Protein-protein interactions among enzymes of starch biosynthesis in high-amylose barley genotypes reveal differential roles of heteromeric enzyme complexes in the synthesis of A and B granules

Plant Science

Volumn 233, Issue , 2015, Pages 95-106

  Ahmed, Zaheer ^a   Tetlow, Ian J ^a   Ahmed, Regina ^b   Morell, Matthew K ^c   Emes, Michael J ^a  

^a UNIVERSITY OF GUELPH   (Canada)

^b CSIRO   (Australia)

^c INTERNATIONAL RICE RESEARCH INSTITUTE   (Philippines)

Author keywords

A and B granules; Barley; Enzyme complexes; Starch biosynthesis

Indexed keywords

HORDEUM;

MULTIENZYME COMPLEX; PROTEOME; STARCH; VEGETABLE PROTEIN;

BIOSYNTHESIS; DOWN REGULATION; ELECTRON MICROSCOPY; ENZYMOLOGY; GENETICS; HORDEUM; METABOLISM; MUTATION; PHOSPHORYLATION; ULTRASTRUCTURE;

DOWN-REGULATION; HORDEUM; MICROSCOPY, ELECTRON; MULTIENZYME COMPLEXES; MUTATION; PHOSPHORYLATION; PLANT PROTEINS; PROTEOME; STARCH;

EID: 84921684619     PISSN: 01689452     EISSN: 18732259     Source Type: Journal    
DOI: 10.1016/j.plantsci.2014.12.016     Document Type: Article

References (47)

1. Keeling P.L., Myers A.M. Biochemistry and genetics of starch synthesis. Annu. Rev. Food Sci. Technol. 2010, 1:271-303.
2. James M.G., Denyer K., Myers A.M. Starch synthesis in the cereal endosperm. Curr. Opin. Plant Biol. 2003, 6:215-222.
3. Bechtel D.B., Zayas I., Kaleikau L., Pomeranz Y. Size-distribution of wheat starch granules during endosperm development. Cereal Chem. 1990, 67:59-63.
4. Bechtel D.B., Wilson J.D. Amyloplast formation and starch granule development in hard red winter wheat. Cereal Chem. 2003, 80:175-183.
5. Evers A.D. The size distribution among starch granules in wheat endosperm. Starch - Stärke 1973, 25:303-304.
6. Wilson J.D., Bechtel D.B., Todd T.C., Seib P.A. Measurement of wheat starch granules. Size distribution using image analysis and laser diffraction technology. Cereal Chem. 2006, 83:259-268.
7. Langeveld S.M., van Wijk R., Stuurman N., Kijne J.W., de Pater S. B-type granule containing protrusions and interconnections between amyloplasts in developing wheat endosperm revealed by transmission electron microscopy and GFP expression. J. Exp. Bot. 2000, 51:1357-1361.
8. Wei C., Zhang J., Chen Y., Zhou W., Xu B., Wang Y., et al. Physicochemical properties and development of wheat large and small starch granules during endosperm development. Acta Physiol. Plant. 2010, 32:905-916.
9. Ball S.G., Morell M.K. From bacterial glycogen to starch: understanding the biogenesis of the plant starch granule. Annu. Rev. Plant Biol. 2003, 54:207-233.
10. James M.G., Robertson D.S., Myers A.M. Characterization of the maize gene sugary 1, a determinant of starch composition in kernels. Plant Cell. 1995, 7:417-429.
11. Leterrier M., Holappa L.D., Broglie K.E., Beckles D.M. Cloning, characterisation and comparative analysis of a starch synthase IV gene in wheat: functional and evolutionary implications. BMC Plant Biol. 2008, 8:98.
12. Patron N.J., Keeling P.J. Common evolutionary origin of starch biosynthetic enzymes in green and red algae. J. Phycol. 2005, 41:1131-1141.
13. Tsai C.Y., Nelson O.E. Mutations at the shrunken-4 locus in maize that produce three altered phosphorylases. Genetics 1969, 61:813-821.
14. Tetlow I.J. Starch biosynthesis in developing seeds. Seed Sci. Res. 2011, 21:5-32.
15. Hennen-Bierwagen T.A., Liu F., Marsh R.S., Kim S., Gan Q., Tetlow I.J., et al. Starch biosynthetic enzymes from developing maize endosperm associate in multisubunit complexes. Plant Physiol. 2008, 146:1892-1908.
16. Liu F., Makhmoudova A., Lee E.A., Wait R., Emes M.J., Tetlow I.J. The amylose extender mutant of maize conditions novel protein-protein interactions between starch biosynthetic enzymes in amyloplasts. J. Exp. Bot. 2009, 60:4423-4440.
17. Liu F., Ahmed Z., Lee E.A., Donner E., Liu Q., Ahmed R., et al. Allelic variants of the amylose extender mutation of maize demonstrate phenotypic variation in starch structure resulting from modified protein-protein interactions. J. Exp. Bot. 2012, 63:1167-1183.
18. Tetlow I.J., Beisel K.G., Cameron S., Makhmoudova A., Liu F., Bresolin N.S., et al. Analysis of protein complexes in wheat amyloplasts reveals functional interactions among starch biosynthetic enzymes. Plant Physiol. 2008, 146:1878-1891.
19. Bancel E., Rogniaux H., Debiton C., Chambon C., Branlard G., Extraction proteome analysis of starch granule-associated proteins in mature wheat kernel (Triticum aestivum L.). J. Proteome Res. 2010, 9:3299-3310.
20. Tetlow I.J., Wait R., Lu Z., Akkasaeng R., Bowsher C.G., Esposito S., et al. Protein phosphorylation in amyloplasts regulates starch branching enzyme activity and protein-protein interactions. Plant Cell. 2004, 16:694-708.
21. Tetlow I.J., Liu F., Emes M.J. Functional interactions between starch synthases and branching enzymes of cereal endosperms. Comp. Biochem. Physiol. 2008, 150:S194-S195.
22. Hennen-Bierwagen T.A., Lin Q., Grimaud F., Planchot V., Keeling P.L., James M.G., et al. 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. 2009, 149:1541-1559.
23. Liu F., Romanova N., Lee E.A., Ahmed R., Evans M., Gilbert E.P., et al. Glucan affinity of starch synthase IIa determines binding of starch synthase I and starch-branching enzyme IIb to starch granules. Biochem. J. 2012, 448:373-387.
24. Regina A., Kosar-Hashemi B., Ling S., Li Z., Rahman S., Morell M. Control of starch branching in barley defined through differential RNAi suppression of starch branching enzyme IIa and IIb. J. Exp. Bot. 2010, 61:1469-1482.
25. Morell M.K., Kosar-Hashemi B., Cmiel M., Samuel M.S., Chandler P., Rahman S., et al. Barley sex6 mutants lack starch synthase IIa activity and contain a starch with novel properties. Plant J. 2003, 34:173-185.
26. Banks W., Greenwood C.T., Muir D.D. The characterization of starch and its components. Starch - Stärke 1971, 4:118-124.
27. Peng M., Gao M., Abdel-Aal E.-S.M., Hucl P., Chibbar R.N. Separation and characterization of A- and B-type starch granules in wheat endosperm. Cereal Chem. 1999, 76:375-379.
28. Tetlow I.J., Davies E.J., Vardy K.A., Bowsher C.G., Burrell M.M., Emes M.J. Subcellular localization of ADPglucose pyrophosphorylase in developing wheat endosperm and analysis of the properties of a plastidial isoform. J. Exp. Bot. 2003, 54:715-725.
29. Deeg R., Kraemer W., Ziegenhorn J. Kinetic determination of serum glucose by use of the hexokinase/glucose-6-phosphate dehydrogenase method. J. Clin. Chem. Clin. Biochem. 1980, 18:49-52.
30. Li Z., Rahman S., Kosar-Hashemi B., Mouille G., Appels R., Morell M.K. Cloning and characterization of a gene encoding wheat starch synthase I. Theoretical Appl. Genet. 1999, 98:1208-1216.
31. Rahman S., Regina A., Li Z., Mukai Y., Yamamoto M., Kosar-Hashemi B., et al. Comparison of starch-branching enzyme genes reveals evolutionary relationships among isoforms. Characterization of a gene for starch-branching enzyme IIa from the wheat genome donor Aegilops tauschii. Plant Physiol. 2001, 125:1314-1324.
32. Regina A., Kosar-Hashemi B., Li Z., Pedler A., Mukai Y., Yamamoto M., et al. 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 2005, 222:899-909.
33. Tetlow I.J., Blissett K.J., Emes M.J. Starch synthesis and carbohydrate oxidation in amyloplasts from developing wheat endosperm. Planta 1994, 194:454-460.
34. Mortz E., Krogh T.N., Vorum H., Görg A. Improved silver staining protocols for high sensitivity protein identification using matrix-assisted laser desorption/ionization-time of flight analysis. Proteomics 2001, 1:1359-1363.
35. Chen M.H., Bergman C.J. Method for determining the amylose content, molecular weights, and weight- and molar-based distributions of degree of polymerization of amylose and fine-structure of amylopectin. Carbohydr. Polym. 2007, 69:562-578.
36. Akerberg A.K.E., Liljeberg H.G.M., Granfeldt Y.E., Drews A.W., Bjorck I.M.E. An in vitro method based on chewing, to predict resistant starch content in foods allows parallel determination of potentially available starch and dietary fiber. J. Nutr. 1998, 128:651-660.
37. Goni I., Garcia-Diz L., Manas E., Saura-Calixto F. Analysis of resistant starch: a method for foods and food products. Food Chem. 1996, 56:445-449.
38. Li Z., Li D., Du X., Wang H., Larroque O., Jenkins C.L.D., et al. 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. 2011, 62:5217-5231.
39. Grimaud F., Rogniaux H., James M.G., Myers A.M., Planchot V., Proteome phosphoproteome analysis of starch granule-associated proteins from normal maize and mutants affected in starch biosynthesis. J. Exp. Bot. 2008, 59:3395-3406.
40. Nishi A., Nakamura Y., Tanaka N., Satoh H. Biochemical and genetic analysis of the effects of amylose-extender mutation in rice endosperm. Plant Physiol. 2001, 127:459-472.
41. Nakamura Y., Ono M., Utsumi C., Steup M. Functional interaction between plastidial starch phosphorylase and starch branching enzymes from rice during the synthesis of branched maltodextrins. Plant Cell Physiol. 2012, 53:869-878.
42. Makhmoudova A., Williams D., Brewer D., Massey S., Patterson J., Silva A., et al. Identification of multiple phosphorylation sites on maize endosperm starch branching enzyme IIb, a key enzyme in amylopectin biosynthesis. J. Biol. Chem. 2014, 289:9233-9246.
43. Peng M., Gao M., Båga M., Hucl P., Chibbar R.N. Starch-branching enzymes preferentially associated with A-type starch granules in wheat endosperm. Plant Physiol. 2000, 124:265-272.
44. Borén M., Larsson H., Falk A., Jansson C. The barley starch granule proteome: internalized granule polypeptides of the mature endosperm. Plant Sci. 2004, 166:617-626.
45. Rahman S., Kosar-Hashemi B., Samuel M., Hill A., Abbott D., Skerritt J., et al. The major proteins of wheat endosperm starch granules. Aust. J. Plant Physiol. 1995, 22:793-803.
46. Umemoto T., Aoki N. Single-nucleotide polymorphisms in rice starch synthase IIa that alter starch gelatinisation and starch association of the enzyme. Funct. Plant Biol. 2005, 32:763-768.
47. Gao M., Fisher D.K., Kim K.N., Shannon J.C., Guiltinan M.J. Evolutionary conservation and expression patterns of maize starch branching enzyme I and IIb genes suggests isoform specialization. Plant Mol. Biol. 1996, 30:1223-1232.