RNAi-mediated down-regulation of ornithine decarboxylase (ODC) leads to reduced nicotine and increased anatabine levels in transgenic Nicotiana tabacum L.

Phytochemistry

Volumn 72, Issue 4-5, 2011, Pages 344-355

  Deboer, Kathleen D ^a   Dalton, Heidi L ^a   Edward, Felicity J ^a   Hamill, John D ^a  

^a MONASH UNIVERSITY   (Australia)

Author keywords

Alkaloid; Anatabine; Arginine decarboxylase; Hairy roots; Metabolism; Nicotiana; Nicotine; Ornithine decarboxylase; RNAi; Solanaceae; Transgenic

Indexed keywords

ALKALOID; ANATABINE; NICOTINE; ORNITHINE DECARBOXYLASE; PYRIDINE DERIVATIVE;

ARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; ENZYMOLOGY; GENETICS; METABOLISM; MICROBIOLOGY; PLANT ROOT; PLANT SEED; RNA INTERFERENCE; TOBACCO; TRANSGENIC PLANT;

ALKALOIDS; MOLECULAR STRUCTURE; NICOTINE; ORNITHINE DECARBOXYLASE; PLANT ROOTS; PLANTS, GENETICALLY MODIFIED; PYRIDINES; RNA INTERFERENCE; SEEDS; TOBACCO;

AGROBACTERIUM RHIZOGENES; AGROBACTERIUM TUMEFACIENS; MAGNOLIOPHYTA; NICOTIANA; NICOTIANA TABACUM; SOLANACEAE;

EID: 79952187000     PISSN: 00319422     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.phytochem.2010.12.012     Document Type: Article

References (65)

1. R. Alcázar, T. Altabella, F. Marco, C. Bortolotti, M. Reymond, C. Koncz, P. Carrasco, and A.F. Tiburcio Polyamines: molecules with regulatory functions in plant abiotic stress tolerance Planta 231 2010 1237 1249
2. I.T. Baldwin Mechanism of damage-induced alkaloid production in wild tobacco J. Chem. Ecol. 15 1989 1661 1680
3. I.T. Baldwin, E.A. Schmelz, and T.E. Ohnmeiss Wound-induced changes in root and shoot jasmonic acid pools correlate with induced nicotine synthesis in Nicotiana sylvestris Spegazzini and Comes J. Chem. Ecol. 20 1994 2139 2157 (Pubitemid 2148221)
4. L.P. Bush, W. Hempfling, and H. Burton Biosynthesis of nicotine and related compounds J.W. Gorrod, P. Jacob III Analytical Determination of Nicotine and Related Compounds and Their Metabolites 1999 Elsevier Science B.V. Amsterdam 13 44
5. K.A. Cane, M. Mayer, A.J. Lidgett, A.J. Michael, and J.D. Hamill Molecular analysis of alkaloid metabolism in AABB vs. aabb genotype Nicotiana tabacum in response to wounding of aerial tissues and methyl jasmonate treatment of cultured roots Funct. Plant Biol. 32 2005 305 320 (Pubitemid 40728155)
6. 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 (Pubitemid 47083888)
7. J.F. Chaplin SC58 Tobacco Crop Sci. 6 1966 97
8. Y. Chintapakorn, and J.D. Hamill Antisense-mediated down-regulation of putrescine N-methyltransferase activity in transgenic Nicotiana tabacum L. can lead to elevated levels of anatabine at the expense of nicotine Plant Mol. Biol. 53 2003 87 105 (Pubitemid 38105641)
9. Y. Chintapakorn, and J.D. Hamill Antisense-mediated reduction in ADC activity causes minor alterations in the alkaloid profile of cultured hairy root and regenerated transgenic plants of Nicotiana tabacum Phytochemistry 68 2007 2465 2479 (Pubitemid 47429716)
10. R.F. Dawson The localisation of the nicotine synthetic mechanism in the tobacco plant Science 94 1941 396 397
11. R.F. Dawson Accumulation of nicotine in reciprocal grafts of tomato and tobacco Am. J. Bot. 29 1942 66 71
12. DeBoer, K.D.; 2010. Studies into the Molecular Genetics of Alkaloid Synthesis in the Genus Nicotiana. Ph.D. Dissertation, School of Biological Sciences, Monash University, Melbourne, Australia.
13. K.D. DeBoer, J.C. Lye, C.D. Aitken, A.K.-K. Su, and J.D. Hamill The A622 gene in Nicotiana glauca (tree tobacco): evidence for a functional role in pyridine alkaloid synthesis Plant Mol. Biol. 69 2009 299 312
14. V. De Sutter, R. Vanderhaeghen, S. Tilleman, F. Lammertyn, I. Vanhoutte, M. Karimi, D. Inzé, A. Goossens, and P. Hilson Exploration of jasmonate signalling via automated and standardized transient expression assays in tobacco cells Plant J. 44 2005 1065 1076 (Pubitemid 43906733)
15. L.F. Fecker, C. Rgenhagen, and J. Berlin Increased production of cadaverine and anabasine in hairy root cultures of Nicotiana tabacum expressing a bacterial lysine decarboxylase gene Plant Mol. Bol. 23 1993 11 21 (Pubitemid 2005171)
16. C. Fuell, K.A. Elliott, C.C. Hanfrey, M. Franceschetti, and A.J. Michael Polyamine biosynthetic diversity in plants and algae Plant Physiol. Biochem. 48 2010 513 520
17. 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 (Pubitemid 47076662)
18. 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 (Pubitemid 44953603)
19. 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 (Pubitemid 350135512)
20. A.P. Gleave A versatile binary vector system with a T-DNA organisational structure conductive to efficient integration of cloned DNA into the plant genome Plant Mol. Biol. 20 1992 1203 1207
21. A. Goossens, S.T. Häkkinen, I. Laakso, T. Seppänen-Laakso, S. Biondi, V. De Sutter, F. Lammertyn, A.M. Nuutila, H. Söderlund, M. Zabeau, D. Inzé, and K.-M. Oksman-Caldentey A functional genomics approach toward the understanding of secondary metabolism in plant cells Proc. Natl. Acad. Sci. USA 100 2003 8595 8600 (Pubitemid 36842589)
22. J.D. Hamill, and A.J. Lidgett Hairy root cultures - opportunities and key protocols for studies in metabolic engineering P.M. Doran, Hairy Roots: Culture and Application 1997 Overseas Publishers Association Amsterdam 1 29
23. J.D. Hamill, A.J. Parr, R.J. Robins, and M.J.C. Rhodes Secondary product formation by cultures of Beta vulgaris and Nicotiana rustica transformed with Agrobacterium rhizogenes Plant Cell Rep. 5 1986 111 114
24. J.D. Hamill, A. Prescott, and C. Martin Assessment of the efficiency of co-transformation by the T-DNA of disarmed binary vectors derived from Agrobacterium tumefaciens and the T-DNA from A. rhizogenes Plant Mol. Biol. 9 1987 573 584
25. J.D. Hamill, R.J. Robins, A.J. Parr, J. Furze, D.J. Evans, and M.J.C. Rhodes Overexpressing a yeast ornithine decarboxylase gene in transgenic roots of Nicotiana rustica can lead to enhanced nicotine accumulation Plant Mol. Biol. 15 1990 27 38
26. S. Herminghaus, P.H. Schreier, J.E.G. McCarthy, J. Landsmann, J. Botterman, and J. Berlin Expression of a bacterial lysine decarboxylase gene and transport of the protein into chloroplasts of transgenic tobacco Plant Mol. Biol. 17 1991 475 486
27. S. Herminghaus, D. Tholl, C. Rgenhagen, L.F. Fecker, C. Leucshner, and J. Berlin Improved metabolic action of a bacterial lysine decarboxylase peptide coding sequence Transgen. Res. 5 1996 193 201
28. N. Hibi, S. Higashiguchi, T. Hashimoto, and Y. Yamada Gene expression in tobacco low-nicotine mutants The Plant Cell 6 1994 723 735
29. R.B. Horsch, J.E. Fry, N.L. Hoffman, D. Eichholtz, S.G. Rogers, and R.T. Fraley A simple and general method for transferring genes into plants Science 227 1985 1229 1231
30. S. Imanishi, K. Hashizume, M. Nakakita, H. Kojima, Y. Matsubayashi, T. Hashimoto, Y. Sakagami, Y. Yamada, and K. Nakamura Differential induction by methyl jasmonate of genes encoding ornithine decarboxylase and other enzymes involved in nicotine biosynthesis in tobacco cell cultures Plant Mol. Biol. 38 1998 1101 1111 (Pubitemid 29000322)
31. D.M. Jackson, A.W. Johnson, and M.G. Stephenson Survival and development of Heliothis virescens (Lepidoptera: Noctuidae) larvae on isogenic tobacco lines with different levels of alkaloids J. Econ. Entomol. 95 2002 1294 1302
32. M. Kajikawa, N. Hirai, and T. Hashimoto A PIP-family protein is required for biosynthesis of tobacco alkaloids Plant Mol. Biol. 69 2009 287 298
33. T. Kusano, T. Berberich, C. Tateda, and Y. Takahashi Polyamines: essential factors for growth and survival Planta 228 2008 367 381
34. Leete, E.; 1975. Biosynthesis of anatabine and anabasine in Nicotiana glutinosa. J C.S. Chem. Commun. 9-10.
35. E. Leete, and S. Slattery Incorporation of [2-14C]- and [6-14C] nicotinic acid into the tobacco alkaloids. Biosynthesis of anatabine and α,β-dipyridyl J. Am. Chem. Soc. 98 1976 6326 6330
36. P.D. Legg, J.F. Chaplin, and G.B. Collins Inheritance of percent total alkaloids in Nicotiana tabacum L.: populations derived from crosses of low alkaloid lines with burley and flue-cured varieties J. Hered. 60 1969 212 219
37. R.S. Lewis, S.W. Bowen, M.R. Keogh, and R.R. Dewey Three nicotine demethylase genes mediate nornicotine biosynthesis in Nicotiana tabacum L.: functional characterization of the CYP82E10 gene Phytochemistry 71 2010 1988 1998
38. Lidgett, A.J.; 1997. Molecular characterization of polyamine biosynthetic genes and effects of genetic manipulation in Nicotiana tabacum L. Ph.D. Dissertation, School of Biological Sciences, Monash University, Melbourne, Australia.
39. A.J. Michael, J.M. Furze, M.J.C. Rhodes, and D. Burtin Molecular cloning and functional identification of a plant ornithine decarboxylase cDNA Biochem. J. 314 1996 241 248 (Pubitemid 26063855)
40. S. Mizusaki, Y. Tanabe, M. Noguchi, and E. Tamaki Changes in the activities of ornithine decarboxylase, putrescine N-methyltransferase and N-methylputrescine oxidase in tobacco roots in relation to nicotine biosynthesis Plant Cell Physiol. 14 1973 103 110
41. G. Nölke, B. Schnieder, R. Fischer, and S. Schillberg Immunomodulation of polyamine biosynthesis in tobacco plants has a significant impact on polyamine levels and generates a dwarf phenotype Plant Biotechnol. 3 2005 237 247 (Pubitemid 41615427)
42. A.J. Parr, and J.D. Hamill Relationships between the biosynthetic capacities of Agrobacterium rhizogenes transformed hairy roots and intact, uninfected plants of Nicotiana species Phytochemistry 26 1987 3241 3245
43. D.G. Reed, and J.G. Jelesko The A and B loci of Nicotiana tabacum have non-equivalent effects on the mRNA levels of four alkaloid biosynthetic genes Plant Sci. 167 2004 1123 1130 (Pubitemid 39081621)
44. F. Saitoh, M. Noma, and N. Kawashima The alkaloid contents of sixty Nicotiana species Phytochemistry 24 1985 477 480
45. J. Sambrook, E.F. Fritsch, and T. Maniatis Molecular Cloning: A Laboratory Manual second ed. 1989 Cold Spring Harbor Laboratory Press New York
46. J.W. Saunders, and L.P. Bush Nicotine biosynthetic enzyme activities in Nicotiana tabacum L. genotypes with different alkaloid levels Plant Physiol. 64 1979 236 240
47. Q. Shi, C. Li, and F. Zhang Nicotine synthesis in Nicotiana tabacum L. induced by mechanical wounding is regulated by auxin J Exp Bot 57 2006 2899 2907 (Pubitemid 44290319)
48. Shoji, T.; Kajikawa, M.; Hashimoto, T.; in press. Clustered transcription factor genes regulate nicotine biosynthesis in tobacco. Plant cell. doi: 10.1105/tpc.110.078543.
49. T. Shoji, T. Ogawa, and T. Hashimoto Jasmonate-induced nicotine formation in tobacco is mediated by tobacco COI1 and JAZ genes Plant Cell Physiol. 49 2008 1003 1012 (Pubitemid 351989688)
50. 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. 102 2005 14919 14924 (Pubitemid 41457156)
51. S.J. Sinclair, K. Murphy, C. Birch, and J.D. Hamill Molecular characterisation of quinolinic acid phosphoribosyltransferase (QPRTase) in Nicotiana Plant Mol. Biol. 44 2000 603 617 (Pubitemid 32143133)
52. S.J. Sinclair, R. Johnson, and J.D. Hamill Analysis of wound-induced gene expression in Nicotiana species with contrasting alkaloid profiles Funct. Plant Biol. 31 2004 1 9
53. V.A. Sisson, and R.F. Severson Alkaloid composition of the Nicotiana species Beiträge zur Tabakforsch. Internat. 14 1990 327 339
54. A. Steppuhn, K. Gase, B. Krock, R. Halitschke, and I.T. Baldwin Nicotine's defensive function in nature PLoS Biol. 2 2004 1074 1080
55. T. Takahashi, and J.-I. Kakehi Polyamines: ubiquitous polycations with unique roles in growth and stress responses Annal. Bot. 105 2009 1 6
56. D. Tepfer Transformation of several species of higher plants by Agrobacterium rhizogenes: sexual transmission of the transformed genotype and phenotype Cell 37 1984 959 968
57. A.F. Tiburcio, and A.W. Galston Arginine decarboxylase as the source of putrescine for tobacco alkaloids Phytochemistry 25 1986 107 110
58. A. Todd, E. Liu, S.L. Polvi, R.T. Pammett, and J.E. Page A functional genomics screen identifies diverse transcription factors that regulate alkaloid biosynthesis in Nicotiana benthamiana Plant J. 62 2010 589 600
59. R. Walden, A. Cordeiro, and A.F. Tiburcio Polyamines: small molecules triggering pathways in plant growth and development Plant Physiol. 113 1997 1009 1013 (Pubitemid 27210598)
60. J.M. Wang, M. Sheehan, H. Brookman, and M.P. Timko Characterization of cDNAs differentially expressed in roots of tobacco (Nicotiana tabacum cv. Burley 21) during the early stages of alkaloid biosynthesis Plant Sci. 158 2000 19 32
61. P. Wang, Z. Liang, J. Zeng, W. Li, X. Sun, Z. Miao, and K. Tang Generation of tobacco lines with widely different reduced nicotine levels via RNA silencing approaches J. Biosci. 33 2008 177 184 (Pubitemid 351840249)
62. P. Wang, J. Zeng, Z. Liang, Z. Miao, X. Sun, and K. Tang Silencing of PMT expression caused a surge of anatabine accumulation in tobacco Mol. Biol. Rep. 36 2009 2285 2289
63. S.V. Wesley, C.A. Helliwell, N.A. Smith, M. Wang, D.T. Rouse, Q. Liu, P.S. Gooding, S.P. Singh, D. Abbott, P.A. Stoutjesdijk, S.P. Robinson, A.P. Gleave, A.G. Green, and P.M. Waterhouse Construct design for efficient, effective and high-throughput gene silencing in plants Plant J. 27 2001 581 589
64. B. Xu, M.J. Sheehan, and M.P. Timko Differential induction of ornithine decarboxylase (ODC) gene family members in transgenic tobacco (Nicotiana tabacum L. cv. Bright Yellow 2) cell suspensions by methyl jasmonate treatment Plant Growth Regul. 44 2004 101 116 (Pubitemid 40134269)
65. D. Xu, Y. Shen, J. Chappell, M. Cui, and M. Nielsen Biochemical and molecular characterizations of nicotine demethylase in tobacco Physiol. Plant. 129 2007 307 319 (Pubitemid 46072486)