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Starch Biosynthesis in Leaves and Its Regulation

  • Chapter
Starch

Abstract

Plants assimilate carbon during photosynthesis using light energy to reduce atmospheric CO2 and to produce sugars and chemical energy (ATP). Sugars are partly incorporated directly into starch granules in leaf chloroplasts for short-term storage or are exported to non-photosynthetic organs for long-term storage. Indeed, starch accumulation in photosynthetic tissues is transient since it undergoes recurrent cycles of synthesis and degradation following day/night oscillation. Transient starch is synthesized during the day while photosynthesis is active and is degraded at night to provide carbon and energy to the plant when photosynthesis is inactive. Conversely, storage starch accumulates over long periods in storage organs such as seeds or tubers where it is degraded to sustain germination before photosynthesis becomes effective. Transient and storage starch syntheses occur in plastid stroma and involve dedicated enzymatic activities typically supported by several genetically independent isoforms. Although highly similar, both processes hold specific features regarding synthesis and regulation. In this chapter, we describe the mechanism of starch synthesis in photosynthetic tissues (mostly leaves) and its regulation. Several aspects are specifically highlighted here such as: (1) the function of starch synthases for the initiation of starch synthesis and the elongation of the amylopectin- and amylose-forming glucans, (2) the implication of branching enzymes and debranching enzymes for the formation of branch points and the control of their distribution within the polysaccharides, and (3) the regulation of the pathway in leaves especially by the circadian clock , the redox state of the cell and the influence of physiological factors, and the formation of protein-protein complexes.

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References

  • Abel GJW, Springer F, Willmitzer L et al (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  PubMed  Google Scholar 

  • Avonce N, Leyman B, Mascorro-Gallardo JO et al (2004) The Arabidopsis trehalose-6-P synthase AtTPS1 gene is a regulator of glucose, abscisic acid, and stress signaling. Plant Physiol 136:3649–3659

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ball S, Marianne T, Dirick L et al (1991) A Chlamydomonas reinhardtii low-starch mutant is defective for 3-phosphoglycerate activation and orthophosphate inhibition of ADP-glucose pyrophosphorylase. Planta 185:17–26

    CAS  PubMed  Google Scholar 

  • Ball S, Guan H-P, James M 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 

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

    CAS  PubMed  Google Scholar 

  • BeMiller JN, Whistler RL (2009) Starch: chemistry and technology. Elsevier Science, New York

    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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Blauth SL, Kim K-N, 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 

  • Blumenfeld ML, Whelan WJ, Krisman CR (1983) The initiation of glycogen biosynthesis in rat heart. Eur J Biochem 135:175–179

    CAS  PubMed  Google Scholar 

  • Brust H, Lehmann 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  PubMed Central  Google Scholar 

  • Buléon A, Gérard C, Riekel C et al (1998) Details of the crystalline ultrastructure of C-starch granules revealed by synchrotron microfocus mapping. Macromolecules 31:6605–6610

    Google Scholar 

  • Burton RA, 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 

  • Buschiazzo A, Ugalde JE, Guerin ME et al (2004) Crystal structure of glycogen synthase: homologous enzymes catalyze glycogen synthesis and degradation. EMBO J 23:3196–3205

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cantarel BL, Coutinho PM, Rancurel C et al (2009) The carbohydrate-active enzymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Res 37:D233–D238

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cao H, Imparl-Radosevich J, Guan H et al (1999) Identification of the soluble starch synthase activities of maize endosperm. Plant Physiol 120:205–216

    CAS  PubMed  PubMed Central  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  PubMed  PubMed Central  Google Scholar 

  • Chatterjee M, Berbezy P, Vyas D et al (2005) Reduced expression of a protein homologous to glycogenin leads to reduction of starch content in Arabidopsis leaves. Plant Sci 168:501–509

    CAS  Google Scholar 

  • Cheetham NWH, Tao L (1998) Variation in crystalline type with amylose content in maize starch granules: an X-ray powder diffraction study. Carbohydr Polym 36:277–284

    CAS  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  PubMed Central  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 

  • 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 Online 10:413–426

    CAS  Google Scholar 

  • Crevillen P, Ballicora MA, Merida A et al (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  PubMed  Google Scholar 

  • Crumpton-Taylor M, Grandison S, Png KMY et al (2012) Control of starch granule numbers in Arabidopsis chloroplasts. Plant Physiol 158:905–916

    CAS  PubMed  PubMed Central  Google Scholar 

  • Crumpton-Taylor M, Pike M, Lu K-J 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • D’Hulst C, Mérida Á (2010) The priming of storage glucan synthesis from bacteria to plants: current knowledge and new developments. New Phytol 188:13–21

    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 

  • Dang P, Boyer C (1989) Comparison of soluble starch synthases and branching enzymes from leaves and kernels of normal and amylose-extender maize. Biochem Genet 27:521–532

    CAS  PubMed  Google Scholar 

  • Dauvillée D, Colleoni C, Mouille G et al (2001a) Two loci control phytoglycogen production in the monocellular green alga Chlamydomonas reinhardtii. Plant Physiol 125:1710–1722

    PubMed  PubMed Central  Google Scholar 

  • Dauvillée D, Colleoni C, Mouille G et al (2001b) 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  PubMed Central  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 

  • Delatte T, Trevisan M, Parker ML et al (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  PubMed  Google Scholar 

  • Delatte T, Umhang M, Trevisan M et al (2006) Evidence for distinct mechanisms of starch granule breakdown in plants. J Biol Chem 281:12050–12059

    CAS  PubMed  Google Scholar 

  • Delvalle 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

    CAS  PubMed  Google Scholar 

  • Denyer K, Clarke B, Hylton C et al (1996) The elongation of amylose and amylopectin chains in isolated starch granules. Plant J 10:1135–1143

    CAS  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

    CAS  PubMed  PubMed Central  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

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  PubMed Central  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  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

    CAS  PubMed  PubMed Central  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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dumez S, Wattebled F, Dauvillee D et al (2006) Mutants of Arabidopsis lacking starch branching enzyme II substitute plastidial starch synthesis by cytoplasmic maltose accumulation. Plant Cell 18:2694–2709

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fisher D, Gao M, Kim K-N et al (1996a) Two closely related cDNAs encoding starch branching enzyme from Arabidopsis thaliana. Plant Mol Biol 30:97–108

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Flipse E, Suurs L, Keetels CJAM et al (1996) Introduction of sense and antisense cDNA for branching enzyme in the amylose-free potato mutant leads to physico-chemical changes in the starch. Planta 198:340–347

    CAS  Google Scholar 

  • Fontaine T, D'Hulst C, Maddelein ML et al (1993) Toward an understanding of the biogenesis of the starch granule. Evidence that Chlamydomonas soluble starch synthase II controls the synthesis of intermediate size glucans of amylopectin. J Biol Chem 268:16223–16230

    CAS  PubMed  Google Scholar 

  • Fu Y, Ballicora MA, Leykam JF et al (1998) Mechanism of reductive activation of potato tuber ADP-glucose pyrophosphorylase. J Biol Chem 273:25045–25052

    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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Furukawa K, Tagaya M, Inouye M et al (1990) Identification of lysine 15 at the active site in Escherichia coli glycogen synthase. Conservation of Lys-X-Gly-Gly sequence in the bacterial and mammalian enzymes. J Biol Chem 265:2086–2090

    CAS  PubMed  Google Scholar 

  • Furukawa K, Tagaya M, Tanizawa K et al (1993) Role of the conserved Lys-X-Gly-Gly sequence at the ADP-glucose-binding site in Escherichia coli glycogen synthase. J Biol Chem 268:23837–23842

    CAS  PubMed  Google Scholar 

  • Gámez-Arjona FM, Raynaud S, Ragel P et al (2014) Starch synthase 4 is located in the thylakoid membrane and interacts with plastoglobule-associated proteins in Arabidopsis. Plant J 80(2):305–316

    PubMed  Google Scholar 

  • Gao M, Fisher D, Kim K-N et al (1996) Evolutionary conservation and expression patterns of maize starch branching enzyme I and IIb genes suggests isoform specialization. Plant Mol Biol 30:1223–1232

    CAS  PubMed  Google Scholar 

  • Gao M, Fisher DK, Kim KN et al (1997) Independent genetic control of maize starch-branching enzymes IIa and IIb (Isolation and characterization of a Sbe2a cDNA). Plant Physiol 114:69–78

    CAS  PubMed  PubMed Central  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 Online 10:399–412

    CAS  Google Scholar 

  • Garwood DL, Shannon JC, Creech RG (1976) Starches of endosperm possessing different alleles at the amylose-extender locus in Zea mays L. Cereal Chem 53:355–364

    CAS  Google Scholar 

  • Gérard C, Planchot V, Colonna P et al (2000) Relationship between branching density and crystalline structure of A- and B-type maize mutant starches. Carbohydr Res 326:130–144

    PubMed  Google Scholar 

  • Gibon Y, Bläsing OE, Palacios-Rojas N et al (2004) Adjustment of diurnal starch turnover to short days: depletion of sugar during the night leads to a temporary inhibition of carbohydrate utilization, accumulation of sugars and post-translational activation of ADP-glucose pyrophosphorylase in the following light period. Plant J 39:847–862

    CAS  PubMed  Google Scholar 

  • Gibson K, Park J-S, Nagai Y et al (2011) Exploiting leaf starch synthesis as a transient sink to elevate photosynthesis, plant productivity and yields. Plant Sci 181:275–281

    CAS  PubMed  Google Scholar 

  • Glaring MA, Skryhan K, Kötting O et al (2012) Comprehensive survey of redox sensitive starch metabolising enzymes in Arabidopsis thaliana. Plant Physiol Biochem 58:89–97

    CAS  PubMed  Google Scholar 

  • Godet MC, Bizot H, Buléon A (1995) Crystallization of amylose—fatty acid complexes prepared with different amylose chain lengths. Carbohydr Polym 27:47–52

    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  PubMed  Google Scholar 

  • Graf A, Schlereth A, Stitt M et al (2010) Circadian control of carbohydrate availability for growth in Arabidopsis plants at night. Proc Natl Acad Sci 107:9458–9463

    CAS  PubMed  PubMed Central  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

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hädrich N, Hendriks JHM, Kötting O et al (2012) Mutagenesis of cysteine 81 prevents dimerization of the APS1 subunit of ADP-glucose pyrophosphorylase and alters diurnal starch turnover in Arabidopsis thaliana leaves. Plant J 70:231–242

    PubMed  Google Scholar 

  • Harn C, Knight M, Ramakrishnan A et al (1998) Isolation and characterization of the zSSIIa and zSSIIb starch synthase cDNA clones from maize endosperm. Plant Mol Biol 37:639–649

    CAS  PubMed  Google Scholar 

  • Haworth WN, Peat S, Bourne EJ (1944) Synthesis of amylopectin. Nature 154:236

    CAS  Google Scholar 

  • Haydon MJ, Mielczarek O, Robertson FC et al (2013) Photosynthetic entrainment of the Arabidopsis thaliana circadian clock. Nature 502:689–692

    CAS  PubMed  Google Scholar 

  • Hedman K, Boyer C (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 

  • Hendriks JHM, Kolbe A, Gibon Y et al (2003) ADP-glucose pyrophosphorylase is activated by posttranslational redox-modification in response to light and to sugars in leaves of Arabidopsis and other plant species. Plant Physiol 133:838–849

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hennen-Bierwagen TA, James MG, Myers AM (2012) Involvement of debranching enzymes in starch biosynthesis. In: Tetlow IJ (ed) Starch: origins, structure and metabolism, vol 5. Society for Experimental Biology, London

    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 (1985) Relationship between the distribution of the chain length of amylopectin and the crystalline structure of starch granules. Carbohydr Res 141:295–306

    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  PubMed  PubMed Central  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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Imberty A, Chanzy H, Pérez S et al (1988) The double-helical nature of the crystalline part of A-starch. J Mol Biol 201:365–378

    CAS  PubMed  Google Scholar 

  • Ingkasuwan P, Netrphan S, Prasitwattanaseree S et al (2012) Inferring transcriptional gene regulation network of starch metabolism in Arabidopsis thaliana leaves using graphical Gaussian model. BMC Syst Biol 6:100

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  Google Scholar 

  • Jane J-L, Kasemsuwan T, Leas S et al (1994) Anthology of starch granule morphology by scanning electron microscopy. Starch-Stärke 46:121–129

    CAS  Google Scholar 

  • Jane J-L, Wong K-S, McPherson AE (1997) Branch-structure difference in starches of A- and B-type X-ray patterns revealed by their Naegeli dextrins. Carbohydr Res 300:219–227

    CAS  Google Scholar 

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

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Jobling SA, Schwall GP, Westcott RJ et al (1999) A minor form of starch branching enzyme in potato (Solanum tuberosum L.) tubers has a major effect on starch structure: cloning and characterisation of multiple forms of SBE A. Plant J 18:163–171

    CAS  PubMed  Google Scholar 

  • Khoshnoodi J, Larsson CT, Larsson H et al (1998) Differential accumulation of Arabidopsis thaliana Sbe2.1 and Sbe2.2 transcripts in response to light. Plant Sci 135:183–193

    CAS  Google Scholar 

  • Kleczkowski LA (2000) Is leaf ADP-glucose pyrophosphorylase an allosteric enzyme? Biochim Biophys Acta Gen Subj 1476:103–108

    CAS  Google Scholar 

  • Kolbe A, Tiessen A, Schluepmann H et al (2005) Trehalose 6-phosphate regulates starch synthesis via posttranslational redox activation of ADP-glucose pyrophosphorylase. Proc Natl Acad Sci U S A 102:11118–11123

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kossmann J, Abel GJW, Springer F et al (1999) Cloning and functional analysis of a cDNA encoding a starch synthase from potato (Solanum tuberosum L.) that is predominantly expressed in leaf tissue. Planta 208:503–511

    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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lee S-K, Hwang S-K, Han M et al (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  PubMed  Google Scholar 

  • Lepistö A, Pakula E, Toivola J et al (2013) Deletion of chloroplast NADPH-dependent thioredoxin reductase results in inability to regulate starch synthesis and causes stunted growth under short-day photoperiods. J Exp Bot 64:3843–3854

    PubMed  PubMed Central  Google Scholar 

  • Li J, Ezquer I, Bahaji A et al (2011) Microbial volatile-induced accumulation of exceptionally high levels of starch in Arabidopsis leaves is a process involving NTRC and starch synthase classes III and IV. Mol Plant-Microbe Interact 24:1165–1178

    CAS  PubMed  Google Scholar 

  • Li J, Almagro G, Muñoz FJ et al (2012) Post-translational redox modification of ADP-glucose pyrophosphorylase in response to light is not a major determinant of fine regulation of transitory starch accumulation in Arabidopsis leaves. Plant Cell Physiol 53:433–444

    CAS  PubMed  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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lin Q, Facon M, Putaux J-L 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 (2012) 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lomako J, Lomako WM, Whelan WJ (1988) A self-glucosylating protein is the primer for rabbit muscle glycogen biosynthesis. FASEB J 2:3097–3103

    CAS  PubMed  Google Scholar 

  • Lomako J, Lomako WM, Whelan WJ (2004) Glycogenin: the primer for mammalian and yeast glycogen synthesis. Biochim Biophys Acta Gen Subj 1673:45–55

    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  PubMed  PubMed Central  Google Scholar 

  • Lunn JE, Feil R, Hendriks JHM et al (2006) Sugar-induced increases in trehalose 6-phosphate are correlated with redox activation of ADPglucose pyrophosphorylase and higher rates of starch synthesis in Arabidopsis thaliana. Biochem J 397:139–148

    CAS  PubMed  PubMed Central  Google Scholar 

  • Makhmoudova A, Williams D, Brewer D et al (2014) Identification of multiple phosphorylation sites on maize endosperm starch branching enzyme IIb, a key enzyme in amylopectin biosynthesis. J Biol Chem 289:9233–9246

    CAS  PubMed  PubMed Central  Google Scholar 

  • Matheson NK (1996) The chemical structure of amylose and amylopectin fractions of starch from tobacco leaves during development and diurnally-nocturnally. Carbohydr Res 282:247–262

    CAS  PubMed  Google Scholar 

  • Michalska J, Zauber H, Buchanan BB et al (2009) NTRC links built-in thioredoxin to light and sucrose in regulating starch synthesis in chloroplasts and amyloplasts. Proc Natl Acad Sci 106:9908–9913

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mikkelsen R, Mutenda KE, Mant A et al (2005) a-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  PubMed  PubMed Central  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 

  • Mortimer JC, Miles GP, Brown DM et al (2010) Absence of branches from xylan in Arabidopsis gux mutants reveals potential for simplification of lignocellulosic biomass. Proc Natl Acad Sci 107:17409–17414

    CAS  PubMed  PubMed Central  Google Scholar 

  • Myers AM, Morell MK, James MG et al (2000) Recent progress toward understanding biosynthesis of the amylopectin crystal. Plant Physiol 122:989–998

    CAS  PubMed  PubMed Central  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 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

    CAS  PubMed  PubMed Central  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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Palopoli N, Busi MV, Fornasari MS et al (2006) Starch-synthase III family encodes a tandem of three starch-binding domains. Protein Struct Funct Bioinf 65:27–31

    CAS  Google Scholar 

  • Pfister B, Lu K-J, 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ragel P, Streb S, Feil R et al (2013) Loss of starch granule initiation has a deleterious effect on the growth of Arabidopsis plants due to an accumulation of ADP-glucose. Plant Physiol 163:75–85

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ral J-P, 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rennie EA, Hansen SF, Baidoo EEK et al (2012) Three members of the Arabidopsis glycosyltransferase family 8 are xylan glucuronosyltransferases. Plant Physiol 159:1408–1417

    CAS  PubMed  PubMed Central  Google Scholar 

  • Roldán I, Wattebled F, Lucas MM et al (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

    PubMed  Google Scholar 

  • Rongine De Fekete MA, Leloir LF, Cardini CE (1960) Mechanism of starch biosynthesis. Nature 187:918–919

    CAS  PubMed  Google Scholar 

  • Rose A, Meier I (2004) Scaffolds, levers, rods and springs: diverse cellular functions of long coiled-coil proteins. Cell Mol Life Sci CMLS 61:1996–2009

    CAS  Google Scholar 

  • Sanz-Barrio R, Corral-Martinez P, Ancin M et al (2013) Overexpression of plastidial thioredoxin f leads to enhanced starch accumulation in tobacco leaves. Plant Biotechnol J 11:618–627

    CAS  PubMed  Google Scholar 

  • Scialdone A, Mugford ST, Feike D et al (2013) Arabidopsis plants perform arithmetic division to prevent starvation at night. eLife 2:e00669

    PubMed  PubMed Central  Google Scholar 

  • Seung D, Thalmann M, Sparla F et al (2013) Arabidopsis thaliana AMY3 is a unique redox-regulated chloroplastic α-amylase. J Biol Chem 288:33620–33633

    CAS  PubMed  PubMed Central  Google Scholar 

  • Silver DM, Silva LP, Issakidis-Bourguet E et al (2013) Insight into the redox regulation of the phosphoglucan phosphatase SEX4 involved in starch degradation. FEBS J 280:538–548

    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(33):22991–23003

    CAS  PubMed  Google Scholar 

  • Smith A, Neuhaus HE, Stitt M (1990) The impact of decreased activity of starch-branching enzyme on photosynthetic starch synthesis in leaves of wrinkled-seeded peas. Planta 181:310–315

    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

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  PubMed Central  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 9:9

    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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sulpice R, Pyl E-T, Ishihara H et al (2009) Starch as a major integrator in the regulation of plant growth. Proc Natl Acad Sci 106:10348–10353

    CAS  PubMed  PubMed Central  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

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Szydlowski N, Ragel P, Hennen-Bierwagen TA et al (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

    CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Tenorio G, Orea A, Romero J et al (2003) Oscillation of mRNA level and activity of granule-bound starch synthase I in Arabidopsis leaves during the day/night cycle. Plant Mol Biol 51:949–958

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tiessen A, Hendriks JHM, Stitt M et al (2002) Starch synthesis in potato tubers is regulated by post-translational redox modification of ADP-glucose pyrophosphorylase: a novel regulatory mechanism linking starch synthesis to the sucrose supply. Plant Cell 14:2191–2213

    CAS  PubMed  PubMed Central  Google Scholar 

  • Toivola J, Nikkanen L, Dahlström KM et al (2013) Overexpression of chloroplast NADPH-dependent thioredoxin reductase in Arabidopsis enhances leaf growth and elucidates in-vivo function of reductase and thioredoxin domains. Front Plant Sci 4:389

    PubMed  PubMed Central  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 

  • Tyynelä J, Schulman AH (1993) An analysis of soluble starch synthase isozymes from the developing grains of normal and shx cv. Bomi barley (Hordeum vulgare). Physiol Plant 89:835–841

    Google Scholar 

  • Ugalde JE, Parodi AJ, Ugalde RA (2003) De novo synthesis of bacterial glycogen: agrobacterium tumefaciens glycogen synthase is involved in glucan initiation and elongation. Proc Natl Acad Sci U S A 100:10659–10663

    CAS  PubMed  PubMed Central  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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Valdez HA, Busi MV, Wayllace NZ et al (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  PubMed  Google Scholar 

  • Valerio C, Costa A, Marri L et al (2011) Thioredoxin-regulated β-amylase (BAM1) triggers diurnal starch degradation in guard cells, and in mesophyll cells under osmotic stress. J Exp Bot 62:545–555

    CAS  PubMed  PubMed Central  Google Scholar 

  • van de Wal M, D’Hulst C, Vincken J-P et al (1998) Amylose is synthesized in vitro by extension of and cleavage from amylopectin. J Biol Chem 273:22232–22240

    PubMed  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  PubMed  PubMed Central  Google Scholar 

  • Wattebled F, Buléon A, Bouchet B et al (2002) Granule-bound starch synthase I. A major enzyme involved in the biogenesis of B-crystallites in starch granules. Eur J Biochem 269:3810–3820

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wu AC, Ral J-P, Morell MK et al (2014) New perspectives on the role of α- and β-amylases in transient starch synthesis. PLoS ONE 9:e100498

    PubMed  PubMed Central  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 

  • Yandeau-Nelson MD, Laurens L, Shi Z et al (2011) Starch-branching enzyme IIa is required for proper diurnal cycling of starch in leaves of maize. Plant Physiol 156:479–490

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zabawinski C, Van Den Koornhuyse N, D'Hulst C et al (2001) Starchless mutants of Chlamydomonas reinhardtii lack the small subunit of a heterotetrameric ADP-glucose pyrophosphorylase. J Bacteriol 183:1069–1077

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zeeman SC, Umemoto T, Lue W-L et al (1998) A mutant of Arabidopsis lacking a chloroplastic isoamylase accumulates both starch and phytoglycogen. Plant Cell 10:1699–1712

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang X, Colleoni C, Ratushna V et al (2004) Molecular characterization demonstrates that the Zea mays gene sugary2 codes for 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

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

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D’Hulst, C., Wattebled, F., Szydlowski, N. (2015). Starch Biosynthesis in Leaves and Its Regulation. In: Nakamura, Y. (eds) Starch. Springer, Tokyo. https://doi.org/10.1007/978-4-431-55495-0_6

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