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Cell-type specific, coordinate expression of two ADP-glucose pyrophosphorylase genes in relation to starch biosynthesis during seed development of Vicia faba L.

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Abstract

Several cDNA clones encoding two different ADP-glucose pyrophosphorylase (AGPase, EC 2.7.7.27) polypeptides denoted VfAGPC and VfAGPP were isolated from a cotyledonary library of Vicia faba L. Both sequences are closely related to AGPase small-subunit sequences from other plants. Whereas mRNA levels of VfAGPP were equally high in developing cotyledons and leaves, the mRNA of VfAGPC was present in considerable amounts only in cotyledons. During development of cotyledons, both mRNAs accumulated until the beginning of the desiccation phase and disappeared afterwards. The increase of AGPase activity in cotyledons during the phase of storage-product synthesis was closely followed by the accumulation of starch. The AGPase activity in crude extracts of cotyledons was insensitive to 3-phosphoglycerate whereas the activity from leaves could be activated more than five-fold. Inorganic phosphate inhibited the enzyme from both tissues but was slightly more effective on the leaf enzyme. There was a correlation at the cellular level between the distribution of VfAGPP and VfAGPC mRNAs and the accumulation of starch, as studied by in-situ hybridisation and by histochemical staining in parallel tissue sections of developing seeds, respectively. During the early phase of seed development (12–15 days after fertilization) VfAGPase mRNA and accumulation of starch were detected transiently in the hypodermal, chlorenchymal and outer parenchymal cell layers of the seed coat but not in the embryo. At 25 days after fertilization both synthesis of VfAGPase mRNA and biosynthesis of starch had started in parenchyma cells of the inner adaxial zone of the cotyledons. During later stages, the expression of VfAGPase and synthesis of starch extended over most of the cotyledons but were absent from peripheral cells of the abaxial zone, provascular and procalyptral cells.

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Abbreviations

AGPase:

ADP-glucose pyrophosphorylase

DAF:

days after fertilization

Glc1P:

glucose-1-phosphate

3-PGA:

3-phosphoglycerate

VfAGPC:

AGPase subunit of Vicia faba mainly expressed in cotyledons

VfAGPP:

AGPase subunit of Vicia faba mainly expressed in leaves and cotyledons

pVfAGPC, pVfAGPP:

plasmids containing VfAGPC and VfAGPP, respectively

References

  • Anderson, J.M., Hnilo, J., Larson, R., Okita, T.W., Morell, M., Preiss, J. (1989) The encoded primary sequence of a rice seed ADP-glucose pyrophosphorylase. J. Biol. Chem. 264, 12238–12242

    Google Scholar 

  • Anderson, J.M., Larsen, R., Laudenica, D., Kim, W.T., Morrow, D., Okita, T.W., Preiss, J. (1991) Molecular characterization of the gene encoding a rice endosperm-specific ADP-glucose pyrophosphorylase subunit and its developmental pattern of transcription. Gene 97, 199–205

    Google Scholar 

  • ap Rees, T. (1992) Synthesis of storage starch. In: Carbon Partitoning within and between organisms, pp. 115–131, Pollock, C.J., Farrer, J.F., Gordon, A.J., (eds.) BIOS Scientific Publishers Limited, Oxford

    Google Scholar 

  • Church, G.M., Gilbert, W. (1984) Genomic sequencing. Proc. Natl. Acad. Sci. USA 81, 1991–1995

    Google Scholar 

  • Cox, K.H., Goldberg, R.B. (1988) Analysis of plant gene expression. In: Plant molecular biology, a practical approach, pp. 25–35, Shaw, C.H., (ed.) IRL Press, Washington

    Google Scholar 

  • Dickinson, D.B., Preiss, J. (1969) Presence of ADP-glucose pyrophosphorylase in shrunken-2 and brittle-2 mutants of maize endosperm. Plant Physiol. 44, 1058–1062

    Google Scholar 

  • Dry, I., Smith, A., Edwards, A., Bhattacharyya, M., Dunn, P., Martin, C. (1992) Characterization of cDNAs encoding two isoforms of granule-bound starch synthase which show differential expression in developing storage organs of pea and potato. Plant J. 2, 193–202

    Google Scholar 

  • Duffus, C.M. (1993) Starch synthesis and deposition in developing cereal endosperms. In: Seed storage compounds, pp. 191–219, Shewry, P.R., Stobart, K., (eds.) Science Publications, Oxford

    Google Scholar 

  • Feinberg, A.P., Vogelstein, B. (1983) A Technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal. Biochem. 132, 6–13

    Google Scholar 

  • Harris, N., Wilkinson, D.G. (1990) In situ hybridisation application to developmental biology and medicine, Cambridge University Press, Cambridge

    Google Scholar 

  • Hauxwell, A.J., Corke, F.M.K., Trevor, L. (1989) Temporal and spatial gene expression in relation to cell division in the pea embryo. In: Oscillations and morphogenesis, pp. 249–258, Rensing, T, (ed). Dekker, New York Basel Hongkong

    Google Scholar 

  • Heim, U., Weber, H., Bäumlein, H., Wobus, U. (1993) A sucrosesynthase gene of Vicia faba L.: Expression pattern in developing seeds in relation to starch synthesis and metabolic regulation. Planta 191, 394–401

    PubMed  Google Scholar 

  • Hylton, C., Smith, A.M. (1992) The rb mutation of peas causes structural and regulatory changes in ADP-Glucose pyrophosphorylase from developing embryos. Plant Physiol. 99, 1626–1634

    Google Scholar 

  • Johansen, D.A. (1940) Plant microtechnique. McGraw-Hill, New York

    Google Scholar 

  • John, M.E. (1992) An efficient method for isolation of RNA and DNA from plant containing polyphenolics. Nuclei. Acids Res. 20, 2381

    Google Scholar 

  • Keegstra, K., Olsen, L.J. (1989) Chloroplastic precursors and their transport across the envelope membranes. Annu. Rev. Plant Physiol. 40, 471–501

    Google Scholar 

  • Kleczkowski, L.A., Villand, P., Lüthi, E., Olsen, O.-A., Preiss, J. (1993) Insensitivity of barley endosperm ADP-Glucose pyrophosphorylase to 3-phosphoglycerate and orthophosphate regulation. Plant Physiol. 101, 179–186

    Google Scholar 

  • Manteuffel, R., Müntz, K., Püchel, M., Scholz, G. (1976) Phase-dependent changes of DNA, RNA and protein accumulation during the ontogenesis of broad bean seeds. Biochem. Physiol. Pflanzen 169, 595–605

    Google Scholar 

  • Morell, M.K., Bloom, M., Knowles, V., Preiss, J. (1987) Subunit structure of spinach leaf ADPglucose pyrophosphorylase. Plant Physiol. 85, 182–187

    Google Scholar 

  • Müller-Röber, B.T., Koßmann, J., Hannah, L.C., Willmitzer, L., Sonnewald, U. (1990) One of two different ADP-glucose pyrophosphorylase genes from potato responds strongly to elevated levels of sucrose. Mol. Gen. Genet. 224, 36–146

    Google Scholar 

  • Müller-Röber, B., Sonnewald, U., Willmitzer, L. (1992) Inhibiton of the ADP-glucose pyrophosphorylase in transgenic potatos leads to sugar-storing tubers and influences tuber formation and expression of tuber storage protein genes. EMBO J. 11, 1229–1238

    Google Scholar 

  • Nakamura, Y Kawaguchi, K. (1992) Multiple forms of ADP-glucose pyrophosphorylase of rice endosperm. Physiol. Plant. 84, 336–342

    Google Scholar 

  • Okita, T.W. (1992) Is there an alternative pathway for starch synthesis? Plant Physiol. 100, 560–564

    Google Scholar 

  • Okita, T.A., Nakata, P.A., Anderson, J.M., Sowokinos, J., Morell, M, Preiss, J. (1990) The subunit structure of potato tuber ADP-glucose pyrophosphorylase. Plant Physiol. 93, 785–790

    Google Scholar 

  • Parsons, T.F., Preiss, J. (1978) Biosynthesis of bacterial glycogen: Isolation and characterisation of the pyridoxal-P allosteric activator site and the ADP-glucose-protected pyridoxal-P binding site of E. coli ADP-glucose synthase. J. Biol. Chem. 253, 7638–7645

    Google Scholar 

  • Perez, C.M., Perdon, A.A., Resurreccion, A.P., Villareal, R.M., Juliano, B.O. (1975) Enzymes of carbohydrate metabolism in developing rice grain. Plant Physiol. 56, 579–586

    Google Scholar 

  • Pich, U., Schubert, I. (1993) Midiprep method for isolation of DNA from plants with a high content of polyphenolics. Nucleic Acids Res. 21, 3328

    Google Scholar 

  • Plaxton, W., Preiss, J. (1987) Purification and properties of nonproteolytic degraded ADPglucose pyrophosphorylase from maize endosperm. Plant Physiol. 83, 105–112

    Google Scholar 

  • Preiss, J. (1984) Bacterial glycogen synthesis and its regulation. Annu. Rev. Microbiol. 38, 419–458

    Google Scholar 

  • Preiss, J. (1991) Biology and molecular biology of starch synthesis and its regulation. In: Oxford survey of plant molecular and cellular biology, pp. 59–114, Miflin, B.J., (ed). University Press, Oxford

    Google Scholar 

  • Prioul, J.L., Jeannette, E., Reyss, A., Gregory, N., Giroux, M., Han-nah, L.C., Causse, M. (1994) Expression of ADP-glucose pyrophosphorylase in maize (Zea mays L.) grain and source leaf during grain filling. Plant Physiol. 104, 179–187

    Google Scholar 

  • Reeves, C.D., Krishnan, H.B., Okita, T.W. (1986) Gene expression in developing wheat endosperm. Plant Physiol. 82, 34–40

    Google Scholar 

  • Riffkin, H.L., Duffus, C.M., Bridges, I.G. (1993) Endosperm ADPglucose pyrophosphorylase during grain development in wheat. (Abstr.) Plant Physiol. 102, Suppl. 6

    Google Scholar 

  • Sanwal, G.G., Greenberg, E, Hardie, J., Cameron, E., Preiss, J. (1968) Regulation of starch biosynthesis in plant leaves: Activation and inhibition of ADP-glucose pyrophosphoprylase. Plant Physiol. 43, 417–427

    Google Scholar 

  • Shaw, J.R., Hannah, L.C. (1992) Genomic nucleotide sequences of a wild-type shrunken-2 allele of Zea mays. Plant Physiol. 98, 1214–1216

    Google Scholar 

  • Smith, A.M. (1988) Major differences in isoforms of starch-branching enzyme between developing embryos of round and wrinkled seeded peas (Pisum sativum L.) Planta 175, 270–279

    Google Scholar 

  • Smith, A.M. (1990) Enzymes of primary metabolism. In: Methods in plant biochemistry, pp. 93–102, Dey, P.M., Harborne, J.B., (eds). Academic Press, London

    Google Scholar 

  • Smith, A.M., Bettey, M., Bedford, I.D. (1989) Evidence that the rb-locus alters the starch content of developing pea embryos through an effect on ADP-glucose pyrophosphorylase. Plant Physiol. 89, 1279–1284

    Google Scholar 

  • Smith, A.M., Denyer, K., Martin, C. (1993) Starch synthesis in peas. In: Seed storage compounds, pp. 210–224, Shewry, P.R., Stobart, K., (eds). Science Publications, Oxford

    Google Scholar 

  • Smith-White, B.J., Preiss, J. (1992) Comparison of proteins of ADP-glucose pyrophosphorylase from diverse sources. J. Mol. Evol. 34, 449–464

    Google Scholar 

  • Sowokinos, J. R. (1981) Pyrophosphorylases in Solanum tuberosum. Plant Physiol. 68, 924–929

    Google Scholar 

  • Sowokinos, J.R., Preiss, J. (1982) Pyrophosphorylases in Solanum tuberosum. III. Purification physical and catalytic properties of ADP-glucose pyrophosphorylase in potatos. Plant Physiol. 69, 1459–1466

    Google Scholar 

  • Stark, D.M., Timmermann, K.P., Barry, G.F., Preiss, J. (1992) Regulation of the amount of starch in plant tissues by ADP-glucose pyrophosphorylase. Science 258, 287–292

    Google Scholar 

  • Villand, P., Olsen, O.-A., Kilian, An., Kleczkowski, L.A. (1992) ADP-glucose pyrophosphorylase large subunit cDNA from barley endosperm. Plant Physiol. 100, 1617–1718

    Google Scholar 

  • Villand, P., Olsen, O.A., Kleczkowski, L.A. (1993) Molecular characterisation of multiple cDNA clones for ADP-glucose pyrophosphorylase from Arabidopsis thaliana. Plant Mol. Biol. 23, 1279–1284

    Google Scholar 

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This work was supported by the Bundesministerium für Forschung und Technologie BCT 0389, Molekular- und Zellbiologie von höheren Pflanzen und Pilzen. U.W acknowledges additional support by the Fonds der chemischen Industrie. We thank Elsa Fessel for excellent technical assistance.

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Weber, H., Heim, U., Borisjuk, L. et al. Cell-type specific, coordinate expression of two ADP-glucose pyrophosphorylase genes in relation to starch biosynthesis during seed development of Vicia faba L.. Planta 195, 352–361 (1995). https://doi.org/10.1007/BF00202592

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