Abstract
This paper describes new information, derived from studies of mutant and transgenic plants, about the synthesis and organisation of the two polymers, amylose and amylopectin, that make up the starch granule.
The organisation of amylopectin molecules to form the matrix of the granule is made possible by the fact that the polymer has a polymodal distribution of branch lengths. It has been suggested that this distribution is brought about through the actions of two different isoforms of starch-branching enzyme with different properties, but data from mutant plants with only one isoform of starch-branching enzyme are not consistent with this idea. Studies of mutant and transgenic plants lacking specific isoforms of starch synthase indicate that individual isoforms of this enzyme play distinct roles in amylopectin synthesis. However, the contributions of particular classes of isoform appears to differ from one organ to another. Recent work on mutations that decrease debranching enzyme and lead to the production of highly-branched phytoglycogen has generated a new model for amylopectin synthesis. The validity of the model is discussed.
The synthesis of amylose is a function of a specific class of granule-bound starch synthases, but the mechanism of synthesis is unknown. New data indicate that amylose synthesis within the starch granule requires the presence of soluble malto-oligosaccharides. The generation of malto-oligosaccharides via a debranching enzyme putatively involved in amylopectin synthesis presents a means by which the synthesis of the two sorts of polymer might be integrated.
A further means by which amylose and amylopectin synthesis may interact is suggested by the relationship — observed across a range of mutant plants with lesions in the pathway from sucrose to ADPglucose — between the rate of starch synthesis and the amylose to amylopectin ratio of the starch. It seems likely that changes in ADPglucose concentration have different effects on the synthesis of the two polymers. Factors that control flux through the pathway of starch synthesis may therefore also affect starch structure. The control of flux through the pathway is not properly understood, but is likely to differ from one organ to another. This is highlighted by the recent discovery that ADPglucose pyrophosphorylase — a enzyme considered to be plastidic in most plant organs — is located primarily outside the plastid in the endosperms of some cereals.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
ap Rees, T. (1995). Where do plants make ADP-Glc? In: Pontis, H. G., Salerno, G. L. and Echeverria, E. J. (Eds). Sucrose metabolism, biochemistry, physiology and molecular biology (pp. 143–155). American Society of Plant Physiologists, Rockville.
Baba, T., Yoshii, M. and Kainuma, K. (1987). Acceptor molecule of granular-bound starch synthase from sweet-potato roots. Starch, 39, 52–56.
Ball, S., Guan, H.-P., James, M., Myers, A., Keeling, P., Mouille, G., Buleon, A., Colonna, P. and Preiss, J. (1996). From glycogen to amylopectin: a model explaining the biogenesis of the plant starch granule. Cell, 86, 349–352.
Bhattacharyya, M.K., Smith, A.M., Ellis, T.H.N., Hedley, C. and Martin, C. (1990). The wrinkled-seed character of pea described by Mendel is caused by a transposon-like insertion in a gene encoding starch branching enzyme. Cell, 60, 115–122.
Bogracheva, T.Y., Davydova, N.I., Genin, Y.V. and Hedley, C.L. (1995). Mutant genes at the r and rb loci affect the structure and physico-chemical properties of pea seed starches. Journal of Experimental Botany, 46, 1905–1913.
Burton, R.A., Bewley, J.D., Smith, A.M., Bhattacharyya, M.K., Tatge, H., Ring, S., Bull, V., Hamilton, W.D.O. and Martin, C. (1995). Starch branching enzymes belonging to distinct enzyme families are differentially expressed during pea embryo development. Plant Journal, 7, 3–15.
Craig, J., Smith, A., Wang, T.L., Lloyd, J. and Hedley, C. (1995). Biochemistry of new wrinkled-seeded mutants of pea. In: Proc. 2nd European Conf. Grain Legumes, Copenhagen. Improving Production and Utilisation of Grain Legumes (p. 396). Association Européenne de Recherche sur les Protéagineux, Paris.
Denyer, K., Barber, L.M., Burton, R., Hedley, C.L., Hylton, C.M., Johnson, S., Jones, D.A., Marshall, J., Smith, A.M., Tatge, H., Tomlinson, K. and Wang, T.L. (1995a). The isolation and characterization of novel low-amylose mutant of Pisum sativum. Plant Cell and Environment, 18, 1019–1026.
Denyer, K., Clarke, B., Hylton, C., Tatge, H. and Smith, A.M. (1996a). The elongation of amylose and amylopectin chains in isolated starch granules. Plant Journal, 10, 1135–1143.
Denyer, K., Dunlap, F., Thorbjørnsen, T., Keeling, P. and Smith, A.M. (1996b). The major form of ADP-glucose pyrophosphorylase in maize (Zea mays L.) endosperm is extra-plastidial. Plant Physiology, 112, 779–785.
Denyer, K., Foster, J. and Smith, A.M. (1995c). The contributions of adenosine 5′-diphosphoglucose pyrophosphorylase and starch-branching enzyme to the control of starch synthesis in developing pea embryos. Planta, 97, 57–62.
Denyer, K., Hylton, C.M., Jenner, C. F. and Smith, A.M. (1995b). Identification of multiple isoforms of soluble and granule-bound starch synthase in developing wheat endosperm. Planta, 196, 256–265.
Denyer, K., Sidebottom, C., Hylton, C.M. and Smith, A.M. (1993). Soluble isoforms of starch synthase and starch-branching enzyme also occur within starch granules in developing pea embryos. Plant Journal, 4, 191–198.
Denyer, K. and Smith, A.M. (1992). The purification and characterisation of the two forms of soluble starch synthase from developing pea embryos. Planta, 186, 609–667.
Doehlert, D.C. and Knutson, C.A. (1991). Two classes of starch debranching enzymes from developing maize kernels. Journal of Plant Physiology, 138, 566–572.
Dry, I., Smith, A.M., Edwards, E.A., Bhattacharyya, M., Dunn, P. and Martin, C. (1992). Characterisation of cDNAs encoding two isoforms of granule-bound starch synthase which show differential expression in developing storage organs. Plant Journal, 2, 193–202.
Edwards, A., Marshall, J., Denyer, K., Sidebottom, C., Visser, R.G.F., Smith A.M. and Martin, C. (1996). Evidence that a 77-kilodalton protein from the starch of pea embryos is an isoform of starch synthase that is both soluble and granule bound. Plant Physiology, 112, 89–97.
Edwards, A., Marshall, J., Sidebottom, C., Visser, R.G.F., Smith, A.M. and Martin, C. (1995). Biochemical and molecular characterisation of a novel starch synthase from potato tubers. Plant Journal, 8, 283–294.
French, D. (1984). Organization of starch granules. In: Whistler, R.L., BeMiller, J.N. and Paschall, E.F. (Eds). Starch: Chemistry and Technology (pp. 183–247). Academic Press, Orlando.
Gidley, M.J. (1992). Structural order in starch granules and its loss during gelatinisation. In: Phillips, G.O., Williams, P.A. and Wedlock, D.J. (Eds). Gums and Stabilisers for the Food Industry 6 (pp. 87–92). IRL Press, Oxford.
Gidley, M.J. and Bociek, S.M. (1988). 13C CP/MAS NMR studies of amylose inclusion complexes, cyclodextrins and the amorphous phase of starch granules: relationships between glycosidic linkage formation and solid-state 13C chemical shifts. Journal of the American Chemical Society, 110, 3820–3829.
Gidley, M.J. and Bulpin, P.V. (1987). Crystallisation of malto-oligosaccharides as models of the crystalline forms of starch: minimum chain-length requirement for the formation of double helices. Carbohydrate Research, 161, 291–300.
Giroux, M. and Hannah, M.C. (1994). ADP-glucose pyrophosphorylase in shrunken-2 and brittle-2 mutants of maize. Molecular and General Genetics, 243, 400–408.
Guan, H., Kuriki, T., Sivak, M. and Preiss, J. (1995). Maize branching enzyme catalyses synthesis of glycogen-like polysaccharide in glgb-deficient Escherichia coli, Proceedings of the National Academy of Sciences USA, 92, 964–967.
Guan, H.P. and Preiss, J. (1993). Differentiation of the properties of the branching isozymes from maize (Zea mays). Plant Physiology, 102, 1269–1273.
Hizukuri, S. (1986). Polymodal distribution of the chain lengths of amylopectin and its significance. Carbohydrate Research, 147, 342–347.
Hylton, C.M., Denyer, K., Keeling, P.L., Chang, M.-T and Smith, A.M. (1996). The effect of waxy mutations on the granule-bound starch synthases of barley and maize endosperms. Planta, 198, 230–237.
James, M.G., Robertson, D.S. and Myers, A.M. (1995). Characterization of the maize gene sugary1, a. determinant of starch composition in kernels. Plant Cell, 7, 417–429.
Jenkins, P.J., Cameron, R.E. and Donald, A.M. (1993). A universal feature in the structure of starch granules from different botanical sources. Starch, 45, 417–420.
Jenkins, P.J. and Donald, A.M. (1995). The influence of amylose on starch granule structure. International Journal of Biological Macromolecules, 17, 315–321.
Leloir, L.F., De Fekete, M.A.R. and Cardini, C.E. (1961). Starch and oligosaccharide synthesis from uridine diphosphate glucose. Journal of Biological Chemistry, 236, 636–641.
Lloyd, J.R. (1995). Effect and interactions of Rugosus genes on pea (Pisum sativum) seeds. PhD thesis. Univ. East Anglia, Norwich, UK
Marshall, J., Sidebottom, C., Debet, M., Martin, C., Smith, A.M. and Edwards, A. (1996). Identification of the major starch synthase in the soluble fraction of potato tubers. Plant Cell, 8, 1121–1135.
Mouille, G., Maddelein, M.-L., Libessart, N., Tagala, P., Decq, A., Delrue, B. and Ball, S. (1996). Pre-amylopectin processing: a mandatory step for starch biosynthesis in plants. Plant Cell, 8, 1353–1356.
Mu-Forster, C., Huang, R., Powers, J.R., Harriman, R.W., Knight, M., Singletary, G.W., Keeling, P.L. and Wasserman, B.P. (1996). Physical association of starch biosynthetic enzymes with starch granules of maize endosperm. Plant Physiology, 111, 821–829.
Nakamura, Y., Umemoto, T., Ogata, N., Kuboki, Y., Yano, M. and Sasaki, T. (1996a). Starch debranching enzyme (R-enzyme or pullulanase) from developing rice endosperm: purification, cDNA and chromosomal localization of the gene. Planta, 199, 209–218.
Nakamura, Y., Umemoto, T., Takahata, Y., Komae, K., Amano, E. and Satoh, H. (1996b). Changes in the structure of starch and enzyme activities affected by sugary mutations in developing rice endosperm. Possible role of starch debranching enzyme (R-enzyme) in amylopectin biosynthesis. Physiologia Plantarum, 97, 491–498.
Pan, D. and Nelson, O.E. (1984). A debranching enzyme deficiency in endosperms of the sugary-1 mutants of maize. Plant Physiology, 74, 324–328.
Preiss, J. and Sivak, M. (1996). Starch synthesis in sinks and sources. In: Zamski, E. and Schaffer, A. A. (Eds). Photoassimilate Distribution in Plants and Crops (pp. 63–94). Marcel Dekker, New York.
Smith, A.M. (1988). Major differences in isoforms of starch-branching enzyme in embryos of round-and wrinkled-seeded peas (Pisum sativum L.). Planta, 175, 270–279.
Smith, A.M. (1990). Evidence that the “waxy” protein of pea (Pisum sativum L.) is not the major starch-granule-bound starch synthase. Planta, 182, 599–604.
Smith, A.M., Denyer, K. and Martin, C. (1995). What controls the amount and structure of starch in storage organs? Plant Physiology, 107, 673–677.
Smith, A.M., Denyer, K. and Martin, C. (1997). The synthesis of the starch granule. Annual. Review of Plant Physiology and Plant Molecular Biology, 48, 67–87.
Takeda, Y., Guan, H.-P and Preiss, J. (1993). Branching of amylose by the branching isoenzymes of maize endosperm. Carbohydrate Research, 240, 253–263.
Thorbjørnsen, T., Villand, P., Denyer, K., Olsen, O.-A. and Smith, A.M. (1996b). Distinct isoforms of ADPglucose pyrophosphorylase occur inside and outside the amyloplasts in barley endosperm. Plant Journal, 10, 243–250.
Thorbjørnsen, T., Villand, P., Kleczkowski, L. and Olsen, O.-A. (1996a). A single gene encodes two different transcripts for the ADP-glucose pyrophosphorylase small subunit from barley (Hordeum vulgare). Biochemical Journal, 131, 149–154.
Tomlinson, K.L., Lloyd, J.R. and Smith, A.M. (1997). Importance of isoforms of starch branching enzyme in determining the structure of starch in pea leaves. Plant Journal, 11, 101–113.
Van den Koornhuyse, N., Libessart, N., Delrue, B., Zabawinski, C., Decq, A., Iglesias, A., Carton, A., Preiss, J. and Ball, S. (1996). Control of starch composition and structure through substrate supply in the monocellular alga Chlamydomonas reinhardtii., Journal of Biological Chemistry, 271, 16281–16287.
Villand, P. and Kleczkowski, L. (1994). Is there an alternative pathway for starch biosynthesis in cereal seeds? Zeitschrift Naturforschung, 49c, 215–219.
Visser, R.G.F., Somhorst, I., Kuipers, G.J., Ruys, N.J., Feenstra, W.J. and Jacobsen, E. (1991). Inhibition of the expression of the gene for granule-bound starch synthase in potato by antisense constructs. Molecular and General Genetics, 225, 289–296.
Wang, T.L., Hadavizideh, A., Harwood, A., Welham, T J., Harwood, W.A., Faulks, R. and Hedley, C.L. (1990). An analysis of seed development in Pisum sativum. XIII The chemical induction of storage product mutants. Plant Breeding 105, 311–320.
Wang, T.L. and Hedley, C.L. (1991). Seed development in peas: knowing your three “r”s’ (or four, or five) Seed Science Research, 1, 3–14.
Wang, T.L., Barber, L., Craig, J., Denyer, K., Harrison, C., Lloyd, J., MacLeod, M., Smith, A. and Hedley, C.L. (1997). In: Richmond, P., Frazier, P.J. and Donald, A.M. (Eds). Starch: structure and function (pp. 188–195). Royal Society of Chemistry, Cambridge.
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 1999 Springer Science+Business Media Dordrecht
About this chapter
Cite this chapter
Smith, A.M. (1999). Regulation of starch synthesis in storage organs. In: Kruger, N.J., Hill, S.A., Ratcliffe, R.G. (eds) Regulation of Primary Metabolic Pathways in Plants. Proceedings of the Phytochemical Society of Europe, vol 42. Springer, Dordrecht. https://doi.org/10.1007/978-94-011-4818-4_9
Download citation
DOI: https://doi.org/10.1007/978-94-011-4818-4_9
Publisher Name: Springer, Dordrecht
Print ISBN: 978-94-010-6021-9
Online ISBN: 978-94-011-4818-4
eBook Packages: Springer Book Archive