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Plant function and evolutionary biology
RESEARCH ARTICLE

Multiple isoforms of starch branching enzyme-I in wheat: lack of the major SBE-I isoform does not alter starch phenotype

Ahmed Regina A B , Behjat Kosar-Hashemi A , Zhongyi Li A , Lynette Rampling A , Mark Cmiel A , Maria C. Gianibelli A , Christine Konik-Rose A , Oscar Larroque A , Sadequr Rahman A and Matthew K. Morell A
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A CSIRO Division of Plant Industry, PO Box 1600, Canberra, ACT 2601, Australia.

B Corresponding author; email: regina.regina@csiro.au

Functional Plant Biology 31(6) 591-601 https://doi.org/10.1071/FP03193
Submitted: 22 October 2003  Accepted: 17 March 2004   Published: 23 June 2004

Abstract

The role of starch branching enzyme-I (SBE-I) in determining starch structure in the endosperm has been investigated. Null mutations of SBE-I at the A, B and D genomes of wheat were identified in Australian wheat varieties by immunoblotting. By combining individual null mutations at the B and D genomes through hybridisation, a double-null mutant wheat, which lacks the B and D isoforms of SBE-I, was developed. Wheat mutants lacking all the three isoforms of SBE-I were generated from a doubled haploid progeny of a cross between the BD double-null mutant line and a Chinese Spring (CS) deletion line lacking the A genome isoform. Comparison of starch from this mutant wheat to that from wild type revealed no substantial alteration in any of the structural or functional properties analysed. Further analysis of this triple-null mutant line revealed the presence of another residual peak of SBE-I activity, referred to as SBE-Ir, in wheat endosperm representing < 3% of the activity of SBE-I in wild type endosperm.

Keywords: branching enzymes, null mutant, isoforms, starch, wheat.


Acknowledgments

Financial assistance from Goodman Fielder Ingredients Pty Ltd and Biogemma, UK, for the conduct of this study is gratefully acknowledged. This research has been facilitated by access to the Australian Proteome Analysis Facility, established under the Australian Government’s Major National Research Facilities Program.


References


Baga M, Glaze S, Mallard CS, Chibbar R (1999a) A starch branching enzyme gene in wheat produces alternatively spliced transcripts. Plant Molecular Biology 40, 1019–1030.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Baga M, Repellin A, Demeke T, Caswell K, Leung N, Abdel-Aal ES, Hucl P, Chibbar RN (1999b) Wheat starch modification through biotechnology. Starch / Starke 51, 111–116.
Crossref | GoogleScholarGoogle Scholar | open url image1

Baga M, Nair R, Repellin A, Scoles GJ, Chibbar R (2000) Isolation of a cDNA encoding a granule-bound 152-kilodalton starch-branching enzyme in wheat. Plant Physiology 124, 253–263.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ball SG, Morell MK (2003) From bacterial glycogen to starch: understanding the biogenesis of the plant starch granule. Annual Review of Plant Biology 54, 207–233.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Batey IL, Curtin BM (1996) Measurement of amylose/amylopectin ratio by high performance liquid chromatography. Starch / Starke 48, 338–344.
Crossref | GoogleScholarGoogle Scholar | open url image1

Batey IL, Curtin BM, Abbot DC, Rahman S (1996) Starch granule size distribution of Chinese Spring chromosome deletion lines. ‘Proceedings of the 48th Australian Cereal Chemistry Conference’. (Ed. CW Wrigley ) pp. 228–230. (Cereal Chemistry Division, Royal Australian Chemical Institute, North Melbourne, Vic.)


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 Physiology 125, 1396–1405.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Blauth SL, Kim K-N, 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 Molecular Biology 48, 287–297.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Boggini G, Cattaneo M, Paganoni C, Vaccino P (2001) Genetic variation of waxy proteins and starch properties in Italian wheat germplasm. Euphytica 119, 113–116.
Crossref | GoogleScholarGoogle Scholar | open url image1

Boyer CD, Preiss J (1978) Multiple forms of (1,4)-α-d-glucan, (1,4)-α-d-glucan-6-glycosyl transferase from developing Zea mays L. kernels. Carbohydrate Research 61, 321–334.
Crossref | d
-glucan, (1,4)-α-d-glucan-6-glycosyl transferase from developing Zea mays L. kernels.&journal=Carbohydrate Research&volume=61&pages=321-334&publication_year=1978&author=J%20Preiss&hl=en&doi=10.1016/S0008-6215(00)84492-4" target="_blank" rel="nofollow noopener noreferrer" class="reftools">GoogleScholarGoogle Scholar | open url image1

Burton RA, Bewley JD, Smith AM, Bhattacharya MK, Tatge H, Ring S, Bull V, Hamilton DO, Martin C (1995) Starch branching enzymes belonging to distinct enzyme families are differentially expressed during pea embryo development. The Plant Journal 7, 3–15.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Fisher DK, Boyer CD, Hannah LC (1993) Starch branching enzyme II from maize endosperm. Plant Physiology 102, 1045–1046.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

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 specialisation. Plant Molecular Biology 30, 1223–1232.
PubMed |
open url image1

Gao M, Wamat J, Stinard PS, James MG, Myers AM (1998) Characterisation of dull 1, a maize gene encoding for a novel starch synthase. The Plant Cell 10, 399–412.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Garwood DL, Shannon JC, Creech RG (1976) Starches of endosperms possessing different alleles at the amylose-extender locus in Zea mays.  Cereal Chemistry 53, 355–364. open url image1

Guan HP, Preiss J (1993) Differentiation of the properties of the branching isozymes from maize (Zea mays). Plant Physiology 102, 1269–1273.
PubMed |
open url image1

Hawker JS, Ozburn JL, Greenberg E, 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 glucan. Archives of Biochemistry and Biophysics 160, 530–551.
PubMed |
open url image1

Hedman KD, Boyer CD (1982) Gene dosage at the amylose-extender locus of maize: effects on the levels of starch branching enzymes. Biochemical Genetics 20, 483–492.
PubMed |
open url image1

James MG, Robertson DS, Myers A (1995) Characterisation of maize gene sugary 1, a determinant of starch composition in kernels. The Plant Cell 7, 417–429.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Jobling SA, Schwall GP, Westcott RJ, Sidebottom CM, Debet M, Gidley MJ, Jeffcoat R, Safford R (1999) A minor form of starch branching enzyme in potato (Solanum tuberosum) tubers has a major effect on the starch structure: cloning and characterisation of multiple forms of SBE A. The Plant Journal 18, 163–171.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kim K-Y, Fisher DK, Gao M, Guiltinan MJ (1998) Genomic organisation and promoter activity of the maize starch branching enzyme 1 gene. Gene 216, 233–243.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kossmann J, Visser RGF, Muller RB, Wilmitzer L, Sonnewald U (1991) Cloning and expression analysis of a potato cDNA that encodes branching enzyme: evidence for co-expression of starch biosynthesis genes. Molecular and General Genetics 230, 39–44.
PubMed |
open url image1

Konik-Rose CM, Moss R, Rahman S, Appels R, Stoddard F, McMaster G (2001) Evaluation of the 40 mg swelling test for measuring starch functionality.   /  53, 14–20. open url image1

Mizuno K, Kobayashi E, Tachibana M, Kawasaki T, Fujimura T, Funane K, Kobayashi M, Baba T (2001) Characterisation of an isoform of rice starch branchning enzyme, RBE4, in developing seeds. Plant and Cell Physiology 42, 349–357.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Mizuno K, Kawasaki T, Shimada H, Satoh H, Kobayashi E, Okumura S, Arai Y, Baba T (1993) Alteration of the structural properties of starch composition by the lack of an isoform of starch branching enzyme in rice seeds. The Journal of Biological Chemistry 268, 19 084–19 091. open url image1

Morell MK, Rahman S, Abrahams SL, Appels R (1995) The biochemistry and molecular biology of starch synthesis in cereals. Journal of Plant Physiology 22, 647–660. open url image1

Morell MK, Blennow A, Kosar-Hashemi B, Samuel MS (1997) Differential expression and properties of starch branching enzyme isoforms in developing wheat endosperm. Plant Physiology 113, 201–208.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Morrison WR, Laignelet B (1983) An improved colorimetric procedure for determining apparent and total amylose in cereal and other starches. Journal of Cereal Science 1, 9–20. open url image1

Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiologia Plantarum 15, 473–497. open url image1

Nakamura Y, Takeichi T, Kawaguchi K, Yamanouchi H (1992) Purification of two forms of starch branching enzyme (Q-enzyme) from developing rice endosperm. Physiologia Plantarum 84, 329–335.
Crossref | GoogleScholarGoogle Scholar | open url image1

Nakamura T, Yamamori M, Hirano H, Hidaka S, Nagamine T (1995) Production of waxy (amylose-free) wheats. Molecular and General Genetics 248, 253–259.
PubMed |
open url image1

Nakamaura Y, Umemoto T, Takahata Y, Komae K, Amano E, Satoh H (1996) Changes in structure of starch and enzyme activities affected by sugary mutations in developing rice endosperm. Possible role of starch debranching enzyme (R-enzyme) in amylopectin synthesis. Physiologia Plantarum 97, 491–498.
Crossref | GoogleScholarGoogle Scholar | open url image1

Nelson OE, Rines HW (1962) The enzymatic deficiency in the waxy mutant of maize. Biochemical and Biophysical Research Communications 9, 297–300.
PubMed |
open url image1

Nelson OE, Pan D (1995) Starch synthesis in maize endosperms. Annual Review of Plant Physiology and Plant Molecular Biology 46, 475–496.
Crossref | GoogleScholarGoogle Scholar | open url image1

O’Shea MG, Samuel MS, Konik CM, Morell MK (1998) Fluorophore-assisted carbohydrate electrophoresis (FACE) of oligosaccharides: efficiency of labelling and high resolution separation. Carbohydrate Research 307, 1–12.
Crossref | GoogleScholarGoogle Scholar | open url image1

Pan D, Nelson OE (1984) A debranching enzyme deficiency in endosperm of the sugary-1 mutants of maize. Plant Physiology 74, 324–328. open url image1

Peng M, Gao M, Baga M, Hucl P, Chibbar RN (2000) Starch branching enzymes preferentially associated with A-type starch granules in wheat endosperm. Plant Physiology 124, 265–272.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Preiss J (1991) Biology and molecular biology of starch synthesis and its regulation. ‘Oxford surveys of plant molecular and cell biology. Vol. 7’. (Ed. BJ Miflin) pp. 59–114. (Oxford University Press: Oxford)

Rahman S, Abrahams S, Mukai Y, Abbott DC, Samuel MS, Morell MK, Appels R (1997) A complex arrangement of genes at a starch branching enzyme 1 locus in the D genome donor of wheat. Genome 40, 465–474.
PubMed |
open url image1

Rahman S, Li Z, Abrahams S, Abbot D, Appels R, Morell MK (1999) Characterisation of a gene encoding wheat endosperm starch branching enzyme-1. Theoretical and Applied Genetics 98, 156–163.
Crossref | GoogleScholarGoogle Scholar | open url image1

Rahman S, Regina A, Li Z, Mukai Y, Yamamoto M, Hashemi BK, Abrahams S, Morell MK (2001) Comparison of starch branching enzyme genes reveals evolutionary relationships among isoforms. Characterisation of a gene for starch branching enzyme IIa from the wheat D genome donor Aegilops tauschii.  Plant Physiology 125, 1314–1324.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Repellin A, Baga M, Chibbar RN (1997) Isolation of a starch branching enzyme I cDNA from a wheat endosperm library (Accession No. Y12320 Plant Gene Register PGR97–094). Plant Physiology 114, 1135.
Crossref | PubMed |
open url image1

Schwall GP, Safford R, Westcott RJ, Jeffcoat RJ, Tayal A, Shi Y-C, Gidley MJ, Jobling SA (2000) Production of very-high-amylose potato starch by inhibition of SBE A and SBE B. Nature Biotechnology 18, 551–554.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Shewry PR, Morell M (2001) Manipulating cereal endosperm structure, development and composition to improve end-use properties. ‘Advances in botanical research incorporating advances in plant pathology biotechnology of cereals. Vol. 34’. (Eds PR Shewry, PA Lazzeri, KJ Edwards) pp. 166–236. (Academic Press: San Diego, CA)

Sidebottom C, Kirkland M, Strongitharm B, Jeffcoal R (1998) Characterisation of the difference of starch branching enzyme activities in normal and low amylopectin maize during kernel development. Journal of Cereal Science 27, 279–287.
Crossref | GoogleScholarGoogle Scholar | open url image1

Stinard PS, Robertson DS, Schnable PS (1993) Genetic isolation, cloning and analysis of mutator-induced, dominant antimorph of maize amylose extender 1 locus. The Plant Cell 5, 1555–1566.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Sun C, Sathish P, Ahlandsberg S, Jansson C (1998) The two genes encoding starch-branching enzymes IIa and IIb are differentially expressed in barley. Plant Physiology 118, 37–49.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Suzuki G, Moriyama M, Fujioka K, Yamamoto M, Subramanyam NC, Li Z, Appels R, Morell M, Mukai Y, Rahman S (2003) The starch branching enzyme 1 locus from Aegilops tauschii, the donor of the D genome to wheat. Functional and Integrative Genomics 3, 69–75.
PubMed |
open url image1

Swanston SJ, Ellis RP, Morrison IM, Mackay GR, Dale MFB , et al . (2001) Combining high-amylose and waxy starch mutations in barley. Journal of the Science of Food and Agriculture 81, 594–603.
Crossref | GoogleScholarGoogle Scholar | open url image1

Takeda Y, Guan H-P, Preiss J (1993) Branching of amylose by the branching isozymes of maize endosperm. Carbohydrate Research 240, 253–263.
Crossref | GoogleScholarGoogle Scholar | open url image1

Thomas DJ, Atwell WA (1999) Starch analysis methods. ‘Starches practical guide for food industry’. pp. 13–24. (Eagan Press, St Paul, MN)

Yamamori M, Fujita S, Hayakawa K, Matsuki J (2000) Genetic elimination of a starch granule protein, SGP-1, of wheat generates an altered starch with apparent high amylose. Theoretical and Applied Genetics 101, 21–29.
Crossref | GoogleScholarGoogle Scholar | open url image1