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The pyridine-nucleotide cycle in tobacco

Enzyme activities for the recycling of NAD

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Abstract

In order to elucidate the NAD-recycling pathway the following enzyme activities have been characterized in different tobacco tissues and in tomato root: NAD pyrophosphatase, nicotinamide mononucleotide (NMN)/nicotinic acid mononucleotide (NaMN) glycohydrolases, nicotinamidase and nicotinic acid phosphoribosyltransferase. The investigations were performed with protein extracts purified by gel filtration and enzymatic activities were determined by high-performance liquid chromatography methods. The kinetic parameters of the different enzymes from tobacco root and their specificity are reported. The data are in favor of the so-called pyridine-nucleotide cycle VI (NAD→NMN→nicotinamide→nicotinic acid→NaMN→nicotinic acid adenine dinucleotide→NAD). In the nicotine-producing tobacco root a further direct route leading from NaMN to nicotinic acid is proposed. These data are reconciled with the assumption that it is nicotinic acid which is provided by the pyridine-nucleotide cycle for the synthesis of nicotine.

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Abbreviations

HPLC:

high-performance liquid chromatography

Na:

nicotinic acid

NaAD:

nicotinic acid adenine dinucleotide

NaMN:

nicotinic acid mononucleotide

NMN:

nicotinamide mononucleotide

PRPP:

5-phosphoribosyl-1-pyrophosphate

References

  • Andreoli, A.J., Okita, T.W., Bloom, R., Grover, T.A. (1972) The pyridine nucleotide cycle: presence of nicotinamide mononucleotide-specific glycohydrolase in Escherichia coli. Biochem. Biophys. Res. Commun. 49, 264–269

    Google Scholar 

  • Ashton, A.R., Polya, G.M. (1975) Higher plant cyclic nucleotide phosphodiesterases: Resolution, partial purification and properties of three phosphodiesterases from potato tuber. Biochem. J. 149, 329–339

    Google Scholar 

  • Bartkiewicz, M., Sierakowska, H., Shugar, D. (1984) Nucleotide pyrophosphatase from potato tubers. Purification and properties. Eur. J. Biochem. 143, 419–426

    Google Scholar 

  • Barz, W. (1985) Metabolism and degradation of nicotinic acid in plant cell cultures. In: Primary and secondary metabolism of plant cell cultures, pp. 186–195, Neumann, K.H., Barz, W., Reinhard, E., eds. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Bischoff, E., Tran-Thi, T.-A., Decker, K.F.A. (1975) Nucleotide pyrophosphatase of rat liver: A comparative study on the enzymes solubilized and purified from plasma membrane and endoplasmic reticulum. Eur. J. Biochem. 51, 353–361

    Google Scholar 

  • Bush, L.P., Saunders, J.L. (1977) Accumulation, manipulation and regulation of nicotine content in tobacco. Tob. Chem. Symp. (Am. Chem. Soc.) New Orleans, pp. 389–415

  • Clayton, R.A., Hanselman, L.M. (1960) Tobacco nucleotide pyrophosphatases. Arch. Biochem. Biophys. 87, 161–166

    Google Scholar 

  • Elliot, G.C. (1982) Evidence for a physiological active nicotinamide phosphoribosyltransferase in cultured human fibroblasts. Biochem. Biophys. Res. Commun. 104, 996–1002

    Google Scholar 

  • Foster, J.W., Moat, A.G. (1980) Nicotinamide adenine dinucleotide biosynthesis and pyridine nucleotide cycle metabolism in microbial systems. Microbiol. Rev. 44, 83–105

    Google Scholar 

  • Gholson, R.K. (1966) The pyridine nucleotide cycle. Nature 212, 933–935

    Google Scholar 

  • Godavari, H.R., Waygood, E.R. (1970) Nicotinamide adenine dinucleotide metabolism in plants. I. Intermediates of biosynthesis in wheat leaves and the effect of benzimidazole. Can. J. Bot. 48, 2267–2278

    Google Scholar 

  • Gopinathan, K.P., Sirsi, M., Vaidyanathan, C.S. (1964) Nicotinamide-adenine dinucleotide glycohydrolase of Mycobacterium tuberculosis H37Rv. Biochem. J. 91, 277–282

    Google Scholar 

  • Hanna, L.S., Hess, S.L., Sloan, D.L. (1983) Kinetic analysis of nicotinate phosphoribosyltransferase from yeast using high pressure liquid chromatography. J. Biol. Chem. 258, 9745–9754

    Google Scholar 

  • Hanna, L., Sloan, D.L. (1980) A high-pressure liquid chromatography procedure for monitoring nicotinate phosphoribosyltransferase activity. Anal. Biochem. 103, 230–234

    Google Scholar 

  • Hayakawa, T., Shibata, K., Iwai, K. (1984) Nicotinate phosphoribosyltransferase from hog liver: regulatory effect of ATP at a physiological concentration of 5-phosphoribosyl-1-pyrophosphate. Agric. Biol. Chem. 48, 455–460

    Google Scholar 

  • Hillyard, D., Rechsteiner, M., Manlapaz-Ramos, P., Imperial, J.S., Cruz, L.J., Olivera, B.M. (1981) The pyridine nucleotide cycle; studies in Escherichia coli and the human cell line D98/AH2. J. Biol. Chem. 256, 8491–8497

    Google Scholar 

  • Hilz, H., Koch, R., Fanick, W., Klapproth, K., Adamietz, P. (1984) Nonenzymatic ADP-ribosylation of specific mitochondrial polypeptides. Proc. Natl. Acad. Sci. USA 81, 3929–3933

    Google Scholar 

  • Imai, T. (1979) Isolation and properties of a glycohydrolase specific for nicotinamide mononucleotide from Azotobacter vinelandii. J. Biochem. 85, 887–899

    Google Scholar 

  • Imsande, J. (1961) Pathway of diphosphopyridine nucleotide biosynthesis in Escherichia coli. J. Biol. Chem. 236, 1494–1497

    Google Scholar 

  • Kole, E., Sierakowska, H., Shugar, D. (1976) Novel activity of potato nucleotide pyrophosphatase. Biochim. Biophys. Acta 438, 540–550

    Google Scholar 

  • Kornberg, A., Pricer, Jr., W.E. (1950) Nucleotide pyrophosphatase. J. Biol. Chem. 182, 763–778

    Google Scholar 

  • Mann, D.F., Byerrum, R.U. (1974) Activaton of the de novo pathway for pyridine nucleotide biosynthesis prior to ricine biosynthesis in Castor beans. Plant Physiol. 53, 603–609

    Google Scholar 

  • Marushige, T., Skoog, F. (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol. Plant. 15, 473–497

    Google Scholar 

  • Meyer, R. (1984) Die Ermittlung des Nucleotid pools in der pflanzlichen Zelle: Methodik und Anwendung. Thesis, Technische Universität, Braunschweig

    Google Scholar 

  • Mizusaki, S., Tanabe, Y., Kisaki, T., Tamaki, E. (1970) Metabolism of nicotinic acid in tobacco plants. Phytochemistry 9, 549–554

    Google Scholar 

  • Ohtsu, E., Nishizuka, Y. (1971) Nicotinamide phosphoribosyltransferase and NAD pyrophosphorylase from Lactobacillus fructosus. Methods Enzymol. 18 B, 127–132

    Google Scholar 

  • Olivera, B.M., Ferro, A.M. (1982) Pyridine nucleotide metabolism and ADP-ribosylation. In: ADP-ribosylation reactions; biology and medicine, pp. 19–40, Hayaishi, O., Ueda, K., eds. Academic Press, New York London

    Google Scholar 

  • Petrack, B., Greengard, P., Craston, A., Sheppy, F. (1965) Nicotinamide deamidase from mammalian liver. J. Biol. Chem. 240, 1725–1730

    Google Scholar 

  • Pietta, P., Pace, M., Menegus, F. (1983) High performance liquid chromatography for assaying NAD glycohydrolase from Neurospora crassa conidia. Anal. Biochem. 131, 533–537

    Google Scholar 

  • Razzel, W.E. (1966) Plant tissue phosphodiesterases. Biochem. Biophys. Res. Commun. 22, 243–247

    Google Scholar 

  • Roberts, D.W.A. (1959) The hydrolysis of diphosphopyridine nucleotide by juice expressed from wheat leaves. J. Biol. Chem. 234, 655–657

    Google Scholar 

  • Ryrie, I.J., Scott, K.J. (1969) Nicotinate, quinolinate and nicotinamide as precursors in the biosynthesis of nicotinamideadenine dinucleotide in barley. Biochem. J. 115, 679–685

    Google Scholar 

  • Sarma, D.S.R., Rajalakshmi, S., Sarma, P.S. (1961) Deamidation of nicotinamide and NMN. Biochem. Biophys. Res. Commun. 6, 389–393

    Google Scholar 

  • Sarma, D.S.R., Rajalakshmi, S., Sarma, P.S. (1964) Studies on the enzymes involved in nicotinamide adenine dinucleotide metabolism in Aspergillus niger. Biochim. Biophys. Acta 81, 311–322

    Google Scholar 

  • Sloan, D.L., Ali, L.Z., Aybar-Batista, D., Yan, C., Hess, S.L. (1984) Enzymatic assay procedures that employ high-performance liquid chromatography: competition between phosphoribosyltransferases for a common substrate. J. Chromatiogr. 316, 43–52

    Google Scholar 

  • Su, S., Chaykin, S. (1971) Nicotinamide deamidase. Methods Enzymol. 18B, 185–192

    Google Scholar 

  • Thomas, E., Davey, M.R. (1975) From single cells to plants, Wykeham Publications, London

    Google Scholar 

  • Thomzik, J. (1983) Untersuchungen zum Stoffwechsel von Nicotinsäure und ihren Derivaten in pflanzlichen Zellsuspensionskulturen und Pflanzen. Thesis, Universität Münster

  • Wagner, R. (1985) Der Pyridin-Nucleotid-Cyclus und die Regulation der Nicotinbiosynthese in Tabak. Thesis, Technische Universität Braunschweig

    Google Scholar 

  • Wagner, R., Wagner, K.G. (1984) Determination of quinolinic acid phosphoribosyltransferase in tobacco. Phytochemistry 23, 1881–1883

    Google Scholar 

  • Wagner, R., Wagner, K.G. (1985) The pyridine nucleotide cycle in tobacco. Enzyme activities for the de novo synthesis of NAD. Planta 165, 532–537

    Google Scholar 

  • Waller, G.R., Dermer, O.C. (1981) Enzymology of alkaloid metabolism in plants and microorganisms. Biochem. Plants 7, 317–402

    Google Scholar 

  • Waller, G.R., Yang, K.S., Gholson, R.K., Hadwiger, L.A., Chaykin, S. (1966) The pyridine nucleotide cycle and its role in the biosynthesis of ricine by Ricinus communis L. J. Biol. Chem. 241, 4411–4418

    Google Scholar 

  • Willmitzer, L. (1979) Demonstration of in vitro covalent modification of chromosomal proteins by poly (ADP) ribosylation in plant nuclei. FEBS Lett. 108, 13–16

    Google Scholar 

  • Willmitzer, L., Wagner, K.G. (1982) Poly (ADP-ribose) synthesis in plants. In: ADP-ribosylation reactions, biology and medicine, pp. 241–252, Hayaishi, O., Ueda, K., eds. Academic Press, New York London

    Google Scholar 

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This contribution is dedicated to Professor Augustin Betz on the occasion of his 65th birthday

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Wagner, R., Feth, F. & Wagner, K.G. The pyridine-nucleotide cycle in tobacco. Planta 167, 226–232 (1986). https://doi.org/10.1007/BF00391419

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