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Starch biosynthesis in developing seeds

Published online by Cambridge University Press:  19 November 2010

Ian J. Tetlow*
Affiliation:
Department of Molecular and Cellular Biology, Science Complex, University of Guelph, Guelph, OntarioN1G 2W1, Canada
*
*Correspondence Email: itetlow@uoguelph.ca

Abstract

Starch is globally important as a source of food and, in addition, has a wide range of industrial applications. Much of this agriculturally produced starch is synthesized in developing seeds, where its biological function is to provide energy for seedling establishment. Storage starch in developing seeds is synthesized in heterotrophic plastids called amyloplasts and is distinct from the transient synthesis of starch in chloroplasts. This article reviews our current understanding of storage starch biosynthesis occurring in these organelles and discusses recent advances in research in this field. The review discusses starch structure and granule initiation, emerging ideas on the evolution of the pathway, the enzymes of starch synthesis, and the post-translational modification and regulation of key enzymes of amylopectin biosynthesis.

Type
Invited Review
Copyright
Copyright © Cambridge University Press 2010

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References

Albrecht, T., Greve, B., Pusch, K., Kossmann, J., Buchner, P., Wobus, U. and Steup, M. (1998) Homodimers and heterodimers of Pho1-type phosphorylase isoforms in Solanum tuberosum L. as revealed by sequence-specific antibodies. European Journal of Biochemistry 251, 343352.Google Scholar
Albrecht, T., Koch, A., Lode, A., Greve, B., Schneider-Mergener, J. and Steup, M. (2001) Plastidic (Pho1-type) phosphorylase isoforms in potato (Solanum tuberosum L.) plants: expression analysis and immunochemical characterisation. Planta 213, 602613.CrossRefGoogle Scholar
Alexander, R.D. and Morris, P.C. (2006) A proteomic analysis of 14-3-3 binding proteins from developing barley grains. Proteomics 6, 18861896.CrossRefGoogle ScholarPubMed
ap Rees, T. and Morrell, S. (1990) Carbohydrate metabolism in developing potatoes. American Potato Journal 6, 835847.Google Scholar
Baba, T., Yoshii, M. and Kainuma, K. (1987) Acceptor molecule of granular-bound starch synthase from sweet-potato roots. Starch-Stärke 39, 5256.Google Scholar
Båga, M., Nair, R.B., Repellin, A., Scoles, G.J. and Chibbar, R.N. (2000) Isolation of a cDNA encoding a granule-bound 152-kiloDalton starch-branching enzyme in wheat. Plant Physiology 124, 253263.Google Scholar
Ball, S.G. and Morell, M.K. (2003) From bacterial glycogen to starch: understanding the biogenesis of the plant starch granule. Annual Review of Plant Biology 54, 207233.Google Scholar
Ball, S., Guan, H., James, M., Myers, A., Keeling, P., Mouille, G., Buléon, A., Colonna, P. and Preiss, J. (1996) From glycogen to amylopectin: a model for the biogenesis of the plant starch granule. Cell 86, 349352.CrossRefGoogle Scholar
Ball, S., Liénard, L., Wattebled, F., Steup, M., Hicks, G. and d'Hulst, C. (2003) Defining the functions of maltodextrin active enzymes in starch metabolism in the unicellular alga Chlamydomonas reinhardtii. Journal of Applied Glycoscience 50, 187189.Google Scholar
Ballicora, M.A., Laughlin, M.J., Fu, Y., Okita, T.W., Barry, G.F. and Preiss, J. (1995) Adenosine 5′-diphosphate-glucose pyrophosphorylase from potato tuber. Significance of the N-terminus of the small subunit for catalytic properties and heat stability. Plant Physiology 109, 245251.CrossRefGoogle Scholar
Banks, W., Greenwood, C.T. and Muir, D.D. (1974) Studies on starches of high amylose content: part 17. A review of current concepts. Starch-Stärke 26, 289300.CrossRefGoogle Scholar
Bao, J., Xiao, P., Hiratsuka, M., Sun, M. and Umemoto, T. (2009) Granule-bound SSIIa protein content and its relationship with amylopectin structure and gelatinization temperature of rice starch. Starch-Stärke 61, 431437.CrossRefGoogle Scholar
Baunsgaard, L., Lütken, H., Mikkelsen, R., Glaring, M.A., Pham, T.T. and Blennow, A. (2005) A novel isoform of glucan, water dikinase phosphorylates prephosphorylated α-glucans and is involved in starch degradation in Arabidopsis. Plant Journal 41, 595605.Google Scholar
Beatty, M.K., Rahman, A., Cao, H., Woodman, W., Lee, M., Myers, A.M. and James, M.G. (1999) Purification and molecular genetic characterization of ZPU1, a pullulanase-type starch-debranching enzyme from maize. Plant Physiology 119, 255266.CrossRefGoogle ScholarPubMed
Bechtel, D.B. and Wilson, J.D. (2003) Amyloplast formation and starch granule development in hard red winter wheat. Cereal Chemistry 80, 175183.CrossRefGoogle Scholar
Bechtel, D.B., Zayas, I.Y., Kaleikau, L. and Pomeranz, Y. (1990) Size-distribution of wheat starch granules during endosperm development. Cereal Chemistry 67, 5963.Google Scholar
Beckles, D.M., Smith, A.M. and ap Rees, T. (2001) A cytosolic ADP-glucose pyrophosphorylase is a feature of graminaceous endosperms, but not of other starch storing organs. Plant Physiology 125, 818827.CrossRefGoogle Scholar
Benmoussa, M., Hamaker, B.R., Huang, C.P., Sherman, D.M., Weil, C.F. and BeMiller, J.N. (2010) Elucidation of maize endosperm starch granule channel proteins and evidence for cytoskeletal structures in maize endosperm amyloplasts. Journal of Cereal Science 52, 2229.CrossRefGoogle Scholar
Bertoft, E. (1986) Hydrolysis of amylopectin by the alpha-amylase of B. subtilis. Carbohydrate Research 149, 379387.Google Scholar
Bertoft, E. (2004) On the nature of categories of chains in amylopectin and their connection to the super helix model. Carbohydrate Polymers 57, 211224.Google Scholar
Bewley, J.D. and Black, M. (1994) Seeds: physiology of development and germination. New York, Plenum Press.CrossRefGoogle Scholar
Blauth, S.L., Yao, Y., Klucinec, J.D., Shannon, J.C., Thompson, D.B. and Guiltinan, M. (2001) Identification of Mutator insertional mutants of starch-branching enzyme 2a in corn. Plant Physiology 125, 13961405.CrossRefGoogle ScholarPubMed
Blauth, S.L., Kim, K.N., Klucinec, J., Shannon, J.C., Thompson, D.B. and Guiltinan, M. (2002) Identification of Mutator insertional mutants of starch-branching enzyme 1 (sbe1) in Zea mays L. Plant Molecular Biology 48, 287297.Google Scholar
Boel, E., Brady, L., Brzozowski, A.M., Derewenda, Z., Dodson, G.G., Jensen, V.J., Petersen, S.B., Swift, H., Thim, L. and Woldike, H.F. (1990) Calcium binding in α-amylases: an X-ray diffraction study at 2.1-Å resolution of two enzymes from Aspergillus. Biochemistry 29, 62446249.CrossRefGoogle Scholar
Bogracheva, T.Y., Cairns, P., Noel, T.R., Hulleman, S., Wang, T., Morris, V.J., Ring, S.G. and Gidley, M.J. (1999) The effect of mutant genes at the r, rb, rug3, rug4, rug5 and lam loci on the granular structure and physico-chemical properties of pea seed starch. Carbohydrate Polymers 39, 303314.Google Scholar
Borén, M., Larsson, H., Falk, A. and Jansson, C. (2004) The barley starch granule proteome: internalized granule polypeptides of the mature endosperm. Plant Science 166, 617626.CrossRefGoogle Scholar
Borovsky, D., Smith, E.E., Whelan, W.J., French, D. and Kikumoto, S. (1979) The mechanism of Q-enzyme action and its influence on the structure of amylopectin. Archives of Biochemistry and Biophysics 198, 627631.Google Scholar
Bowsher, C.G., Scrase-Field, E.F.A.L., Esposito, S., Emes, M.J. and Tetlow, I.J. (2007) Characterization of ADP-glucose transport across the cereal endosperm amyloplast envelope. Journal of Experimental Botany 58, 13211332.Google Scholar
Boyer, C.D. and Preiss, J. (1979) Properties of citrate-stimulated starch synthesis catalyzed by starch synthase I of developing maize kernels. Plant Physiology 64, 10391042.CrossRefGoogle ScholarPubMed
Boyer, C.D. and Preiss, J. (1981) Evidence for independent genetic control of the multiple forms of maize endosperm branching enzymes and starch synthases. Plant Physiology 67, 11411145.Google Scholar
Bresolin, N.S., Li, Z., Kosar-Hashemi, B., Tetlow, I.J., Chaterjee, M., Rahman, S., Morell, M.K. and Howitt, C.A. (2005) Characterisation of disproportionating enzyme from wheat endosperm. Planta 224, 2031.CrossRefGoogle ScholarPubMed
Briarty, L.G., Hughes, C.E. and Evers, A.D. (1979) The developing endosperm of wheat – a stereological analysis. Annals of Botany 44, 641658.CrossRefGoogle Scholar
Brocklehurst, P.A. (1977) Factors controlling grain weight in wheat. Nature 266, 348349.Google Scholar
Buchbinder, J.L., Rath, V.L. and Fletterick, R.J. (2001) Structural relationships among regulated and unregulated phosphorylases. Annual Review of Biophysics and Biomolecular Structure 30, 191209.Google Scholar
Buléon, A., Colonna, P., Planchot, V. and Ball, S. (1998) Starch granules: structure and biosynthesis. International Journal of Biological Macromolecules 23, 85112.Google Scholar
Burrell, M.M. (2003) Starch: the need for improved quality or quantity – an overview. Journal of Experimental Botany 54, 451456.Google Scholar
Burton, R.A., Jenner, H., Carrangis, L., Fahy, B., Fincher, G.B., Hylton, C., Laurie, D.A., Parker, M., Waite, D., van Wegen, S., Verhoeven, T. and Denyer, K. (2002) Starch granule initiation and growth are altered in barley mutants that lack isoamylase activity. Plant Journal 31, 97112.Google Scholar
Busi, M., Palapoli, N., Valdez, H.A., Fornasari, M.S., Wayllace, N.Z., Gomez-Casati, D.F., Parisi, G. and Ugalde, R.A. (2008) Functional and structural characterization of the catalytic domain of the starch synthase III from Arabidopsis thaliana. Proteins 70, 3140.Google Scholar
Bustos, R., Fahy, B., Hylton, C.M., Seale, R., Nebane, N.M., Edwards, A., Martin, C. and Smith, A.M. (2004) Starch granule initiation is controlled by a heteromultimeric isoamylase in potato tubers. Proceedings of the National Academy of Sciences, USA 101, 22152220.CrossRefGoogle ScholarPubMed
Buttrose, M.S. (1960) Submicroscopic development and structure of starch granules in cereal endosperms. Journal of Ultrastructural Research 4, 231257.Google Scholar
Buttrose, M.S. (1963) Ultrastructure of the developing wheat endosperm. Australian Journal of Biological Science 16, 305317.CrossRefGoogle Scholar
Cao, H., Imparl-Radosevich, J., Guan, H., Keeling, P.L., James, M.G. and Myers, A.M. (1999) Identification of the soluble starch synthase activities of maize endosperm. Plant Physiology 120, 205215.CrossRefGoogle ScholarPubMed
Cao, H., James, M.G. and Myers, A.M. (2000) Purification and characterization of soluble starch synthases from maize endosperm. Archives of Biochemistry and Biophysics 373, 135146.Google Scholar
Cavalier-Smith, T. (2009) Predation and eukaryote cell origins: a coevolutionary perspective. International Journal of Biochemistry and Cell Biology 41, 307322.Google Scholar
Chatterjee, M., Berbezy, P., Vyas, D., Coates, S. and Barsby, T. (2005) Reduced expression of a protein homologous to glycogenin leads to a reduction of starch content in Arabidopsis leaves. Plant Science 168, 501509.CrossRefGoogle Scholar
Chen, C.L. and Sung, J.M. (1994) Carbohydrate metabolism enzymes in CO2-enriched developing rice grains varying in grain size. Physiologia Plantarum 90, 7985.Google Scholar
Chen, H.-M., Chang, S.-C., Wu, C.-C., Cuo, T.-S., Wu, J.-S. and Juang, R.-H. (2002) Regulation of the catalytic behaviour of L-form starch phosphorylase from sweet potato roots by proteolysis. Physiologia Plantarum 114, 506515.Google Scholar
Clarke, B.R., Denyer, K., Jenner, C.F. and Smith, A.M. (1999) The relationship between the rate of starch synthesis, the adenosine 5′-diphosphoglucose concentration and the amylose content of starch in developing pea embryos. Planta 209, 324329.Google Scholar
Colleoni, C., Dauvillée, D., Mouille, G., Buléon, A., Gallant, D., Bouchet, B., Morell, M.K., Samuel, M., Delrue, B., d'Hulst, C., Bliard, C., Nuzillard, J.M. and Ball, S. (1999a) Genetic and biochemical evidence for the involvement of α-1,4 glucanotransferases in amylopectin synthesis. Plant Physiology 120, 9931004.Google Scholar
Colleoni, C., Dauvillée, D., Mouille, G., Morell, M.K., Samuel, M., Slomiany, M.C., Liénard, L., Wattebled, F., d'Hulst, C. and Ball, S. (1999b) Biochemical characterization of the Chlamydomonas reinhardtii α-1,4 glucanotransferase supports a direct function in amylopectin biosynthesis. Plant Physiology 120, 10051014.Google Scholar
Colleoni, C., Myers, A.M. and James, M.G. (2003) One- and two-dimensional native PAGE activity gel analyses of maize endosperm proteins reveal functional interactions between specific starch metabolizing enzymes. Journal of Applied Glycoscience 50, 207212.Google Scholar
Commuri, P.D. and Keeling, P.L. (2001) Chain-length specificities of maize starch synthase I enzyme: studies of glucan affinity and catalytic properties. Plant Journal 25, 475486.Google Scholar
Comparot, S., Lingiah, G. and Martin, T. (2003) Function and specificity of 14-3-3 proteins in the regulation of carbohydrate and nitrogen metabolism. Journal of Experimental Botany 54, 595604.Google Scholar
Comparot-Moss, S. and Denyer, K. (2009) The evolution of the starch biosynthetic pathway in cereals and other grasses. Journal of Experimental Botany 60, 24812492.CrossRefGoogle ScholarPubMed
Comparot-Moss, S., Kötting, O., Stettler, M., Edner, C. and Graf, A. (2010) A putative phosphatase, LSF1 is required for normal starch turnover in Arabidopsis leaves. Plant Physiology 152, 685697.Google Scholar
Cooke, D. and Gidley, M.J. (1992) Loss of crystalline and molecular order during starch gelatinization: origin of the enthalpic transition. Carbohydrate Research 227, 103112.Google Scholar
Coppin, A., Varré, J.-S., Lienard, L., Dauvillée, D., Guérardel, Y., Soyer-Gobillard, M.-O., Buléon, A., Ball, S. and Tomavo, S. (2005) Evolution of plant-like crystalline storage polysaccharide in the protozoan parasite Toxoplasma gondii argues for a red algal ancestry. Journal of Molecular Evolution 60, 257267.Google Scholar
Cowie, J.M.G. and Greenwood, C.T. (1957) Physicochemical studies on starches part VI: aqueous leaching and the fractionation of potato starch. Journal of the Chemical Society 559, 28622866.Google Scholar
Crevillén, P., Ballicora, M.A., Mérida, A., Preiss, J. and Romero, J.M. (2003) The different large subunit isoforms of Arabidopsis thaliana ADP-glucose pyrophosphorylase confer distinct kinetic and regulatory properties to the heterotetrameric enzyme. Journal of Biological Chemistry 278, 2850828515.Google Scholar
Crevillén, P., Ventriglia, T., Pinto, F., Orea, A., Mérida, A. and Romero, J.M. (2005) Differential pattern of expression and sugar regulation of Arabidopsis thaliana ADP-glucose pyrophosphorylase-encoding genes. Journal of Biological Chemistry 280, 81438149.CrossRefGoogle ScholarPubMed
Critchley, J.H., Zeeman, S.C., Takaha, T., Smith, A.M. and Smith, S.M. (2001) A critical role for disproportionating enzyme in starch breakdown is revealed by a knock-out mutation in Arabidopsis. Plant Journal 26, 89100.Google Scholar
Cross, J.M., Clancy, M., Shaw, J.R., Boehlein, S.K., Greene, T.W., Schmidt, R.R., Okita, T.W. and Hannah, L.C. (2005) A polymorphic motif in the small subunit of ADP-glucose pyrophosphorylase modulates interactions between the small and large subunits. Plant Journal 41, 501511.Google Scholar
Dale, E.M. and Housely, T.L. (1986) Sucrose synthase activity in developing wheat endosperms differing in maximum weight. Plant Physiology 82, 710.CrossRefGoogle ScholarPubMed
Datta, R., Chamusco, K.C. and Choury, P.S. (2002) Starch biosynthesis during pollen maturation is associated with altered patterns of gene expression in maize. Plant Physiology 130, 16451656.Google Scholar
Dauvillée, D., Colleoni, C., Shaw, E., Mouille, G., D'Hulst, C., Morell, M., Samuel, M.S., Bouchet, B., Gallant, D.J., Sinsky, A. and Ball, S. (1999) Novel, starch-like polysaccharides are synthesized by an unbound form of granule-bound starch synthase in glycogen-accumulating mutants of Chlamydomonas reinhardtii. Plant Physiology 119, 321330.Google Scholar
Dauvillée, D., Chochois, V., Steup, M., Haebel, S., Eckermann, N., Ritte, G., Ral, J.-P., Colleoni, C., Hicks, G., Wattebled, F., Deschamps, P., d'Hulst, C., Liénard, L., Cournac, L., Puteaux, J.-L., Dupeyre, D. and Ball, S.G. (2006) Plastidial phosphorylase is required for normal starch synthesis in Chlamydomonas reinhardtii. Plant Journal 48, 274285.Google Scholar
Dauvillée, D., Deschamps, P., Ral, J.-P., Planke, C., Puteaux, J.-L., Devassine, J., Durand-Terrasson, A., Devin, A. and Ball, S.G. (2009) Genetic dissection of floridean starch synthesis in the cytosol of the model dinoflagellate Crypthecodinium cohnii. Proceedings of the National Academy of Sciences, USA 106, 2112621130.Google Scholar
De Fekete, M.A.R., Leloir, L.F. and Cardini, C.E. (1960) Mechanism of starch biosynthesis. Nature 187, 918919.Google Scholar
Delatte, T., Trevisan, M., Parker, M.L. and Zeeman, S.C. (2005) Arabidopsis mutants Atisa1 and Atisa2 have identical phenotypes and lack the same multimeric isoamylase, which influences the branch point distribution of amylopectin during starch synthesis. Plant Journal 41, 815830.Google Scholar
Delrue, B., Fontaine, T., Routier, F., Decq, A., Wieruszeski, J.M. and Ball, S. (1992) Waxy Chlamydomonas reinhardtii: monocellular algal mutants defective in amylose biosynthesis and granule-bound starch synthase activity accumulate a structurally modified amylopectin. Journal of Bacteriology 174, 36123620.Google Scholar
Delvallé, D., Dumez, S., Wattebled, F., Roldán, I., Planchot, V., Berbezy, P., Colonna, P., Vyas, D., Chatterjee, M., Ball, S., Mérida, A. and D'Hulst, C. (2005) Soluble starch synthase I: a major determinant for the synthesis of amylopectin in Arabidopsis thaliana leaves. Plant Journal 43, 398412.Google Scholar
Denyer, K., Sidebottom, C., Hylton, C.M. and Smith, A.M. (1993) Soluble isoforms of starch synthase and starch-branching enzyme also occur within starch granules in developing pea embryos. Plant Journal 4, 191198.Google Scholar
Denyer, K., Hylton, C.M., Jenner, C.F. and Smith, A.M. (1995) Identification of multiple isoforms of soluble and granule-bound starch synthase in developing wheat endosperm. Planta 196, 256265.CrossRefGoogle Scholar
Denyer, K., Clarke, B., Hylton, C., Tatge, H. and Smith, A.M. (1996a) The elongation of amylose and amylopectin chains in isolated starch granules. Plant Journal 10, 11351143.Google Scholar
Denyer, K., Dunlap, F., Thorbjørnsen, T., Keeling, P. and Smith, A.M. (1996b) The major form of ADPglucose pyrophosphorylase in maize endosperm is extraplastidial. Plant Physiology 112, 779783.Google Scholar
Denyer, K., Waite, D., Edwards, A., Martin, C. and Smith, A.M. (1999) Interaction with amylopectin influences the ability of granule-bound starch synthase I to elongate malto-oligosaccharides. Biochemical Journal 342, 647653.Google Scholar
Denyer, K., Johnson, P., Zeeman, S. and Smith, A.M. (2001) The control of amylose synthesis. Journal of Plant Physiology 158, 479487.CrossRefGoogle Scholar
Deschamps, P., Moreau, H., Worden, A.Z., Dauvillée, D. and Ball, S.G. (2008a) Early gene duplication within Chloroplastida and its correspondence with relocation of starch metabolism to chloroplasts. Genetics 178, 23732387.Google Scholar
Deschamps, P., Haferkamp, I., d'Hulst, C., Neuhaus, H.E. and Ball, S.G. (2008b) The relocation of starch metabolism to chloroplasts: when, why and how. Trends in Plant Science 13, 574582.Google Scholar
D'Hulst, C. and Mérida, Á. (2010) The priming of storage glucan synthesis from bacteria to plants: current knowledge and new developments. New Phytologist 188, 1321.Google Scholar
Dian, W., Jiang, H. and Wu, P. (2005) Evolution and expression analysis of starch synthase III and IV in rice. Journal of Experimental Botany 56, 623632.Google Scholar
Dinges, J.R., Colleoni, C., Myers, A.M. and James, M.G. (2001) Molecular structure of three mutations at the maize sugary1 locus and their allele-specific phenotype effects. Plant Physiology 125, 14061418.Google Scholar
Dinges, J.R., Colleoni, C., James, M.G. and Myers, A.M. (2003) Mutational analysis of the pullulanase-type debranching enzyme of maize indicates multiple functions in starch metabolism. Plant Cell 15, 666680.CrossRefGoogle ScholarPubMed
Dumez, S., Wattebled, F., Dauvillée, D., Delvallé, D., Planchot, V., Ball, S.G. and D'Hulst, C. (2006) Mutants of Arabidopsis lacking starch branching enzyme II substitute plastidial starch synthesis by cytoplasmic maltose accumulation. Plant Cell 18, 26942709.CrossRefGoogle ScholarPubMed
Duwenig, E., Steup, M. and Kossmann, J. (1997) Induction of genes encoding plastidic phosphorylase from spinach (Spinacia oleracea L.) and potato (Solanum tuberosum L.) by exogenously supplied carbohydrates in excised leaf discs. Planta 203, 111120.Google Scholar
Edwards, A., Fulton, D.C., Hylton, C.M., Jobling, S.A., Gidley, M., Rössner, U., Martin, C. and Smith, A.M. (1999) A combined reduction in activity of starch synthases II and III of potato has novel effects on the starch of tubers. Plant Journal 17, 251261.Google Scholar
Evans, A. and Thompson, D.B. (2004) Resistance to α-amylase digestion in four native high-amylose maize starches. Cereal Chemistry 81, 3137.Google Scholar
Evers, A.D. (1973) The size distribution among starch granules in wheat endosperm. Starch-Stärke 25, 303304.Google Scholar
Fannon, J.E., Hauber, R.J. and BeMiller, J.N. (1992) Surface pores of starch granules. Cereal Chemistry 69, 284288.Google Scholar
Fannon, J.E., Gray, J.A., Gunawan, N., Huber, K.C. and BeMiller, J.N. (2004) Heterogeneity of starch granules and the effect of granule channelization on starch modification. Cellulose 11, 247254.Google Scholar
Fernandez-Sanchez, M.E., Criado-Garcia, O., Heath, K.E., Garcia-Fojeda, B., Medrano-Fernandez, I., Gomez-Garre, P., Sanz, P., Serratosa, J.M. and Rodriguez de Cordoba, S. (2003) Laforin, the dual-phosphatase responsible for Lafora disease, interacts with R5 (PTG), a regulatory subunit of protein phosphatase-1 that enhances glycogen accumulation. Human Molecular Genetics 12, 31613171.Google Scholar
Fettke, J., Albrecht, T., Hejazi, M., Mahlow, S., Nakamura, Y. and Steup, M. (2010) Glucose 1-phosphate is efficiently taken up by potato (Solanum tuberosum) tuber parenchyma cells and converted to reserve starch granules. New Phytologist 185, 663675.Google Scholar
Fisher, D.K., Gao, M., Kim, K.-N., Boyer, C.D. and Guiltinan, M.J. (1996) Two closely related cDNAs encoding starch branching enzyme from Arabidopsis thaliana. Plant Molecular Biology 30, 97108.Google Scholar
Flipse, E., Suurs, L., Keetels, C.J.A., Kossmann, J., Jacobsen, E. and Visser, R.G.F. (1996) Introduction of sense and antisense cDNA for branching enzyme in the amylose-free potato mutant leads to physico-chemical changes in the starch. Planta 198, 340347.Google Scholar
Fontaine, T., D'Hulst, C., Maddelein, M.-L., Routier, F., Pépin, T.M., Decq, A., Wieruszeski, J.-M., Delrue, B., Van den Koornhuyse, N., Bossu, J.-P., Fournet, B. and Ball, S. (1993) Toward an understanding of the biogenesis of the starch granule. Evidence that Chlamydomonas soluble starch synthase II controls the synthesis of intermediate glucans of amylopectin. Journal of Biological Chemistry 268, 1622316230.Google Scholar
Fordham-Skelton, A.P., Chilley, P., Lumbreras, V., Reignoux, S., Fenton, T.R., Dahm, C.R., Pages, M. and Gatehouse, J.A. (2002) A novel higher plant protein tyrosine phosphatase interacts with SNF1-related protein kinases via a KIS (kinase interaction sequence) domain. Plant Journal 29, 705715.CrossRefGoogle Scholar
French, D. (1984) Organization of starch granules. pp. 183237in Whistler, R.L.; BeMiller, J.N.; Paschall, E.F. (Eds) Starch: chemistry and technology. Orlando, Academic Press.Google Scholar
Fu, Y., Ballicora, M.A., Leykam, J.F. and Preiss, J. (1998) Mechanism of reductive activation of potato tuber ADP-glucose pyrophosphorylase. Journal of Biological Chemistry 273, 2504525052.Google Scholar
Fujita, N. and 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, 125132.CrossRefGoogle ScholarPubMed
Fujita, N., Yoshida, M., Asakura, N., Ohdan, T., Miyao, A., Hirochika, H. and Nakamura, Y. (2006) Function and characterization of starch synthase I using mutants in rice. Plant Physiology 140, 10701084.CrossRefGoogle ScholarPubMed
Fujita, N., Yoshida, M., Kondo, T., Saito, K., Utsumi, Y., Tokunaga, T., Nishi, A., Satoh, H., Park, J.-H., Jane, J.-L., Miyao, A., Hirochika, H. and Nakamura, Y. (2007) Characterization of SSIIIa-deficient mutants of rice: the function of SSIIIa and pleiotropic effects by SSIIIa deficiency in the rice endosperm. Plant Physiology 144, 20092023.Google Scholar
Fujita, N., Toyosawa, Y., Utsumi, Y., Higuchi, T., Hanashiro, I., Ikegami, A., Akuzawa, S., Yoshida, M., Mori, A., Inomata, K., Itoh, R., Miyao, A., Hirochika, H., Satoh, H. and Nakamura, Y. (2009) Characterization of pullulanase (PUL)-deficient mutants of rice (Oryza sativa L.) and the function of PUL on starch biosynthesis in the developing rice endosperm. Journal of Experimental Botany 60, 10091023.Google Scholar
Fulton, D.C., Edwards, A., Pilling, E., Robinson, H.L., Fahy, B., Seale, R., Kato, L., Donald, A.M., Geigenberger, P., Martin, C. and Smith, A.M. (2002) Role of granule-bound starch synthase in determination of amylopectin structure and starch granule morphology in potato. Journal of Biological Chemistry 277, 1083410841.Google Scholar
Furukawa, K., Tagaya, M., Inouye, M., Preiss, J. and Fukui, T. (1990) Identification of lysine 15 at the active site in Escherichia coli glycogen synthase. Conservation of Lys-X-Gly-Gly sequence in the bacterial and mammalian enzymes. Journal of Biological Chemistry 265, 20862090.Google Scholar
Furukawa, K., Tagaya, M., Tanizawa, K. and Fukui, T. (1993) Role of the conserved Lys-X-Gly-Gly sequence at the ADP-glucose-binding site in Escherichia coli glycogen synthase. Journal of Biological Chemistry 268, 2383723842.Google Scholar
Gallant, D.J., Bouchet, B. and Baldwin, P.M. (1997) Microscopy of starch: evidence of a new level of granule organization. Carbohydrate Polymers 32, 177191.Google Scholar
Gao, M., Fisher, D.K., Kim, K.N., Shannon, J.C. and Guiltinan, M.J. (1996) Evolutionary conservation and expression patterns of maize starch branching enzyme I and IIb genes suggests isoform specialization. Plant Molecular Biology 30, 12231232.Google Scholar
Gao, M., Fisher, D.K., Kim, K.-N., Shannon, J.C. and Guiltinan, M.J. (1997) Independent genetic control of maize starch-branching enzymes IIa and IIb. Plant Physiology 114, 6978.Google Scholar
Gao, M., Wanat, J., Stinard, P.S., James, M.G. and Myers, A.M. (1998) Characterization of dull1, a maize gene encoding for a novel starch synthase. Plant Cell 10, 399412.Google Scholar
Gao, Z., Keeling, P., Shibles, R. and Guan, H. (2004) Involvement of lysine-193 of the conserved ‘K-T-G-G’ motif in the catalysis of maize starch synthase IIa. Archives of Biochemistry and Biophysics 427, 17.Google Scholar
Ghosh, H.P. and Preiss, J. (1966) Adenosine diphosphate glucose pyrophosphorylase: a regulatory enzyme in the biosynthesis of starch in spinach leaf chloroplasts. Journal of Biological Chemistry 241, 44914504.Google Scholar
Giroux, M. and Hannah, L.C. (1994) ADPglucose pyrophosphorylase in shrunken-2 and brittle-2 mutants of maize. Molecular and General Genetics 243, 400408.Google Scholar
Giroux, M.J., Shaw, J., Barry, G., Cobb, B.G., Greene, T., Okita, T. andHannah, L.C. (1996) A single gene mutation that increases maize seed weight. Proceedings of the National Academy of Sciences, USA 93, 58245829.Google Scholar
Glaring, M.A., Koch, C.B. and Blennow, A. (2006) Genotype-specific spatial distribution of starch molecules in the starch granule: a combined CLSM and SEM approach. Biomacromolecules 7, 23102320.Google Scholar
Gómez-Casati, D.F. and Iglesias, A.A. (2002) ADP-glucose pyrophosphorylase from wheat endosperm. Purification and characterisation of an enzyme with novel regulatory properties. Planta 214, 428434.Google Scholar
Greenberg, E. and Preiss, J. (1964) The occurrence of adenosine diphosphate glucose:glycogen transglucosylase in bacteria. Journal of Biological Chemistry 239, 43144315.Google Scholar
Grimaud, F., Rogniaux, H., James, M.G., Myers, A.M. and Planchot, V. (2008) Proteome and phosphoproteome analysis of starch granule-associated proteins from normal maize and mutants affected in starch biosynthesis. Journal of Experimental Botany 59, 33953406.Google Scholar
Gross, P. and ap Rees, T. (1986) Alkaline inorganic pyrophosphatase and starch synthesis in amyloplasts. Planta 167, 140145.Google Scholar
Guan, H. and Keeling, P.L. (1998) Starch biosynthesis: understanding the functions and interactions of multiple isozymes of starch synthase and branching enzyme. Trends in Glycoscience and Glycotechnology 10, 307319.Google Scholar
Guan, H.-P. and Preiss, J. (1993) Differentiation of the properties of the branching isozymes from maize (Zea mays). Plant Physiology 102, 12691273.Google Scholar
Hall, D.M. and Sayre, J.G. (1973) A comparison of starch granules as seen by both scanning and ordinary light microscopy. Starch-Stärke 25, 292297.Google Scholar
Hamada, S., Ito, H., Hiraga, S., Inagaki, K., Nozaki, K., Isono, N., Yoshimoto, Y., Takeda, Y. and Matsui, H. (2002) Differential characteristics and subcellular localization of two starch-branching enzyme isoforms encoded by a single gene in Phaseolus vulgaris L. Journal of Biological Chemistry 277, 1653816546.Google Scholar
Hanashiro, I., Itoh, K., Kuratomi, Y., Yamazaki, M., Igarishi, T., Matsugasako, J. and Takeda, Y. (2008) Granule-bound starch synthase I is responsible for biosynthesis of extra-long chains of amylopectin in rice. Plant and Cell Physiology 49, 925933.Google Scholar
Haugen, T.H. and Preiss, J. (1979) Biosynthesis of bacterial glycogen. The nature of the binding of substrates and effectors to ADP-glucose synthase. Journal of Biological Chemistry 254, 127136.Google Scholar
Hawker, J.S., Ozbun, J.L., Ozaki, H., Greenberg, E. and Preiss, J. (1974) Interaction of spinach leaf adenosine diphosphate glucose α-1, 4-glucan α-4-glucosyl transferase and α-1, 4-glucan, α-1, 4-glucan-6-glycosyl transferase in synthesis of branched α-glucan. Archives of Biochemistry and Biophysics 160, 530551.Google Scholar
Hejazi, M., Fettke, J., Haebel, S., Edner, C., Paris, O., Frohberg, C., Steup, M. and Ritte, G. (2008) Glucan, water dikinase phosphorylates crystalline maltodextrins and thereby initiates solubilisation. Plant Journal 55, 323334.Google Scholar
Hennen-Bierwagen, T.A., Liu, F., Marsh, R.S., Kim, S., Gan, Q., Tetlow, I.J., Emes, M.J., James, M.G. and Myers, A.M. (2008) Starch biosynthetic enzymes from developing Zea mays endosperm associate in multisubunit complexes. Plant Physiology 146, 18921908.CrossRefGoogle ScholarPubMed
Hennen-Bierwagen, T.A., Lin, Q., Grimaud, F., Planchot, V., Keeling, P.L., James, M.G. and Myers, A.M. (2009) Proteins from multiple metabolic pathways associate with starch biosynthetic enzymes in high molecular weight complexes: a model for regulation of carbon allocation in maize amyloplasts. Plant Physiology 149, 15411559.Google Scholar
Hilbert, G.E. and MacMasters, M.M. (1946) Pea starch, a starch of high amylose content. Journal of Biological Chemistry 162, 229238.CrossRefGoogle ScholarPubMed
Hirose, T. and Terao, T. (2004) A comprehensive expression analysis of the starch synthase gene family in rice (Oryza sativa L.). Planta 220, 916.Google Scholar
Hizukuri, S. (1986) Polymodal distribution of the chain lengths of amylopectin, and its significance. Carbohydrate Research 147, 342347.Google Scholar
Hizukuri, S., Takeda, Y., Maruta, N. and Juliano, B.O. (1989) Molecular structures of rice starch. Carbohydrate Research 189, 227235.Google Scholar
Huber, K.C. and BeMiller, J.N. (1997) Visualization of channels and cavities of corn and sorghum starch granules. Cereal Chemistry 74, 537541.Google Scholar
Hussain, H., Mant, A., Seale, R., Zeeman, S., Hinchliffe, E., Edwards, A., Hylton, C., Bornemann, S., Smith, A.M., Martin, C. and Bustos, R. (2003) Three forms of isoamylase contribute catalytic properties for the debranching of potato glucans. Plant Cell 15, 133149.Google Scholar
Hylton, C. and Smith, A.M. (1992) The rb mutation of peas causes structural and regulatory changes in ADP glucose pyrophosphorylase from developing embryos. Plant Physiology 99, 16261634.Google Scholar
Imparl-Radosevich, J.M., Li, P., Zhang, L., McKean, A.L., Keeling, P. and Guan, H. (1998) Purification and characterization of maize starch synthase I and its truncated forms. Archives of Biochemistry and Biophysics 353, 6472.Google Scholar
Imparl-Radosevich, J.M., Nichols, D.J., Li, P., McKean, A.L., Keeling, P. and Guan, H. (1999) Analysis of purified maize starch synthases IIa and IIb: SS isoforms can be distinguished based on their kinetic properties. Archives of Biochemistry and Biophysics 362, 131138.Google Scholar
Imparl-Radosevich, J.M., Gameon, J.R., McKean, A., Wetterberg, D., Keeling, P. and Guan, H. (2003) Understanding catalytic properties and functions of maize starch synthase isozymes. Journal of Applied Glycoscience 50, 177182.CrossRefGoogle Scholar
Inouchi, N., Glover, D.V., Takaya, T. and Fuwa, H. (1983) Development changes in fine structure of starches of several endosperm mutants of maize. Starch-Stärke 35, 371376.Google Scholar
James, M.G., Robertson, D.S. and Myers, A.M. (1995) Characterization of the maize gene sugary1, a determinant of starch composition in kernels. Plant Cell 7, 417429.Google Scholar
James, M.G., Denyer, K. and Myers, A.M. (2003) Starch synthesis in the cereal endosperm. Current Opinion in Plant Biology 6, 215222.Google Scholar
Jane, J.-L., Xu, A., Radosavljevic, M. and Seib, P.A. (1992) Location of amylose in normal starch granules. I. Susceptibility of amylose and amylopectin to cross-linking reagents. Cereal Chemistry 69, 405409.Google Scholar
Jane, J.-L., Kasemsuwan, T., Leas, S., Ames, I., Zobel, H.F. and Robyt, J.F. (1994) Anthology of starch granule morphology by scanning electron microscopy. Starch-Stärke 46, 121129.Google Scholar
Jenkins, P.J., Cameron, R.E. and Donald, A.M. (1993) A universal feature in the starch granules from different botanical sources. Starch- Stärke 45, 417420.Google Scholar
Jenkins, P.J. and Donald, A.M. (1995) The influence of amylose on starch granule structure. International Journal of Biological Macromolecules 17, 315321.CrossRefGoogle ScholarPubMed
Jenner, C.F., Siwek, K. and Hawker, J.S. (1993) The synthesis of [14C]starch from [14C]sucrose in isolated wheat grains is dependent upon the activity of soluble starch synthase. Australian Journal of Plant Physiology 20, 329335.Google Scholar
Jespersen, H.M., MacGregor, E.A., Henrissat, B., Sierks, M.R. and Svensson, B. (1993) Starch- and glycogen-debranching and branching enzymes: prediction of structural features of the catalytic (β/α)8-barrel domain and evolutionary relationship to other amylolytic enzymes. Journal of Protein Chemistry 12, 791805.Google Scholar
Ji, Q., Oomen, R.J.F.J., Vincken, J.-P., Bolam, D.N., Gilbert, H.J., Suurs, L.C.J.M. and Visser, R.G.F. (2004) Reduction of starch granule size by expression of an engineered tandem starch-binding domain in potato plants. Plant Biotechnology Journal 2, 251260.Google Scholar
Jobling, S. (2004) Improving starch for food and industrial applications. Current Opinion in Plant Biology 7, 210218.Google Scholar
Kainuma, K. (1988) Structure and biochemistry of the starch granule. pp. 141180in Preiss, J. (Ed.) The biochemistry of plants. Vol. 14. New York, Academic Press.Google Scholar
Kawagoe, Y., Kubo, A., Satoh, H., Takaiwa, F. and Nakamura, Y. (2005) Roles of isoamylase and ADP-glucose pyrophosphorylase in starch granule synthesis in rice endosperm. Plant Journal 42, 164174.Google Scholar
Keeling, P.L. and Myers, A.M. (2010) Biochemistry and genetics of starch synthesis. Annual Review of Food Science and Technology 1, 271303.Google Scholar
Keeling, P.L., Bacon, P.J. and Holt, D.C. (1993) Elevated temperature reduces starch deposition in wheat endosperm by reducing the activity of soluble starch synthase. Planta 191, 342348.Google Scholar
Kempa, S., Rozhon, W., Šamaj, J., Erban, A., Baluška, F., Becker, T., Haselmayer, J., Schleiff, E., Kopka, J., Hirt, H. and Jonak, C. (2007) A plastid-localized glycogen synthase kinase 3 modulates stress tolerance and carbohydrate metabolism. Plant Journal 49, 10761090.Google Scholar
Kerk, D., Conley, T.R., Rodriguez, F.A., Tran, H.T., Nimick, M., Muench, D.G. and Moorhead, G.B.G. (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 Journal 46, 400413.Google Scholar
Kim, H.-S. and Huber, K.C. (2008) Channels within soft wheat starch A- and B-type granules. Journal of Cereal Science 48, 159172.Google Scholar
Kirchberger, S., Leroch, M., Huynen, M.A., Wahl, M., Neuhaus, H.E. and Tjaden, J. (2007) Molecular and biochemical analysis of the plastidic ADP-glucose transporter (ZmBT1) from Zea mays. Journal of Biological Chemistry 282, 2248122491.Google Scholar
Kleczkowski, L.A. (1994) Glucose activation and metabolism through UDP-glucose pyrophosphorylase in plants. Phytochemistry 37, 15071515.Google Scholar
Kleczkowski, L.A., Villand, P., Lüthi, E., Olsen, O.A. and Preiss, J. (1993) Insensitivity of barley endosperm ADP-glucose pyrophosphorylase to 3-phosphoglycerate and orthophosphate regulation. Plant Physiology 101, 179186.Google Scholar
Klucinec, J.D. and Thompson, D.B. (2002) Structure of amylopectins from ae-containing maize starches. Cereal Chemistry 79, 1923.Google Scholar
Köhler, R.H., Cao, J., Zipfel, W.R., Webb, W.W. and Hanson, M.R. (1997) Exchange of protein molecules through connections between higher plant plastids. Science 276, 20392042.Google Scholar
Kolbe, A., Tiessen, A., Schluepmann, H., Paul, M., Ulrich, S. and Geigenberger, P. (2005) Trehalose 6-phosphate regulates starch synthesis via posttranslational redox activation of ADP-glucose pyrophosphorylase. Proceedings of the National Academy of Sciences, USA 102, 1111811123.Google Scholar
Kosar-Hashemi, B., Li, Z., Larroque, O., Regina, A., Yamamori, M., Morell, M.K. and Rahman, S. (2007) Multiple effects of the starch synthase II mutation in developing wheat endosperm. Functional Plant Biology 34, 431438.Google Scholar
Kötting, O., Pusch, K., Tiessen, A., Geigenberger, P., Steup, M. and Ritte, G. (2005) Identification of a novel enzyme required for starch metabolism in Arabidopsis leaves. The phosphoglucan, water dikinase. Plant Physiology 137, 242252.Google Scholar
Kötting, O., Santelia, D., Edner, C., Eicke, S., Marthaler, T., Gentry, M.S., Comparot-Moss, S., Chen, J., Smith, A.M., Steup, M., Ritte, G. and Zeeman, S.C. (2009) SEX4, a glucan phosphatase, dephosphorylates amylopectin at the granule surface during starch breakdown in Arabidopsis leaves. Plant Cell 21, 334346.Google Scholar
Kötting, O., Kossmann, J., Zeeman, S.C.andLloyd, J.R. (2010) Regulation of starch metabolism: the age of enlightenment? Current Opinion in Plant Biology 13, 321329.Google Scholar
Kubo, A., Rahman, S., Utsumi, Y., Li, Z., Makai, Y., Yamamoto, M., Ugaki, M., Harada, K., Satoh, H., Konik-Rose, C., Morell, M. and Nakamura, Y. (2005) Complementation of sugary-1 phenotype in rice endosperm with the wheat isoamylase1 gene supports a direct role for isoamylase1 in amylopectin biosynthesis. Plant Physiology 137, 4356.Google Scholar
Kubo, A., Colleoni, C., Dinges, J.R., Lin, Q., Lappe, R.R., Rivenbark, J.G., Meyer, A.J., Ball, S.G., James, M.G., Hennen-Bierwagen, T.A. and Myers, A.M. (2010) Functions of heteromeric and homomeric isoamylase-type starch-debranching enzymes in developing maize endosperm. Plant Physiology 153, 956969.Google Scholar
Kuriki, T., Guan, H.P., Sivak, M. and Preiss, J. (1996) Analysis of the active center of branching enzyme II from maize endosperm. Journal of Protein Chemistry 15, 305313.Google Scholar
Kuriki, T., Stewart, D.C. and Preiss, J. (1997) Construction of chimeric enzymes out of maize endosperm branching enzymes I and II: activity and properties. Journal of Biological Chemistry 272, 2899929004.Google Scholar
La Cognata, U., Willmitzer, L. and Müller-Röber, B. (1995) Molecular cloning and characterisation of novel isoforms of potato ADP-glucose pyrophosphorylase. Molecular and General Genetics 246, 538548.Google Scholar
Langeveld, S.M.J., van Wijk, R., Stuurman, N., Kijne, J.W. and de Pater, S. (2000) B-type granule containing protrusions and interconnections between amyloplasts in developing wheat endosperm revealed by transmission electron microscopy and GFP expression. Journal of Experimental Botany 51, 13571361.Google Scholar
Lee, S.-K., Hwang, S.-K., Han, M., Eom, J.-S., Kang, H.-G., Han, Y., Choi, S.-B., Cho, M.-H., Bhoo, S.H., An, G., Hahn, T.-R., Okita, T.W. and Jeon, J.-S. (2007) Identification of the ADP-glucose pyrophosphorylase isoforms essential for starch synthesis in the leaf and seed endosperm of rice (Oryza sativa L.). Plant Molecular Biology 65, 531546.Google Scholar
Leterrier, M., Holappa, L., Broglie, K.E. and Beckles, D.M. (2008) Cloning, characterization and comparative analysis of a starch synthase IV gene in wheat: functional and evolutionary implications. BMC Plant Biology 8, 98.Google Scholar
Lin, T.-P., Spilatro, S.R. and Preiss, J. (1988) Characterization of D-enzyme 4-alpha glucanotransferase in Arabidopsis leaf. Plant Physiology 86, 260265.Google Scholar
Lin, Y., Sun, L., Nguyen, L.V., Rachubinski, R.A. and Goodman, H.M. (1999) The pex16b homologue SSE1 and storage organelle formation in Arabidopsis seeds. Science 284, 328330.Google Scholar
Lindeboom, N., Chang, P.R. and Tyler, R.T. (2004) Analytical, biochemical and physicochemical aspects of starch granule size, with emphasis on small granule starches: a review. Starch-Stärke 56, 8999.Google Scholar
Liu, F., Makhmoudova, A., Lee, E.A., Wait, R., Emes, M.J. and Tetlow, I.J. (2009) The amylose extender mutant of maize conditions novel protein-protein interactions between starch biosynthetic enzymes in amyloplasts. Journal of Experimental Botany 60, 44234440.Google Scholar
Lloyd, J.R., Landschütze, V. and Kossmann, J. (1999a) Simultaneous antisense inhibition of two starch-synthase isoforms in potato tubers leads to accumulation of grossly modified amylopectin. Biochemical Journal 338, 515521.Google Scholar
Lloyd, J.R., Springer, F., Buléon, A., Müller-Rober, B., Willmitzer, L. and Kossmann, J. (1999b) The influence of alterations in ADP glucose pyrophosphorylase activities on starch structure and composition in potato tubers. Planta 209, 230238.Google Scholar
Lohi, H., Ianzano, L., Zhao, X.C., Chan, E.M., Turnbull, J., Scherer, S.W., Ackerley, C.A. and Minassian, B.A. (2005) Novel glycogen synthase kinase 3 and ubiquitination pathways in progressive myoclonus epilepsy. Human Molecular Genetics 14, 27272736.Google Scholar
Maddelein, M.L., Libessart, N., Bellanger, F., Delrue, B., D'Hulst, C. and Ball, S. (1994) Toward an understanding of the biogenesis of the starch granule: determination of granule-bound and soluble starch synthase functions in amylopectin synthesis. Journal of Biological Chemistry 269, 2515025157.Google Scholar
Mangelsdorf, P.C. (1947) The inheritance of amylaceous sugary endosperm and its derivatives in maize. Genetics 32, 448458.CrossRefGoogle ScholarPubMed
Manners, D.J. (1989) Recent developments in our understanding of amylopectin structure. Carbohydrate Polymers 11, 87112.Google Scholar
May, L.H. and Buttrose, M.S. (1959) Physiology of cereal grain. II. Starch granule formation in the developing barley kernel. Australian Journal of Biological Science 12, 146159.Google Scholar
Meredith, P. (1981) Large and small starch granules in wheat – Are they really different? Starch-Stärke 33, 4044.Google Scholar
Möhlmann, T., Tjaden, J., Henrichs, G., Quick, W.P., Hausler, R. and Neuhaus, H.E. (1997) ADPglucose drives starch synthesis in isolated maize endosperm amyloplasts: characterisation of starch synthesis and transport properties across the amyloplast envelope. Biochemical Journal 324, 503509.Google Scholar
Morell, M.K., Blennow, A., Kosar-Hashemi, B. and Samuel, M.S. (1997) Differential expression and properties of starch branching enzyme isoforms in developing wheat endosperm. Plant Physiology 113, 201208.Google Scholar
Morell, M.K., Kosar-Hashemi, B., Cmiel, M., Samuel, M.S., Chandler, P., Rahman, S., Buléon, A., Batey, I.L. and Li, Z. (2003) Barley sex6 mutants lack starch synthase IIa activity and contain a starch with novel properties. Plant Journal 34, 173185.Google Scholar
Morris, D.L. and Morris, C.T. (1939) Glycogen in the seed of Zea mays. Journal of Biological Chemistry 130, 535544.Google Scholar
Mouille, G., Maddelein, M.-L., Libessart, N., Talaga, P., Decq, A., Delrue, B. and Ball, S. (1996) Phytoglycogen processing: a mandatory step for starch biosynthesis in plants. Plant Cell 8, 13531366.Google Scholar
Mu, H.M., Yu, Y., Wasserman, B.P. and Carman, G.M. (2001) Purification and characterization of the maize amyloplast stromal 112 kDa starch phosphorylase. Archives of Biochemistry and Biophysics 388, 155164.Google Scholar
Mu-Forster, C., Huang, R., Powers, J.R., Harriman, R.W., Knight, M., Singletary, G.W., Keeling, P.L. and Wasserman, B.P. (1996) Physical association of starch biosynthetic enzymes with starch granules of maize endosperm. Granule-associated forms of starch synthase I and starch branching enzyme II. Plant Physiology 111, 821829.Google Scholar
Müller-Rober, B., Kossmann, J., Hannah, L.C., Willmitzer, L. and Sonnewald, U. (1990) Only one of two different ADPglucose pyrophosphorylase genes from potato responds strongly to elevated levels of sucrose. Molecular and General Genetics 224, 136146.Google Scholar
Myers, A.M., Morell, M.K., James, M.G. and Ball, S.G. (2000) Recent progress toward understanding the biosynthesis of the amylopectin crystal. Plant Physiology 122, 989998.Google Scholar
Nakamura, T., Vrinten, P., Hayakawa, K. and Ikeda, J. (1998) Characterization of a granule-bound starch synthase isoform found in the pericarp of wheat. Plant Physiology 118, 451459.Google Scholar
Nakamura, Y. (2002) Towards a better understanding of the metabolic system for amylopectin biosynthesis in plants: rice endosperm as a model tissue. Plant and Cell Physiology 43, 718725.Google Scholar
Nakamura, Y. and Kawaguchi, K. (1992) Multiple forms of ADP-glucose pyrophosphorylase of rice endosperm. Physiologia Plantarum 84, 336342.Google Scholar
Nakamura, Y., Takahashi, J., Sakurai, A., Inaba, Y., Suzuki, E., Nihei, S., Fujiwara, S., Tsuzuki, M., Miyashita, H., Ikemoto, H., Kawachi, M., Sekiguchi, H. and Kurano, N. (2005) Some cyanobacteria synthesize semi-amylopectin type α-polyglucans instead of glycogen. Plant Cell Physiology 46, 539545.Google Scholar
Nakano, K. and Fukui, T. (1986) The complete amino acid sequence of potato α-glucan phosphorylase. Journal of Biological Chemistry 261, 82308236.Google Scholar
Nelson, O.E. and Rines, H.W. (1962) The enzymatic deficiency in the waxy mutant of maize. Biochemical and Biophysical Research Communications 9, 297300.Google Scholar
Nichols, D.J., Keeling, P.L., Spalding, M. and Guan, H. (2000) Involvement of conserved aspartate and glutamate residues in the catalysis and substrate binding of maize starch synthase. Biochemistry 39, 78207825.CrossRefGoogle ScholarPubMed
Nielsen, T.H., Baunsgaard, L. and Blennow, A. (2002) Intermediary glucan structures formed during starch granule biosynthesis are enriched in short side chains, a dynamic pulse labelling approach. Journal of Biological Chemistry 277, 2024920255.Google Scholar
Niittylä, T., Messerli, G., Trevisan, M., Chen, J., Smith, A.M. and Zeeman, S.C. (2004) A previously unknown maltose transporter essential for starch degradation in leaves. Science 303, 8789.Google Scholar
Niittylä, T., Comparot-Moss, S., Lue, W.L., Messerli, G., Trevisan, M., Seymour, M.D.J., Gatehouse, J.A., Villadsen, D., Smith, S.M., Chen, J., Zeeman, S.C. and Smith, A.M. (2006) Similar protein phosphatases control starch metabolism in plants and glycogen metabolism in mammals. Journal of Biological Chemistry 281, 1181511818.Google Scholar
Nishi, A., Nakamura, Y., Tanaka, N. and Satoh, H. (2001) Biochemical and genetic effects of amylose-extender mutation in rice endosperm. Plant Physiology 127, 459472.Google Scholar
Olive, M.R., Ellis, R.J. and Schuch, W.W. (1989) Isolation and nucleotide sequences of cDNA clones encoding ADPglucose pyrophosphorylase polypeptides from wheat leaf and endosperm. Plant Molecular Biology 12, 525538.Google Scholar
Olsen, O.A. (2001) Endosperm development: cellularization and cell fate specification. Annual Review of Plant Physiology and Plant Molecular Biology 52, 233267.Google Scholar
Parker, M.L. (1985) The relationship between A-type and B-type starch granules in the developing endosperm of wheat. Journal of Cereal Science 3, 271278.Google Scholar
Patron, N.J. and Keeling, P.J. (2005) Common evolutionary origin of starch biosynthetic enzymes in green and red algae. Journal of Phycology 41, 11311141.Google Scholar
Peng, M., Gao, M., Båga, M., Hucl, P. and Chibbar, R.N. (2000) Starch-branching enzymes preferentially associated with A-type starch granules in wheat endosperm. Plant Physiology 124, 265272.Google Scholar
Peng, M., Hucl, P. and Chibbar, R.N. (2001) Isolation, characterization and expression analysis of starch synthase I from wheat (Triticum aestivum L.). Plant Science 161, 10551062.Google Scholar
Pilling, E. and Smith, A.M. (2003) Growth ring formation in the starch granules of potato tubers. Plant Physiology 132, 365371.Google Scholar
Preiss, J. (1991) Biology and molecular biology of starch synthesis and its regulation. pp. 59114in Miflin, B.J. (Ed.) Oxford surveys of cellular and molecular biology. Vol. 7. Oxford, Oxford University Press.Google Scholar
Preiss, J. and Sivak, M. (1996) Starch synthesis in sinks and sources. pp. 6369in Zamski, E.; Schaffter, A.A. (Eds) Photoassimilate distribution in plants and crops. New York, Marcel Dekker.Google Scholar
Prioul, J.-L., Jeanette, E., Reyss, A., Grégory, N., Giroux, M., Hannah, L.C. and Causse, M. (1994) Expression of ADPglucose pyrophosphorylase in maize (Zea mays L.) grain and source leaf during grain filling. Plant Physiology 104, 179187.Google Scholar
Puteaux, J.L., Potocki-Veronese, G., Remaud-Simeon, M. and Buléon, A. (2006) Alpha-D-glucan-based dendritic nanoparticles prepared by in vitro enzymatic chain extension of glycogen. Biomacromolecules 7, 17201728.Google Scholar
Rahman, S., Kosar-Hashemi, B., Samuel, M.S., Hill, A., Abbott, D.C., Skerritt, J.H., Preiss, J., Appels, R. and Morell, M.K. (1995) The major proteins of wheat endosperm starch granules. Australian Journal Plant Physiology 22, 793803.Google Scholar
Rahman, S., Regina, A., Li, Z., Mukai, Y., Yamamoto, M., Kosar-Hashemi, B., Abrahams, S. and Morell, M.K. (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 Physiology 125, 13141324.Google Scholar
Ral, J.P., Derelle, E., Ferraz, C., Wattebled, F., Farinas, B., Corellou, F., Buléon, A., Slomianny, M.C., Delvallé, D., d'Hulst, C., Rombauts, S., Moreau, H. and Ball, S. (2004) Starch division and partitioning. A mechanism for granule propagation and maintenance in the picophytoplanktonic green alga Ostreococcus taurii. Plant Physiology 136, 33333340.Google Scholar
Ral, J.P., Colleoni, C., Wattebled, F., Dauvillée, D., Nempont, C., Deschamps, P., Li, Z., Morell, M.K., Chibbar, R., Purton, S., d'Hulst, C. and Ball, S.G. (2006) Circadian clock regulation of starch metabolism establishes GBSSI as a major contributor to amylopectin synthesis in Chlamydomonas reinhardtii. Plant Physiology 142, 305317.Google Scholar
Recondo, E. and Leloir, L. (1961) Adenosine diphosphate glucose and starch biosynthesis. Biochemical and Biophysical Research Communications 6, 8588.Google Scholar
Regina, A., Kosar-Hashemi, B., Li, Z., Pedler, A., Mukai, Y., Yamamoto, M., Gale, K., Sharp, P.J., Morell, M.K. and Rahman, S. (2005) Starch branching enzyme IIb in wheat is expressed at low levels in the endosperm compared to other cereals and encoded at a non-syntenic locus. Planta 222, 899909.Google Scholar
Regina, A., Li, Z., Bird, A., Topping, D., Bowden, S., Freeman, J., Barsby, T., Kosar-Hashemi, B., Li, Z., Rahman, S. and Morell, M.K. (2006) High-amylose wheat generated by RNA interference improves indices of large-bowel health in rats. Proceedings of the National Academy of Sciences, USA 103, 35463551.Google Scholar
Ritte, G., Lloyd, J.R., Eckermann, N., Rotmann, A., Kossmann, J. and Steup, M. (2002) The starch related R1 protein is an α-glucan, water dikinase. Proceedings of the National Academy of Sciences, USA 99, 17661771.Google Scholar
Ritte, G., Scharf, A., Eckermann, N., Haebel, S. and Steup, M. (2004) Phosphorylation of transitory starch is increased during degradation. Plant Physiology 135, 20682077.Google Scholar
Roach, P.J. (2002) Glycogen and its metabolism. Current Molecular Medicine 2, 101120.Google Scholar
Roberts, M.R. (2003) 14-3-3 Proteins find new partners in plant cell signalling. Trends in Plant Science 8, 218223.Google Scholar
Robin, J.P., Mercier, C., Charbonniere, R. and Guilbot, A. (1974) Lintnerized starches: gel filtration and enzymatic studies of insoluble residues from prolonged acid treatment of potato starch. Cereal Chemistry 51, 389406.Google Scholar
Rodriguez, I.R. and Whelan, W.J. (1985) A novel glycosyl-amino acid linkage: rabbit-muscle glycogen is covalently linked to a protein via tyrosine. Biochemical and Biophysical Research Communications 132, 829836.Google Scholar
Roldán, I., Lucas, M.M., Delvallé, D., Planchot, V., Jimenez, S., Perez, R., Ball, S., D'Hulst, C. and Mérida, A. (2007) The phenotype of soluble starch synthase IV defective mutants of Arabidopsis thaliana suggests a novel function of elongation enzymes in the control of starch granule formation. Plant Journal 49, 492504.Google Scholar
Rolletschek, H., Hajirezaei, M.-R., Wobus, U. and Weber, H. (2002) Antisense-inhibition of ADP-glucose pyrophosphorylase in Vicia narbonensis seeds increases soluble sugars and leads to higher water and nitrogen uptake. Planta 214, 954964.Google Scholar
Rolletschek, H., Koch, K., Wobus, U. and Borisjuk, L. (2005) Positional cues for the starch/lipid balance in maize kernels and resource partitioning to the embryo. Plant Journal 42, 6983.Google Scholar
Röper, H. (2002) Renewable raw materials in Europe – industrial utilization of starch and sugar. Starch-Stärke 54, 8999.Google Scholar
Rowland-Bamford, A.J., Allen, L.H. Jr, Baker, J.T. and Boote, K.J. (1990) Carbon dioxide effects on carbohydrate status and partitioning in rice. Plant Cell and Environment 14, 16011608.Google Scholar
Rydberg, U., Andersson, L., Andersson, R., Åman, P. and Larsson, H. (2001) Comparison of starch branching enzyme I and II from potato. European Journal of Biochemistry 268, 61406145.Google Scholar
Ryoo, N., Yu, C., Park, C.-S., Baik, Y., Park, I.M., Cho, M.-H., Bhoo, S.H., An, G., Hahn, F.R. and Jeon, J.-S. (2007) Knockout of a starch synthase gene OsSSIIIa/Flo5 causes white-core floury endosperm in rice (Oryza sativa L.). Plant Cell Reports 26, 10831095.Google Scholar
Sakulsingharoj, C., Choi, S.-B., Hwang, S.-K., Edwards, G.E., Bork, J., Meyer, C.R., Preiss, J. and Okita, T.W. (2004) Engineering starch biosynthesis for increasing seed weight: the role of the cytoplasmic ADP-glucose pyrophosphorylase. Plant Science 167, 13231333.Google Scholar
Satoh, H., Nishi, A., Yamashita, K., Takemoto, Y., Tanaka, Y., Hosaka, Y., Sakurai, A., Fujita, N. and Nakamura, Y. (2003) Starch-branching enzyme I-deficient mutation specifically affects the structure and properties of starch in rice endosperm. Plant Physiology 133, 11111121.Google Scholar
Sawada, T., Francisco, P.B. Jr, Aihara, S., Utsumi, Y., Yoshida, M., Oyama, Y., Tsusuki, M., Satoh, H. and Nakamura, Y. (2009) Chlorella starch branching enzyme (BE) can complement the function of BEIIb in rice endosperm. Plant and Cell Physiology 50, 10621074.Google Scholar
Schiefer, S., Lee, E.Y.C. and Whelan, W.J. (1973) Federation of the European Biochemical Society Letters 30, 129.Google Scholar
Schwall, G.P., Safford, R., Westcott, R.J., Jeffcoat, R., Tayal, A., Shi, Y.C., Gidley, M.J. and Jobling, S.A. (2000) Production of very-high-amylose potato starch by inhibition of SBE A and B. Nature Biotechnology 18, 551554.Google Scholar
Sehnke, P.C. and Ferl, R.J. (2002) 14-3-3 protein: effectors of enzyme function. Annual Plant Reviews 7, 5376.Google Scholar
Sehnke, P.C., Henry, R., Cline, K. and Ferl, R.J. (2000) Interaction of a plant 14-3-3 protein with the signal peptide of a thylakoid-targetted chloroplast precursor protein and the presence of 14-3-3 isoforms in the chloroplast stroma. Plant Physiology 122, 235240.Google Scholar
Sehnke, P.C., Chung, H.-J., Wu, K. and Ferl, R.J. (2001) Regulation of starch accumulation by granule-associated plant 14-3-3 proteins. Proceedings of the National Academy of Sciences, USA 98, 765770.Google Scholar
Seo, B-s., Kim, S., Scott, M.P., Singletary, G.W., Wong, K-s., James, M.G. and Myers, A.M. (2002) Functional interactions between heterologously expressed starch-branching enzymes of maize and glycogen synthases of Brewer's yeast. Plant Physiology 128, 11891199.Google Scholar
Shure, M., Wessler, S. and Fedoroff, N. (1983) Molecular identification and isolation of the waxy locus in maize. Cell 35, 225233.Google Scholar
Sikka, V.K., Choi, S., Kavakli, I.H., Sakulsingharoj, C., Gupta, S., Ito, H. and Okita, T.W. (2001) Subcellular compartmentation and allosteric regulation of the rice endosperm ADPglucose pyrophosphorylase. Plant Science 161, 461468.Google Scholar
Smith, A.M. (2008) Prospects for increasing starch and sucrose yields for bioethanol production. Plant Journal 54, 546558.Google Scholar
Smith, A.M. and Stitt, M. (2007) Coordination of carbon supply and plant growth. Plant, Cell and Environment 30, 11261149.Google Scholar
Smith, A.M., Denyer, K. and Martin, C. (1997) The synthesis of the starch granule. Annual Review of Plant Physiology and Plant Molecular Biology 48, 6787.Google Scholar
Sokolov, L.N., Dominguez-Solis, J.R., Allary, A.L., Buchannan, B.B. and Luan, S. (2006) A redox-regulated protein phosphatase binds to starch diurnally and functions in its accumulation. Proceedings of the National Academy of Sciences, USA 103, 97329737.Google Scholar
Stahl, Y., Coates, S., Bryce, J.H. and Morris, P.C. (2004) Antisense downregulation of the barley limit dextrinase inhibitor modulates starch granule size distribution, starch composition and amylopectin structure. Plant Journal 39, 599611.Google Scholar
Stark, D.M., Timmerman, K.P., Barry, G.F., Preiss, J. and Kishore, G.M. (1992) Regulation of the amount of starch in plant tissues by ADP glucose pyrophosphorylase. Science 258, 287292.Google Scholar
Streb, S., Delatte, T., Umhang, M., Eicke, S., Schorderet, M., Reinhardt, D. and Zeeman, S.C. (2008) Starch granule biosynthesis in Arabidopsis is abolished by removal of all debranching enzymes but restored by the subsequent removal of an endoamylase. Plant Cell 20, 34483466.Google Scholar
Sun, C., Sathish, P., Ahlandsberg, S. and Jansson, C. (1998) The two genes encoding starch-branching enzymes IIa and IIb are differentially expressed in barley. Plant Physiology 118, 3749.Google Scholar
Szydlowski, N., Ragel, P., Raynaud, S., Lucas, M.M., Roldán, I., Montero, M., Munoz, F.J., Ovecka, M., Bahaji, A., Planchot, V., Pozueta-Romero, J., D'Hulst, C. and Mérida, A. (2009) Starch granule initiation in Arabidopsis requires the presence of either class IV or class III starch synthases. Plant Cell 21, 24432457.Google Scholar
Takaha, T., Yanase, M., Okada, S. and Smith, S.M. (1993) Disproportionating enzyme (4-α-glucanotransferase: EC 2.4.1.25) of potato. Journal of Biological Chemistry 268, 13911396.Google Scholar
Takaha, T., Critchley, J., Okada, S. and Smith, S.M. (1998) Normal starch content and composition in tubers of antisense potato plants lacking D-enzyme (4-α-glucanotransferase). Planta 205, 445451.Google Scholar
Takeda, Y., Guan, H.-P. and Preiss, J. (1993) Branching of amylose by the branching isoenzymes of maize endosperm. Carbohydrate Research 240, 253263.Google Scholar
Tetlow, I.J., Bowsher, C.G., Scrase-Field, E.F.A.L., Davies, E.J. and Emes, M.J. (2003a) The synthesis and transport of ADPglucose in cereal endosperms. Journal of Applied Glycoscience 50, 231236.Google Scholar
Tetlow, I.J., Davies, E.J., Vardy, K.A., Bowsher, C.G., Burrell, M.M. and Emes, M.J. (2003b) Subcellular localization of ADPglucose pyrophosphorylase in developing wheat endosperm and analysis of a plastidial isoform. Journal of Experimental Botany 54, 715725.Google Scholar
Tetlow, I.J., Wait, R., Lu, Z., Akkasaeng, R., Bowsher, C.G., Esposito, S., Kosar-Hashemi, B., Morell, M.K. and Emes, M.J. (2004) Protein phosphorylation in amyloplasts regulates starch branching enzyme activity and protein-protein interactions. Plant Cell 16, 694708.Google Scholar
Tetlow, I.J., Beisel, K.G., Cameron, S., Makhmoudova, A., Liu, F., Bresolin, N.S., Wait, R., Morell, M.K. and Emes, M.J. (2008) Analysis of protein complexes in amyloplasts reveals functional interactions among starch biosynthetic enzymes. Plant Physiology 146, 18781891.Google Scholar
Thompson, D.B. (2000) On the non-random nature of amylopectin branching. Carbohydrate Polymers 43, 223239.Google Scholar
Thorbjørnsen, T., Villand, P., Denyer, K., Olsen, O.A. and Smith, A.M. (1996a) Distinct isoforms of ADPglucose pyrophosphorylase occur inside and outside the amyloplasts in barley endosperm. Plant Journal 10, 243250.Google Scholar
Thorbjørnsen, T., Villand, P., Kleczkowski, L.A. and Olsen, O.A. (1996b) A single gene encodes two different transcripts for the ADP-glucose pyrophosphorylase small subunit from barley (Hordeum vulgare). Biochemical Journal 313, 149154.Google Scholar
Tiessen, A., Hendriks, J.H.M., Stitt, M., Branscheid, A., Gibon, Y., Farré, E.M. and Geigenberger, P. (2002) Starch synthesis in potato tuber is regulated by post-translational redox modification of ADP-glucose pyrophosphorylase. Plant Cell 14, 21912213.Google Scholar
Tiessen, A., Prescha, K., Branscheid, A., Palacios, N., McKibbin, R., Halford, N.G. and 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 Journal 35, 490500.Google Scholar
Tomlinson, K. and Denyer, K. (2003) Starch synthesis in cereal grains. Advances in Botanical Research 40, 161.Google Scholar
Tsai, C.-Y. (1974) The function of the waxy locus in starch synthesis in maize endosperm. Biochemical Genetics 11, 8396.Google Scholar
Umemoto, T. and Aoki, N. (2005) Single-nucleotide polymorphisms in rice starch synthase IIa that alter starch gelatinisation and starch association of the enzyme. Functional Plant Biology 32, 763768.Google Scholar
Valdez, H.A., Busi, M.V., Wayllace, N.Z., Parisi, G., Ugalde, R.A. and Gomez-Casati, D.F. (2008) Role of the N-terminal starch-branching domains in the kinetic properties of starch synthase III from Arabidopsis thaliana. Biochemistry 47, 30263032.Google Scholar
Van Berkel, J., Conrads-Strauch, J. and Steup, M. (1991) Glucan-phosphorylase forms in cotyledons of Pisum sativum L.: localization, developmental change, in-vitro translation, and processing. Planta 185, 432439.Google Scholar
Van den Koornhuyse, N., Libessart, N., Delrue, B., Zabawinski, C., Decq, A., Iglesias, A., Carlton, A., Preiss, J. and Ball, S. (1996) Control of starch composition and structure through substrate supply in the mono-cellular alga Chlamydomonas reinhardtii. Journal of Biological Chemistry 271, 1628116287.Google Scholar
Van de Wal, M., D'Hulst, C., Vincken, J.-P., Buléon, A., Visser, R. and Ball, S. (1998) Amylose is synthesized in vitro by extension of and cleavage from amylopectin. Journal of Biological Chemistry 273, 2223222240.Google Scholar
Villand, P., Aalen, R., Olsen, O.-A., Lonneborg, A., Lüthi, E. and Kleczkowski, L.A. (1992a) PCR-amplification and sequence of cDNA clones for the small and large subunits of ADP-glucose pyrophosphorylase from barley tissues. Plant Molecular Biology 19, 381389.Google Scholar
Villand, P., Olsen, O.-A., Killan, A. and Kleczkowski, L.A. (1992b) ADPglucose pyrophosphorylase large subunit cDNA from barley endosperm. Plant Physiology 100, 16171618.Google Scholar
Vrinten, P. and Nakamura, T. (2000) Wheat granule-bound starch synthase I and II are encoded by separate genes that are expressed in different tissues. Plant Physiology 122, 255263.Google Scholar
Waigh, T.A., Perry, P., Reikel, C., Gidley, M.J. and Donald, A.M. (1998) Chiral side-chain liquid-crystalline polymeric properties of starch. Macromolecules 31, 79807984.Google Scholar
Wattebled, F., Dong, Y., Dumez, S., Delvallé, D., Planchot, V., Berbezy, P., Vyas, D., Colonna, P., Chatterjee, S., Ball, S. and D'Hulst, C. (2005) Mutants of Arabidopsis lacking a chloroplastic isoamylase accumulate phytoglycogen and an abnormal form of amylopectin. Plant Physiology 138, 184195.Google Scholar
Wattebled, F., Planchot, V., Dong, Y., Szydlowski, N., Pontoire, B., Devin, A., Ball, S. and D'Hulst, C. (2008) Further evidence for the mandatory nature of polysaccharide debranching for the aggregation of semicrystalline starch and for overlapping functions of debranching enzymes in Arabidopsis leaves. Plant Physiology 148, 13091323.Google Scholar
Wayllace, N.Z., Valdez, H.A., Ugalde, R.A., Busi, M.V. and Gomez-Casati, D.F. (2010) The starch biding capacity of the noncatalytic SBD2 region and the interaction between the N- and C-terminal domains are involved in the modulation of the activity of starch synthase III from Arabidopsis thaliana. FEBS Journal 277, 428440.Google Scholar
Weber, A.P.M., Schwacke, R. and Flügge, U.-I. (2005) Solute transporters of the plastid envelope membrane. Annual Review of Plant Biology 56, 133164.Google Scholar
Weber, H., Heim, U., Borisjuk, L. and Wobus, U. (1995) Cell-type specific, coordinate expression of two ADPglucose pyrophosphorylase genes in relation to starch biosynthesis during seed development in Vicia faba L. Planta 195, 352361.Google Scholar
Weber, H., Rolletschek, H., Heim, U., Golombek, S., Gubatz, S. and Wobus, U. (2000) Antisense-inhibition of ADP-glucose pyrophosphorylase in developing seeds of Vicia narbonensis moderately decreases starch but increases protein content and affects seed maturation. Plant Journal 24, 3343.Google Scholar
Wei, C., Zhang, J., Chen, Y., Zhou, W., Xu, B., Wang, Y. and Chen, J. (2010) Physicochemical properties and development of wheat large and small starch granules during endosperm development. Acta Physiologia Plantarum 32, 905916.Google Scholar
Weigelt, K., Küster, H., Rutten, T., Fait, A., Ffernie, A.R., Miersch, O., Wasternack, C., Emery, R.J.N., Desel, C., Hosein, F., Müller, M., Saalbach, I. and Weber, H. (2009) ADP-Glucose pyrophosphorylase-deficient pea embryos reveal specific transcriptional and metabolic changes of carbon–nitrogen metabolism and stress responses. Plant Physiology 149, 395411.Google Scholar
Whelan, W.J. (1986) The initiation of glycogen synthesis. Bioessays 5, 136140.Google Scholar
Wilson, J.D., Bechtel, D.B., Todd, T.C. and Seib, P.A. (2006) Measurement of wheat starch granule size distribution using image analysis and laser diffraction technology. Cereal Chemistry 83, 259268.Google Scholar
Wobus, U. and Weber, H. (1999) Sugars as signal molecules in plant seed development. Biological Chemistry 380, 937944.Google Scholar
Woodrow, I.E. and Berry, J.A. (1988) Enzymatic regulation of photosynthetic CO2 fixation. Annual Review of Plant Physiology and Plant Molecular Biology 39, 533594.Google Scholar
Wurzburg, O.B. (1986) Modified starches – their chemistry and properties in Wurzburg, O.B. (Ed.) Modified starches: properties and uses. Boca Raton, CRC Press.Google Scholar
Xie, X. and Liu, Q. (2004) Development and physicochemical characterization of new resistant citrate starch from different corn starches. Starch-Stärke 56, 364370.Google Scholar
Yamanouchi, H. and Nakamura, Y. (1992) Organ specificity of isoforms of starch branching enzyme (Q-enzyme) in rice. Plant and Cell Physiology 33, 985991.Google Scholar
Yao, Y., Guiltinan, M.J., Shannon, J.C. and Thompson, D.B. (2002) Single kernel sampling method for maize starch analysis while maintaining kernel vitality. Cereal Chemistry 79, 757762.Google Scholar
Yao, Y., Thompson, D.B. and Guiltinan, M.J. (2004) Maize starch-branching enzyme isoforms and amylopectin structure. In the absence of starch-branching enzyme IIb, the further absence of starch-branching enzyme Ia leads to increased branching. Plant Physiology 136, 35153523.Google Scholar
Young, G.-H., Chen, H.-M., Lin, C.-T., Tseng, K.-C., Wu, J.-S. and Juang, R.-H. (2006) Site-specific phosphorylation of L-form starch phosphorylase by the protein kinase activity from sweet potato roots. Planta 223, 468478.Google Scholar
Yu, Y., Mu, H.H., Wasserman, B.P. and Carman, G.M. (2001) Identification of the maize amyloplast stromal 112-kD protein as a plastidic starch phosphorylase. Plant Physiology 125, 351359.Google Scholar
Zeeman, S.C., Umemoto, T., Lue, W.L., Au-Yeung, P., Martin, C., Smith, A.M. and Chen, J. (1998) A mutant of Arabidopsis lacking a chloroplastic isoamylase accumulates both starch and phytoglycogen. Plant Cell 10, 16991712.Google Scholar
Zeeman, S.C., Pilling, E., Tiessen, A., Kato, L., Donald, A.M. and Smith, A.M. (2002) Starch synthesis in Arabidopsis: granule synthesis, composition and structure. Plant Physiology 129, 516529.Google Scholar
Zeeman, S.C., Kossman, J. and Smith, A.M. (2010) Starch, its metabolism, evolution, and biotechnological modification in plants. Annual Review of Plant Biology 61, 209234.Google Scholar
Zhang, X., Colleoni, C., Ratushna, V., Sirghie-Colleoni, M., James, M.G. and Myers, A.M. (2004) Molecular characterization demonstrates that the Zea mays gene sugary2 codes for the starch synthase isoform SSIIa. Plant Molecular Biology 54, 865879.Google Scholar
Zhang, X., Myers, A.M. and James, M.G. (2005) Mutations affecting starch synthase III in Arabidopsis alter leaf starch structure and increase the rate of starch synthesis. Plant Physiology 138, 663674.Google Scholar
Zhang, X., Szydlowski, N., Delvallé, D., D'Hulst, C., James, M.G. and Myers, A.M. (2008) Overlapping functions of the starch synthases SSII and SSIII in amylopectin biosynthesis in Arabidopsis. BMC Plant Biology 8, 96.Google Scholar
Ziegler, G.R., Creek, J.A. and Runt, J. (2005) Spherulitic crystallization in starch as a model for starch granule initiation. Biomacromolecules 6, 15471554.Google Scholar