From Bacterial Glycogen to Starch: Understanding the Biogenesis of the Plant Starch Granule

Annual Review of Plant Biology

Volumn 54, Issue , 2003, Pages 207-233

  Ball, Steven G ^a   Morell, Matthew K ^b  

^a UNIVERSITÉ DES SCIENCES ET TECHNOLOGIES DE LILLE   (France)

^b CSIRO   (Australia)

Author keywords

Amylopectin; Amylose; Branching enzyme; Isoamylase; Malto oligosaccharide metabolism

Indexed keywords

ALGAE; BACTERIA (MICROORGANISMS); CHLOROPHYTA; CYANOBACTERIA; ESCHERICHIA COLI; EUKARYOTA;

ADENOSINE DIPHOSPHATE GLUCOSE; AMYLOSE; GLYCOGEN; STARCH; STARCH SYNTHASE;

BACTERIUM; BIOSYNTHESIS; METABOLISM; MICROBIOLOGY; PLANT; REVIEW;

ADENOSINE DIPHOSPHATE GLUCOSE; AMYLOSE; BACTERIA; GLYCOGEN; PLANTS; STARCH; STARCH SYNTHASE;

EID: 0142040430     PISSN: 15435008     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.arplant.54.031902.134927     Document Type: Review

References (113)

1. Alonso MD, Lomako J, Lomako WM, Whelan WJ. 1995. A new look at the biogenesis of glycogen. FASEB J. 12:1126-37
2. Baba T, Nishihara M, Mizuno K, Kawasaki T, Shimada H, et al. 1993. Identification, cDNA cloning, and gene expression of soluble starch synthase in rice (Oryza sativa L.) immature seeds. Plant Physiol. 103:565-73
3. Ball SG. 2002. The intricate pathway of starch biosynthesis and degradation in the monocellular alga Chlamydomonas reinhardtii. Aust. J. Chem. 55:49-59
4. Ball S, Guan H-P, James M, Myers A, Keeling P, et al. 1996. From glycogen to amylopectin: a model explaining the biogenesis of the plant starch granule. Cell 86:349-52
5. Ball SG, van de Wal MHBJ, Visser RGF. 1998. Progress in understanding the biosynthesis of amylose. Trends Plant Sci. 3:462-67
6. Ballicora M, Frueauf JB, Fu Y, Schurmann P, Preiss J. 2000. Activation of the potato tuber ADPglucose pyrophosphorylase by thioredoxin. J. Biol. Chem. 275:1315-20
7. Beatty MK, Rahman A, Cao H, Woodman W, Lee M, et al. 1999. Purification and molecular genetic characterization of ZPU1, a pullulanase-type starch debranching enzyme from maize. Plant Physiol. 119:255-66
8. Beckles DM, Craig J, Smith AM. 2001. ADPglucose pyrophosphorylase is located in the plastid in developing tomato fruit. Plant Physiol. 126:261-66
9. Blauth SL, Kim KN, Klucinec J, Shannon JC, Thompson D, Guiltinan M. 2002. Identification of Mutator insertional mutants of starch-branching enzyme 1 (sbe1) in Zea mays L. Plant Mol. Biol. 48:287-97
10. Blauth SL, Yao Y, Klucinec JD, Shannon JC, Thompson DB, Guilitinan MJ. 2001. Identification of Mutator insertional mutants of starch-branching enzyme 2a in corn. Plant Physiol. 125:1396-405
11. Boos W, Shuman H. 1998. Maltose/maltodextrin system of Escherichia coli: transport, metabolism, and regulation. Microbiol. Mol. Biol. Rev. 62:204-29
12. Buléon A, Ball S, Planchot V, Colonna P. 1998. Starch granules: structure and biosynthesis. Int. J. Biol. Macromol. 23:85-12
13. Buléon A, Gallant DJ, Bouchet B, Mouille G, D'Hulst C, et al. 1997. Starches from A to C. Chlamydomonas reinhardtiias a model microbial system to investigate the biosynthesis of the plant amylopectin crystal. Plant Physiol. 115:949-57
14. Burton RA, Bewley JD, Smith AM, Bhattacharyya MK, Tatge H, et al. 1995. Starch branching enzymes belonging to distinct enzyme families are differentially expressed during pea embryo development. Plant J. 7:3-15
15. Cheng C, Mu J, Farkas I, Huang D, Goebl MG, et al. 1995. Requirement of the self-glucosylating initiator proteins G1g1p and G1g2p for glycogen accumulation in Saccharomyces cerevisiae. Mol. Cell. Biol. 12:6632-40
16. Cho MJ, Wong JH, Marx C, Jiang W, Lemaux PG, et al. 1999. Overexpression of thioredoxin h leads to enhanced activity of starch debranching enzyme (pullulanase) in barley grain. Proc. Natl. Acad. Sci. USA 96:14641-46
17. Clarke BR, Denyer K, Jenner CF, Smith AM. 1999. The relationship between the rate of starch synthesis, the adenosine 5′-diphosphoglucose concentration and the amylose content of starch in developing pea embryos. Planta 209:324-29
18. Colleoni C, Dauvillée D, Mouille G, Buléon A, Gallant D, et al. 1999. Genetic and biochemical evidence for the involvement of α-1, 4 glucanotransferases in amylopectin synthesis. Plant Physiol. 120:993-1004
19. Colleoni C, Dauvillée D, Mouille G, Morell M, Samuel M, et al. 1999. Biochemical characterization of the Chlamydomonas reinhardtii α-1,4 glucanotransferase supports a direct function in amylopectin biosynthesis. Plant Physiol. 120:1005-14
20. Craig J, Lloyd JR, Tomlinson K, Barber L, Edwards A, et al. 1998. Mutations in the gene encoding starch synthase II profoundly alter amylopectin structure in pea embryos. Plant Cell 10:413-26
21. Critchley JM, Zeeman SC, Takaha T, Smith AM, Smith SM. 2001. A critical role for disproportionating enzyme in starch breakdown is revealed by a knock-out mutation in Arabidopsis. Plant J. 26:89-100
22. Damotte M, Cattaneo J, Sigal N, Puig J. 1968. Mutants of Escherichia coli K 12 altered in their ability to store glycogen. Biochem. Biophys. Res. Commun. 6:916-20
23. Dauvillée D, Colleoni C, Shaw E, Mouille G, D'Hulst C, et al. 1999. Novel starch-like polysaccharides are synthesized by a soluble form of granule-bound starch synthase in glycogen accumulating mutants of Chlamydomonas reinhardtii. Plant Physiol. 119:321-30
24. Dauvillée D, Mestre V, Colleoni C, Slomiany M-C, Mouille G, et al. 2000. The debranching enzyme complex missing in glycogen accumulating mutants of Chlamydomonas reinhardtii displays an isoamylase-type specificity. Plant Sci. 157:145-56
25. Dauvillée D, Colleoni C, Mouille G, Buléon A, Gallant DJ, et al. 2001. Two loci control phytoglycogen production in the monocellular green alga Chlamydomonas reinhardtii. Plant Physiol. 125:1710-22
26. Dauvillée D, Colleoni C, Mouille G, Morell MK, d'Hulst C, 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. 125:1723-31
27. de Fekete MAR, Leloir LF, Cardini CE. 1960. Mechanism of starch biosynthesis. Nature 187:918-19
28. Delrue B, Fontaine, T, Routier F, Decq A, Wieruszeski JM, 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. 174:3612-20
29. Denyer K, Clarke B, Hylton C, Tatge H, Smith A. 1996. The elongation of amylose and amylopectin chains in isolated starch granules. Plant J. 10:1135-43
30. Denyer K, Dunlap F, Thorbjornsen T, Keeling P, Smith AM. 1996. The major form of ADPglucose pyrophosphorylase in maize endosperm is extra-plastidial. Plant Physiol. 112:779-85
31. Denyer K, Hylton CM, Jenner CF, Smith AM. 1995. Identification of multiple isoforms of soluble and granule- bound starch synthase in developing wheat endosperm. Planta 196:256-65
32. Denyer K, Waite D, Edwards A, Martin C, Smith AM. 1999. Interaction with amylopectin influences the ability of granule-bound starch synthase I to elongate malto-oligosaccharides. Biochem. J. 342:647-53
33. Dinges JR, Colleoni C, Myers AM, James MG. 2001. Molecular structure of three mutations at the maize sugary 1 locus and their allele-specific phenotypic effects. Plant Physiol. 125:1406-18
34. Doehlert DC, Knutson CA. 1991. Two classes of starch debranching enzymes from developing maize kernels. J. Plant Physiol. 138:566-72
35. Edwards A, Fulton DC, Hylton CM, Jobling SA, Gidley M, et al. 1999. A combined reduction in activity of starch synthases II and III of potato has novel effects on the starch of tubers. Plant J. 17:251-61
36. Edwards A, Vincken JP, Suurs LCJM, Visser RGF, Zeeman S, et al. 2002. Discrete forms of amylose are synthesized by isoforms of GBSSI in Pea. Plant Cell 14:1767-85
37. Emes MJ, Neuhaus HE. 1997. Metabolism and transport in non-photosynthetic plastids. J. Exp. Bot. 48:1995-2005
38. Flipse E, Suurs L, Keetels CJA, Kossmann J, Jacobsen E, Visser RGF. 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 198:340-47
39. Fontaine T, D'Hulst C, Maddelein M-L, Routier F, Marianne-Pepin T, 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. 268:16223-30
40. Fu Y, Ballicora M, Leykam JF, Preiss J. 1998. Mechanism of reductive activation of potato tuber ADPglucose pyrophosphorylase. J. Biol. Chem. 273:25045-52
41. Fujita N, Kubo A, Francisco PB Jr, Nakakita M, Harada K, et al. 1999. Purification, characterization, and cDNA structure of isoamylase from developing endosperm of rice. Planta 208:283-93
42. Fujita N, Taira T. 1998. A 56-kda protein is a novel granule-bound starch synthase existing in the pericarps, aleurone layers, and embryos of immature seed in diploid wheat (Triticum monococcum L.). Planta 207:125-32
43. Fulton DC, Edwards A, Pilling E, Robinson HL, Fahy B, et al. 2002. Role of granule-bound starch synthase in determination of amylopectin structure and starch granule morphology in potato. J. Biol. Chem. 277:10834-41
44. Gao M, Fisher DK, Kim KN, Shannon JC, Guiltinan MJ. 1996. Evolutionary conservation and expression patterns of maize starch branching enzyme I and IIb genes suggests isoform specialization. Plant Mol. Biol. 30:1223-32
45. Gao M, Wanat J, Stinard PS, James MG, Myers AM. 1998. Characterization of dull1, a maize gene coding for a novel starch synthase. Plant Cell 10:399-412
46. Ghosh HP, Preiss J. 1966. Adenosine diphosphate glucose pyrophosphorylase. A regulatory enzyme in the biosynthesis of starch in spinach leaf chloroplasts. J. Biol. Chem. 241:4491-504
47. Gomez-Casati DF, Iglesias AA. 2002. ADPglucose pyrophosphorylase from wheat endosperm. Purification and characterization of an enzyme with novel regulatory properties. Planta 214:428-34
48. Govons S, Vinopal R, Ingraham J, Preiss J. 1969. Isolation of mutants of Escherichia coli B altered in their ability to synthesize glycogen. J. Bacteriol. 2:970-72
49. Guan HP, Kuriki T, Sivak M, Preiss J. 1995. Maize branching enzyme catalyzes synthesis of glycogen-like polysaccharide in glgB-deficient E. coli. Proc. Natl. Acad. Sci. USA 92:964-67
50. Guan HP, Li P, Imparl-Radosevich J, Preiss J, Keeling P. 1997. Comparing the properties of Escherichia coli branching enzyme and maize branching enzyme. Arch. Biochem. Biophys. 342:92-98
51. Harn C, Knight M, Ramakrishnan A, Guan HP, Keeling PL, Wasserman BP. 1998. Isolation and characterization of the ZSSIIa and ZSSIIb starch synthase cDNA clones from maize endosperm. Plant Mol. Biol. 37:639-49
52. Hedley CL, Bogracheva TY, Wang TL. 2002. A genetic approach to studying the morphology, structure and function of starch granules using pea as a model. Starch-Starke 54:235-42
53. Henker A, Schindler I, Renz A, Beck E. 1998. Protein heterogeneity of spinach pullulanase results from the coexistence of interconvertible isomeric forms of the monomeric enzyme. Biochem. J. 331:929-35
54. Henrissat B, Coutinho PM, Davies GJ. 2001. A census of carbohydrate-active enzymes in the genome of Arabidopsis thaliana. Plant Mol. Biol. 47:55-72
55. Hicks GR, Hironaka CM, Dauvillée D, Funke RP, D'Hulst C, et al. 2001. When simpler is better. Unicellular green algae for discovering new genes and functions in carbohydrate metabolism. Plant Physiol. 127:1334-38
56. Ishizaki Y, Taniguchi H, Maruyama Y, Nakamura M. 1983. Debranching enzymes of potato tuber Solanum tuberosum L. I. Purification and some properties of potato isoamylase. Agric. Biol. Chem. 47:771-79
57. James MG, Robertson DS, Meyers AM. 1995. Characterization of the maize gene sugaryl, a determinant of starch composition in kernels. Plant Cell 7:417-29
58. Jeanningros R, Creuzet-Sigal N, Frixon C, Cattaneo J. 1976. Purification and properties of a debranching enzyme from Escherichia coli. Biochem. Biophys. Acta 438:186-99
59. Jobling SA, Schwall GP, Westcott RJ, Sidebottom CM, Debet M, 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. 18:163-71
60. Khoshnoodi J, Larsson CT, Larsson H, Rask L. 1998. Differential accumulation of Arabidopsis thaliana SBE2.1 and SBE2.2 transcripts in response to light. Plant Sci. 135:183-93
61. Kleczkowski LA, Villand P, Lüthi E, Olsen O-A, Preiss J. 1993. Insensitivity of barley endosperm ADPglucose pyrophosphorylase to 3-phosphoglycerate and orthophosphate regulation. Plant Physiol. 101:179-86
62. Kossman J, Lloyd JR. 2000. Understanding and influencing starch biochemistry. Crit. Rev. Plant Sci. 19:171-226
63. Kubo A, Fujita N, Harada K, Matsuda T, Satoh H, et al. 1999. The starch-debranching enzymes isoamylase and pullulanase are both involved in amylopectin biosynthesis in rice endosperm. Plant Physiol. 121:399-410
64. Leloir LF, De Fekete MAR, Cardini CE. 1961. Starch and oligosaccharide synthesis from uridine diphosphate glucose. J. Biol. Chem. 236:636-41
65. Li Z, Rahman S, Kosar-Hashemi B, Mouille G, Appels R, Morell MK. 1999. Cloning and characterization of a gene encoding wheat starch synthase I. Theor. Appl. Genet. 98:1208-16
66. Li ZY, Chu XS, Mouille G, Yan LL, Kosar-Hashemi B, et al. 1999. The localization and expression of the class II starch synthases of wheat. Plant Physiol. 120:1147-55
67. Li ZY, Mouille G, Kosar-Hashemi B, Rahman S, Clarke B, et al. 2000. The structure and expression of the wheat starch synthase III gene. Motifs in the expressed gene define the lineage of the starch synthase III gene family. Plant Physiol. 123:613-24
68. Libessart N, Maddelein ML, Van Den Koornhuyse N, Decq A, Delrue B, et al. 1995. Storage, photosynthesis and growth: the conditional nature of mutations affecting starch synthesis and structure in Chlamydomonas reinhardtii. Plant Cell 7:1117-27
69. Lloyd JR, Springer F, Buléon A, Muller-Rober B, Willmitzer L, et al. 1999. The influence of alterations in ADPglucose pyrophosphorylase activities on starch structure and composition in potato tubers. Planta 209:230-38
70. Maddelein ML, Libessart N, Bellanger F, Delrue B, D'Hulst C, et al. 1994. Toward an understanding of the biogenesis of the starch granule: Determination of granule-bound and soluble starch synthase functions in amylopectin synthesis. J. Biol. Chem. 269:25150-57
71. Manners D. 1991. Recent developments in our understanding of glycogen structure. Carbohydr. Polymers 16:37-82
72. Marin K, Zuther E, Kerstan T, Kunert A, Hagemann M. 1998. The ggpS gene from Synechocystis sp. strain PCC 6803 encoding glucosyl-glycerol-phosphate synthase is involved in osmolyte synthesis. J. Bacteriol. 18:4843-49
73. McCracken DA, Cain JR. 1981. Amylose in floridean starch. New Phytol. 88:67-71
74. Merida A, Rodriguez-Galan JM, Vincent C, Romero JM. 1999. Expression of granule-bound starch synthase I (waxy) gene from snapdragon is developmentally and circadian clock regulated. Plant Physiol. 120:401-9
75. Morell MK, Blennow A, Kosar-Hashemi B, Samuel MS. 1997. Differential expression and properties of starch branching enzyme isoforms in developing wheat endosperm. Plant Physiol. 113:201-8
76. Mouille G, Maddelein M-L, Libessart N, Talaga P, Decq A, et al. 1996. Phytoglycogen processing: a mandatory step for starch biosynthesis in plants. Plant Cell 8:1353-66
77. Mu C, Harn C, Ko Y-T, Singletary GW, Keeling PL, Wasserman BP. 1994. Association of a 76 kDa polypeptide with soluble starch synthase I activity in maize (cv B73) endosperm. Plant J. 6:151-59
78. Mukerjea R, Yu L, Robyt JF. 2002. Starch biosynthesis: mechanism for the elongation of starch chains. Carbohydr. Res. 337:1015-22
79. Myers, AM, Morell MK, James MG, Ball SG. 2000. Recent progress in understanding biosynthesis of the amylopectin crystal. Plant Physiol. 122:989-98
80. Nakamura Y, Kubo A, Shimamune T, Matsuda T, Harada K, et al. 1997. Correlation between activities of starch debranching enzymes and α-polyglucan structure in endosperms of sugary-1 mutants of rice. Plant J. 12:143-53
81. Nakamura Y, Umemoto T, Takahata Y, Komae K, Amano E, et al. 1996. Changes in structure of starch and enzyme activities affected by sugary mutations. Possible role of starch debranching enzyme (R-enzyme) in amylopectin biosynthesis. Physiol Plant. 97:491-98
82. Nelson OE, Rines HW. 1962. The enzymatic deficiency in the waxy mutant of maize. Biochem. Biophys. Res. Commun. 9:297-300
83. Neuhaus HE, Emes MJ. 2000. Nonphotosynthetic metabolism in plastids. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51:111-40
84. Pan O, Nelson OE. 1984. A debranching enzyme deficiency in endosperms of the sugary-1 mutants of maize. Plant Physiol. 74:324-28
85. Preiss J, Romeo T. 1989. Physiology, biochemistry and genetics of bacterial glycogen synthesis. Adv. Microb. Physiol. 30:183-238
86. Preiss J, Romeo T. 1994. Molecular biology and regulatory aspects of glycogen biosynthesis in bacteria. Prog. Nucleic Acid Res. Mol. Biol. 47:299-329
87. Preiss J, Sivak MN. 1998. Biochemistry, molecular biology and regulation of starch synthesis. Genet. Eng. 20:177-223
88. Raha M, Kawagishi I, Muller V, Kihara M, Macnab RM. 1992. Escherichia coli produces a cytoplasmic alpha-amylase, AmyA. J. Bacteriol. 174:6644-52
89. Rahman A, Wong K-S, Jane J-L, Myers AM, James MG. 1998. Characterization of SU1 isoamylase, a determinant of storage starch structure in maize. Plant Physiol. 117:425-35
90. Rahman S, Regina A, Li ZY, Mukai Y, Yamamoto M, 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. 125:1314-24
91. Recondo E, Leloir L. 1961. Adenosine diphosphate glucose and starch biosynthesis. Biochem. Biophys. Res. Commun. 6:85-88
92. Renz A, Schikora S, Schmid R, Kossmann J, Beck E 1998. cDNA sequence and heterologous expression of monomeric spinach pullulanase: multiple isomeric forms arise from the same polypeptide. Biochem. J. 331:937-45
93. Roach PJ, Cheng C, Huang D, Lin A, Mu J, et al. 1998. Novel aspects of the regulation of glycogen storage. J. Basic Clin. Physiol. Pharmacol. 9:139-51
94. Schindler I, Renz A, Schmid FX, Beck E. 2001. Activation of spinach pullulanase by reduction results in a decrease in the number of isomeric forms. Biochim. Biophys. Acta 1548:175-86
95. Schwall GP, Safford R, Westcott RJ, Jeffcoat R, Tayal A, et al. 2000. Production of very-high-amylose potato starch by inhibition of SBE A and B. Nat. Biotechnol. 18:551-54
96. Seo BS, Kim S, Scott MP, Singletary GW, Wong KS, et al. 2002. Functional interactions between heterologously expressed starch-branching enzymes of maize and the glycogen Synthases of brewer's yeast. Plant Physiol. 128:1189-99
97. Seok YJ, Koo BM, Sondej M, Peterkofsky A. 2001. Regulation of E. coli glycogen phosphorylase activity by HPr. J. Mol. Microbiol. Biotechnol. 3:385-93
98. Singh DG, Lomako J, Lomako WM, Whelan WJ, Meyer HE, et al. 1995. β-glucosylarginine: a new glucose-protein bond in a self-glucosylating protein from sweet corn. FEBS Lett. 376:61-64
99. Smith AM, Denyer K, Martin C. 1997. The synthesis of the starch granule. Annu. Rev. Plant. Physiol. Plant Mol. Biol. 48:67-87
100. Takeda Y, Guan HP, Preiss J. 1993. Branching of amylose by the branching enzymes of maize endosperm. Carbohydr. Res. 240:253-63
101. Teste MA, Enjalbert B, Parrou JL, Francois JM. 2000. The Saccharomyces cerevisiae YPR184w gene encodes the glycogen debranching enzyme. FEMS Microbiol. Lett. 193:105-10
102. Tiessen A, Hendriks JHM, Stitt M, Branscheid A, Gibon Y, et al. 2002. Starch synthesis in potato tubers is regulated by post-translational redox modification of ADPglucose pyrophosphorylase: a novel regulatory mechanism linking starch synthesis to the sucrose supply. Plant Cell 14:2191-213
103. Thorbjornsen T, Villand P, Denyer K, Olsen OA, Smith AM. 1996. Distinct isoforms of ADPglucose pyrophosphorylase occur inside and outside the amyloplasts in barley endosperm. Plant J. 10:243-50
104. Umemoto T, Yano M, Satoh H, Shomura A, Nakamura Y. 2002. Mapping of a gene responsible for the difference in amylopectin structure between japonica-type and indica-type rice varieties. Theor. Appl. Genet. 104:1-8
105. Van den Koornhuyse N, Libessart N, Delrue B, Zabawinski C, Decq A, et al. 1996. Control of starch composition and structure through substrate supply in the monocellular alga Chlamydomonas reinhardtii. J. Biol. Chem. 271:16281-88
106. van de Wal M, D'Hulst C, Vincken J-P, Buléon A, Visser R, Ball S. 1998. Amylose is synthesized in vitro by extension of and cleavage from amylopectin. J. Biol. Chem. 273:22232-40
107. Viola R, Nyvall P, Pedersen M. 2001. The unique features of starch metabolism in red algae. Proc. R. Soc. London Ser. B 268:1417-22
108. 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. 122:255-63
109. Wattebled F, Buléon A, Bouchet B, Gallant D, Decq A, et al. 2002. Granule-bound starch synthase: a major enzyme involved in the biogenesis of B-crystallites in starch granules. Eur. J. Biochem. 26:3810-20
110. Wu C, Colleoni C, Myers AM, James MG. 2002. Enzymatic properties and regulation of ZPU1, the maize pullulanase-type starch debranching enzyme. Arch. Biochem. Biophys. 406:21-32
111. Yamamori M, Fujita S, Hayakawa K, Matsuki J, Yasui T. 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
112. Zabawinski C, Van den Koornhuyse N, D'Hulst C, Slichting R, Decq A, et al. 2001. Starchless mutants of Chlamydomonas reinhardtii lack the small subunit of an heterotetrameric ADPglucose pyrophosphorylase. J. Bacteriol. 183:1069-77
113. Zeeman SC, Umemoto T, Lue WL, Au-Yeung P, Martin C, et al. 1998. A mutant of Arabidopsis lacking a chloroplastic isoamylase accumulates both starch and phytoglycogen. Plant Cell 10:1699-712