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2008 | 55 | 3 | 435-445
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Starch metabolism in leaves

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Starch is the most abundant storage carbohydrate produced in plants. The initiation of transitory starch synthesis and degradation in plastids depends mainly on diurnal cycle, post-translational regulation of enzyme activity and starch phosphorylation. For the proper structure of starch granule the activities of all starch synthase isoenzymes, branching enzymes and debranching enzymes are needed. The intensity of starch biosynthesis depends mainly on the activity of AGPase (adenosine 5'-diphosphate glucose pyrophosphorylase). The key enzymes in starch degradation are β-amylase, isoamylase 3 and disproportionating enzyme. However, it should be underlined that there are some crucial differences in starch metabolism between heterotrophic and autotrophic tissues, e.g. is the ability to build multiprotein complexes responsible for biosynthesis and degradation of starch granules in chloroplasts. The observed huge progress in understanding of starch metabolism was possible mainly due to analyses of the complete Arabidopsis and rice genomes and of numerous mutants with altered starch metabolism in leaves. The aim of this paper is to review current knowledge on transient starch metabolism in higher plants.
Physical description
  • Department of Biochemistry, Faculty of Agriculture and Biology, Warsaw University of Life Sciences (SGGW), Warszawa, Poland
  • Alexander RD, Morris PC (2006) A proteomic analysis of 14-3-3 binding proteins from developing barley grains. Proteomics 6: 1886-1896.
  • Ball S, Morell MK (2003) From bacterial glycogen to starch: understanding the biogenesis of the plant starch granule. Annu Rev Plant Biol 54: 207-233.
  • Ball S, Guan H, James M, Myers A, Keeling P, Mouille G, Buleon A, Colonna P, Preiss J (1996) From glycogen to amylopectin: a model for the biogenesis of the plant starch granule. Cell 86: 349-352.
  • Bläsing OE, Gibon Y, Günther M, Höhne M, Morcuende R, Osuna D, Thimm O, Usadel B, Scheible WR, Stitt M (2005) Sugars and circadian regulation make major contributions to the global regulation of diurnal gene expression in Arabidopsis. Plant Cell 17: 3257-3281.
  • Blauth SL, Kim K-N, Klucinec J, Shannon JC, Thompson D, Guiltinan M (2002) Identification of Mutator insertional mutants of starch-branching enzyme 1 (sbe1) in Zea mays L. Plant Mol Biol 48: 287-297.
  • Borovsky D, Smith EE, Whelan WJ (1975) Purification and properties of potato 1,4-α-d-glucan: 1,4-α-d-glucan 6-α-(1,4-α-glucano)-transferase. Evidence against a dual catalytic function in amylose-branching enzyme. Eur J Biochem 59: 615-625.
  • Buchanan BB, Schurmann P, Wolosiuk RA, Jacquot JP (2002) The ferredoxin/thioredoxin system: from discovery to molecular structures and beyond. Photosynth Res 73: 215-222.
  • Buleon A, Colonna P, Planchot V, Ball S (1998) Starch granules: structure and biosynthesis. Int J Biol Macromol 23: 85-112.
  • Burton RA, Bewley JD, Smith AM, Bhattacharyya MK, Tatge H, Ring S, Bull V, Hamilton WD, Martin C (1995) Starch branching enzymes belonging to distinct enzyme families are differentially expressed during pea embryo development. Plant J 7: 3-15.
  • Burton RA, Jenner H, Carrangis L, Fahy B, Fincher GB, Hylton C, Laurie DA, Parker M, Waite D, van Wegen S, Verhoeven T, Denyer K (2002) Starch granule initiation and growth are altered in barley mutants that lack isoamylase activity. Plant J 31: 97-112.
  • Bustos R, Fahy B, Hylton CM, Seale R, Nebane NM, Edwards A, Martin C, Smith AM (2004) Starch granule initiation is controlled by a heteromultimeric isoamylase in potato tubers. Proc Natl Acad Sci USA 101: 2215-2220.
  • Caspar T (1994) Genetic dissection of the biosynthesis, degradation and biological functions of starch. In Arabidopsis. Meyerowitz EM, Somerville CR eds, pp 913-936. Cold Spring Harbor Laboratory Press, New York.
  • Caspar T, Lin T-P, Kakefuda G, Benbow L, Preiss J, Somerville Ch (1991) Mutants of Arabidopsis with altered regulation of starch degradation Plant Physiol 95: 1181-1188.
  • Chia T, Thorneycroft D, Chapple A, Messerli G, Chen J, Zeeman SC, Smith SM, Smith AM (2004) A cytosolic glucosyltransferase is required for conversion of starch to sucrose in Arabidopsis leaves at night. Plant J 37: 853-863.
  • Cossegal M, Chambrier P, Mbelo S, Balzergue S, Martin-Magniette M-L, Moing A, Deborde C, Guyon V, Perez P, Rogowsky P (2008) Transcriptional and metabolic adjustments in ADP-glucose pyrophosphorylase-deficient bt2 maize kernels. Plant Physiol 146: 1553-1570.
  • Critchley JH, Zeeman SC, Takaha T, Smith AM, Smith SM (2001) A critical role for disproportionating enzyme in starch breakdown is revealed by a knock-out mutant in Arabidopsis. Plant J 26: 89-100.
  • Delatte T, Umhang M, Trevisan M, Eicke S, Thorneycroft D, Smith SM, Zeeman SC (2006) Evidence for distinct mechanisms of starch granule breakdown in plants. J Biol Chem 281: 12050-12059.
  • Denyer K, Dunlap F, Thorbjørnsen T, Keeling P, Smith AM (1996) The major form of ADP-glucose pyrophosphorylase in maize endosperm is extra-plastidial. Plant Physiol 112: 779-783.
  • Dinges JR, Colleoni C, Myers AM, James MG (2001) Molecular structure of three mutations at the maize sugary1 locus and their allele-specific phenotypic effects. Plant Physiol 125: 1406-1418.
  • Dinges JR, Colleoni C, James MG, Myers AM (2003) Mutational analysis of the pullulanase-type debranching enzyme of maize indicates multiple functions in starch metabolism. Plant Cell 15: 666-680.
  • Edner Ch, Li J, Albrecht T, Mahlow S, Hejazi M, Hussain H, Kaplan F, Guy Ch, Smith SM, Steup M, Ritte G (2007) Glucan, water dikinase activity stimulates breakdown of starch granules by plastidial β-amylases. Plant Physiol 145: 17-28.
  • Edwards A, Fulton DC, Hylton CM, Jobling SA, Gidley M, Roessner U, Martin C, Smith AM (1999) A combined reduction in activity of starch synthases II and III of potato has novel effects on the starch of tubers. Plant J 17: 251-261.
  • Engelsen SB, Madsen A, Blennow A, Motawia MS, Møller BL, Larsen S (2003) The phosphorylation site in double helical amylopectin as investigated by a combined approach using chemical synthesis, crystallography and molecular modelling. FEBS Lett 541: 137-144.
  • Fettke J, Chia T, Eckermann N, Smith A, Steup M (2006a) A transglucosidase necessary for starch degradation and maltose metabolism in leaves at night acts on cytosolic heteroglycans (SHG). Plant J 46: 668-684.
  • Fettke J, Eckermann N, Kötting O, Ritte G, Steup M (2006b) Novel starch-related enzymes and carbohydrates. Cell Mol Biol 52 (Suppl) OL883-OL904.
  • Fettke J, Eckermann N, Tiessen A, Geigenberger P, Steup M (2005) Identification, subcellular localization and biochemical characterization of water-soluble heteroglycans (SHG) in the leaves of Arabidopsis thaliana L.: distinct SHG reside in the cytosol and in the apoplast. Plant J 43: 568-585.
  • Fondy BR, Geiger DR, Servaites JC (1989) Photosynthesis, carbohydrate metabolism and export in Beta vulgaris L. and Phasoleus vulgaris L. during square and sinusoidal light regimes. Plant Physiol 89: 396-402.
  • Fordham-Skelton AP, Chilley P, Lumbreras V, Reignoux S, Fenton TR, Dahm CC, Pages M, Gatehouse JA (2002) A novel higher plant protein tyrosine phosphatase interacts with SNF1-related protein kinases via a KIS (kinase interaction sequence) domain. Plant J 29: 705-715.
  • Fu Y, Ballicora MA, Leykam J, Preiss J (1998) Mechanism of reductive activation of potato tuber ADP-glucose pyrophosphorylase. J Biol Chem 273: 25045-25052.
  • Fujita N, Taira T (1998) A 56-kDa protein is a novel granule bound starch synthase existing in the pericarps, aleurone layers, and embryos of immature seed in diploid wheat (Triticum monococcum L.). Planta 207: 125-132.
  • Fulton DC, Stettler M, Mettler T, Vaughan CK, Li J, Francisco P, Gil M, Reinhold H, Eicke S, Messerli G, Dorken G, Halliday K, Smith AM, Smith SM, Zeeman SC (2008) β-Amylase 4, a noncatalytic protein required for starch breakdown, acts upstream of three active α-amylases in Arabidopsis chloroplasts Plant Cell 20: 1040-1058.
  • Geigenberger P, Kolbe A, Tiessen A (2005) Redox regulation of carbon storage and partitioning in response to light and sugars. J Exp Bot 56: 1469-1479.
  • Gibon Y, Bläsing OE, Palacios-Rojas N, Pankovic D, Hendriks JH, Fisahn J, Höhne M, Gunther M, Stitt M (2004) Adjustment of diurnal starch turnover to short days, depletion of sugar during the night leads to a temporary inhibition of carbohydrate utilization, accumulation of sugars and post-translational activation of ADP-glucose pyrophosphorylase in the following light period. Plant J 39: 847-862.
  • Glaring MA, Zygadlo A, Thorneycroft D, Schulz A, Smith SM, Blennow A, Baunsgaard L (2007) An extra-plastidial-glucan, water dikinase from Arabidopsis phosphorylates amylopectin in vitro and is not necessary for transient starch degradation. J Exp Bot 58: 3949-3960.
  • Guan H-P, Preiss J (1993) Differentiation of the properties of the branching isozymes from maize (Zea mays). Plant Physiol 102: 1269-1273.
  • Hejazi M, Fettke J, Haebel S, Edner C, Paris O, Frohberg C, Steup M, Ritte G (2008) Glucan, water dikinase phosphorylates crystalline maltodextrins and thereby initiates solubilization. Plant J 55: 323-334.
  • Hendriks JHM, Kolbe A, Gibon Y, Stitt M, Geigenberger P (2003) ADP-glucose pyrophosphorylase is activated by post-translational redox-modification in response to light and to sugars in leaves of Arabidopsis and other plant species. Plant Physiol 133: 838-849.
  • Hennen-Bierwagen TA, Liu F, Marsh RS, Kim S, Gan Q, Tetlow IJ, Emes MJ, James MG, Myers AM (2008) Starch biosynthetic enzymes from developing maize endosperm associate in multisubunit complexes Plant Physiol 146: 1892-1908.
  • Hizukuri S (1986) Polymodal distribution of the chain lengths of amylopectin, and its significance. Carbohydr Res 147: 342-347.
  • Jenkins PJ, Donald AM (1995) The influence of amylose on starch granule structure. Int J Biol Macromol 17: 315-321.
  • Jobling SA, Schwall GP, Westcott RJ, Sidebottom CM, Debet M, Gidley MJ, Jeffcoat R, Safford R (1999) A minor form of starch branching enzyme in potato (Solanum tuberosum L.) tubers has a major effect on starch structure: cloning and characterisation of multiple forms of SBE A. Plant J 18: 163-171.
  • Johnson PE, Patron NJ, Bottrill AR, Dinges JR, Fahy BF, Parker ML, Waite DN, Denyer K (2003) A low-starch barley mutant, Risø 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 131: 684-696.
  • Kaplan F, Guy CL (2005) RNA interference of Arabidopsis beta-amylase8 prevents maltose accumulation upon cold shock and increases sensitivity of PSII photochemical efficiency to freezing stress. Plant J 44: 730-744.
  • Kawagoe Y, Kubo A, Satoh H, Takaiwa F, Nakamura Y (2005) Roles of isoamylase and ADP-glucose pyrophosphorylase in starch granule synthesis in rice endosperm. Plant J 42: 164-174.
  • Kerk D, Conley TR, Rodriguez FA, Tran HT, Nimick M, Muench D, Moorhead GB (2006) A chloroplast-localized dual-specificity protein phosphatase in Arabidopsis contains a phylogenetically dispersed and ancient carbohydrate-binding domain, which binds the polysaccharide starch. Plant J 46: 400-413.
  • Kleczkowski LA (1999) A phosphoglycerate to inorganic phosphate ratio is the major factor in controlling starch levels in chloroplasts via ADP-glucose pyrophosphorylase regulation. FEBS Lett 448: 153-156.
  • Kleczkowski LA (2000) Is leaf ADP-glucose pyrophosphorylase an allosteric enzyme? Biochim Biophys Acta 1476: 103-108.
  • Kleczkowski LA (2001) A new player in the starch field. Plant Physiol Biochem 39: 759-761.
  • Kleczkowski LA, Sokolov LN, Luo Ch, Villand P (1999) Molecular cloning and spatial expression of an ApL1 cDNA for the large subunit of ADP-glucose pyrophosphorylase from Arabidopsis thaliana. Z Naturforsch C 54: 353-358.
  • Klimecka M, Muszyńska G (2007) Structure and functions of plant calcium-dependent protein kinases. Acta Biochim Polon 54: 219-233.
  • Kolbe A, Tiessen A, Schluepmann H, Paul M, Ulrich S, Geigenberger P (2005) Trehalose 6-phosphate regulates starch synthesis via post-translational redox activation of ADP-glucose pyrophosphorylase. Proc Natl Acad Sci USA 102: 11118-11123.
  • Kötting O, Pusch K, Tiessen A, Geigenberger P, Steup M, Ritte G (2005) Identification of a novel enzyme required for starch metabolism in Arabidopsis leaves. The phosphoglucan, water dikinase. Plant Physiol 137: 242-252.
  • Lao NT, Schoneveld O, Mould RM, Hibberd JM, Gray JC, Kavanagh TA (1999) An Arabidopsis gene encoding a chloroplast-targeted β-amylase. Plant J 20: 519-527.
  • Li L, Ilarslan H, James MG, Myers AM, Wurtele ES (2007) Genome wide co-expression among the starch debranching enzyme genes AtISA1, AtISA2, and AtISA3 in Arabidopsis thaliana. J Exp Bot 58: 3323-3342.
  • Lloyd JR, Landschutze V, Kossmann J (1999) Simultaneous antisense inhibition of two starch-synthase isoforms in potato tubers leads to accumulation of grossly modified amylopectin. Biochem J 338: 515-521.
  • Lloyd JR, Kossmann J, Ritte G (2005) Leaf starch degradation comes out of the shadows. Trends Plant Sci 10: 130-137.
  • Lorberth R, Ritte G, Willmitzer L, Kossmann J (1998) Inhibition of a starch-granule-bound protein leads to modified starch and repression of cold sweetening. Nat Biotechnol 16: 473-479.
  • Lovegrove A, Hooley R (2000) Gibberellin and abscisic acid signalling in aleurone. Trends Plant Sci 5: 102-110.
  • Lu Y, Gehan JP, Sharkey TD (2005) Daylength and circadian effects on starch degradation and maltose metabolism. Plant Physiol 138: 2280-2291.
  • Lu Y, Steichen JM, Yao J, Sharkey TD (2006) The role of cytosolic α-glucan phosphorylase in maltose metabolism and the comparison of amylomaltase in Arabidopsis and Escherichia coli. Plant Physiol 142: 878-889.
  • Messerli G, Nia VP, Trevisan M, Kolbe A, Schauer N, Geigenberger P, Chen J, Davison AC, Fernie AR, Zeeman SC (2007) Rapid classification of phenotypic mutants of Arabidopsis via metabolite ringerprinting. Plant Physiol 143: 1484-1492.
  • Mikkelsen R, Mutenda KE, Mant A, Schürmann P, Blennow A (2005) α-glucan, water dikinase (GWD): A plastidic enzyme with redox-regulated and coordinated catalytic activity and binding affinity. Proc Natl Acad Sci USA 102: 1785-1790.
  • Morell MK, Kosar-Hashemi B, Cmiel M, Samuel MS, Chandler P, Rahman S, Buleon A, Batey IL, Li Z (2003) Barley sex6 mutants lack starch synthase IIa activity and contain a starch with novel properties. Plant J 34: 173-185.
  • Mouille G, Maddelein M-L, Libessart N, Talaga P, Decq A, Delrue B, Ball S (1996) Phytoglycogen processing: a mandatory step for starch biosynthesis in plants. Plant Cell 8: 1353-1366.
  • Myers AM, Morel MK, James MG, Ball SG (2000) Recent progress toward understanding biosynthesis of the amylopectin crystal. Plant Physiol 122: 989-997.
  • Nakamura Y (2002) Towards a better understanding of the metabolic system for amylopectin biosynthesis in plants: rice endosperm as a model tissue. Plant Cell Physiol 43: 718-725.
  • Nelson OE, Rines HW (1962) The enzymatic deficiency in the waxy mutant of maize. Biochem Biophys Res Commun 9: 297-300.
  • Niittylä T, Messerli G, Trevisan M, Chen J, Smith AM, Zeeman SC (2004) A previously unknown maltose transporter essential for starch degradation in leaves. Science 303: 87-89.
  • Niittylä T, Comparot-Moss S, Lue WL, Messerli G, Trevisan M, Seymour MDJ, Gatehouse JA, Villadsen D, Smith SM, Chen J, Zeeman SC, Smith AM (2006) Similar protein phosphatases control starch metabolism in plant and glycogen metabolism in mammals. J Biol Chem 281: 11815-11818.
  • Nishi A, Nakamura Y, Tanaka N, Satoh H (2001) Biochemical and genetic effects of amylose-extender mutation in rice endosperm. Plant Physiol 127: 459-472.
  • Ohdan T, Francisco Jr PB, Sawada T, Hirose T, Terao T, Satoh H, Nakamura Y (2005) Expression profiling of genes involved in starch synthesis in sink and source organs of rice. J Exp Bot 56: 3229-3244.
  • Rahman S, Regina A, Li Z, Mukai Y, Yamamoto M, Kosar-Hashemi B, Abrahams S, Morell MK (2001) Comparison of starch-branching enzyme genes reveals evolutionary relationships among isoforms. Characterization of a gene for starch-branching enzyme IIa from wheat D genome donor Aegilops tauschii. Plant Physiol 125: 1314-1324.
  • Regina A, Bird D, Topping D, Bowden S, Freeman J, Barsby T, Kosar-Hashemi B, Li Z, Rahman S, Morell M (2006) High amylose wheat generated by RNA-interference improves indices of large bowel health in rats. Proc Natl Acad Sci USA 103: 3546-3551.
  • Ritchie S, Swanson SJ, Gilroy S (2000) Physiology of the aleurone layer and starchy endosperm during grain development and early seedling growth: new insights from cell and molecular biology. Seed Sci Res 10: 193-212.
  • Ritte G, Lorberth R, Steup M (2000) Reversible binding of the starch-related R1 protein to the surface of transitory starch granule. Plant J 21: 387-391.
  • Ritte G, Lloyd JR, Eckermann N, Rotmann A, Kossmann J, Steup M (2002) The starch related R1 protein is an α-glucan, water dikinase. Proc Natl Acad Sci USA 99: 7166-7171.
  • Ritte G, Heydenreich M, Mahlow S, Haebel S, Kötting O, Steup M (2006) Phosphorylation of C6- and C3-positions of glucosyl residues in starch is catalysed by distinct dikinases. FEBS Lett 580: 4872-4876.
  • Rösti S, Rudi H, Rudi K, Opsahl-Sorteberg H-G, Fahy B, Denyer K (2006) The gene encoding the cytosolic small subunit of ADP-glucose pyrophosphorylase in barley endosperm also encodes the major plastidial small subunit in the leaves J Exp Bot 57: 3619-3626.
  • Safford R, Jobling SA, Sidebottom CM, Westcott RJ, Cooke D, Tober KJ, Strongitharm BH, Russell AL, Gidley MJ (1998) Consequences of antisense RNA inhibition of starch branching enzyme activity on properties of potato starch. Carbohydr Polym 35: 155-168.
  • Satoh H, Nishi A, Yamashita K, Takemoto Y, Tanaka Y, Hosaka Y, Sakurai A, Fujita N, Nakamura Y (2003) Starch-branching enzyme I-deficient mutation specifically affects the structure and properties of starch in rice endosperm. Plant Physiol 133: 1111-1121.
  • Scheidig A, Frölich A, Schulze S, Lloyd JR, Kossmann J (2002) Downregulation of a chloroplast-targeted β-amylase leads to a starch-excess phenotype in leaves. Plant J 30: 581-591.
  • Sehnke PC, Chung H-J, Wu K, Ferl RJ (2001) Regulation of starch accumulation by granule-associated plant 14-3-3 proteins. Proc Natl Acad Sci USA 98: 765-770.
  • Siedlecka A, Ciereszko I, Mellerowicz E, Martz F, Chen J, Kleczkowski LA (2003) The small subunit ADP-glucose pyrophosphorylase (ApS) promoter mediates okadaic acid-sensitive uidA expression in starch-synthesizing tissues and cells in Arabidopsis. Planta 217: 184-192.
  • Smith AM, Stitt M (2007) Coordination of carbon supply and plant growth. Plant Cell Environ 30: 1126-1149.
  • Smith AM, Denyer K, Martin C (1997) The synthesis of the starch granule. Annu Rev Plant Physiol Plant Mol Biol 48: 67-87.
  • Smith SM, Fulton DC, Chia T, Thorneycroft D, Chapple A, Dunstan H, Hylton C, Zeeman SC, Smith AM (2004) Diurnal changes in the transcriptome encoding enzymes of starch metabolism provide evidence for both transcriptional and posttranscriptional regulation of starch metabolism in Arabidopsis leaves. Plant Physiol 136: 2687-2699.
  • Smith AM, Zeeman SC, Smith SM (2005) Starch degradation. Annu Rev Plant Biol 56: 73-98.
  • Sokolov LN, Dejardin A, Kleczkowski LA (1998) Sugars and light/dark exposure trigger differential regulation of ADP-glucose pyrophosphorylase genes in Arabidopsis thaliana (thale cress). Biochem J 336: 681-687.
  • Sokolov LN, Dominguez-Solis JR, Allary A-L, Buchanan BB, Luan S (2006) A redox-regulated chloroplast protein phosphatase binds to starch diurnally and functions in its accumulation. Proc Natl Acad Sci USA 103: 9732-9737.
  • Sparla F, Costa A, Lo Schiavo F, Pupillo P, Trost P (2006) Redox regulation of a novel plastid-targeted β-amylase of Arabidopsis thaliana. Plant Physiol 141: 840-850.
  • Stanley D, Farnden KJF, MacRae EA (2005) Plant α-amylases: functions and roles in carbohydrate metabolism. Biologia (Bratis) 16: 65-71.
  • Stitt M, Gerhardt R, Kurzel B, Heldt HW (1983) A role for fructose 2,6-bisphosphate in the regulation of sucrose synthesis in spinach leaves. Plant Physiol 72: 1139-1141.
  • Tester RF, Karkalas J, Qi X (2004) Starch structure and digestibility enzyme-structure relationship. World's Poultry Sci J 60: 186-195.
  • Tetlow IJ, Morell MK, Emes MJ (2004a) Recent developments in undersanding the regulation of starch metabolism in higher plants. J Exp Bot 55: 2131-2145.
  • Tetlow IJ, Wait R, Lu Z, Akkasaeng R, Bowsher CG, Esposito S, Kosar-Hashemi B, Morell MK, Emes MJ (2004b) Protein phosphorylation in amyloplasts regulates starch branching enzyme activity and protein-protein interactions. Plant Cell 16: 694-708.
  • Tetlow IJ (2006) Understanding storage starch biosynthesis in plants: a means to quality improvement. Can J Bot 84: 1167-1185.
  • Tetlow IJ, Beisel KG, Cameron S, Makhmoudova A, Liu F, Bresolin NS, Wait R, Morell MK, Emes MJ (2008) Analysis of protein complexes in wheat amyloplasts reveals functional interactions among starch biosynthetic enzymes. Plant Physiol 146: 1878-1891.
  • Thompson DB (2000) On the non-random nature of amylopectin branching. Carbohydr Polym 43: 223-239.
  • Thorbjørnsen T, Villand P, Denyer K, Olsen OA, Smith AM (1996) Distinct isoforms of ADP-glucose pyrophosphorylase occur inside and outside the amyloplasts in barley endosperm. Plant J 10: 243-250.
  • Tiessen A, Hendriks JHM, Stitt M, Branscheid A, Gibon Y, Farre EM, Geigenberger P (2002) Starch synthesis in potato tubers is regulated by post-translational redox modification of ADP-glucose pyrophosphorylase, a novel regulatory mechanism linking starch synthesis to the sucrose supply. Plant Cell 14: 2191-2213.
  • Tiessen A, Prescha K, Branscheid A, Palacios N, McKibbin R, Halford NG, Geigenberger P (2003) Evidence that SNF1-related kinase and hexokinase are involved in separate sugar signalling pathways modulating post-translational redox activation of ADP-glucose pyrophosphorylase in potato tubers. Plant J 35: 490-500.
  • Usadel B, Bläsing OE, Gibon Y, Retzlaff K, Höhne M, Günther M, Stitt M (2008) Global transcript levels respond to small changes of the carbon status during progressive exhaustion of carbohydrates in Arabidopsis rosettes. Plant Physiol 146: 1834-1861.
  • Vermeylen R, Goderis B, Reynaers H, Delcour JA (2004) Amylopectin molecular structure reflected in macromolecular organization of granular starch. Biomacromolecules 5: 1775-1786.
  • Villand P, Olsen OA, Kleczkowski LA (1993) Molecular characterization of multiple cDNA clones for ADP-glucose pyrophosphorylase from Arabidopsis thaliana. Plant Mol Biol 23: 1279-1284.
  • Vrinten PL, Nakamura T (2000) Wheat granule-bound starch synthase I and II are encoded by separate genes that are expressed in different tissues. Plant Physiol 122: 255-263.
  • Waigh TA, Perry P, Reikel C, Gidley MJ, Donald AM (1998) Chiral side-chain liquid-crystalline polymeric properties of starch. Macromolecules 31: 7980-7984.
  • Wang SM, Chu B, Lue WL, Yu TS, Eimert K, Chen J (1997) adg2-1 represents a missense mutation in the ADPG pyrophosphorylase large subunit gene of Arabidopsis thaliana. Plant J 11: 1121-1126.
  • Weise SE, Schrader SM, Kleinbeck KR, Sharkey TD (2006) Carbon balance and circadian regulation of hydrolytic and phosphorolytic breakdown of transitory starch. Plant Physiol 141: 879-886.
  • Worby CA, Gentry MS, Dixon JE (2006) Laforin, a dual specificity phosphatase that dephosphorylates complex carbohydrates. J Biol Chem 281: 30412-30418.
  • Yun SH, Matheson NK (1993) Structures of the amylopectins of waxy, normal, amylose-extender, and wx:ae genotypes and of the phytoglycogen of maize. Carbohydr Res 243: 307-321.
  • Yu TS, Kofler H, Häusler RE, Hille D, Flügge UJ, Zeeman SC, Smith AM, Kossmann J, Lloyd J, Ritte G, Steup M, Lue WL, Chen J, Weber A (2001a) 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: 1907-1918.
  • Yu Y, Mu HH, Wasserman BP, Carman GM (2001b) Identification of the maize amyloplast stromal 112-kD protein as a plastidic starch phosphorylase. Plant Physiol 125: 351-359.
  • Yu TS, Zeeman SC, Thorneycroft D, Fulton DC, Dunstan H, Lue WL, Hegemann B, Tung SY, Umemoto T, Chapple A, Tsai DL, Wang SM, Smith AM, Chen J, Smith SM (2005) α-amylase is not required for breakdown of transitory starch in Arabidopsis leaves. J Biol Chem 280: 9773-9779.
  • Zeeman SC, Umemoto T, Lue WL, Au-Yeung P, Martin C, Smith AM, Chen J (1998) A mutant of Arabidopsis lacking a chloroplastic isoamylase accumulates both starch and phytoglycogen. Plant Cell 10: 1699-1712.
  • Zeeman SC, Rees T (1999) Changes in carbohydrate metabolism and assimilate export in starch-excess mutants of Arabidopsis. Plant Cell Environ 22: 1445-1453.
  • Zeeman SC, Tiessen A, Pikling E, Kato KL, Donald AM, Smith AM (2002) Starch synthesis in Arabidopsis. Granule synthesis, composition, and structure. Plant Physiol 129: 516-529.
  • Zeeman SC, Smith SM, Smith AM (2004a) The breakdown of starch in leaves. New Phytol 163: 247-261.
  • Zeeman SC, Thorneycroft D, Schupp N, Chapple A, Weck M, Dunstan H, Haldimann P, Bechtold N, Smith AM, Smith SM (2004b) Chloroplastic starch phosphorylase is not required for transitory starch degradation in Arabidopsis leaves but has a role in the tolerance of abiotic stress. Plant Physiol 135: 849-858.
  • Zeeman SC, Delatte T, Messerli G, Umhang M, Stettler M, Mettler T, Steb S, Reinhold H, Kötting O (2007a) Starch breakdown: recent discoveries suggest distinct pathways and novel mechanisms. Funct Plant Biol 34: 465-473.
  • Zeeman SC, Smith SM, Smith AM (2007b) The diurnal metabolism of leaf starch. Biochem J 401: 13-28.
  • Zhang X, Myers AM, James MG (2005) Mutations affecting starch synthase III in Arabidopsis alter leaf starch structure and increase the rate of starch synthesis. Plant Physiol 138: 663-674.
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