Caffeine and related purine alkaloids: Biosynthesis, catabolism, function and genetic engineering

Phytochemistry

Volumn 69, Issue 4, 2008, Pages 841-856

  Ashihara, Hiroshi ^a   Sano, Hiroshi ^b   Crozier, Alan ^c  

^a OCHANOMIZU UNIVERSITY   (Japan)

^b STOCKHOLM UNIVERSITY   (Sweden)

^c UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

Caffeine; Camellia sinensis; Coffea sp.; Metabolism; Review; Rubiaceae; Sterculiaceae; Theaceae; Theobroma cacao

Indexed keywords

ALKALOID; CAFFEINE; PURINE; PURINE DERIVATIVE;

BIOSYNTHESIS; CACAO; COFFEE; GENETICS; ILEX; METABOLISM; REVIEW; TEA; TRANSGENIC PLANT;

ALKALOIDS; CACAO; CAFFEINE; CAMELLIA; COFFEA; ILEX; PLANTS, GENETICALLY MODIFIED; PURINES;

CAMELLIA; CAMELLIA SINENSIS; COFFEA; ILEX; MALVACEAE; NICOTIANA OBTUSIFOLIA; NICOTIANA TABACUM; RUBIACEAE; THEACEAE; THEOBROMA; THEOBROMA CACAO;

EID: 39149121177     PISSN: 00319422     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.phytochem.2007.10.029     Document Type: Review

References (94)

1. Anan T., and Nakagawa M. Effect of light on chemical constituents in the tea leaves. Nippon Nogeikagaku Kaishi 48 (1974) 91-98
2. Anaya A.L., Cruz-Ortega R., and Waller G.R. Metabolism and ecology of purine alkaloids. Front. Biosci. 11 (2006) 2354-2370
3. Aneja M., and Gianfagna T. Induction and accumulation of caffeine in young, actively growing leaves of cocoa (Theobroma cacao L.) by wounding or infection with Crinipellis perniciosa. Physiol. Mol. Plant Pathol. 59 (2001) 13-16
4. Ashihara H. Purine metabolism and the biosynthesis of caffeine in maté leaves. Phytochemistry 33 (1993) 1427-1430
5. Ashihara H., and Crozier A. Biosynthesis and metabolism of caffeine and related purine alkaloids in plants. Adv. Bot. Res. 30 (1999) 118-205
6. Ashihara H., and Crozier A. Biosynthesis and catabolism of caffeine in low-caffeine-containing species of Coffea. J. Agric. Food Chem. 47 (1999) 3425-3431
7. Ashihara H., Gillies F.M., and Crozier A. Metabolism of caffeine and related purine alkaloids in leaves of tea (C amellia sinensis L.). Plant Cell Physiol. 38 (1997) 413-419
8. Ashihara H., Kato M., and Ye C.-X. Biosynthesis and metabolism of purine alkaloids in leaves of cocoa tea (Camellia ptilophylla). J. Plant Res. 111 (1998) 599-604
9. Ashihara H., and Kubota H. Patterns of adenine metabolism and caffeine biosynthesis in different parts of tea seedlings. Physiol. Plant. 68 (1986) 275-281
10. Ashihara H., and Kubota H. Biosynthesis of purine alkaloids in Camellia plants. Plant Cell Physiol. 28 (1987) 535-539
11. Ashihara H., Monteiro A.M., Moritz T., Gillies F.M., and Crozier A. Catabolism of caffeine and related purine alkaloids in leaves of Coffea arabica L. Planta 198 (1996) 334-339
12. Ashihara H., and Suzuki T. Distribution and biosynthesis of caffeine in plants. Front. Biosci. 9 (2004) 1864-1876
13. Ashihara H., Takasawa Y., and Suzuki T. Metabolic fate of guanosine in higher plants. Physiol. Plant 100 (1997) 909-916
14. Ashihara H., Zheng X.Q., Katahira R., Morimoto M., Ogita S., and Sano H. Caffeine biosynthesis and adenine metabolism in transgenic Coffea canephora plants with reduced expression of N-methyltransferase genes. Phytochemistry 67 (2006) 882-886
15. Athaydea M.L., Coelhob G.C., and Schenkel E.P. Caffeine and theobromine in epicuticular wax of Ilex paraguariensis A. St.-Hil. Phytochemistry 55 (2000) 853-857
16. Bailey B.A., Bae H., Strem M.D., Bowers J.H., Antéz de Mayolo G., Guiltinan M.J., Verica J.A., and Maximova S.N. Developmental expression of stress response genes in Theobroma cacao leaves and their response to Nep1 treatment and a compatible infection by Phytophthora megakarya. Plant Physiol. Biochem. 43 (2005) 611-622
17. Baker B., Zambryski P., Staskawicz B., and Dinesh-Kumar S.P. Signaling in plant-microbe interactions. Science 267 (1997) 726-733
18. Baumann T.W., Oechslin M., and Wanner H. Caffeine and methylated uric acids: chemical patterns during vegetative development of Coffea liberica. Biochem. Physiol. Pflanzen. 170 (1976) 217-225
19. Baumann T.W., and Wanner H. The 1,3,7,9-tetramethyluric acid content of cupu (Theobroma grandiflorum). Acta Amaz. 10 (1980) 425
20. Baumann T.W., Schulthess B.H., and Hanni K. Guarana (Paullinia cupana) rewards seed dispersers without intoxicating them by caffeine. Phytochemistry 39 (1995) 1063-1070
21. Chang H., Ye C., Zhang R., Ma Y., and Zhang P. A discovery of new tea resource Cocoa tea tree containing theobromine from China. Acta Sci. Natur. Univ. Sunyatseni 27 (1988) 131-133
22. Coelho G.C., Rachwal M.F.G., Dedecek R.A., Curcio G.R., Nietsche K., and Schenkel E.P. Effect of light intensity on methylxanthine contents of Ilex paraguariensis A. St. Hil. Biochem. System. Ecol. 35 (2007) 75-80
23. Clifford M.N., Gibson C.L., Rakotomalala J.-J.R., Cros E., and Charrier A. Caffeine from green beans of Mascarocoffea. Phytochemistry 30 (1991) 4039-4040
24. Frischknecht P.M., Ulmer-Dufek J., and Baumann T.W. Purine alkaloid formation in buds and developing leaflets of Coffea arabica: expression of an optimal defence strategy?. Phytochemistry 25 (1986) 613-616
25. Fujimori N., and Ashihara H. Adenine metabolism and the synthesis of purine alkaloids in flowers of Camellia plants. Phytochemistry 29 (1990) 3513-3516
26. Fujimori N., and Ashihara H. Biosynthesis of theobromine and caffeine in developing leaves of Coffea arabica. Phytochemistry 36 (1994) 1359-1361
27. Fujimori N., Suzuki T., and Ashihara H. Seasonal variations in biosynthetic capacity for the synthesis of caffeine in tea leaves. Phytochemistry 30 (1991) 2245-2248
28. Gluck M., and Lingens F. Heteroxanthinedemethylase, a new enzyme in the degradation of caffeine by Pseudomonas putida. Appl. Microbiol. Biotechnol. 28 (1988) 59-62
29. Green T.R., and Ryan C.A. Wound-induced protease inhibitor in plant leaves: a possible defense mechanism against insects. Science 175 (1972) 776-777
30. Guerreiro Filho O., and Mazzafera P. Caffeine and resistance of coffee to the berry borer Hypothenemus hampei (Coleoptera: Scolytidae). J. Agric. Food Chem. 51 (2003) 6987-6991
31. Hammerstone J.F., Romanczyk L.J., and Aitken W.M. Purine alkaloid distribution within Herrania and Theobroma. Phytochemistry 35 (1994) 1237-1240
32. Hohnloser W., Osswald B., and Lingens F. Enzymological aspects of caffeine demethylation and formaldehyde oxidation by Pseudomonas putida C1. Hoppe Seyler's Z. Physiol. Chem. 361 (1980) 1763-1766
33. Hollingsworth R.G., Armstrong J.W., and Campbell E. Caffeine as a repellent for slugs and snails. Nature 417 (2002) 915-916
34. Huber, M., Baumann, T.W., 1998. The first step of caffeine degradation in coffee - still a mistery. In: Symposium Future Trends in Phytochemistry. The Phytochemical Society of Europe, Rolduc, The Netherlands.
35. Ito E., and Ashihara H. Contribution of purine nucleotide biosynthesis de novo to the formation of caffeine in young tea (Camellia sinensis) leaves. J. Plant Physiol. 254 (1999) 145-151
36. Ito E., Crozier A., and Ashihara H. Theophylline metabolism in higher plants. Biochim. Biophys. Acta 1336 (1997) 323-330
37. Iwasaki, M., 2006. Alkaloid metabolism in cacao (Theobroma cacao) plants. B.Sc Thesis, Faculty of Science, Ochanomizu University.
38. Jouanin L., Bonade-Bottino M., Girard C., Morrot G., and Giband M. Transgenic plants for insect resistance. Plant Sci. 131 (1998) 1-11
39. Kalberer P. Breakdown of caffeine in the leaves of Coffea arabica L. Nature 205 (1965) 597-598
40. Kodama, Y., Shinya, T., Sano, H., 2007. Dimerization of N-methyltransferases involved in caffeine biosynthesis. Biochimie, in press. doi:10.1016/j.biochi.2007.10.001.
41. Kato M., and Mizuno K. Caffeine synthase and related methyltransferases in plants. Front. Biosci. 9 (2004) 1833-1842
42. Kato M., Mizuno K., Crozier A., Fujimura T., and Ashihara H. A gene encoding caffeine synthase from tea leaves. Nature 406 (2000) 956-957
43. Kato M., Mizuno K., Fujimura T., Iwama M., Irie M., Crozier A., and Ashihara H. Purification and characterization of caffeine synthase from tea leaves. Plant Physiol. 120 (1999) 586-597
44. Keya C.A., Crozier A., and Ashihara H. Inhibition of caffeine biosynthesis in tea (Camellia sinensis) and coffee (Coffea arabica) plants by ribavirin. FEBS Lett. 554 (2003) 473-477
45. Kim Y.-S., Uefuji H., Ogita S., and Sano H. Transgenic tobacco plants producing caffeine: a potential new strategy for insect pest control. Transgenic Res. 15 (2006) 667-672
46. Kim, Y.-S., Sano, H., 2007. Pathogen resistance in transgenic tobacco plants producing caffeine. Phytochemistry, in press. doi:10.1016/j.phytochem.2007.10.021.
47. Koshiishi C., Ito E., Kato A., Yoshida Y., Crozier A., and Ashihara H. Purine alkaloid biosynthesis in young leaves of Camellia sinensis in light and darkness. J. Plant Res. 113 (2000) 217-221
48. Koshiishi C., Kato A., Yama S., Crozier A., and Ashihara H. A new caffeine biosynthetic pathway in tea leaves: utilisation of adenosine released from the S-adenosyl-L-methionine cycle. FEBS Lett. 499 (2001) 50-54
49. Koshiro Y., Zheng X.Q., Wang M., Nagai C., and Ashihara H. Changes in content and biosynthetic activity of caffeine and trigonelline during growth and ripening of Coffea arabica and Coffea canephora fruits. Plant Sci. 171 (2006) 242-250
50. Koyama Y., Tomoda Y., Kato M., and Ashihara H. Metabolism of purine bases, nucleosides and alkaloids in theobromine-forming Theobroma cacao leaves. Plant Physiol. Biochem. 41 (2003) 977-984
51. Kretschmar J.A., and Baumann T.W. Caffeine in Citrus flowers. Phytochemistry 52 (1999) 19-23
52. Kumar N.S., Hewavitharanage P., and Adikaram N.K.B. Attack on tea by Xyleborus fornicatus: inhibition of the symbiote, Monacrosporium ambrosium, by caffeine. Phytochemistry 40 (1995) 1113-1116
53. Li,Y., Ogita, S., Keya, C.A., Ashihara, H., accepted for publication. Expression of caffeine biosynthesis genes in tea (Camellia sinensis). Z. Naturforsch. 62c.
54. Marx F., Jannssen M.J.J., Urfer P., and Scherer R. Caffeine and theobromine composition of maté (Ilex paraguariensis) leaves in five plantations of Misiones, Argentina. Plant Foods Human Nutr. 58 (2003) 1-8
55. Mazzafera P. 7-Methylxanthine is not involved in caffeine catabolism in Coffea dewevrei. J. Agric. Food Chem. 41 (1993) 1541-1543
56. Mazzafera P. Caffeine, theobromine and theophylline distribution in Ilex paraguariensis. Rev. Brasil Fisiol. Veg. 6 (1994) 149-151
57. Mazzafera P. Growth and biochemical alterations in coffee due to selenite toxicity. Plant Soil 201 (1998) 189-196
58. Mazzafera P. Catabolism of caffeine in plants and microorganisms. Front. Biosci. 9 (2004) 1348-1359
59. Mazzafera P., and Carvalho A. Breeding for low seed caffeine content of coffee (Coffea L.) by interspecific hybridization. Euphytica 59 (1992) 55-60
60. McCarthy A.A., and McCarthy J.G. The structure of two N-methyltransferases from the caffeine biosynthetic pathway. Plant Physiol. 144 (2007) 879-889
61. Mizuno K., Kato M., Irino F., Yoneyama N., Fujimura T., and Ashihara H. The first committed step reaction of caffeine biosynthesis: 7-methylxanthosine synthase is closely homologous to caffeine synthases in coffee (Coffea arabica L.). FEBS Lett. 547 (2003) 56-60
62. Mizuno K., Okuda A., Kato M., Yoneyama N., Tanaka H., Ashihara H., and Fujimura T. Isolation of a new dual-functional caffeine synthase gene encoding an enzyme for the conversion of 7-methylxanthine to caffeine from coffee (Coffea arabica L.). FEBS Lett. 534 (2003) 75-81
63. Mizuno K., Tanaka H., Kato M., Ashihara H., and Fujimura T. cDNA cloning of caffeine (theobromine) synthase from coffee (Coffea arabica L.). Proceedings of the 19th International Conference on Coffee Science, Treiste (2001), ASIC, Paris pp. 815-818
64. Nagata T., and Sakai S. Differences in caffeine, flavanols and amino acids contents in leaves of cultivated species of Camellia. Jpn. J. Breed. 34 (1984) 459-467
65. Nathanson J.A. Caffeine and related methylxanthines: possible naturally occurring pesticides. Science 226 (1984) 184-187
66. Negishi O., Ozawa T., and Imagawa H. N-methylnucleosidase from tea leaves. Agric. Biol. Chem. 52 (1988) 169-175
67. Negishi O., Ozawa T., and Imagawa H. Guanosine deaminase and guanine deaminase from tea leaves. Biosci. Biotech. Biochem. 58 (1994) 1277-1281
68. Ogawa M., Herai Y., Koizumi N., Kusano T., and Sano H. 7-Methylxanthine methyltransferase of coffee plants: gene isolation and enzymatic properties. J. Biol. Chem. 276 (2001) 8213-8218
69. Ogita S., Uefuji H., Yamaguchi Y., Koizumi N., and Sano H. Production of decaffeinated coffee plants by genetic engineering. Nature 423 (2003) 823
70. Ogita S., Uefuji H., Morimoto M., and Sano H. Application of RNAi to confirm theobromine as the major intermediate for caffeine biosynthesis in coffee plants with potential for construction of decaffeinated varieties. Plant Mol. Biol. 54 (2004) 931-941
71. Ogita S., Uefuji H., Morimoto M., and Sano H. Metabolic engineering of caffeine production. Plant Biotechnol. 22 (2005) 461-468
72. Ohta S., Mita S., Hattori T., and Nakamura K. Construction and expression in tobacco of a β-glucuronidase (GUS) reporter gene containing an intron within the coding sequence. Plant Cell Physiol. 31 (1990) 805-813
73. Petermann J., and Baumann T.W. Metabolic relations between methylxanthines and methyluric acids in Coffea. Plant Physiol. 73 (1983) 961-964
74. Saijo R. Effect of shade treatment on biosynthesis of catechins in tea plants. Plant Cell Physiol. 21 (1980) 989-998
75. Schulthess B.H., Morath P., and Baumann T.W. Caffeine biosynthesis starts with the metabolically channelled formation of 7-methyl-XMP - a new hypothesis. Phytochemistry 41 (1996) 169-175
76. Senanayake U.M., and Wijesekera R.O.B. Theobromine and caffeine content of the cocoa bean during its growth. J. Sci. Food Agric. 22 (1971) 262-263
77. Silvarolla M.B., Mazzafera P., and Fazuoli L.C. A naturally decaffeinated arabica coffee. Nature 429 (2004) 826
78. Stasolla C., Katahira R., Thorpe T.A., and Ashihara H. Purine and pyrimidine nucleotide metabolism in higher plants. J. Plant Physiol. 160 (2003) 1271-1295
79. Suzuki T., and Waller G.R. Biodegradation of caffeine: formation of theophylline and caffeine in mature Coffea arabica fruits. J. Sci. Food Agric. 35 (1984) 66-70
80. Suzuki T., and Waller G.R. Purine alkaloids of fruits of Camellia sinensis L. and Coffea arabica L. during fruit development. Ann. Bot. 56 (1985) 537-542
81. Suzuki T., Ashihara H., and Waller G.R. Purine and purine alkaloid metabolism in Camellia and Coffea plants. Phytochemistry 31 (1992) 2575-2584
82. Terrasaki Y., Suzuki T., and Ashihara H. Purine metabolism and the biosynthesis of purine alkaloids in tea fruits during development. Plant Physiol. (Life Sci. Adv.) 13 (1994) 135-142
83. Uefuji H., Ogita S., Yamaguchi Y., Koizumi N., and Sano H. Molecular cloning and functional characterization of three distinct N-methyltransferases involved in the caffeine biosynthetic pathway in coffee plants. Plant Physiol. 132 (2003) 372-380
84. Uefuji H., Tatsumi Y., Morimoto M., Kaothien-Nakayama P., Ogita S., and Sano H. Caffeine production in tobacco plants by simultaneous expression of three coffee N-methyltransferases and its potential as a pest repellant. Plant Mol. Biol. 59 (2005) 221-227
85. Vitória A.P., and Mazzafera P. Caffeine degradation in leaves and fruits of Coffea arabica and Coffea dewevrei. Pesquisa Agropecuaria Brasil 33 (1998) 1957-1961
86. Weckerle C.S., Stutz M.A., and Baumann T.W. Purine alkaloids in Paullinia. Phytochemistry 64 (2003) 735-742
87. Ye C., Un Y., Zhou H., Cheng F., and Li X. Isolation and analysis of purine alkaloids from Camellia ptilophylla Chang. Acta Sci. Natur. Univ. Sunyatseni 36 (1997) 30-33
88. Yoneyama N., Morimoto H., Ye C.X., Ashihara H., Mizuno K., and Kato M. Substrate specificity of N-methyltransferase involved in purine alkaloids synthesis is dependent upon one amino acid residue of the enzyme. Mol. Gen. Genom. 275 (2006) 125-135
89. Zheng X.Q., Koyama Y., Nagai C., and Ashihara H. Biosynthesis, accumulation and degradation of theobromine in developing Theobroma cacao fruits. J. Plant Physiol. 161 (2004) 363-369
90. Zheng X.Q., and Ashihara H. Distribution, biosynthesis and function of purine and pyridine alkaloids in Coffea arabica seedlings. Plant Sci. 166 (2004) 807-813
91. Zheng X.Q., Ye C.X., Kato M., Crozier A., and Ashihara H. Theacrine (1,3,7,9-tetramethyluric acid) synthesis in leaves of a Chinese tea, kucha (Camellia assamica var. kucha). Phytochemistry 60 (2002) 129-134
92. Zrenner R., Stitt M., Sonnewald U., and Boldt R. Pyrimidine and purine biosynthesis and degradation in plants. Annu. Rev. Plant Biol. 57 (2006) 805-836
93. Zubieta C., Ross J.R., Koscheski P., Yang Y., Pichersky E., and Noel J.P. Structural basis for substrate recognition in the salicylic acid carboxyl methyltransferase family. Plant Cell 15 (2003) 1704-1716
94. Zulak K.G., Liscome D.K., Ashihara H., and Facchini P.J. Alkaloids. In: Crozier A., Clifford M.N., and Ashihara H. (Eds). Plant Secondary Metabolites: Occurrence Structure, and Role in the Human Diet (2006), Blackwell, Oxford 102-136