Multiple forms of starch branching enzyme of maize: Evidence for independent genetic control

doi:10.1016/0006-291X(78)91119-1

Biochemical and Biophysical Research Communications

Volume 80, Issue 1, 13 January 1978, Pages 169-175

https://doi.org/10.1016/0006-291X(78)91119-1 Get rights and content

Abstract

Purification of starch branching enzymes from kernels of two nonlinked mutants of maize, $sugary$ and $amylose-extender$ , showed the basis of the two mutations to be associated with branching enzymes I and IIb, respectively. Branching enzyme I from $sugary$ kernels purified as nonmutant branching enzyme I, but had an altered pattern of activity when amylose was used as a substrate. In addition to the typical fall in absorbance at high wavelengths (550–700 nm) of the amylose-iodine complex, branching of amylose by $sugary$ branching enzyme I caused an increase in absorbance at low wavelengths (400–550 nm). Branching enzyme IIb was undetected in extracts of $amylose-extender$ kernels, while branching enzymes I and IIa appeared unaltered. Low umprimed starch synthase activity was also observed in DEAE-cellulose fractions of $amylose-extender$ maize, but this activity was regenerated by the addition of any branching enzyme.

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High-amylose maize starch has great potential for widespread industrial use due to its ability to form strong gels and film and in the food processing field, thus serving as a resistant starch source. However, there is still a substantial shortage of high-amylose maize due to the limitation of natural germplasm resources, although the well-known amylose extender (ae) gene mutants have been found to produce high-amylose maize lines since 1948. In this context, high-amylose maize lines (13 inbreds and 18 hybrids) originating from a natural amylose mutant in our testing field were utilized to study the correlation between amylose content (AC) and phenotypic traits (kernel morphology and endosperm glossiness), grain filling characteristics, gene expression, and amylose inheritance. Our results showed that AC was negatively correlated with total starch content but was not correlated with grain phenotypes, such as kernel fullness, kernel morphology and endosperm glossiness. Maize lines with higher amylose had a greater grain filling rate than that of the control (B73) during the first 20 days after pollination (DAP). Both starch debranching enzyme (DBE) groups and starch branching enzyme IIb (SBEIIb) groups showed a greater abundance in the control (B73) than in the high-amylose maize lines. Male parents directly predicted AC of F₁, which was moderately positively correlated with the F₂ generation.
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This chapter reviews enzymic reactions involved in starch synthesis in higher plants and algae. Existing information on the properties of various starch biosynthetic enzymes in the plant, algal, and cyanobacterial systems will be described and compared. Alteration of starch structure due to the mutational effects on these biosynthetic enzymes allows postulation for some specific functions for starch synthases and branching enzymes. Finally regulation of starch synthesis at the enzymatic level will be discussed and in relation to this regulation, recent results indicating how starch content has been increased in certain plants will be indicated. A previous chapter (Shannon and Garwood, l984) in the second edition of Starch Chemistry and Technology discusses the various maize endosperm mutants or mutant combinations (26 of them) that shows an effect on the quantity or the nature of the starch formed and is still of interest. This information remains of interest and the reader is referred to that review.
Critical and speculative review of the roles of multi-protein complexes in starch biosynthesis in cereals
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In this review, we described protein–protein interactions in cereal endosperm between starch biosynthetic enzymes, including SSs, starch branching enzymes (BEs), starch debranching enzymes, and plastidial Pho1. The formation of protein–protein complexes for starch biosynthesis has been suggested in biochemical studies of enzymes from developing wild-type and mutant maize kernels after chromatographic fractionation [14–16]. Moreover, direct evidence of phosphorylation-dependent multi-enzyme complex formation in starch biosynthesis was first shown in developing wheat endosperm [17].
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2017, Starch in Food: Structure, Function and Applications
This chapter reviews enzymic reactions involved in starch synthesis in higher plants and algae. Existing information on the properties of various starch biosynthetic enzymes in the plant, algal, and cyanobacterial systems will be described and compared. Alteration of starch structure due to the mutational effects on these biosynthetic enzymes allows postulation for some specific functions for starch synthases and branching enzymes. Finally regulation of starch synthesis at the enzymatic level will be discussed and in relation to this regulation, recent results indicating how starch content has been increased in certain plants will be indicated. A previous chapter (Shannon and Garwood, l984) in the second edition of Starch Chemistry and Technology discusses the various maize endosperm mutants or mutant combinations (26 of them) that shows an effect on the quantity or the nature of the starch formed and is still of interest. This information remains of interest and the reader is referred to that review.
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There is a marked decrease in the proportion of chain lengths of DP 4–12 and a corresponding increase in the chain lengths greater than DP 12. Whereas no effect is associated with the loss of expression of SBEIIb in wheat (Regina et al., 2006; Sestili et al., 2010b), the absence of expression in maize and rice results in a phenotype, designated as amylose extender (ae) (Mizuno et al., 1993; Boyer and Preiss, 1978), with a profound effect on the amount of amylose and the structure of amylopectin. It should be stressed that reduction or elimination of starch branching enzyme activity will not result in the production of true amylose; the major effect will be the reduction of branch points in the amylopectin fraction that will result in the formation of an amylopectin polymer with amylose-like properties (Morell et al., 2004).
Starch and cell wall polysaccharides (dietary fibre) of cereal grains contribute to the health benefits associated with the consumption of whole grain cereal products, including reduced risk of obesity, type 2 diabetes, cardiovascular disease and colorectal cancer. The physiological bases for these effects are reviewed in relation to the structures and physical properties of the polysaccharides and their behaviour (including digestion and fermentation) in the gastro-intestinal tract. Strategies for modifying the content and composition of grain polysaccharides to increase their health benefits are discussed, including exploiting natural variation and using mutagenesis and transgenesis to generate further variation. These studies will facilitate the development of new types of cereals and cereal products to face the major health challenges of the 21st century.
Characterization of substrate and product specificity of the purified recombinant glycogen branching enzyme of Rhodothermus obamensis
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Alternatively, this band may correspond to contaminating proteins co-purified with RoBE but without any glucan-modifying/degrading activity. Subsequently, the specific activity of the recombinant enzyme was estimated by an in vitro assay following a previously described method [24] and at 30 °C and pH 7, which does not correspond to the optimal temperature and pH as previously described [19]. Such suboptimal conditions were selected in the future perspective to combine RoBE activity with other non-thermostable enzymes for the in vitro production of new polymers from low-cost renewable resources.
Glycogen and starch branching enzymes catalyze the formation of α(1 → 6) linkages in storage polysaccharides by rearrangement of preexisting α-glucans. This reaction occurs through the cleavage of α(1 → 4) linkage and transfer in α(1 → 6) of the fragment in non-reducing position. These enzymes define major elements that control the structure of both glycogen and starch.
The kinetic parameters of the branching enzyme of Rhodothermus obamensis (RoBE) were established after in vitro incubation with different branched or unbranched α-glucans of controlled structure.
A minimal chain length of ten glucosyl units was required for the donor substrate to be recognized by RoBE that essentially produces branches of DP 3–8. We show that RoBE preferentially creates new branches by intermolecular mechanism. Branched glucans define better substrates for the enzyme leading to the formation of hyper-branched particles of 30–70 nm in diameter (dextrins). Interestingly, RoBE catalyzes an additional α-4-glucanotransferase activity not described so far for a member of the GH13 family.
RoBE is able to transfer α(1 → 4)-linked-glucan in C4 position (instead of C6 position for the branching activity) of a glucan to create new α(1 → 4) linkages yielding to the elongation of linear chains subsequently used for further branching. This result is a novel case for the thin border that exists between enzymes of the GH13 family.
This work reveals the original catalytic properties of the thermostable branching enzyme of R. obamensis. It defines new approach to produce highly branched α-glucan particles in vitro.

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Multiple forms of starch branching enzyme of maize: Evidence for independent genetic control

Abstract

J. Biol. Chem

Arch. Biochem. Biophys

J. Biol. Chem

Anal. Biochem

Biochim. Biophys. Acta

FEBS lett

Arch. Biochem. Biophys