A review of starch-branching enzymes and their role in amylopectin biosynthesis

IUBMB Life

Volumn 66, Issue 8, 2014, Pages 546-558

  Tetlow, Ian J ^a   Emes, Michael J ^a  

^a UNIVERSITY OF GUELPH   (Canada)

Author keywords

amylopectin; amylose; branching enzyme; glycoside hydrolase family; polyglucan; protein complexes; protein phosphorylation; starch; starch synthesis; starch branching enzyme

Indexed keywords

1,4 ALPHA GLUCAN BRANCHING ENZYME; AMYLOPECTIN; ISOPROTEIN; MULTIPROTEIN COMPLEX;

BIOSYNTHESIS; COMPARATIVE STUDY; ENZYMOLOGY; GENETICS; METABOLISM; MOLECULAR EVOLUTION; PHOSPHORYLATION; PHYLOGENY; PLANT; PROTEIN TERTIARY STRUCTURE; SPECIES DIFFERENCE;

1,4-ALPHA-GLUCAN BRANCHING ENZYME; AMYLOPECTIN; EVOLUTION, MOLECULAR; MULTIPROTEIN COMPLEXES; PHOSPHORYLATION; PHYLOGENY; PLANTS; PROTEIN ISOFORMS; PROTEIN STRUCTURE, TERTIARY; SPECIES SPECIFICITY;

EID: 84930146241     PISSN: 15216543     EISSN: 15216551     Source Type: Journal    
DOI: 10.1002/iub.1297     Document Type: Review

References (70)

1. Leloir, L. F., (1971) Two decades of research on the biosynthesis of saccharides. Science 172, 1299-1303.
2. Haworth, W. N., Peat, S., and, Bourne, E. J., (1944) Synthesis of amylopectin. Nature (Lond.) 154, 236-238.
3. Barker, S. A., and, Bourne, E. J., (1951) Enzymic synthesis of polysaccharides. Q. Rev. 5, 56-83.
4. Borovsky, D., Smith, E. E., and, Whelan, W. J., (1976) On the mechanism of amylose branching by potato Q-enzyme. Eur. J. Biochem. 62, 307-312.
5. Borovsky, D., Smith, E. E., Whelan, W. J., French, D., and, Kikumoto, S., (1979) The mechanism of Q-enzyme action and its influence on the structure of amylopectin. Arch. Biochem. Biophys. 198, 627-631.
6. Hawker, J. S., Ozbun, H., Ozaki, E., Greenberg, E., and, Preiss, J., (1974) Interaction of spinach leaf adenosine diphosphate glucose α-1,4-glucan α-4-glucosyl transferase and α-1,4-glucan, α-1,4-glucan-6-glycosyl transferase in synthesis of branched α-glucan. Arch. Biochem. Biophys. 160, 530-551.
7. Tetlow, I. J., Wait, R., Lu, Z., Akkasaeng, R., Bowsher, C. G., et al. (2004) Protein phosphorylation in amyloplasts regulates starch branching enzyme activity and protein-protein interactions. Plant Cell 16, 694-708.
8. Liu, F., Makhmoudova, A., Lee, E. A., Wait, R., Emes, M. J., et al. (2009) The amylose extender mutant of maize conditions novel protein-protein interactions between starch biosynthetic enzymes in amyloplasts. J. Exp. Bot. 60, 4423-4440.
9. Tetlow, I. J., Beisel, K. G., Cameron, S., Makhmoudova, A., Liu, F., et al. (2008) Analysis of protein complexes in amyloplasts reveals functional interactions among starch biosynthetic enzymes. Plant Physiol. 146, 1878-1891.
10. Glaring, M. A., Skryhan, K., Kötting, O., Zeeman, S. C., and, Blennow, A., (2012) A comprehensive survey of redox sensitive starch metabolising enzymes in Arabidopsis thaliana. Plant Physiol. Biochem. 58, 89-97.
11. Takeda, Y., Guan, H.-P., and, Preiss, J., (1993) Branching of amylose by the branching isoenzymes of maize endosperm. Carbohydr. Res. 240, 253-263.
12. Kuriki, T., Stewart, D. C., and, Preiss, J., (1997) Construction of chimeric enzymes out of maize endosperm branching enzymes I and II: Activity and properties. J. Biol. Chem. 272, 28999-29004.
13. Guan, H., Kuriki, T., Sivak, M., and, Preiss, J., (1997) Maize branching enzyme catalyzes synthesis of glycogen-like polysaccharide in glgB-deficient Escherichia coli. Proc. Natl. Acad. Sci. USA 92, 964-967.
14. Makhmoudova, A., Williams, D., Brewer, D., Massey, S., Patterson, J., 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.
15. Nakamura, Y., Utsumi, Y., Sawada, T., Aihara, S., Utsumi, C., et al. (2010) Characterization of the reactions of starch branching enzymes from rice endosperm. Plant Cell Physiol. 51, 776-794.
16. Mizuno, K., Kawasaki, T., Shimada, H., Satoh, H., Kobayashi, E., 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.
17. Liu, F., Romanova, N., Lee, E. A., Ahmed, R., Evans, M., et al. (2012) 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.
18. Sawada, T., Francisco, P. B., Jr., Aihara, S., Utsumi, Y., Yoshida, M., et al. (2009) Chlorella starch branching enzyme II (BEII) can complement the function of BEIIb in rice endosperm. Plant Cell Physiol. 50, 1062-1074.
19. Nakamura, Y., Ono, M., Utsumi, C., and, Steup, M., (2012) Functional interaction between plastidial starch phosphorylase and starch branching enzymes from rice during the synthesis of branched maltodextrins. Plant Cell Physiol. 53, 869-878.
20. Morell, M. K., Blennow, A., Kosar-Hashemi, B., and, Samuel, M. S., (1997) Differential expression and properties of starch branching enzyme isoforms in developing wheat endosperm. Plant Physiol. 113, 201-208.
21. Alexander, R. D., and, Morris, P. C., (2006) A proteomic analysis of 14-3-3 binding proteins from developing barley grains. Proteomics 6, 1886-1896.
22. Sun, C., Sathish, P., Ahlandsberg, S., and, Jansson, C., (1998) The two genes encoding starch-branching enzymes IIa and IIb are differentially expressed in barley. Plant Physiol. 118, 37-49.
23. Subasinghe, R. M., Liu, F., Polack, U. C., Lee, E. A., Emes, M. J., et al. Multimeric states of starch phosphorylase determine protein-protein interactions with starch biosynthetic enzymes in maize endosperm amyloplasts. Plant Physiol. Biochem. 83, 168-179.
24. Mizuno, K., Kobayashi, E., Tachibana, M., Kawasaki, T., Fujimura, T., et al. (2001) Characterization of an isoform of rice starch branching enzyme, RBE4, in developing seeds. Plant Cell Physiol. 42, 349-357.
25. Vos-Scheperkeuter, G. H., De Wit, J. G., Ponstein, A. S., Feenstra, W. J., and, Witholt, B., (1989) Immunological comparison of the starch branching enzymes from potato tubers and maize kernels. Plant Physiol. 90, 75-84.
26. Nozaki, K., Hamada, S., Nakamori, T., Ito, H., Sagisaka, S., et al. (2001) Major isoforms of starch branching enzymes in premature seeds of kidney bean (Phaseolus vulgaris L.). Biosci. Biotechnol. Biochem. 65, 1141-1148.
27. Hamada, S., Ito, H., Hiraga, S., Inagaki, K., Nozaki, K., 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.
28. Seo, B.-S., Kim, S., Scott, M. P., Singletary, G. W., Wong, K.-S., et al. (2002) Functional interactions between heterologously expressed starch-branching enzymes of maize and glycogen synthases of brewer's yeast. Plant Physiol. 128, 1189-1199.
29. Guan, H.-P., and, Preiss, J., (1993) Differentiation of the properties of the branching isozymes from maize (Zea mays). Plant Physiol. 102, 1269-1273.
30. Rydberg, U., Andersson, L., Andersson, R., Åman, P., and, Larsson, H., (2001) Comparison of starch branching enzyme I and II from potato. Eur. J. Biochem. 268, 6140-6145.
31. Hizukuri, S., (1986) Polymodal distribution of the chain lengths of amylopectin, and its significance. Carbohydr. Res. 147, 342-347.
32. Bertoft, E., and, Seetharaman, K., (2012) Starch structure. In Starch: Origins, Structure and Metabolism (, Tetlow, I. J., ed.). pp. 1-28, Society for Experimental Biology, London, Great Britain.
33. Tetlow, I. J., (2011) Starch biosynthesis in developing seeds. Seed Sci. Res. 21, 5-32.
34. Wolfe, K. H., Gouy, M., Yang, Y. W., Sharp, P. M., and, Li, W. H., (1989) Date of the monocot-dicot divergence estimated from chloroplast DNA sequence data. Proc. Natl. Acad. Sci. USA 86, 6201-6205.
35. Gao, M., Fisher, D. K., Kim, K.-N., Shannon, J. C., and, Guiltinan, M. J., (1997) Independent genetic control of maize starch-branching enzymes IIa and IIb. Plant Physiol. 114, 69-78.
36. Regina, A., Kosar-Hashemi, B., Li, Z., Pedler, A., Mukai, Y., 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.
37. Blauth, S. L., Yao, Y., Klucinec, J. D., Shannon, J. C., Thompson, D. B., et al. (2001) Identification of Mutator insertional mutants of starch-branching enzyme 2a in corn. Plant Physiol. 125, 1396-1405.
38. Yandeau-Nelson, M. D., Laurens, L., Shi, Z., Xia, H., Smith, A. M., et al. (2011) Starch-branching enzyme IIa is required for proper diurnal cycling of starch in leaves of maize. Plant Physiol. 156, 479-490.
39. Bhattacharyya, M. K., Smith, A. M., Ellis, T. H. N., Hedley, C., and, Martin, C., (1990) The wrinkle-seeded character of peas described by Mendel is caused by a transposon-like insertion in a gene encoding starch branching enzyme. Cell 60, 115-122.
40. Banks, W., Greenwood, C. T., and, Muir, D. D., (1974) Studies on starches of high amylose content, Part 17: A review of current concepts. Starch 26, 289-300.
41. Hilbert, G. E., and, MacMasters, M. M., (1946) Pea starch, a starch of high amylose content. J. Biol. Chem. 162, 229-238.
42. Boyer, C. D., Daniels, R. R., and, Shannon, J. C., (1976) Abnormal starch granule formation in Zea mays L. endosperms possessing the amylose-extender mutant. Crop Sci. 16, 298-301.
43. Regina, A., Li, Z., Bird, A., Topping, D., Bowden, S., et al. (2006) High-amylose wheat generated by RNA interference improves indices of large-bowel health in rats. Proc. Natl. Acad. Sci. USA 103, 3546-3551.
44. Schwall, G. P., Safford, R., Westcott, R. J., Jeffcoat, R., Tayal, A., et al. (2000) Production of very-high-amylose potato starch by inhibition of SBE A and B. Nat. Biotechnol. 18, 551-554.
45. Blauth, S. L., Kim, K. N., Klucinec, J., Shannon, J. C., Thompson, D. B., et al. (2002) Identification of Mutator insertional mutants of starch-branching enzyme 1 (sbe1) in Zea mays L. Plant Mol. Biol. 48, 287-297.
46. Yao, Y., Thompson, D. B., and, Guiltinan, M. J., (2004) Maize starch-branching enzyme isoforms and amylopectin structure. In the absence of starch-branching enzyme IIb, the further absence of starch-branching enzyme Ia leads to increased branching. Plant Physiol. 136, 3515-3523.
47. Fisher, D. K., Gao, M., Kim, K.-N., Boyer, C. D., and, Guiltinan, M. J., (1996) Two closely related cDNAs encoding starch branching enzyme from Arabidopsis thaliana. Plant Mol. Biol. 30, 97-108.
48. Dumez, S., Wattebled, F., Dauvillée, D., Delvallé, D., Planchot, V., et al. (2006) Mutants of Arabidopsis lacking starch branching enzyme II substitute plastidial starch synthesis by cytoplasmic maltose accumulation. Plant Cell 18, 2694-2709.
49. Denyer, K., Sidebottom, C., Hylton, C. M., and, Smith, A. M., (1993) Soluble isoforms of starch synthase and starch-branching enzyme also occur within starch granules in developing pea embryos. Plant J. 4, 191-198.
50. Mu-Forster, C., Huang, R., Powers, J. R., Harriman, R. W., Knight, M., et al. (1996) Physical association of starch biosynthetic enzymes with starch granules of maize endosperm. Granule-associated forms of starch synthase I and starch branching enzyme II. Plant Physiol. 111, 821-829.
51. Grimaud, F., Rogniaux, H., James, M. G., Myers, A. M., and, Planchot, V., (2008) Proteome and phosphoproteome analysis of starch granule associated proteins from normal maize and mutants affected in starch biosynthesis. J. Exp. Bot. 59, 3395-3406.
52. Peng, M., Gao, M., Båga, M., Hucl, P., and, Chibbar, R. N., (2000) Starch-branching enzymes preferentially associated with A-type starch granules in wheat endosperm. Plant Physiol. 124, 265-272.
53. Liu, F., Ahmed, Z., Lee, E. A., Weber, E., Liu, Q., 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.
54. Guan, H., Li, P., and, Keeling, P. L., (1998) Starch biosynthesis: understanding the functions and interactions of multiple isozymes of starch synthase and branching enzyme. Trends Glycosci. Glycotechnol. 10, 307-319.
55. Xia, H., Yandeau-Nelson, M., Thompson, D. B., and, Guiltinan, M. J., (2011) Deficiency of maize starch-branching enzyme I results in altered fine structure, decreased digestibility and reduced coleoptile growth during germination. BMC Plant Biol. 11, 95.
56. Tanaka, N., Fujita, N., Nishi, A., Satoh, H., Hosaka, Y., et al. (2004) The structure of starch can be manipulated by changing the expression levels of starch branching enzyme IIb in rice endosperm. Plant Biotechnol. J. 2, 507-516.
57. Robin, J. P., Mercier, C., Charbonniere, R., and, Guilbot, A., (1974) Lintnerized starches: gel filtration and enzymatic studies of insoluble residues from prolonged acid treatment of potato starch. Cereal Chem. 51, 389-406.
58. MacGregor, E. A., Janacek, S., and, Svensson, B., (2001) Relationship of sequence and structure to specificity in the α-amylase family of enzymes. Biochim. Biophys. Acta 1546, 1-20.
59. Abad, M., Binderup, K., Rios-Steiner, K., Arni, R., Preiss, J., et al. (2002) The X-ray crystallographic structure of Escherichia coli branching enzyme. J. Biol. Chem. 277, 42164-42170.
60. Libessart, N., and, Preiss, J., (1998) Arginine residue 384 at the catalytic center is important for branching enzyme II from maize endosperm. Arch. Biochem. Biophys. 360, 135-141.
61. Noguchi, J., Chaen, K., Vu, N. T., Akasaka, T., Shimada, H., 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.
62. Palomo, M., Pijning, T., Booiman, T., Dobruchowska, J. M., van der Vlist, J., et al. (2011) Thermus thermophilus glycoside hydrolase family 57 branching enzyme: crystal structure, mechanism of action, and products formed. J. Biol. Chem. 286, 3520-3530.
63. Binderup, K., Mikkelsen, R., and, Preiss, J., (2000) Truncation of the amino terminus of branching enzyme changes its chain transfer pattern. Arch. Biochem. Biophys. 397, 279-285.
64. Kuriki, T., Guan, H. P., Sivak, M., and, Preiss, J., (1996) Analysis of the active center of branching enzyme II from maize endosperm. J. Protein Chem. 15, 305-313.
65. Funane, K., Libessart, N., Stewart, D., Michishita, T., and, Preiss, J., (1998) Analysis of essential histidine residues of maize branching enzymes by chemical modification and site-directed mutagenesis. J. Protein Chem. 17, 579-590.
66. 8-barrel domain and evolutionary relationship to other amylolytic enzymes. J. Protein Chem. 12, 791-805.
67. Hong, S., and, Preiss, J., (2000) Localization of C-terminal domains required for the maximal activity or for the determination of substrate preference of maize branching enzymes. Arch. Biochem. Biophys. 378, 349-355.
68. Hennen-Bierwagen, T. A., Liu, F., Marsh, R. S., Kim, S., Gan, Q., et al. (2008) Starch biosynthetic enzymes from developing Zea mays endosperm associate in multisubunit complexes. Plant Physiol. 146, 1892-1908.
69. Hennen-Bierwagen, T. A., Lin, Q., Grimaud, F., Planchot, V., Keeling, P. L., 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.
70. Walley, J. W., Shen, Z., Sartor, R., Wu, K., Osbom, J., et al. (2013) Reconstruction of protein networks from an atlas of maize seed proteotypes. Proc. Natl. Acad. Sci. 110, 4808-4817.