Methyl jasmonate-elicited transcriptional responses and pentacyclic triterpene biosynthesis in sweet basil

Plant Physiology

Volumn 164, Issue 2, 2014, Pages 1028-1044

  Misra, Rajesh Chandra ^a   Maiti, Protiti ^b   Chanotiya, Chandan Singh ^a   Shanker, Karuna ^a   Ghosh, Sumit ^a  

^a CSIR CENTRAL INSTITUTE OF MEDICINAL AND AROMATIC PLANTS   (India)

^b JAWAHARLAL NEHRU UNIVERSITY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ACETIC ACID DERIVATIVE; CYCLOPENTANE DERIVATIVE; JASMONIC ACID METHYL ESTER; LANOSTEROL SYNTHASE; MESSENGER RNA; MUTASE; OXYLIPIN; PENTACYCLIC TRITERPENE;

AMINO ACID SEQUENCE; ARTICLE; BASIL; BIOSYNTHESIS; CHEMISTRY; CYTOLOGY; DRUG EFFECT; EXPRESSED SEQUENCE TAG; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE LIBRARY; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; MOLECULAR CLONING; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; PLANT EPIDERMIS; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY; TIME;

ACETATES; AMINO ACID SEQUENCE; BIOSYNTHETIC PATHWAYS; CLONING, MOLECULAR; CYCLOPENTANES; EXPRESSED SEQUENCE TAGS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; GENE LIBRARY; INTRAMOLECULAR TRANSFERASES; MOLECULAR SEQUENCE DATA; OCIMUM BASILICUM; OXYLIPINS; PENTACYCLIC TRITERPENES; PHYLOGENY; PLANT EPIDERMIS; RNA, MESSENGER; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY, AMINO ACID; TIME FACTORS; TRANSCRIPTION, GENETIC;

EID: 84893457272     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.113.232884     Document Type: Article

References (92)

1. Abe I (2007) Enzymatic synthesis of cyclic triterpenes. Nat Prod Rep 24: 1311-1331
2. Abe I, Prestwich GD (1995) Identification of the active site of vertebrate oxidosqualene cyclase. Lipids 30: 231-234
3. Aerts RJ, Gisi D, De Carolis E, De Luca V, Baumann TW (1994) Methyl jasmonate vapor increases the developmentally controlled synthesis of alkaloids in Catharanthus and Cinchona seedlings. Plant J 5: 635-643
4. Alfermann AW (2010) Production of natural products by plant cell and organ cultures. In M Wink, ed, Functions and Biotechnology of Plant Secondary Metabolites, Annual Plant Reviews, Ed 2, Vol 39, Wiley-Blackwell, Oxford, pp 381-399
5. Arshad Qamar K, Dar A, Siddiqui BS, Kabir N, Aslam H, Ahmed S, Erum S, Habib S, Begum S (2010) Anticancer activity of Ocimum basilicum and the effect of ursolic acid on the cytoskeleton of MCF-7 human breast cancer cells. Lett Drug Des Discov 7: 726-736
6. Asamizu E, Nakamura Y, Sato S, Tabata S (2000) A large scale analysis of cDNA in Arabidopsis thaliana: generation of 12,028 non-redundant expressed sequence tags from normalized and size-selected cDNA libraries. DNA Res 7: 175-180
7. Besser K, Harper A, Welsby N, Schauvinhold I, Slocombe S, Li Y, Dixon RA, Broun P (2009) Divergent regulation of terpenoid metabolism in the trichomes of wild and cultivated tomato species. Plant Physiol 149: 499-514
8. Bilal A, Jahan N, Ahmed A, Bilal SN, Habib S, Hajra S (2012) Phytochemical and pharmacological studies on Ocimum basilicum. Int J Curr Res Rev 4: 73-83
9. Bohlmann J, Keeling CI (2008) Terpenoid biomaterials. Plant J 54: 656-669
10. Brendolise C, Yauk YK, Eberhard ED, Wang M, Chagne D, Andre C, Greenwood DR, Beuning LL (2011) An unusual plant triterpene synthase with predominant a-amyrin-producing activity identified by characterizing oxidosqualene cyclases from Malus 3 domestica. FEBS J 278: 2485-2499
11. Buschhaus C, Jetter R (2012) Composition and physiological function of the wax layers coating Arabidopsis leaves: b-amyrin negatively affects the intracuticular water barrier. Plant Physiol 160: 1120-1129
12. Canter PH, Thomas H, Ernst E (2005) Bringing medicinal plants into cultivation: opportunities and challenges for biotechnology. Trends Biotechnol 23: 180-185
13. Carelli M, Biazzi E, Panara F, Tava A, Scaramelli L, Porceddu A, Graham N, Odoardi M, Piano E, Arcioni S, et al (2011) Medicago truncatula CYP716A12 is a multifunctional oxidase involved in the biosynthesis of hemolytic saponins. Plant Cell 23: 3070-3081
14. Chen D, Ye H, Li G (2000) Expression of a chimeric farnesyl diphosphate synthase gene in Artemisia annua L. transgenic plants via Agrobacterium tumefaciens-mediated transformation. Plant Sci 155: 179-185
15. Cheong JJ, Choi YD (2003) Methyl jasmonate as a vital substance in plants. Trends Genet 19: 409-413
16. Choudhury GB, Prabhat KJ, Nayak BS, Panda SK, Tripathy SK (2010) Phytochemical investigation and evaluation of analgesic activity of leafy extracts of various Ocimum (tulsi) species. The Indian Pharmacist 8: 67-70
17. Christianson DW (2006) Structural biology and chemistry of the terpenoid cyclases. Chem Rev 106: 3412-3442
18. da Silva Ferreira D, Esperandim VR, Toldo MP, Kuehn CC, do Prado Júnior JC, Cunha WR, e Silva ML, de Albuquerque S (2013) In vivo activity of ursolic and oleanolic acids during the acute phase of Trypanosoma cruzi infection. Exp Parasitol 134: 455-459
19. Dasgupta T, Rao AR, Yadava PK (2004) Chemomodulatory efficacy of basil leaf (Ocimum basilicum) on drug metabolizing and antioxidant enzymes, and on carcinogen-induced skin and forestomach papillomagenesis. Phytomedicine 11: 139-151
20. Dashputre NL, Naikwade NS (2010) Preliminary immunomodulatory activity of aqueous and ethanolic leaves extracts of Ocimum basilicum Linn. in mice. Int J Pharm Tech Res 2: 1342-1349
21. De Geyter N, Gholami A, Goormachtig S, Goossens A (2012) Transcriptional machineries in jasmonate-elicited plant secondary metabolism. Trends Plant Sci 17: 349-359
22. Ee SF, Oh JM, Mohd Noor N, Kwon TR, Mohamed-Hussein ZA, Ismail I, Zainal Z (2013) Transcriptome profiling of genes induced by salicylic acid and methyl jasmonate in Polygonum minus. Mol Biol Rep 40: 2231-2241
23. Facchini PJ, De Luca V (2008) Opium poppy and Madagascar periwinkle: model non-model systems to investigate alkaloid biosynthesis in plants. Plant J 54: 763-784
24. Fathiazad F, Matlobi A, Khorrami A, Hamedeyazdan S, Soraya H, Hammami M, Maleki-Dizaji N, Garjani A (2012) Phytochemical screening and evaluation of cardioprotective activity of ethanolic extract of Ocimum basilicum L. (basil) against isoproterenol induced myocardial infarction in rats. Daru 20: 87
25. Gang DR, Beuerle T, Ullmann P, Werck-Reichhart D, Pichersky E (2002a) Differential production of meta hydroxylated phenylpropanoids in sweet basil peltate glandular trichomes and leaves is controlled by the activities of specific acyltransferases and hydroxylases. Plant Physiol 130: 1536-1544
26. Gang DR, Lavid N, Zubieta C, Chen F, Beuerle T, Lewinsohn E, Noel JP, Pichersky E (2002b) Characterization of phenylpropene O-methyltransferases from sweet basil: facile change of substrate specificity and convergent evolution within a plant O-methyltransferase family. Plant Cell 14: 505-519
27. Gang DR, Wang J, Dudareva N, Nam KH, Simon JE, Lewinsohn E, Pichersky E (2001) An investigation of the storage and biosynthesis of phenylpropenes in sweet basil. Plant Physiol 125: 539-555
28. Gershenzon J, Dudareva N (2007) The function of terpene natural products in the natural world. Nat Chem Biol 3: 408-414
29. Ghosh S, Meli VS, Kumar A, Thakur A, Chakraborty N, Chakraborty S, Datta A (2011) The N-glycan processing enzymes a-mannosidase and b-D-N-acetylhexosaminidase are involved in ripening-associated softening in the non-climacteric fruits of capsicum. J Exp Bot 62: 571-582
30. Ghosh S, Singh UK, Meli VS, Kumar V, Kumar A, Irfan M, Chakraborty N, Chakraborty S, Datta A (2013) Induction of senescence and identification of differentially expressed genes in tomato in response to monoterpene. PLoS ONE 8: e76029
31. González-Coloma A, Lopez-Balboa C, Santana O, Reina M, Fraga BM (2011) Triterpene-based plant defences. Phytochem Rev 10: 245-260
32. Goossens A, Häkkinen ST, Laakso I, Seppänen-Laakso T, Biondi S, De Sutter V, Lammertyn F, Nuutila AM, Söderlund H, Zabeau M, et al (2003) A functional genomics approach toward the understanding of secondary metabolism in plant cells. Proc Natl Acad Sci USA 100: 8595-8600
33. Gundlach H, Müller MJ, Kutchan TM, Zenk MH (1992) Jasmonic acid is a signal transducer in elicitor-induced plant cell cultures. Proc Natl Acad Sci USA 89: 2389-2393
34. Han JY, Kim HJ, Kwon YS, Choi YE (2011) The Cyt P450 enzyme CYP716A47 catalyzes the formation of protopanaxadiol from dammarenediol-II during ginsenoside biosynthesis in Panax ginseng. Plant Cell Physiol 52: 2062-2073
35. Hartmann T (2007) From waste products to ecochemicals: fifty years research of plant secondary metabolism. Phytochemistry 68: 2831-2846
36. Heilmann J (2010) New medical applications of plant secondary metabolites. In M Wink, ed, Functions and Biotechnology of Plant Secondary Metabolites, Annual Plant Reviews, Ed 2, Vol 39, Wiley-Blackwell, Oxford, pp 348-380
37. Huang L, Li J, Ye H, Li C, Wang H, Liu B, Zhang Y (2012) Molecular characterization of the pentacyclic triterpenoid biosynthetic pathway in Catharanthus roseus. Planta 236: 1571-1581
38. Iijima Y, Davidovich-Rikanati R, Fridman E, Gang DR, Bar E, Lewinsohn E, Pichersky E (2004a) The biochemical and molecular basis for the divergent patterns in the biosynthesis of terpenes and phenylpropenes in the peltate glands of three cultivars of basil. Plant Physiol 136: 3724-3736
39. Iijima Y, Gang DR, Fridman E, Lewinsohn E, Pichersky E (2004b) Characterization of geraniol synthase from the peltate glands of sweet basil. Plant Physiol 134: 370-379
40. Jasiňski M, Stukkens Y, Degand H, Purnelle B, Marchand-Brynaert J, Boutry M(2001) A plant plasma membrane ATP binding cassette-type transporter is involved in antifungal terpenoid secretion. Plant Cell 13: 1095-1107
41. Kim HJ, Chen F, Wang X, Rajapakse NC (2006) Effect of methyl jasmonate on secondary metabolites of sweet basil (Ocimum basilicum L.). J Agric Food Chem 54: 2327-2332
42. Kong L, Li S, Liao Q, Zhang Y, Sun R, Zhu X, Zhang Q, Wang J, Wu X, Fang X, et al (2013) Oleanolic acid and ursolic acid: novel hepatitis C virus antivirals that inhibit NS5B activity. Antiviral Res 98: 44-53
43. Kunkel SD, Suneja M, Ebert SM, Bongers KS, Fox DK, Malmberg SE, Alipour F, Shields RK, Adams CM (2011) mRNA expression signatures of human skeletal muscle atrophy identify a natural compound that increases muscle mass. Cell Metab 13: 627-638
44. Kurek A, Nadkowska P, Pliszka S, Wolska KI (2012) Modulation of antibiotic resistance in bacterial pathogens by oleanolic acid and ursolic acid. Phytomedicine 19: 515-519
45. Kushiro T, Shibuya M, Ebizuka Y (1998) Beta-amyrin synthase-cloning of oxidosqualene cyclase that catalyzes the formation of the most popular triterpene among higher plants. Eur J Biochem 256: 238-244
46. Kushiro T, Shibuya M, Masuda K, Ebizuka Y (2000) Mutational studies on triterpene synthases: engineering lupeol synthase into b-amyrin synthase. J Am Chem Soc 122: 6816-6824
47. Lange BM, Ahkami A (2013) Metabolic engineering of plant monoterpenes, sesquiterpenes and diterpenes-current status and future opportunities. Plant Biotechnol J 11: 169-196
48. Lee SJ, Umano K, Shibamoto T, Lee KG (2005) Identification of volatile components in basil (Ocimum basilicum L.) and thyme leaves (Thymus vulgaris L.) and their antioxidant properties. Food Chem 91: 131-137
49. Lenka SK, Boutaoui N, Paulose B, Vongpaseuth K, Normanly J, Roberts SC, Walker EL (2012) Identification and expression analysis of methyl jasmonate responsive ESTs in paclitaxel producing Taxus cuspidata suspension culture cells. BMC Genomics 13: 148
50. 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
51. Li Z, Wang X, Chen F, Kim HJ (2007) Chemical changes and overexpressed genes in sweet basil (Ocimum basilicum L.) upon methyl jasmonate treatment. J Agric Food Chem 55: 706-713
52. Louie GV, Baiga TJ, Bowman ME, Koeduka T, Taylor JH, Spassova SM, Pichersky E, Noel JP (2007) Structure and reaction mechanism of basil eugenol synthase. PLoS ONE 2: e993
53. Masoudi-Nejad A, Tonomura K, Kawashima S, Moriya Y, Suzuki M, Itoh M, Kanehisa M, Endo T, Goto S (2006) EGassembler: online bioinformatics service for large-scale processing, clustering and assembling ESTs and genomic DNA fragments. Nucleic Acids Res 34: W459-W462
54. Meera R, Devi P, Kameswari B, Madhumitha B, Merlin NJ (2009) Antioxidant and hepatoprotective activities of Ocimum basilicum Linn. and Trigonella foenum-graecum Linn. against H2O2 and CCL4 induced hepatotoxicity in goat liver. Indian J Exp Biol 47: 584-590
55. Meli VS, Ghosh S, Prabha TN, Chakraborty N, Chakraborty S, Datta A (2010) Enhancement of fruit shelf life by suppressing N-glycan processing enzymes. Proc Natl Acad Sci USA 107: 2413-2418
56. Mishra S, Triptahi V, Singh S, Phukan UJ, Gupta MM, Shanker K, Shukla RK (2013) Wound induced tanscriptional regulation of benzylisoquinoline pathway and characterization of wound inducible PsWRKY transcription factor from Papaver somniferum. PLoS ONE 8: e52784
57. Morita M, Shibuya M, Kushiro T, Masuda K, Ebizuka Y (2000) Molecular cloning and functional expression of triterpene synthases from pea (Pisum sativum) new alpha-amyrin-producing enzyme is a multifunctional triterpene synthase. Eur J Biochem 267: 3453-3460
58. Muralidharan A, Dhananjayan R (2004) Cardiac stimulant activity of Ocimum basilicum Linn. extracts. Indian J Pharmacol 36: 163-166
59. 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
60. Naoumkina MA, He X, Dixon RA (2008) Elicitor-induced transcription factors for metabolic reprogramming of secondary metabolism in Medicago truncatula. BMC Plant Biol 8: 132
61. Ohlrogge J, Benning C (2000) Unraveling plant metabolism by EST analysis. Curr Opin Plant Biol 3: 224-228
62. 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
63. Pauwels L, Inzé D, Goossens A (2009) Jasmonate-inducible gene: What does it mean? Trends Plant Sci 14: 87-91
64. Phillips DR, Rasbery JM, Bartel B, Matsuda SPT (2006) Biosynthetic diversity in plant triterpene cyclization. Curr Opin Plant Biol 9: 305-314
65. Pighin JA, Zheng H, Balakshin LJ, Goodman IP, Western TL, Jetter R, Kunst L, Samuels AL (2004) Plant cuticular lipid export requires an ABC transporter. Science 306: 702-704
66. Poralla K, Hewelt A, Prestwich GD, Abe I, Reipen I, Sprenger G (1994) A specific amino acid repeat in squalene and oxidosqualene cyclases. Trends Biochem Sci 19: 157-158
67. Rastogi S, Kumar R, Chanotiya CS, Shanker K, Gupta MM, Nagegowda DA, Shasany AK (2013) 4-coumarate: CoA ligase partitions metabolites for eugenol biosynthesis. Plant Cell Physiol 54: 1238-1252
68. Reichling J (2010) Plant-microbe interactions and secondary metabolites with antibacterial, antifungal and antiviral properties. In M Wink, ed, Functions and Biotechnology of Plant Secondary Metabolites, Annual Plant Reviews, Ed 2, Vol 39, Wiley-Blackwell, Oxford, pp 214-347
69. Reigosa MJ, Malvido-Pazos E (2007) Phytotoxic effects of 21 plant secondary metabolites on Arabidopsis thaliana germination and root growth. J Chem Ecol 33: 1456-1466
70. Saimaru H, Orihara Y, Tansakul P, Kang YH, Shibuya M, Ebizuka Y (2007) Production of triterpene acids by cell suspension cultures of Olea europaea. Chem Pharm Bull (Tokyo) 55: 784-788
71. Sasaki Y, Asamizu E, Shibata D, Nakamura Y, Kaneko T, Awai K, Amagai M, Kuwata C, Tsugane T, Masuda T, et al (2001) Monitoring of methyl jasmonate-responsive genes in Arabidopsis by cDNA macroarray: self-activation of jasmonic acid biosynthesis and crosstalk with other phytohormone signaling pathways. DNA Res 8: 153-161
72. Sawai S, Saito K (2011) Triterpenoid biosynthesis and engineering in plants. Front Plant Sci 2: 25
73. Siddiqui BS, Aslam H, Ali ST, Begum S, Khatoon N (2007) Two new triterpenoids and a steroidal glycoside from the aerial parts of Ocimum basilicum. Chem Pharm Bull (Tokyo) 55: 516-519
74. Silva MG, Vieira IG, Mendes FN, Albuquerque IL, dos Santos RN, Silva FO, Morais SM (2008) Variation of ursolic acid content in eight Ocimum species from northeastern Brazil. Molecules 13: 2482-2487
75. Strazzer P, Guzzo F, Levi M (2011) Correlated accumulation of anthocyanins and rosmarinic acid in mechanically stressed red cell suspensions of basil (Ocimum basilicum). J Plant Physiol 168: 288-293
76. Sun G, Yang Y, Xie F, Wen JF, Wu J, Wilson IW, Tang Q, Liu H, Qiu D (2013) Deep sequencing reveals transcriptome re-programming of Taxus 3 media cells to the elicitation with methyl jasmonate. PLoS ONE 8: e62865
77. Suzuki H, Reddy MS, Naoumkina M, Aziz N, May GD, Huhman DV, Sumner LW, Blount JW, Mendes P, Dixon RA (2005) Methyl jasmonate and yeast elicitor induce differential transcriptional and metabolic reprogramming in cell suspension cultures of the model legume Medicago truncatula. Planta 220: 696-707
78. 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: 2731-2739
79. Tholl D, Lee S (2011) Terpene specialized metabolism in Arabidopsis thaliana. The Arabidopsis Book 9: e0143, doi:10.1199/tab.0143
80. Verma RS, Padalia RC, Chauhan A (2012) Variation in the volatile terpenoids of two industrially important basil (Ocimum basilicum L.) cultivars during plant ontogeny in two different cropping seasons from India. J Sci Food Agric 92: 626-631
81. Wilkinson K, Boyd JD, Glicksman M, Moore KJ, El Khoury J (2011) A high content drug screen identifies ursolic acid as an inhibitor of amyloid beta protein interactions with its receptor CD36. J Biol Chem 286: 34914-34922
82. Wink M (2010a) Introduction. In M Wink, ed, Functions and Biotechnology of Plant Secondary Metabolites, Annual Plant Reviews, Ed 2, Vol 39, Wiley-Blackwell, Oxford, pp 1-20
83. Wink M (2010b) Introduction: biochemistry, physiology and ecological functions of secondary metabolites. In M Wink, ed, Biochemistry of Plant Secondary Metabolism, Annual Plant Reviews, Ed 2, Vol 40, Wiley-Blackwell, Oxford, pp 1-19
84. Wójciak-Kosior M (2007) Separation and determination of closely related triterpenic acids by high performance thin-layer chromatography after iodine derivatization. J Pharm Biomed Anal 45: 337-340
85. Yeats TH, Rose JK (2013) The formation and function of plant cuticles. Plant Physiol 163: 5-20
86. Yu F, Thamm AM, Reed D, Villa-Ruano N, Quesada AL, Gloria EL, Covello P, De Luca V (2013) Functional characterization of amyrin synthase involved in ursolic acid biosynthesis in Catharanthus roseus leaf epidermis. Phytochemistry 91: 122-127
87. Yu ZX, Li JX, Yang CQ, Hu WL, Wang LJ, Chen XY (2012) The jasmonateresponsive AP2/ERF transcription factors AaERF1 and AaERF2 positively regulate artemisinin biosynthesis in Artemisia annua L. Mol Plant 5: 353-365
88. Yun DJ, Hashimoto T, Yamada Y (1992) Metabolic engineering of medicinal plants: transgenic Atropa belladonna with an improved alkaloid composition. Proc Natl Acad Sci USA 89: 11799-11803
89. Zeggwagh NA, Sulpice T, Eddouks M (2007) Anti-hyperglycaemic and hypolipidemic effects of Ocimum basilicum aqueous extract in diabetic rats. Am J Pharmacol Toxicol 2: 123-129
90. Zhang JW, Li SK, Wu WJ (2009) The main chemical composition and in vitro antifungal activity of the essential oils of Ocimum basilicum Linn. var. pilosum (Willd.) Benth. Molecules 14: 273-278
91. Zhang L, Ding R, Chai Y, Bonfill M, Moyano E, Oksman-Caldentey KM, Xu T, Pi Y, Wang Z, Zhang H, et al (2004) Engineering tropane biosynthetic pathway in Hyoscyamus niger hairy root cultures. Proc Natl Acad Sci USA 101: 6786-6791
92. Zhao J, Davis LC, Verpoorte R (2005) Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnol Adv 23: 283-333