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Effects of combined elicitors on parthenolide production and expression of parthenolide synthase (TpPTS) in Tanacetum parthenium hairy root culture

  • Farzaneh Pourianezhad
  • Hassan RahnamaEmail author
  • Amir MousaviEmail author
  • Mahmood Khosrowshahli
  • Sudabeh Mafakheri
Original Article
  • 28 Downloads

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.

Keywords

Elicitation Feverfew (Tanacetum partheniumHairy root Parthenolide PN synthase 

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

Notes

Author contributions

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.

Compliance with ethical standards

Conflict of interest

The authors declare no conflicts of interest.

References

  1. 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 10:7787–7795CrossRefGoogle Scholar
  2. 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 108:401–409CrossRefGoogle Scholar
  3. 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 18:7473–7485CrossRefGoogle Scholar
  4. 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 129:257–268CrossRefGoogle Scholar
  5. 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 52:435–443Google Scholar
  6. Hadjiakhondi A, Ameri N, Khalighi-Sigaroodi F, Rustaiyan A (2003) A new Guaianolide from Tanacetum fruticulosum Ledeb. DARU J Pharm Sci 11:171–174Google Scholar
  7. 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 62:24–31CrossRefGoogle Scholar
  8. 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 44:391–395CrossRefGoogle Scholar
  9. 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 851–898Google Scholar
  10. 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 1147–1157Google Scholar
  11. Kai G et al (2012) Molecular mechanism of elicitor-induced tanshinone accumulation in Salvia miltiorrhiza hairy root cultures. Acta Physiol Plant 34:1421–1433CrossRefGoogle Scholar
  12. Khalili M, Hasanloo T, Kazemi Tabar SK (2010) Ag {+} enhanced silymarin production in hairy root cultures of Silybum marianum (L.) Gaertn. Plant Omics 3:109Google Scholar
  13. Kombrink E (2012) Chemical and genetic exploration of jasmonate biosynthesis and signaling paths. Planta 236:1351–1366CrossRefGoogle Scholar
  14. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2 −∆∆CT method. Methods 25:402–408CrossRefGoogle Scholar
  15. Majdi M et al (2011) Biosynthesis and localization of parthenolide in glandular trichomes of feverfew (Tanacetum parthenium L. Schulz Bip.). Phytochemistry 72:1739–1750CrossRefGoogle Scholar
  16. 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 29:127–132CrossRefGoogle Scholar
  17. Matkowski A (2008) Plant in vitro culture for the production of antioxidants—a review. Biotechnol Adv 26:548–560CrossRefGoogle Scholar
  18. Montesano M, Brader G, Palva ET (2003) Pathogen derived elicitors: searching for receptors in plants. Mol Plant Pathol 4:73–79CrossRefGoogle Scholar
  19. 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 33:314–324Google Scholar
  20. Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497CrossRefGoogle Scholar
  21. 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 16:371–383Google Scholar
  22. Oztekin S, Martinov M (2014) Medicinal and aromatic crops: harvesting, drying, and processing. CRC Press, Boca RatonCrossRefGoogle Scholar
  23. 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 167–184CrossRefGoogle Scholar
  24. 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 26:252–258CrossRefGoogle Scholar
  25. Prakash G, Srivastava AK (2008) Statistical elicitor optimization studies for the enhancement of azadirachtin production in bioreactor Azadirachta indica cell cultivation. Biochem Eng J 40:218–226CrossRefGoogle Scholar
  26. 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 29:1143–1146CrossRefGoogle Scholar
  27. 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 29:2125–2131CrossRefGoogle Scholar
  28. 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 14:603–615CrossRefGoogle Scholar
  29. 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 7:32CrossRefGoogle Scholar
  30. Stojakowska A, Kisiel W (1997) Acetylenes in A grobacterium rhizogenes Transformed Root Culture of Tanacetum parthenium. Pol J Chem 71:509–512Google Scholar
  31. Stojakowska A, Malarz J, Kisiel W (2002) Salicylate and methyl jasmonate differentially influence diacetylene accumulation pattern in transformed roots of feverfew. Plant Sci 163:1147–1152CrossRefGoogle Scholar
  32. 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 77:17–21CrossRefGoogle Scholar
  33. 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 38:85–99CrossRefGoogle Scholar
  34. Tripathi L, Tripathi JN (2003) Role of biotechnology in medicinal plants. Trop J Pharm Res 2:243–253Google Scholar
  35. 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 1:1503–1508CrossRefGoogle Scholar
  36. Won Y-K, Ong C-N, Shen H-M (2005) Parthenolide sensitizes ultraviolet (UV)-B-induced apoptosis via protein kinase C-dependent pathways. Carcinogenesis 26:2149–2156CrossRefGoogle Scholar
  37. 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 170:853–858CrossRefGoogle Scholar
  38. 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 28:1027–1031CrossRefGoogle Scholar
  39. Zayed R, Wink M (2004) Induction of tropane alkaloid formation in transformed root cultures of Brugmansia suaveolens (Solanaceae). Z Naturforsch C 59:863–867CrossRefGoogle Scholar
  40. Zhang H, Memelink J (2009) Regulation of secondary metabolism by jasmonate hormones. In: Plant-derived Natural Products. Springer, New York, pp 181–194Google Scholar
  41. 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 225:887–896CrossRefGoogle Scholar
  42. 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 28:673–681CrossRefGoogle Scholar
  43. Zhao J, Davis LC, Verpoorte R (2005) Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnol Adv 23:283–333CrossRefGoogle Scholar
  44. 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 87:137–144CrossRefGoogle Scholar
  45. 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 10:234CrossRefGoogle Scholar
  46. 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 2:187CrossRefGoogle Scholar

Copyright information

© Korean Society for Plant Biotechnology 2019

Authors and Affiliations

  1. 1.Department of Horticultural Sciences, Science and Research BranchIslamic Azad UniversityTehranIran
  2. 2.Agricultural Biotechnology Research Institute of Iran (ABRII)Agricultural Research Education and Extension Organization (AREEO)KarajIran
  3. 3.Department of Plant Molecular BiotechnologyNational Institute of Genetic Engineering and Biotechnology (NIGEB)TehranIran
  4. 4.Department of Biotechnology, Science and Research BranchIslamic Azad UniversityTehranIran
  5. 5.Department of Technical and EngineeringImam Khomeini International UniversityQazvinIran

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