Abstract
Feverfew (Tanacetum parthenium) is a medicinal herb that has multiple pharmacologic properties. This plant is rich parthenolide (PN). Hairy roots (HRs) culture is a valuable biotechnological tool for the production of plant secondary metabolites. Furthermore, application of elicitors is one of the most effective strategies to induce the metabolite biosynthesis. This study has investigated the effects of various elicitors on the production of PN in feverfew hairy root culture and the expression of parthenolide synthase (TpPTS) gene. Three elicitors were used separately and in combination, including yeast extract (YE) (2.5 mgL− 1), methyl jasmonate (MJ) (100 µM), Ag+ (100 µM), YE + MJ, Ag+ + MJ, YE + Ag+, and YE + MJ + Ag+ which were added to the 1/2MS medium on day 18 and after 48 h and 96 h, hairy roots were collected to determine the PN content. Total RNA was extracted from hairy roots and used for cDNA synthesis and real-time PCR analysis to investigate the gene expression of TpPTS. The PN content was determined by HPLC. The highest PN content (0.05 mg g− 1 dry weight) was achieved after application of elicitors (in 2.5 mgL− 1 YE and 100 µM MJ) and the highest expression of TpPTS gene also occurred after 96 h in the same treatment. It was concluded that some of the combined elicitors could efficiently increase the parthenolide content of feverfew in vitro culture. The additive effect of elicitors might be due to the separate mechanisms of each substance that is acting in an independent pathway.
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Abbreviations
- PN:
-
Parthenolide
- YE:
-
Yeast extract
- MJ:
-
Methyl jasmonate
- HPLC:
-
High-performance liquid chromatography
- PTS :
-
Parthenolide synthase
- MVA:
-
Mevalonate
- MEP:
-
2-C-Methyl-d-erythritol 4-phosphate
- IPP:
-
Isopentenyl pyrophosphate
- DMAPP:
-
Dimethylallyl pyrophosphate
- FPP:
-
Farnesyl diphosphate
- FPS:
-
Farnesyl diphosphate synthase
- SA:
-
Salicylic acid
- RGE:
-
Relative gene expression
- LSD:
-
Least significant difference
- ANOVA:
-
Analysis of variance
References
Abraham F, Bhatt A, Keng CL, Indrayanto G, Sulaiman SF (2011) Effect of yeast extract and chitosan on shoot proliferation, morphology and antioxidant activity of Curcuma mangga in vitro plantlets. Afr J Biotechnol 10:7787–7795
Cai Z, Kastell A, Mewis I, Knorr D, Smetanska I (2012) Polysaccharide elicitors enhance anthocyanin and phenolic acid accumulation in cell suspension cultures of Vitis vinifera. Plant Cell Tissue Organ 108:401–409
Cheng Q, He Y, Li G, Liu Y, Gao W, Huang L (2013) Effects of combined elicitors on tanshinone metabolic profiling and SmCPS expression in Salvia miltiorrhiza hairy root cultures. Molecules 18:7473–7485
De Kraker J-W, Franssen MC, Joerink M, De Groot A, Bouwmeester HJ (2002) Biosynthesis of costunolide, dihydrocostunolide, and leucodin. Demonstration of cytochrome P450-catalyzed formation of the lactone ring present in sesquiterpene lactones of chicory. Plant Physiol 129:257–268
Gupta SK, Liu R-B, Liaw S-Y, Chan H-S, Tsay H-S (2011) Enhanced tanshinone production in hairy roots of ‘Salvia miltiorrhiza Bunge’under the influence of plant growth regulators in liquid culture. Bot Stud 52:435–443
Hadjiakhondi A, Ameri N, Khalighi-Sigaroodi F, Rustaiyan A (2003) A new Guaianolide from Tanacetum fruticulosum Ledeb. DARU J Pharm Sci 11:171–174
Hao X, Shi M, Cui L, Xu C, Zhang Y, Kai G (2015) Effects of methyl jasmonate and salicylic acid on tanshinone production and biosynthetic gene expression in transgenic Salvia miltiorrhiza hairy roots. Biotechnol Appl Biochem 62:24–31
Heptinstall S, Awang D, Dawson B, Kindack D, Knight D, May J (1992) Parthenolide content and bioactivity of feverfew (Tanacetum parthenium (L.) Schultz-Bip.). Estimation of commercial and authenticated feverfew products. J Pharm Pharmacol 44:391–395
Heywood VH, Humphries CJ (1977) Anthemideae systematic review. In: Heywood VH, Harborne JB, Turner BL (eds) The biology and chemistry of the Compositae. Academic Press, New York, pp 851–898
Jeong G-T, Park D-H, Ryu H-W, Hwang B, Woo J-C, Kim D, Kim S-W Production of antioxidant compounds by culture of Panax ginseng CA Meyer hairy roots. In: Twenty-Sixth Symposium on Biotechnology for Fuels and Chemicals (2005) Springer, pp 1147–1157
Kai G et al (2012) Molecular mechanism of elicitor-induced tanshinone accumulation in Salvia miltiorrhiza hairy root cultures. Acta Physiol Plant 34:1421–1433
Khalili M, Hasanloo T, Kazemi Tabar SK (2010) Ag {+} enhanced silymarin production in hairy root cultures of Silybum marianum (L.) Gaertn. Plant Omics 3:109
Kombrink E (2012) Chemical and genetic exploration of jasmonate biosynthesis and signaling paths. Planta 236:1351–1366
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2 −∆∆CT method. Methods 25:402–408
Majdi M et al (2011) Biosynthesis and localization of parthenolide in glandular trichomes of feverfew (Tanacetum parthenium L. Schulz Bip.). Phytochemistry 72:1739–1750
Malarz J, Stojakowska A, Kisiel 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
Matkowski A (2008) Plant in vitro culture for the production of antioxidants—a review. Biotechnol Adv 26:548–560
Montesano M, Brader G, Palva ET (2003) Pathogen derived elicitors: searching for receptors in plants. Mol Plant Pathol 4:73–79
Mousavi H, Nezhad NM, Fakheri B, Majdi M, Heidari F (2017) Effects of some nanoparticles on expression of germacrene A synthase (TpGAS) and parthenolide synthase (TpPTS) genes in Tanacetum parthenium L. under water deficit stress. Iran J Med Sci Aro Plants 33:314–324
Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497
Nieto-Trujillo A, Buendía-González L, García-Morales C, Román-Guerrero A, Cruz-Sosa F, Estrada-Zúñiga M (2017) Phenolic compounds and parthenolide production from in vitro cultures of Tanacetum parthenium. Revista Mexicana de Ingeniería Química 16:371–383
Oztekin S, Martinov M (2014) Medicinal and aromatic crops: harvesting, drying, and processing. CRC Press, Boca Raton
Pistelli L, Giovannini A, Ruffoni B, Bertoli A, Pistelli L (2010) Hairy root cultures for secondary metabolites production. In: Bio-farms for nutraceuticals. Springer, Boston, pp 167–184
Pitta–Alvarez SI, Spollansky TC, Giulietti AM (2000) The influence of different biotic and abiotic elicitors on the production and profile of tropane alkaloids in hairy root cultures of Brugmansia candida. Enzyme Microb Technol 26:252–258
Prakash G, Srivastava AK (2008) Statistical elicitor optimization studies for the enhancement of azadirachtin production in bioreactor Azadirachta indica cell cultivation. Biochem Eng J 40:218–226
Putalun W, Luealon W, De-Eknamkul W, Tanaka H, Shoyama Y (2007) Improvement of artemisinin production by chitosan in hairy root cultures of Artemisia annua L. Biotechnol Lett 29:1143–1146
Sharafi A, Sohi HH, Mousavi A, Azadi P, Dehsara B, Khalifani BH (2013) Increasing morphinan alkaloid production by over-expressing salutaridinol 7-o—acetyltransferase in Iranian poppy hairy roots. World J Microbiol Biotechnol 29:2125–2131
Shi M et al (2014) Increased accumulation of the cardio-cerebrovascular disease treatment drug tanshinone in Salvia miltiorrhiza hairy roots by the enzymes 3-hydroxy-3-methylglutaryl CoA reductase and 1-deoxy-d-xylulose 5-phosphate reductoisomerase. Funct Integr Genom 14:603–615
Spinsanti G, Panti C, Lazzeri E, Marsili L, Casini S, Frati F, Fossi CM (2006) Selection of reference genes for quantitative RT-PCR studies in striped dolphin (Stenella coeruleoalba) skin biopsies. BMC Mol Biol 7:32
Stojakowska A, Kisiel W (1997) Acetylenes in A grobacterium rhizogenes Transformed Root Culture of Tanacetum parthenium. Pol J Chem 71:509–512
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
Stojakowska A, Burczyk J, Kisiel W, Zych M, Banas A, Duda T (2008) Effects of various elicitors on the accumulation and secretion of spiroketal enol ether diacetylenes in feverfew hairy root culture. Acta Soc Bot Pol 77:17–21
Sykłowska-Baranek K et al (2019) Comparison of elicitor-based effects on metabolic responses of Taxus × media hairy roots in perfluorodecalin-supported two-phase culture system. Plant Cell Rep 38:85–99
Tripathi L, Tripathi JN (2003) Role of biotechnology in medicinal plants. Trop J Pharm Res 2:243–253
van Klink J, Becker H, Andersson S, Boland W (2003) Biosynthesis of anthecotuloide, an irregular sesquiterpene lactone from Anthemis cotula L. (Asteraceae) via a non-farnesyl diphosphate route. Org Biomol Chem 1:1503–1508
Won Y-K, Ong C-N, Shen H-M (2005) Parthenolide sensitizes ultraviolet (UV)-B-induced apoptosis via protein kinase C-dependent pathways. Carcinogenesis 26:2149–2156
Yan Q, Shi M, Ng J, Wu JY (2006) Elicitor-induced rosmarinic acid accumulation and secondary metabolism enzyme activities in Salvia miltiorrhiza hairy roots. Plant Sci 170:853–858
Yu Z-Z, Fu C-X, Han Y-S, Li Y-X, Zhao D-X (2006) Salicylic acid enhances jaceosidin and syringin production in cell cultures of Saussurea medusa. Biotechnol Lett 28:1027–1031
Zayed R, Wink M (2004) Induction of tropane alkaloid formation in transformed root cultures of Brugmansia suaveolens (Solanaceae). Z Naturforsch C 59:863–867
Zhang H, Memelink J (2009) Regulation of secondary metabolism by jasmonate hormones. In: Plant-derived Natural Products. Springer, New York, pp 181–194
Zhang L et al (2007) Tropane alkaloids production in transgenic Hyoscyamus niger hairy root cultures over-expressing putrescine N-methyltransferase is methyl jasmonate-dependent. Planta 225:887–896
Zhao J, Zhu W-H, Hu Q (2001) Enhanced catharanthine production in Catharanthus roseus cell cultures by combined elicitor treatment in shake flasks and bioreactors. Enzyme Microb Technol 28:673–681
Zhao J, Davis LC, Verpoorte R (2005) Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnol Adv 23:283–333
Zhao J-L, Zhou L-G, Wu J-Y (2010) Effects of biotic and abiotic elicitors on cell growth and tanshinone accumulation in Salvia miltiorrhiza cell cultures. Appl Microbiol Biotechnol 87:137–144
Zhao J-L, Zou L, Zhang C-Q, Li Y-Y, Peng L-X, Xiang D-B, Zhao G (2014) Efficient production of flavonoids in Fagopyrum tataricum hairy root cultures with yeast polysaccharide elicitation and medium renewal process. Pharmacogn Mag 10:234
Zhou J, Fang L, Wang X, Guo L, Huang L (2012) La dramaticaly enhances the accumulation of tanshinones in Salvia miltiorrhiza hairy root cultures. Earth Sci Res 2:187
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HR and AM conceived and designed the research. FP conducted experiments and wrote the manuscript. MK and SM results elaboration and discussion, critical reading of the manuscript. All authors read and approved the manuscript.
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Pourianezhad, F., Rahnama, H., Mousavi, A. et al. Effects of combined elicitors on parthenolide production and expression of parthenolide synthase (TpPTS) in Tanacetum parthenium hairy root culture. Plant Biotechnol Rep 13, 211–218 (2019). https://doi.org/10.1007/s11816-019-00526-3
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DOI: https://doi.org/10.1007/s11816-019-00526-3