Time-dependent behavior of phenylpropanoid pathway in response to methyl jasmonate in Scrophularia striata cell cultures

  • Ehsan Sadeghnezhad
  • Mohsen SharifiEmail author
  • Hassan Zare-Maivan
  • Najmeh Ahmadian Chashmi
Original Article


Key message

MeJA triggers a time-dependent behavior of the phenylpropanoid compounds.


Plant cells produce a large number of metabolites in response to environmental factors. The cellular responses to environmental changes are orchestrated by signaling molecules, such as methyl jasmonate (MeJA). To understand how the MeJA changes the behavior of amino acids, carbohydrates, and phenylpropanoid compounds such as phenolic acids, phenylethanoid-glycosides, and flavonoids in Scrophularia striata cells; we monitored the metabolic responses for different times of exposure. In this study, we performed a time course analysis of metabolites and enzymes in S. striata cells exposed to MeJA (100 µM) and evaluated the metabolic flux towards carbon-rich secondary metabolites production. Moreover, we calculated the biosynthetic energy cost for free amino acids. Our results indicated that MeJA accelerates the sucrose degradation and directs the metabolic fluxes towards a pool of flavonoids and phenylethanoid glycosides through a change in enzyme behavior in the entry point and center of the phenylpropanoid pathway. MeJA also decreased and then raised the amino acid biosynthesis cost in S. striata cells in a time-dependent manner, indicating the cells evolve to utilize amino acids more economically by reducing cell growth. Finally, we classified the marked changes in the metabolites level and enzyme activities into three groups including early-, late-, and oscillatory-response groups to MeJA and summarized our findings as a model depicting pathway interactions during MeJA elicitation. Determination of metabolic levels in response to MeJA suggests that the changes in metabolic responses are time-dependent.


Energy cost Metabolic response Methyl jasmonate Phenylpropanoid Scrophularia striata 



Cytoplasmic or alkaline invertase


4-Coumarate: CoA ligase


Functional clusters


Methyl jasmonate


Phenylalanine ammonia-lyase


Principal component analysis


Phenylethanoid glycosides


Partial least squares discriminate analysis


Reactive oxygen species


Tyrosine ammonia lyase


Vacuolar or acidic invertase



This work was supported by Tarbiat Modares University.

Author contribution statement

ES, MS, and HZM designed the research and collected the experimental data. ES and NAC performed the biological and computational analysis. ES wrote the original manuscript and all co-authors edited the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

299_2019_2486_MOESM1_ESM.docx (4.8 mb)
Supplementary material 1 (DOCX 4910 kb)


  1. Ahmadi-Sakha S, Sharifi M, Niknam V (2016) Bioproduction of phenylethanoid glycosides by plant cell culture of Scrophularia striata Boiss.: from shake-flasks to bioreactor. Plant Cell Tissue Organ Cult 124(2):275–281CrossRefGoogle Scholar
  2. Ahmadi-Sakha S, Sharifi M, Niknam V, Ahmadian-Chashmi N (2018) Phenolic compounds profiling in shake flask and bioreactor system cell cultures of Scrophularia striata Boiss. In Vitro Cell Dev Biol Plant 54(4):444–453CrossRefGoogle Scholar
  3. Ali M, Abbasi BH, Ahmad N, Ali SS, Ali S, Ali GS (2016) Sucrose-enhanced biosynthesis of medicinally important antioxidant secondary metabolites in cell suspension cultures of Artemisia absinthium L. Bioprocess Biosyst Eng 39(12):1945–1954PubMedCrossRefGoogle Scholar
  4. Azadmehr A, Oghyanous KA, Hajiaghaee R, Amirghofran Z, Azadbakht M (2013) Antioxidant and neuroprotective effects of scrophularia striata extract against oxidative stress-induced neurotoxicity. Cell Mol Neurobiol 33(8):1135–1141PubMedCrossRefGoogle Scholar
  5. Barros J, Serrani-Yarce JC, Chen F, Baxter D, Venables BJ, Dixon RA (2016) Role of bifunctional ammonia-lyase in grass cell wall biosynthesis. Nat Plants 2(6):16050PubMedCrossRefGoogle Scholar
  6. Beshamgan ES, Sharifi M, Zarinkamar F (2019) Crosstalk among polyamines, phytohormones, hydrogen peroxide, and phenylethanoid glycosides responses in Scrophularia striata to Cd stress. Plant Physiol Biochem 143:129–141PubMedCrossRefGoogle Scholar
  7. Bhandari P, Kumar N, Singh B, Kaul VK (2008) Simultaneous determination of sugars and picrosides in Picrorhiza species using ultrasonic extraction and high-performance liquid chromatography with evaporative light scattering detection. J Chromatogr A 1194:257–261PubMedCrossRefGoogle Scholar
  8. Bharti N, Yadav D, Barnawal D, Maji D, Kalra A (2013) Exiguobacterium oxidotolerans a halotolerant plant growth promoting rhizobacteria, improves yield and content of secondary metabolites in Bacopa monnieri (L.) Pennell under primary and secondary salt stress. World J Microbiol Biotechnol 29:379–387PubMedCrossRefGoogle Scholar
  9. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254PubMedPubMedCentralCrossRefGoogle Scholar
  10. Cankar K, Jongedijk E, Klompmaker M, Majdic T, Mumm R, Bouwmeester H, Bosch D, Beekwilder J (2015) (+)-Valencene production in Nicotiana benthamiana is increased by down-regulation of competing pathways. Biotechnol J 10(1):180–189PubMedCrossRefGoogle Scholar
  11. Carlson RP (2007) Metabolic systems cost-benefit analysis for interpreting network structure and regulation. Bioinformatics 23(10):1258–1264PubMedCrossRefGoogle Scholar
  12. Chen JY, Wen PF, Kong WF, Pan QH, Wan SB, Huang WD (2006) Changes and subcellular localizations of the enzymes involved in phenylpropanoid metabolism during grape berry development. J Plant Physiol 163:115–127PubMedCrossRefGoogle Scholar
  13. Chen Y, Pang Q, Dai S, Wang Y, Chen S, Yan X (2011) Proteomic identification of differentially expressed proteins in Arabidopsis in response to methyl jasmonate. J Plant Physiol 168(10):995–1008PubMedCrossRefGoogle Scholar
  14. D’Onofrio C, Cox A, Davies C, Boss PK (2009) Induction of secondary metabolism in grape cell cultures by jasmonates. Funct Plant Biol 36(4):323–338CrossRefGoogle Scholar
  15. De Sutter V, Vanderhaeghen R, Tilleman S, Lammertyn F, Vanhoutte I, Karimi M, Inzé D, Goossens A, Hilson P (2005) Exploration of jasmonate signalling via automated and standardized transient expression assays in tobacco cells. Plant J 44(6):1065–1076PubMedCrossRefGoogle Scholar
  16. Falahi H, Sharifi M, Maivan HZ, Chashmi NA (2018) Phenylethanoid glycosides accumulation in roots of Scrophularia striata as a response to water stress. Environ Exp Bot 147:13–21CrossRefGoogle Scholar
  17. Gális I, Šimek P, Narisawa T, Sasaki M, Horiguchi T, Fukuda H, Matsuoka K (2006) A novel R2R3 MYB transcription factor NtMYBJS1 is a methyl jasmonate-dependent regulator of phenylpropanoid-conjugate biosynthesis in tobacco. Plant J 46(4):573–592PubMedCrossRefGoogle Scholar
  18. Gebauer RL, Strain BR, Reynolds JF (1997) The effect of elevated CO 2 and N availability on tissue concentrations and whole plant pools of carbon-based secondary compounds in loblolly pine (Pinus taeda). Oecologia 113(1):29–36PubMedCrossRefPubMedCentralGoogle Scholar
  19. Geiger M, Walch-Liu P, Engels C, Harnecker J, Schulze ED, Ludewig F, Sonnewald U, Scheible WR, Stitt M (1998) Enhanced carbon dioxide leads to a modified diurnal rhythm of nitrate reductase activity in older plants, and a large stimulation of nitrate reductase activity and higher levels of amino acids in young tobacco plants. Plant Cell Environ 21:253–268CrossRefGoogle Scholar
  20. Gigliotti E (2007) Discovering statistics using SPSS. J Adv Nurs 58:303–304CrossRefGoogle Scholar
  21. Goodspeed D, Chehab EW, Min-Venditti A, Braam J, Covington MF (2012) Arabidopsis synchronizes jasmonate-mediated defense with insect circadian behavior. Proc Natl Acad Sci USA 109:4674–4677PubMedCrossRefGoogle Scholar
  22. Guerra D, Anderson AJ, Salisbury FB (1985) Reduced phenylalanine ammonia-lyase and tyrosine ammonia-lyase activities and lignin synthesis in wheat grown under low pressure sodium lamps. Plant Physiol 78:126–130PubMedPubMedCentralCrossRefGoogle Scholar
  23. Guo Q, Major IT, Howe GA (2018) Resolution of growth–defense conflict: mechanistic insights from jasmonate signaling. Curr Opin Plant Biol 44:72–81PubMedCrossRefGoogle Scholar
  24. Hamilton JG, Zangerl AR, DeLucia EH, Berenbaum MR (2001) The carbon-nutrient balance hypothesis: its rise and fall. Ecol Lett 4:86–95CrossRefGoogle Scholar
  25. Hartmann T (2007) From waste products to ecochemicals: fifty years research of plant secondary metabolism. Phytochemistry 68(22–24):2831–2846PubMedCrossRefGoogle Scholar
  26. Havir EA, Reid PD, Marsh HV (1971) L-phenylalanine ammonia-lyase (maize): evidence for a common catalytic site for L-phenylalanine and L-tyrosine. Plant Physiol 48(2):130–136PubMedPubMedCentralCrossRefGoogle Scholar
  27. Hildebrandt TM, Nesi AN, Araújo WL, Braun HP (2015) Amino acid catabolism in plants. Mol Plant 8(11):1563–1579PubMedCrossRefGoogle Scholar
  28. Howe GA, Major IT, Koo AJ (2018) Modularity in jasmonate signaling for multistress resilience. Annu Rev Plant Biol 69:387–415PubMedCrossRefGoogle Scholar
  29. Hsieh LS, Ma GJ, Yang CC, Lee PD (2010) Cloning, expression, site-directed mutagenesis and immunolocalization of phenylalanine ammonia-lyase in Bambusa oldhamii. Phytochemistry 71(17–18):1999–2009PubMedCrossRefGoogle Scholar
  30. Huber SC (1989) Biochemical mechanism for regulation of sucrose accumulation in leaves during photosynthesis. Plant Physiol 91:656–662PubMedPubMedCentralCrossRefGoogle Scholar
  31. James JT, Tugizimana F, Steenkamp PA, Dubery IA (2013) Metabolomic analysis of methyl jasmonate-induced triterpenoid production in the medicinal herb Centella asiatica (L.) urban. Molecules 18(4):4267–4281PubMedPubMedCentralCrossRefGoogle Scholar
  32. Jangaard NO (1974) The characterization of phenylalanine ammonia-lyase from several plant species. Phytochemistry 13(9):1765–1768CrossRefGoogle Scholar
  33. Jia C, Shi H, Jin W, Zhang K, Jiang Y, Zhao M, Tu P (2008) Metabolism of echinacoside, a good antioxidant, in rats: isolation and identification of its biliary metabolites. Drug Metab Dispos 37:431–438PubMedCrossRefPubMedCentralGoogle Scholar
  34. Kamalipourazad M, Sharifi M, Maivan HZ, Behmanesh M, Chashmi NA (2016) Induction of aromatic amino acids and phenylpropanoid compounds in Scrophularia striata Boiss. cell culture in response to chitosan-induced oxidative stress. Plant Physiol Biochem 107:374–384PubMedCrossRefPubMedCentralGoogle Scholar
  35. Karuppusamy S (2009) A review on trends in production of secondary metabolites from higher plants by in vitro tissue, organ and cell cultures. J Med Plant Res 3:1222–1239Google Scholar
  36. Keinänen M, Oldham NJ, Baldwin IT (2001) Rapid HPLC screening of jasmonate-induced increases in tobacco alkaloids, phenolics, and diterpene glycosides in Nicotiana attenuata. J Agric Food Chem 49:3553–3558PubMedCrossRefPubMedCentralGoogle Scholar
  37. Khanpour-Ardestani N, Sharifi M, Behmanesh M (2015) Establishment of callus and cell suspension culture of Scrophularia striata Boiss.: an in vitro approach for acteoside production. Cytotechnology 67:475–485PubMedCrossRefPubMedCentralGoogle Scholar
  38. Kim SG, Yon F, Gaquerel E, Gulati J, Baldwin IT (2011) Tissue specific diurnal rhythms of metabolites and their regulation during herbivore attack in a native tobacco, Nicotiana attenuata. PloS One 6(10):e26214PubMedPubMedCentralCrossRefGoogle Scholar
  39. Kim SH, Kim YH, Ahn YO, Ahn MJ, Jeong JC, Lee HS, Kwak SS (2013) Downregulation of the lycopene ϵ-cyclase gene increases carotenoid synthesis via the β-branch-specific pathway and enhances salt-stress tolerance in sweetpotato transgenic calli. Physiol Plant 147(4):432–442PubMedCrossRefPubMedCentralGoogle Scholar
  40. Krzyzanowska J, Czubacka A, Pecio L, Przybys M, Doroszewska T, Stochmal A, Oleszek W (2012) The effects of jasmonic acid and methyl jasmonate on rosmarinic acid production in Mentha × piperita cell suspension cultures. Plant Cell Tissue Organ Cult 108(1):73–81CrossRefGoogle Scholar
  41. Lattanzio V, Cardinali A, Ruta C, Fortunato IM, Lattanzio VM, Linsalata V, Cicco N (2009) Relationship of secondary metabolism to growth in oregano (Origanum vulgare L.) shoot cultures under nutritional stress. Environ Exp Bot 65(1):54–62CrossRefGoogle Scholar
  42. Lavhale SG, Kalunke RM, Giri AP (2018) Structural, functional and evolutionary diversity of 4-coumarate-CoA ligase in plants. Planta 248(5):1063–1078PubMedCrossRefGoogle Scholar
  43. Lindermayr C, Möllers B, Fliegmann J, Uhlmann A, Lottspeich F, Meimberg H, Ebel J (2002) Divergent members of a soybean (Glycine max L.) 4-coumarate: co-enzyme A ligase gene family. Eur J Biochem 269:1304–1315PubMedCrossRefGoogle Scholar
  44. Liu Z, Zhang S, Sun N, Liu H, Zhao Y, Liang Y, Zhang L, Han Y (2015) Functional diversity of jasmonates in rice. Rice 8(1):5PubMedCentralCrossRefPubMedGoogle Scholar
  45. Liu X, Yan Y, Liu Y, Mo T, Wang X, Song Y, Chen Q, Zhao Y, Shi S, Tu P (2018) Cell culture establishment and regulation of two phenylethanoid glycosides accumulation in cell suspension culture of desert plant Cistanche tubulosa. Plant Cell Tissue Organ Cult 134(1):107–118CrossRefGoogle Scholar
  46. Lou Y, Baldwin IT (2004) Nitrogen supply influences herbivore-induced direct and indirect defenses and transcriptional responses in Nicotiana attenuata. Plant Physiol 135(1):496–506PubMedPubMedCentralCrossRefGoogle Scholar
  47. Louie GV, Bowman ME, Moffitt MC, Baiga TJ, Moore BS, Noel JP (2006) Structural determinants and modulation of substrate specificity in phenylalanine-tyrosine ammonia-lyases. Chem Biol 13(12):1327–1338PubMedPubMedCentralCrossRefGoogle Scholar
  48. Lv Z, Zhang F, Pan Q, Fu X, Jiang W, Shen Q, Yan T, Shi P, Lu X, Sun X, Tang K (2016) Branch pathway blocking in Artemisia annua is a useful method for obtaining high yield artemisinin. Plant Cell Physiol 57(3):588–602PubMedCrossRefGoogle Scholar
  49. Maitra S, Yan J (2008) Principle component analysis and partial least squares: two dimension reduction techniques for regression. Appl Multivar Stat Models 79:79–90Google Scholar
  50. McCready RM, Guggolz J, Owens HS (1950) Determination of starch and amylose in vegetables. Anal Chem 22:1156–1158CrossRefGoogle Scholar
  51. Meyer RC, Steinfath M, Lisec J, Becher M, Witucka-Wall H, Törjék O et al (2007) The metabolic signature related to high plant growth rate in Arabidopsis thaliana. Proc Natl Acad Sci USA 104:4759–4764PubMedCrossRefGoogle Scholar
  52. Miller GL (1972) Use of dinitrosalicylic acid reagent for determination of reducing sugars. Anal Chem 31:426–428CrossRefGoogle Scholar
  53. Monsef-Esfahani HR, Hajiaghaee R, Shahverdi AR, Khorramizadeh MR, Amini M (2010) Flavonoids, cinnamic acid and phenylpropanoid from aerial parts of Scrophularia striata. Pharm Biol 48:333–336PubMedCrossRefGoogle Scholar
  54. Muro-Villanueva F, Mao X, Chapple C (2019) Linking phenylpropanoid metabolism, lignin deposition, and plant growth inhibition. Curr Opin Biotechnol 56:202–208PubMedCrossRefGoogle Scholar
  55. Nakane E, Kawakita K, Doke N, Yoshioka H (2003) Elicitation of primary and secondary metabolism during defense in the potato. J Gen Plant Pathol 69:378–384CrossRefGoogle Scholar
  56. Naoumkina MA, Zhao Q, Gallego-Giraldo LINA, Dai X, Zhao PX, Dixon RA (2010) Genome-wide analysis of phenylpropanoid defence pathways. Mol Plant Pathol 11(6):829–846PubMedPubMedCentralGoogle Scholar
  57. Narayani M, Srivastava S (2017) Elicitation: a stimulation of stress in in vitro plant cell/tissue cultures for enhancement of secondary metabolite production. Phytochem Rev 16(6):1227–1252CrossRefGoogle Scholar
  58. Nartop P (2018) Engineering of biomass accumulation and secondary metabolite production in plant cell and tissue cultures. Plant metabolites and regulation under environmental stress. Academic Press, Cambridge, pp 169–194CrossRefGoogle Scholar
  59. Nejad ES, Askari H, Soltani S (2012) Regulatory TGACG-motif may elicit the secondary metabolite production through inhibition of active Cyclin-dependent kinase/Cyclin complex. Plant Omics 5(6):553Google Scholar
  60. Nunes-Nesi A, Fernie AR, Stitt M (2010) Metabolic and signaling aspects underpinning the regulation of plant carbon nitrogen interactions. Mol Plant 3(6):973–996PubMedCrossRefGoogle Scholar
  61. Patil RA, Lenka SK, Normanly J, Walker EL, Roberts SC (2014) Methyl jasmonate represses growth and affects cell cycle progression in cultured Taxus cells. Plant Cell Rep 33(9):1479–1492PubMedPubMedCentralCrossRefGoogle Scholar
  62. Peng C, Uygun S, Shiu SH, Robert L (2015) The impact of the branched-chain ketoacid dehydrogenase complex on amino acid homeostasis in Arabidopsis. Plant Physiol 169:1807–1820PubMedPubMedCentralGoogle Scholar
  63. Pourcel L, Routaboul JM, Cheynier V, Lepiniec L, Debeaujon I (2007) Flavonoid oxidation in plants: from biochemical properties to physiological functions. Trends Plant Sci 12:29–36PubMedCrossRefGoogle Scholar
  64. Ramirez-Estrada K, Vidal-Limon H, Hidalgo D, Moyano E, Golenioswki M, Cusidó RM, Palazon J (2016) Elicitation, an effective strategy for the biotechnological production of bioactive high-added value compounds in plant cell factories. Molecules 21:182PubMedPubMedCentralCrossRefGoogle Scholar
  65. Razal RA, Ellis S, Singh S, Lewis NG, Towers GHN (1996) Nitrogen recycling in phenylpropanoid metabolism. Phytochemistry 41:31–35CrossRefGoogle Scholar
  66. Rezaie-Tavirani M, Mortazavi SA, Barzegar M, Moghadamnia SH, Rezaee MB (2010) Study of anti cancer property of Scrophularia striata extract on the human astrocytoma cell line (1321). Iran J Pharm Res 9(4):403PubMedPubMedCentralGoogle Scholar
  67. Rischer H, Orešič M, Seppänen-Laakso T, Katajamaa M, Lammertyn F, Ardiles-Diaz W, Van Montagu MC, Inzé D, Oksman-Caldentey KM, Goossens A (2006) Gene-to-metabolite networks for terpenoid indole alkaloid biosynthesis in Catharanthus roseus cells. Proc Natl Acad Sci USA 103(14):5614–5619PubMedCrossRefGoogle Scholar
  68. Rosler J, Krekel F, Amrhein N, Schmid J (1997) Maize phenylalanine ammonia-lyase has tyrosine ammonia-lyase activity. Plant Physiol 113(1):175–179PubMedPubMedCentralCrossRefGoogle Scholar
  69. Sadeghnezhad E, Sharifi M, Zare-Maivan H (2016) Profiling of acidic (amino and phenolic acids) and phenylpropanoids production in response to methyl jasmonate-induced oxidative stress in Scrophularia striata suspension cells. Planta 244(1):75–85PubMedCrossRefGoogle Scholar
  70. Saimaru H, Orihara Y (2010) Biosynthesis of acteoside in cultured cells of Olea europaea. J Nat Med 64:139–145PubMedCrossRefPubMedCentralGoogle Scholar
  71. Santner A, Estelle M (2009) Recent advances and emerging trends in plant hormone signalling. Nature 459(7250):1071CrossRefGoogle Scholar
  72. Saw NMMT, Moser C, Martens S, Franceschi P (2017) Applying generalized additive models to unravel dynamic changes in anthocyanin biosynthesis in methyl jasmonate elicited grapevine (Vitis vinifera cv. Gamay) cell cultures. Hortic Res 4:17038PubMedPubMedCentralCrossRefGoogle Scholar
  73. Scheible WR, Lauerer M, Schulze ED, Caboche M, Stitt M (1997) Accumulation of nitrate in the shoot acts as a signal to regulate shoot-root allocation in tobacco. Plant J 11(4):671–691CrossRefGoogle Scholar
  74. Singh A, Dwivedi P (2018) Methyl-jasmonate and salicylic acid as potent elicitors for secondary metabolite production in medicinal plants: a review. J Pharmacogn Phytochem 7(1):750–757Google Scholar
  75. Stamp N (2003) Out of the quagmire of plant defense hypotheses. Q Rev Biol 78:23–55PubMedCrossRefPubMedCentralGoogle Scholar
  76. Sweetlove LJ, Ratcliffe RG (2011) Flux-balance modeling of plant metabolism. Front Plant Sci 2:38PubMedPubMedCentralCrossRefGoogle Scholar
  77. Tang GQ, Lüscher M, Sturm A (1999) Antisense repression of vacuolar and cell wall invertase in transgenic carrot alters early plant development and sucrose partitioning. Plant Cell 11:177–189PubMedPubMedCentralCrossRefGoogle Scholar
  78. Vogt T (2010) Phenylpropanoid biosynthesis. Mol Plant 3(1):2–20PubMedCrossRefPubMedCentralGoogle Scholar
  79. Wagner A (2005) Energy constraints on the evolution of gene expression. Mol Biol Evol 22:1365–1374PubMedCrossRefPubMedCentralGoogle Scholar
  80. Wang R, Xu S, Wang N, Xia B, Jiang Y, Wang R (2017) Transcriptome analysis of secondary metabolism pathway, transcription factors, and transporters in response to methyl jasmonate in Lycoris aurea. Front Plant Sci 7:1971PubMedPubMedCentralGoogle Scholar
  81. Wasternack C, Hause B (2013) Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in annals of botany. Ann Bot 111:1021–1058PubMedPubMedCentralCrossRefGoogle Scholar
  82. Watts KT, Mijts BN, Lee PC, Manning AJ, Schmidt-Dannert C (2006) Discovery of a substrate selectivity switch in tyrosine ammonia-lyase, a member of the aromatic amino acid lyase family. Chem Biol 13(12):1317–1326PubMedCrossRefPubMedCentralGoogle Scholar
  83. Xia J, Psychogios N, Young N, Wishart DS (2009) MetaboAnalyst: a web server for metabolomic data analysis and interpretation. Nucleic Acids Res 37:652–660CrossRefGoogle Scholar
  84. Zhang L, Chen J, Zhou X, Chen X, Li Q, Tan H, Dong X, Xiao Y, Chen L, Chen W (2016) Dynamic metabolic and transcriptomic profiling of methyl jasmonate-treated hairy roots reveals synthetic characters and regulators of lignan biosynthesis in Isatis indigotica Fort. Plant Biotechnol J 14(12):2217–2227PubMedPubMedCentralCrossRefGoogle Scholar
  85. Zhao JL, Zhou LG, Wu JY (2010) Effects of biotic and abiotic elicitors on cell growth and tanshinone accumulation in Salvia miltiorrhiza cell cultures. Appl Microbiol Biotechnol 87:137–144PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Ehsan Sadeghnezhad
    • 1
  • Mohsen Sharifi
    • 1
    Email author
  • Hassan Zare-Maivan
    • 1
  • Najmeh Ahmadian Chashmi
    • 2
  1. 1.Department of Plant Biology, Faculty of Biological SciencesTarbiat Modares UniversityTehranIran
  2. 2.Interfaculty Institute of BiochemistryTübingenGermany

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