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Biosynthesis of Reserve Starch

  • Chapter
Starch

Abstract

Plants have developed two distinct starch biosynthetic systems composed of over 30 kinds of enzymatic reaction network in photosynthetic and non-photosynthetic cells. Higher plants have also evolved a process in which cells can accumulate huge amounts of starch as granules inside the amyloplast of the reserve organs. Primarily the coordinated expression of several sets of distinct isozymes with specific enzymatic properties enables plant cells to synthesize starch with distinct fine structure and form the starch granules with specific semicrystalline structure, granular morphology, and physicochemical properties in plastids. This chapter overviews the current status of our understanding of metabolic regulation of starch biosynthesis in reserve organs by focusing on functions of individual isozymes examined by numerous in vivo and in vitro studies that have been performed to reveal how individual isozymes contribute to the synthesis of the reserve starch. The results raised the high possibility that at least some isozymes have multiple functions in starch biosynthesis under different conditions depending on the presence of various glucans and interaction/association with other enzymes. The features of starch biosynthetic process in plant tissues are also discussed with emphasis on the biochemical mechanism(s) underlying the coordinate actions among various enzymes.

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References

  • Abe N, Asai H, Yago H et al (2014) Relationships between starch synthase I and branching enzyme isozymes determined using double mutant rice lines. BMC Plant Biol 14:80

    PubMed Central  PubMed  Google Scholar 

  • Asai H, Abe N, Matsushima R, et al. (2014) Deficiencies in both starch synthase (SS) IIIa and branching enzyme IIb lead to a significant increase in amylose in SSIIa-inactive japonica rice seeds. J Exp Bot 65:5497–5507

    Google Scholar 

  • Baba T, Arai Y, Yamamoto T et al (1982) Some structural features of amylomaize starch. Phytochemistry 21:2291–2296

    CAS  Google Scholar 

  • Baba T, Nishihara M, Mizuno K et al (1993) Identification, cDNA cloning, and gene expression of soluble starch synthase in rice (Oryza sativa L.) immature seeds. Plant Physiol 103:565–573

    PubMed Central  CAS  PubMed  Google Scholar 

  • Båga M, Nair RB, Repellin A et al (2000) Isolation of a cDNA encoding a granule-bound 152-kilodalton starch-branching enzyme in wheat. Plant Physiol 124:253–263

    PubMed Central  PubMed  Google Scholar 

  • Ball S, Guan H-P, James MG et al (1996) From glycogen to amylopectin: a model for the biogenesis of the plant starch granule. Cell 86:349–352

    CAS  PubMed  Google Scholar 

  • Ball S, Colleoni C, Cenci U et al (2011) The evolution of glycogen and starch metabolism in eukaryotes gives molecular clues to understand the establishment of plastid endosymbiosis. J Exp Bot 62:1775–1801

    CAS  PubMed  Google Scholar 

  • Banks W, Greenwood CT, Muir DD (1974) Studies on starches of high amylose content. Part 17. A review of current concepts. Starch 26:289–300

    CAS  Google Scholar 

  • Beatty MK, Rahman A, Cao H et al (1999) Purification and molecular genetic characterization of ZPU1, a pullulanase-type starch-debranching enzyme from maize. Plant Physiol 119:255–265

    PubMed Central  CAS  PubMed  Google Scholar 

  • Bhattacharya D, Price DD, Chan CX et al (2013) Genome of the red alga Porphyridium purpureum. Nat Commun 4:2931

    Google Scholar 

  • Bhattacharyya MK, Smith AM, Ellis THN et al (1990) The wrinkled-seed character of pea described by Mendel is caused by a transposon-like insertion in a gene encoding starch-branching enzyme. Cell 60:115–122

    CAS  PubMed  Google Scholar 

  • Blauth SL, Yao Y, Klucinec JD et al (2001) Identification of Mutator insertional mutants of starch-branching enzyme 2a in corn. Plant Physiol 125:1396–1405

    PubMed Central  CAS  PubMed  Google Scholar 

  • Blauth SL, Kim KN, Klucinec J et al (2002) Identification of Mutator insertional mutants of starch-branching enzyme 1 (sbe1) in Zea mays L. Plant Mol Biol 48:287–297

    CAS  PubMed  Google Scholar 

  • Borovsky D, Smith EC, Whelan WJ et al (1979) The mechanism of Q-enzyme action and its influence on the structure of amylopectin. Arch Biochem Biophys 198:627–631

    CAS  PubMed  Google Scholar 

  • Boyer CD, Preiss J (1978) Multiple forms of (1–4)-α-D-glucan, (1–4)-α-D-glucan-6-glycosyl transferase from developing Zea mays L. kernels. Carbohydr Res 61:321–334

    CAS  Google Scholar 

  • Boyer CD, Preiss J (1979) Properties of citrate-stimulated starch synthesis catalyzed by starch synthase I of developing maize kernels. Plant Physiol 64:1039–1042

    PubMed Central  CAS  PubMed  Google Scholar 

  • Brust H, Lehman T, D’Hulst C et al (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

    PubMed Central  PubMed  Google Scholar 

  • Burton R, Bewley JD, Smith AM et al (1995) Starch branching enzymes belonging to distinct enzyme families are differentially expressed during pea embryo development. Plant J 7:3–15

    CAS  PubMed  Google Scholar 

  • Burton RA, Jenner H, Carrangis L et al (2002) Starch granule initiation and growth are altered in barley mutants that lack isoamylase activity. Plant J 31:97–112

    CAS  PubMed  Google Scholar 

  • Bustos R, Fahy B, Hylton CM et al (2004) Starch granule initiation is controlled by a heteromultimeric isoamylase in potato tubers. Proc Natl Acad Sci U S A 101:2215–2220

    PubMed Central  CAS  PubMed  Google Scholar 

  • Butardo VM, Fitzgerald MA, Bird AR et al (2011) Impact of down-regulation of starch branching enzyme IIb in rice by artificial microRNA- and hairpin RNA-mediated RNA silencing. J Exp Bot 62:4927–4941

    PubMed Central  CAS  PubMed  Google Scholar 

  • Cao H, Imparl-Radosevich J, Guan H et al (1999) Identification of the soluble starch synthase activities of maize endosperm. Plant Physiol 120:205–215

    PubMed Central  CAS  PubMed  Google Scholar 

  • Carciofi M, Blennow A, Jensen SL et al (2012) Concerted suppression of all starch branching enzyme genes in barley produces amylase-only starch granules. BMC Plant Biol 12:223

    PubMed Central  CAS  PubMed  Google Scholar 

  • Cenci U, Chabi M, Ducatez M et al (2013) Convergent evolution of polysaccharide debranching defines a common mechanism for starch accumulation in cyanobacteria and plants. Plant Cell 25:3961–3975

    PubMed Central  CAS  PubMed  Google Scholar 

  • Chaen K, Noguchi J, Omori T (2012) Crystal structure of the rice branching enzyme I (BEI) in complex with maltopentaose. Biochem Biophys Res Commun 424:508–511

    CAS  PubMed  Google Scholar 

  • Colleoni C, Suzuki E (2012) Storage polysaccharide metabolism in cyanobacteria. In: Tetlow I (ed) Starch: origins, structure and metabolism, vol 5, Essential reviews in experimental biology. The Society for Experimental Biology, London, pp 217–253

    Google Scholar 

  • Colleoni C, Dauvillee D, Mouille G et al (1999a) Genetic and biochemical evidence for the involvement of α-1,4 glucanotransferases in amylopectin synthesis. Plant Physiol 120:993–1004

    PubMed Central  CAS  PubMed  Google Scholar 

  • Colleoni C, Dauvillee D, Mouille G et al (1999b) Biochemical characterization of the Chlamydomonas reinhardtii α-1,4 glucanotransferase supports a direct function in amylopectin biosynthesis. Plant Physiol 120:1005–1014

    PubMed Central  CAS  PubMed  Google Scholar 

  • Collins GN, Kempton JF (1911) Inheritance of waxy endosperm in hybrids of Chinese maize. Proc IV Int Genet Congr (Paris) 347–356

    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  PubMed  Google Scholar 

  • Coppin A, Varre JS, Lienard L et al (2005) Evolution of plant-like crystalline storage polysaccharide in the protozoan parasite Toxoplasma gondii argues for a red alga ancestry. J Mol Evol 60:257–267

    CAS  PubMed  Google Scholar 

  • Craig J, Lloyd JR, Tomlinson K et al (1998) Mutations in the gene encoding starch synthase II profoundly alter amylopectin structure in pea embryos. Plant Cell 10:413–426

    PubMed Central  CAS  PubMed  Google Scholar 

  • Critchley JH, Zeeman S, Takaha T et al (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  PubMed  Google Scholar 

  • Crumpton-Taylor M, Pike M, Lu K et al (2013) Starch synthase 4 is essential for coordination of starch granule formation with chloroplast division during Arabidopsis leaf expansion. New Phytol 200:1064–1075

    PubMed Central  CAS  PubMed  Google Scholar 

  • Cuesta-Seijo JA, Nielsen MM, Marri L et al (2013) Structure of starch synthase I from barley: insight into regulatory mechanisms of starch synthase activity. Acta Crystallogr D Biol Crystallogr D69:1013–1025

    Google Scholar 

  • D’Hulst C, Merida A (2012) Once upon a time: inception of the understanding of starch initiation in plants. In: Tetlow I (ed) Starch: origins, structure and metabolism. , vol 5, Essential reviews in experimental biology. The Society for Experimental Biology, London, pp 55–76

    Google Scholar 

  • Damager I, Denyer K, Motawia MS et al (2001) The action of starch synthase II on 6’-α-maltotoriosyl-maltohexaose comprising the branch point amylopectin. Eur J Biochem 268:4878–4884

    CAS  PubMed  Google Scholar 

  • Dang PL, Boyer CD (1988) Maize leaf and kernel starch synthases and starch branching enzymes. Phytochemistry 27:1255–1259

    CAS  Google Scholar 

  • Dauvillée D, Mestre V, Colleoni C et al (2000) The debranching enzyme complex missing in glycogen accumulating mutants of Chlamydomonas reinhardtii displays an isoamylase-type specificity. Plant Sci 157:145–156

    PubMed  Google Scholar 

  • Dauvillée D, Colleoni C, Mouille G et al (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

    PubMed Central  PubMed  Google Scholar 

  • Dauvillée D, Kinderf IS, Li Z et al (2005) Role of the Escherichia coli glgX gene in glycogen metabolism. J Bacteriol 187:1465–1473

    PubMed Central  PubMed  Google Scholar 

  • Dauvillée D, Chochois V, Steup M et al (2006) Plastidial phosphorylase is required for normal starch synthesis in Chlamydomonas reinhardtii. Plant J 48:274–285

    PubMed  Google Scholar 

  • Davis JH, Kramer HH, Whistler RL (1955) Expression of the gene du in the endosperm of maize. Agron J 47:232–235

    Google Scholar 

  • Dellate T, Trevisan M, Parker ML et al (2005) Arabidopsis mutants Atisa1 and Atisa2 have identical phenotypes and lack the multimeric isoamylase, which influences the branch point distribution of amylopectin during starch synthesis. Plant J 41:815–830

    Google Scholar 

  • Delrue B, Fontaine T, Routier F et al (1992) Waxy Chlamydomonas reinhardtii: monocellular algal mutants defective in amylose biosynthesis and granule-bound starch synthase activity accumulate a structurally modified amylopectin. J Bacteriol 174:3612–3620

    PubMed Central  CAS  PubMed  Google Scholar 

  • Delvallé D, Dumez S, Wattebled F et al (2005) Soluble starch synthase I: a major determinant for the synthesis of amylopectin in Arabidopsis thaliana leaves. Plant J 43:398–412

    PubMed  Google Scholar 

  • Denyer K, Dunlap F, Thornbjørnsen T et al (1996) The major form of ADP-glucose pyrophosphorylase in maize (Zea mays L.) endosperm is extra-plastidial. Plant Physiol 112:779–785

    PubMed Central  CAS  PubMed  Google Scholar 

  • Denyer K, Waite D, Edwards A et al (1999a) Interaction with amylopectin influences the ability of granule-bound starch synthase I to elongate malto-oligosaccharides. Biochem J 342:647–653

    PubMed Central  CAS  PubMed  Google Scholar 

  • Denyer K, Waite D, Motawia S et al (1999b) Granule-bound starch synthase I in isolated starch granules elongates malto-oligosaccharides processively. Biochem J 340:183–191

    PubMed Central  CAS  PubMed  Google Scholar 

  • Deschamps P, Colleoni C, Nakamura Y et al (2008) Metabolic symbiosis and the birth of the plant kingdom. Mol Biol Evol 25:536–548

    CAS  PubMed  Google Scholar 

  • Dian W, Jiang H, Chen Q et al (2003) Cloning and characterization of the granule-bound starch synthase II gene in rice: gene expression is regulated by the nitrogen level, sugar and circadian rhythm. Planta 218:261–268

    CAS  PubMed  Google Scholar 

  • Dinges JR, Colleoni C, Myers AM et al (2001) Molecular structure of three mutations at the maize sugary1 locus and their allele-specific phenotypic effects. Plant Physiol 125:1406–1418

    PubMed Central  CAS  PubMed  Google Scholar 

  • Dinges JR, Colleoni C, James MG et al (2003) Mutational analysis of the pullulanase-type debranching enzyme of maize indicates multiple functions in starch metabolism. Plant Cell 15:666–680

    PubMed Central  CAS  PubMed  Google Scholar 

  • Edwards A, Borthakur A, Bornemann S et al (1999a) Specificity of starch synthase isoforms from potato. Eur J Biochem 266:724–736

    CAS  PubMed  Google Scholar 

  • Edwards A, Fulton DC, Hylton CM et al (1999b) 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 

  • Emes MJ, Tetlow IJ (2012) The role of heteromeric protein complexes in starch synthesis. In: Tetlow I (ed) Starch: origins, structure and metabolism, vol 5, Essential reviews in experimental biology. The Society for Experimental Biology, London, pp 255–278

    Google Scholar 

  • Facon M, Lin Q, Azzaz AM et al (2013) Distinct functional properties of isoamylase-type starch debranching enzymes in monocot and dicot leaves. Plant Physiol 163:1363–1375

    PubMed Central  CAS  PubMed  Google Scholar 

  • Fettke J, Albrecht T, Hejazi M et al (2010a) 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  PubMed  Google Scholar 

  • Fettke J, Malinova I, Albrecht T et al (2010b) Glucose-1-phosphate transport into protoplasts and chloroplasts from leaves of Arabidopsis. Plant Physiol 155:1723–1734

    PubMed Central  PubMed  Google Scholar 

  • Fettke J, Leifels L, Brust H et al (2012) Two carbon fluxes to reserve starch in potato (Solanum tuberosum L.) tuber cells are closely interconnected but differently modulated by temperature. J Exp Bot 63:3011–3029

    PubMed Central  CAS  PubMed  Google Scholar 

  • Fisher DK, Gao M, Kim K (1996) Allelic analysis of the maize amylose-extender locus suggests that independent genes encode starch-branching enzymes IIa and IIb. Plant Physiol 110:611–619

    PubMed Central  CAS  PubMed  Google Scholar 

  • Fontaine T, D-Hulst C, Maddelein ML et al (1993) Toward an understanding of the biogenesis of the starch granules. Evidence that Chlamydomonas starch synthase II controls the synthesis of intermediate size glucans of amylopectin. J Biol Chem 268:16223–16230

    CAS  PubMed  Google Scholar 

  • Fujita N, Nakamura Y (2012) Distinct and overlapping functions of starch synthase isoforms. In: Tetlow I (ed) Starch: origins, structure and metabolism, vol 5, Essential reviews in experimental biology. The Society for Experimental Biology, London, pp 115–140

    Google Scholar 

  • Fujita N, Taira T (1998) A 56 kDa protein is a novel granule-bound starch synthase existing in the pericarps, aleurone layers, and embryos of immature seeds of diploid wheat (Triticum monococcum L.). Planta 207:125–132

    CAS  PubMed  Google Scholar 

  • Fujita N, Kubo A, Francisco PB Jr et al (1999) Purification, characterization, and cDNA structure of isoamylase from developing endosperm of rice. Planta 208:283–293

    CAS  PubMed  Google Scholar 

  • Fujita N, Kubo A, Suh DS et al (2003) Antisense inhibition of isoamylase alters the structure of amylopectin and the physiological properties of starch in rice endosperm. Plant Cell Physiol 44:607–618

    CAS  PubMed  Google Scholar 

  • Fujita N, Yoshida M, Asakura N et al (2006) Function and characterization of starch synthase I using mutants in rice. Plant Physiol 140:1070–1084

    PubMed Central  CAS  PubMed  Google Scholar 

  • Fujita N, Yoshida M, Kondo T et al (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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Fujita N, Toyosawa Y, Utsumi Y et al (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. J Exp Bot 60:1009–1023

    PubMed Central  CAS  PubMed  Google Scholar 

  • Gámez-Arjona FM, Li J, Raynaud S et al (2011) Enhancing the expression of starch synthase class IV results in increased levels of both transitory and long-term storage starch. Plant Biotechnol J 9:1049–1060

    PubMed  Google Scholar 

  • Gao M, Fisher DK, Kim K et al (1996) Evolutionary conservation and expression patterns of maize starch branching enzyme I and IIb genes suggest isoform specialization. Plant Mol Biol 30:11223–11232

    Google Scholar 

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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Gidley MJ, Bulpin PV (1987) Crystallization of malto-oligosaccharides as models of the crystalline forms of starch. Carbohydr Res 161:291–300

    CAS  Google Scholar 

  • Grimaud F, Rogniaux H, James MG et al (2008) Proteome and phosphoproteome analysis of starch granule-associated proteins from normal maize and mutants affected in starch biosynthesis. J Exp Bot 59:3395–3406

    PubMed Central  CAS  PubMed  Google Scholar 

  • Guan H, Preiss J (1993) Differentiation of the properties of the branching isozymes from maize (Zea mays). Plant Physiol 102:1269–1273

    PubMed Central  CAS  PubMed  Google Scholar 

  • Guan H, Li P, Imparl-Radosevich J et al (1997) Comparing the properties of Escherichia coli branching enzyme and maize branching enzyme. Arch Biochem Biophys 342:92–98

    CAS  PubMed  Google Scholar 

  • Hamada S, Nozaki K, Ito H et al (2001) Two starch-branching-enzyme isoforms occur in different fractions of developing seeds of kidney bean. Biochem J 359:23–34

    PubMed Central  CAS  PubMed  Google Scholar 

  • Hamada S, Ito H, Hiraga S et al (2002) Differential characteristics and subcellular localization of two starch-branching enzyme isoforms encoded by a single gene in Phaseolus vulgaris L. J Biol Chem 277:16538–16546

    CAS  PubMed  Google Scholar 

  • Han Y, Bendik E, Sun F et al (2007a) Genomic isolation of genes encoding starch branching enzyme II (SBEII) in apple: Towards characterization of evolutionary disparity in SbeII genes between monocots and eudicots. Planta 226:1265–1276

    CAS  PubMed  Google Scholar 

  • Han Y, Sun F, Rosales-Mendoza S et al (2007b) Three orthologs in rice, Arabidopsis, and Populus encoding starch branching enzymes (SBEs) are different from other SBE gene families in plants. Gene 401:123–130

    CAS  PubMed  Google Scholar 

  • Hanashiro I, Matsunaga J, Egashira T et al (2005) Structural characterization of long unit-chains of amylopectin. J Appl Glycosci 52:233–237

    CAS  Google Scholar 

  • Hanashiro I, Ito K, Kuratomi Y et al (2008) Granule-bound starch synthase I is responsible for biosynthesis of extra-long unit chains of amylopectin in rice. Plant Cell Physiol 49:925–933

    CAS  PubMed  Google Scholar 

  • Hanashiro I, Sakaguchi I, Yamashita H (2013) Branched structures of rice amylose examined by differential fluorescence detection of side-chain distribution. J Appl Glycosci 60:79–85

    CAS  Google Scholar 

  • Hawker JS, Ozbun JL, Preiss J (1972) Unprimed starch synthesis by soluble ADPglucose-starch glucosyltransferase from potato tubers. Phytochemistry 11:1287–1293

    CAS  Google Scholar 

  • Hawker JS, Ozbun JL, Ozaki H et al (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-glucosyl transferase in synthesis of branched α-glucan. Arch Biochem Biophys 160:530–551

    CAS  PubMed  Google Scholar 

  • Hedman KD, Boyer CD (1982) Gene dosage at the amylose-extender locus of maize: effects on the levels of starch branching enzymes. Biochem Genet 20:483–492

    CAS  PubMed  Google Scholar 

  • Hennen-Bierwagen TA, Liu F, Marsh RS et al (2008) Starch biosynthetic enzymes from developing Zea mays endosperm associate in multisubunit complexes. Plant Physiol 146:1892–1908

    PubMed Central  CAS  PubMed  Google Scholar 

  • Hennen-Bierwagen TA, Lin Q, Grimaud F et al (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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Hennen-Bierwagen TA, James MG, Myers AM (2012) Involvement of debranching enzymes in starch biosynthesis. In: Tetlow I (ed) Starch: origins, structure and metabolism, vol 5, Essential reviews in experimental biology. The Society for Experimental Biology, London, pp 179–215

    Google Scholar 

  • Hirabaru C, Izumo A, Fujiwara S et al (2010) The primitive rhodophyte Cyanidioschyzon merolae contains a semiamylopectin-type, but not an amylose-type α-glucan. Plant Cell Physiol 51:682–693

    CAS  PubMed  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  PubMed  Google Scholar 

  • Hizukuri S (1986) Polymodal distribution of the chain lengths of amylopectins, and its significance. Carbohydr Res 147:342–347

    CAS  Google Scholar 

  • Hizukuri S (1996) Starch: analytical aspects. In: Eliasson AC (ed) Carbohydrates in food starch. Essential reviews in experimental biology, vol 5. Marcel Dekker Inc, New York/Basel/Hong Kong; The Society for Experimental Biology, London, pp 115–140

    Google Scholar 

  • Hizukuri S, Takeda Y, Yasuda M et al (1981) Multi-branched nature of amylose and the action of debranching enzymes. Carbohydr Res 94:205–213

    CAS  Google Scholar 

  • Horibata T, Nakamoto M, Fuwa H et al (2004) Structural and physicochemical characteristics of endosperm starches of rice cultivars recently bred in Japan. J Appl Glycosci 51:303–313

    CAS  Google Scholar 

  • Hussain H, Mant A, Seale R et al (2003) Three isoforms of isoamylase contribute different catalytic properties for the debranching of potato glucans. Plant Cell 15:133–149

    PubMed Central  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Ikeno S (1914) Über die Bestäubung und die Bastardierung von Reis. Z Pflanzenzucht 2:495–503

    Google Scholar 

  • Imparl-Radosevich JM, Gameon JR, McKean A et al (2003) Understanding catalytic properties and functions of maize starch synthase isozymes. J Appl Glycosci 50:177–182

    CAS  Google Scholar 

  • Inouchi N, Hibiu H, Li T et al (2005) Structure and properties of endosperm starches from cultivated rice of Asia and other countries. J Appl Glycosci 52:239–246

    CAS  Google Scholar 

  • Ishizaki Y, Taniguchi H, Maruyama Y et al (1983) Debranching enzymes of potato tubers (Solanum tuberosum L.). I. Purification and some properties of potato isoamylase. Agric Biol Chem 47:771–779

    CAS  Google Scholar 

  • Jacobsen E, Hovenkamp-Hermelink JHM, Krijgheld HT et al (1989) Phenotypic and genotypic characterization of an amylase-free starch mutant of the potato. Euphytica 44:43–48

    Google Scholar 

  • James MG, Robertson DS, Myers AM (1995) Characterization of the maize gene sugary1, a determinant of starch composition in kernels. Plant Cell 7:417–429

    PubMed Central  CAS  PubMed  Google Scholar 

  • Janeček Š, Svensson B, MacGregor EA (2011) Structural and evolutional aspects of two families of non-catalytic domains present in starch and glycogen binding proteins from microbes, plants and animals. Enzym Microb Technol 49:429–440

    Google Scholar 

  • Jenkins PJ, Cameron RE, Donald AM (1993) A universal feature in the starch granules from different botanical sources. Starch 45:417–420

    CAS  Google Scholar 

  • Kainuma K, French D (1972) Naegeli amylodextrin and its relationship to starch granule structures. III Role of water in crystallization of B-starch. Biopolymers 11:2241–2250

    CAS  Google Scholar 

  • Katayama K, Komae K, Kohyama K et al (2002) New sweet potato line having low gelatinization temperature and altered starch structure. Starch 54:51–57

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Kawagoe Y (2013) The characteristic polyhedral, sharp-edged shape of compound-type starch granules in rice endosperm is achieved via the septum-like structure of the amyloplast. J Appl Glycosci 60:29–36

    CAS  Google Scholar 

  • Kitahara K, Fukunaga S, Katayama K et al (2005) Physicochemical properties of sweet potato starches with different gelatinization temperatures. Starch 57:473–479

    CAS  Google Scholar 

  • Klucinec JD, Thompson DB (2002) Structure of amylopectins from ae-containing maize starches. Cereal Chem 79:19–23

    CAS  Google Scholar 

  • Kubo A, Fujita N, Harada K et al (1999) The starch-debranching enzymes isoamylase and pullulanase are both involved in amylopectin biosynthesis in rice endosperm. Plant Physiol 121:399–409

    PubMed Central  CAS  PubMed  Google Scholar 

  • Kubo A, Rahman S, Utsumi Y et al (2005) Complementation of sugary-1 phenotype in rice endosperm with the wheat Isoamylase1 gene supports a direct role for isoamylase1 in amylopectin biosynthesis. Plant Physiol 137:43–56

    PubMed Central  CAS  PubMed  Google Scholar 

  • Kubo A, Colleoni C, Dinges JR et al (2010) Functions of heteromeric and homomeric isoamylase-type starch debranching enzymes in developing maize endosperm. Plant Physiol 153:956–969

    PubMed Central  CAS  PubMed  Google Scholar 

  • Larsson CT, Hofvander P, Khoshnoodi J et al (1996) Three isoforms of starch synthase and two isoforms of branching enzyme are present in potato tuber starch. Plant Sci 117:9–16

    CAS  Google Scholar 

  • Lee EYC, Whelan WJ (1971) Glycogen and starch debranching enzymes. In: Boyer PD (ed) The enzymes, vol 5. Academic, New York, pp 191–234

    Google Scholar 

  • Leterrier M, Holappa L, Broglie KE et al (2008) Cloning, characterization and comparative analysis of a starch synthase IV gene in wheat: functional and evolutional implications. BMC Plant Biol 8:98

    PubMed Central  PubMed  Google Scholar 

  • Li Z, Mouille G, Kosar-Hashemi B et al (2000) The structure and expression of the wheat starch synthase III gene: motif in the expressed gene define the lineage of the starch synthase III gene family. Plant Physiol 123:613–624

    PubMed Central  CAS  PubMed  Google Scholar 

  • Li L, Jiang H, Campbell M, et al. (2008) Characterization of maize amylose-extender (ae) mutant starches. Part I: Relationship between resistant starch contents and molecular structures. Carbohydr Polym 74:396–404

    Google Scholar 

  • Li Z, Li D, Du X et al (2011) The barley amo1 locus is tightly linked to the starch synthase IIIa gene and negatively regulates expression of granule-bound starch synthetic genes. J Exp Bot 62:5217–5231

    Google Scholar 

  • Lin Q, Huang B, Zhang M et al (2012) Functional interactions between starch synthase III and isoamylase-type starch-debranching enzyme in maize endosperm. Plant Physiol 158:679–692

    PubMed Central  CAS  PubMed  Google Scholar 

  • Lin Q, Facon M, Putaux JL et al (2013) Function of isoamylase-type starch debranching enzymes ISA1 and ISA2 in the Zea mays leaf. New Phytol 200:1009–1021

    CAS  PubMed  Google Scholar 

  • Liu F, Ahmed Z, Lee EA et al (2012a) Allelic variants of the amylose-extender mutation of maize demonstrate phenotypic variation in starch structure resulting from modified protein-protein interactions. J Exp Bot 63:1167–1183

    PubMed Central  CAS  PubMed  Google Scholar 

  • Liu F, Romanova N, Lee EA et al (2012b) Glucan affinity of starch synthase IIa determines binding of starch synthase I and starch-branching enzyme IIb to starch granules. Biochem J 448:373–387

    CAS  PubMed  Google Scholar 

  • Lloyd JR, Landschütze V, Kossman J (1999) Simultaneous antisense inhibition of two starch-synthase isoforms in potato tubers leads to accumulation of grossy modified amylopectin. Biochem J 338:515–521

    PubMed Central  CAS  PubMed  Google Scholar 

  • Maddelein ML, Libessart N, Bellanger F et al (1994) Toward an understanding of the biogenesis of the starch granule. J Biol Chem 269:25150–25157

    CAS  PubMed  Google Scholar 

  • Mangelsdorf PC (1947) The inheritance of amylaceous sugary endosperm and its derivatives in maize. Genetics 32:448–458

    PubMed Central  CAS  PubMed  Google Scholar 

  • Marshall J, Sidebottom C, Debet M et al (1996) Identification of the major starch synthase in the soluble fraction of potato tuber. Plant Cell 8:1121–1135

    PubMed Central  CAS  PubMed  Google Scholar 

  • McMaugh SJ, Thistleton JL, Anschaw E et al (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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Mizuno K, Kawasaki T, Shimada H et al (1993) Alteration of the structural properties of starch components by the lack of an isoform of starch branching enzyme in rice seeds. J Biol Chem 268:19084–19091

    CAS  PubMed  Google Scholar 

  • Mizuno K, Kobayashi E, Tachibana M et al (2001) Characterization of an isoform of rice starch branching enzyme, RBE4, in developing seeds. Plant Cell Physiol 42:349–357

    CAS  PubMed  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 structural analysis. Biosci Biotechnol Biochem 76(8):1591–1595

    Google Scholar 

  • Morell M, Blennow A, Kosar-Hashemi B (1997) Differential expression and properties of starch branching enzyme isoforms in developing wheat endosperm. Plant Physiol 113:201–208

    PubMed Central  CAS  PubMed  Google Scholar 

  • Morell MK, Kosar-Hashemi B, Cmiel M et al (2003) Barley sex6 mutants lack starch synthase IIa activity and contain a starch with novel properties. Plant J 34:173–185

    CAS  PubMed  Google Scholar 

  • Mouille G, Maddelein M-L, Libessart N et al (1996) Preamylopectin processing: a mandatory step for starch biosynthesis in plants. Plant Cell 8:1353–1366

    PubMed Central  CAS  PubMed  Google Scholar 

  • Mu-Forster C, Huang R, Powers JR et al (1996) Physical association of starch biosynthetic enzymes with starch granules of maize endosperm. Plant Physiol 111:821–829

    PubMed Central  CAS  PubMed  Google Scholar 

  • Murakami T, Kanai T, Takata H et al (2006) A novel branching enzyme of the GH-57 family in the hyperthermophilic archaeon Thermococcus kodakaraensis KODI. J Bacteriol 188:5915–5924

    PubMed Central  CAS  PubMed  Google Scholar 

  • Murata T, Sugiyama T, Akazawa T (1965) Enzymic mechanism of starch synthesis in glutinous rice grains. Biochem Biophys Res Commun 18:371–376

    CAS  PubMed  Google Scholar 

  • Mutisya J, Sathish P, Sun C et al (2003) Starch branching enzymes in sorghum (Sorghum bicolor) and barley (Hordeum vulgare): Comparative analyses of enzyme structure and gene expression. J Plant Physiol 160:921–930

    CAS  PubMed  Google Scholar 

  • Myers AM, Morell MK, James MG et al (2000) Recent progress toward understanding biosynthesis of the amylopectin crystal. Plant Physiol 122:989–997

    PubMed Central  CAS  PubMed  Google Scholar 

  • Nakamura Y (1996) Some properties of starch debranching enzymes and their possible role in amylopectin biosynthesis. Plant Sci 121:1–18

    CAS  Google Scholar 

  • Nakamura Y (2002) Towards a better understanding of the metabolic system for amylopectin biosynthesis plants: Rice endosperm as a model tissue. Plant Cell Physiol 43:718–725

    CAS  PubMed  Google Scholar 

  • Nakamura Y (2014) Mutagenesis and transformation of starch biosynthesis of rice and the production of novel starches. In: Tomlekova N, Kozgar I, Wani R (eds) Mutagenesis: exploring novel genes and pathways. Wageningen, Wageningen Academic, pp 251–278

    Google Scholar 

  • Nakamura Y, Yuki K, Park SY et al (1989) Carbohydrate metabolism in the developing endosperm of rice grains. Plant Cell Physiol 30:833–839

    CAS  Google Scholar 

  • Nakamura Y, Takeichi T, Kawaguchi K et al (1992a) Purification of two forms of starch branching enzyme (Q-enzyme) from developing rice endosperm. Physiol Plant 84:329–335

    CAS  Google Scholar 

  • Nakamura Y, Umemoto T, Takahata Y et al (1992b) Characteristics and roles of key enzymes associated with starch biosynthesis in rice endosperm. Gamma Field Symp 31:25–44

    Google Scholar 

  • Nakamura Y, Umemoto T, Takahata Y et al (1996) Changes in structure of starch and enzyme activities affected by sugary mutations in developing rice endosperm. Possible role of starch debranching enzyme (R-enzyme) in amylopectin biosynthesis. Physiol Plant 97:491–498

    CAS  Google Scholar 

  • Nakamura Y, Kubo A, Shimamune T et al (1997) Correlation between activities of starch debranching enzyme (R-enzyme or pullulanase) and α-glucan structure in endosperms of sugary-1 mutants of rice. Plant J 12:143–153

    CAS  Google Scholar 

  • Nakamura T, Vrinten P, Hayakawa K et al (1998) Characterization of a granule-bound starch synthase isoform found in the pericarp of wheat. Plant Physiol 118:451–459

    PubMed Central  CAS  PubMed  Google Scholar 

  • Nakamura Y, Sakurai A, Inaba Y et al (2002) The fine structure of amylopectin in endosperm from Asian cultivated rice can be largely classified into two classes. Starch 54:117–131

    CAS  Google Scholar 

  • Nakamura Y, Francisco PB Jr, Hosaka Y et al (2005a) Essential amino acids of starch synthase IIa differentiate amylopectin structure and starch quality between japonica and indica rice varieties. Plant Mol Biol 58:213–227

    CAS  PubMed  Google Scholar 

  • Nakamura Y, Takahashi J, Sakurai A et al (2005b) Some cyanobacteria synthesize semi-amylopectin type α-polyglucan instead of glycogen. Plant Cell Physiol 46:539–545

    CAS  PubMed  Google Scholar 

  • Nakamura Y, Fujita N, Utsumi Y et al (2009) Revealing the complex system of starch biosynthesis in higher plants using rice mutants and transformants. In: Shu Q (ed) Induced mutations in the genomics era. Food and Agriculture Organization of the United Nations, Rome, pp 165–167

    Google Scholar 

  • Nakamura Y, Utsumi Y, Sawada T et al (2010) Characterization of the reactions of starch branching enzymes from rice endosperm. Plant Cell Physiol 51:776–794

    CAS  PubMed  Google Scholar 

  • Nakamura Y, Ono M, Utsumi Y et al (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  PubMed  Google Scholar 

  • Nakamura Y, Aihara S, Crofts N et al (2014) In vitro studies of enzymatic properties of starch synthases and interactions between starch synthase I and starch branching enzymes from rice. Plant Sci 224:1–8

    CAS  PubMed  Google Scholar 

  • Nelson OE, Rines HW (1962) The enzymatic deficiency in the waxy mutant of maize. Biochem Biophys Res Commun 9:297–300

    CAS  PubMed  Google Scholar 

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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Noguchi J, Chaen K, Vu NT et al (2011) Crystal structure of the branching enzyme I (BEI) from Oryza sativa L with implications for catalysis and substrate binding. Glycobiology 21:1108–1116

    CAS  PubMed  Google Scholar 

  • Nozaki K, Hamada S, Nakamori T et al (2001) Major isoforms of starch branching enzymes in premature seeds of kidney bean (Phaseolus vulgaris L.). Biosci Biotechnol Biochem 65:1141–1148

    CAS  PubMed  Google Scholar 

  • Ohdan T, Francisco PB Jr, Hosaka Y et al (2005) Expression profiling of genes involved in starch synthesis in sink and source organs of rice. J Exp Bot 56:3229–3244

    CAS  PubMed  Google Scholar 

  • Ohdan T, Sawada T, Nakamura Y (2011) Effects of temperature on starch branching enzyme properties of rice. J Appl Glycosci 58:19–26

    CAS  Google Scholar 

  • Ozbun JL, Hawker JS, Preiss J (1971a) Multiple forms of α-1,4 glucan synthetase from spinach leaves. Biochem Biophys Res Commun 43:631–636

    CAS  PubMed  Google Scholar 

  • Ozbun JL, Hawker JS, Preiss J (1971b) Adenosine diphosphoglucose-starch glucosyl transferases from developing kernels of waxy maize. Plant Physiol 48:765–769

    PubMed Central  CAS  PubMed  Google Scholar 

  • Ozbun JL, Hawker JS, Preiss J (1972) Soluble adenosine diphosphate glucose-arufa-1,4-glucan arufa-4-glucosyltransferases from spinach leaves. Biochem J 126:953–963

    PubMed Central  CAS  PubMed  Google Scholar 

  • Palomo M, Kralj S, van der Maarel MJEC et al (2009) The unique branching pattern of Deinococcus glycogen branching enzymes are determined by their N-terminal domains. Appl Environ Microbiol 75:1355–1362

    PubMed Central  CAS  PubMed  Google Scholar 

  • Pan D, Nelson NE (1984) A debranching enzyme deficiency in endosperms of sugary-1 mutants of maize. Plant Physiol 74:324–328

    PubMed Central  CAS  PubMed  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 

  • Peng C, Wang Y, Liu F et al (2014) FLOURY ENDOSPERM6 encodes a CBM48 domain-containing protein involved in compound granule formation and starch synthesis in rice endosperm. Plant J 77:917–930

    CAS  PubMed  Google Scholar 

  • Pérez S, Bertoft E (2010) The molecular structures of starch components and their contribution to the architecture of starch granules: a comprehensive review. Starch 62:389–420

    Google Scholar 

  • Pfister B, Lu K, Eicke S, et al (2014) Genetic evidence that chain length and branch point distributions are linked determinants of starch granule formation in Arabidopsis. Plant Physiol 165:1457–1474

    Google Scholar 

  • Pollock C, Preiss J (1980) The citrate-stimulated starch synthase of starchy maize kernels: Purification and properties. Arch Biochem Biophys 204:578–588

    CAS  PubMed  Google Scholar 

  • Rahman S, Kosar-Hashemi B, Samuel MS et al (1995) The major proteins of wheat starch granules. Aust J Plant Physiol 22:793–803

    CAS  Google Scholar 

  • Rahman S, Regina A, Li Z et al (2001) Comparison of starch-branching enzyme genes reveals evolutionary relationships among isoforms. Characterization of a gene for starch-branching enzyme IIa from the wheat D genome donor Aegilops tauschii. Plant Physiol 125:1314–1324

    PubMed Central  CAS  PubMed  Google Scholar 

  • Rahman S, Nakamura Y, Li Z et al (2003) The sugary-type isoamylase gene from rice and Aegilops tauschii: characterization and comparison with maize and Arabidopsis. Genome 46:496–506

    CAS  PubMed  Google Scholar 

  • Ral JP, Colleoni C, Wattebled F et al (2006) Circadian clock regulation of starch metabolism establishes GBSSI as a major contributor to amylopectin synthesis in Chlamydomonas reinhardtii. Plant Physiol 142:305–317

    PubMed Central  CAS  PubMed  Google Scholar 

  • Regina A, Kosar-Hashemi B, Li Z et al (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  PubMed  Google Scholar 

  • Regina A, Bird A, Topping D et al (2006) High-amylose wheat generated by RNA interference improves indices of large-bowel health in rats. Proc Natl Acad Sci U S A 103:3546–3551

    PubMed Central  CAS  PubMed  Google Scholar 

  • Regina A, Kosar-Hashemi B, Ling S et al (2010) Control of starch branching in barley defined through differential RNAi suppression of starch branching enzyme IIa and IIb. J Exp Bot 61:1469–1482

    PubMed Central  CAS  PubMed  Google Scholar 

  • Roldán L, Wattebled F, Lucas MM et al (2007) The phenotype of soluble starch synthase IV defective mutant of Arabidopsis thaliana suggests a novel function of elongation enzymes in the control of starch granule formation. Plant J 49:492–504

    PubMed  Google Scholar 

  • Rundle RE, Daasch L, French D (1944) The structure of the “B” modification of starch from film and fiber diffraction diagrams. J Am Chem Soc 66:130–134

    CAS  Google Scholar 

  • Rydberg U, Andersson L, Andersson R et al (2001) Comparison of starch branching enzyme I and II from potato. Eur J Biochem 268:6140–6145

    CAS  PubMed  Google Scholar 

  • Satoh H, Nishi A, Yamashita K et al (2003) Starch-b ranching enzyme I-deficient mutation specifically affects the structure and properties of starch in rice endosperm. Plant Physiol 133:1111–1121

    PubMed Central  CAS  PubMed  Google Scholar 

  • Satoh H, Shibahara K, Tokunaga T et al (2008) Mutation of the plastidial α-glucan phosphorylase gene in rice affects the synthesis of branched maltodextrins. Plant Cell 20:1833–1849

    PubMed Central  CAS  PubMed  Google Scholar 

  • Sawada T, Francisco PB Jr, Aihara S et al (2009) Chlorella starch branching enzyme II (BEII) can complement the function of BEIIb in rice endosperm. Plant Cell Physiol 50:1062–1074

    CAS  PubMed  Google Scholar 

  • Sawada T, Nakagami T, Utsumi Y et al (2013) Characterization of starch and glycogen branching enzymes from various sources. J Appl Glycosci 60:69–78

    CAS  Google Scholar 

  • Sawada T, Nakamura Y, Ohdan T et al (2014) Diversity of reaction characteristics of glucan branching enzymes and the fine structure of α-glucan from various sources. Arch Biochem Biophys 562:9–21

    CAS  PubMed  Google Scholar 

  • Schwarte S, Brust H, Steup M et al (2013) Intraspecific sequence variation and differential expression in starch synthase genes of Arabidopsis thaliana. BMC Res Notes 6:84

    PubMed Central  CAS  PubMed  Google Scholar 

  • Senoura T, Isono N, Yoshikawa M et al (2007) Characterization of starch synthase I and II expressed in early developing seeds of kidney bean (Phaseolus vulgaris L.). Biosci Biotechnol Biochem 68:1949–1960

    Google Scholar 

  • Sestili F, Janni M, Doherty A et al (2010) Increasing the amylose content of durum wheat through silencing of the SBEIIa genes. BMC Plant Biol 10:144

    PubMed Central  PubMed  Google Scholar 

  • Shannon JC, Garwood DL (1984) Genetics and physiology of starch development. In: Whistler RL, BeMiller JN, Paschall EF (eds) Starch: chemistry and technology, 2nd edn. Academic, New York, pp 25–86

    Google Scholar 

  • Shannon JC, Pein FM, Cao HP et al (1998) Brittle-1, an adenylate translocator, facilitates transfer of extraplastidial synthesized ADP-glucose into amyloplasts of maize endosperms. Plant Physiol 117:1235–1252

    PubMed Central  CAS  PubMed  Google Scholar 

  • Shannon JC, Garwood DL, Boyer CD (2007) Genetics and physiology of starch development. In: BeMiller JN, Whistler RL (eds) Starch: chemistry and technology, 3rd edn. Academic, New York, pp 23–82

    Google Scholar 

  • She K, Kusano H, Koizumi K et al (2010) A novel factor FLOURY ENDOSPERM2 is involved in regulation of rice grain size and starch quality. Plant Cell 22:3280–3294

    PubMed Central  CAS  PubMed  Google Scholar 

  • Shimonaga T, Fujiwara S, Kaneko M et al (2006) Variation in storage α-polyglucans of red algae: Amylose and semi-amylopectin-types in Porphyridium and glycogen-type in Cyanidium. Mar Biotechnol 9:192–202

    PubMed  Google Scholar 

  • Shimonaga T, Konishi M, Oyama Y et al (2008) Variation in storage α-glucans of the Porphyridiales (Rhodophyta). Plant Cell Physiol 49:103–116

    CAS  PubMed  Google Scholar 

  • Sim L, Beeren SR, Findinier J, et al (2014) Crystal structure of the Chlamydomonas starch debranching enzyme isoamylase ISA1 reveals insights into the mechanism of branch trimming and complex assembly. J Biol Chem 289:22991–23003

    Google Scholar 

  • Smith AM (1988) Major differences in isoforms of starch-branching enzyme between developing embryos of round- and wrinkled-seeded peas (Pisum sativum L.). Planta 175:270–279

    CAS  PubMed  Google Scholar 

  • Smith SM, Fulton DC, Chia T et al (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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Stam MR, Danchin EGJ, Ranchured C et al (2006) Dividing the large glycoside hydrolase family 13 into subfamilies: towards improved functional annotations of amylase-related proteins. Protein Eng Des Sel 19:555–562

    CAS  PubMed  Google Scholar 

  • Streb S, Zeeman SC (2014) Replacement of the endogenous starch debranching enzymes ISA1 and ISA2 of Arabidopsis with the rice orthologs reveals a degree of functional conservation during starch synthesis. PLoS One 9:e92174

    PubMed Central  PubMed  Google Scholar 

  • Streb S, Delatte T, Umhang M et al (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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Sullivan TD (1995) The maize brittle1 gene encodes amyloplast membrane polypeptides. Planta 196:477–484

    CAS  PubMed  Google Scholar 

  • Sun C, Sathish P, Ahlandsberg S et al (1998) The two genes encoding starch-branching enzymes IIa and IIb are differentially expressed in barley. Plant Physiol 118:37–49

    PubMed Central  CAS  PubMed  Google Scholar 

  • Szydlowsky N, Ragel P, Raynaud S et al (2009) Starch granule initiation in Arabidopsis requires the presence of either class IV or class II starch synthases. Plant Cell 21:2443–2457

    Google Scholar 

  • Szydlowsky N, Ragel P, Hennen-Bierwagen TA (2011) Integrated functions among multiple starch synthases determine both amylopectin chain length and branch linkage location in Arabidopsis leaf starch. J Exp Bot 62:4547–4559

    Google Scholar 

  • Takashima Y, Senoura T, Yoshizaki T et al (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  PubMed  Google Scholar 

  • Takeda Y, Hizukuri S, Juliano BO (1987a) Structure of rice amylopectins with low and high affinities for iodine. Carbohydr Res 168:79–88

    CAS  Google Scholar 

  • Takeda Y, Hizukuri S, Takeda C et al (1987b) Structures of branched molecules of amyloses of various botanical origins, and molar fractions of branched and unbranched molecules. Carbohydr Res 165:139–145

    CAS  Google Scholar 

  • Takeda Y, Guan H, Preiss J (1993) Branching of amylose by the branching isoenzymes of maize endosperm. Carbohydr Res 240:253–263

    CAS  Google Scholar 

  • Takeda Y, Preiss J (1993) Structures of B90 (sugary) and W64A (normal) maize starches. Carbohydr Res 240:265–275

    CAS  Google Scholar 

  • Tanaka Y, Akazawa T (1971) Enzymic mechanism of starch synthesis in ripening rice grains VI. Isozymes of starch synthase. Plant Cell Physiol 12:493–505

    CAS  Google Scholar 

  • Tanaka N, Fujita N, Nishi A et al (2004) The structure of starch can be manipulated by changing expression levels of starch branching enzyme IIb in rice endosperm. Plant Biotechnol J 2:507–516

    CAS  PubMed  Google Scholar 

  • Tetlow I (2012) Branching enzymes and their role in determining structural and functional properties of polyglucan. In: Tetlow I (ed) Starch: origins, structure and metabolism, vol 5, Essential reviews in experimental biology. The Society for Experimental Biology, London, pp 141–177

    Google Scholar 

  • Tetlow IJ, Wait R, Lu Z et al (2004) Protein phosphorylation in amyloplasts regulates starch branching enzyme activity and protein-protein interactions. Plant Cell 16:694–708

    PubMed Central  CAS  PubMed  Google Scholar 

  • Tetlow IJ, Beisel KG, Cameron S et al (2008) Analysis of protein complexes in amyloplasts reveals functional interactions among starch biosynthetic enzymes. Plant Physiol 146:1878–1891

    PubMed Central  CAS  PubMed  Google Scholar 

  • Thompson DB (2000) On the non-random nature of amylopectin branching. Carbohydr Polym 43:223–239

    CAS  Google Scholar 

  • Tomlinson KL, Lloyd JR, Smith AM (1997) Importance of isoforms of starch-branching enzyme in determining the structure of starch in pea leaves. Plant J 11:31–43

    CAS  Google Scholar 

  • Tomlinson KL, Lloyd JR, Smith AM (1998) Major differences in isoform composition of starch synthase between leaves and embryos of pea (Pisum sativum L.). Planta 204:86–92

    CAS  Google Scholar 

  • Toyosawa Y, Kawagoe Y, Matsushima R, et al. (2015) Deficiency of starch synthase IIIa and IVb leads to dramatic changes in starch granule morphology in rice endosperm (submitted)

    Google Scholar 

  • Umemoto T, Nakamura Y, Satoh H et al (1999) Differences of amylopectin structure between two rice varieties in relation to the effects of temperature during grain-filling. Starch 51:58–62

    CAS  Google Scholar 

  • Umemoto T, Yano M, Satoh H et al (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  PubMed  Google Scholar 

  • Usui T, Ogata M, Murata T et al (2009) Sequential analysis of α-glucooligosaccharides with α-(1–4) and α-(1–6) linkages by negative ion Q-TOF MS/MS spectrometry. J Carbohydr Chem 28:421–430

    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  PubMed  Google Scholar 

  • Utsumi Y, Utsumi C, Sawada T et al (2011) Functional diversity of isoamylase oligomers: The ISA1 homo-oligomer is essential for amylopectin biosynthesis in rice endosperm. Plant Physiol 156:61–77

    PubMed Central  CAS  PubMed  Google Scholar 

  • Vester-Christensen MB, Hachem MA, Svensson B et al (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  PubMed  Google Scholar 

  • Vikso-Nielsen A, Blennow A (1998) Isolation of starch branching enzyme I from potato using γ-cyclodextrin affinity chromatography. J Chromatogr 800:382–385

    CAS  Google Scholar 

  • Visser RGF, Somhorst I, Kuipers GJ et al (1991) Inhibition of the expression of the gene for granule-bound starch synthase in potato by antisense constructs. Mol Gen Genet 225:289–296

    CAS  PubMed  Google Scholar 

  • Wang J, Xu H, Zhu Y et al (2013) OsbZIP58, a basic leucine zipper transcription factor, regulates starch biosynthesis in rice endosperm. J Exp Bot 64:3453–3466

    PubMed Central  CAS  PubMed  Google Scholar 

  • Wattebled F, Ral JP, Dauvillée D et al (2003) STA11, a Chlamydomonas reinhardtii locus required for normal starch granule biogenesis, encodes disproportionating enzyme. Further evidence for a function of α-1,4 glucanotransferases during starch granule biosynthesis in green algae. Plant Physiol 132:137–145

    PubMed Central  CAS  PubMed  Google Scholar 

  • Wattebled F, Dong Y, Dumez S et al (2005) Mutants of Arabidopsis lacking a chloroplastic isoamylase accumulates phytoglycogen and an abnormal form of amylopectin. Plant Physiol 138:184–195

    PubMed Central  CAS  PubMed  Google Scholar 

  • Wattebled F, Planchot V, Dong Y et al (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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Weber APM, Linka N (2011) Connecting the plastids: Transporters of the plastid envelope and their role in linking plastidial with cytosolic metabolism. Annu Rev Plant Biol 62:53–77

    CAS  PubMed  Google Scholar 

  • Xia H, Yandeau-Nelson M, Thompson DB et al (2011) Deficiency of maize starch-branching enzyme I results in altered starch fine structure, decreased digestibility and reduced coleoptiles growth during germination. BMC Plant Biol 11:95

    PubMed Central  CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Yamanouchi H, Nakamura Y (1992) Organ specificity of isoforms of starch branching enzyme (Q-enzyme) in rice. Plant Cell Physiol 33:985–991

    CAS  Google Scholar 

  • Yao Y, Thompson DB, Guiltinan MJ (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 Physiol 136:3515–3523

    PubMed Central  CAS  PubMed  Google Scholar 

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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Zeeman SC, Umemoto T, Lue W et al (1998) A mutant of Arabidopsis lacking a chloroplastic isoamylase accumulates both starch and phytoglycogen. Plant Cell 10:1699–1711

    PubMed Central  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Zhang X, Colleoni C, Ralushana V et al (2004) Molecular characterization demonstrates that the Zea mays gene sugary2 codes the starch synthase isoform SSIIa. Plant Mol Biol 54:865–879

    CAS  PubMed  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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Zhang X, Szydlowski N, Delvallé D et al (2008) Overlapping functions of the starch synthase SSII and SSIII in amylopectin biosynthesis in Arabidopsis. BMC Plant Biol 8:96–113

    PubMed Central  CAS  PubMed  Google Scholar 

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Acknowledgments

The author thanks Dr. Perigio B. Francisco, Jr. for critical reading of the manuscript and polishing the English used in the paper. The author also thanks Dr. Takayuki Sawada for the assistance with some figures.

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Authors and Affiliations

  1. Faculty of Bioresource Sciences, Akita Prefectural University, Shimoshinjo-Nakano, Akita, 010-0195, Japan

    Yasunori Nakamura

  2. Akita Natural Science Laboratory, 25-44 Oiwake-Nishi, Tennoh, Katagami, Akita, 010-0101, Japan

    Yasunori Nakamura

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  1. Yasunori Nakamura
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Correspondence to Yasunori Nakamura .

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  1. Faculty of Bioresource Sciences, Akita Prefectural University, Akita, Japan

    Yasunori Nakamura

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Nakamura, Y. (2015). Biosynthesis of Reserve Starch. In: Nakamura, Y. (eds) Starch. Springer, Tokyo. https://doi.org/10.1007/978-4-431-55495-0_5

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