Class II cytochrome P450 reductase governs the biosynthesis of alkaloids

Plant Physiology

Volumn 172, Issue 3, 2016, Pages 1563-1577

  Parage, Claire ^a   Foureau, Emilien ^a   Kellner, Franziska ^b   Burlat, Vincent ^c   Mahroug, Samira ^a   Lanoue, Arnaud ^a   de Bernonville, Thomas Dugé ^a   Londono, Monica Arias ^a,d   Carqueijeiro, Inês ^a   Oudin, Audrey ^a   Besseau, Sébastien ^a   Papon, Nicolas ^e   Glévarec, Gaëlle ^a   Atehortùa, Lucia ^d   Giglioli Guivarc’h, Nathalie ^a   St Pierre, Benoit ^a   Clastre, Marc ^a   O’Connor, Sarah E ^b   Courdavault, Vincent ^a  

^a UNIVERSITÉ DE TOURS   (France)

^b JOHN INNES CENTRE   (United Kingdom)

^c UNIVERSITÉ DE TOULOUSE   (France)

^d UNIVERSIDAD DE ANTIOQUIA   (Colombia)

^e UNIVERSITÉ D'ANGERS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ALKALOID; INDOLE ALKALOID; MESSENGER RNA; PROTEIN BINDING; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE FERRIHEMOPROTEIN REDUCTASE;

BIOCATALYSIS; BIOSYNTHESIS; CATHARANTHUS; CELL FRACTIONATION; CHEMISTRY; COTYLEDON; ENDOPLASMIC RETICULUM; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; METABOLISM; PLANT GENE; PLANT LEAF; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY;

ALKALOIDS; BIOCATALYSIS; BIOSYNTHETIC PATHWAYS; CATHARANTHUS; COTYLEDON; ENDOPLASMIC RETICULUM; GENE EXPRESSION REGULATION, PLANT; GENE SILENCING; GENES, PLANT; INDOLE ALKALOIDS; NADPH-FERRIHEMOPROTEIN REDUCTASE; PLANT LEAVES; PROTEIN BINDING; RNA, MESSENGER; SEQUENCE ANALYSIS, PROTEIN; SEQUENCE HOMOLOGY, AMINO ACID; SUBCELLULAR FRACTIONS;

EID: 84994641730     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.16.00801     Document Type: Article

References (73)

1. Andersen TB, Hansen NB, Laursen T, Weitzel C, Simonsen HT (2016) Evolution of NADPH-cytochrome P450 oxidoreductases (POR) in Apiales: POR 1 is missing. Mol Phylogenet Evol 98: 21-28
2. Bailey TL, Bodén M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37: W202-W208
3. Bak S, Beisson F, Bishop G, Hamberger B, Höfer R, Paquette S, Werck-Reichhart D (2011) Cytochromes p450. The Arabidopsis Book 9: e0144 doi: 10.1199/tab.0144
4. Bassard JE, Mutterer J, Duval F, Werck-Reichhart D (2012) A novel method for monitoring the localization of cytochromes P450 and other endoplasmic reticulum membrane associated proteins: a tool for investigating the formation of metabolons. FEBS J 279: 1576-1583
5. Benveniste I, Lesot A, Hasenfratz MP, Kochs G, Durst F (1991) Multiple forms of NADPH-cytochrome P450 reductase in higher plants. Biochem Biophys Res Commun 177: 105-112
6. Besseau S, Kellner F, Lanoue A, Thamm AM, Salim V, Schneider B, Geu-Flores F, Höfer R, Guirimand G, Guihur A, et al (2013) A pair of tabersonine 16-hydroxylases initiates the synthesis of vindoline in an organ-dependent manner in Catharanthus roseus. Plant Physiol 163: 1792-1803
7. Brown S, Clastre M, Courdavault V, O’Connor SE (2015) De novo production of the plant-derived alkaloid strictosidine in yeast. Proc Natl Acad Sci USA 112: 3205-3210
8. Burlat V, Oudin A, Courtois M, Rideau M, St-Pierre B (2004) Coexpression of three MEP pathway genes and geraniol 10-hydroxylase in internal phloem parenchyma of Catharanthus roseus implicates multicellular translocation of intermediates during the biosynthesis of monoterpene indole alkaloids and isoprenoid-derived primary metabolites. Plant J 38: 131-141
9. Canto-Canché BB, Loyola-Vargas VM (2001) Multiple forms of NADPHcytochrome P450 oxidoreductases in the Madagascar periwinkle Catharanthus roseus. In Vitro Cell Dev Biol Plant 37: 622-628
10. Carqueijeiro I, Masini E, Foureau E, Sepúlveda LJ, Marais E, Lanoue A, Besseau S, Papon N, Clastre M, Dugé de Bernonville T, et al (2015) Virus-induced gene silencing in Catharanthus roseus by biolistic inoculation of tobacco rattle virus vectors. Plant Biol (Stuttg) 17: 1242-1246
11. Chatel G, Montiel G, Pré M, Memelink J, Thiersault M, Saint-Pierre B, Doireau P, Gantet P (2003) CrMYC1, a Catharanthus roseus elicitor-and jasmonate-responsive bHLH transcription factor that binds the G-box element of the strictosidine synthase gene promoter. J Exp Bot 54: 2587-2588
12. Collu G, Unver N, Peltenburg-Looman AM, van der Heijden R, Verpoorte R, Memelink J (2001) Geraniol 10-hydroxylase, a cytochrome P450 enzyme involved in terpenoid indole alkaloid biosynthesis. FEBS Lett 508: 215-220
13. Courdavault V, Papon N, Clastre M, Giglioli-Guivarc’h N, St-Pierre B, Burlat V (2014) A look inside an alkaloid multisite plant: the Catharanthus logistics. Curr Opin Plant Biol 19: 43-50
14. Denisov IG, Baas BJ, Grinkova YV, Sligar SG (2007) Cooperativity in cytochrome P450 3A4: linkages in substrate binding, spin state, uncoupling, and product formation. J Biol Chem 282: 7066-7076
15. Dugé de Bernonville T, Clastre M, Besseau S, Oudin A, Burlat V, Glévarec G, Lanoue A, Papon N, Giglioli-Guivarc’h N, St-Pierre B, et al (2015a) Phytochemical genomics of the Madagascar periwinkle: unravelling the last twists of the alkaloid engine. Phytochemistry 113: 9-23
16. Dugé de Bernonville T, Foureau E, Parage C, Lanoue A, Clastre M, Londono MA, Oudin A, Houillé B, Papon N, Besseau S, et al (2015b) Characterization of a second secologanin synthase isoform producing both secologanin and secoxyloganin allows enhanced de novo assembly of a Catharanthus roseus transcriptome. BMC Genomics 16: 619
17. El-Sayed M, Verpoorte R (2007) Catharanthus terpenoid indole alkaloids: biosynthesis and regulation. Phytochem Rev 6: 277-305
18. Foureau E, Carqueijeiro I, Dugé de Bernonville TD, Melin C, Lafontaine F, Besseau S, Lanoue A, Papon N, Oudin A, Glévarec G, et al (2016) Prequels to synthetic biology: from candidate gene identification and validation to enzyme subcellular localization in plant and yeast cells. Methods Enzymol 576: 167-206
19. 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
20. 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
21. Góngora-Castillo E, Childs KL, Fedewa G, Hamilton JP, Liscombe DK, Magallanes-Lundback M, Mandadi KK, Nims E, Runguphan W, Vaillancourt B, et al (2012) Development of transcriptomic resources for interrogating the biosynthesis of monoterpene indole alkaloids in medicinal plant species. PLoS ONE 7: e52506
22. Guengerich FP, Munro AW (2013) Unusual cytochrome p450 enzymes and reactions. J Biol Chem 288: 17065-17073
23. Guengerich FP, Sohl CD, Chowdhury G (2011) Multi-step oxidations catalyzed by cytochrome P450 enzymes: processive vs. distributive kinetics and the issue of carbonyl oxidation in chemical mechanisms. Arch Biochem Biophys 507: 126-134
24. 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
25. Guirimand G, Courdavault V, Lanoue A, Mahroug S, Guihur A, Blanc N, Giglioli-Guivarc’h N, St-Pierre B, Burlat V (2010) Strictosidine activation in Apocynaceae: towards a “nuclear time bomb”? BMC Plant Biol 10: 182
26. 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
27. 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
28. Hasemann CA, Kurumbail RG, Boddupalli SS, Peterson JA, Deisenhofer J (1995) Structure and function of cytochromes P450: a comparative analysis of three crystal structures. Structure 15: 41-62
29. 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
30. Höfer R, Dong L, André F, Ginglinger JF, Lugan R, Gavira C, Grec S, Lang G, Memelink J, Van der Krol S, et al (2013) Geraniol hydroxylase and hydroxygeraniol oxidase activities of the CYP76 family of cytochrome P450 enzymes and potential for engineering the early steps of the (seco)iridoid pathway. Metab Eng 20: 221-232
31. Hotze M, Schröder G, Schröder J (1995) Cinnamate 4-hydroxylase from Catharanthus roseus, and a strategy for the functional expression of plant cytochrome P450 proteins as translational fusions with P450 reductase in Escherichia coli. FEBS Lett 374: 345-350
32. Huang FC, Sung PH, Do YY (2012) Differential expression and functional characterization of the NADPH cytochrome P450 reductase genes from Nothapodytes foetida. Plant Sci 190: 16-23
33. Irmler S, Schröder G, St-Pierre B, Crouch NP, Hotze M, Schmidt J, Strack D, Matern U, Schröder J (2000) Indole alkaloid biosynthesis inCatharanthus roseus: new enzyme activities and identification of cytochrome P450 CYP72A1 as secologanin synthase. Plant J 24: 797-804
34. Jensen K, Møller BL (2010) Plant NADPH-cytochrome P450 oxidoreductases. Phytochemistry. 71: 132-141
35. Kellner F, Geu-Flores F, Sherden NH, Brown S, Foureau E, Courdavault V, O’Connor SE (2015a) Discovery of a P450-catalyzed step in vindoline biosynthesis: a link between the aspidosperma and eburnamine alkaloids. Chem Commun (Camb) 51: 7626-7628
36. Kellner F, Kim J, Clavijo BJ, Hamilton JP, Childs KL, Vaillancourt B, Cepela J, Habermann M, Steuernagel B, Clissold L, et al (2015b) Genome-guided investigation of plant natural product biosynthesis. Plant J 82: 680-692
37. Koopmann E, Hahlbrock K (1997) Differentially regulated NADPH:cytochrome P450 oxidoreductases in parsley. Proc Natl Acad Sci USA 94: 14954-14959
38. Liscombe DK, O’Connor SE (2011) A virus-induced gene silencing approach to understanding alkaloid metabolism in Catharanthus roseus. Phytochemistry 72: 1969-1977
39. Liu S, Liang QM, Zhou WW, Jiang YD, Zhu QZ, Yu H, Zhang CX, Gurr GM, Zhu ZR (2015) RNA interference of NADPH-cytochrome P450 reductase of the rice brown planthopper, Nilaparvata lugens, increases susceptibility to insecticides. Pest Manag Sci 71: 32-39
40. Mackenzie NC, Lillico SG, Brown K, Wolf CR, Whitelaw CB (2010) Evaluation of RNA-knockdown strategies for modulation of cytochrome P450 reductase activity in mouse hepatocytes. J RNAi Gene Silencing 6: 416-421
41. Madyastha KM, Coscia CJ (1979) Detergent-solubilized NADPHcytochrome c(P-450) reductase from the higher plant, Catharanthus roseus: purification and characterization. J Biol Chem 254: 2419-2427
42. 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
43. Mazourek M, Pujar A, Borovsky Y, Paran I, Mueller L, Jahn MM (2009) A dynamic interface for capsaicinoid systems biology. Plant Physiol 150: 1806-1821
44. Meijer AH, Lopes Cardoso MI, Voskuilen JT, de Waal A, Verpoorte R, Hoge JHC (1993) Isolation and characterization of a cDNA clone from Catharanthus roseus encoding NADPH:cytochrome P-450 reductase, an enzyme essential for reactions catalysed by cytochrome P-450 monooxygenases in plants. Plant J 4: 47-60
45. Miettinen K, Dong L, Navrot N, Schneider T, Burlat V, Pollier J, Woittiez L, van der Krol S, Lugan R, Ilc T, et al (2014) The seco-iridoid pathway from Catharanthus roseus. Nat Commun 5: 3606
46. Mizutani M, Ohta D (2010) Diversification of P450 genes during land plant evolution. Annu Rev Plant Biol 61: 291-315
47. Mizutani M, Sato F (2011) Unusual P450 reactions in plant secondary metabolism. Arch Biochem Biophys 507: 194-203
48. Munro AW, Girvan HM, Mason AE, Dunford AJ, McLean KJ (2013) What makes a P450 tick? Trends Biochem Sci 38: 140-150
49. 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: 1126-1236
50. Paddon CJ, Westfall PJ, Pitera DJ, Benjamin K, Fisher K, McPhee D, Leavell MD, Tai A, Main A, Eng D, et al (2013) High-level semisynthetic production of the potent antimalarial artemisinin. Nature 496: 528-532
51. Patro R, Duggal G, Kingsford C (2015) Accurate, fast, and model-aware transcript expression quantification with Salmon. bioRxiv 021592
52. 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
53. Qu X, Pu X, Chen F, Yang Y, Yang L, Zhang G, Luo Y (2015a) Molecular cloning, heterologous expression, and functional characterization of an NADPH-cytochrome P450 reductase gene from Camptotheca acuminata, a camptothecin-producing plant. PLoS ONE 10: e0135397
54. Qu Y, Easson ML, Froese J, Simionescu R, Hudlicky T, De Luca V (2015b) Completion of the seven-step pathway from tabersonine to the anticancer drug precursor vindoline and its assembly in yeast. Proc Natl Acad Sci USA 112: 6224-6229
55. R Development Core Team (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
56. Rana S, Lattoo SK, Dhar N, Razdan S, Bhat WW, Dhar RS, Vishwakarma R (2013) NADPH-cytochrome P450 reductase: molecular cloning and functional characterization of two paralogs from Withania somnifera (L.) Dunal. PLoS ONE 8: e57068
57. Ro DK, Ehlting J, Douglas CJ (2002) Cloning, functional expression, and subcellular localization of multiple NADPH-cytochrome P450 reductases from hybrid poplar. Plant Physiol 130: 1837-1851
58. Salim V, Wiens B, Masada-Atsumi S, Yu F, De Luca V (2014) 7-Deoxyloganetic acid synthase catalyzes a key 3 step oxidation to form 7-deoxyloganetic acid in Catharanthus roseus iridoid biosynthesis. Phytochemistry 101: 23-31
59. Salim V, Yu F, Altarejos J, De Luca V (2013) Virus-induced gene silencing identifies Catharanthus roseus 7-deoxyloganic acid-7-hydroxylase, a step in iridoid and monoterpene indole alkaloid biosynthesis. Plant J 76: 754-765
60. 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
61. Schwarz H, Liu B, Peters S, Barillas W, Beerhues L (2009) Purification, cDNA cloning and functional expression of NADPH-cytochrome P450 reductase from Centaurium erythraea cell cultures. Plant Biol (Stuttg) 11: 300-306
62. Shephard EA, Phillips IR, Bayney RM, Pike SF, Rabin BR (1983) Quantification of NADPH:cytochrome P-450 reductase in liver microsomes by a specific radioimmunoassay technique. Biochem J 211: 333-340
63. Soitamo AJ, Piippo M, Allahverdiyeva Y, Battchikova N, Aro EM (2008) Light has a specific role in modulating Arabidopsis gene expression at low temperature. BMC Plant Biol 8: 13
64. 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
65. Sundin L, Vanholme R, Geerinck J, Goeminne G, Höfer R, Kim H, Ralph J, Boerjan W (2014) Mutation of the inducible ARABIDOPSIS THALIANA CYTOCHROME P450 REDUCTASE2 alters lignin composition and improves saccharification. Plant Physiol 166: 1956-1971
66. Takei K, Yamaya T, Sakakibara H (2004) Arabidopsis CYP735A1 and CYP735A2 encode cytokinin hydroxylases that catalyze the biosynthesis of trans-zeatin. J Biol Chem 279: 41866-41872
67. Tang T, Zhao C, Feng X, Liu X, Qiu L (2012) Knockdown of several components of cytochrome P450 enzyme systems by RNA interference enhances the susceptibility of Helicoverpa armigera to fenvalerate. Pest Manag Sci 68: 1501-1511
68. Urban P, Mignotte C, Kazmaier M, Delorme F, Pompon D (1997) Cloning, yeast expression, and characterization of the coupling of two distantly related Arabidopsis thaliana NADPH-cytochrome P450 reductases with P450 CYP73A5. J Biol Chem 272: 19176-19186
69. Van Moerkercke A, Fabris M, Pollier J, Baart GJ, Rombauts S, Hasnain G, Rischer H, Memelink J, Oksman-Caldentey KM, Goossens A (2013) CathaCyc, a metabolic pathway database built from Catharanthus roseus RNA-Seq data. Plant Cell Physiol 54: 673-685
70. Varadarajan J, Guilleminot J, Saint-Jore-Dupas C, Piégu B, Chabouté ME, Gomord V, Coolbaugh RC, Devic M, Delorme V (2010) ATR3 encodes a diflavin reductase essential for Arabidopsis embryo development. New Phytol 187: 67-82
71. Wang M, Roberts DL, Paschke R, Shea TM, Masters BS, Kim JJ (1997) Three-dimensional structure of NADPH-cytochrome P450 reductase: prototype for FMN-and FAD-containing enzymes. Proc Natl Acad Sci USA 94: 8411-8416
72. Xiao M, Zhang Y, Chen X, Lee EJ, Barber CJ, Chakrabarty R, Desgagné-Penix I, Haslam TM, Kim YB, Liu E, et al (2013) Transcriptome analysis based on next-generation sequencing of non-model plants producing specialized metabolites of biotechnological interest. J Biotechnol 166: 122-134
73. Yang CQ, Lu S, Mao YB, Wang LJ, Chen XY (2010) Characterization of two NADPH:cytochrome P450 reductases from cotton (Gossypium hirsutum). Phytochemistry 71: 27-35