An inducible NADPH-cytochrome P450 reductase from Picrorhiza kurrooa - An imperative redox partner of cytochrome P450 enzymes

Functional and Integrative Genomics

Volumn 14, Issue 2, 2014, Pages 381-399

  Bhat, Wajid Waheed ^a   Rana, Satiander ^a   Dhar, Niha ^a   Razdan, Sumeer ^a   Pandith, Shahzad A ^a   Vishwakarma, Ram ^a   Lattoo, Surrinder K ^a  

^a CSIR INDIAN INSTITUTE OF INTEGRATIVE MEDICINE   (India)

Author keywords

Elicitors; Functional characterization; Homology modelling; NADPH cytochrome P450 reductase; Picrorhiza kurrooa; Picrosides

Indexed keywords

2,4 DICHLOROPHENOXYACETIC ACID; CYTOCHROME P450 REDUCTASE; JASMONIC ACID METHYL ESTER; PHYTOHORMONE; PICROSIDE I; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE FERRIHEMOPROTEIN REDUCTASE; SALICYLIC ACID; UNSPECIFIC MONOOXYGENASE; ACETIC ACID DERIVATIVE; CYCLOPENTANE DERIVATIVE; IRIDOID; OXYLIPIN; RECOMBINANT PROTEIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE FERRIHEMOPROTEIN REDUCTASE; VEGETABLE PROTEIN;

ARTICLE; BIOACCUMULATION; CONTROLLED STUDY; ELECTRON TRANSPORT; HORMONE ACTION; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; OXIDATION REDUCTION STATE; PHYLOGENETIC TREE; PICRORHIZA KURROA; PLANT DEFENSE; PLANT TISSUE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; STRUCTURE ANALYSIS; TRANSCRIPTION REGULATION; ULTRAVIOLET B RADIATION; ALTITUDE; DRUG EFFECTS; ENZYME ACTIVATION; ENZYMOLOGY; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETIC TRANSCRIPTION; GENETICS; KINETICS; METABOLISM; OXIDATION REDUCTION REACTION; PLANT LEAF;

ESCHERICHIA COLI; PICRORHIZA KURROOA;

2,4-DICHLOROPHENOXYACETIC ACID; ACETATES; ALTITUDE; CYCLOPENTANES; ENZYME ACTIVATION; ESCHERICHIA COLI; GENE EXPRESSION REGULATION, PLANT; GENE REGULATORY NETWORKS; IRIDOID GLUCOSIDES; KINETICS; METABOLIC NETWORKS AND PATHWAYS; NADPH-FERRIHEMOPROTEIN REDUCTASE; OXIDATION-REDUCTION; OXYLIPINS; PICRORHIZA; PLANT GROWTH REGULATORS; PLANT LEAVES; PLANT PROTEINS; PROMOTER REGIONS, GENETIC; RECOMBINANT PROTEINS; SALICYLIC ACID; TRANSCRIPTION, GENETIC;

EID: 84903394422     PISSN: 1438793X     EISSN: 14387948     Source Type: Journal    
DOI: 10.1007/s10142-014-0362-7     Document Type: Article

References (63)

1. Ansari RA, Tripathi SC, Patnaik GK, Dhawan BN (1991) Antihepatotoxic properties of picroliv: an active fraction from rhizomes of Picrorhiza kurrooa. J Ethnopharmacol 34(1):61-68
2. Bahuguna R, Purohit M, Rawat M, Purohit A (2000) Qualitative and quantitative variations in alkaloids of Aconitum species from Garhwal Himalaya. J Plant Biol 27(2):179-183
3. Barnes PW, Flint SD, Caldwell MM (1987) Photosynthesis damage and protective pigments in plants from a latitudinal arctic/alpine gradient exposed to supplemental UV-B radiation in the field. Arct Alp Res 19:21-27
4. Bartwal A,Mall R, Lohani P, Guru SK, Arora S (2013) Role of secondary metabolites and brassinosteroids in plant defense against environmental stresses. J Plant Growth Regul 32(1):216-232. doi:10.1007/s00344-012-9272-x
5. Benveniste I, Gabriac B, Durst F (1986) Purification and characterization of the NADPH-cytochrome P-450 (cytochrome c) reductase from higher-plant microsomal fraction. Biochem J 235:365-373
6. Bhandari P, Kumar N, Singh B, Gupta AP, Kaul VK, Ahuja PS (2009) Stability-indicating LC-PDA method for determination of picrosides in hepatoprotective Indian herbal preparations of Picrorhiza kurroa. Chromatographia 69(3-4):221-227
7. Bhat WW, Dhar RS, Vishwakarma RA, Lattoo SK (2012a) Metabolic profiling of Picrorhiza kurrooa and molecular characterization of key regulatory genes of picroside biosynthesis. In: The 4th EMBO meeting, Nice, France. EuropeanMolecular biology Organisation, p 183
8. Bhat WW, Lattoo SK, Rana S, Razdan S, Dhar N, Dhar RS, Vishwakarma RA (2012b) Efficient plant regeneration via direct organogenesis and Agrobacterium tumefaciens-mediated genetic transformation of Picrorhiza kurroa: an endangered medicinal herb of the alpine Himalayas. In Vitro Cell Dev Plant 48:1-9
9. Bhat WW, Lattoo SK, Razdan S, Dhar N, Rana S, Dhar RS, Khan S, Vishwakarma RA (2012c) Molecular cloning, bacterial expression and promoter analysis of squalene synthase from Withania somnifera (L.) Dunal. Gene 499(1):25-36. doi:10.1016/j.gene.2012.03.004
10. Bhat WW, Dhar N, Razdan S, Rana S, Mehra R, Nargotra A, Dhar RS, Ashraf N, Vishwakarma R, Lattoo SK (2013) Molecular characterization of UGT94F2 and UGT86C4, two glycosyltransferases from Picrorhiza kurrooa: comparative structural insight and evaluation of substrate recognition. PLoS One. doi:10.1371/journal.pone. 0073804
11. Brosché M, Fant C, Bergkvist SW, Strid H, Svensk A, Olsson O, Strid AÅ (1999) Molecular markers for UV-B stress in plants: alteration of the expression of four classes of genes in Pisum sativum and the formation of high molecular mass RNA adducts. Biochim Biophys Acta Gene Struct Expr 1447(2-3):185-198. doi:10.1016/S0167- 4781(99)00154-2
12. Caldwell MM, Robberecht R, Flint SD (1983) Internal filters: prospects for UVacclimation in higher plants. Physiol Plant 58(3):445-450
13. Camas N, Radusiene J, Ivanauskas L, Jakstas V, Cirak C (2013) Altitudinal changes in the content of bioactive substances in Hypericum orientale and Hypericum pallens. Acta Physiol Plant : 1-12. doi: 10.1007/s11738-013-1446-z
14. Chander R, Kapoor NK, Dhawan BN (1992) Picroliv, picroside-I and kutkoside from Picrorhiza kurrooa are scavengers of superoxide anions. Biochem Pharmacol 44(1):180-183
15. Clarke SM,Mur LA,Wood JE, Scott IM(2004) Salicylic acid dependent signaling promotes basal thermotolerance but is not essential for acquired thermotolerance in Arabidopsis thaliana. Plant J 38(3): 432-447 (Pubitemid 38601042)
16. Dorsch W, Stuppner H, Wagner H, Gropp M, Demoulin S, Ring J (1991) Antiasthmatic effects of Picrorhiza kurroa : androsin prevents allergen- and PAF-induced bronchial obstruction in guinea pigs. Int Arch Allergy Appl Immunol 95(2-3):128-133
17. Duan H, Schuler MA (2006) Heterologous expression and strategies for encapsulation of membrane-localized plant P450s. Phytochem Rev 5(2-3):507-523 (Pubitemid 44900363)
18. Eberle D, Ullmann P, Werck-Reichhart D, Petersen M (2009) cDNA cloning and functional characterisation of CYP98A14 and NADPH:cytochrome P450 reductase from Coleus blumei involved in rosmarinic acid biosynthesis. Plant Mol Biol 69(3):239-253. doi: 10.1007/s11103-008-9420-7
19. El-Beltagi HS, Ahmed OK, El-DesoukyW(2011) Effect of low doses γ- irradiation on oxidative stress and secondary metabolites production of rosemary (Rosmarinus officinalis L.) callus culture. Radiat Phys Chem 80(9):968-976. doi:10.1016/j.radphyschem.2011.05.002
20. Gahlan P, Singh HR, Shankar R, Sharma N, Kumari A, Chawla V, Ahuja PS, Kumar S (2012) De novo sequencing and characterization of Picrorhiza kurrooa transcriptome at two temperatures showed major transcriptome adjustments. BMC Genomics 13(1):126. doi:10.1186/1471-2164-13-126
21. Gupta A, Khajuria A, Singh J, Bedi KL, Satti NK, Dutt P, Suri KA, Suri OP, Qazi GN (2006) Immunomodulatory activity of biopolymeric fraction RLJ-NE-205 f rom Picrorhiza kurroa . Int Immunopharmacol 6(10):1543-1549. doi:10.1016/j.intimp.2006.05.002 (Pubitemid 44216197)
22. Huang F-C, Sung P-H, Do Y-Y, Huang P-L (2012) Differential expression and functional characterization of the NADPH cytochrome P450 reductase genes from Nothapodytes foetida. Plant Sci 190: 16-23
23. Jennewein S, Park H, DeJong JHM, Long RM, Bollon AP, Croteau RB (2005) Coexpression in yeast of Taxus cytochrome P450 reductase with cytochrome P450 oxygenases involved in Taxol biosynthesis. Biotechnol Bioeng 89(5):588-598 (Pubitemid 40444813)
24. Joy K, Kuttan R (1999) Anti-diabetic activity of Picrorrhiza kurroa extract. J Ethnopharmacol 67(2):143-148 (Pubitemid 29421668)
25. Joy K, Rajeshkumar N, Kuttan G, Kuttan R (2000) Effect of Picrorrhiza kurroa extract on transplanted tumours and chemical carcinogenesis in mice. J Ethnopharmacol 71(1):261-266 (Pubitemid 30440677)
26. Katoch M, Fazli I, Suri K, Ahuja A, Qazi G (2011) Effect of altitude on picroside content in core collections of Picrorhiza kurrooa from the north western Himalayas. J Nat Med 65(3-4):578-582
27. Kawoosa T, Singh H, Kumar A, Sharma S, Devi K, Dutt S, Vats S, Sharma M, Ahuja P, Kumar S (2010) Light and temperature regulated terpene biosynthesis: hepatoprotective monoterpene picroside accumulation in Picrorhiza kurrooa. Funct Integr Genom 10(3): 393-404. doi:10.1007/s10142-009-0152-9
28. Kawoosa T, Gahlan P,DeviAS, Kumar S (2013) TheGATAand SORLIP motifs in the 3-hydroxy-3-methylglutaryl-CoA reductase promoter of Picrorhiza kurrooa for the control of light-mediated expression. Funct Integr Genom. doi:10.1007/s10142-013-0350-3
29. Keasling JD (2012) Synthetic biology and the development of tools for metabolic engineering. Metab Eng 14(3):189-195. doi:10.1016/j.ymben.2012.01.004
30. Koopmann E, Hahlbrock K (1997) Differentially regulated NADPH: cytochrome P450 oxidoreductases in parsley. Proc Natl Acad Sci U S A 94(26):14954-14959 (Pubitemid 28041481)
31. Kumar V, Sood H, Sharma M, Chauhan RS (2013) A proposed biosynthetic pathway of picrosides linked through the detection of biochemical intermediates in the endangered medicinal herb Picrorhiza kurroa. Phytochem Anal 24(6):598-602
32. Madronich S,McKenzie RL, Björn LO, CaldwellMM(1998) Changes in biologically active ultraviolet radiation reaching the Earth's surface. J Photochem Photobiol B Biol 46(1):5-19 (Pubitemid 29017147)
33. Martin D, Tholl D, Gershenzon J, Bohlmann J (2002) Methyl jasmonate induces traumatic resin ducts, terpenoid resin biosynthesis, and terpenoid accumulation in developing xylem of Norway spruce stems. Plant Physiol 129(3):1003-1018. doi:10.1104/pp.011001 (Pubitemid 34801074)
34. Matsuura H, Costa F, Yendo A, Fett-Neto A (2013) Photoelicitation of bioactive secondary metabolites by ultraviolet radiation: Mechanisms, strategies, and applications. In: Chandra S, Lata H, Varma A (eds) Biotechnology for medicinal plants. Springer, Berlin, pp 171-190. doi:10.1007/978-3-642- 29974-2-7
35. Meijer AH, Cardoso M, Voskuilen JT, 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 mono-oxygenases in plants. Plant J 4(1):47-60
36. Mizutani M, Ohta D (1998) Two isoforms of NADPH:cytochrome P450 reductase in Arabidopsis thaliana. Gene structure, heterologous expression in insect cells, and differential regulation. Plant Physiol 116(1):357-367 (Pubitemid 28503871)
37. Mondal TK, Bantawa P, Sarkar B, Ghosh P, Chand PK (2012) Cellular differentiation, regeneration, and secondary metabolite production in medicinal Picrorhiza spp. Plant Cell Tissue Organ 112:1-16
38. Morant M, Jorgensen K, Schaller H, Pinot F, Moller BL, Werck- Reichhart D, Bak S (2007) CYP703 is an ancient cytochrome P450 in land plants catalyzing in-chain hydroxylation of lauric acid to provide building blocks for sporopollenin synthesis in pollen. Plant Cell 19(5):1473-1487 (Pubitemid 47025371)
39. Ohta D, Mizutani M (2004) Redundancy or flexibility: molecular diversity of the electron transfer components for P450 monooxygenases in higher plants. Front Biosci 9:1587-1597 (Pubitemid 38918617)
40. Pandit S, Shitiz K, Sood H, Chauhan RS (2012a) Differential biosynthesis and accumulation of picrosides in an endangered medicinal herb Picrorhiza kurroa. J Plant Biochem Biotechnol 22(3):335-342
41. Pandit S, Shitiz K, Sood H, Naik PK, Chauhan RS (2012b) Expression pattern of fifteen genes of non-mevalonate (MEP) and mevalonate (MVA) pathways in different tissues of endangered medicinal herb Picrorhiza kurroa with respect to picrosides content. Mol Biol Rep 40(2):1053-1063. doi:10.1007/s11033-012- 2147-1
42. Porter TD, Beck TW, Kasper CB (1990) NADPH-cytochrome P-450 oxidoreductase gene organization correlates with structural domains of the protein. Biochemistry 29(42):9814-9818 (Pubitemid 20348513)
43. Rajkumar V, Guha G, Kumar RA (2011) Antioxidant and anti-neoplastic activities of Picrorhiza kurroa extracts. Food Chem Toxicol 49(2): 363-369. doi:10.1016/j.fct.2010.11.009
44. 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(2):e57068
45. Reichhart D, Salaün J-P, Benveniste I, Durst F (1980) Time course of induction of cytochrome P-450, NADPH-cytochrome c reductase, and cinnamic acid hydroxylase by phenobarbital, ethanol, herbicides, and manganese in higher plant microsomes. Plant Physiol 66(4):600-604
46. 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(4):1837-1851. doi: 10.1104/pp. 008011
47. Saraswat B,Visen PK, Patnaik GK, Dhawan BN (1997) Protective effect of picroliv, active constituent of Picrorhiza kurrooa, against oxytetracycline induced hepatic damage. Indian J Exp Biol 35(12):1302-1305 (Pubitemid 28011599)
48. Schreiner M, Mewis I, Huyskens-Keil S, Jansen MAK, Zrenner R, Winkler JB, O'Brien N, Krumbein A (2012) UV-B-induced secondary plant metabolites - potential benefits for plant and human health. Crit Rev Plant Sci 31(3):229-240. doi:10.1080/07352689.2012.664979
49. Schuler MA, Werck-Reichhart D (2003) Functional genomics of P450s. Annu Rev Plant Biol 54(1):629-667 (Pubitemid 37400008)
50. Shet MS, Sathasivan K, Arlotto MA, Mehdy MC, Estabrook RW (1993) Purification, characterization, and cDNA cloning of an NADPH- cytochrome P450 reductase from mung bean. Proc Natl Acad Sci U S A 90(7):2890-2894 (Pubitemid 23113523)
51. Singh H, Gahlan P, Dutt S, Ahuja PS, Kumar S (2011) Why uproot Picrorhiza kurrooa, an endangered medicinal herb? Curr Sci 100(7):1055-1059
52. Singh H, Gahlan P, Kumar S (2013) Cloning and expression analysis of ten genes associated with picrosides biosynthesis in Picrorhiza kurrooa. Gene 515(2):320-328
53. Sood H, Chauhan R (2010) Biosynthesis and accumulation of amedicinal compound, Picroside-I, in cultures of Picrorhiza kurroa Royle ex Benth. Plant Cell Tissue Organ 100(1):113-117
54. Spitaler R, Schlorhaufer PD, Ellmerer EP, Merfort I, Bortenschlager S, Stuppner H, Zidorn C (2006) Altitudinal variation of secondary metabolite profiles in flowering heads of Arnica montana cv. ARBO. Phytochemistry 67:409-417 (Pubitemid 43148953)
55. Spitaler R, Winkler A, Lins I, Yanar S, Stuppner H, Zidorn C (2008) Altitudinal variation of phenolic contents in flowering heads of Arnica montana cv. ARBO: a 3-year comparison. J Chem Ecol 34(3):369-375. doi:10.1007/s10886- 007-9407-x
56. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods.Mol Biol Evol 28(10):2731-2739
57. Tripathy MK, Tyagi W, Goswami M, Kaul T, Singla-Pareek SL, Deswal R, Reddy MK, Sopory SK (2012) Characterization and functional validation of tobacco PLC Delta for abiotic stress tolerance. Plant Mol Biol Report 30(2):488-497
58. Turunen M, Latola K (2005) UV-B radiation and acclimation in timberline plants. Environ Pollut 137(3):390-403 (Pubitemid 40991245)
59. Vermilion J, Ballou D,MasseyV, CoonM(1981) Separate roles forFMN and FAD in catalysis by liver microsomal NADPH-cytochrome P-450 reductase. J Biol Chem 256(1):266-277
60. Vickers CE, Gershenzon J, Lerdau MT, Loreto F (2009) A unified mechanism of action for volatile isoprenoids in plant abiotic stress. Nat Chem Biol 5(5):283-291
61. Wang M, Roberts DL, Paschke R, Shea TM, Masters BSS, Kim J-JP (1997) Three-dimensional structure of NADPH-cytochrome P450 reductase: prototype for FMN-and FAD-containing enzymes. Proc Natl Acad Sci U S A 94(16):8411-8416 (Pubitemid 27335052)
62. Yang C-Q, Lu S, Mao Y-B,Wang L-J, Chen X-Y (2010) Characterization of two NADPH: cytochrome P450 reductases from cotton (Gossypium hirsutum). Phytochemistry 71(1):27-35
63. Zhang L, Lu X, Shen Q, Chen Y, Wang T, Zhang F,Wu S, JiangW, Liu P, Zhang L (2012) Identification of putative Artemisia annua ABCG transporter unigenes related to artemisinin yield following expression analysis in different plant tissues and in response tomethyl jasmonate and abscisic acid treatments. Plant Mol Biol Rep 30(4):838-847