Abstract
Pyridine compounds, including nicotinic acid and nicotinamide, are key metabolites of both the salvage pathway for NAD and the biosynthesis of related secondary compounds. We examined the in situ metabolic fate of [carbonyl-14C]nicotinamide, [2-14C]nicotinic acid and [carboxyl-14C]nicotinic acid riboside in tissue segments of tea (Camellia sinensis) plants, and determined the activity of enzymes involved in pyridine metabolism in protein extracts from young tea leaves. Exogenously supplied 14C-labelled nicotinamide was readily converted to nicotinic acid, and some nicotinic acid was salvaged to nicotinic acid mononucleotide and then utilized for the synthesis of NAD and NADP. The nicotinic acid riboside salvage pathway discovered recently in mungbean cotyledons is also operative in tea leaves. Nicotinic acid was converted to nicotinic acid N-glucoside, but not to trigonelline (N-methylnicotinic acid), in any part of tea seedlings. Active catabolism of nicotinic acid was observed in tea leaves. The fate of [2-14C]nicotinic acid indicates that glutaric acid is a major catabolite of nicotinic acid; it was further metabolised, and carbon atoms were finally released as CO2. The catabolic pathway observed in tea leaves appears to start with the nicotinic acid N-glucoside formation; this pathway differs from catabolic pathways observed in microorganisms. Profiles of pyridine metabolism in tea plants are discussed.
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Ashihara H, Stasolla C, Yin Y, Loukanina N, Thorpe TA (2005) De novo and salvage biosynthetic pathways of pyridine nucleotides and nicotinic acid conjugates in cultured plant cells. Plant Sci 169:107–114
Ashihara H, Luit B, Belmonte M, Stasolla C (2008) Metabolism of nicotinamide, adenine and inosine in developing microspore-derived canola (Brassica napus) embryos. Plant Physiol Biochem 46:752–759
Ashihara H, Deng W-W, Mullen W, Crozier A (2010) Distribution and biosynthesis of flavan-3-ols in Camellia sinensis seedlings and expression of genes encoding biosynthetic enzymes. Phytochemistry 71:559–566
Ashihara H, Deng W-W, Nagai C (2011a) Trigonelline biosynthesis and the pyridine nucleotide cycle in Coffea arabica fruits: metabolic fate of [carboxyl-14C]nicotinic acid riboside. Phytochem Lett 4:235–239
Ashihara H, Yin Y, Watanabe S (2011b) Nicotinamide metabolism in ferns: Formation of nicotinic acid glucoside. Plant Physiol Biochem 49:275–279
Barz W (1985) Metabolism and degradation of nicotinic acid in plant cell cultures. In: Neumann KH, Barz W, Reinhard E (eds) Primary and secondary metabolism of plant cell cultures. Springer, Berlin, pp 186–195
Berger F, Ramirez-Hernandez MH, Ziegler M (2004) The new life of a centenarian: signalling functions of NAD(P). Trends Biochem Sci 29:111–118
Bieganowski P, Brenner C (2004) Discoveries of nicotinamide riboside as a nutrient and conserved NRK genes establish a Preiss–Handler independent route to NAD+ in fungi and humans. Cell 117:495–502
Crozier A, Ashihara H, Tomas-Barberan F (2011) Teas, cocoa and coffee: plant secondary metabolites and health. Wiley-Blackwell, Oxford
Deng W-W, Ashihara H (2010) Profiles of purine metabolism in leaves and roots of Camellia sinensis seedlings. Plant Cell Physiol 51:2105–2118
Deng W-W, Ogita S, Ashihara H (2008) Biosynthesis of theanine (γ-ethylamino-l-glutamic acid) in seedlings of Camellia sinensis. Phytochem Lett 1:115–119
Deng W-W, Ogita S, Ashihara H (2010) Distribution and biosynthesis of theanine in Theaceae plants. Plant Physiol Biochem 48:70–72
Gholson RK (1966) The pyridine nucleotide cycle. Nature 212:933–935
Hashida SN, Takahashi H, Uchimiya H (2009) The role of NAD biosynthesis in plant development and stress responses. Ann Bot 103:819–824
Hiles RA, Byerrum RU (1969) The role of the pyridine nucleotide cycle in the biosynthesis of ricinine. Phytochemistry 8:1927–1930
Hunt L, Lerner F, Ziegler M (2004) NAD—new roles in signalling and gene regulation in plants. New Phytol 163:31–44
Jiménez JI, Canales Á, Jiménez-Barbero J, Ginalski K, Rychlewski L, García JL, Díaz E (2008) Deciphering the genetic determinants for aerobic nicotinic acid degradation: the nic cluster from Pseudomonas putida KT2440. Proc Natl Acad Sci 105:11329–11334
Katahira R, Ashihara H (2009) Profiles of the biosynthesis and metabolism of pyridine nucleotides in potatoes (Solanum tuberosum L.). Planta 231:35–42
Katoh A, Hashimoto T (2004) Molecular biology of pyridine nucleotide and nicotine biosynthesis. Front Biosci 9:1577–1586
Katoh A, Uenohara K, Akita M, Hashimoto T (2006) Early steps in the biosynthesis of NAD in Arabidopsis start with aspartate and occur in the plastid. Plant Physiol 141:851–857
Komoßa D, Barz W (1988) Glutaric acid as a catabolites of nicotinic acid in parsley cell suspension cultures. Z Naturforsch 43c:843–849
Matsui A, Ashihara H (2008) Nicotinate riboside salvage in plants: Presence of nicotinate riboside kinase in mungbean seedlings. Plant Physiol Biochem 46:104–108
Matsui A, Yin Y, Yamanaka K, Iwasaki M, Ashihara H (2007) Metabolic fate of nicotinamide in higher plants. Physiol Plant 131:191–200
Mizusaki S, Tanabe Y, Kisaki T, Tamaki E (1970) Metabolism of nicotinic acid in tobacco plants. Phytochemistry 9:549–554
Moat AG, Foster JW (1987) Biosynthesis and salvage pathways of pyridine nucleotides. In: Dolphin D, Avramovic O, Poulson R (eds) Pyridine nucleotide coenzymes chemical, biochemical, and medical aspects, part B. Wiley, New York, pp 1–24
Noctor G, Queval G, Gakiere B (2006) NAD(P) synthesis and pyridine nucleotide cycling in plants and their potential importance in stress conditions. J Exp Bot 57:1603–1620
Noctor G, Hager J, Li S (2011) Biosynthesis of NAD and its manipulation in plants. In: Fabrice R, Roland D (eds) Advances in botanical research, vol 58. Academic Press, London, pp 153–201
Rongvaux A, Andris F, Van Gool F, Leo O (2003) Reconstructing eukaryotic NAD metabolism. BioEssays 25:683–690
Shoji T, Hashimoto T (2011) Nicotine biosynthesis. In: Ashihara H, Crozier A, Komamine A (eds) Plant metabolism and biotechnology. Wiley, Chichester, pp 191–216
Upmeier B, Thomzik JE, Barz W (1988) Nicotinic acid-N-glucoside in heterotrophic parsley cell suspension cultures. Phytochemistry 27:3489–3493
Wagner R, Feth F, Wagner KG (1986) The pyridine-nucleotide cycle in tobacco: enzyme activities for the recycling of NAD. Planta 167:226–232
Waller GR, Yang KS, Gholson RK, Hadwiger LA, Chaykin S (1966) The pyridine nucleotide cycle and its role in the biosynthesis of ricinine by Ricinus communis L. J Biol Chem 241:4411–4418
Willeke U, Heeger V, Meise M, Neuhann H, Schindelmeiser I, Vordemfelde K, Barz W (1979) Mutually exclusive occurrence and metabolism of trigonelline and nicotinic acid arabinoside in plant cell cultures. Phytochemistry 18:105–110
Zheng XQ, Ashihara H (2004) Distribution, biosynthesis and function of purine and pyridine alkaloids in Coffea arabica seedlings. Plant Sci 166:807–813
Zheng XQ, Nagai C, Ashihara H (2004) Pyridine nucleotide cycle and trigonelline (N-methylnicotinic acid) synthesis in developing leaves and fruits of Coffea arabica. Physiol Plant 122:404–411
Zrenner R, Ashihara H (2011) Nucleotide Metabolism. In: Ashihara H, Crozier A, Komamine A (eds) Plant metabolism and biotechnology. Wiley, Chichester, pp 135–162
Acknowledgments
We thank Dr. Junichi Tanaka (National Institute of Vegetable and Tea Science, Japan) and Dr. Eduardo Diaz (Centro de Investigaciones Biologicas, Madrid, Spain) for their generous supply of plant materials and pyridine standards. The authors also wish to thank Professor Alan Crozier, University of Glasgow, U.K. for his critical evaluation of the text and linguistic advice during the preparation of the final version of the paper. This research was supported by a JSPS Grant-in-Aid for Scientific Research (No. 22510226).
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Ashihara, H., Deng, WW. Pyridine metabolism in tea plants: salvage, conjugate formation and catabolism. J Plant Res 125, 781–791 (2012). https://doi.org/10.1007/s10265-012-0490-x
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DOI: https://doi.org/10.1007/s10265-012-0490-x