A pair of tabersonine 16-hydroxylases initiates the synthesis of vindoline in an organ-dependent manner in Catharanthus roseus

Plant Physiology

Volumn 163, Issue 4, 2013, Pages 1792-1803

  Besseau, Sébastien ^a   Kellner, Franziska ^b   Lanoue, Arnaud ^a   Thamm, Antje M K ^c   Salim, Vonny ^c   Schneider, Bernd ^d   Geu Flores, Fernando ^b   Höfer, René ^e   Guirimand, Grégory ^a   Guihur, Anthony ^a   Oudin, Audrey ^a   Glevarec, Gaëlle ^a   Foureau, Emilien ^a   Papon, Nicolas ^a   Clastre, Marc ^a   Giglioli Guivarc'h, Nathalie ^a   St Pierre, Benoit ^a   Werck Reichhart, Danièle ^e   Burlat, Vincent ^f,g   De Luca, Vincenzo ^c   O'Connor, Sarah E ^b   Courdavault, Vincent ^a   more..

^a UNIVERSITÉ DE TOURS   (France)

^b JOHN INNES CENTRE   (United Kingdom)

^c BROCK UNIVERSITY   (Canada)

^d MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

^e UNIVERSITÉ DE STRASBOURG   (France)

^f UNIVERSITÉ PAUL SABATIER   (France)

^g CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; CYP71D12 PROTEIN, CATHARANTHUS ROSEUS; CYTOCHROME P450; DRUG DERIVATIVE; INDOLE ALKALOID; MESSENGER RNA; QUINOLINE DERIVATIVE; TABERSONINE; VEGETABLE PROTEIN; VINBLASTINE; VINDOLINE;

ANTIBODY SPECIFICITY; ARTICLE; BIOCATALYSIS; BIOSYNTHESIS; CATHARANTHUS; CHEMISTRY; CYTOLOGY; ENDOPLASMIC RETICULUM; ENZYME SPECIFICITY; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; HYDROXYLATION; ISOLATION AND PURIFICATION; KINETICS; METABOLISM; METABOLOME; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PLANT EPIDERMIS; PLANT GENE;

BIOCATALYSIS; BIOSYNTHETIC PATHWAYS; CATHARANTHUS; CYTOCHROME P-450 ENZYME SYSTEM; DNA, COMPLEMENTARY; ENDOPLASMIC RETICULUM; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, PLANT; GENE SILENCING; GENES, PLANT; HYDROXYLATION; INDOLE ALKALOIDS; KINETICS; METABOLOME; MOLECULAR SEQUENCE DATA; ORGAN SPECIFICITY; PLANT EPIDERMIS; PLANT PROTEINS; QUINOLINES; RNA, MESSENGER; SUBSTRATE SPECIFICITY; VINBLASTINE;

EID: 84888866723     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.113.222828     Document Type: Article

References (39)

1. Balsevich J, Bishop GJ (1989) Distribution of catharanthine, vindoline and 3'4'-anhydrovinblastine in the aerial parts of some Catharanthus roseus plants and the significance thereof in relation to alkaloid production in cultured cells. In WGW Kurz, ed, Primary and Secondary Metabolism of Plant Cell Cultures. Springer Verlag, Berlin, pp 149-153
2. De Luca V, Balsevich J, Tyler RT, Kurz WGW (1987) Characterization of a novel N-methyltransferase (NMT) from Catharanthus roseus plants. Plant Cell Rep 6: 458-461
3. Deus-Neumann B, Stöckigt J, Zenk MH (1987) Radioimmunoassay for the quantitative determination of catharanthine. Planta Med 53: 184-188
4. Facchini PJ, De Luca V (2008)Opium poppy andMadagascar periwinkle: model nonmodel systems to investigate alkaloid biosynthesis in plants. Plant J 54: 763-784
5. Geu-Flores F, Sherden NH, Courdavault V, Burlat V, Glenn WS, Wu C, Nims E, Cui Y, O'Connor SE (2012) An alternative route to cyclic terpenes by reductive cyclization in iridoid biosynthesis. Nature 492: 138-142
6. Giddings LA, Liscombe DK, Hamilton JP, Childs KL, DellaPenna D, Buell CR, O'Connor SE (2011) A stereoselective hydroxylation step of alkaloid biosynthesis by a unique cytochrome P450 in Catharanthus roseus. J Biol Chem 286: 16751-16757
7. Gigant B, Wang C, Ravelli RB, Roussi F, Steinmetz MO, Curmi PA, Sobel A, Knossow M (2005) Structural basis for the regulation of tubulin by vinblastine. Nature 435: 519-522
8. Guirimand G, Burlat V, Oudin A, Lanoue A, St-Pierre B, Courdavault V (2009) Optimization of the transient transformation of Catharanthus roseus cells by particle bombardment and its application to the subcellular localization of hydroxymethylbutenyl 4-diphosphate synthase and geraniol 10-hydroxylase. Plant Cell Rep 28: 1215-1234
9. Guirimand G, Courdavault V, Lanoue A, Mahroug S, Guihur A, Blanc N, Giglioli-Guivarc'h N, St-Pierre B, Burlat V (2010a) Strictosidine activation in Apocynaceae: towards a "nuclear time bomb"? BMC Plant Biol 10: 182
10. Guirimand G, Courdavault V, St-Pierre B, Burlat V (2010b) Biosynthesis and regulation of alkaloids. In EC Pua, M Davey, eds, Plant Developmental Biology: Biotechnological Perspectives, Vol 2. Springer-Verlag, Berlin, pp 139-160
11. Guirimand G, Guihur A, Ginis O, Poutrain P, Héricourt F, Oudin A, Lanoue A, St-Pierre B, Burlat V, Courdavault V (2011a) The subcellular organization of strictosidine biosynthesis in Catharanthus roseus epidermis highlights several trans-tonoplast translocations of intermediate metabolites. FEBS J 278: 749-763
12. Guirimand G, Guihur A, Phillips MA, Oudin A, Glévarec G, Melin C, Papon N, Clastre M, St-Pierre B, Rodríguez-Concepción M, et al (2012) A single gene encodes isopentenyl diphosphate isomerase isoforms targeted to plastids, mitochondria and peroxisomes in Catharanthus roseus. Plant Mol Biol 79: 443-459
13. Guirimand G, Guihur A, Poutrain P, Héricourt F, Mahroug S, St-Pierre B, Burlat V, Courdavault V (2011b) Spatial organization of the vindoline biosynthetic pathway in Catharanthus roseus. J Plant Physiol 168: 549-557
14. He L, Yang L, Tan R, Zhao S, Hu Z (2011) Enhancement of vindoline production in suspension culture of the Catharanthus roseus cell line C20hi by light and methyl jasmonate elicitation. Anal Sci 27: 1243-1248
15. He YL, Chen WM, Feng XZ (1994) Melomorsine, a new dimeric indoline alkaloid from Melodinus morsei. J Nat Prod 57: 411-414
16. Heitz T, Widemann E, Lugan R, Miesch L, Ullmann P, Désaubry L, Holder E, Grausem B, Kandel S, Miesch M, et al (2012) Cytochromes P450 CYP94C1 and CYP94B3 catalyze two successive oxidation steps of plant hormone jasmonoyl-isoleucine for catabolic turnover. J Biol Chem 287: 6296-6306
17. Laflamme P, St-Pierre B, De Luca V (2001) Molecular and biochemical analysis of a Madagascar periwinkle root-specific minovincinine-19-hydroxy-O-acetyltransferase. Plant Physiol 125: 189-198
18. Levac D, Murata J, Kim WS, De Luca V (2008) Application of carborundum abrasion for investigating the leaf epidermis: molecular cloning of Catharanthus roseus 16-hydroxytabersonine-16-O-methyltransferase. Plant J 53: 225-236
19. Liscombe DK, O'Connor SE (2011) A virus-induced gene silencing approach to understanding alkaloid metabolism in Catharanthus roseus. Phytochemistry 72: 1969-1977
20. Liscombe DK, Usera AR, O'Connor SE (2010) Homolog of tocopherol C methyltransferases catalyzes N methylation in anticancer alkaloid biosynthesis. Proc Natl Acad Sci USA 107: 18793-18798
21. Liu JJ, Ekramoddoullah AKM (2006) The family 10 of plant pathogenesisrelated proteins: their structure, regulation, and function in response to biotic and abiotic stresses. Physiol Mol Plant Pathol 68: 3-13
22. Magnotta M, Murata J, Chen J, De Luca V (2006) Identification of a low vindoline accumulating cultivar of Catharanthus roseus (L.) G. Don by alkaloid and enzymatic profiling. Phytochemistry 67: 1758-1764
23. Mahroug S, Courdavault V, Thiersault M, St-Pierre B, Burlat V (2006) Epidermis is a pivotal site of at least four secondary metabolic pathways in Catharanthus roseus aerial organs. Planta 223: 1191-1200
24. Murata J, De Luca V (2005) Localization of tabersonine 16-hydroxylase and 16-OH tabersonine-16-O-methyltransferase to leaf epidermal cells defines them as a major site of precursor biosynthesis in the vindoline pathway in Catharanthus roseus. Plant J 44: 581-594
25. Murata J, Roepke J, Gordon H, De Luca V (2008) The leaf epidermome of Catharanthus roseus reveals its biochemical specialization. Plant Cell 20: 524-542
26. Nelson BK, Cai X, Nebenführ A (2007) A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J 51: 1126-1136
27. Nelson DR (2006) Cytochrome P450 nomenclature, 2004. Methods Mol Biol 320: 1-10
28. Oudin A, Mahroug S, Courdavault V, Hervouet N, Zelwer C, Rodríguez-Concepción M, St-Pierre B, Burlat V (2007) Spatial distribution and hormonal regulation of gene products from methyl erythritol phosphate and monoterpene-secoiridoid pathways in Catharanthus roseus. Plant Mol Biol 65: 13-30
29. Pompon D, Louerat B, Bronine A, Urban P (1996) Yeast expression of animal and plant P450s in optimized redox environments. Methods Enzymol 272: 51-64
30. Quinlan RF, Shumskaya M, Bradbury LM, Beltrán J, Ma C, Kennelly EJ, Wurtzel ET (2012) Synergistic interactions between carotene ring hydroxylases drive lutein formation in plant carotenoid biosynthesis. Plant Physiol 160: 204-214
31. Roepke J, Salim V, Wu M, Thamm AM, Murata J, Ploss K, BolandW, De Luca V (2010) Vinca drug components accumulate exclusively in leaf exudates of Madagascar periwinkle. Proc Natl Acad Sci USA 107: 15287-15292
32. Schröder G, Unterbusch E, Kaltenbach M, Schmidt J, Strack D, De Luca V, Schröder J (1999) Light-induced cytochrome P450-dependent enzyme in indole alkaloid biosynthesis: tabersonine 16-hydroxylase. FEBS Lett 458: 97-102
33. St-Pierre B, De Luca V (1995) A cytochrome P-450 monooxygenase catalyzes the first step in the conversion of tabersonine to vindoline in Catharanthus roseus. Plant Physiol 109: 131-139
34. St-Pierre B, Laflamme P, Alarco AM, De Luca V (1998) The terminal O-acetyltransferase involved in vindoline biosynthesis defines a new class of proteins responsible for coenzyme A-dependent acyl transfer. Plant J 14: 703-713
35. St-Pierre B, Vazquez-Flota FA, De Luca V (1999) Multicellular compartmentation of Catharanthus roseus alkaloid biosynthesis predicts intercellular translocation of a pathway intermediate. Plant Cell 11: 887-900
36. Sung PH, Huang FC, Do YY, Huang PL (2011) Functional expression of geraniol 10-hydroxylase reveals its dual function in the biosynthesis of terpenoid and phenylpropanoid. J Agric Food Chem 59: 4637-4643
37. Vazquez-Flota F, De Carolis E, Alarco AM, De Luca V (1997) Molecular cloning and characterization of desacetoxyvindoline-4-hydroxylase, a 2-oxoglutarate dependent-dioxygenase involved in the biosynthesis of vindoline in Catharanthus roseus (L.) G. Don. Plant Mol Biol 34: 935-948
38. Wenkert E, Cochran DW, Hagaman EW, Schell FM, Neuss N, Katner AS, Potier P, Kan C, Plat M, Koch M, et al (1973) Carbon-13 nuclear magnetic resonance spectroscopy of naturally occurring substances. XIX. Aspidosperma alkaloids. J Am Chem Soc 95: 4990-4995
39. Westekemper P, Wieczorek U, Gueritte F, Langlois N, Langlois Y, Potier P, Zenk MH (1980) Radioimmunoassay for the determination of the indole alkaloid vindoline in Catharanthus. Planta Med 39: 24-37