Production of Iridoid and Phenylethanoid Glycosides by In Vitro Systems of Plants from the Buddlejaceae, Orobanchaceae, and Scrophulariaceae Families

  • Ewelina PiątczakEmail author
  • Renata Grąbkowska
  • Halina Wysokińska
Reference work entry
Part of the Reference Series in Phytochemistry book series (RSP)


The plants belonging to Buddlejaceae, Orobanchaceae, and Scrophulariaceae families are rich sources of iridoid and phenylethanoid glycosides, which are widely used as anti-inflammatory, hypoglycemic, and nourishing agents. Recent years have seen the application of various in vitro culture systems as alternative source of these metabolites. We discuss the use of callus, cell suspension cultures, shoot cultures, and the whole regenerated plants as possible approaches for production of the compounds. Additionally, methods of efficiently improving metabolite accumulation in in vitro cultures through elicitation, precursor feeding, and both Agrobacterium rhizogenes- and A. tumefaciens-mediated genetic transformations (hairy roots, transformed plants) among the plant families are also presented.


Buddlejaceae Bioreactor Callus Cell suspension culture Elicitation Hairy roots Iridoid glycosides Orobanchaceae Phenylethanoid glycosides (PeGs) Scrophulariaceae 


  1. 1.
    Tietze LF (1983) Secologanin, a biogenetic key compound- synthesis and biogenesis of the iridoid and secoiridoid glycosides. Angew Chem 22:828–841CrossRefGoogle Scholar
  2. 2.
    Ghisalberti EL (1998) Biological and pharmacological activity of naturally occurring iridoids and secoiridoids. Phytomedicine 5:147–163PubMedCrossRefGoogle Scholar
  3. 3.
    Jensen RS (1991) Plant iridoids, their biosynthesis and distribution in angiosperms. In: Harborne JB, Tomas-Barberan FA (eds) Ecological chemistry and biochemistry of plant terpenoids, Proceedings of the Phytochemical Society of Europe. Clarendon, OxfordGoogle Scholar
  4. 4.
    Dewick PM (1997) The biosynthesis of C5–C25 terpenoid compounds. Nat Prod Rep 14:11–144CrossRefGoogle Scholar
  5. 5.
    Dinda B, Debnath S, Harigaya Y (2007) Naturally occurring secoiridoids and bioactivity of naturally occurring iridoids and secoiridoids. A review, part 2. Chem Pharm Bull 55:689–728PubMedCrossRefGoogle Scholar
  6. 6.
    Chang IM (1998) Liver protective activities of aucubin derived from 323 traditional oriental medicine. Res Commun Mol Pathol Pharmacol 102:189–204PubMedGoogle Scholar
  7. 7.
    Hung JY, Yang CJ, Tsai YM, Huang HW, Huang MS (2008) Antiproliferative activity of aucubin is through cell cycle arrest and apoptosis in human non-small cell lung cancer A549 cells. Clin Exp Pharmacol Physiol 35:995–1001PubMedCrossRefGoogle Scholar
  8. 8.
    Háznagy-Radnai E, Réthy B, Czigle Sz, Zupkó I, Wéber E, Martinek T, Falkay Gy, Máthé I (2008) Cytotoxic activities of Stachys species. Fitoterapia 79:595–597PubMedCrossRefGoogle Scholar
  9. 9.
    Zhu HF, Wan D, Luo Y, Zhou JL, Chen L, Xu XY (2010) Catalpol increases brain angiogenesis and up-regulates VEGF and EPO in the rat after permanent middle cerebral artery occlusion. Int J Biol Sci 6:443–453PubMedPubMedCentralCrossRefGoogle Scholar
  10. 10.
    Li DQ, Bao YM, Li Y, Wang CF, Liu Y, An LJ (2006) Catalpol modulates the expressions of Bcl-2 and Bax and attenuates apoptosis in gerbils after ischemic injury. Brain Res 1115:179–185PubMedCrossRefGoogle Scholar
  11. 11.
    Liu GC, Du HQ, Liang L (1992) Determination of catalpol in Rehmannia glutinosa Libosch. by HPLC. Chin Tradit Herb Drug 23:71–73Google Scholar
  12. 12.
    Zhang RX, Li MX, Jia ZP (2008) Rehmannia glutinosa: review of botany, chemistry and pharmacology. J Ethnopharmacol 117:199–214PubMedCrossRefGoogle Scholar
  13. 13.
    Kupeli E, Harput US, Varel M, Yesilada E, Saracoglu I (2005) Bioassay-guided isolation of iridoid glucosides with antinociceptive and anti-inflammatory activities from Veronica anagallis-aquatica L. J Ethnopharmacol 102:170–176PubMedCrossRefGoogle Scholar
  14. 14.
    Oh H, Pae HO, Oh GS, Lee SY, Chai KY, Song CE, Kwon TO, Chung HT, Lee HS (2002) Inhibition of inducible nitric oxide synthesis by catalposide from Catalpa ovata. Planta Med 68:685–689PubMedCrossRefGoogle Scholar
  15. 15.
    An SJ, Pae HO, Oh GS, Choi BM, Jeong S, Jang SI, Oh H, Kwon TO, Song CE, Chung HT (2002) Inhibition of TNF-α, IL-1β and IL-6 productions and NF-кB activation in lipopolysaccharide-activated RAW 264.7 macrophages by catalposide, an iridoid glycoside isolated from Catalpa ovata G. Don. Int Immunopharmacol 2:1173–1181Google Scholar
  16. 16.
    Loew D, Mollerfeld J, Schrodter A, Puttkammer S (2001) Investigations on the pharmacokinetic properties in humans of Harpagophytum extracts and their effects on eicosanoid biosynthesis in vitro and ex vivo. Clin Pharmacol Ther 69:356–364PubMedCrossRefGoogle Scholar
  17. 17.
    Georgiev MI, Ivanovska N, Alipieva K, Dimitrova P, Verpoorte R (2013) Harpagoside: from Kalahari Desert to pharmacy shelf. Phytochemistry 92:8–15PubMedCrossRefGoogle Scholar
  18. 18.
    Bermejo P, Abad MJ, Diaz AM, Fernandez L, Santos JD, Sanchez S, Villaescusa L, Carrasco L, Irurzun A (2002) Antiviral activity of seven iridoids, three saikosaponins and one phenylpropanoid glycoside extracted from Bupleurum rigidum and Scrophularia scorodonia. Planta Med 68:106–110PubMedCrossRefGoogle Scholar
  19. 19.
    Tasdemir D, Brun R, Franzblan SG, Sezgin Y, Calis I (2008) Evaluation of antiprotozoal and antimycobacterial activities of the resin glycosides and the other metabolites of Scrophularia cryptophila. Phytomedicine 15:209–215PubMedCrossRefGoogle Scholar
  20. 20.
    Kim SR, Lee KY, Koo KA, Sung SH, Lee N-G, Kim J, Kim YC (2002) Four new neuroprotective iridoid glycosides from Scrophularia buergeriana roots. J Nat Prod 65:1696–1699PubMedCrossRefGoogle Scholar
  21. 21.
    Kawada T, Asano R, Makino K, Sakuno T (2002) Synthesis of isoacteoside, a dihydroxyphenylethyl glycoside. J Wood Sci 48:512–515CrossRefGoogle Scholar
  22. 22.
    Dembitsky VM (2005) Astonishing diversity of natural surfactants: 5. Biologically active glycosides of aromatic metabolites. Lipids 40:869–900PubMedCrossRefGoogle Scholar
  23. 23.
    Jiménez C, Riguera R (1994) Phenylethanoid glycosides in plants: structure and biological activity. Nat Prod Rep 11:591–606PubMedCrossRefGoogle Scholar
  24. 24.
    He J, Hu X-P, Zeng Y, Li Y, Wu H-Q, Qiu R-Z, Ma W-J, Li T, Li C-Y, He Z-D (2011) Advanced research on acteoside for chemistry and bioactivities. J Asian Nat Prod Res 13:449–464PubMedCrossRefGoogle Scholar
  25. 25.
    Alipieva K, Korkina L, Orhan IE, Georgiev MI (2014) Verbascoside – a review of its occurrence, (bio)synthesis and pharmacological significance. Biotechnol Adv 32:1065–1076PubMedCrossRefGoogle Scholar
  26. 26.
    Cardinali A, Linsalata V, Lattanzio V, Ferruzzi MG (2011) Verbascoside from olive mill waste water: assessment of their bioaccessibility and intestinal uptake using an in vitro digestion/Caco-2 model system. J Food Sci 76:H48–H54PubMedCrossRefGoogle Scholar
  27. 27.
    Funari CS, Gullo FP, Napolitano A, Carneiro RL, Mendes-Giannini MJS, Fusco-Almeida AM, Piacente S, Pizza C, Silva DHS (2012) Chemical and antifungal investigations of six Lippia species (Verbenaceae) from Brazil. Food Chem 135:2086–2094PubMedCrossRefGoogle Scholar
  28. 28.
    Gyurkowska V, Alipieva K, Maciuk A, Dimitrova P, Iwanovska N, Haas C, Bley T, Georgiev M (2011) Anti-inflammatory activity of Devil’s claw in vitro systems and their active constituents. Food Chem 125:171–178CrossRefGoogle Scholar
  29. 29.
    López-Laredo A, Gómez-Aguirre Y, Medina-Pérez V, Salcedo-Morales G, Sepúlveda- Jiménez G, Trejo-Tapia G (2012) Variation in antioxidant properties and phenolics concentration in different organs of wild growing and greenhouse cultivated Castilleja tenuiflora Benth. Acta Physiol Plant 34:2435–2442CrossRefGoogle Scholar
  30. 30.
    Pettit GR, Numata A, Takemura T, Ode RH, Narula AS, Schmidt JM, Cragg GM, Pase CP (1990) Antineoplastic agents, 107. Isolation of acteoside and isoacteoside from Castilleja linariaefolia. J Nat Prod 53:456–458PubMedCrossRefGoogle Scholar
  31. 31.
    Singh N, Shukla N, Singh P, Sharma R, Rajendran SM, Maurya R, Palit G (2010) Verbascoside isolated from Tectona grandis mediates gastric protection in rats via inhibiting proton pump activity. Fitoterapia 81:755–761PubMedCrossRefGoogle Scholar
  32. 32.
    Georgiev M, Alipieva K, Orhan I, Abrashev R, Denev P, Angelova M (2011) Antioxidant and cholinesterases inhibitory activities of Verbascum xanthopoeniceum Griseb. and its phenylethanoid glycosides. Food Chem 128:100–105PubMedCrossRefGoogle Scholar
  33. 33.
    Xiong Q, Hase K, Tezuka Y, Tani T, Namba T, Kadota S (1998) Hepatoprotective activity of phenylethanoids from Cistanche deserticola. Planta Med 64:120–125PubMedCrossRefGoogle Scholar
  34. 34.
    Díaz AM, Abad MJ, Fernández L, Silván AM, Santos JS, Bermejo P (2004) Phenylpropanoid glycosides from Scrophularia scorodonia: in vitro anti-inflammatory activity. Life Sci 74:2515–2526PubMedCrossRefGoogle Scholar
  35. 35.
    Shikanga EA, Combrinck S, Regnier T (2010) South African Lippia herbal infusions: total phenolic content, antioxidant and antibacterial activities. S Afr J Bot 76:567–571CrossRefGoogle Scholar
  36. 36.
    Korkina LG, Mikhalchik E, Suprun M, Pastore S, Dal Toso R (2007) Molecular mechanisms underlying wound healing and anti-inflammatory properties of naturally occurring biotechnologically produced phenylpropanoid glycosides. Cell Mol Biol 53:78–83Google Scholar
  37. 37.
    Chen RC, Su JH, Yang SM, Li J, Wang TJ, Zhou H (2002) Effect of isoverbascoside, a phenylpropanoid glycoside antioxidant, on proliferation and differentiation of human gastric cancer cell. Acta Pharmacol Sin 23:997–1001PubMedGoogle Scholar
  38. 38.
    Cheminat A, Zawatsky R, Becker H, Brouillard R (1988) Caffeoyl conjugates from Echinacea species: structure and biological activity. Phytochemistry 27:2787–2794CrossRefGoogle Scholar
  39. 39.
    Pennacchio M, Alexander E, Syah YM, Ghisalberti EL (1996) The effect of verbascoside on cyclic 3′, 5′-adenosine monophosphate levels in isolated rat heart. Eur J Pharmacol 305:169–171PubMedCrossRefGoogle Scholar
  40. 40.
    Tu PF, Wang B, Deyama T, Zhang ZG, Lou ZC (1997) Analysis of phenylethanoid glycoside of Herba Cistanchis by RP-HPLC. Acta Pharmacol Sin 32:294–300Google Scholar
  41. 41.
    Deng M, Zhao JY, Tu PF, Jiang Y, Li ZB, Wang YH (2004) Echinacoside rescues the SHSY5Y neuronal cells from TNFalpha-induced apoptosis. Eur J Pharmacol 505:11–18PubMedCrossRefGoogle Scholar
  42. 42.
    Morikawa T, Ninomiya K, Imamura M, Akaki J, Fujikura S, Pan Y, Yuan D, Yoshikawa M, Jia X, Li Z, Muraoka O (2014) Acylated phenylethanoid glycosides, echinacoside and acteoside from Cistanche tubulosa, improve glucose tolerance in mice. J Nat Med 68:561–566PubMedCrossRefGoogle Scholar
  43. 43.
    Chen X, Liu J, Gu X, Ding F (2008) Salidroside attenuates glutamate-induced apoptotic cell death in primary cultured hippocampal neurons of rats. Brain Res 1238:189–198PubMedCrossRefGoogle Scholar
  44. 44.
    Chen X, Zhang Q, Cheng Q, Ding F (2009) Protective effect of salidroside against H2O2-induced cell apoptosis in primary culture of rat hippocampal neurons. Mol Cell Biochem 332:85–93PubMedCrossRefGoogle Scholar
  45. 45.
    Wang S, He H, Chen L, Zhang W, Zhang X, Chen J (2015) Protective effects of salidroside in the MPTP/MPP+-induced model of Parkinson’s disease through ROS-NO-related mitochondrion pathway. Mol Neurobiol 51:718–728PubMedCrossRefGoogle Scholar
  46. 46.
    Tao K, Wang B, Feng D, Zhang W, Lu F, Lai J, Huang L, Nie T, Yang Q (2016) Salidroside protects against 6-hydroxydopamine-induced cytotoxicity by attenuating ER stress. Neurosci Bull 32:61–69PubMedPubMedCentralCrossRefGoogle Scholar
  47. 47.
    Tang H, Gao L, Mao J, He H, Liu J, Cai X, Lin H, Wu T (2016) Salidroside protects against bleomycin-induced pulmonary fibrosis: activation of Nrf2-antioxidant signaling, and inhibition of NF-κB and TGF-β1/Smad-2/-3 pathways. Cell Stress Chaperones 21:239–249PubMedCrossRefGoogle Scholar
  48. 48.
    Zheng K, Sheng Z, Li Y, Lu H (2014) Salidroside inhibits oxygen glucose deprivation (OGD)/re-oxygenation-induced H9c2 cell necrosis through activating of Akt-Nrf2 signaling. Biochem Biophys Res Commun 451:79–85PubMedCrossRefGoogle Scholar
  49. 49.
    Guan S, Xiong Y, Song B, Song Y, Wang D, Chu X, Chen N, Huo M, Deng X, Lu J (2012) Protective effects of salidroside from Rhodiola rosea on LPS-induced acute lung injury in mice. Immunopharmacol Immunotoxicol 34:667–672PubMedCrossRefGoogle Scholar
  50. 50.
    Zhang Z, Ding L, Wu L, Xu L, Zheng L, Huang X (2014) Salidroside alleviates paraquat-induced rat acute lung injury by repressing TGF-beta1 expression. Int J Clin Exp Pathol 7:8841–8847PubMedPubMedCentralGoogle Scholar
  51. 51.
    Inagaki N, Nishimura H, Okada M, Mitsuhashi H (1991) Verbascoside production by plant cell cultures. Plant Cell Rep 9:484–487PubMedCrossRefGoogle Scholar
  52. 52.
    Ouyang J, Wang X-D, Zhao B, Wang Y-Ch (2005) Enhanced production of phenylethanoid glycosides by precursor feeding to cell culture of Cistanche deserticola. Process Biochem 40:3480–3484CrossRefGoogle Scholar
  53. 53.
    Song Y-X, Guo S-H, Zhang L-Y, Li M, Ma H-A, Niu D-L, Zheng G-G, Wang Y-H (2006) Callus culture of Cistanche deserticola and its acteoside content. Chin Tradit Herb Drug 8:1237–1241Google Scholar
  54. 54.
    Estrada-Zúñiga ME, Cruz-Sosa F, Rodríguez-Monroy M, Verde-Calvo JR, Vernon- Carter EJ (2009) Phenylpropanoid production in callus and cell suspension cultures of Buddleja cordata Kunth. Plant Cell Tiss Org Cult 97:39–47CrossRefGoogle Scholar
  55. 55.
    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 67:475–485PubMedCrossRefGoogle Scholar
  56. 56.
    Piątczak E, Kuźma Ł, Sitarek P, Wysokińska H (2015) Shoot organogenesis, molecular analysis and secondary metabolite production of micropropagated Rehmannia glutinosa Libosch. Plant Cell Tiss Org Cult 120:539–549CrossRefGoogle Scholar
  57. 57.
    Gamborg OL, Miller RA, Ojima K (1968) Nutrient requirements of suspension cultures of soybean root cells. Exp Cell Res 50:1551–1558CrossRefGoogle Scholar
  58. 58.
    Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiol Plant 15:473–497CrossRefGoogle Scholar
  59. 59.
    Farsi M, Zolali J (2011) Principles of plant biotechnology. Ferdowsi University of Mashhad Press, MashhadGoogle Scholar
  60. 60.
    Monsef-Esfahani H, Hajiaghaee R, Shahverdi AR, Khorramizadeh MR, Amini M (2010) Flavonoids, cinnamic acid and phenyl propanoid from aerial parts of Scrophularia striata. Pharm Biol 48:333–336PubMedCrossRefGoogle Scholar
  61. 61.
    Bahrami AM, Valadi A (2010) Effect of Scrophularia striata ethanolic leaves extracts on staphylococcus aureus. Int J Pharmacol 6:393–396CrossRefGoogle Scholar
  62. 62.
    Martínez M (1989) Las plantas medicinales de México. Ediciones Botas, México (in Spanish)Google Scholar
  63. 63.
    Li J, Li Ch, Shen H-H, Yi L-J, Liu H-Y (2006) Effects of sucrose on the growth suspension of Cistanche deserticola cells and synthesis of phenylethanoid glycosides. J Shihezi Univ (Nat Sci) 1:30–33Google Scholar
  64. 64.
    Piątczak E, Talar A, Kuźma Ł, Wysokińska H (2015) Iridoid and phenylethanoid glycoside production in multiple shoots and regenerated Rehmannia elata N. E. Brown ex Prain plants following micropropagation. Acta Physiol Plant 37:255–262CrossRefGoogle Scholar
  65. 65.
    Sagare AP, Kuo Ch-L, Chueh F-S, Tsay H-S (2001) De novo regeneration of Scrophularia yoshimurae Yamazaki (Scrophulariaceae) and quantitative analysis of harpagoside, an iridoid glycoside, formed in aerial and underground parts of in vitro propagated and wild plants by HPLC. Biol Pharm Bull 24:1311–1315CrossRefGoogle Scholar
  66. 66.
    Sesterhenn K, Distl M, Wink M (2007) Occurrence of iridoid glycosides in in vitro cultures and intact plants of Scrophularia nodosa L. Plant Cell Rep 26:365–371PubMedCrossRefGoogle Scholar
  67. 67.
    Sivanesan I, Lim MY, Jeong BR (2012) Micropropagation and greenhouse cultivation of Scrophularia takesimensis Nakai, a rare endemic medicinal plant. Pak J Bot 44:1657–1662Google Scholar
  68. 68.
    Martínez-Bonfil B, Salcedo-Morales G, López-Laredo AR, Ventura-Zapata E, Evangelista-Lozano S, Trejo-Tapia G (2011) Shoot regeneration and determination of iridoid levels in the medicinal plant Castilleja tenuiflora Benth. Plant Cell Tiss Org Cult 107:195–203CrossRefGoogle Scholar
  69. 69.
    Tank DC, Olmstead RG (2008) From annuals to perennials: phylogeny of subtribe Castillejinae (Orobanchaceae). Am J Bot 95:608–625PubMedCrossRefGoogle Scholar
  70. 70.
    Stevenson PC, Simmonds MSJ, Sampson J, Houghton PJ, Grice P (2002) Wound healing activity of acylated iridoid glycosides from Scrophularia nodosa. Phytother Res 16:33–35PubMedCrossRefGoogle Scholar
  71. 71.
    Tomilov AA, Tomilova N, Yoder J (2007) Agrobacterium tumefaciens and Agrobacterium rhizogenes transformed roots of the parasitic plant Triphysaria versicolor retain parasitic competence. Planta 225:1059–1071PubMedCrossRefGoogle Scholar
  72. 72.
    Wysokińska H, Chmiel A (2006) Secondary metabolites production in cultures of transformed plant organs. Biotechnologia 4:124–135 (in Polish)Google Scholar
  73. 73.
    Georgiev M, Georgiev V, Weber J, Bley TH, Ilieva M, Pavlov A (2008) Agrobacterium rhizogenes-mediated genetic transformations: a powerful tool for the production of metabolites. In: Wolf T, Koch J (eds) Genetically modified plants. Nova Science Publishers Inc., New YorkGoogle Scholar
  74. 74.
    Ishida JK, Yoshida S, Ito M, Namba S, Shirasu K (2011) Agrobacterium rhizogenes mediated transformation of the parasitic plant Phtheirospermum japonicum. PLoS One 6:e25802. doi:10.1371/journal.pone.0025802.g002CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Georgiev MI, Ludwig-Müller J, Alipieva K, Lippert A (2011) Sonication-assisted Agrobacterium rhizogenes-mediated transformation of Verbascum xanthopoeniceum Griseb. for bioactive metabolite accumulation. Plant Cell Rep 30:859–866PubMedCrossRefGoogle Scholar
  76. 76.
    Trick HN, Finer JJ (1997) SAAT: sonication-assisted Agrobacterium-mediated transformation. Transgenic Res 6:329–336CrossRefGoogle Scholar
  77. 77.
    Georgiev MI, Radziszewska A, Neumann M, Marchev A, Alipieva K, Ludwig-Müller J (2015) Metabolic alterations of Verbascum nigrum L. plants and SAArT transformed roots as revealed by NMR-based metabolomics. Plant Cell Tiss Org Cult 123:349–356CrossRefGoogle Scholar
  78. 78.
    Piątczak E, Królicka A, Wielanek M, Wysokińska H (2012) Hairy root cultures of Rehmannia glutinosa and production of iridoid and phenylethanoid glycosides. Acta Physiol Plant 34:2215–2224CrossRefGoogle Scholar
  79. 79.
    Lloyd G, McCown B (1980) Commercially-feasible micropropagation of mountain laurel Kalmia latifolia by use of shoot-tip culture. Int Plant Propag Soc 30:421–427Google Scholar
  80. 80.
    Hwang SJ (2005) Growth characteristics and catalpol production on Chinese foxglove (Rehmannia glutinosa Liboschitz) hairy roots transformed with Agrobacterium rhizogenes ATCC15834. J Plant Biol 48:380–386CrossRefGoogle Scholar
  81. 81.
    Schenk RV, Hildebrandt AC (1972) Medium techniques for induction and growth of monocotyledonous and dicotyledonous plant cell cultures. Can J Bot 50:199–204CrossRefGoogle Scholar
  82. 82.
    Piątczak E, Kuźma Ł, Skała E, Żebrowska M, Balcerczak E, Wysokińska H (2015) Iridoid and phenylethanoid glycoside production and phenotypical changes in plants regenerated from hairy roots of Rehmannia glutinosa Libosch. Plant Cell Tiss Org Cult 122:259–266CrossRefGoogle Scholar
  83. 83.
    Zhou YQ, Duan HY, Zhou CE, Li JJ, Gu FP, Wang F, Hang ZY, Gao ZM (2009) Hairy root induction and plant regeneration of Rehmannia glutinosa Libosch. f. hueichingensis Hsiao via Agrobacterium rhizogenes-mediated transformation. Russ J Plant Physiol 56:224–231CrossRefGoogle Scholar
  84. 84.
    Kim YS, Kim YK, Xu H, Uddin MR, Park NI, Kim HH, Chae SCh, Park SU (2012) Improvement of ornamental characteristics in Rehmannia elata through Agrobacterium rhizogenes-mediated transformation. POJ 5:376–380Google Scholar
  85. 85.
    Chetana R, Ramawat KG (2009) Elicitor induced accumulation of stilbenes in cell suspension cultures of Cayratia trifolia (L.) Domin. Plant Biotechnol Rep 3:135–138CrossRefGoogle Scholar
  86. 86.
    D’Onofrio C, Cox A, Davis C, Boss PK (2009) Induction of secondary metabolism in grape cell cultures by jasmonates. Funct Plant Biol 36:323–338CrossRefGoogle Scholar
  87. 87.
    Ozawa R, Arimura G, Takabayashi J, Shimoda T, Nishioka T (2000) Involvement of jasmonate- and salicylate-related signaling pathways for the production of specific herbivore-induced volatiles in plants. Plant Cell Physiol 41:391–398PubMedCrossRefGoogle Scholar
  88. 88.
    Schenk PM, Kazan K, Wilson I, Anderson JP, Richmond T, Somerville SC, Manners JM (2000) Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proc Natl Acad Sci U S A 97:11655–11660PubMedPubMedCentralCrossRefGoogle Scholar
  89. 89.
    Cheng X-Y, Zhou H-Y, Cui X, Ni W, Liu Ch-Z (2006) Improvement of phenylethanoid glycosides biosynthesis in Cistanche deserticola cell suspension cultures by chitosan elicitor. J Biotechnol 121:253–260PubMedCrossRefGoogle Scholar
  90. 90.
    Hu GS, Hur YJ, Jia JM, Lee JH, Chung YS, Yi YB, Yun DJ, Park SK, Kim DH (2011) Effects of 2-aminoindan-2-phosphonic acid treatment on the accumulation of salidroside and four phenylethanoid glycosides in suspension cell culture of Cistanche deserticola. Plant Cell Rep 30:665–674PubMedCrossRefGoogle Scholar
  91. 91.
    Namdeo AG (2007) Plant cell elicitation for production of secondary metabolites: a review. Pharmacogn Rev 1:69–79Google Scholar
  92. 92.
    Lu C-T, Mei X-G (2003) Improvement of phenylethanoid glycosides production by a fungal elicitor in cell suspension culture of Cistanche deserticola. Biotechnol Lett 25:1437–1439PubMedCrossRefGoogle Scholar
  93. 93.
    Ouyang J, Wang X, Zhao B, Yuan X, Wang Y (2003) Effects of rare earth elements on the growth of Cistanche deserticola cells and the production of phenylethanoid glycosides. J Biotechnol 102:129–134PubMedCrossRefGoogle Scholar
  94. 94.
    Xu LS, Xue XF, Fu CX, Jin ZP, Chen YQ, Zhao DX (2005) Effects of methyl jasmonate and salicylic acid on phenylethanoid glycosides synthesis in suspension cultures of Cistanche deserticola. Chin J Biotechnol 21:402–406Google Scholar
  95. 95.
    Chen W-H, Xu Ch-M, Zeng J-L, Zhao B, Wang X-D, Wang Y-Ch (2007) Improvement of echinacoside and acteoside production by two-stage elicitation in cell suspension culture of Cistanche deserticola. World J Microbiol Biotechnol 23:1451–1458CrossRefGoogle Scholar
  96. 96.
    Cheng X-Y, Guo B, Zhou H-Y, Ni W, Liu Ch-Z (2005) Repeated elicitation enhances phenylethanoid glycosides accumulation in cell suspension cultures of Cistanche deserticola. Biochem Eng J 24:203–207CrossRefGoogle Scholar
  97. 97.
    Liu Ch-Z, Cheng X-Y (2008) Enhancement of phenylethanoid glycosides biosynthesis in cell cultures of Cistanche deserticola by osmotic stress. Plant Cell Rep 27:357–362PubMedCrossRefGoogle Scholar
  98. 98.
    Chen J, Yan Y-X, Guo Z-G (2015) Identification of hydrogen peroxide responsive ESTs involved in phenylethanoid glycoside biosynthesis in Cistanche salsa cell culture. Biol Plant 59:695–700CrossRefGoogle Scholar
  99. 99.
    Cao Y-J, Jia J-M (2011) Effects of nitric oxide, methyl jasmonate and salicylic acid on the phenylethanoid glycosides production and cell growth in suspension cultures of Cistanche deserticola. Chin Pharm J 46:1069–1073Google Scholar
  100. 100.
    Piątczak E, Kuźma Ł, Wysokińska H (2016) The influence of methyl jasmonate and salicylic acid on secondary metabolite production in Rehmannia glutinosa Libosch. hairy root culture. Acta Biol Cracov Bot 58:57–65Google Scholar
  101. 101.
    DiCosmo F, Misawa M (1995) Plant cell and tissue culture: alternatives for metabolite production. Biotechnol Adv 13:425–453PubMedPubMedCentralCrossRefGoogle Scholar
  102. 102.
    Liu J-Y, Guo Z-G, Zeng Z-L (2007) Improved accumulation of phenylethanoid glycosides by precursor feeding to suspension culture of Cistanche salsa. Biochem Eng J 33:88–93CrossRefGoogle Scholar
  103. 103.
    Hu G-S, Jia J-M, Doh HK (2014) Effects of feeding tyrosine and phenylalanine on the accumulation of phenylethanoid glycosides to Cistanche deserticola cell suspension culture. Chin J Nat Med 12:367–372PubMedGoogle Scholar
  104. 104.
    Cheng X-Y, Wei T, Guo B, Ni W, Liu Ch-Z (2005) Cistanche deserticola cell suspension cultures: phenylethanoid glycosides biosynthesis and antioxidant activity. Process Biochem 40:3119–3124CrossRefGoogle Scholar
  105. 105.
    Ouyang J, Wang X-D, Zhao B, Wang Y-Ch (2003) Formation of phenylethanoid glycosides by Cistanche deserticola callus grown on solid media. Biotechnol Lett 25:223–225Google Scholar
  106. 106.
    Ouyang J, Wang X, Zhao B, Wang Y (2003) Light intensity and spectral quality influencing the callus growth of Cistanche deserticola and biosynthesis of phenylethanoid glycosides. Plant Sci 165:657–661CrossRefGoogle Scholar
  107. 107.
    Jeong BR, Sivanesan I (2015) Direct adventitious shoot regeneration, in vitro flowering, fruiting, secondary metabolite content and antioxidant activity of Scrophularia takesimensis Nakai. Plant Cell Tiss Org Cult 123:607–618CrossRefGoogle Scholar
  108. 108.
    Endress R (1994) Plant cell biotechnology. Springer, Berlin/HeidelbergCrossRefGoogle Scholar
  109. 109.
    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 Tiss Org Cult 124:275–281CrossRefGoogle Scholar
  110. 110.
    Ouyang J, Wang X-D, Zhao B, Wang Y-Ch (2005) Improved production of phenylethanoid glycosides by Cistanche deserticola cells cultured in an internal loop airlift bioreactor with sifter riser. Enzyme Microb Technol 36:982–988CrossRefGoogle Scholar
  111. 111.
    Medina-Pérez V, López-Laredo AR, Sepúlveda-Jiménez G, Zamilpa A, Trejo-Tapia G (2015) Nitrogen deficiency stimulates biosynthesis of bioactive phenylethanoid glycosides in the medicinal plant Castilleja tenuiflora Benth. Acta Physiol Plant 37:93–100CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Ewelina Piątczak
    • 1
    Email author
  • Renata Grąbkowska
    • 1
  • Halina Wysokińska
    • 1
  1. 1.Department of Biology and Pharmaceutical BotanyMedical UniversityŁódźPoland

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