Three nicotine demethylase genes mediate nornicotine biosynthesis in Nicotiana tabacum L.: Functional characterization of the CYP82E10 gene

Phytochemistry

Volumn 71, Issue 17-18, 2010, Pages 1988-1998

  Lewis, Ramsey S ^a   Bowen, Steven W ^a   Keogh, Matthew R ^a   Dewey, Ralph E ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

Alkaloids; CYP82E10; Cytochrome P450; Gene function; Nicotiana tabacum; Nornicotine; Solanaceae; Tobacco specific nitrosamine (TSNA)

Indexed keywords

CARCINOGEN; CYTOCHROME P450; DRUG DERIVATIVE; N'-NITROSONORNICOTINE; NICOTINE; NICOTINE DEMETHYLASE, TOBACCO; NITROSAMINE; NITROSONORNICOTINE; NORNICOTINE; VEGETABLE PROTEIN;

ARTICLE; BIOSYNTHESIS; CHEMICAL STRUCTURE; CHEMISTRY; ENZYMOLOGY; GENETICS; METABOLISM; PLANT LEAF; TOBACCO;

CARCINOGENS; CYTOCHROME P-450 ENZYME SYSTEM; MOLECULAR STRUCTURE; NICOTINE; NITROSAMINES; PLANT LEAVES; PLANT PROTEINS; TOBACCO;

ANIMALIA; MAGNOLIOPHYTA; NICOTIANA TABACUM; SOLANACEAE;

EID: 78249275539     PISSN: 00319422     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.phytochem.2010.09.011     Document Type: Article

References (37)

1. S.F. Altschul, W. Gish, W. Miller, E.W. Myers, and D.J. Lipman Basic local alignment search tool J. Mol. Biol. 215 1990 403 410
2. S.F. Altschul, T.L. Madden, A.A. Schaffer, J. Zhang, Z. Zhang, W. Miller, and D.J. Lipman Gapped BLAST and PSI-BLAST: a new generation of protein database search programs Nucl. Acids Res. 25 1997 3389 3402
3. I.T. Baldwin Mechanism of damage-induced alkaloid production in wild tobacco J. Chem. Ecol. 15 1989 1661 1680
4. M.D. Boyette, and L.A. Hamm Results of year 2000 TSNA sampling program in flue-cured tobacco Rec. Adv. Tob. Sci. 27 2001 17 22
5. A.P. Brogan, T.J. Dickerson, G.E. Boldt, and K.D. Janda Altered retinoid homeostasis catalyzed by a nicotine metabolite: implications in macular degeneration and normal development Proc. Natl. Acad. Sci. USA 102 2005 10433 10438
6. L.P. Bush, W.P. Hempfling, and H. Burton Biosynthesis of nicotine and related compounds J.W. Gorrod, P. Jacob, Analytical Determination of Nicotine and Related Compounds and Their Metabolites 1999 Elsevier New York 13 44
7. L.P. Bush, M. Cui, H. Shi, H.R. Burton, F.F. Fannin, L. Lei, and N. Dye Formation of tobacco-specific nitrosamines in air-cured tobacco Rec. Adv. Tob. Sci. 27 2001 23 46
8. M. Chakrabarti, K.M. Meekins, L.B. Gavilano, and B. Siminszky Inactivation of the cytochrome P450 gene CYP82E2 by degenerative mutations was a key event in the evolution of the alkaloid profile of modern tobacco New Phytol. 175 2007 565 574
9. M. Chakrabarti, S.W. Bowen, N.P. Coleman, K.M. Meekins, R.E. Dewey, and B. Siminszky CYP82E4-mediated nicotine to nornicotine conversion in tobacco is regulated by a senescence-specific signaling pathway Plant Mol. Biol. 66 2008 415 427
10. T.J. Dickerson, and K.D. Janda A previously undescribed chemical link between smoking and metabolic disease Proc. Natl. Acad. Sci. USA 99 2002 15084 15088
11. L.B. Gavilano, and B. Siminszky Isolation and characterization of the cytochrome P450 gene CYP82E5v2 that mediates nicotine to nornicotine conversion in the green leaves of tobacco Plant Cell Physiol. 48 2007 1567 1574
12. L.B. Gavilano, N.P. Coleman, L.-E. Burnley, M.L. Bowman, N.E. Kalengamaliro, A. Hayes, L. Bush, and B. Siminszky Genetic engineering of Nicotiana tabacum for reduced nornicotine content J. Agric. Food. Chem. 54 2006 9071 9078
13. L.B. Gavilano, N.P. Coleman, S.W. Bowen, and B. Siminszky Functional analysis of nicotine demethylase genes reveals insights into the evolution of modern tobacco J. Biol. Chem. 282 2007 249 256
14. D. Geitz, A. Stjean, R.A. Woods, and R.H. Schiestl Improved method for high-efficiency transformation of intact yeast cells Nucl. Acids Res. 20 1992 1425
15. T. Hashimoto, and Y. Yamada New genes in alkaloid metabolism and transport Curr. Opin. Biotechnol. 14 2003 163 168
16. S.S. Hecht Tobacco carcinogens, their biomarkers and tobacco-induced cancer Nat. Rev. Cancer 3 2003 733 744
17. S.S. Hecht, and D. Hoffmann The relevance of tobacco specific nitrosamines to human cancer Cancer Surv. 8 1990 273 294
18. W.G. Heim, K.A. Sykes, S.B. Hildreth, J. Sun, R.-H. Lu, and J.G. Jelesko Cloning and characterization of a Nicotiana tabacum methylputrescine oxidase transcript Phytochemistry 68 2007 454 463
19. D. Hoffmann, K.D. Brunnemann, B. Prokopczyk, and M.V. Djordjevic Tobacco-specific N-nitrosamines and Areca-derived N-nitrosamine chemistry, biochemistry, carcinogenicity and relevance to humans J. Toxicol. Environ. Health 41 1994 1 52
20. A. Jack, N. Fannin, and L.P. Bush Implications of reducing nornicotine accumulation in burley tobacco: appendix A - the LC protocol Rec. Adv. Tob. Sci. 33 2007 58 79
21. E. Julio, F. Laporte, S. Reis, C. Rothan, and F. Dorlhac de Borne Reducing the content of nornicotine in tobacco via targeted mutation breeding Mol. Breed. 21 2008 369 381
22. A. Katoh, T. Shoji, and T. Hashimoto Molecular cloning of N-methylputrescine oxidase from tobacco Plant Cell Physiol. 48 2007 550 554
23. J. Katz, R.M. Caudle, I. Bhattacharyya, C.M. Stewart, and D.M. Cohen Receptor for advanced glycation end product (RAGE) upregulation in human gingival fibroblasts incubated with nornicotine J. Periodontol. 76 2005 1171 1174
24. R.S. Lewis, A.M. Jack, J.W. Morris, V.J.M. Robert, L. Gavilano, B. Siminszky, L.P. Bush, A.J. Hayes, and R.E. Dewey RNAi-induced suppression of nicotine demethylase activity reduces levels of a key carcinogen in cured tobacco leaves Plant Biotech. J. 6 2008 346 354
25. T.J. Mann, J.A. Weybrew, D.F. Matzinger, and J.F. Hall Inheritance of the conversion of nicotine to nornicotine in varieties of Nicotiana tabacum L. and related amphidiploids Crop Sci. 4 1964 349 353
26. M. Morita, N. Shitan, K. Sawada, M.C.E. Van Montagu, D. Inze, H. Rischer, A. Goossens, K.-M. Oksman-Caldentey, Y. Moriyama, and K. Yazaki Vacuolar transport of nicotine is mediated by a multidrug and toxic compound extrusion (MATE) transporter in Nicotiana tabacum Proc. Natl. Acad. Sci. USA 106 2009 2447 2452
27. L. Murad, K.Y. Lim, V. Christopodulou, R. Matyasek, C.P. Lichtenstein, A. Kovarik, and A.R. Leitch The origin of tobacco's T genome is traced to a particular lineage within Nicotiana tomentosiformis (Solanaceae) Am. J. Bot. 89 2002 921 928
28. D.R. Nelson, L. Koymans, T. Kamataki, J.J. Stegeman, R. Feyereisen, D.J. Waxman, M.R. Waterman, O. Gotoh, M.J. Coon, R.W. Estabrook, I.C. Gunsalus, and D.W. Nebert P450 superfamily: update on new sequences, gene mapping, accession numbers and nomenclature Pharmacogenetics 6 1996 1 42
29. Peele, D.M., Gentry, J.S., 1999. Formation of tobacco-specific nitrosamines in flue-cured tobacco. CORESTA Meeting, Agro-Phyto Groups, Suzhou, China.
30. D. Pompon, B. Louerat, A. Bronine, and P. Urban Yeast expression of animal and plant P450s in optimized redox environments Methods Enzymol. 272 1996 51 64
31. T. Shoji, K. Inai, Y. Yazaki, Y. Sato, H. Takase, N. Shitan, K. Yazaki, Y. Goto, K. Toyooka, K. Matsuoka, and T. Hashimoto Multidrug and toxic compound extrusion-type transporters implicated in vacuolar sequestration of nicotine in tobacco roots Plant Physiol. 149 2009 708 718
32. B. Siminszky, L. Gavilano, S.W. Bowen, and R.E. Dewey Conversion of nicotine to nornicotine in Nicotiana tabacum is mediated by CYP82E4, a cytochrome P450 monooxygenase Proc. Natl. Acad. Sci. USA 102 2005 14919 14924
33. V.A. Sisson, and R.F. Severson Alkaloid composition of the Nicotiana species Beitr. Tabakforsch. 14 1990 327 399
34. E.A. Wernsman, and D.F. Matzinger Time and site of nicotine conversion in tobacco Tob. Sci. 12 1968 226 228
35. P. Xu, Y. Zhang, L. Kang, M.J. Roossinck, and K.S. Mysore Computational estimation and experimental verification of off-target silencing during posttranscriptional gene silencing in plants Plant Physiol. 142 2006 429 440
36. D. Xu, Y. Shen, J. Chappell, M. Cui, and M. Nielsen Biochemical and molecular characterization of nicotine demethylase in tobacco Physiol. Plantarum 129 2007 307 319
37. M. Yukawa, T. Tsudzuki, and M. Sugiura The chloroplast genome of Nicotiana sylvestris and Nicotiana tomentosiformis: complete sequencing confirms that the Nicotiana sylvestris progenitor is the maternal genome donor of Nicotiana tabacum Mol. Genet. Genom. 275 2006 367 373