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Induction of the plastidic starch-phosphorylase gene in potato storage sink tissue

Effect of sucrose and evidence for coordinated regulation of phosphorylase and starch biosynthetic genes

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Abstract

The expression of the gene encoding the plastidic enzyme starch phosphorylase (EC 2.4.1.1) varies according to tissue carbohydrate status. Incubation of excised potato (Solanum tuberosum L. cv. Désirée) leaves carrying a portion of the stem under a short photoperiod resulted in a drastic accumulation of starch, accompanied by a rapid increase in the level of phosphorylase mRNA and by a similar change in phosphorylase protein level. However, under the same incubation conditions, the transcriptional activity of the phosphorylase promoter in transgenic plants did not change markedly. Therefore, the increased expression of the phosphorylase gene in petioles of stem cuttings is not controlled by the level of initiation of transcription. Phosphorylase mRNA accumulated to a high level in petioles of detached leaves kept under constant light for 24 h, but not in petioles kept in the dark. The effect of light on the accumulation of the mRNA was appreciably reduced if the petioles were incubated in ethylendiaminetetraacetic acid (EDTA), a treatment known to increase phloem exudation in detached leaves. The inhibition by EDTA could be partially counteracted by the addition of sucrose to the incubation solution. Furthermore, incubation of petioles in darkness in solutions with high levels of sucrose resulted in enhanced expression of the gene. These results suggest that sucrose, the main compound transported by phloem in potato, is involved in the regulation of the starch phosphorylase gene. This also indicates that conditions favouring starch synthesis lead to increased expression of the phosphorylase gene.

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Abbreviations

GUS:

β-glucuronidase

References

  • Bhatt, A.M., Knowler, J.T. (1992) Tissue distribution and change in potato starch phosphorylase mRNA levels in wounded tissue and sprouting tubers. Eur. J. Biochem. 204, 971–975

    Google Scholar 

  • Brisson, N., Giroux, H., Zollinger, M., Camirand A., Simard, C. (1989) Maturation and subcellular compartmentation of potato starch-phosphorylase. Plant Cell 1, 559–566

    Google Scholar 

  • Camirand, A., St-Pierre, B., Marineau C., Brisson, N. (1990) Occurrence of a copia-like transposable element in one of the introns of the potato starch-phosphorylase gene. Mol. Gen. Genet. 224, 33–39

    Google Scholar 

  • Chang, T.-C., Lu, S.-C, Su, J.-C. (1987) Sweet potato starch-phosphorylase-Purification and characterization. Agric. Biol. Chem. 51, 187–195

    Google Scholar 

  • Chiang, C.-L., Lu, Y.-L., Juang, R.-H., Lee, P.-D., Su, J.-C. (1991) Native and degraded forms of sweet potato starch-phosphorylase. Agric. Biol. Chem. 55, 641–646

    Google Scholar 

  • Cohn, M. (1961) Phosphorylases (survey). In:The enzymes, vol. V, pp. 179–206, Boyer, P.D., Lardy, H., Myrback, K. eds. Academic Press, New York

    Google Scholar 

  • Conrads, J., van Berkel, J., Schächtele, C., Steup, M. (1986) Nonchloroplast α-1,4-glucan phosphorylase from pea leaves: characterization and in-situ localization by indirect immunofluorescence. Biochim. Biophys. Acta 882, 452–463

    Google Scholar 

  • Davies, H.V., Ross, H.A. (1987) Hydrolytic and phosphorolytic enzyme activity and reserve mobilization in sprouting tubers of potato (Solanum tuberosum L.). J. Plant Physiol. 126, 387–397

    Google Scholar 

  • Duncan, D.A., Ewing, E.E. (1984) Initial anatomical changes associated with tuber formation on single-node potato (Solanum tuberosum L.) cuttings. Ann. Bot. 53, 607–610

    Google Scholar 

  • Fischer, E.H., Heilmeyer, L.M.G.jr., Haschke, R.H. (1971) Phosphorylase and the control of glycogen degradation. Curr. Top. Cell. Reg. 4, 211–251

    Google Scholar 

  • Fukui, T, Nakano, K., Tagaya, M., Nakayama, H. (1987) Phosphorylase isozymes of higher plants. In: Biochemistry of vitamin B6, pp. 267–276, Korpela, T., Christen, P., eds. Birkhauser Verlag, Basel

    Google Scholar 

  • Groussol, J., Delrot, S, Caruhel, P., Bonnemain, J.L. (1986) Design of an improved exudation method for phloem sap collection and its use for the study of phloem mobility of pesticides. Physiol. Vég. 24, 123–133

    Google Scholar 

  • Hargreaves, J.A., ap Rees, T. (1988) Turnover of starch and sucrose in roots of Pisum sativum. Phytochemistry 27, 1627–1629

    Google Scholar 

  • Hatzfeld, W.-D., Dancer, J., Stitt, M. (1990) Fructose-2,6-bisphosphate, metabolites and ‘coarse’ control of pyrophosphate: fructose-6-phosphate phosphotransferase during triose-phosphate cycling in heterotrophic cell-suspension cultures of Chenopodium rubrum. Planta 180, 205–211

    Google Scholar 

  • Hawker, J.S., Marschner, H., Krauss, A. (1979) Starch synthesis in developing potato tubers. Physiol. Plant. 46, 25–30

    Google Scholar 

  • Iwata, S., Fukui, T. (1973) The subunit stucture of α-glucan phosphorylase from potato. FEBS Lett. 36, 222–226

    Google Scholar 

  • Jefferson, R.A., Kavanagh, T.A., Bevan, M.W. (1987) GUS fusion: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6, 3901–3907

    Google Scholar 

  • Jones, J.D.G., Dunsmuir, P., Bedbrook, J. (1985) High level expression of introduced chimeric genes in regenerated transformed plants. EMBO J. 4, 2411–2418

    Google Scholar 

  • Kauss, H. (1990) The role of the plasma membrane in host-pathogen interactions. In:The plant plasma membrane, pp. 320–350, Larsson, C., Moller, I.M., eds. Springer, Berlin

    Google Scholar 

  • Keeling, P.L., Wood, J.R., Tyson, R.H., Bridges, I.G. (1988) Starch biosynthesis in developing wheat grain: Evidence against the direct involvement of triose phosphates in the metabolic pathway. Plant Physiol. 87, 311–319

    Google Scholar 

  • Koßmann, J., Visser, R.G.F., Müller-Röber, B., Willmitzer, L., Sonnewald, U. (1991) Cloning and expression analysis of a potato cDNA that encodes branching enzyme: evidence for co-expression of starch biosynthetic genes. Mol. Gen. Genet. 230, 39–44

    Google Scholar 

  • Lovell, P.H., Booth, A. (1967) Effects of gibberellic acid on growth, tuber formation and carbohydrate distribution in Solanum tuberosum. New Phytol. 66, 525–537

    Google Scholar 

  • Mori, H., Tanizawa, K., Fukui, T. (1991) Potato tuber type H phosphorylase isozyme. Molecular cloning, nucleotide sequence, and expression of a full-length cDNA in Escherichia coli. J. Biol. Chem. 266, 18446–18453

    Google Scholar 

  • Müller-Röber, B., 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, 136–146

    Google Scholar 

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

    Google Scholar 

  • Nakano, K., Fukui, T. (1986) The complete amino acid sequence of potato α-glucan phosphorylase. J. Biol. Chem. 261, 8230–8236

    Google Scholar 

  • Nakano, K., Mori, H., Fukui, T. (1989) Molecular cloning of cDNA encoding potato amyloplast α-glucan phosphorylase and the structure of its transit peptide. J. Biochem. (Tokyo) 106, 691–695

    Google Scholar 

  • Obata-Sasamoto, H., Suzuki, H. (1979a) Activities of enzymes relating to starch synthesis and endogenous levels of growth regulators in potato stolon tips during tuberization. Physiol. Plant. 45, 320–324

    Google Scholar 

  • Obata-Sasamoto, H., Suzuki, H. (1979b) Activities of enzymes relating to starch synthesis and endogenous levels of growth regulators during tuberization of isolated potato stolons cultured in vitro. Z. Pflanzenphysiol. 95, 69–75

    Google Scholar 

  • Paiva, E., Lister, R.M., Park, W.D. (1983) Induction and accumulation of major tuber proteins of potato in stems and petioles. Plant Physiol. 71, 161–168

    Google Scholar 

  • Preiss, J., Levi, C. (1979) Metabolism of starch in leaves. In:Encyclopedia of plant physiology, N.S., vol. 6: Photosynthesis II, pp. 282–312, Gibbs, M., Latzko, E., eds. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Sambrook, J., Fritsch, E.F., Maniatis, T. (1989) Molecular cloning: A laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • Schächtele, C., Steup, M. (1986) α-1,4-Glucan phosphorylase forms from leaves of spinach (Spinacia oleracea L.) I. In situ localization by indirect immunofluorescence. Planta 167, 444–451

    Google Scholar 

  • Schneider, E.M., Becker, J.-U., Volkmann, D. (1981) Biochemical properties of potato phosphorylase change with its intracellular localization as revealed by immunological methods. Planta 151, 124–134

    Google Scholar 

  • Sivak, M.N., Tandecarz, J.S., Cardini, C.E. (1981) Studies on potato tuber phosphorylase-catalyzed reaction in the absence of an exogenous acceptor I. Characterization and properties of the enzymes. Arch. Biochem. Biophys. 212, 525–536

    Google Scholar 

  • Smith, O.W., Palmer, C.E. (1970) Cytokinin-induced tuber formation of Solanum tuberosum. Physiol. Plant. 25, 599–606

    Google Scholar 

  • Steup, M. (1988) Starch degrading enzymes. In:Biochemistry of plants, vol. 14: Carbohydrates, pp. 255–296, Preiss, J., ed. Academic Press, New York

    Google Scholar 

  • Steup, M., Schächtele, C. (1981) Mode of glucan degradation by purified phosphorylase forms from spinach leaves. Planta 153, 351–361

    Google Scholar 

  • Stitt, M., Steup, M. (1985) Starch and sucrose degradation. In:Higher plant cell respiration, Encyclopedia of plant physiology, N.S., vol. 18, pp. 345–390, Douce, R., Day, D.A. eds Springer, Berlin Heidelberg New York

    Google Scholar 

  • van Berkel, J., Conrads-Strauch, J., Steup, M. (1991) Glucan-phosphorylase forms in cotyledons of Pisum sativum L.: Localization, developmental change, in-vitro translation, and processing. Planta 185, 432–439

    Google Scholar 

  • Varns, J.L., Sowokinos, J.R. (1974) A rapid micro-starch quantitation method for potato callus and its application with potato tubers. Am. Potato J. 51, 383–392

    Google Scholar 

  • Viola, R., Davies, H.V., Chudeck, A.R. (1991) Pathways of starch and sucrose biosynthesis in developing tubers of potato (Solanum tuberosum L.) and seeds of faba bean (Vicia faba L.). Elucidation by 13C-nuclear-magnetic-resonance spectroscopy. Planta 183, 202–208

    Google Scholar 

  • Weibull, J., Ronquist, F., Brishammar, S. (1990) Free amino acid composition of leaf exudates and phloem sap. Plant Physiol. 92, 222–226

    Google Scholar 

  • Wirtz, W, Stitt, M., Heldt, H.W. (1980) Enzymic determination of metabolites in the subcellular compartments of spinach protoplasts. Plant Physiol. 66, 187–193

    Google Scholar 

  • Yang, Y, Steup, M. (1990) Polysaccharide fraction from higher plants which strongly interacts with the cytosolic phosphorylase isozyme. I. Isolation and characterization. Plant Physiol. 94, 960–969

    Google Scholar 

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Correspondence to Normand Brisson.

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We thank C. Marineau, C. Bertrand and M. Dehbi for helpful advices, and A. Camirand for reviewing the manuscript. This work was supported by the Medical Research Council of Canada (MRC). B. St-P. was supported by a MRC studentship.

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St-Pierre, B., Brisson, N. Induction of the plastidic starch-phosphorylase gene in potato storage sink tissue. Planta 195, 339–344 (1995). https://doi.org/10.1007/BF00202590

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