata in relation to their seed protein content. Planta 211: 833–840CrossRefPubMedGoogle Scholar
  94. Lohaus G, Winter H, Riens B and Heldt HW (1995) Further studies of the phloem loading process in leaves of barley and spinach: Comparison of metabolite concentrations in the apoplastic compartment with those in the cytosolic compartment and in the sieve tubes. Bot Acta 3: 270–275Google Scholar
  95. Lohaus G, Büker M, Huβmann M and Heldt HW (1998) Transport of amino acids with special emphasis on the synthesis and transport of asparagine in Illinois Low Protein and Illinois High Protein strains of maize. Planta 205: 181–188CrossRefGoogle Scholar
  96. Lohaus G, Hussmann M, Pennewiss K, Schneider H, Zhu JJ and Sattelmacher B (2000) Solute balance of a maize (Zea mays L.) source leaf as affected by salt treatment with special emphasis on phloem re-translocation and ion leaching. J Exp Bot 51: 1721–1732CrossRefPubMedGoogle Scholar
  97. Möhlmann T and Neuhaus HE (1997) Analysis of the precursor and effector dependency of lipid synthesis in amyloplasts isolated from developing wheat-or maize-endosperm tissue. J Cereal Sci 26: 161–167Google Scholar
  98. Möhlmann T, Batz O, Maaβ U and Neuhaus HE (1995) Analysis of carbohydrate transport across the envelope of isolated cauliflower-bud amyloplasts. Biochem J 307: 521–526PubMedGoogle Scholar
  99. Möhlmann T, Tjaden J, Henrichs G, Quick WP, Häusler RE and Neuhaus HE (1997) ADP glucose drives starch synthesis in isolated maize endosperm amyloplasts. Characterization of starch synthesis and transport properties across the amyloplastidic envelope. Biochem J 324: 503–509PubMedGoogle Scholar
  100. Moing A, Escobar-Gutiérrez AJ and Gaudillère JP (1994) Modeling carbon export out of mature peach leaves. Plant Physiol 106: 591–600PubMedGoogle Scholar
  101. Moing A, Carbonne F, Zipperlin B, Svanella L and Gaudillère JP (1997) Phloem loading in peach: symplastic or apoplastic? Physiol Plant 101:489–496CrossRefGoogle Scholar
  102. Münch E (1930) Die Stoffbewegung in der Pflanze. Gustav Fischer, Jena, GermanyGoogle Scholar
  103. Naeem M, Tetlow IJ and Emes MJ (1997) Starch synthesis in amyloplasts purified from developing potato tubers. Plant J 11: 1095–1103CrossRefGoogle Scholar
  104. Neuhaus HE, Henrichs G and Scheibe R (1993a) Characterization of glucose-6-P incorporation into starch by isolated intact cauliflower-bud plastids. Plant Physiol 101: 573–578PubMedGoogle Scholar
  105. Neuhaus HE, Thom E, Batz O and Scheibe R (1993b) Purification of highly intact plastids from various heterotrophic plant tissues. Analysis of enzymic equipment and precursor dependency for starch biosynthesis. Biochem J 296: 395–401PubMedGoogle Scholar
  106. Noiraud N, Delrot S and Lemoine R (2000) The sucrose transporter of celery. Identification and expression during salt stress. Plant Physiol 122: 1447–1455CrossRefPubMedGoogle Scholar
  107. Noiraud N, Maurousset L and Lemoine R (2001) Identification of a mannitol transporter, AgMaT1, in celery phloem. Plant Cell 13: 695–705CrossRefPubMedGoogle Scholar
  108. Ohnishi J and Kanai R (1990) Pyruvate uptake induced by a pH jump in mesophyll chloroplasts of maize and sorghum, NADP-malic enzyme type C4 species. FEBS Lett 269: 122–124CrossRefPubMedGoogle Scholar
  109. Ohnishi J, Flügge UI and Heldt HW (1989) Phosphate translocator of mesophyll and bundle sheath chloroplasts of a C4 plant, Panicum miliaceum. Identification and kinetic characterization. Plant Physiol 91: 1507–1511Google Scholar
  110. 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
  111. Okita T (1992) Is there an alternative pathway for starch synthesis? Plant Physiol 100: 560–64Google Scholar
  112. Oparka KJ and Turgeon R (1999) Sieve elements and companion cells-Traffic control centers of the phloem. Plant Cell 11: 739–750CrossRefPubMedGoogle Scholar
  113. Pate J and Gunning BES (1972) Transfer cells. Annu Rev Plant Physiol 23: 173–196CrossRefGoogle Scholar
  114. Pozueto-Romero J, Frehner M, Viale AM and Akazawa T (1991) Direct transport of ADP glucose by an adenylate translocator is linked to starch biosynthesis in amyloplasts. Proc Natl Acad Sci USA 88: 5769–5773Google Scholar
  115. Preiss J (1991) Biology and molecular biology of starch synthesis and its regulation. Oxf Surv Plant Mol Cell Biol 7: 59–114Google Scholar
  116. Proudlove MO and Thurman DA (1981) The uptake of 2-oxoglutarate and pyruvate by isolated pea chloroplasts. New Phytol 88: 255–264Google Scholar
  117. Quick WP and Neuhaus HE (1996) Evidence for two types of phosphate translocators in sweet pepper (Capsicum annuum) fruit chromoplasts. Biochem J 320: 7–10PubMedGoogle Scholar
  118. Quick WP, Scheibe R and Neuhaus E (1995) Induction of a hexose-phosphate translocator activity in spinach chloroplasts. Plant Physiol 109: 113–121PubMedGoogle Scholar
  119. Rentsch D, Hirner B, Schmelzer E and Frommer WB (1996) Salt stress-induced proline transporters and salt stress-repressed broad specificity amino acid permeases identified by suppression of a yeast amino acid permease-targeting mutant. Plant Cell 8: 1437–1446CrossRefPubMedGoogle Scholar
  120. Riens B, Lohaus G, Winter H and Heldt HW (1994) Production and diurnal utilization of assimilates in leaves of spinach (Spinacia oleracea L.) and barley (Hordeum vulgare L.). Planta 192: 497–501CrossRefGoogle Scholar
  121. Riesmeier JW, Willmitzer L and Frommer WB (1992) Isolation and characterization of a sucrose carrier cDNA from spinach by functional expression in yeast. EMBO J 11: 4705–4713PubMedGoogle Scholar
  122. Riesmeier JW, Flügge UI, Schulz B, Heineke D, Heldt HW, Willmitzer L and Frommer WB (1993a) Antisense repression of the chloroplast triose phosphate translocator affects carbon partitioning in transgenic potato plants. Proc Natl Acad Sci USA 90: 6160–6164PubMedGoogle Scholar
  123. Riesmeier JW, Hirner B and Frommer WB (1993b) Potato sucrose transporter expression in minor veins indicates a role in phloem loading. Plant Cell 5: 1591–1598CrossRefPubMedGoogle Scholar
  124. 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
  125. Roblin G, Sakr S, Bonmort J and Delrot S (1998) Regulation of a plant plasma membrane sucrose transporter by phosphorylation. FEBS Lett 424: 165–168CrossRefPubMedGoogle Scholar
  126. Rost S, Frank C and Beck E (1996) The chloroplast envelope is permeable for maltose but not for maltodextrins. Biochim Biophys Acta 1291: 221–227PubMedGoogle Scholar
  127. Rumpho ME, Edwards GE and Loescher WH (1983) A pathway for photosynthetic carbon flow to mannitol in celery leaves. Activity and localization of key enzymes. Plant Physiol 73: 869–873Google Scholar
  128. Russian 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 defective maize mutant. Plant Cell 8: 645–658Google Scholar
  129. Salmon S, Lemoine R, Jamai A, Bouché-Pillon S and Fromont JC (1995) Study of sucrose and mannitol transport in plasma-membrane vesicles from phloem and non-phloem tissues of celery (Apium graveolens L.) petioles. Planta 197: 76–83CrossRefGoogle Scholar
  130. 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: 67–77CrossRefPubMedGoogle Scholar
  131. Schäfer G, Heber U and Heldt HW (1977) Glucose transport into spinach chloroplasts. Plant Physiol 60: 286–289Google Scholar
  132. Schleucher J, Vanderveer PJ and Sharkey TD (1998) Export of carbon from chloroplasts at night. Plant Physiol 118: 1439–1445CrossRefPubMedGoogle Scholar
  133. Schmid J and Amrhein N (1995) Molecular organization of the shikimate pathway in higher plants. Phytochemistry 39: 737–749CrossRefGoogle Scholar
  134. Schott K, Borchert S, Muller-Röber B and Heldt HW (1995) Transport of inorganic phosphate and C3-and C6-sugar phosphates across the envelope membranes of potato tuber amyloplasts. Planta 196: 647–652Google Scholar
  135. Schulz B, Frommer WB, Flügge UI, Hummel S, Fischer K and Willmitzer L (1993) Expression of the triose phosphate translocator gene from potato is light dependent and restricted to green tissues. Mol Gen Genet 238: 357–361CrossRefPubMedGoogle Scholar
  136. Schünemann D and Borchert S (1994) Specific transport of inorganic phosphate and C3-and C6-sugar phosphates across the envelope membranes of tomato leaf chloroplasts, tomato fruit chloroplasts and fruit chromoplasts. Bot Acta 107: 461–467Google Scholar
  137. Schwacke R, Grallath S, Breitkreuz KE, Stransky E, Stransky H, Frommer WB and Rentsch D (1999) LeProT1, a transporter for proline, glycine betaine, and γ-amino butyric acid in tomato pollen. Plant Cell 11: 377–391CrossRefPubMedGoogle Scholar
  138. Shakya R and Sturm A (1998) Characterization of source-and sink-specific sucrose/H+ symporters from carrot. Plant Physiol 118: 1473–1480CrossRefPubMedGoogle Scholar
  139. Shannon JC, Pien FM, Cao H and Liu KC (1998) Brittle-1, an adenylate translocator, facilitates transfer of extraplastidial synthesized ADP-glucose into amyloplasts of maize endosperm. Plant Physiol 117: 1235–1252CrossRefPubMedGoogle Scholar
  140. Sjölund RD (1997) The phloem sieve element: A river runs through it. Plant Cell 9: 1137–1146PubMedGoogle Scholar
  141. Sprenger N and Keller F (2000) Allocation of raffinose family oligosaccharides to transport and storage pools in Ajuga reptans: the roles of two distinct galactinol synthases. Plant J 21: 249–258CrossRefPubMedGoogle Scholar
  142. Stadler R and Sauer N (1996) The Arabidopsis thaliana AtSUC2 gene is specifically expressed in companion cells. Bot Acta 109:299–308Google Scholar
  143. 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: 1545–1554CrossRefPubMedGoogle Scholar
  144. 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 Arabidopsis. Plant J 19:269–278CrossRefPubMedGoogle Scholar
  145. Stitt M (1990) Fructose 2,6 bisphosphate in plants. Annu Rev Plant Physiol Plant Mol Biol 41: 153–185CrossRefGoogle Scholar
  146. Stitt M and ap Rees T (1979) Capacities of pea chloroplasts to catalyse the oxidative pentose phosphate pathway and glycolysis. Phytochemistry 18: 1905–1911CrossRefGoogle Scholar
  147. Stitt M and Quick WP (1989) Photosynthetic carbon partitioning: Its regulation and possibilities for manipulation. Physiol Plant 77: 633–641Google Scholar
  148. Stitt M, Bulpin PV and ap Rees T (1978) Pathway of starch breakdown in photosynthetic tissues of Pisum sativum. Biochim Biophys Acta 544: 200–214PubMedGoogle Scholar
  149. Stitt M, Wirtz W, Gerhardt R, Heldt HW, Spencer C, Walker DA and Foyer C (1985) A comparative study of metabolite levels in plant leaf material in the dark. Planta 166: 354–364CrossRefGoogle Scholar
  150. Streatfield SJ, Weber A, Kinsman EA, Häusler RE, Li J, Post-Beittenmiller D, Kaiser WM, Pyke KA, Flügge UI and Chory J (1999) The phosphoenolpyruvate/phosphate translocator is required for phenolic metabolism, palisade cell development and plastid-dependent nuclear gene expression. Plant Cell 11: 1609–1621CrossRefPubMedGoogle Scholar
  151. Sturm A and Tang GQ (1999) The sucrose-cleaving enzymes of plants are crucial for development, growth and carbon partitioning. Trends Plant Sci 4: 401–407CrossRefPubMedGoogle Scholar
  152. Sullivan TD and Kaneko Y (1995) The maize brittle 1 gene encodes amyloplast membrane polypeptides. Planta 196:477–484CrossRefPubMedGoogle Scholar
  153. Sullivan TD, Strelow LI, Illingworth CA, Phillips RL and Nelson OE (1991) Analysis of maize Brittle-1 alleles and a defective suppressor-mutator-induced mutable allele. Plant Cell 3: 1337–1348CrossRefPubMedGoogle Scholar
  154. Tauberger E, Fernie AR, Emmermann M, Renz A, Kossmann J, Willmitzer L and Trethewey RN (2000) Antisense inhibition of plastidial phosphoglucomutase provides compelling evidence that potato tuber amyloplasts import carbon from the cytosol in the form of glucose-6-phosphate. Plant J 23: 43–53CrossRefPubMedGoogle Scholar
  155. Tegeder M, Wang X-D, Frommer W, Offler CE and Patrick JW (1999) Sucrose transport into developing seeds of Pisum sativum L. Plant J 18: 151–161CrossRefPubMedGoogle Scholar
  156. Tetlow IJ, Blisset KJ and Emes MJ (1994) Starch synthesis and carbohydrate oxidation in amyloplasts from developing wheat endosperm. Planta 194: 454–460CrossRefGoogle Scholar
  157. Tetlow IJ, Bowshcr CG and Emes MJ (1996) Reconstitution of the hexose phosphate translocator from the envelope membranes of wheat endosperm amyloplasts. Biochem J 319: 717–723PubMedGoogle Scholar
  158. Thom E, Möhlmann T, Quick WP, Camara B and Neuhaus HE (1998) Sweet pepper plastids: Enzymic equipment, characterisation of the plastidic oxidative pentose-phosphate pathway, and transport of phosphorylated intermediates across the envelope membrane. Planta 204: 226–233CrossRefGoogle Scholar
  159. Thompson AG, Brailsford MA and Beechey RB (1987) Identification of the phosphate translocator from maize mesophyll chloroplasts. Biochem Biophys Res Commun 143: 164–169PubMedGoogle Scholar
  160. Thorbjørnsen T, Villand P, Denyer K, Olsen OA and Smith AM (1996a) Distinct isoforms of ADP glucose pyrophosphorylase occur inside and outside the amyloplasts in barley endosperm. Plant J 10: 243–250Google Scholar
  161. Thorbjørnsen T, Villand P, Kleczkowski LA and Olsen OA (1996b) A single gene encodes two different transcripts for the ADP-glucose pyrophosphorylase small subunit from barley. Biochem J 313: 149–154PubMedGoogle Scholar
  162. Trethewey RN and ap Rees T (1994) A mutant of Arabidopsis lacking the ability to transport glucose across the chloroplast envelope. Biochem J 301: 449–454PubMedGoogle Scholar
  163. Trethewey RN and Smith AM (2000) Starch metabolism in leaves. In: Leegood RC, Sharkey TD and von Caemmerer S (eds) Photosynthesis: Physiology and Metabolism, pp 205–231. Kluwer Academic Publishers, DordrechtGoogle Scholar
  164. Truernit E and Sauer N (1995) The promoter of the Arabidopsis thaliana SUC2 sucrose-H+ symporter gene directs expression of β-glucuronidase to the phloem: Evidence for phloem loading and unloading by SUC2. Planta 196: 564–570CrossRefPubMedGoogle Scholar
  165. Turgeon R (1991) Symplastic phloem loading and the sink-source transition in leaves: A model. In: Bonnemain J-L, Delrot S, Lucas WJ, Dainty J (eds) Recent advances in Phloem Transport and Assimilate Compartimentation, pp 18–22. Quest Editions, ParisGoogle Scholar
  166. Turgeon R (1996) Phloem loading and plasmodesmata. Trends Plant Sci 1: 403–411CrossRefGoogle Scholar
  167. Turgeon R, Webb JA and Evert RF (1975) Ultrastructure of minor veins of Cucurbita pepo leaves. Protoplasma 83: 217–232CrossRefGoogle Scholar
  168. Turgeon R, Beebe DU and Gowan E (1993) The intermediary cell: Minor-vein anatomy and raffinose oligosaccharide synthesis in the Scrophulariaceae. Planta 191: 446–456CrossRefGoogle Scholar
  169. Tyson RH and ap Rees T (1988) Starch synthesis by isolated amyloplasts from wheat endosperm. Planta 175: 33–38CrossRefGoogle Scholar
  170. Van Bel AJE, Hendriks JHM, Boon EJMC, Gamalei YV and van de Merwe AP (1996) Different ratios of sucrose/raffinose-induced membrane depolarizations in the mesophyll of species with symplasmic (Catharanthus roseus, Ocimum basilicum) or apoplasmic (Impatiens walleriana, Vicia faba) minor-vein configurations. Planta 199: 185–192CrossRefGoogle Scholar
  171. Wallsgrove RM, Keys AJ, Lea PJ and Miflin BJ (1983) Photosynthesis, photorespiration and nitrogen metabolism. Plant Cell Environ 6: 301–309Google Scholar
  172. Weathcrley PE, Peel AJ and Hill GP (1959) The physiology of the sieve tube. Preliminary experiments using aphid mouth parts. J Exp Bot 10: 1–16Google Scholar
  173. Webb KL and Burley JWA (1962) Sorbitol translocation in apple. Science 137: 766Google Scholar
  174. Weber A, Menzlaff E, Arbinger B, Gutensohn M, Eckerskorn C and Flügge UI (1995) The 2-oxoglutarate/malate translocator of chloroplast envelope membranes: Molecular cloning of a transporter protein containing a 12-helix motif and expression of the functional protein in yeast cells. Biochemistry 34:2621–2627PubMedGoogle Scholar
  175. Weber A, Servaites JC, Geiger DR, Kofler H, Hille D, Gröner F, Hebbeker U and Flügge UI (2000) Identification, purification and molecular cloning of a plastidic glucose translocator. Plant Cell 12: 787–801CrossRefPubMedGoogle Scholar
  176. Weber H, Borisjuk L, Heim U, Sauer N and Wobus U (1997) A role for sugar transporters during seed development: Molecular characterization of a hexose and a sucrose carrier in fava bean seeds. Plant Cell 9: 895–908CrossRefPubMedGoogle Scholar
  177. Weig A and Komor E (1996) An active sucrose carrier (Scr 1) that is predominantly expressed in the seedling of Ricinus communis L. J Plant Physiol 147: 685–690Google Scholar
  178. Wiese A, Gröner F, Sonnewald U, Deppner H, Lerchl J, Hebbeker U, Flügge UI and Weber A (1999) Spinach hexokinase I is located in the outer envelope membrane of plastids. FEBS Lett 461: 13–18CrossRefPubMedGoogle Scholar
  179. 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: 455–467CrossRefPubMedGoogle Scholar
  180. Willey DL, Fischer K, Wachter E, Link TA and Flügge UI (1991) Molecular cloning and structural analysis of the phosphate translocator from pea chloroplasts and its comparison to the spinach phosphate translocator. Planta 183: 451–461CrossRefGoogle Scholar
  181. Winter H, Lohaus G and Heldt HW (1992) Phloem transport of amino acids in relation to their cytosolic levels in barley leaves. Plant Physiol 99: 996–1004Google Scholar
  182. Winzer T, Lohaus G and Heldt HW (1996) Influence of phloem transport, N-fertilization and ion accumulation on the sucrose storage in the taproots of fodder beet and sugar beet. J Exp Bot 47: 863–870Google Scholar
  183. Yu TS, Lue, WL, Wang SM and Chen J (2000) Mutation of Arabidopsis plastid phosphoglucose isomerase affects leaf starch synthesis and floral initiation. Plant Physiol 123: 319–325PubMedGoogle Scholar
  184. Yu TS, Kofler H, Häusler RE, Hille D, Flügge UI, Zeeman SC, Smith AM, Kossmann J, Lloyd J, Ritte G, Steup M, Lue WL, Chen J and Weber A (2001) The Arabidopsis sex1 mutant is defective in the R1 protein, a general regulator of starch degradation in plants, and not in the chloroplast hexose transporter. Plant Cell 13: 1907–1918PubMedGoogle Scholar
  185. Zeeman SC, Northorp F, Smith AM and ap Rees T (1998) A starch-accumulating mutant of Arabidopsis thaliana deficient in a chloroplastic starch-hydrolysing enzyme. Plant J 15: 357–365CrossRefPubMedGoogle Scholar
  186. Ziegler H (1975) Nature of transported substances. In: Zimmermann MH and Milburn JA (eds) Encyclopedia of Plant Physiology, Vol 1, pp 59–100. Springer Verlag, BerlinGoogle Scholar
  187. Zimmermann MH (1957) Translocation of organic substances in trees. I. The nature of the sugars in the sieve-tube exudate of trees. Plant Physiol 32: 288–291Google Scholar
  188. Zimmermann MH and Ziegler H (1975) List of sugars and sugar alcohols in sieve-tube exudates. In: Zimmermann MH, Milburn JA (eds) Encyclopedia of Plant Physiology, Vol 1, pp 480–503. Springer Verlag, BerlinGoogle Scholar

Copyright information

© Kluwer Academic Publishers 2002

Authors and Affiliations

  • Gertrud Lohaus
    • 1
  • Karsten Fischer
    • 2
  1. 1.Biochemie der PflanzeAlbrecht-von-Haller Institut für PflanzenwissenschaftenGöttingenGermany
  2. 2.Botanisches Institut der Universität zuKölnKölnGermany

Personalised recommendations