Skip to main content
SpringerLink
Log in

Starch Metabolism in Green Plants

  • Reference work entry
  • First Online:
Polysaccharides

Abstract

Starch is a substantial component of the human diet providing about 50 % of daily energy uptake, mostly through unrefined cereals. Starch and sucrose are the primary products of photosynthesis. Starch represents the main plant storage carbohydrate that provides energy during heterotrophic growth. Its synthesis and degradation have been studied deeply, reaching a good level of knowledge of the metabolism as a whole. Not only the enzymes involved but also the intracellular localization of the reactions, its regulation, its dependence on light–dark cycle, its evolution from ancestral bacteria, and its correlation with parameters of agronomic interest have been studied. In this work we have attempted a comprehensive review of the starch metabolism in Arabidopsis thaliana and other species of agronomic interest and the modular structures present in starch-related enzymes from Arabidopsis thaliana.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 999.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 549.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abel GJ, Springer F, Willmitzer L, Kossmann J (1996) Cloning and functional analysis of a cDNA encoding a novel 139 kDa starch synthase from potato (Solanum tuberosum L.). Plant J 10:981–991

    CAS  Google Scholar 

  • Armisen D, Lecharny A, Aubourg S (2008) Unique genes in plants: specificities and conserved features throughout evolution. BMC Evol Biol 8:280

    Google Scholar 

  • Asatsuma S, Sawada C, Itoh K, Okito M, Kitajima A, Mitsui T (2005) Involvement of alpha-amylase I-1 in starch degradation in rice chloroplasts. Plant Cell Physiol 46:858–869

    CAS  Google Scholar 

  • Bae JM, Giroux M, Hannah LC (1990) Cloning and characterization of the Brittle-2 gene of maize. Maydica 35:317–322

    Google Scholar 

  • Ball SG, Morell MK (2003) From bacterial glycogen to starch: understanding the biogenesis of the plant starch granule. Annu Rev Plant Biol 54:207–233

    CAS  Google Scholar 

  • Ball S, Guan HP, 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

    CAS  Google Scholar 

  • Ballicora MA, Frueauf JB, Fu Y, Schurmann P, Preiss J (2000) Activation of the potato tuber ADP-glucose pyrophosphorylase by thioredoxin. J Biol Chem 275:1315–1320

    CAS  Google Scholar 

  • Ballicora MA, Iglesias AA, Preiss J (2004) ADP-Glucose Pyrophosphorylase: A Regulatory Enzyme for Plant Starch Synthesis. Photosynth Res 79:1–24

    CAS  Google Scholar 

  • Balmer Y, Koller A, del Val G, Manieri W, Schurmann P, Buchanan BB (2003) Proteomics gives insight into the regulatory function of chloroplast thioredoxins. Proc Natl Acad Sci U S A 100:370–375

    CAS  Google Scholar 

  • Barrero JM, Mrva K, Talbot MJ, White RG, Taylor J, Gubler F, Mares DJ (2013) Genetic, hormonal, and physiological analysis of late maturity alpha-amylase in wheat. Plant Physiol 161:1265–1277

    CAS  Google Scholar 

  • Barrett AJ (1995) Nomenclature committee of the international union of biochemistry and molecular biology (NC-IUBMB). Enzyme nomenclature. Recommendations 1992. Supplement 2: corrections and additions (1994). Eur J Biochem 232:1–6

    CAS  Google Scholar 

  • Baunsgaard L, Lutken H, Mikkelsen R, Glaring MA, Pham TT, Blennow A (2005) A novel isoform of glucan, water dikinase phosphorylates pre-phosphorylated alpha-glucans and is involved in starch degradation in Arabidopsis. Plant J 41:595–605

    CAS  Google Scholar 

  • Beatty MK, Rahman A, Cao H, Woodman W, Lee M, Myers AM, James MG (1999) Purification and molecular genetic characterization of ZPU1, a pullulanase-type starch-debranching enzyme from maize. Plant Physiol 119:255–266

    CAS  Google Scholar 

  • Bertoft E (1991) Investigation of the fine structure of alpha-dextrins derived from amylopectin and their relation to the structure of waxy-maize starch. Carbohydr Res 212:229–244

    CAS  Google Scholar 

  • Bhave MR, Lawrence S, Barton C, Hannah LC (1990) Identification and molecular characterization of shrunken-2 cDNA clones of maize. Plant Cell 2:581–588

    CAS  Google Scholar 

  • Blennow A, Bay-Smidt AM, Olsen CE, Moller BL (2000) The distribution of covalently bound phosphate in the starch granule in relation to starch crystallinity. Int J Biol Macromol 27:211–218

    CAS  Google Scholar 

  • Blennow A, Nielsen TH, Baunsgaard L, Mikkelsen R, Engelsen SB (2002) Starch phosphorylation: a new front line in starch research. Trends Plant Sci 7:445–450

    CAS  Google Scholar 

  • Boraston AB, Bolam DN, Gilbert HJ, Davies GJ (2004) Carbohydrate-binding modules: fine-tuning polysaccharide recognition. Biochem J 382:769–781

    CAS  Google Scholar 

  • Botticella E, Sestili F, Hernandez-Lopez A, Phillips A, Lafiandra D (2011) High resolution melting analysis for the detection of EMS induced mutations in wheat SBEIIa genes. BMC Plant Biol 11:156

    CAS  Google Scholar 

  • Bourne Y, Henrissat B (2001) Glycoside hydrolases and glycosyltransferases: families and functional modules. Curr Opin Struct Biol 11:593–600

    CAS  Google Scholar 

  • Boyer CD, Preiss J (1981) Evidence for independent genetic control of the multiple forms of maize endosperm branching enzymes and starch synthases. Plant Physiol 67:1141–1145

    CAS  Google Scholar 

  • Breton C, Mucha J, Jeanneau C (2001) Structural and functional features of glycosyltransferases. Biochimie 83:713–718

    CAS  Google Scholar 

  • Brust H, Lehmann T, d’Hulst C, Fettke J (2014) Analysis of the functional interaction of Arabidopsis starch synthase and branching enzyme isoforms reveals that the cooperative action of SSI and BEs results in glucans with polymodal chain length distribution similar to amylopectin. PLoS One 9:e102364

    Google Scholar 

  • Buschiazzo A, Ugalde JE, Guerin ME, Shepard W, Ugalde RA, Alzari PM (2004) Crystal structure of glycogen synthase: homologous enzymes catalyze glycogen synthesis and degradation. Embo J 23:3196–3205

    CAS  Google Scholar 

  • Busi MV, Palopoli N, Valdez HA, Fornasari MS, Wayllace NZ, Gomez-Casati DF, Parisi G, Ugalde RA (2008) Functional and structural characterization of the catalytic domain of the starch synthase III from Arabidopsis thaliana. Proteins 70:31–40

    CAS  Google Scholar 

  • Busi MV, Martin M, Gomez Casati DF (2012) Plant biotechnology for the development of design starches. In: Karunaratne DN (ed) The complex world of polysaccharides. InTech pp 491–510

    Google Scholar 

  • Busi MV, Barchiesi J, Martin M, Gomez Casati DF (2014) Starch metabolism in green algae. Starch-Starke 66:28–40

    CAS  Google Scholar 

  • 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 U S A 101:2215–2220

    CAS  Google Scholar 

  • Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B (2009) The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res 37:D233–238

    CAS  Google Scholar 

  • Cao H, Imparl-Radosevich J, Guan H, Keeling PL, James MG, Myers AM (1999) Identification of the soluble starch synthase activities of maize endosperm. Plant Physiol 120:205–216

    CAS  Google Scholar 

  • Caspar T, Huber SC, Somerville C (1985) Alterations in growth, photosynthesis, and respiration in a starchless mutant of Arabidopsis thaliana (L.) deficient in chloroplast phosphoglucomutase activity. Plant Physiol 79:11–17

    CAS  Google Scholar 

  • Cavalier-Smith T (2009) Predation and eukaryote cell origins: a coevolutionary perspective. Int J Biochem Cell Biol 41:307–322

    CAS  Google Scholar 

  • Chandler JW, Appel K, Melzer S (2001) A novel putative Beta-amylase gene and Atb-Amy from A. thaliana are circadian regulated. Plant Sci 161:1019–1024

    CAS  Google Scholar 

  • Charnock SJ, Davies GJ (1999) Structure of the nucleotide-diphospho-sugar transferase, SpsA from Bacillus subtilis, in native and nucleotide-complexed forms. Biochemistry 38:6380–6385

    CAS  Google Scholar 

  • Cheng CL, Lo YC, Lee KS, Lee DJ, Lin CY, Chang JS (2011) Biohydrogen production from lignocellulosic feedstock. Bioresour Technol 102:8514–8523

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Christiansen C, Abou Hachem M, Janecek S, Vikso-Nielsen A, Blennow A, Svensson B (2009) The carbohydrate-binding module family 20–diversity, structure, and function. Febs J 276:5006–5029

    CAS  Google Scholar 

  • Commuri PD, Keeling PL (2001) Chain-length specificities of maize starch synthase I enzyme: studies of glucan affinity and catalytic properties. Plant J 25:475–486

    CAS  Google Scholar 

  • Comparot-Moss S, Denyer K (2009) The evolution of the starch biosynthetic pathway in cereals and other grasses. J Exp Bot 60:2481–2492

    CAS  Google Scholar 

  • Comparot-Moss S, Kotting O, Stettler M, Edner C, Graf A, Weise SE, Streb S, Lue WL, MacLean D, Mahlow S, Ritte G, Steup M, Chen J, Zeeman SC, Smith AM (2010) A putative phosphatase, LSF1, is required for normal starch turnover in Arabidopsis leaves. Plant Physiol 152:685–697

    CAS  Google Scholar 

  • Crevillen P, Ballicora MA, Merida A, Preiss J, Romero JM (2003) The different large subunit isoforms of Arabidopsis thaliana ADP-glucose pyrophosphorylase confer distinct kinetic and regulatory properties to the heterotetrameric enzyme. J Biol Chem 278:28508–28515

    CAS  Google Scholar 

  • 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 mutation in Arabidopsis. Plant J 26:89–100

    CAS  Google Scholar 

  • Cuesta-Seijo JA, Nielsen MM, Marri L, Tanaka H, Beeren SR, Palcic MM (2013) Structure of starch synthase I from barley: insight into regulatory mechanisms of starch synthase activity. Acta Crystallogr D Biol Crystallogr 69:1013–1025

    CAS  Google Scholar 

  • Dauvillee D, Colleoni C, Mouille G, Morell MK, d’Hulst C, Wattebled F, Lienard L, Delvalle D, Ral JP, Myers AM, Ball SG (2001) Biochemical characterization of wild-type and mutant isoamylases of Chlamydomonas reinhardtii supports a function of the multimeric enzyme organization in amylopectin maturation. Plant Physiol 125:1723–1731

    CAS  Google Scholar 

  • Dauvillee D, Deschamps P, Ral JP, Plancke C, Putaux JL, Devassine J, Durand-Terrasson A, Devin A, Ball SG (2009) Genetic dissection of floridean starch synthesis in the cytosol of the model dinoflagellate Crypthecodinium cohnii. Proc Natl Acad Sci U S A 106:21126–21130

    CAS  Google Scholar 

  • Davies EJ, Tetlow IJ, Bowsher CG, Emes MJ (2003) Molecular and biochemical characterization of cytosolic phosphoglucomutase in wheat endosperm (Triticum aestivum L. cv. Axona). J Exp Bot 54:1351–1360

    CAS  Google Scholar 

  • Delatte T, Trevisan M, Parker ML, Zeeman SC (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 J 41:815–830

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Delcour JA, Bruneel C, Derde LJ, Gomand SV, Pareyt B, Putseys JA, Wilderjans E, Lamberts L (2010) Fate of starch in food processing: from raw materials to final food products. Annu Rev Food Sci Technol 1:87–111

    CAS  Google Scholar 

  • Delvalle D, Dumez S, Wattebled F, Roldan I, Planchot V, Berbezy P, Colonna P, Vyas D, Chatterjee M, Ball S, Merida A, d’Hulst C (2005) Soluble starch synthase I: a major determinant for the synthesis of amylopectin in Arabidopsis thaliana leaves. Plant J 43:398–412

    CAS  Google Scholar 

  • Denyer K, Dunlap F, Thorbjornsen T, Keeling P, Smith AM (1996) The major form of ADP-glucose pyrophosphorylase in maize endosperm is extra-plastidial. Plant Physiol 112:779–785

    CAS  Google Scholar 

  • Derelle E, Ferraz C, Rombauts S, Rouze P, Worden AZ, Robbens S, Partensky F, Degroeve S, Echeynie S, Cooke R, Saeys Y, Wuyts J, Jabbari K, Bowler C, Panaud O, Piegu B, Ball SG, Ral JP, Bouget FY, Piganeau G, De Baets B, Picard A, Delseny M, Demaille J, Van de Peer Y, Moreau H (2006) Genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features. Proc Natl Acad Sci U S A 103:11647–11652

    CAS  Google Scholar 

  • Deschamps P, Haferkamp I, d’Hulst C, Neuhaus HE, Ball SG (2008a) The relocation of starch metabolism to chloroplasts: when, why and how. Trends Plant Sci 13:574–582

    CAS  Google Scholar 

  • Deschamps P, Moreau H, Worden AZ, Dauvillee D, Ball SG (2008b) Early gene duplication within chloroplastida and its correspondence with relocation of starch metabolism to chloroplasts. Genetics 178:2373–2387

    CAS  Google Scholar 

  • Dian W, Jiang H, Wu P (2005) Evolution and expression analysis of starch synthase III and IV in rice. J Exp Bot 56:623–632

    CAS  Google Scholar 

  • Dickinson DB, Preiss J (1969) Presence of ADP-glucose pyrophosphorylase in shrunken-2 and brittle-2 mutants of maize endosperm. Plant Physiol 44:1058–1062

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Dismukes GC, Carrieri D, Bennette N, Ananyev GM, Posewitz MC (2008) Aquatic phototrophs: efficient alternatives to land-based crops for biofuels. Curr Opin Biotechnol 19:235–240

    CAS  Google Scholar 

  • Doyle EA, Lane AM, Sides JM, Mudgett MB, Monroe JD (2007) An alpha-amylase (At4g25000) in Arabidopsis leaves is secreted and induced by biotic and abiotic stress. Plant Cell Environ 30:388–398

    CAS  Google Scholar 

  • Dumez S, Wattebled F, Dauvillee D, Delvalle D, Planchot V, Ball SG, d’Hulst C (2006) Mutants of Arabidopsis lacking starch branching enzyme II substitute plastidial starch synthesis by cytoplasmic maltose accumulation. Plant Cell 18:2694–2709

    CAS  Google Scholar 

  • Edwards A, Fulton DC, Hylton C, Jobling SA, Gidley M, Rössner U, Martin C, Smith A (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

    CAS  Google Scholar 

  • Egli B, Kolling K, Kohler C, Zeeman SC, Streb S (2010) Loss of cytosolic phosphoglucomutase compromises gametophyte development in Arabidopsis. Plant Physiol 154:1659–1671

    CAS  Google Scholar 

  • Fernie AR, Tauberger E, Lytovchenko A, Roessner U, Willmitzer L, Trethewey RN (2002) Antisense repression of cytosolic phosphoglucomutase in potato (Solanum tuberosum) results in severe growth retardation, reduction in tuber number and altered carbon metabolism. Planta 214:510–520

    CAS  Google Scholar 

  • Fettke J, Albrecht T, Hejazi M, Mahlow S, Nakamura Y, Steup M (2010) Glucose 1-phosphate is efficiently taken up by potato (Solanum tuberosum) tuber parenchyma cells and converted to reserve starch granules. New Phytol 185:663–675

    CAS  Google Scholar 

  • Francisco P, Li J, Smith SM (2010) The gene encoding the catalytically inactive beta-amylase BAM4 involved in starch breakdown in Arabidopsis leaves is expressed preferentially in vascular tissues in source and sink organs. J Plant Physiol 167:890–895

    CAS  Google Scholar 

  • Fujita N, Kubo A, Francisco PB Jr, Nakakita M, Harada K, Minaka N, Nakamura Y (1999) Purification, characterization, and cDNA structure of isoamylase from developing endosperm of rice. Planta 208:283–293

    CAS  Google Scholar 

  • Fujita N, Yoshida M, Asakura N, Ohdan T, Miyao A, Hirochika H, Nakamura Y (2006) Function and characterization of starch synthase I using mutants in rice. Plant Physiol 140:1070–1084

    CAS  Google Scholar 

  • Fujita N, Yoshida M, Kondo T, Saito K, Utsumi Y, Tokunaga T, Nishi A, Satoh H, Park JH, Jane JL, Miyao A, Hirochika H, 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 Physiol 144:2009–2023

    CAS  Google Scholar 

  • 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) Beta-AMYLASE4, a noncatalytic protein required for starch breakdown, acts upstream of three active beta-amylases in Arabidopsis chloroplasts. Plant Cell 20:1040–1058

    CAS  Google Scholar 

  • Gamez-Arjona FM, Raynaud S, Ragel P, Merida A (2014) Starch synthase 4 is located in the thylakoid membrane and interacts with plastoglobule-associated proteins in Arabidopsis. Plant J 80:305–316

    CAS  Google Scholar 

  • Gao M, Wanat J, Stinard PS, James MG, Myers AM (1998) Characterization of dull1, a maize gene coding for a novel starch synthase. Plant Cell 10:399–412

    CAS  Google Scholar 

  • Garcia-Cantalejo J, Baladron V, Esteban PF, Santos MA, Bou G, Remacha MA, Revuelta JL, Ballesta JP, Jimenez A, del Rey F (1994) The complete sequence of an 18,002 bp segment of Saccharomyces cerevisiae chromosome XI contains the HBS1, MRP-L20 and PRP16 genes, and six new open reading frames. Yeast 10:231–245

    CAS  Google Scholar 

  • Geigenberger P (2011) Regulation of starch biosynthesis in response to a fluctuating environment. Plant Physiol 155:1566–1577

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Gibon Y, Pyl ET, Sulpice R, Lunn JE, Hohne M, Gunther M, Stitt M (2009) Adjustment of growth, starch turnover, protein content and central metabolism to a decrease of the carbon supply when Arabidopsis is grown in very short photoperiods. Plant Cell Environ 32:859–874

    CAS  Google Scholar 

  • Giroux MJ, Hannah LC (1994) ADP-glucose pyrophosphorylase in shrunken-2 and brittle-2 mutants of maize. Mol Gen Genet 243:400–408

    CAS  Google Scholar 

  • Giroux M, Smith-White B, Gilmore V, Hannah LC, Preiss J (1995) The large subunit of the embryo isoform of ADP glucose pyrophosphorylase from maize. Plant Physiol 108:1333–1334

    CAS  Google Scholar 

  • Glaring MA, Zygadlo A, Thorneycroft D, Schulz A, Smith SM, Blennow A, Baunsgaard L (2007) An extra-plastidial alpha-glucan, water dikinase from Arabidopsis phosphorylates amylopectin in vitro and is not necessary for transient starch degradation. J Exp Bot 58:3949–3960

    CAS  Google Scholar 

  • Glaring MA, Skryhan K, Kotting O, Zeeman SC, Blennow A (2012) Comprehensive survey of redox sensitive starch metabolising enzymes in Arabidopsis thaliana. Plant Physiol Biochem 58:89–97

    CAS  Google Scholar 

  • Gomez Casati DF, Aon MA, Iglesias AA (2000) Kinetic and structural analysis of the ultrasensitive behaviour of cyanobacterial ADP-glucose pyrophosphorylase. Biochem J 350(Pt 1):139–147

    CAS  Google Scholar 

  • Gomez-Casati DF, Iglesias AA (2002) ADP-glucose pyrophosphorylase from wheat endosperm. Purification and characterization of an enzyme with novel regulatory properties. Planta 214:428–434

    CAS  Google Scholar 

  • Gomez-Casati DF, Aon MA, Iglesias AA (1999) Ultrasensitive glycogen synthesis in Cyanobacteria. FEBS Lett 446:117–121

    CAS  Google Scholar 

  • Gomez-Casati DF, Martin M, Busi MV (2013) Polysaccharide-synthesizing glycosyltransferases and carbohydrate binding modules: the case of starch synthase III. Protein Pept Lett 20:856–863

    CAS  Google Scholar 

  • Graf A, Smith AM (2011) Starch and the clock: the dark side of plant productivity. Trends Plant Sci 16:169–175

    CAS  Google Scholar 

  • Graham LE, Cook ME, Busse JS (2000) The origin of plants: body plan changes contributing to a major evolutionary radiation. Proc Natl Acad Sci U S A 97:4535–4540

    CAS  Google Scholar 

  • Greene TW, Hannah LC (1998) Enhanced stability of maize endosperm ADP-glucose pyrophosphorylase is gained through mutants that alter subunit interactions. Proc Natl Acad Sci U S A 95:13342–13347

    CAS  Google Scholar 

  • Grennan AK (2006) Regulation of starch metabolism in Arabidopsis leaves. Plant Physiol 142:1343–1345

    CAS  Google Scholar 

  • Hannah LC, Shaw JR, Giroux MJ, Reyss A, Prioul JL, Bae JM, Lee JY (2001) Maize genes encoding the small subunit of ADP-glucose pyrophosphorylase. Plant Physiol 127:173–183

    CAS  Google Scholar 

  • Harmer SL, Hogenesch JB, Straume M, Chang HS, Han B, Zhu T, Wang X, Kreps JA, Kay SA (2000) Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science 290:2110–2113

    CAS  Google Scholar 

  • Harris BZ, Lim WA (2001) Mechanism and role of PDZ domains in signaling complex assembly. J Cell Sci 114:3219–3231

    CAS  Google Scholar 

  • Hejazi M, Fettke J, Kotting O, Zeeman SC, Steup M (2010) The Laforin-like dual-specificity phosphatase SEX4 from Arabidopsis hydrolyzes both C6- and C3-phosphate esters introduced by starch-related dikinases and thereby affects phase transition of alpha-glucans. Plant Physiol 152:711–722

    CAS  Google Scholar 

  • Hennen-Bierwagen TA, Myers AM (2013) Genomic specification of starch biosynthesis in maize endosperm. In: Becraft PW (ed) Seed genomics. Wiley, New York, pp 123–137

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • Hennen-Bierwagen TA, Lin Q, Grimaud F, Planchot V, Keeling PL, James MG, Myers AM (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 Physiol 149:1541–1559

    CAS  Google Scholar 

  • Henrissat B, Davies G (1997) Structural and sequence-based classification of glycoside hydrolases. Curr Opin Struct Biol 7:637–644

    CAS  Google Scholar 

  • Henrissat B, Davies GJ (2000) Glycoside hydrolases and glycosyltransferases. Families, modules, and implications for genomics. Plant Physiol 124:1515–1519

    CAS  Google Scholar 

  • Herzberg O, Chen CC, Kapadia G, McGuire M, Carroll LJ, Noh SJ, Dunaway-Mariano D (1996) Swiveling-domain mechanism for enzymatic phosphotransfer between remote reaction sites. Proc Natl Acad Sci U S A 93:2652–2657

    CAS  Google Scholar 

  • Hirano T, Takahashi Y, Fukuyama H, Michiyama H (2011) Identification of two plastid-targeted beta-amylases in rice. Plant Prod Sci 14:318–324

    CAS  Google Scholar 

  • Hirose T, Terao T (2004) A comprehensive expression analysis of the starch synthase gene family in rice (Oryza sativa L.). Planta 220:9–16

    CAS  Google Scholar 

  • Hirose T, Aoki N, Harada Y, Okamura M, Hashida Y, Ohsugi R, Akio M, Hirochika H, Terao T (2013) Disruption of a rice gene for alpha-glucan water dikinase, OsGWD1, leads to hyperaccumulation of starch in leaves but exhibits limited effects on growth. Front Plant Sci 4:147

    Google Scholar 

  • Huang N, Sutliff TD, Litts JC, Rodriguez RL (1990) Classification and characterization of the rice alpha-amylase multigene family. Plant Mol Biol 14:655–668

    CAS  Google Scholar 

  • Huang B, Hennen-Bierwagen TA, Myers AM (2014) Functions of multiple genes encoding ADP-glucose pyrophosphorylase subunits in maize endosperm, embryo, and leaf. Plant Physiol 164:596–611

    CAS  Google Scholar 

  • Hudson ER, Pan DA, James J, Lucocq JM, Hawley SA, Green KA, Baba O, Terashima T, Hardie DG (2003) A novel domain in AMP-activated protein kinase causes glycogen storage bodies similar to those seen in hereditary cardiac arrhythmias. Curr Biol 13:861–866

    CAS  Google Scholar 

  • Hummel I, Pantin F, Sulpice R, Piques M, Rolland G, Dauzat M, Christophe A, Pervent M, Bouteille M, Stitt M, Gibon Y, Muller B (2010) Arabidopsis plants acclimate to water deficit at low cost through changes of carbon usage: an integrated perspective using growth, metabolite, enzyme, and gene expression analysis. Plant Physiol 154:357–372

    CAS  Google Scholar 

  • Hussain H, Mant A, Seale R, Zeeman S, Hinchliffe E, Edwards A, Hylton C, Bornemann S, Smith AM, Martin C, Bustos R (2003) Three isoforms of isoamylase contribute different catalytic properties for the debranching of potato glucans. Plant Cell 15:133–149

    CAS  Google Scholar 

  • Hwang SK, Salamone PR, Okita TW (2005) Allosteric regulation of the higher plant ADP-glucose pyrophosphorylase is a product of synergy between the two subunits. FEBS Lett 579:983–990

    CAS  Google Scholar 

  • Hwang SK, Nishi A, Satoh H, Okita TW (2010) Rice endosperm-specific plastidial alpha-glucan phosphorylase is important for synthesis of short-chain malto-oligosaccharides. Arch Biochem Biophys 495:82–92

    CAS  Google Scholar 

  • Janecek S (1997) alpha-Amylase family: molecular biology and evolution. Prog Biophys Mol Biol 67:67–97

    CAS  Google Scholar 

  • Janecek S, Svensson B, Henrissat B (1997) Domain evolution in the alpha-amylase family. J Mol Evol 45:322–331

    CAS  Google Scholar 

  • Jeon JS, Ryoo N, Hahn TR, Walia H, Nakamura Y (2010) Starch biosynthesis in cereal endosperm. Plant Physiol Biochem 48:383–392

    CAS  Google Scholar 

  • Jespersen HM, MacGregor EA, Henrissat B, Sierks MR, Svensson B (1993) Starch- and glycogen-debranching and branching enzymes: prediction of structural features of the catalytic (beta/alpha)8-barrel domain and evolutionary relationship to other amylolytic enzymes. J Protein Chem 12:791–805

    CAS  Google Scholar 

  • Jiang H, Dian W, Liu F, Wu P (2004) Molecular cloning and expression analysis of three genes encoding starch synthase II in rice. Planta 218:1062–1070

    CAS  Google Scholar 

  • Jin X, Ballicora MA, Preiss J, Geiger JH (2005) Crystal structure of potato tuber ADP-glucose pyrophosphorylase. Embo J 24:694–704

    CAS  Google Scholar 

  • Kadziola A, Sogaard M, Svensson B, Haser R (1998) Molecular structure of a barley alpha-amylase-inhibitor complex: implications for starch binding and catalysis. J Mol Biol 278:205–217

    CAS  Google Scholar 

  • 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 44:730–743

    CAS  Google Scholar 

  • Katsuya Y, Mezaki Y, Kubota M, Matsuura Y (1998) Three-dimensional structure of Pseudomonas isoamylase at 2.2 A resolution. J Mol Biol 281:885–897

    CAS  Google Scholar 

  • Knight ME, Harn C, Lilley CE, Guan H, Singletary GW, MuForster C, Wasserman BP, Keeling PL (1998) Molecular cloning of starch synthase I from maize (W64) endosperm and expression in Escherichia coli. Plant J 14:613–622

    CAS  Google Scholar 

  • Kofler H, Hausler RE, Schulz B, Groner F, Flugge UI, Weber A (2000) Molecular characterisation of a new mutant allele of the plastid phosphoglucomutase in Arabidopsis, and complementation of the mutant with the wild-type cDNA. Mol Gen Genet 263:978–986

    CAS  Google Scholar 

  • Kotting 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

    Google Scholar 

  • Kotting O, Santelia D, Edner C, Eicke S, Marthaler T, Gentry MS, Comparot-Moss S, Chen J, Smith AM, Steup M, Ritte G, Zeeman SC (2009) STARCH-EXCESS4 is a laforin-like Phosphoglucan phosphatase required for starch degradation in Arabidopsis thaliana. Plant Cell 21:334–346

    CAS  Google Scholar 

  • Kotting O, Kossmann J, Zeeman SC, Lloyd JR (2010) Regulation of starch metabolism: the age of enlightenment? Curr Opin Plant Biol 13:321–329

    Google Scholar 

  • Kristensen M, Lok F, Planchot V, Svendsen I, Leah R, Svensson B (1999) Isolation and characterization of the gene encoding the starch debranching enzyme limit dextrinase from germinating barley. Biochim Biophys Acta 1431:538–546

    CAS  Google Scholar 

  • Kruger NJ, Ap Rees T (1983) Properties of a-glucan phosphorylase from pe chloroplasts. Phytochemistry 22:1891–1898

    CAS  Google Scholar 

  • Laby RJ, Kim D, Gibson SI (2001) The ram1 mutant of Arabidopsis exhibits severely decreased beta-amylase activity. Plant Physiol 127:1798–1807

    CAS  Google Scholar 

  • Lairson LL, Henrissat B, Davies GJ, Withers SG (2008) Glycosyltransferases: structures, functions, and mechanisms. Annu Rev Biochem 77:521–555

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Lee SK, Hwang SK, Han M, Eom JS, Kang HG, Han Y, Choi SB, Cho MH, Bhoo SH, An G, Hahn TR, Okita TW, Jeon JS (2007) Identification of the ADP-glucose pyrophosphorylase isoforms essential for starch synthesis in the leaf and seed endosperm of rice (Oryza sativa L.). Plant Mol Biol 65:531–546

    CAS  Google Scholar 

  • Leterrier M, Holappa LD, Broglie KE, Beckles DM (2008) Cloning, characterisation and comparative analysis of a starch synthase IV gene in wheat: functional and evolutionary implications. BMC Plant Biol 8:98

    Google Scholar 

  • Levasseur A, Drula E, Lombard V, Coutinho PM, Henrissat B (2013) Expansion of the enzymatic repertoire of the CAZy database to integrate auxiliary redox enzymes. Biotechnol Biofuels 6:41

    CAS  Google Scholar 

  • Levin S, Almo SC, Satir BH (1999) Functional diversity of the phosphoglucomutase superfamily: structural implications. Protein Eng 12:737–746

    CAS  Google Scholar 

  • Li Z, Chu X, Mouille G, Yan L, Kosar-Hashemi B, Hey S, Napier J, Shewry P, Clarke B, Appels R, Morell MK, Rahman S (1999) The localization and expression of the class II starch synthases of wheat. Plant Physiol 120:1147–1156

    CAS  Google Scholar 

  • Li Z, Mouille G, Kosar-Hashemi B, Rahman S, Clarke B, Gale KR, Appels R, Morell MK (2000) The structure and expression of the wheat starch synthase III gene. Motifs in the expressed gene define the lineage of the starch synthase III gene family. Plant Physiol 123:613–624

    CAS  Google Scholar 

  • Li J, Francisco P, Zhou W, Edner C, Steup M, Ritte G, Bond CS, Smith SM (2009) Catalytically-inactive beta-amylase BAM4 required for starch breakdown in Arabidopsis leaves is a starch-binding-protein. Arch Biochem Biophys 489:92–98

    CAS  Google Scholar 

  • Lin TP, Caspar T, Somerville C, Preiss J (1988a) Isolation and Characterization of a Starchless Mutant of Arabidopsis thaliana (L.) Heynh Lacking ADPglucose Pyrophosphorylase Activity. Plant Physiol 86:1131–1135

    CAS  Google Scholar 

  • Lin TP, Caspar T, Somerville CR, Preiss J (1988b) A starch deficient mutant of Arabidopsis thaliana with low ADPglucose pyrophosphorylase activity lacks one of the two subunits of the enzyme. Plant Physiol 88:1175–1181

    CAS  Google Scholar 

  • Lloyd JR, Kossmann J, Ritte G (2005) Leaf starch degradation comes out of the shadows. Trends Plant Sci 10:130–137

    CAS  Google Scholar 

  • Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B (2014) The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res 42:D490–495

    CAS  Google Scholar 

  • 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 16:473–477

    CAS  Google Scholar 

  • Lu Y, Sharkey TD (2006) The importance of maltose in transitory starch breakdown. Plant Cell Environ 29:353–366

    CAS  Google Scholar 

  • Lu Y, Gehan JP, Sharkey TD (2005) Daylength and circadian effects on starch degradation and maltose metabolism. Plant Physiol 138:2280–2291

    CAS  Google Scholar 

  • Lu Y, Steichen JM, Weise SE, Sharkey TD (2006a) Cellular and organ level localization of maltose in maltose-excess Arabidopsis mutants. Planta 224:935–943

    CAS  Google Scholar 

  • Lu Y, Steichen JM, Yao J, Sharkey TD (2006b) The role of cytosolic alpha-glucan phosphorylase in maltose metabolism and the comparison of amylomaltase in Arabidopsis and Escherichia coli. Plant Physiol 142:878–889

    CAS  Google Scholar 

  • Lutken H, Lloyd JR, Glaring MA, Baunsgaard L, Laursen KH, Haldrup A, Kossmann J, Blennow A (2010) Repression of both isoforms of disproportionating enzyme leads to higher malto-oligosaccharide content and reduced growth in potato. Planta 232:1127–1139

    Google Scholar 

  • Ma J, Jiang QT, Zhang XW, Lan XJ, Pu ZE, Wei YM, Liu C, Lu ZX, Zheng YL (2013) Structure and expression of barley starch phosphorylase genes. Planta (in press)

    Google Scholar 

  • Ma J, Jiang QT, Wei L, Yang Q, Zhang XW, Peng YY, Chen GY, Wei YM, Liu C, Zheng YL (2014) Conserved structure and varied expression reveal key roles of phosphoglucan phosphatase gene starch excess 4 in barley. Planta (in press)

    Google Scholar 

  • Maddelein ML, Libessart N, Bellanger F, Delrue B, D’Hulst C, Van den Koornhuyse N, Fontaine T, Wieruszeski JM, Decq A, 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. J Biol Chem 269:25150–25157

    CAS  Google Scholar 

  • Mahlow S, Hejazi M, Kuhnert F, Garz A, Brust H, Baumann O, Fettke J (2014) Phosphorylation of transitory starch by alpha-glucan, water dikinase during starch turnover affects the surface properties and morphology of starch granules. New Phytol 203:495–507

    CAS  Google Scholar 

  • Majzlova K, Pukajova Z, Janecek S (2013) Tracing the evolution of the alpha-amylase subfamily GH13_36 covering the amylolytic enzymes intermediate between oligo-1,6-glucosidases and neopullulanases. Carbohydr Res 367:48–57

    CAS  Google Scholar 

  • Manjunath S, Lee CH, VanWinkle P, Bailey-Serres J (1998) Molecular and biochemical characterization of cytosolic phosphoglucomutase in maize. Expression during development and in response to oxygen deprivation. Plant Physiol 117:997–1006

    CAS  Google Scholar 

  • Marchler-Bauer A, Bryant SH (2004) CD-Search: protein domain annotations on the fly. Nucleic Acids Res 32:W327–331

    CAS  Google Scholar 

  • Marchler-Bauer A, Anderson JB, Chitsaz F, Derbyshire MK, DeWeese-Scott C, Fong JH, Geer LY, Geer RC, Gonzales NR, Gwadz M, He S, Hurwitz DI, Jackson JD, Ke Z, Lanczycki CJ, Liebert CA, Liu C, Lu F, Lu S, Marchler GH, Mullokandov M, Song JS, Tasneem A, Thanki N, Yamashita RA, Zhang D, Zhang N, Bryant SH (2009) CDD: specific functional annotation with the conserved domain database. Nucleic Acids Res 37:D205–210

    CAS  Google Scholar 

  • Marchler-Bauer A, Lu S, Anderson JB, Chitsaz F, Derbyshire MK, DeWeese-Scott C, Fong JH, Geer LY, Geer RC, Gonzales NR, Gwadz M, Hurwitz DI, Jackson JD, Ke Z, Lanczycki CJ, Lu F, Marchler GH, Mullokandov M, Omelchenko MV, Robertson CL, Song JS, Thanki N, Yamashita RA, Zhang D, Zhang N, Zheng C, Bryant SH (2011) CDD: a conserved domain database for the functional annotation of proteins. Nucleic Acids Res 39:D225–229

    CAS  Google Scholar 

  • Marshall J, Sidebottom C, Debet M, Martin C, Smith AM, Edwards A (1996) Identification of the major starch synthase in the soluble fraction of potato tubers. Plant Cell 8:1121–1135

    CAS  Google Scholar 

  • McMaugh SJ, Thistleton JL, Anschaw E, Luo J, Konik-Rose C, Wang H, Huang M, Larroque O, Regina A, Jobling SA, Morell MK, Li Z (2014) Suppression of starch synthase I expression affects the granule morphology and granule size and fine structure of starch in wheat endosperm. J Exp Bot 65:2189–2201

    CAS  Google Scholar 

  • Meekins DA, Guo HF, Husodo S, Paasch BC, Bridges TM, Santelia D, Kotting O, Vander Kooi CW, Gentry MS (2013) Structure of the Arabidopsis glucan phosphatase like sex four2 reveals a unique mechanism for starch dephosphorylation. Plant Cell 25:2302–2314

    CAS  Google Scholar 

  • Meekins DA, Raththagala M, Husodo S, White CJ, Guo HF, Kotting O, Vander Kooi CW, Gentry MS (2014) Phosphoglucan-bound structure of starch phosphatase starch excess4 reveals the mechanism for C6 specificity. Proc Natl Acad Sci U S A 111:7272–7277

    CAS  Google Scholar 

  • Meyer RC, Steinfath M, Lisec J, Becher M, Witucka-Wall H, Torjek O, Fiehn O, Eckardt A, Willmitzer L, Selbig J, Altmann T (2007) The metabolic signature related to high plant growth rate in Arabidopsis thaliana. Proc Natl Acad Sci U S A 104:4759–4764

    CAS  Google Scholar 

  • Mikami B, Adachi M, Kage T, Sarikaya E, Nanmori T, Shinke R, Utsumi S (1999) Structure of raw starch-digesting Bacillus cereus beta-amylase complexed with maltose. Biochemistry 38:7050–7061

    CAS  Google Scholar 

  • Mikkelsen R, Mutenda KE, Mant A, Schurmann P, Blennow A (2005) Alpha-glucan, water dikinase (GWD): a plastidic enzyme with redox-regulated and coordinated catalytic activity and binding affinity. Proc Natl Acad Sci U S A 102:1785–1790

    CAS  Google Scholar 

  • Momma M, Fujimoto Z (2012) Interdomain disulfide bridge in the rice granule bound starch synthase I catalytic domain as elucidated by X-ray structure analysis. Biosci Biotechnol Biochem 76:1591–1595

    CAS  Google Scholar 

  • Morell MK, Konik-Rose C, Ahmed R, Li Z, Rahman S (2004) Synthesis of resistant starches in plants. J AOAC Int 87:740–748

    CAS  Google Scholar 

  • Moreno R, Poltl-Frank F, Stuber D, Matile H, Mutz M, Weiss NA, Pluschke G (2001) Rhoptry-associated protein 1-binding monoclonal antibody raised against a heterologous peptide sequence inhibits Plasmodium falciparum growth in vitro. Infect Immun 69:2558–2568

    CAS  Google Scholar 

  • Mu HH, Yu Y, Wasserman BP, Carman GM (2001) Purification and characterization of the maize amyloplast stromal 112-kDa starch phosphorylase. Arch Biochem Biophys 388:155–164

    CAS  Google Scholar 

  • Munoz FJ, Baroja-Fernandez E, Moran-Zorzano MT, Viale AM, Etxeberria E, Alonso-Casajus N, Pozueta-Romero J (2005) Sucrose synthase controls both intracellular ADP glucose levels and transitory starch biosynthesis in source leaves. Plant Cell Physiol 46:1366–1376

    CAS  Google Scholar 

  • Nakamura T, Yamamori M, Hirano H, Hidaka S, Nagamine T (1995) Production of waxy (amylose-free) wheats. Mol Gen Genet 248:253–259

    CAS  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, Kurano N (2005) Some cyanobacteria synthesize semi-amylopectin type alpha-polyglucans instead of glycogen. Plant Cell Physiol 46:539–545

    CAS  Google Scholar 

  • Nakamura Y, Ono M, Utsumi C, Steup M (2012) Functional interaction between plastidial starch phosphorylase and starch branching enzymes from rice during the synthesis of branched maltodextrins. Plant Cell Physiol 53:869–878

    CAS  Google Scholar 

  • Nashilevitz S, Melamed-Bessudo C, Aharoni A, Kossmann J, Wolf S, Levy AA (2009) The legwd mutant uncovers the role of starch phosphorylation in pollen development and germination in tomato. Plant J 57:1–13

    CAS  Google Scholar 

  • Neuhaus HE, Emes MJ (2000) Nonphotosynthetic metabolism in plastids. Annu Rev Plant Physiol Plant Mol Biol 51:111–140

    CAS  Google Scholar 

  • Nishi A, Nakamura Y, Tanaka N, Satoh H (2001) Biochemical and genetic analysis of the effects of amylose-extender mutation in rice endosperm. Plant Physiol 127:459–472

    CAS  Google Scholar 

  • Palopoli N, Busi MV, Fornasari MS, Gomez-Casati D, Ugalde R, Parisi G (2006) Starch-synthase III family encodes a tandem of three starch-binding domains. Proteins 65:27–31

    CAS  Google Scholar 

  • Patron NJ, Keeling PJ (2005) Common evolutionary origin of starch biosynthetic enzymes in green and red algae. J Phycol 41:1131–1141

    CAS  Google Scholar 

  • Patron NJ, Greber B, Fahy BF, Laurie DA, Parker ML, Denyer K (2004) The lys5 mutations of barley reveal the nature and importance of plastidial ADP-Glc transporters for starch synthesis in cereal endosperm. Plant Physiol 135:2088–2097

    CAS  Google Scholar 

  • Pazur JH, Okada S (1968) The isolation and mode of action of a bacterial glucanosyltransferase. J Biol Chem 243:4732–4738

    CAS  Google Scholar 

  • Plancke C, Colleoni C, Deschamps P, Dauvillee D, Nakamura Y, Haebel S, Ritte G, Steup M, Buleon A, Putaux JL, Dupeyre D, D’Hulst C, Ral JP, Loffelhardt W, Ball SG (2008) Pathway of cytosolic starch synthesis in the model glaucophyte Cyanophora paradoxa. Eukaryot Cell 7:247–257

    CAS  Google Scholar 

  • Preiss J, Sivak MN (1998) Biochemistry, molecular biology and regulation of starch synthesis. Genet Eng (NY) 20:177–223

    CAS  Google Scholar 

  • Preiss J, Ball K, Smith-White B, Iglesias A, Kakefuda G, Li L (1991) Starch biosynthesis and its regulation. Biochem Soc Trans 19:539–547

    CAS  Google Scholar 

  • Prioul JL, Jeannette E, Reyss A, Gregory N, Giroux M, Hannah LC, Causse M (1994) Expression of ADP-glucose pyrophosphorylase in maize (Zea mays L.) grain and source leaf during grain filling. Plant Physiol 104:179–187

    CAS  Google Scholar 

  • Raetz CR, Roderick SL (1995) A left-handed parallel beta helix in the structure of UDP-N-acetylglucosamine acyltransferase. Science 270:997–1000

    CAS  Google Scholar 

  • Ral JP, Bowerman AF, Li Z, Sirault X, Furbank R, Pritchard JR, Bloemsma M, Cavanagh CR, Howitt CA, Morell MK (2012) Down-regulation of Glucan, water-dikinase activity in wheat endosperm increases vegetative biomass and yield. Plant Biotechnol J 10:871–882

    CAS  Google Scholar 

  • Regina A, Kosar-Hashemi B, Li Z, Pedler A, Mukai Y, Yamamoto M, Gale K, Sharp PJ, Morell MK, 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 222:899–909

    CAS  Google Scholar 

  • Reinhold H, Soyk S, Simkova K, Hostettler C, Marafino J, Mainiero S, Vaughan CK, Monroe JD, Zeeman SC (2011) beta-amylase-like proteins function as transcription factors in Arabidopsis, controlling shoot growth and development. Plant Cell 23:1391–1403

    CAS  Google Scholar 

  • Ritte G, Lorberth R, Steup M (2000) Reversible binding of the starch-related R1 protein to the surface of transitory starch granules. Plant J 21:387–391

    CAS  Google Scholar 

  • Ritte G, Lloyd JR, Eckermann N, Rottmann A, Kossmann J, Steup M (2002) The starch-related R1 protein is an alpha -glucan, water dikinase. Proc Natl Acad Sci U S A 99:7166–7171

    CAS  Google Scholar 

  • Ritte G, Scharf A, Eckermann N, Haebel S, Steup M (2004) Phosphorylation of transitory starch is increased during degradation. Plant Physiol 135:2068–2077

    CAS  Google Scholar 

  • Ritte G, Heydenreich M, Mahlow S, Haebel S, Kotting 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

    CAS  Google Scholar 

  • Roach PJ (2002) Glycogen and its metabolism. Curr Mol Med 2:101–120

    CAS  Google Scholar 

  • Roldan I, Wattebled F, Mercedes Lucas M, Delvalle D, Planchot V, Jimenez S, Perez R, Ball S, D’Hulst C, Merida 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 J 49:492–504

    CAS  Google Scholar 

  • Sano Y (1984) Differential regulation of waxy gene expression in rice endosperm. Theor Appl Genet 68:467–473

    CAS  Google Scholar 

  • Santelia D, Zeeman SC (2011) Progress in Arabidopsis starch research and potential biotechnological applications. Curr Opin Biotechnol 22:271–280

    CAS  Google Scholar 

  • Santelia D, Kotting O, Seung D, Schubert M, Thalmann M, Bischof S, Meekins DA, Lutz A, Patron N, Gentry MS, Allain FH, Zeeman SC (2011) The phosphoglucan phosphatase like sex Four2 dephosphorylates starch at the C3-position in Arabidopsis. Plant Cell 23:4096–4111

    CAS  Google Scholar 

  • Satoh H, Shibahara K, Tokunaga T, Nishi A, Tasaki M, Hwang SK, Okita TW, Kaneko N, Fujita N, Yoshida M, Hosaka Y, Sato A, Utsumi Y, Ohdan T, Nakamura Y (2008) Mutation of the plastidial alpha-glucan phosphorylase gene in rice affects the synthesis and structure of starch in the endosperm. Plant Cell 20:1833–1849

    CAS  Google Scholar 

  • Sawada T, Nakamura Y, Ohdan T, Saitoh A, Francisco PB Jr, Suzuki E, Fujita N, Shimonaga T, Fujiwara S, Tsuzuki M, Colleoni C, Ball S (2014) Diversity of reaction characteristics of glucan branching enzymes and the fine structure of alpha-glucan from various sources. Arch Biochem Biophys 562:9–21

    CAS  Google Scholar 

  • Scheidig A, Frohlich A, Schulze S, Lloyd JR, Kossmann J (2002) Downregulation of a chloroplast-targeted beta-amylase leads to a starch-excess phenotype in leaves. Plant J 30:581–591

    CAS  Google Scholar 

  • Schindler I, Renz A, Schmid FX, Beck E (2001) Activation of spinach pullulanase by reduction results in a decrease in the number of isomeric forms. Biochim Biophys Acta 1548:175–186

    CAS  Google Scholar 

  • Schnable PS, Ware D, Fulton RS, Stein JC, Wei F, Pasternak S, Liang C, Zhang J, Fulton L, Graves TA, Minx P, Reily AD, Courtney L, Kruchowski SS, Tomlinson C, Strong C, Delehaunty K, Fronick C, Courtney B, Rock SM, Belter E, Du F, Kim K, Abbott RM, Cotton M, Levy A, Marchetto P, Ochoa K, Jackson SM, Gillam B, Chen W, Yan L, Higginbotham J, Cardenas M, Waligorski J, Applebaum E, Phelps L, Falcone J, Kanchi K, Thane T, Scimone A, Thane N, Henke J, Wang T, Ruppert J, Shah N, Rotter K, Hodges J, Ingenthron E, Cordes M, Kohlberg S, Sgro J, Delgado B, Mead K, Chinwalla A, Leonard S, Crouse K, Collura K, Kudrna D, Currie J, He R, Angelova A, Rajasekar S, Mueller T, Lomeli R, Scara G, Ko A, Delaney K, Wissotski M, Lopez G, Campos D, Braidotti M, Ashley E, Golser W, Kim H, Lee S, Lin J, Dujmic Z, Kim W, Talag J, Zuccolo A, Fan C, Sebastian A, Kramer M, Spiegel L, Nascimento L, Zutavern T, Miller B, Ambroise C, Muller S, Spooner W, Narechania A, Ren L, Wei S, Kumari S, Faga B, Levy MJ, McMahan L, Van Buren P, Vaughn MW, Ying K, Yeh CT, Emrich SJ, Jia Y, Kalyanaraman A, Hsia AP, Barbazuk WB, Baucom RS, Brutnell TP, Carpita NC, Chaparro C, Chia JM, Deragon JM, Estill JC, Fu Y, Jeddeloh JA, Han Y, Lee H, Li P, Lisch DR, Liu S, Liu Z, Nagel DH, McCann MC, SanMiguel P, Myers AM, Nettleton D, Nguyen J, Penning BW, Ponnala L, Schneider KL, Schwartz DC, Sharma A, Soderlund C, Springer NM, Sun Q, Wang H, Waterman M, Westerman R, Wolfgruber TK, Yang L, Yu Y, Zhang L, Zhou S, Zhu Q, Bennetzen JL, Dawe RK, Jiang J, Jiang N, Presting GG, Wessler SR, Aluru S, Martienssen RA, Clifton SW, McCombie WR, Wing RA, Wilson RK (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326:1112–1115

    CAS  Google Scholar 

  • Shimonaga T, Konishi M, Oyama Y, Fujiwara S, Satoh A, Fujita N, Colleoni C, Buleon A, Putaux JL, Ball SG, Yokoyama A, Hara Y, Nakamura Y, Tsuzuki M (2008) Variation in storage alpha-glucans of the Porphyridiales (Rhodophyta). Plant Cell Physiol 49:103–116

    CAS  Google Scholar 

  • Shoseyov O, Shani Z, Levy I (2006) Carbohydrate binding modules: biochemical properties and novel applications. Microbiol Mol Biol Rev 70:283–295

    CAS  Google Scholar 

  • Silver DM, Kotting O, Moorhead GB (2014) Phosphoglucan phosphatase function sheds light on starch degradation. Trends Plant Sci 19:471–478

    CAS  Google Scholar 

  • Skeffington AW, Graf A, Duxbury Z, Gruissem W, Smith AM (2014) Glucan, water dikinase exerts little control over starch degradation in arabidopsis leaves at night. Plant Physiol 165:866–879

    CAS  Google Scholar 

  • Slewinski TL, Ma Y, Baker RF, Huang M, Meeley R, Braun DM (2008) Determining the role of Tie-dyed1 in starch metabolism: epistasis analysis with a maize ADP-glucose pyrophosphorylase mutant lacking leaf starch. J Hered 99:661–666

    CAS  Google Scholar 

  • Smith AM, Stitt M (2007) Coordination of carbon supply and plant growth. Plant Cell Environ 30:1126–1149

    CAS  Google Scholar 

  • Smith AM, Zeeman SC (2006) Quantification of starch in plant tissues. Nat Protoc 1:1342–1345

    CAS  Google Scholar 

  • Smith AM, Denyer K, Martin C (1997) The Synthesis of the Starch Granule. Annu Rev Plant Physiol Plant Mol Biol 48:67–87

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Smith AM, Zeeman SC, Smith SM (2005) Starch degradation. Annu Rev Plant Biol 56:73–98

    CAS  Google Scholar 

  • Sokolov LN, Dominguez-Solis JR, Allary AL, Buchanan BB, Luan S (2006) A redox-regulated chloroplast protein phosphatase binds to starch diurnally and functions in its accumulation. Proc Natl Acad Sci U S A 103:9732–9737

    CAS  Google Scholar 

  • Soliman A, Ayele BT, Daayf F (2014) Biochemical and molecular characterization of barley plastidial ADP-glucose transporter (HvBT1). PLoS One 9:e98524

    Google Scholar 

  • Southall SM, Simpson PJ, Gilbert HJ, Williamson G, Williamson MP (1999) The starch-binding domain from glucoamylase disrupts the structure of starch. FEBS Lett 447:58–60

    CAS  Google Scholar 

  • Soyk S, Simkova K, Zurcher E, Luginbuhl L, Brand LH, Vaughan CK, Wanke D, Zeeman SC (2014) The enzyme-like domain of arabidopsis nuclear beta-amylases is critical for dna sequence recognition and transcriptional activation. Plant Cell 26:1746–1763

    CAS  Google Scholar 

  • Sparla F, Costa A, Lo Schiavo F, Pupillo P, Trost P (2006) Redox regulation of a novel plastid-targeted beta-amylase of Arabidopsis. Plant Physiol 141:840–850

    CAS  Google Scholar 

  • Spradlin J, Thoma JA (1970) Beta-amylase thiol groups. Possible regulator sites. J Biol Chem 245:117–127

    CAS  Google Scholar 

  • Stark DM, Timmerman KP, Barry GF, Preiss J, Kishore GM (1992) Regulation of the amount of starch in plant tissues by ADP glucose pyrophosphorylase. Science 258:287–292

    CAS  Google Scholar 

  • Stitt M, Zeeman SC (2012) Starch turnover: pathways, regulation and role in growth. Curr Opin Plant Biol 15:282–292

    CAS  Google Scholar 

  • Streb S, Zeeman S (2012) Starch metabolism in Arabidopsis. In: The Arabidopsis book. American Society of Plant Biologists, pe0160

    Google Scholar 

  • Streb S, Delatte T, Umhang M, Eicke S, Schorderet M, Reinhardt D, Zeeman SC (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 20:3448–3466

    CAS  Google Scholar 

  • Streb S, Egli B, Eicke S, Zeeman SC (2009) The debate on the pathway of starch synthesis: a closer look at low-starch mutants lacking plastidial phosphoglucomutase supports the chloroplast-localized pathway. Plant Physiol 151:1769–1772

    CAS  Google Scholar 

  • Streb S, Eicke S, Zeeman SC (2012) The simultaneous abolition of three starch hydrolases blocks transient starch breakdown in Arabidopsis. J Biol Chem 287:41745–41756

    CAS  Google Scholar 

  • Strobl S, Maskos K, Betz M, Wiegand G, Huber R, Gomis-Ruth FX, Glockshuber R (1998) Crystal structure of yellow meal worm alpha-amylase at 1.64 A resolution. J Mol Biol 278:617–628

    CAS  Google Scholar 

  • Sulpice R, Pyl ET, Ishihara H, Trenkamp S, Steinfath M, Witucka-Wall H, Gibon Y, Usadel B, Poree F, Piques MC, Von Korff M, Steinhauser MC, Keurentjes JJ, Guenther M, Hoehne M, Selbig J, Fernie AR, Altmann T, Stitt M (2009) Starch as a major integrator in the regulation of plant growth. Proc Natl Acad Sci U S A 106:10348–10353

    CAS  Google Scholar 

  • Szydlowski N, Ragel P, Raynaud S, Lucas MM, Roldan I, Montero M, Munoz FJ, Ovecka M, Bahaji A, Planchot V, Pozueta-Romero J, D’Hulst C, Merida A (2009) Starch granule initiation in Arabidopsis requires the presence of either class IV or class III starch synthases. Plant Cell 21:2443–2457

    CAS  Google Scholar 

  • Takaha T, Yanase M, Okada S, Smith SM (1993) Disproportionating enzyme (4-alpha-glucanotransferase; EC 2.4.1.25) of potato. Purification, molecular cloning, and potential role in starch metabolism. J Biol Chem 268:1391–1396

    CAS  Google Scholar 

  • Takashima Y, Senoura T, Yoshizaki T, Hamada S, Ito H, Matsui H (2007) Differential chain-length specificities of two isoamylase-type starch-debranching enzymes from developing seeds of kidney bean. Biosci Biotechnol Biochem 71:2308–2312

    CAS  Google Scholar 

  • Tanaka T, Antonio BA, Kikuchi S, Matsumoto T, Nagamura Y, Numa H, Sakai H, Wu J, Itoh T, Sasaki T, Aono R, Fujii Y, Habara T, Harada E, Kanno M, Kawahara Y, Kawashima H, Kubooka H, Matsuya A, Nakaoka H, Saichi N, Sanbonmatsu R, Sato Y, Shinso Y, Suzuki M, Takeda J, Tanino M, Todokoro F, Yamaguchi K, Yamamoto N, Yamasaki C, Imanishi T, Okido T, Tada M, Ikeo K, Tateno Y, Gojobori T, Lin YC, Wei FJ, Hsing YI, Zhao Q, Han B, Kramer MR, McCombie RW, Lonsdale D, O’Donovan CC, Whitfield EJ, Apweiler R, Koyanagi KO, Khurana JP, Raghuvanshi S, Singh NK, Tyagi AK, Haberer G, Fujisawa M, Hosokawa S, Ito Y, Ikawa H, Shibata M, Yamamoto M, Bruskiewich RM, Hoen DR, Bureau TE, Namiki N, Ohyanagi H, Sakai Y, Nobushima S, Sakata K, Barrero RA, Souvorov A, Smith-White B, Tatusova T, An S, An G, OO S, Fuks G, Messing J, Christie KR, Lieberherr D, Kim H, Zuccolo A, Wing RA, Nobuta K, Green PJ, Lu C, Meyers BC, Chaparro C, Piegu B, Panaud O, Echeverria M (2008) The rice annotation project database (RAP-DB): 2008 update. Nucleic Acids Res 36:D1028–1033

    CAS  Google Scholar 

  • Tauberger E, Fernie AR, Emmermann M, Renz A, Kossmann J, Willmitzer L, Trethewey RN (2000) Antisense inhibition of plastidial phosphoglucomutase provides compelling evidence that potato tuber amyloplasts import carbon from the cytosol in the form of glucose-6-phosphate. Plant J 23:43–53

    CAS  Google Scholar 

  • Teas HJ, Teas AN (1953) Heritable characters in maize: description and linkage of brittle endosperm-2. J Hered 44:156–158

    Google Scholar 

  • Tetlow IJ (2011) Starch biosynthesis in developing seeds. Seed Sci Res 21:5–32

    CAS  Google Scholar 

  • Tetlow IJ, Bowsher CG, Emes MJ (1996) Reconstitution of the hexose phosphate translocator from the envelope membranes of wheat endosperm amyloplasts. Biochem J 319(Pt 3):717–723

    CAS  Google Scholar 

  • Tetlow IJ, Davies EJ, Vardy KA, Bowsher CG, Burrell MM, Emes MJ (2003) Subcellular localization of ADPglucose pyrophosphorylase in developing wheat endosperm and analysis of the properties of a plastidial isoform. J Exp Bot 54:715–725

    CAS  Google Scholar 

  • Thorbjornsen T, Villand P, Kleczkowski LA, Olsen OA (1996) A single gene encodes two different transcripts for the ADP-glucose pyrophosphorylase small subunit from barley (Hordeum vulgare). Biochem J 313(Pt 1):149–154

    Google Scholar 

  • Tickle P, Burrell MM, Coates SA, Emes MJ, Tetlow IJ, Bowsher CG (2009) Characterization of plastidial starch phosphorylase in Triticum aestivum L. endosperm. J Plant Physiol 166:1465–1478

    CAS  Google Scholar 

  • Topping DL, Fukushima M, Bird AR (2003) Resistant starch as a prebiotic and synbiotic: state of the art. Proc Nutr Soc 62:171–176

    CAS  Google Scholar 

  • Tormo J, Lamed R, Chirino AJ, Morag E, Bayer EA, Shoham Y, Steitz TA (1996) Crystal structure of a bacterial family-III cellulose-binding domain: a general mechanism for attachment to cellulose. Embo J 15:5739–5751

    CAS  Google Scholar 

  • Tsai CY, Nelson OE (1966) Starch-deficient maize mutant lacking adenosine dephosphate glucose pyrophosphorylase activity. Science 151:341–343

    CAS  Google Scholar 

  • Tschoep H, Gibon Y, Carillo P, Armengaud P, Szecowka M, Nunes-Nesi A, Fernie AR, Koehl K, Stitt M (2009) Adjustment of growth and central metabolism to a mild but sustained nitrogen-limitation in Arabidopsis. Plant Cell Environ 32:300–318

    CAS  Google Scholar 

  • Umemoto T, Yano M, Satoh H, Shomura A, Nakamura Y (2002) Mapping of a gene responsible for the difference in amylopectin structure between japonica-type and indica-type rice varieties. Theor Appl Genet 104:1–8

    CAS  Google Scholar 

  • Usadel B, Blasing OE, Gibon Y, Retzlaff K, Hohne M, Gunther 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

    CAS  Google Scholar 

  • Utsumi Y, Nakamura Y (2006) Structural and enzymatic characterization of the isoamylase1 homo-oligomer and the isoamylase1-isoamylase2 hetero-oligomer from rice endosperm. Planta 225:75–87

    CAS  Google Scholar 

  • Valdez HA, Busi MV, Wayllace NZ, Parisi G, Ugalde RA, Gomez-Casati DF (2008) Role of the N-terminal starch-binding domains in the kinetic properties of starch synthase III from Arabidopsis thaliana. Biochemistry 47:3026–3032

    CAS  Google Scholar 

  • Valdez HA, Peralta DA, Wayllace NZ, Grisolía MJ, Gomez-Casati DF, Busi MV (2011) Preferential binding of SBD from Arabidopsis thaliana SSIII to polysaccharides: study of amino acid residues involved. Starch/Stärke 63:451–460

    CAS  Google Scholar 

  • Vander Kooi CW, Taylor AO, Pace RM, Meekins DA, Guo HF, Kim Y, Gentry MS (2010) Structural basis for the glucan phosphatase activity of starch excess 4. Proc Natl Acad Sci U S A 107:15379–15384

    CAS  Google Scholar 

  • Ventriglia T, Kuhn ML, Ruiz MT, Ribeiro-Pedro M, Valverde F, Ballicora MA, Preiss J, Romero JM (2008) Two Arabidopsis ADP-glucose pyrophosphorylase large subunits (APL1 and APL2) are catalytic. Plant Physiol 148:65–76

    CAS  Google Scholar 

  • Vester-Christensen MB, Abou Hachem M, Svensson B, Henriksen A (2010) Crystal structure of an essential enzyme in seed starch degradation: barley limit dextrinase in complex with cyclodextrins. J Mol Biol 403:739–750

    CAS  Google Scholar 

  • Vitha S, Zhao L, Sack FD (2000) Interaction of root gravitropism and phototropism in Arabidopsis wild-type and starchless mutants. Plant Physiol 122:453–462

    CAS  Google Scholar 

  • 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 122:255–264

    CAS  Google Scholar 

  • Wang Y, White P, Pollak L, Jane J (1993a) Amylopectin and intermediate materials in starches from mutant genotypes of the Oh43 inbred line. Cereal Chem 70:521–525

    CAS  Google Scholar 

  • Wang Y, White P, Pollak L, Jane J (1993b) Characterization of starch structures of 17 maize endosperm mutant genotype with Oh43 inbred line background. Cereal Chem 70:171–179

    CAS  Google Scholar 

  • Wang X, Xue L, Sun J, Zuo J (2010) The Arabidopsis BE1 gene, encoding a putative glycoside hydrolase localized in plastids, plays crucial roles during embryogenesis and carbohydrate metabolism. J Integr Plant Biol 52:273–288

    CAS  Google Scholar 

  • Wang K, Henry RJ, Gilbert RG (2014) Causal relations among starch biosynthesis structure and properties. Springer Sci Rev 1–19

    Google Scholar 

  • Wattebled F, Dong Y, Dumez S, Delvalle D, Planchot V, Berbezy P, Vyas D, Colonna P, Chatterjee M, Ball S, D’Hulst C (2005) Mutants of Arabidopsis lacking a chloroplastic isoamylase accumulate phytoglycogen and an abnormal form of amylopectin. Plant Physiol 138:184–195

    CAS  Google Scholar 

  • Wattebled F, Planchot V, Dong Y, Szydlowski N, Pontoire B, Devin A, Ball S, 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 Physiol 148:1309–1323

    CAS  Google Scholar 

  • Wayllace NZ, Valdez HA, Ugalde RA, Busi MV, Gomez-Casati DF (2010) The starch-binding 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 J 277:428–440

    CAS  Google Scholar 

  • Whan A, Dielen AS, Mieog J, Bowerman AF, Robinson HM, Byrne K, Colgrave M, Larkin PJ, Howitt CA, Morell MK, Ral JP (2014) Engineering alpha-amylase levels in wheat grain suggests a highly sophisticated level of carbohydrate regulation during development. J Exp Bot 65:5443–5457

    Google Scholar 

  • Wu C, Colleoni C, Myers AM, James MG (2002) Enzymatic properties and regulation of ZPU1, the maize pullulanase-type starch debranching enzyme. Arch Biochem Biophys 406:21–32

    CAS  Google Scholar 

  • Yamamori M, Fujita S, Hayakawa K, Matzuki JTY (2000) Genetic elimination of starch granule protein, SGP-1, of wheat generates an altered starch with apparent high amylose. Theor Appl Genet 101:21–29

    CAS  Google Scholar 

  • Yan H, Jiang H, Pan X, Li M, Chen Y, Wu G (2009a) The gene encoding starch synthase IIc exists in maize and wheat. Plant Sci 176:51–57

    CAS  Google Scholar 

  • Yan HB, Pan XX, Jiang HW, Wu GJ (2009b) Comparison of the starch synthesis genes between maize and rice: copies, chromosome location and expression divergence. Theor Appl Genet 119:815–825

    Google Scholar 

  • Yoo SH, Jane JL (2002) Structural and physical characteristics of waxy and other wheat starches. Carbohydr Polym 49:297–305

    CAS  Google Scholar 

  • Yu TS, Kofler H, Hausler RE, Hille D, Flugge UI, 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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) alpha-Amylase is not required for breakdown of transitory starch in Arabidopsis leaves. J Biol Chem 280:9773–9779

    CAS  Google Scholar 

  • Yun MS, Umemoto T, Kawagoe Y (2011) Rice debranching enzyme isoamylase3 facilitates starch metabolism and affects plastid morphogenesis. Plant Cell Physiol 52:1068–1082

    CAS  Google Scholar 

  • Zeeman SC, Northrop F, Smith AM, Rees T (1998) A starch-accumulating mutant of Arabidopsis thaliana deficient in a chloroplastic starch-hydrolysing enzyme. Plant J 15:357–365

    CAS  Google Scholar 

  • Zeeman SC, Thorneycroft D, Schupp N, Chapple A, Weck M, Dunstan H, Haldimann P, Bechtold N, Smith AM, Smith SM (2004) Plastidial alpha-glucan phosphorylase is not required for starch degradation in Arabidopsis leaves but has a role in the tolerance of abiotic stress. Plant Physiol 135:849–858

    CAS  Google Scholar 

  • Zeeman SC, Smith SM, Smith AM (2007) The diurnal metabolism of leaf starch. Biochem J 401:13–28

    CAS  Google Scholar 

  • Zeeman SC, Kossmann J, Smith AM (2010) Starch: its metabolism, evolution, and biotechnological modification in plants. Annu Rev Plant Biol 61:209–234

    CAS  Google Scholar 

  • Zhang X, Colleoni C, Ratushna V, Sirghie-Colleoni M, James MG, Myers AM (2004) Molecular characterization demonstrates that the Zea mays gene sugary2 codes for the starch synthase isoform SSIIa. Plant Mol Biol 54:865–879

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Zhang X, Szydlowski N, Delvalle D, D’Hulst C, James MG, Myers AM (2008) Overlapping functions of the starch synthases SSII and SSIII in amylopectin biosynthesis in Arabidopsis. BMC Plant Biol 8:96

    CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by grants from the Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET, PIP 00237 and 00134) and Agencia Nacional de Promoción Científica y Tecnológica (ANPCyT, PICT 2010 – 0543; PICT 2011 – 0982; PICT 2012–0981; and PICT 2013–2438). MVB, DFGC, MM, and JB are research members from CONICET. MJG and JBC are fellows from CONICET. NH is a fellow from ANPCyT.

Author information

Authors and Affiliations

  1. Molecular Biology and Plant Biotechnology Laboratory, Centro de Estudios Fotosintéticos y Bioquímicos (CEFOBI-CONICET), Universidad Nacional de Rosario, Suipacha 531, 2000, Rosario, Argentina

    Maria V. Busi, Diego F. Gomez-Casati, Mariana Martín, Julieta Barchiesi, Mauricio J. Grisolía, Nicolás Hedín & Julieta B. Carrillo

Authors
  1. Maria V. Busi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Diego F. Gomez-Casati
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mariana Martín
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Julieta Barchiesi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mauricio J. Grisolía
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Nicolás Hedín
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Julieta B. Carrillo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Maria V. Busi .

Editor information

Editors and Affiliations

  1. Botany Department, M.L.Sukhadia University, Udaipur, India

    Kishan Gopal Ramawat

  2. Groupe d’Etude des Substances Végétales à Activité Biologique, Université de Bordeaux, Institut des Sciences de la Vigne et du Vin, Villenave d'Ornon, France

    Jean-Michel Mérillon

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer International Publishing Switzerland

About this entry

Cite this entry

Busi, M.V. et al. (2015). Starch Metabolism in Green Plants. In: Ramawat, K., Mérillon, JM. (eds) Polysaccharides. Springer, Cham. https://doi.org/10.1007/978-3-319-16298-0_78

Download citation

Publish with us

Policies and ethics

Search

Navigation