Functional Plant Biology Functional Plant Biology Society
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
+ Author Affiliations
- Author Affiliations

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 | PubMed |

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 |

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 | PubMed |

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 | PubMed |

Batey IL, Curtin BM (1996) Measurement of amylose/amylopectin ratio by high performance liquid chromatography. Starch / Starke 48, 338–344.
CrossRef |

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 | PubMed |

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 | PubMed |

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 |

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 |

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 | PubMed |

Fisher DK, Boyer CD, Hannah LC (1993) Starch branching enzyme II from maize endosperm. Plant Physiology 102, 1045–1046.
CrossRef | PubMed |

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 |


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 | PubMed |

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.

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


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 |


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 |


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 | PubMed |

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 | PubMed |

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 | PubMed |

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 |


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.

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 | PubMed |

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.

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.

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 | PubMed |

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.

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

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 |

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 |


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 |

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


Nelson OE, Pan D (1995) Starch synthesis in maize endosperms. Annual Review of Plant Physiology and Plant Molecular Biology 46, 475–496.
CrossRef |

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 |

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

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 | PubMed |

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 |


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 |

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 | PubMed |

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 |


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 | PubMed |

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 |

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 | PubMed |

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 | PubMed |

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 |


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 |

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

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 |








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