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Parthenolide accumulation and expression of genes related to parthenolide biosynthesis affected by exogenous application of methyl jasmonate and salicylic acid in Tanacetum parthenium

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Abstract

Key message

Up-regulation of germacrene A synthase and down-regulation of parthenolide hydroxylase genes play key role in parthenolide accumulation of feverfew plants treated with methyl jasmonate and salicylic acid.

Abstract

Parthenolide is an important sesquiterpene lactone due to its anti-migraine and anti-cancer properties. Parthenolide amount was quantified by high-performance liquid chromatography after foliar application of methyl jasmonate (100 µM) or salicylic acid (1.0 mM) on feverfew leaves in time course experiment (3–96 h). Results indicate that exogenous application of methyl jasmonate or salicylic acid activated parthenolide biosynthesis. Parthenolide content reached its highest amount at 24 h after methyl jasmonate or salicylic acid treatments, which were 3.1- and 1.96-fold higher than control plants, respectively. Parthenolide transiently increased due to methyl jasmonate or salicylic acid treatments until 24 h, but did not show significant difference compared with control plants at 48 and 96 h time points in both treatments. Also, the transcript levels of early pathway (upstream) genes of terpene biosynthesis including 3-hydroxy-3-methylglutaryl-coenzyme A reductase, 1-deoxy-d-xylulose-5-phosphate reductoisomerase and hydroxy-2-methyl-2-(E)-butenyl 4-diphosphate reductase and the biosynthetic genes of parthenolide including germacrene A synthase, germacrene A oxidase, costunolide synthase and parthenolide synthase were increased by methyl jasmonate and salicylic acid treatments, but with different intensity. The transcriptional levels of these genes were higher in methyl jasmonate-treated plants than salicylic acid-treated plants. Parthenolide content measurements along with expression pattern analysis of the aforementioned genes and parthenolide hydroxylase as side branch gene of parthenolide suggest that the expression patterns of early pathway genes were not directly consistent with parthenolide accumulation pattern; hence, parthenolide accumulation is probably further modulated by the expression of its biosynthetic genes, especially germacrene A synthase and also its side branch gene, parthenolide hydroxylase.

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Abbreviations

MEP:

Methyl erythritol phosphate

MVA:

Mevalonic acid

IDP:

Isopentenyl diphosphate

DMADP:

Dimethylallyl diphosphate

FDP:

Farnesyl diphosphate

RGE:

Relative gene expression

HMGR :

3-Hydroxy-3-methylglutaryl-coenzyme A reductase

GAS :

Germacrene A synthase

DXR :

1-Deoxy-d-xylulose-5-phosphate reductoisomerase

HDR :

Hydroxy-2-methyl-2-(E)-butenyl 4-diphosphate reductase

GAO :

Germacrene A oxidase

COS :

Costunolide synthase

PTS :

Parthenolide synthase

PTH :

Parthenolide hydroxylase

MJ:

Methyl jasmonate

SA:

Salicylic acid

DW:

Dry weight

References

  • Aftab T, Mansoor M, Khan A, Idrees M, Naeem M, Moinuddin (2010) Salicylic acid acts as potent enhancer of growth, photosynthesis and artemisinin production in Artemisia annua L. J Crop Sci Biotech 13:183–188

    Article  Google Scholar 

  • Bouwmeester HJ, Gershenzon J, Konings MC, Croteau R (1998) Biosynthesis of the monoterpenes limonene and carvone in the fruit of caraway. I. Demonstration of enzyme activities and their changes with development. Plant Physiol 117:901–912

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bouwmeester HJ, Wallaart TE, Janssen MH, van Loo B, Jansen BJ, Posthumus MA, Schmidt CO, de Kraker JW, Konig WA, Franssen MC (1999) Amorpha-4, 11-diene synthase catalyses the first probable step in artemisinin biosynthesis. Phytochemistry 52:843–854

    Article  CAS  PubMed  Google Scholar 

  • Bulgakov VP, Tchernoded GK, Mischenko NP, Khodakovskaya MV, Glazunov VP, Radchenko SV, Zvereva EV, Fedoreyev SA, Zhuravlev YN (2002) Effect of salicylic acid, methyl jasmonate, ethephon and cantharidin on anthraquinone production by Rubia cordifolia callus cultures transformed with the rol B and rolC genes. J Biotechnol 97:213–221

    Article  CAS  PubMed  Google Scholar 

  • Chen H, Chen F (1999) Effects of methyl jasmonate and salicylic acid on cell growth and cryptotanshinone formation in Ti transformed Salvia miltiorrhiza cell suspension cultures. Biotechnol Lett 21:803–807

    Article  CAS  Google Scholar 

  • Cretnik L, Skerget M, Knez Z (2005) Separation of parthenolide from feverfew: performance of convectional and high pressure extraction techniques. Sep Purific Technol 41:13–20

    Article  CAS  Google Scholar 

  • de Kraker JW, Franssen MCR, de Groot A, Konig WA, Bouwmeester HJ (1998) (+)-Germacrene A biosynthesis—the committed step in the biosynthesis of bitter sesquiterpene lactones in chicory. Plant Physiol 117:1381–1392

    Article  PubMed Central  PubMed  Google Scholar 

  • Dudareva N, Andersson S, Orlova I, Gatto N, Reichelt M, Rhodes D, Boland W, Gershenzon J (2005) The nonmevalonate pathway supports both monoterpene and sesquiterpene formation in snapdragon flowers. Proc Natl Acad Sci USA 102:933–938

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Fang Y, Smith MAL, Pepin MF (1999) Effects of exogenous methyl jasmonate in elicited anthocyanin-producing cell cultures of ohelo (Vaccinium pahalae). In Vitro Cell Dev Biol Plant 35:106–113

    Article  CAS  Google Scholar 

  • Fonseca JM, Rushing JW, Rajapakse NC, Thomas RL, Riley MB (2005) Parthenolide and abscisic acid synthesis in feverfew are associated but environmental factors affect them dissimilarly. J Plant Physiol 162:485–494

    Article  CAS  PubMed  Google Scholar 

  • Fujita M, Fujita Y, NoutoshiY Takahashi F, Narusaka Y, Yamaguchi-Shinozaki K, Shinozaki K (2006) Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Curr Opin Plant Biol 9:436–442

    Article  PubMed  Google Scholar 

  • Gershenzon J (1994) Metabolic costs of terpenoid accumulation in higher plants. J Chem Ecol 20:1281–1328

    Article  CAS  PubMed  Google Scholar 

  • Goldstein JL, Brown MS (1990) Regulation of the mevalonate pathway. Nature 343:425–430

    Article  CAS  PubMed  Google Scholar 

  • Hsieh MH, Goodman HM (2005) The Arabidopsis IspH homolog is involved in the plastid nonmevalonate pathway of isoprenoid biosynthesis. Plant Physiol 138:641–653

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Huang JZ, Cheng TC, Wen PJ, Hsieh MH, Chen FC (2009) Molecular characterization of the Oncidium orchid HDR gene encoding 1-hydroxy-2-methyl-2-(E)-butenyl 4-diphosphate reductase, the last step of the methylerythritol phosphate pathway. Plant Cell Rep 28:1475–1486

    Article  CAS  PubMed  Google Scholar 

  • Ishihara A, Ogura Y, Tebayashi S, Iwamura H (2002) Jasmonate-induced changes in flavonoid metabolism in barley (Hordeum vulgare) leaves. Biosci Biotech Biochem 66:2176–2182

    Article  CAS  Google Scholar 

  • Kang SM, Min JY, Kim YD, Kang YM, Park DJ, Jung HN, Kim SW, Choi MS (2006) 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 42:44–49

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Li W, Koike K, Asada Y (2005) Rosmarinic acid production by Coleus forskohlii hairy root cultures. Plant Cell Tissue Organ Cult 80:151–155

    Article  CAS  Google Scholar 

  • Liu Q, Manzano D, Tanić N, Pesic M, Bankovic J, Pateraki I, Ricard L, Ferrer A, de Vos R, van de Krol S, Bouwmeester H (2014) Elucidation and in planta reconstitution of the parthenolide biosynthetic pathway. Metab Eng 23:145–153

    Article  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-Delta Delta C) method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Majdi M, Karimzadeh Gh, Malboobi MA, Omidbaigi R, Mirzaghaderi Gh (2010) Induction of tetraploidy to feverfew (Tanacetum parthenium Schulz. Bip): morphological, physiological, cytological and phytochemical changes. HortScience 45:16–21

    Google Scholar 

  • Majdi M, Liu Q, Karimzadeh G, Malboobi MA, Beekwilder J, Cankar K, de Vos R, Todorovic S, Simonovic A, Bouwmeester H (2011) Biosynthesis and localization of parthenolide in glandular trichomes of feverfew (Tanacetum parthenium L. Schulz Bip.). Phytochemistry 72:1739–1750

    Article  CAS  PubMed  Google Scholar 

  • Majdi M, Charnikhova T, Bouwmeester H (2013) Genetical, developmental and spatial factors influencing parthenolide and its precursor costunolide in feverfew (Tanacetum parthenium L. Schulz Bip.). Ind Crops Prod 47:270–276

    Article  CAS  Google Scholar 

  • Majdi M, Karimzadeh Gh, Malboobi MA (2014) Spatial and developmental expression of key genes of terpene biosynthesis in Tanacetum parthenium. Biol Plant 58:379–384

    Article  CAS  Google Scholar 

  • Malarz J, Stojakowska A, Kisie W (2007) Effect of methyl jasmonate and salicylic acid on sesquiterpene lactone accumulation in hairy roots of Cichorium intybus. Acta Physiol Plant 29:127–132

    Article  CAS  Google Scholar 

  • Mehmetoglu U, Curtis WR (1997) Effects of abiotic inducers on sesquiterpene synthesis in hairy root and cell-suspension cultures of Hyoscyamus muticus. Appl Biochem Biotechnol 67:71–77

    Article  CAS  Google Scholar 

  • Palevitch D, Earon G, Carasso R (1997) Feverfew (Tanacetum parthenium) as a prophylactic treatment for migraine: a double-blind placebo-controlled study. Photother Res 11:508–511

    Article  Google Scholar 

  • Pastirova A, Repcak M, Eliasova A (2004) Salicylic acid induces changes of coumarin metabolites in Matricaria chamomilla L. Plant Sci 167:819–824

    Article  CAS  Google Scholar 

  • Peng Z, Han C, Yuan L, Zhang K, Huang H, Ren C (2011) Brassinosteroid enhances jasmonate-induced anthocyanin accumulation in Arabidopsis seedlings. J Int Plant Biol 58:632–640

    Article  Google Scholar 

  • Perez AG, Sanz C, Olias R, Olias JM (1997) Effect of methyl jasmonate on in vitro strawberry ripening. J Agric Food Chem 45:3733–3737

    Article  CAS  Google Scholar 

  • Pichersky E, Raguso RA, Lewinsohn E, Croteau R (1994) Floral scent production in Clarkia (Onagraceae) (I. Localization and developmental modulation of monoterpene emission and linalool synthase activity). Plant Physiol 106:1533–1540

    PubMed Central  CAS  PubMed  Google Scholar 

  • Pu GB, Ma DM, Chen JL, Ma LQ, Wang H, Ye HC, Li GF, Liu BY (2009) Salicylic acid activates artemisinin biosynthesis in Artemisia annua L. Plant Cell Rep 28:1127–1135

    Article  CAS  PubMed  Google Scholar 

  • Rezaei A, Ghanati F, Behmanesh M (2011) Methyl jasmonate-induced biosynthesis of taxol and expression of certain related genes by Hazelnut (Corylus avellana L.) cells. Planta Med 77:PI14

  • Rohmer M, Knani M, Simonin P, Sutter B, Sahm H (1993) Isoprenoid biosynthesis in bacteria:a novel pathway for the early steps leading to isopentenyldiphosphate. Biochem J 295:517–524

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Saranitzky E, White CM, Baker LE, Baker LW, Coleman IC (2009) Feverfew for migraine prophylaxis: a systematic review. J Diet Suppl 6:91–103

    Article  PubMed  Google Scholar 

  • Singh G, Gavrielli J, Oakey JS, Curtis WR (1998) Interaction of methyl jasmonate, wounding, and fungal elicitation during sesquiterpene induction in Hyoscyamus muticus in root cultures. Plant Cell Rep 17:391–395

    Article  CAS  Google Scholar 

  • Stermer BA, Bostock RM (1987) Involvement of 3-hydroxy-3- methylglutaryl coenzyme-a reductase in the regulation of sesquiterpenoid phytoalexin synthesis in potato. Plant Physiol 84:404–408

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Stojakowska A, Malarz J, Kisiel W (2002) Salicylate and methyl jasmonate differentially influence diacetylene accumulation pattern in transformed roots of feverfew. Plant Sci 163:1147–1152

    Article  CAS  Google Scholar 

  • Takahashi S, Kuzuyama T, Watanabe H, Seto H (1998) A 1-deoxy-d-xylulose 5-phosphate reductoisomerase catalyzing the formation of 2-C-methyl-d-erythritol 4-phosphate in an alternative non-mevalonate pathway for terpenoid biosynthesis. Proc Natl Acad Sci USA 95:9879–9884

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • van der Fits L, Memelink J (2000) ORCA3, a jasmonate responsive transcriptional regulator of plant primary and secondary metabolism. Science 289:295–297

    Article  PubMed  Google Scholar 

  • Wang YD, Yuan YJ, Wu JC (2004) Induction studies of methyl jasmonate and salicylic acid on taxane production in suspension cultures of Taxus chinensis var. mairei. Biochem Eng J 19:259–265

    Article  Google Scholar 

  • Wang H, Ma C, Li Z, Ma L, Wang H, Ye H, Xu G, Liu B (2010) Effects of exogenous methyl jasmonate on artemisinin biosynthesis and secondary metabolites in Artemisia annua L. Ind Crops Prod 31:214–218

    Article  Google Scholar 

  • Watson C, Miller DA, Chin-Sinex H, Losch A, Hughes W, Sweeney C, Mendonca MS (2009) Suppression of nf-κb activity by parthenolide induces x-ray sensitivity through inhibition of split-dose repair in tp53 null prostate cancer cells. Radiat Res 171:389–396

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This research was financially supported by the University of Kurdistan, Sanandaj, Iran.

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Correspondence to Mohammad Majdi.

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The authors have declared that no competing interests exist.

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Communicated by M. Petersen.

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Majdi, M., Abdollahi, M.R. & Maroufi, A. Parthenolide accumulation and expression of genes related to parthenolide biosynthesis affected by exogenous application of methyl jasmonate and salicylic acid in Tanacetum parthenium . Plant Cell Rep 34, 1909–1918 (2015). https://doi.org/10.1007/s00299-015-1837-2

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