Molecular characterization of two A-type P450s, WsCYP98A and WsCYP76A from Withania somnifera (L.) Dunal: Expression analysis and withanolide accumulation in response to exogenous elicitations

BMC Biotechnology

Volumn 14, Issue 1, 2014, Pages

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

^a CSIR INDIAN INSTITUTE OF INTEGRATIVE MEDICINE   (India)

Author keywords

Cytochrome P450 monooxygenase; E.coli; mRNA; Phytohormones; Withania somnifera; Withanolides

Indexed keywords

AMINO ACIDS; BIOCHEMISTRY; CHARACTERIZATION; CLONING; ESCHERICHIA COLI; GENE EXPRESSION; GENES; METABOLISM; MOLECULES; PLANTS (BOTANY); POLYMERASE CHAIN REACTION;

E.COLI; MONOOXYGENASES; MRNA; PHYTOHORMONES; WITHANIA SOMNIFERA; WITHANOLIDES;

SALICYLIC ACID;

AMINO ACID; COMPLEMENTARY DNA; GIBBERELLIC ACID; JASMONIC ACID METHYL ESTER; SALICYLIC ACID; WITHANOLIDE;

ARTICLE; BIOACCUMULATION; CONTROLLED STUDY; ESCHERICHIA COLI; EXPRESSION VECTOR; GENE EXPRESSION; GENE SEQUENCE; GENETIC TRANSCRIPTION; HETEROLOGOUS EXPRESSION; MOLECULAR CLONING; NONHUMAN; OPEN READING FRAME; PLANT GENE; PLANT LEAF; PLANT RESPONSE; PLANT STEM; PLANT STRESS; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SECONDARY METABOLISM; TRANSCRIPTION REGULATION; WITHANIA SOMNIFERA; WSCYP76A GENE; WSCYP98A GENE;

EID: 84928739077     PISSN: None     EISSN: 14726750     Source Type: Journal    
DOI: 10.1186/s12896-014-0089-5     Document Type: Article

References (67)

1. Cheng Q, Guengerich FP: Identification of Endogenous Substrates of Orphan Cytochrome P450 Enzymes Through the Use of Untargeted Metabolomics Approaches. In Cytochrome P450 Protocols, Volume 987. Edited by Phillips IR, Shephard EA, de Montellano PR O. New York: Humana Press; 2013:71-77.
2. Nelson DR, Nebert DW: Cytochrome P450 (CYP) Gene Superfamily. In eLS. West Sussex: John Wiley & Sons, Ltd; 2011.
3. Nelson D, Ming R, Alam M, Schuler M: Comparison of cytochrome P450 genes from six plant genomes. Trop Plant Biol 2008, 1(3-4):216-235.
4. Nelson D, Werck-Reichhart D: A P450-centric view of plant evolution. Plant J 2011, 66(1):194-211.
5. Schuler MA, Werck-Reichhart D: Functional genomics of P450s. Annu Rev Plant Biol 2003, 54:629-667.
6. de Montellano PRO: Cytochrome P450: Structure, Mechanism, and Biochemistry. New York: Springer; 2005.
7. Bak S, Beisson F, Bishop G, Hamberger B, Hofer R, Paquette S, Werck-Reichhart D: Cytochromes P450. Arabidopsis Book 2011, 9(10):6.
8. Werck-Reichhart D, Feyereisen R: Cytochromes P450: a success story. Genome Biol 2000, 1(6):8.
9. Schuler MA: The role of cytochrome P450 monooxygenases in plant-insect interactions. Plant Physiol 1996, 112(4):1411-1419.
10. Miners JO: Evolution of drug metabolism: hitchhiking the technology bandwagon. Clin Exp Pharmacol Physiol 2002, 29(11):1040-1044.
11. Guengerich FP: Cytochrome P450 enzymes in the generation of commercial products. Nat Rev Drug Discov 2002, 1(5):359-366.
12. Guengerich FP: Special issue: P450 catalysis mechanisms introduction. Arch Biochem Biophys 2011, 507(1):1-2.
13. Sono M, Roach MP, Coulter ED, Dawson JH: Heme-containing oxygenases. Chem Rev 1996, 96(7):2841-2888.
14. Guengerich FP: Uncommon P450-catalyzed reactions. Curr Drug Metab 2001, 2(2):93-115.
15. Coon M: Cytochrome P450: Nature's most versatile biological catalyst. Annu Rev Pharmacol Toxicol 2005, 45:1-25.
16. Kirson I, Glotter E, Lavie D, Abraham A: Constitutents of Withania somnifera Dun. Part XII The withanolides of an indian chemotype. J Chem Soc C: Organic 1971, 2032-2044.
17. Lattoo SK, Dhar RS, Khan S, Bamotra S, Dhar AK: Temporal sexual maturation and incremental staminal movement encourages mixed mating in Withania somnifera -An insurance for reproductive success. Curr Sci 2007, 92(10):1390-1399.
18. Rana S, Dhar N, Bhat WW, Razdan S, Khan S, Dhar RS, Dutt P, Lattoo SK: A 12-deoxywithastramonolide-rich somaclonal variant in Withania somnifera (L.) Dunal-molecular cytogenetic analysis and significance as a chemotypic resource. In Vitro Cell Dev Biol-Plant 2012, 48(5):546-554.
19. Chaurasiya ND, Sangwan NS, Sabir F, Misra L, Sangwan RS: Withanolide biosynthesis recruits both mevalonate and DOXP pathways of isoprenogenesis in Ashwagandha Withania somnifera L. (Dunal). Plant Cell Rep 2012, 31(10):1889-1897.
20. Dhar N, Rana S, Razdan S, Bhat WW, Hussain A, Dhar RS, Vaishnavi S, Hamid A, Vishwakarma R, Lattoo SK: Cloning and functional characterization of three branch point oxidosqualene cyclases from Withania somnifera (L.) dunal. J Biol Chem 2014, 289(24):17249-17267.
21. Rana S, Lattoo SK, Dhar N, Razdan S, Bhat WW, Dhar RS, Vishwakarma R: NADPH-cytochrome P450 reductase: molecular cloning and functional characterization of Two paralogs from Withania somnifera (L.) dunal. PLoS One 2013, 8(2):e57068.
22. Dhar N, Rana S, Bhat WW, Razdan S, Pandith SA, Khan S, Dutt P, Dhar RS, Vaishnavi S, Vishwakarma R, Lattoo SK: Dynamics of withanolide biosynthesis in relation to temporal expression pattern of metabolic genes in Withania somnifera (L.) Dunal: a comparative study in two morpho-chemovariants. Mol Biol Rep 2013, 40(12):7007-7016.
23. Bhat WW, Dhar N, Razdan S, Rana S, Mehra R, Nargotra A, Dhar RS, Ashraf N, Vishwakarma R, Lattoo SK: Molecular characterization of UGT94F2 and UGT86C4, Two glycosyltransferases from picrorhiza kurrooa: comparative structural insight and evaluation of substrate recognition. PLoS One 2013, 8(9):e73804.
24. Karamat F, Olry A, Doerper S, Vialart G, Ullmann P, Werck-Reichhart D, Bourgaud F, Hehn A: CYP98A22, a phenolic ester 3'-hydroxylase specialized in the synthesis of chlorogenic acid, as a new tool for enhancing the furanocoumarin concentration in Ruta graveolens. BMC Plant Biol 2012, 12(1):152.
25. Miettinen K, Dong L, Navrot N, Schneider T, Burlat V, Pollier J, Woittiez L, van der Krol S, Lugan R, Ilc T, Verpoorte R, Oksman-Caldentey KM, Martinoia E, Bouwmeester H, Goossens A, Memelink J, Werck-Reichhart D: The seco-iridoid pathway from Catharanthus roseus. Nat Commun 2014, 5, doi:10.1038/ncomms4606.
26. Hofer R, Dong L, Andre F, Ginglinger JF, Lugan R, Gavira C, Grec S, Lang G, Memelink J, Van der Krol S, Bouwmeester H, Werck-Reichhart D: 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 2013, 20:221-232.
27. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG: Clustal W and ClustalX version 2.0. Bioinformatics 2007, 23(21):2947-2948.
28. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S: MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 2013, 30(12):2725-2729.
29. Geourjon C, Deleage G: SOPMA: significant improvements in protein secondary structure prediction by consensus prediction from multiple alignments. Comput Appl Biosci 1995, 11(6):681-684.
30. Kelley LA, Sternberg MJE: Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 2009, 4(3):363-371.
31. Lovell SC, Davis IW, Arendall WB 3rd, de Bakker PI, Word JM, Prisant MG, Richardson JS, Richardson DC: Structure validation by Calpha geometry: phi, psi and Cbeta deviation. Proteins 2003, 50(3):437-450.
32. Celniker G, Nimrod G, Ashkenazy H, Glaser F, Martz E, Mayrose I, Pupko T, Ben-Tal N: ConSurf: using evolutionary data to raise testable hypotheses about protein function. Isr J Chem 2013, 53(3-4):199-206.
33. -ΔΔCT method. Methods 2001, 25(4):402-408.
34. Dhar RS, Verma V, Suri KA, Sangwan RS, Satti NK, Kumar A, Tuli R, Qazi GN: Phytochemical and genetic analysis in selected chemotypes of Withania somnifera. Phytochemistry 2006, 67(20):2269-2276.
35. Sterky F, Regan S, Karlsson J, Hertzberg M, Rohde A, Holmberg A, Amini B, Bhalerao R, Larsson M, Villarroel R, Van Montagu M, Sandberg G, Olsson O, Teeri TT, Boerjan W, Gustafsson P, Uhlen M, Sundberg B, Lundeberg J: Gene discovery in the wood-forming tissues of poplar: analysis of 5, 692 expressed sequence tags. Proc Natl Acad Sci U S A 1998, 95(22):13330-13335.
36. Allona I, Quinn M, Shoop E, Swope K, St Cyr S, Carlis J, Riedl J, Retzel E, Campbell MM, Sederoff R, Whetten RW: Analysis of xylem formation in pine by cDNA sequencing. Proc Natl Acad Sci U S A 1998, 95(16):9693-9698.
37. Schoch G, Goepfert S, Morant M, Hehn A, Meyer D, Ullmann P, Werck-Reichhart D: CYP98A3 from Arabidopsis thaliana is a 3 '-hydroxylase of phenolic esters, a missing link in the phenylpropanoid pathway. J Biol Chem 2001, 276(39):36566-36574.
38. Matsuno M, Compagnon V, Schoch GA, Schmitt M, Debayle D, Bassard JE, Pollet B, Hehn A, Heintz D, Ullmann P, Lapierre C, Bernier F, Ehlting J, Werck-Reichhart D: Evolution of a novel phenolic pathway for pollen development. Science 2009, 325(5948):1688-1692.
39. Imaishi H, Ishitobi U: Molecular cloning of CYP76A3, a novel cytochrome P450 from Petunia hybrida catalyzing the omega-hydroxylation of myristic acid. Biologia Plantarum 2008, 52(2):242-250.
40. Yang L, Ding G, Lin H, Cheng H, Kong Y, Wei Y, Fang X, Liu R, Wang L, Chen X, Chen X, Yang C: Transcriptome analysis of medicinal plant Salvia miltiorrhiza and identification of genes related to tanshinone biosynthesis. PLoS One 2013, 8(11):e80464.
41. Martin D, Tholl D, Gershenzon J, Bohlmann J: Methyl jasmonate induces traumatic resin ducts, terpenoid resin biosynthesis, and terpenoid accumulation in developing xylem of Norway spruce stems. Plant Physiol 2002, 129(3):1003-1018.
42. Oudin A, Mahroug S, Courdavault V, Hervouet N, Zelwer C, Rodriguez-Concepcion M, St-Pierre B, Burlat V: Spatial distribution and hormonal regulation of gene products from methyl erythritol phosphate and monoterpene-secoiridoid pathways in Catharanthus roseus. Plant Mol Biol 2007, 65(1-2):13-30.
43. Draper J: Salicylate, superoxide synthesis and cell suicide in plant defence. Trends Plant Sci 1997, 2(5):162-165.
44. Ali MB, Yu KW, Hahn EJ, Paek KY: Methyl jasmonate and salicylic acid elicitation induces ginsenosides accumulation, enzymatic and non-enzymatic antioxidant in suspension culture Panax ginseng roots in bioreactors. Plant Cell Rep 2006, 25(6):613-620.
45. Hayat Q, Hayat S, Irfan M, Ahmad A: Effect of exogenous salicylic acid under changing environment: a review. Environ Exp Bot 2010, 68(1):14-25.
46. Shabani L, Ehsanpour AA, Asghari G, Emami J: Glycyrrhizin production by in vitro cultured Glycyrrhiza glabra elicited by methyl jasmonate and salicylic acid. Russ J Plant Physiol 2009, 56(5):621-626.
47. Kang SM, Min JY, Kim YD, Kang YM, Park DJ, Jung HN, Kim SW, Choi MS: Effects of methyl jasmonate and salicylic acid on the production of bilobalide and ginkgolides in cell cultures of Ginkgo biloba. In Vitro Cell Dev Biol-Plant 2006, 42(1):44-49.
48. Pu GB, Ma DM, Chen JL, Ma LQ, Wang H, Li GF, Ye HC, Liu BY: Salicylic acid activates artemisinin biosynthesis in Artemisia annua L. Plant Cell Rep 2009, 28(7):1127-1135.
49. Narusaka Y, Narusaka M, Seki M, Umezawa T, Ishida J, Nakajima M, Enju A, Shinozaki K: Crosstalk in the responses to abiotic and biotic stresses in Arabidopsis: analysis of gene expression in cytochrome P450 gene superfamily by cDNA microarray. Plant Mol Biol 2004, 55(3):327-342.
50. Basson AE, Dubery IA: Identification of a cytochrome P450 cDNA (CYP98A5) from Phaseolus vulgaris, inducible by 3,5-dichlorosalicylic acid and 2,6-dichloro isonicotinic acid. J Plant Physiol 2007, 164(4):421-428.
51. Pu G, Wang P, Zhou B, Liu Z, Xiang F: Cloning and characterization of Lonicera japonica p-coumaroyl ester 3-hydroxylase which is involved in the biosynthesis of chlorogenic acid. Biosci Biotechnol Biochem 2013, 77(7):1403-1409.
52. Peng X, Li W, Wang W, Bai G: Cloning and characterization of a cDNA coding a hydroxycinnamoyl-CoA quinate hydroxycinnamoyl transferase involved in chlorogenic acid biosynthesis in Lonicera japonica. Planta Med 2010, 76(16):1921-1926.
53. Nawrath C: The biopolymers cutin and suberin. The Arabidopsis book/Am Soc Plant Biol 2002, 1:e0021.
54. Swaminathan S, Morrone D, Wang Q, Fulton DB, Peters RJ: CYP76M7 is an ent-cassadiene C11 alpha-hydroxylase defining a second multifunctional diterpenoid biosynthetic gene gluster in rice. Plant Cell 2009, 21(10):3315-3325.
55. Ehlting J, Sauveplane V, Olry A, Ginglinger JF, Provart NJ, Werck-Reichhart D: An extensive (co-)expression analysis tool for the cytochrome P450 superfamily in Arabidopsis thaliana. BMC Plant Biol 2008, 8:47.
56. Olszewski N, Sun TP, Gubler F: Gibberellin signaling: biosynthesis, catabolism, and response pathways. Plant Cell 2002, 14(Suppl):S61-S80.
57. Bai MY, Shang JX, Oh E, Fan M, Bai Y, Zentella R, Sun TP, Wang ZY: Brassinosteroid, gibberellin and phytochrome impinge on a common transcription module in Arabidopsis. Nat Cell Biol 2012, 14(8):810-817.
58. Mansouri H, Asrar Z, Mehrabani M: Effects of gibberellic acid on primary terpenoids and delta-tetrahydrocannabinol in Cannabis sativa at flowering stage. J Integr Plant Biol 2009, 51(6):553-561.
59. Jones AMP, Saxena PK, Murch SJ: Elicitation of secondary metabolism in Echinacea purpurea L. by gibberellic acid and triazoles. Eng Life Sci 2009, 9(3):205-210.
60. Ebel J, Mithofer A: Early events in the elicitation of plant defence. Planta 1998, 206(3):335-348.
61. van der Fits L, Memelink J: ORCA3, a jasmonate-responsive transcriptional regulator of plant primary and secondary metabolism. Science 2000, 289(5477):295-297.
62. Weiss D, Ori N: Mechanisms of cross talk between gibberellin and other hormones. Plant Physiol 2007, 144(3):1240-1246.
63. Bhat WW, Lattoo SK, Razda S, Dhar N, Rana S, Dhar RS, Khan S, Vishwakarma RA: Molecular cloning, bacterial expression and promoter analysis of squalene synthase from Withania somnifera (L.) Dunal. Gene 2012, 499(1):25-36.
64. Paddon CJ, Keasling JD: Semi-synthetic artemisinin: a model for the use of synthetic biology in pharmaceutical development. Nat Rev Microbiol 2014, 12(5):355-367.
65. Morant M, Bak S, Moller BL, Werck-Reichhart D: Plant cytochromes P450: tools for pharmacology, plant protection and phytoremediation. Curr Opin Biotechnol 2003, 14(2):151-162.
66. Keasling JD: Synthetic biology and the development of tools for metabolic engineering. Metab Eng 2012, 14(3):189-195.
67. Razdan S, Bhat WW, Rana S, Dhar N, Lattoo SK, Dhar RS, Vishwakarma RA: Molecular characterization and promoter analysis of squalene epoxidase gene from Withania somnifera (L.) Dunal. Mol Biol Rep 2013, 40(2):905-916.