A Model for the Reproduction of Amylopectin Cluster by Coordinated Actions of Starch Branching Enzyme Isoforms

Overview

Journal Plant Mol Biol

Date 2023 Jun 9

PMID 37294528

Authors

Yasunori Nakamura

Affiliations

Soon will be listed here.

Abstract

Amylopectin is a highly branched glucan which accounts for approximately 65-85% of starch in most plant tissues. It is crucially important to understand the biosynthetic process of this glucan in regulating the structure and functional properties of starch granules. Currently, the most accepted ideas of structural feature and biosynthesis of amylopectin are that amylopectin is composed of a branched element called "cluster" and that the essential process of amylopectin biosynthesis is to reproduce a new cluster from the existing cluster. The present paper proposes a model explaining the whole process of amylopectin biosynthesis as to how the new cluster is reproduced by concerted actions of multiple isoforms of starch biosynthetic enzymes, particularly by combinations of distinct roles of starch branching enzyme (BE) isoforms. This model proposes for the first time the molecular mechanism as to how the formation of a new cluster is initiated, and the reason why BEI can play a major role in this step. This is because BEI has a rather broad chain-length preference compared to BEIIb, because a low preference of BEI for the substrate chain-length is advantageous for branching a couple of elongated chains that are not synchronously formed and thus these chains having varied lengths could be safely attacked by this isoform. On the contrary, it is unlikely that BEIIb is involved in this reaction because it can react to only short chains having degree of polymerization of 12-14. BEIIa is possibly able to complement the role of BEI to some extent, because BEIIa can attack basically short chains but its chain-length preference is lower compared with BEIIb. The model implies that the first branches mainly formed by BEI to construct the amorphous lamellae whereas the second branches predominantly formed by BEIIb are located mainly in the crystalline lamellae. This paper provides new insights into the roles of BEI, BEIIb, and BEIIa in amylopectin biosynthesis in cereal endosperm.

Citing Articles

Characterization of Med1 LxxLL Motif Involved in Fumonisin Biosynthesis.

Zhou Z, Liu J, Zhang J, Yan H, Yi T, Shim W Toxins (Basel). 2023; 15(11).

PMID: 37999515 PMC: 10675092. DOI: 10.3390/toxins15110652.

References

Ball S, Guan H, James M, Myers A, Keeling P, Mouille G . From glycogen to amylopectin: a model for the biogenesis of the plant starch granule. Cell. 1996; 86(3):349-52. DOI: 10.1016/s0092-8674(00)80107-5. View

Borovsky D, Smith E, WHELAN W . Temperature-independence of the action of Q-enzyme and the nature of the substrate for Q-enzyme. FEBS Lett. 1975; 54(2):201-5. DOI: 10.1016/0014-5793(75)80074-3. View

Borovsky D, Smith E, WHELAN W . On the mechanism of amylose branching by potato Q-enzyme. Eur J Biochem. 1976; 62(2):307-12. DOI: 10.1111/j.1432-1033.1976.tb10162.x. View

Borovsky D, Smith E, WHELAN W, French D, Kikumoto S . The mechanism of Q-enzyme action and its influence on the structure of amylopectin. Arch Biochem Biophys. 1979; 198(2):627-31. DOI: 10.1016/0003-9861(79)90540-x. View

Buleon A, Colonna P, Planchot V, Ball S . Starch granules: structure and biosynthesis. Int J Biol Macromol. 1998; 23(2):85-112. DOI: 10.1016/s0141-8130(98)00040-3. View

Chanzy H, Putaux J, Dupeyre D, Davies R, Burghammer M, Montanari S . Morphological and structural aspects of the giant starch granules from Phajus grandifolius. J Struct Biol. 2006; 154(1):100-10. DOI: 10.1016/j.jsb.2005.11.007. View

Commuri P, Keeling P . Chain-length specificities of maize starch synthase I enzyme: studies of glucan affinity and catalytic properties. Plant J. 2001; 25(5):475-86. DOI: 10.1046/j.1365-313x.2001.00955.x. View

Crini G, French A, Kainuma K, Jane J, Szente L . Contributions of Dexter French (1918-1981) to cycloamylose/cyclodextrin and starch science. Carbohydr Polym. 2021; 257:117620. DOI: 10.1016/j.carbpol.2021.117620. View

Crofts N, Abe N, Oitome N, Matsushima R, Hayashi M, Tetlow I . Amylopectin biosynthetic enzymes from developing rice seed form enzymatically active protein complexes. J Exp Bot. 2015; 66(15):4469-82. PMC: 4507757. DOI: 10.1093/jxb/erv212. View

10.

Crofts N, Nakamura Y, Fujita N . Critical and speculative review of the roles of multi-protein complexes in starch biosynthesis in cereals. Plant Sci. 2017; 262:1-8. DOI: 10.1016/j.plantsci.2017.05.007. View

11.

Crofts N, Satoh Y, Miura S, Hosaka Y, Abe M, Fujita N . Active-type starch synthase (SS) IIa from indica rice partially complements the sugary-1 phenotype in japonica rice endosperm. Plant Mol Biol. 2021; 108(4-5):325-342. DOI: 10.1007/s11103-021-01161-9. View

12.

Cuesta-Seijo J, Nielsen M, Ruzanski C, Krucewicz K, Beeren S, Rydhal M . In vitro Biochemical Characterization of All Barley Endosperm Starch Synthases. Front Plant Sci. 2016; 6:1265. PMC: 4730117. DOI: 10.3389/fpls.2015.01265. View

13.

Fujita N, Yoshida M, Asakura N, Ohdan T, Miyao A, Hirochika H . Function and characterization of starch synthase I using mutants in rice. Plant Physiol. 2006; 140(3):1070-84. PMC: 1400558. DOI: 10.1104/pp.105.071845. View

14.

Fujita N, Yoshida M, Kondo T, Saito K, Utsumi Y, Tokunaga T . Characterization of SSIIIa-deficient mutants of rice: the function of SSIIIa and pleiotropic effects by SSIIIa deficiency in the rice endosperm. Plant Physiol. 2007; 144(4):2009-23. PMC: 1949899. DOI: 10.1104/pp.107.102533. View

15.

Gavgani H, Fawaz R, Ehyaei N, Walls D, Pawlowski K, Fulgos R . A structural explanation for the mechanism and specificity of plant branching enzymes I and IIb. J Biol Chem. 2021; 298(1):101395. PMC: 8695356. DOI: 10.1016/j.jbc.2021.101395. View

16.

Guan H, Li P, Preiss J, Keeling P . Comparing the properties of Escherichia coli branching enzyme and maize branching enzyme. Arch Biochem Biophys. 1997; 342(1):92-8. DOI: 10.1006/abbi.1997.0115. View

17.

Hayashi M, Suzuki R, Colleoni C, Ball S, Fujita N, Suzuki E . Bound Substrate in the Structure of Cyanobacterial Branching Enzyme Supports a New Mechanistic Model. J Biol Chem. 2017; 292(13):5465-5475. PMC: 5392689. DOI: 10.1074/jbc.M116.755629. View

18.

Imberty A, Chanzy H, Perez S, Buleon A, Tran V . The double-helical nature of the crystalline part of A-starch. J Mol Biol. 1988; 201(2):365-78. DOI: 10.1016/0022-2836(88)90144-1. View

19.

Liu F, Makhmoudova A, Lee E, Wait R, Emes M, Tetlow I . The amylose extender mutant of maize conditions novel protein-protein interactions between starch biosynthetic enzymes in amyloplasts. J Exp Bot. 2009; 60(15):4423-40. DOI: 10.1093/jxb/erp297. View

20.

Liu F, Romanova N, Lee E, Ahmed R, Evans M, Gilbert E . Glucan affinity of starch synthase IIa determines binding of starch synthase I and starch-branching enzyme IIb to starch granules. Biochem J. 2012; 448(3):373-87. DOI: 10.1042/BJ20120573. View