New enzymes, new pathways and an alternative view on starch biosynthesis in both photosynthetic and heterotrophic tissues of plants

References

• Andon NL, Hollingworth S, Koller A, Greenland AJ, Yates JR, Haynes PA. Proteomic characterization of wheat amyloplasts using identification of proteins by tandem mass spectrometry. Proteomics 2002; 2: 1156–1168
   PubMedGoogle Scholar
• Asano T, Kunieda N, Omura Y, Ibe H, Kawasaki T, Takano M, Sato M, Furuhashi H, Mujin T, Takaiwa F, Wu C-Y, Tada Y, Satozawa T, Sakamoto M, Shimada H. Rice SPK, a calmodulin-like domain protein kinase, is required for storage product accumulation during seed development: phosphorylation of sucrose synthase is a possible factor. Plant Cell 2002; 14: 619–628
   PubMed Web of Science ®Google Scholar
• ap Rees, T. (1995). In: Sucrose metabolism, biochemistry, physiology and molecular biology. Pontis HG, Salerno GL, Echeverria EJ, Editors. Rockville MD: American Society of Plant Physiologists, 14, 143–155
   Google Scholar
• Arnon DI. The chloroplast as a complete photosynthetic unit. Science 1955; 122: 9–16
   PubMedGoogle Scholar
• Backhausen JE, Jöstingmeyer P, Scheibe R. Competitive inhibition of spinach leaf phosphoglucose isomerase isoenzymes by erythrose 4-phosphate. Plant Sci 1997; 130: 121–131
   Google Scholar
• Baroja-Fernández E, Muñoz FJ, Akazawa T, Pozueta-Romero J. Reappraisal of the currently prevailing model of starch biosynthesis in photosynthetic tissues: A proposal involving the cytosolic production of ADP-glucose by sucrose synthase and occurrence of cyclic turnover of starch in chloroplast. Plant Cell Physiol 2001; 42: 1311–1320
   PubMedGoogle Scholar
• Baroja-Fernández E, Muñoz FJ, Pozueta-Romero J. A response to Neuhaus et al. Trends Plant Sci 2005; 10: 156–159
   Google Scholar
• Baroja-Fernández E, Muñoz FJ, Saikusa T, Rodríguez-López M, Akazawa T, Pozueta-Romero J. Sucrose synthase catalyzes the de novo production of ADPglucose linked to starch biosynthesis in heterotrophic tissues of plants. Plant Cell Physiol 2003; 44: 500–509
   PubMed Web of Science ®Google Scholar
• Baroja-Fernández E, Muñoz FJ, Zandueta-Criado A, Morán-Zorzano MT, Viale AM, Alonso-Casajús N, Pozueta-Romero J. Most of ADPglucose linked to starch biosynthesis occurs outside the chloroplast in source leaves. Proc Natl Acad Sci USA. 2004; 101: 13080–13085
   PubMed Web of Science ®Google Scholar
• Baroja-Fernández E, Zandueta-Criado A, Rodríguez-López M, Akazawa T, Pozueta-Romero J. Distinct isoforms of ADPglucose pyrophosphatase and ADPglucose pyrophosphorylase occur in the suspension-cultured cells of sycamore (Acer pseudoplatanus L.). FEBS Lett 2000; 480: 277–282
   PubMedGoogle Scholar
• Bassham JA, Krause GH. Free energy changes and metabolic regulation in steady-state photosynthetic carbon reduction. Biochim Biophys Acta 1969; 189: 207–221
   PubMedGoogle Scholar
• Beckles DM, Smith AM, ap Rees T. A cytosolic ADP-glucose pyrophosphorylase is a feature of graminaceous endosperms. Plant Physiol 2001; 125: 818–827
   PubMedGoogle Scholar
• Belanger AE, Hatfull G. Exponential-phase glycogen recycling is essential for growth of Mycobacterium smegmatis. J Bacteriol 1999; 181: 6670–6678
   PubMedGoogle Scholar
• Bessman MJ, Frick DN, O′Handley SF. The MutT proteins or ‘Nudix’ hydrolases, a family of versatile, widely distributed, housecleaning enzymes. J Biol Chem 1996; 271: 25059–25062
   PubMed Web of Science ®Google Scholar
• Brangeon J, Reyss A, Prioul J-L. In situ detection of ADPglucose pyrophosphorylase expression during maize endosperm development. Plant Physiol Biochem 1997; 35: 847–858
   Google Scholar
• Burton RA, Johnosn PE, Beckles DM, Fincher GB, Jenner HL, Naldrett MJ, Denyer K. Characterization of the genes encoding the cytosolic and plastidial isoforms of ADP-glucose pyrophosphorylase in wehat endosperm. Plant Physiol 2002; 130: 1464–1475
   PubMed Web of Science ®Google Scholar
• Cao H, Sullivan TD, Boyer CD, Shannon JC. Bt1, a structural gene for the major 30–44 kDa amyloplast membrane polypeptides. Physiol Plant 1995; 95: 176–186
   Google Scholar
• Caspar T, Huber SC, Somerville C. Alterations in growth, photosynthesis, and respiration in a starchless mutant of Arabidopsis thaliana (L.) deficient in chloroplast phosphoglucomutase activity. Plant Physiol 1985; 79: 11–17
   PubMed Web of Science ®Google Scholar
• Chan T-T, Bird IF. Starch dissolution in tobacco leaves in the light. J Exp Bot 1960; 11: 335–340
   Google Scholar
• Chourey PS, Nelson OE. The enzymatic deficiency conditioned by the shrunken-1 mutations in maize. Biochem Genet 1976; 14: 1041–1055
   Google Scholar
• Crevillén P, Ballicora MA, Mérida A, Preiss J, Romero JM. The different large subunit isoforms of Arabidopsis thaliana ADP-glucose pyrophosphorylase confer distinct kinetic and regulatory properties to the heterotetrameric enzyme. J Biol Chem 2003; 278: 28508–28515
   PubMedGoogle Scholar
• David M, Petit WA, Laughlin MR, Shulman RG, King JE, Barrett EJ. Simultaneous synthesis and degradation of rat liver glycogen. J Clin Invest 1990; 86: 612–617
   PubMedGoogle Scholar
• Davies Hv, Shepherd LVT, Burrell MM, Carrari F, Urbanczyk-Wochniak E, Leisse A, Hancock RD, Taylor M, Viola R, Ros H, McRae D, Willmitzer L, Fernie AR. Modulation of fructokinase activity of potato (Solanum tuberosum) results in substantial shifts in tuber metabolism. Plant Cell Physiol 2005; 46: 1103–1115
   PubMedGoogle Scholar
• Delmer DP. The purification and properties of sucrose synthetase from etiolated Phaseolus aureus seedlings. J Biol Chem 1972; 247: 3822–3828
   PubMedGoogle Scholar
• Denyer K, Dunlap F, Thornbjørnsen T, Keeling P, Smith AM. The major form of ADP-glucose pyrophosphorylase in maize (Zea mays L.) endosperm is extra-plastidial. Plant Physiol 1996; 112: 779–785
   PubMedGoogle Scholar
• Dickinson DB, Preiss J. Presence of ADP-glucose pyrophosphorylase in shrunken-2 and brittle-2 mutants of maize endosperm. Plant Physiol 1969; 44: 1058–1062
   PubMedGoogle Scholar
• Dietz K-J. A possible rate-limiting function of chloroplast hexosemonophosphate isomerase in starch synthesis of leaves. Biochim Biophys Acta 1985; 839: 240–248
   Google Scholar
• Entwistle G, ap Rees T. Enzymic capacities of amyloplasts from wheat endosperm. Biochem J 1988; 255: 391–396
   PubMedGoogle Scholar
• Etxeberria E, Baroja-Fernandez E, Muñoz FJ, Pozueta-Romero J. Sucrose inducible endocytosis as a mechanism for nutrient uptake in heterotrophic plant cells. Plant Cell Physiol 2005a; 46: 474–481
   PubMed Web of Science ®Google Scholar
• Etxeberria E, Gonzalez P. Evidence for a tonoplast-associated form of sucrose synthase and its potential involvement in sucrose mobilization from the vacuole. J Exp Bot 2003; 54: 1407–1414
   PubMed Web of Science ®Google Scholar
• Etxeberria E, Gonzalez P, Pozueta-Romero J. Sucrose transport in Citrus juice cells: Evidence for an endocytic transport system. J Am Soc Hort Sci 2005b; 130: 269–274
   Web of Science ®Google Scholar
• Fernie AR, Riesmeier JW, Martini JW, Ramalingan S, Willmitzer L, Trethewey RN. Consequences of the expression of a bacterial glukokinase in potato tubers, both in combination with and independently of a yeast derived invertases. Australian J Plant Physiol 2000; 27: 827–833
   Google Scholar
• Fernie AR, Tauberger E, Lytovchenko A, Roessner U, Willmitzer L, Trethewey RN. Antisense repression of cytosolic phosphoglucomutase in potato (Solanum tuberosum) results in severe growth retardation, reduction in tuber number and altered carbon metabolism. Planta 2002a; 214: 510–520
   PubMed Web of Science ®Google Scholar
• Fernie AR, Swiedrych A, Tauberger E, Lytovchenko A, Trethewey RN, Willmitzer L. Potato plants exhibiting combined antisense repression of cytosolic and plastidial isoforms of phosphoglucomutase surprisingly approximate wild type with respect to the rate of starch synthesis. Plant Physiol Biochem 2002b; 40: 921–927
   Google Scholar
• Fernie AR, Willmitzer L, Trethewey RN. Sucrose to starch: a transition in molecular plant physiology. Trends Plant Sci 2002c; 7: 35–41
   PubMed Web of Science ®Google Scholar
• Frehner M, Pozueta-Romero J, Akazawa T. Enzyme sets of glycolysis, gluconeogenesis, and oxidative pentose phosphate pathway are not complete in nongreen highly purified amyloplasts of sycamore (Acer pseudoplatanus L.) cells suspension cultures. Plant Physiol 1990; 94: 538–544
   PubMed Web of Science ®Google Scholar
• Fritzius T, Aeschbacher R, Wiemken A, Wingler A. Induction of ApL3 expression by trehalose complements the starch-deficient Arabidopsis mutant adg2-1 lacking ApL1, the large subunit of ADP-glucose pyrophosphorylase. Plant Physiol 2001; 126: 883–889
   PubMed Web of Science ®Google Scholar
• Fu H, Kim SY, Park WD. A potato Sus3 sucrose synthase gene contains a context-dependent 3′ element and a leader intron with both positive and negative tissue-specific effects. Plant Cell 1995; 7: 1395–1403
   PubMedGoogle Scholar
• Gaudet G, Forano E, Dauphin G, Delort A-M. Futile cycling of glycogen in Fibrobacter succinogenes as shown by in situ1H-NMR and 13C-NMR investigation. Eur J Biochem 1992; 207: 155–162
   PubMedGoogle Scholar
• Geigenberger P. Regulation of sucrose to starch conversion in growing potato tubers. J Exp Bot 2003; 54: 457–465
   PubMedGoogle Scholar
• Geigenberger P, Stamme C, Tjaden J, Schulz A, Quick PW, Betsche T, Kersting HJ, Neuhaus E. Tuber physiology and properties of starch from tubers of transgenic potato plants with altered plastidic adenylate transporter activity. Plant Physiol 2001; 125: 1667–1678
   PubMed Web of Science ®Google Scholar
• Geigenberger P, Stitt M. A ‘futile’ cycle of sucrose synthesis and degradation is involved in regulating partitioning between sucrose, starch and respiration in cotyledons of germinating Ricinus communis L. seedlings when phloem transport is inhibited. Planta 1991; 185: 81–90
   PubMedGoogle Scholar
• Gross P, ap Rees T. Alkaline inorganic pyrophosphatase and starch synthesis in amyloplasts. Planta 1986; 167: 140–145
   PubMedGoogle Scholar
• Guedon E, Desvaux M, Petitdemange H. Kinetic analysis of Clostridium cellulolyticum carbohydrate metabolism: importance of glucose 1-phosphate and glucose 6-phosphate branch points for distribution of carbon fluxes inside and outside cells as revealed by steady-state continuous culture. J Bacteriol 2000; 183: 2010–2017
   Google Scholar
• Haake V, Zrenner R, Sonnewald U, Stitt M. A moderate decrease of plastid aldolase activity inhibits photosynthesis, alters the levels of sugars and starch, and inhibits growth of potato plants. Plant J 1998; 14: 147–158
   PubMed Web of Science ®Google Scholar
• Hajirezaei MR, Takahata Y, Trethewey RN, Willmitzer L, Sonnewald U. Impact of elevated cytosolic and apoplastic invertases activity on carbon metabolism during potato tuber development. J Exp Bot 2000; 51: 439–445
   PubMedGoogle Scholar
• Harrison CJ, Hedley CL, Wang TL. Evidence that the rug3 locus of pea (Pisum sativum L.) encodes plastidial phosphoglucomutase confirms that the imported substrate for starch synthesis in pea amyloplasts is glucose-6-phosphate. Plant J 1998; 13: 753–762
   Google Scholar
• Hatzfeld W-D, Stitt M. A study of the rate of recycling of triose phosphates in heterotrophic Chenopodium rubrum cells, potato tubers, and maize endosperm. Planta 1990; 180: 198–204
   PubMedGoogle Scholar
• Häusler RE, Schlieben NH, Schulz B, Flügge U-I. Compensation of decreased triose phosphate/phosphate translocator activity by accelerated starch turnover and glucose transport in transgenic tobacco. Planta 1998; 204: 366–376
   PubMed Web of Science ®Google Scholar
• Heineke D, Kruse A, Flügge UI, Frommer WB, Riesmeier JW, Willmitzer L, Heldt HW. Effect of antisense repression of the chloroplast triose-phosphate translocator on photosynthetic metabolism in transgenic potato plants. Planta 1994; 193: 174–180
   Web of Science ®Google Scholar
• Heldt HW, Chon CJ, Maronde D, Herold A, Stankovic ZS, Walker DA, Kraminer A, Kirk MR, Heber U. Role of orthophosphate and other factors in the regulation of starch formation in leaves and isolated chloroplasts. Plant Physiol 1977; 59: 1146–1155
   PubMed Web of Science ®Google Scholar
• Hendriks JHM, Kolbe A, Gibon Y, Stitt M, Geigenberger P. ADP-glucose pyrophosphorylase is activated by posttranslational redox-modification in response to light and to sugars in leaves of Arabidopsis and other plant species. Plant Physiol 2003; 133: 838–849
   PubMed Web of Science ®Google Scholar
• Johnson PE, Patron NJ, Bottrill AR, Dinges JR, Fahy BF, Parker ML, Waite DN, Denyer K. A low-starch barley mutant, Riso 16, lacking the cytosolic small subunit of ADP-glucose pyrophosphorylase, reveals the importance of the cytosolic isoform and the identity of the plastidial small subunit. Plant Physiol 2003; 131: 684–696
   PubMed Web of Science ®Google Scholar
• Jones TWA, Gottlieb LD, Pichersky E. Reduced enzyme activity and starch level in an induced mutant of chloroplast phosphoglucose isomerase. Plant Physiol 1986; 81: 367–371
   PubMedGoogle Scholar
• Jones H, Martin RV, Porter HK. Translocation of 14Carbon in tobacco following assimilation of 14Carbon dioxide by a single leaf. Ann Bot 1959; 23: 493–508
   Google Scholar
• Kammerer B, Fischer K, Hilpert B, Schubert S, Gutensohn M, Weber A, Flügge U-I. Molecular characterization of a carbon transporter in plastids from heterotrophic tissues: the glucose 6-phosphate/phosphate antiporter. Plant Cell 1998; 10: 105–117
   PubMed Web of Science ®Google Scholar
• Keeling PL, Wood JR, Tyson RH, Bridges IG. Starch biosynthesis in developing wheat grain: evidence against the direct involvement of triose phosphates in the metabolic pathway. Plant Physiol 1988; 87: 311–319
   PubMedGoogle Scholar
• Kelly GJ, Latzko E. Oat leaf phosphoglucose isomerase: competitive inhibition by erythrose-4-phosphate. Photosynth Res 1980; 1: 181–187
   PubMedGoogle Scholar
• Kleczkowski LA. Back to the drawing board: redefining starch synthesis in cereals. Trends Plant Sci 1996; 1: 363–364
   Google Scholar
• Kleczkowski LA. A phosphoglycerate to inorganic phosphate ratio is the major factor in controlling starch levels in chloroplasts via ADP-glucose pyrophosphorylase regulation. FEBS Lett 1999; 448: 153–156
   PubMedGoogle Scholar
• Kleczkowski LA. Is leaf ADP-glucose pyrophosphorylase an allosteric enzyme. Biochim Biophys Acta 2000; 1476: 103–108
   PubMedGoogle Scholar
• Kleczkowski LA, Geisler M, Ciereszko I, Johansson H. UDP-glucose pyrophosphorylase. An old protein with new tricks. Plant Physiol 2004; 134: 912–918
   PubMed Web of Science ®Google Scholar
• Koch KE, Nolte KD, Duke ER, McCarty DR, Avigne WT. Sugar levels modulate differential expression of maize sucrose synthase genes. Plant Cell 1992; 4: 59–69
   PubMed Web of Science ®Google Scholar
• Kossmann J, Sonnewald U, Willmitzer L. Reduction of the chloroplastic fructose-1,6-bisphosphatase in transgenic potato plants impairs photosynthesis and plant growth. Plant J 1994; 6: 637–650
   Web of Science ®Google Scholar
• Kruckeberg L, Neuhaus HE, Feil R, Gottlieb LD, Stitt M. Decreased-activity mutants of phosphoglucose isomerase in the cytosol and chloroplast of Clarkia xantiana. Biochem J 1989; 261: 457–467
   PubMed Web of Science ®Google Scholar
• Landau BR. Methods for measuring glycogen cycling. Am J Physiol Endocrinol Metab 2001; 281: E413–E419
   Google Scholar
• Lefebvre S, Lawson T, Fryer M, Zakhleniuk OV, Lloyd JC, Raines CA. Increased sedoheptulose-1,7-bisphosphatase activity in transgenic tobacco plants stimulates photosynthesis and growth from an early stage in development. Plant Physiol 2005; 138: 451–460
   PubMed Web of Science ®Google Scholar
• Leroch M, Kirchberger S, Haferkamp I, Wahl M, Neuhaus HE, Tjaden J. Identification and characterization of a novel plastidic adenine nucleotide uniporter from Solanum tuberosum. J Biol Chem 2005; 280: 17992–18000
   PubMedGoogle Scholar
• Lin T-P, Caspar T, Somerville CR, Preiss J. Isolation and characterization of a starchless mutant of Arabidopsis thaliana (L.) Heynh lacking ADPglucose pyrophosphorylase activity. Plant Physiol 1988; 86: 1131–1135
   PubMedGoogle Scholar
• Lloyd JR, Kossmann J, Ritte G. Leaf starch degradation comes out of the shadows. Trends Plant Sci 2005; 10: 130–137
   PubMed Web of Science ®Google Scholar
• Massillon D, Bollen M, De Wulf H, Overloop K, Vanstapel F, Van Hecke P, Stalmans W. Demonstration of a glycogen/glucose 1-phosphate cycle in hepatocytes from fasted rats. J Biol Chem 1995; 270: 19351–19356
   PubMedGoogle Scholar
• McLachlan GA, Porter DA. Replacement of oxidation by light as the energy source for glucose metabolism in tobacco leaf. Proc R Soc Lond 1959; 150: 460–473
   PubMedGoogle Scholar
• Miller ME, Chourey PS. Intracellular immunolocalization of adenosine 5′-diphosphoglucose pyrophosphorylase in developing endosperm cells of maize (Zea mays L.). Planta 1995; 197: 522–527
   Google Scholar
• Miyagawa Y, Tamoi M, Shigeoka S. Overexpression of a cyanobacterial fructose-1,6-/sedoheptulose-1,7-bisphosphatase in tobacco enhance photosynthesis and growth. Nat Biotechnol 2001; 19: 965–969
   PubMed Web of Science ®Google Scholar
• Möhlmann T, Tjaden J, Henrichs G, Quick WP, Häusler R, Neuhaus HE. ADPglucose drives starch synthesis in isolated maize endosperm amyloplasts. Characterization of starch synthesis and transport properties across the amyloplast envelope. Biochem J 1997; 324: 503–509
   PubMedGoogle Scholar
• Moreno-Bruna B, Baroja-Fernández E, Muñoz FJ, Bastarrica-Berasategui A, Zandueta-Criado A, Rodríguez-López M, Lasa I, Akazawa T, Pozueta-Romero J. Adenosine diphosphate sugar pyrophosphatase prevents glycogen biosynthesis in Escherichia coli. Proc Natl Acad Sci USA 2001; 98: 8128–8132
   PubMedGoogle Scholar
• Mukerjea R, Robyt JF. Starch biosynthesis: the primer nonreducing-end mechanism versus the nonprimer reducing-end two-site insertion mechanism. Carbohydr Res 2004; 340: 245–255
   Google Scholar
• Mukerjea R, Yu L, Robyt JF. Starch biosynthesis: mechanism for the elongation of starch chains. Carbohydr Res 2002; 337: 1015–1022
   PubMedGoogle Scholar
• Müller-Röber BT, Sonnewald U, Willmitzer L. Inhibition of the ADP-glucose pyrophosphorylase in transgenic potatoes leads to sugar-storing tubers and influences tuber formation and expression of tuber storage protein genes. EMBO J 1992; 11: 1229–1238
   PubMed Web of Science ®Google Scholar
• Muñoz, FJ, Baroja-Fernández, E, Morán-Zorzano, MT, Viale, AM, Etxeberria, E, Alonso-Casajús, N, Pozueta-Romero, J. (2005). Sucrose synthase controls both intracellular ADPglucose levels and transitory starch biosynthesis in source leaves. Plant Cell Physiol, (in press).
   Google Scholar
• Murata T, Minamikawa T, Akazawa T. Adenosine diphosphate glucose in rice and its role in starch synthesis. Biochem Biophys Res Commun 1963; 13: 439–443
   Google Scholar
• Naeem M, Tetlow IJ, Emes MJ. Starch synthesis in amyloplasts purified from developing tubers. Plant J 1997; 11: 1095–1103
   Google Scholar
• Nakai T, Konishi T, Zhang X-Q, Chollet R, Tonouchi N, Tsuchida T, Yoshinaga F, Mori H, Sakai F, Hayashi T. An increase in apparent affinity for sucrose of mung bean sucrose synthase is caused by in vitro phosphorylation or directed mutagenesis of Ser11. Plant Cell Physiol 1998; 39: 1337–1341
   PubMed Web of Science ®Google Scholar
• Neuhaus HE, Kruckeberg AL, Feil R, Stitt M. Reduced-activity mutants of phosphoglucose isomerase in the cytosol and chloroplast of Clarkia xantiana. Planta 1989; 178: 110–122
   PubMedGoogle Scholar
• Neuhaus HE, Thom E, Möhlmann T, Steup M, Kampfenkel K. Characterization of a novel eukaryotic ATP/ADP translocator located in the plastid envelope of Arabidopsis thaliana L. Plant J 1997; 11: 73–82
   PubMedGoogle Scholar
• Nguyen-Quoc B, Foyer CH. A role for ‘futile cycles’ involving invertase and sucrose synthase in sucrose metabolism of tomato fruit. J Exp Bot 2001; 52: 881–889
   PubMedGoogle Scholar
• Niittylä T, Messerli G, Trevisan M, Chen J, Smith AM, Zeeman SC. A novel maltose transporter essential for starch degradation in leaves. Science 2004; 303: 881–889
   Google Scholar
• Okita TW. Is there an alternative pathway for starch synthesis?. Plant Physiol 1992; 100: 560–564
   PubMedGoogle Scholar
• Patron NJ, Greber B, Fahy BF, Laurie DA, Parker ML, Denyer K. The lys5 mutations of barley reveal the nature and importance of plastidial ADP-glc transporters for starch synthesis in cereal endosperm. Plant Physiol 2004; 135: 2088–2097
   PubMedGoogle Scholar
• Porchia AC, Curatti L, Salerno GL. Sucrose metabolism in cyanobacteria: sucrose synthase from Anabaena sp. strain PCC 7119 is remarkably different from the plant enzymes with respect to substrate affinity and amino-terminal sequence. Planta 1999; 210: 34–40
   PubMedGoogle Scholar
• Pozueta-Romero J, Akazawa T. Biochemical mechanism of starch biosynthesis in amyloplasts from cultured cells of sycamore (Acer pseudoplatanus). J Exp Bot 1993; 44S: 297–306
   Google Scholar
• Pozueta-Romero J, Ardila F, Akazawa T. ADP-glucose transport by the chloroplast adenylate translocator is linked to starch biosynthesis. Plant Physiol 1991a; 97: 1565–1572
   PubMed Web of Science ®Google Scholar
• Pozueta-Romero J, Frehner M, Viale A, Akazawa T. Direct transport of ADPglucose by an adenylate translocator is linked to starch biosynthesis in amyloplasts. Proc Natl Acad Sci USA 1991b; 88: 5769–5773
   PubMed Web of Science ®Google Scholar
• Pozueta-Romero J, Perata P, Akazawa T. Sucrose-starch conversion in heterotrophic tissues of plants. Crit Rev Plant Sci 1999; 18: 489–525
   Web of Science ®Google Scholar
• Pozueta-Romero J, Pozueta-Romero D, González P, Etxeberria E. Activity of membrane-associated sucrose synthase is regulated by its phosphorylastion status in cultured cells of sycamore (Acer pseudoplatanus). Physiol Plantarum 2004; 122: 275–280
   Google Scholar
• Preiss J. (1988). In: The biochemistry of plants. Preiss, J. editor. Academic Press, NY. Vol. 14, pp. 181–254.
   Google Scholar
• Recondo E, Dankert M, Leloir LF. Adenosine diphosphate glucose and starch synthesis. Biochem Biophys Res Commun 1963; 12: 204–207
   Google Scholar
• Riesmeier JW, Flügge UI, Schulz B, Heineke D, Heldt HW, Willmitzer L, Frommer WB. Antisense repression of the chloroplast triose phosphate translocator affects carbon partitioning in transgenic potato plants. Proc Natl Acad Sci USA 1993; 90: 6160–6164
   PubMed Web of Science ®Google Scholar
• Rodríguez-López M, Baroja-Fernández E, Zandueta-Criado A, Pozueta-Romero J. Adenosine diphosphate glucose pyrophosphatase: a plastidial phosphodiesterase that prevents starch biosynthesis. Proc Natl Acad Sci USA 2000; 97: 8705–8710
   PubMedGoogle Scholar
• Roscher A, Emsley L, Raymond P, Roby C. Unidirectional steady state rates of central metabolism enzymes measured simultaneously in a living plant tissue. J Biol Chem 1998; 273: 25053–25061
   PubMed Web of Science ®Google Scholar
• Ruan Y-L, Llewellyn DJ, Furbank RT. A fiberless seed mutation in cotton is associated with lack of fibre cell initiation in ovule epidermis and alterations in sucrose synthase expression and carbon partitioning in developing seeds. Plant Cell 2003; 15: 952–964
   PubMed Web of Science ®Google Scholar
• Saether N, Iversen T-H. Gravitropism and starch statoliths in an Arabidopsis mutant. Planta 1991; 184: 491–497
   PubMedGoogle Scholar
• Sakulsingharoj C, Choi S-B, Hwang S-K, Edwards GE, Bork J, Meyer CR, Preiss J, Okita TW. Engineering starch biosynthesis for increasing rice seed weight: the role of the cytoplasmic ADP-glucose pyrophosphorylase. Plant Sci 2004; 167: 1323–1333
   Web of Science ®Google Scholar
• Scheidig A, Fröhlich A, Schulze S, Lloyd JR, Kossmann J. Downregulation of a chloroplast-targeted b-amylase leads to a starch-excess phenotype in leaves. Plant J 2002; 30: 581–591
   PubMed Web of Science ®Google Scholar
• Schneider A, Häusler RE, Kolukisaoglu Ü, Kunze R, van der Graaff E, Schwacke R, Catoni E, Desimone M, Flügge U-I. An Arabidopsis thaliana knock-out mutant of the chloroplast triose phosphate/phosphate translocator is severely compromised only when starch synthesis, but not starch mobilisation is abolished. Plant J 2002; 32: 685–699
   PubMed Web of Science ®Google Scholar
• Scott P, Kruger NJ. Influence of elevated fructose-2,6-bisphosphate levels on starch mobilization in transgenic tobacco leaves in the dark. Plant Physiol 1995; 108: 1569–1577
   PubMedGoogle Scholar
• Shannon JC, Pien F-M, Liu K-C. Nucleotides and nucleotide sugars in developing maize endosperms. Synthesis of ADP-glucose in brittle 1. Plant Physiol 1996; 110: 835–843
   PubMedGoogle Scholar
• Shannon JC, Pien F-M, Cao H, Liu K-C. Brittle-1, an adenylate translocator, facilitates transfer of extraplastidial synthesized ADP-glucose into amyloplasts of maize endosperms. Plant Physiol 1998; 117: 1235–1252
   PubMedGoogle Scholar
• Silvius JE, Snyder FW. Comparative enzymic studies of sucrose metabolism in the taproots and fibrous roots of Beta vulgaris L. Plant Physiol 1979; 64: 1070–1073
   PubMedGoogle Scholar
• Smidansky ED, Clancy M, Meyer FD, Lanning SP, Blake NK, Talbert LE, Giroux MJ. Enhanced ADP-glucose pyrophosphorylase activity in wheat endosperm increases seed yield. Proc Natl Acad Sci USA 2002; 99: 1724–1729
   PubMed Web of Science ®Google Scholar
• Smith AM, Neuhaus HE, Stitt M. The impact of decreased activity of starch-branching enzyme on photosynthetic starch synthesis in leaves of wrinkled-seeded peas. Planta 1990; 181: 310–315
   PubMedGoogle Scholar
• Smith AM, Zeeman SC, Smith SM. Starch degradation. Ann Rev Plant Biol 2005; 56: 73–98
   PubMed Web of Science ®Google Scholar
• Sonnewald U, Hajirezaei MR, Kossmann J, Heyer A, Trethewey RN, Willmitzer L. Expression of a yeast invertase in the apoplast of potato tubers increased tuber size. Nat Biotechnol 1997; 15: 794–797
   PubMedGoogle Scholar
• Stark DM, Timmerman KP, Barry GF, Preiss J, Kishore GM. Regulation of the amount of starch in plant tissues by ADPglucose pyrophosphorylase. Science 1992; 258: 287–292
   PubMed Web of Science ®Google Scholar
• Steup, M. (1988). In: The biochemistry of plants. Stumpf PK, Conn EE editors. Academic Press, NY. Vol. 14, pp. 255–295.
   Google Scholar
• Stitt M, ap Rees T. Carbohydrate breakdown by chloroplasts of Pisum sativum. Biochim Biophys Acta 1980; 627: 131–143
   PubMedGoogle Scholar
• Stitt M, Heldt HW. Simultaneous synthesis and degradation of starch in spinach chloroplasts in the light. Biochim Biophys Acta 1981a; 638: 1–11
   Google Scholar
• Stitt M, Heldt HW. Physiological rates of starch breakdown in isolated intact spinach chloroplasts. Plant Physiol 1981b; 68: 755–761
   PubMedGoogle Scholar
• Strand A, Zrenner R, Trevanion S, Stitt M, Gustafsson P, Gardeström P. Decreased expression of two key enzymes in the sucrose biosynthesis pathway, cytosolic fructose-1,6-bisphosphatase and sucrose phosphate synthase, has remarkably different consequences for photosynthetic carbon metabolism in transgenic Arabidopsis thaliana. Plant J 2000; 23: 759–770
   PubMed Web of Science ®Google Scholar
• Sullivan TD, Kaneko Y. The maize brittle 1 gene encodes amyloplast membrane polypeptides. Planta 1995; 196: 477–484
   PubMedGoogle Scholar
• Sweetlove LJ, Burrell MM, ap Rees T. Starch metabolism in tubers of transgenic potato (Solanum tuberosum) with increased ADPglucose pyrophosphorylase. Biochem J 1996; 320: 493–498
   PubMedGoogle Scholar
• Tanase K, Yamaki S. Purification and characterization of two sucrose synthase isoforms from japanese pear fruit. Plant Cell Physiol 2000; 41: 408–414
   Google Scholar
• Tang G-Q, Sturm A. Antisense repression of sucrose synthase in carrot (Daucus carota L.) affects growth rather than sucrose partitioning. Plant Mol Biol 1999; 41: 465–479
   PubMedGoogle Scholar
• Tauberger E, Fernie AR, Emmermann M, Renz A, Kossmann J, Willmitzer L, Trethewey RN. 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 2000; 23: 43–53
   PubMedGoogle Scholar
• Tetlow IJ, Davies EJ, Vardy KA, Bowsher CG, Burrell MM, Emes MJ. Starch synthesis and carbohydrate oxidation in amyloplasts from developing wheat endosperm. J Exp Bot 2003; 54: 715–725
   PubMedGoogle Scholar
• Tetlow IJ, Morell MK, Emes MJ. Recent developments in understanding the regulation of starch metabolism in higher plants. J Exp Bot 2004; 55: 2131–2145
   PubMed Web of Science ®Google Scholar
• Thornbjørnsen T, Villand P, Denyer K, Olsen O-A, Smith AM. Distinct isoforms of ADPglucose pyrophosphorylase occur inside and outside the amyloplast in barley endosperm. Plant J 1996a; 10: 243–250
   Google Scholar
• Thornbjørnsen T, Villand P, Kleczkowski LA, Olsen OA. A single gene encodes two different transcripts of ADP-glucose pyrophosphorylase small subunit from barley (Hordeum vulgare). Biochem J 1996b; 313: 149–154
   PubMedGoogle Scholar
• Trethewey RN, Fernie AR, Bachmann A, Fleischer-Notter H, Geigenberger P, Willmitzer L. Expression of a bacterial sucrose phosphorylase in potato tubers results in a glucose-independent induction of glycolysis. Plant Cell Environ 2001; 24: 357–365
   Google Scholar
• Trethewey RN, Geigenberger P, Riedel K, Hajirezaei M-R, Sonnewald U, Stitt M, Riesmeier JW, Willmitzer L. Combined expression of glucokinase and invertase in potato tubers leads to a dramatic reduction in starch accumulation and a stimulation of glycolysis. Plant J 1998; 15: 109–118
   PubMedGoogle Scholar
• Tsai CY, Nelson OE. Starch-deficient maize mutant lacking adenosine diphosphate glucose pyrophosphorylase activity. Science 1966; 151: 341–343
   PubMedGoogle Scholar
• Villand P, Kleczkowski LA. Is there an alternative pathway for starch biosynthesis in cereal seeds?. Z Naturforsch 1994; 49: 215–219
   Google Scholar
• Wang A-Y, Kao M-H, Yang W-H, Sayion Y, Liu L-F, Lee P-D, Su J-C. Differentially and developmentally regulated expression of three rice sucrose synthase genes. Plant Cell Physiol 1999; 40: 800–807
   PubMedGoogle Scholar
• Weber H, Rolletschek H, Heim U, Golombek S, Gubatz S, Wobus U. Antisense-inhibition of ADP-glucose pyrophosphorylase in developing seeds of Vicia narbonensis moderately decreases starch but increases protein content and affects seed maturation. Plant J 2000; 24: 33–43
   PubMedGoogle Scholar
• Yu T-S, Lue W-L, Wang S-M, Chen J. Mutation of Arabidopsis plastid phosphoglucose isomerase affects leaf starch synthesis and floral initiation. Plant Physiol 2000; 123: 319–325
   PubMedGoogle Scholar
• Zeeman SC, Tiessen A, Pilling E, Kato KL, Donald AM, Smith AM. Starch synthesis in Arabidopsis. Granule synthesis, composition, and structure. Plant Physiol 2002; 129: 516–529
   PubMedGoogle Scholar
• Zervosen A, Römer U, Elling L. Application of recombinant sucrose synthase-large scale synthesis of ADP-glucose. J Mol Catal 1998; 5: 25–28
   Google Scholar
• Zrenner R, Krause KP, Apel P, Sonnewald U. Reduction of the cytosolic fructose-1,6-bisphosphatase in transgenic potato plants limits photosynthetic sucrose biosynthesis with no impact on plant growth and tuber yield. Plant J 1996; 9: 671–681
   PubMed Web of Science ®Google Scholar
• Zrenner R, Salanoubat M, Willmitzer L, Sonnewald U. Evidence of the crucial role of sucrose synthase for sink strength using transgenic potato plants (Solanum tuberosum L.). Plant J 1995; 7: 97–107
   PubMed Web of Science ®Google Scholar
• Zrenner R, Willmitzer L, Sonnewald U. Analysis of the expression of potato uridinediphosphate-glucose pyrophosphorylase and its inhibition by antisense RNA. Planta 1993; 190: 247–252
   PubMed Web of Science ®Google Scholar