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Morphogenesis, Genetic Stability, and Secondary Metabolite Production in Untransformed and Transformed Cultures

Plant Cell and Tissue Differentiation and Secondary Metabolites

Part of the book series: Reference Series in Phytochemistry ((RSP))

Abstract

In addition to the primary metabolites, plants produce a vast number of chemically diversified economically valuable secondary metabolites (SMs) in specific cell types or tissue or organ of phylogenetically related family or genus or species or even to a single chemical race under tight environmental, developmental, and genetic control. Some SMs such as morphine and codeine are only synthesized in a particular organized and differentiated tissue or organ. Advancement in plant tissue culture and transcriptomic and metabolomic technologies have opened up a window to understand how the differentiation process is correlated to the secondary metabolic networks in diverse plant species. In vitro plant tissue culture provides a control artificial system for plant growth and development that nullified several other affecting factors associated with SM biosynthesis in ex vitro condition. Dedifferentiation, redifferentiation, and differentiation can be induced in in vitro culture by the exogenous application of different PGRs. Callus and cell suspension cultures represent undifferentiated or less differentiated state, and shoot or root organ cultures present more organized and differentiated state, whereas in vitro grown regenerated or micropropagated plants show fully differentiated and organized system with metabolic networks between different organs. Nowadays, differentiated and non-differentiated transformed cultures are very commonly utilized for production of SMs due to several advantages over other systems. This review attempts to highlight an overall knowledge about the role of differentiation and morphogenesis on SM production with genetic and biochemical stability of commonly used different in vitro cultures.

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References

  1. Neumann KH, Kumar A, Imani J (2009) Plant cell and tissue culture- a tool in biotechnology: basics and application. Springer, Berlin/Heidelberg

    Google Scholar 

  2. Naik PM, Al–Khayri JM (2016) Abiotic and biotic elicitors–role in secondary metabolites production through in vitro culture of medicinal plant. In: Shanker AK, Shanker C (eds) Abiotic and biotic stress in plants-recent advances and future perspectives. InTech, Rijeka

    Google Scholar 

  3. Halder M, Sarkar S, Jha S (2019) Elicitation: a biotechnological tool for enhanced production of secondary metabolites in hairy root cultures. Eng Life Sci 25:4693–4717

    Google Scholar 

  4. Kaur K, Pati PK (2018) Stress-induced metabolite production utilizing plant hairy roots. In: Srivastava V, Mehrotra S, Mishra S (eds) Hairy roots- an effective tool of plant biotechnology. Springer, Singapore

    Google Scholar 

  5. Matsuura HN, Malik S, de Costa F, Yousefzadi M, Mirjalili MH, Arroo R, Bhambra AS, Strnad M, Bonfill M, Fett-Neto AG (2018) Specialized plant metabolism characteristics and impact on target molecule biotechnological production. Mol Biotechnol 60:169–183

    Article  CAS  PubMed  Google Scholar 

  6. Hartmann T (2007) From waste products to ecochemicals: fifty years research of plant secondary metabolism. Phytochemistry 68:2831–2846

    Article  CAS  PubMed  Google Scholar 

  7. Collin HA (2001) Secondary product formation in plant tissue cultures. Plant Growth Regul 34:119–134

    Article  CAS  Google Scholar 

  8. Luckner M, Nover L, Böhm H (1977) Secondary metabolism and cell differentiation. Springer, Berlin/Heidelberg/New York

    Book  Google Scholar 

  9. Bennett JW (1983) Secondary metabolism as differentiation. J Food Saf 5:1–1

    Article  Google Scholar 

  10. Bartoshevich YE, Zaslavskaya PL, Novak MJ, Yudina OD (1990) Acremonium chrysogenum differentiation and biosynthesis of cephalosporin. J Basic Microbiol 30:313–320

    Article  CAS  PubMed  Google Scholar 

  11. Lindsey K, Yeoman MM (1983) The relationship between growth rate, differentiation and alkaloid accumulation in cell cultures. J Exp Bot 34:1055–1065

    Article  CAS  Google Scholar 

  12. De Luca V, Salim V, Thamm A, Masada SA, Yu F (2014) Making iridoids/secoiridoids and monoterpenoid indole alkaloids: progress on pathway elucidation. Curr Opin Plant Biol 19:35–42

    Article  CAS  PubMed  Google Scholar 

  13. Gonçalves S, Romano A (2018) Production of plant secondary metabolites by using biotechnological tools. In: Vijayakumar R, Raja SSS (eds) Secondary metabolites- sources and applications. IntechOpen, London

    Google Scholar 

  14. Courdavault V, Papon N, Clastre M, Giglioli-Guivarc’h N, St-Pierre B, Burlat V (2014) A look inside an alkaloid multisite plant: the Catharanthus logistics. Curr Opin Plant Biol 19:43–50

    Article  CAS  PubMed  Google Scholar 

  15. Nour-Eldin HH, Halkier BA (2013) The emerging field of transport engineering of plant specialized metabolites. Curr Opin Biotechnol 24:263–270

    Article  CAS  PubMed  Google Scholar 

  16. 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 Plants Res 3:1222–1239

    CAS  Google Scholar 

  17. Murthy HN, Lee EJ, Paek KY (2014) Production of secondary metabolites from cell and organ cultures: strategies and approaches for biomass improvement and metabolite accumulation. Plant Cell Tissue Organ Cult 118:1–16

    Article  CAS  Google Scholar 

  18. Isah T, Umar S, Mujib A, Sharma MP, Rajasekharan PE, Zafar N, Frukh A (2018) Secondary metabolism of pharmaceuticals in the plant in vitro cultures: strategies, approaches, and limitations to achieving higher yield. Plant Cell Tissue Organ Cult 132:239–265

    Article  CAS  Google Scholar 

  19. Jha S (1995) Transgenic organ cultures and their use in plant secondary metabolism. Proc Indian Natl Sci Acad Part B 61:63–72

    CAS  Google Scholar 

  20. Opabode JT (2006) Agrobacterium-mediated transformation of plants: emerging factors that influence efficiency. Biotechnol Mol Biol Rev 1:12–20

    Google Scholar 

  21. Roychowdhury D, Majumder A, Jha S (2013) Agrobacterium rhizogenes-mediated transformation in medicinal plants: prospects and challenges. In: Chandra S, Lata H, Varma A (eds) Biotechnology for medicinal plants. Springer, Berlin/Heidelberg

    Google Scholar 

  22. Mehrotra S, Srivastava V, Rahman LU, Kukreja AK (2015) Hairy root biotechnology- indicative timeline to understand missing links and future outlook. Protoplasma 252:1189–1201

    Article  CAS  PubMed  Google Scholar 

  23. Vaghari H, Jafarizadeh-Malmiri H, Anarjan N, Berenjian A (2017) Hairy root culture: a biotechnological approach to produce valuable metabolites. In: Meena VS, Mishra PK, Bisht JK, Pattanayak A (eds) Agriculturally important microbes for sustainable agriculture. Springer, Singapore

    Google Scholar 

  24. Srivastava V, Mehrotra S, Mishra S (2018) Hairy roots: an effective tool of plant biotechnology. Springer, Singapore

    Book  Google Scholar 

  25. Jha S (1988) Bufadienolides. In: Constabel F, Vasil IK (eds) Phytochemicals in plant cell cultures. Academic, San Diego

    Google Scholar 

  26. Almagro L, Belchi-Navarro S, Sabater-Jara AB, Vera-Urbina JC, Sellés-Marchart S, Bru R, Pedreño MA (2013) Bioproduction of trans-resveratrol from grapevine cell cultures. In: Ramawat K, Mérillon JM (eds) Natural products: phytochemistry, botany and metabolism of alkaloids, phenolics and terpenes. Springer, Berlin/Heidelberg

    Google Scholar 

  27. Goto S, Thakur RC, Ishii K (1998) Determination of genetic stability in long-term micropropagated shoots of Pinus thunbergii Parl. using RAPD markers. Plant Cell Rep 18:193–197

    Article  CAS  PubMed  Google Scholar 

  28. Bidabadi SS, Meon S, Wahab Z, Mahmood M (2010) Study of genetic and phenotypic variability among somaclones induced by BAP and TDZ in micropropagated shoot tips of banana (Musa spp.) using RAPD markers. J Agric Sci 2:49–60

    Google Scholar 

  29. Khoddamzadeh AA (2010) Detection of somaclonal variation by random amplified polymorphic DNA analysis during micropropagation of Phalaenopsis bellina (Rchb. f.) Christenson. Afr J Biotechnol 9:6632–6639

    CAS  Google Scholar 

  30. Roychowdhury D, Halder M, Jha S (2017) Agrobacterium rhizogenes-mediated transformation in medicinal plants: genetic stability in long-term culture. In: Jha S (ed) Transgenesis and secondary metabolism. Springer, Cham

    Google Scholar 

  31. Thakore D, Srivastava AK, Sinha AK (2017) Mass production of ajmalicine by bioreactor cultivation of hairy roots of Catharanthus roseus. Biochem Eng J 119:84–91

    Article  CAS  Google Scholar 

  32. Yue W, Ming QL, Lin B, Rahman K, Zheng CJ, Han T, Qin LP (2016) Medicinal plant cell suspension cultures: pharmaceutical applications and high-yielding strategies for the desired secondary metabolites. Crit Rev Biotechnol 36:215–232

    Article  CAS  PubMed  Google Scholar 

  33. Rao SR, Ravishankar GA (2002) Plant cell cultures: chemical factories of secondary metabolites. Biotechnol Adv 20:101–153

    Article  CAS  PubMed  Google Scholar 

  34. Hussain MS, Fareed S, Saba Ansari M, Rahman A, Ahmad IZ, Saeed M (2012) Current approaches toward production of secondary plant metabolites. J Pharm Bioallied Sci 4:10–20

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Efferth T (2019) Biotechnology applications of plant callus cultures. Engineering 5:50–59

    Article  CAS  Google Scholar 

  36. Luckner M, Nover L, Böhm H (1977) Secondary metabolism and cell differentiation. Springer, Verlag/Berlin/Heidelberg

    Google Scholar 

  37. Moscatiello R, Baldan B, Navazio L (2013) Plant cell suspension cultures. Methods Mol Biol 953:77–93

    CAS  PubMed  Google Scholar 

  38. Pandey H, Nandi SK, Kumar A, Palni UT, Chandra B, Palni LM (2004) In vitro propagation of Aconitum balfourii Stapf.: an important aconite of the Himalayan alpines. J Hortic Sci Biotechnol 79:34–41

    Article  Google Scholar 

  39. Rawat JM, Rawat B, Chandra A, Nautiyal S (2013) Influence of plant growth regulators on indirect shoot organogenesis and secondary metabolite production in Aconitum violaceum Jacq. Afr J Biotechnol 12:6287–6293

    Article  CAS  Google Scholar 

  40. Baumert A, Groger D, Kuzovkina IN, Reisch J (1992) Secondary metabolites produced by callus cultures of various Ruta species. Plant Cell Tissue Organ Cult 28:159–162

    Article  CAS  Google Scholar 

  41. Zhao J, Hu Q, Guo YQ, Zhu WH (2001) Effects of stress factors, bioregulators, and synthetic precursors on indole alkaloid production in compact callus clusters cultures of Catharanthus roseus. Appl Microbiol Biotechnol 55:693–638

    Article  CAS  PubMed  Google Scholar 

  42. Maharik N, Elgengaihi S, Taha H (2009) Anthocyanin production in callus cultures of Crataegus sinaica boiss. Int J Acad Res 1:30–34

    Google Scholar 

  43. Sudha G, Ravishankar GA (2003) Elicitation of anthocyanin production in callus cultures of Daucus carota and the involvement of methyl jasmonate and salicylic acid. Acta Physiol Plant 25:249–256

    Article  CAS  Google Scholar 

  44. Rajendran L, Ravishankar GA, Venkataraman LV, Prathiba KR (1992) Anthocyanin production in callus cultures of Daucus carota as influenced by nutrient stress and osmoticum. Biotechnol Lett 14:707–712

    Article  CAS  Google Scholar 

  45. Rajendran L, Suvarnalatha G, Ravishankar GA, Venkataraman LV (1994) Enhancement of anthocyanin production in callus cultures of Daucus canota L. under the influence of fungal elicitors. Appl Microbiol Biotechnol 42:227–231

    CAS  Google Scholar 

  46. Nakamura M, Takeuchi Y, Miyanaga K, Seki M, Furusaki S (1999) High anthocyanin accumulation in the dark by strawberry (Fragaria ananassa) callus. Biotechnol Lett 21:695–699

    Article  CAS  Google Scholar 

  47. Miura H, Kitamura Y, Ikenaga T, Mizobe K, Shimizu T, Nakamura M, Kato Y, Yamada T, Maitani T, Goda Y (1988) Anthocyanin production of Glehnia littoralis callus cultures. Phytochemistry 48:279–283

    Article  Google Scholar 

  48. Mizukami H, Tomita K, Ohashi H, Hiraoka N (1988) Anthocyanin production in callus cultures of roselle (Hibiscus sabdariffa L.). Plant Cell Rep 7:553–556

    Article  CAS  PubMed  Google Scholar 

  49. Makunga NP, Van Staden J, Cress WA (1997) The effect of light and 2, 4-D on anthocyanin production in Oxalis reclinata callus. Plant Growth Regul 23:153–158

    Article  CAS  Google Scholar 

  50. Mathur A, Mathur AK, Gangwar A, Yadav S, Verma P, Sangwan RS (2010) Anthocyanin production in a callus line of Panax sikkimensis Ban. In Vitro Cell Dev Biol Plant 46:13–21

    Article  CAS  Google Scholar 

  51. Blando F, Scardino AP, De Bellis L, Nicoletti I, Giovinazzo G (2005) Characterization of in vitro anthocyanin-producing sour cherry (Prunus cerasus L.) callus cultures. Food Res Int 38:937–942

    Article  CAS  Google Scholar 

  52. Ram M, Prasad KV, Singh SK, Hada BS, Kumar S (2013) Influence of salicylic acid and methyl jasmonate elicitation on anthocyanin production in callus cultures of Rosa hybrida L. Plant Cell Tissue Organ Cult 113:459–467

    Article  CAS  Google Scholar 

  53. Smith SL, Slywka GW, Krueger RJ (1981) Anthocyanins of Strobilanthes dyeriana and their production in callus culture. J Nat Prod 44:609–610

    Article  CAS  Google Scholar 

  54. Hiroyuki H, Kousuke H, Eiji N, Mariko O, Yoshihito K, Setsuro H, Takeshi K (2002) Enhanced anthocyanin production from grape callus in an air-lift type bioreactor using a viscous additive-supplemented medium. J Biosci Bioeng 94:135–139

    Article  Google Scholar 

  55. Kim SH, Kim SK (2002) Effect of nitrogen source on cell growth and anthocyanin production in callus and cell suspension culture of ‘Sheridan’ grapes. J Plant Biotechnol 4:83–89

    Google Scholar 

  56. Nazif NM, Rady MR, El-Nasr MS (2000) Stimulation of anthraquinone production in suspension cultures of Cassia acutifolia by salt stress. Fitoterapia 71:34–40

    Article  CAS  PubMed  Google Scholar 

  57. Wijnsma R, Verpoorte R, Mulder-Krieger T, Svendsen AB (1984) Anthraquinones in callus cultures of Cinchona ledgeriana. Phytochemistry 23:2307–2311

    Article  CAS  Google Scholar 

  58. Wijnsma R, Go JT, Harkes PA, Verpoorte R, Svendsen AB (1986) Anthraquinones in callus cultures of Cinchona pubescens. Phytochemistry 25:1123–1126

    Article  CAS  Google Scholar 

  59. Anjusha S, Gangaprasad A (2017) Callus culture and in vitro production of anthraquinone in Gynochthodes umbellata (L.) Razafim. & B. Bremer (Rubiaceae). Ind Crop Prod 95:608–614

    Article  CAS  Google Scholar 

  60. Mischenko NP, Fedoreyev SA, Glazunov VP, Chernoded GK, Bulgakov VP, Zhuravlev YN (1999) Anthraquinone production by callus cultures of Rubia cordifolia. Fitoterapia 70:552–557

    Article  CAS  Google Scholar 

  61. Orbán N, Boldizsár I, Bóka K (2007) Structural and chemical study of callus formation from leaves of Rubia tinctorum. Biol Plant 51:421–429

    Article  Google Scholar 

  62. Baldi A, Dixit VK (2008) Enhanced artemisinin production by cell cultures of Artemisia annua. Curr Trend Biotechnol Pharmacol 2:341–348

    CAS  Google Scholar 

  63. Nair AJ, Sudhakaran PR, Rao JM, Ramakrishna SV (1992) Berberine synthesis by callus and cell suspension cultures of Coscinium fenestratum. Plant Cell Tissue Organ Cult 29:7–10

    Article  CAS  Google Scholar 

  64. Suzuki M, Nakagawa K, Fukui H, Tabata M (1987) Relationship of berberine-producing capability between Thalictrum plants and their tissue cultures. Plant Cell Rep 6:260–263

    Article  CAS  PubMed  Google Scholar 

  65. Pandey H, Pandey P, Singh S, Gupta R, Banerjee S (2015) Production of anti-cancer triterpene (betulinic acid) from callus cultures of different Ocimum species and its elicitation. Protoplasma 252:647–655

    Article  CAS  PubMed  Google Scholar 

  66. Bernabé-Antonio A, Estrada-Zúñiga ME, Buendía-González L, Reyes-Chilpa R, Chávez-Ávila VM, Cruz-Sosa F (2010) Production of anti-HIV-1 calanolides in a callus culture of Calophyllum brasiliense (Cambes). Plant Cell Tissue Organ Cult 103:33–40

    Article  CAS  Google Scholar 

  67. Van Hengel AJ, Harkes MP, Wichers HJ, Hesselink PG, Buitelaar RM (1992) Characterization of callus formation and camptothecin production by cell lines of Camptotheca acuminata. Plant Cell Tissue Organ Cult 28:11–18

    Article  Google Scholar 

  68. Kulkarni AV, Patwardhan AA, Lele U, Malpathak NP (2010) Production of camptothecin in cultures of Chonemorpha grandiflora. Pharm Res 2:296–299

    CAS  Google Scholar 

  69. Thengane SR, Kulkarni DK, Shrikhande VA, Joshi SP, Sonawane KB, Krishnamurthy KV (2003) Influence of medium composition on callus induction and camptothecin(s) accumulation in Nothapodytes foetida. Plant Cell Tissue Organ Cult 72:247–251

    Article  CAS  Google Scholar 

  70. Fulzele DP, Satdive R, Kamble S, Singh S, Singh S (2015) Improvement of anticancer drug camptothecin production by gamma irradiation on callus cultures of Nothapodytes foetida. Int J Pharm Res Allied Sci 4:19–27

    CAS  Google Scholar 

  71. Ochoa-Alejo N, Gómez-Peralta JE (1993) Activity of enzymes involved in capsaicin biosynthesis in callus tissue and fruits of chili pepper (Capsicum annuum L.). J Plant Physiol 141:147–152

    Article  CAS  Google Scholar 

  72. Umamaheswai A, Lalitha V (2007) In vitro effect of various growth hormones in Capsicum annum L. on the callus induction and production of Capsiacin. J Plant Sci 2:545–551

    Article  Google Scholar 

  73. Hao C, Shujuan Y, Yushu W, Li W (1993) Tea callus culture and the catechin accumulation [J]. J Tea Sci 13:109–114

    Google Scholar 

  74. Hodges CC, Rapoport H (1982) Morphinan alkaloids in callus cultures of Papaver somniferum. J Nat Prod 45:481–485

    Article  CAS  Google Scholar 

  75. Sivakumar G, Krishnamurthy KV, Hahn EJ, Paek KY (2004) Enhanced in vitro production of colchicine in Gloriosa superba L.- an emerging industrial medicinal crop in South India. J Hortic Sci Biotechnol 79:602–605

    Article  CAS  Google Scholar 

  76. Sivakumar G, Krishnamurthy KV, Hao J, Paek KY (2004a) Colchicine production in Gloriosa superba calluses by feeding precursors. Chem Nat Compd 40:499–502

    Article  CAS  Google Scholar 

  77. Staniszewska I, Królicka A, Maliński E, Łojkowska E, Szafranek J (2003) Elicitation of secondary metabolites in in vitro cultures of Ammi majus L. Enzym Microb Technol 33:565–568

    Article  CAS  Google Scholar 

  78. Shabana MM, El-Alfy TS, El-Tantawy ME, Ibrahim AI, Ibrahim GF (2002) Tissue culture and evaluation of some active constituents of Ruta graveolens L. II: effect of plant growth regulators, explant type and precursor on coumarin content of Ruta graveolens L. callus cultures. Arab J Biotechnol 5:45–56

    Google Scholar 

  79. Chen SA, Wang X, Zhao B, Yuan X, Wang Y (2003) Production of crocin using Crocus sativus callus by two-stage culture system. Biotechnol Lett 25:1235–1238

    Article  CAS  PubMed  Google Scholar 

  80. Wu CT, Mulabagal V, Nalawade SM, Chen CL, Yang TF, Tsay HS (2003) Isolation and quantitative analysis of cryptotanshinone, an active quinoid diterpene formed in callus of Salvia miltiorrhiza B UNGE. Biol Pharm Bull 26:845–848

    Article  CAS  PubMed  Google Scholar 

  81. Shinde AN, Malpathak N, Fulzele DP (2010) Determination of isoflavone content and antioxidant activity in Psoralea corylifolia L. callus cultures. Food Chem 118:128–132

    Article  CAS  Google Scholar 

  82. Šavikin-Fodulović K, Grubišić D, Ćulafić L, Menković N, Ristić M (1998) Diosgenin and phytosterols content in five callus lines of Dioscorea balcanica. Plant Sci 135:63–67

    Article  Google Scholar 

  83. Oncina R, Del Rı́o JA, Gomez P, Ortuno A (2002) Effect of ethylene on diosgenin accumulation in callus cultures of Trigonella foenum-graecum L. Food Chem 76:475–459

    Article  CAS  Google Scholar 

  84. Pawar KD, Joshi SP, Bhide SR, Thengane SR (2007) Pattern of anti HIV dypiranocoumarin expression in callus cultures of Calophyllum inophyllum Linn. J Biotechnol 130:346–353

    Article  CAS  PubMed  Google Scholar 

  85. Murthy HN, Kim YS, Georgiev MI, Paek KY (2014) Biotechnological production of eleutherosides: current state and perspectives. Appl Microbiol Biotechnol 98:7319–7329

    Article  CAS  PubMed  Google Scholar 

  86. Kouadio K, Chenieux JC, Rideau M, Viel C (1984) Antitumor alkaloids in callus cultures of Ochrosia elliptica. J Nat Prod 47:872–874

    Article  CAS  PubMed  Google Scholar 

  87. Vetrichelvan T, Kavimani S, Elango R, Jaykar B (1996) Effect of L-dopa and L-methionine supplementation on bioproduction of ementine in callus cultures of Cephaelis ipecacuanha. Anc Sci Life 16:74–78

    CAS  PubMed  PubMed Central  Google Scholar 

  88. Jha S, Sahu NP, Mahato SB (1998) Production of the alkaloids emetine and cephaeline in callus cultures of Cephaelis ipecacuanha. Planta Med 54:504–506

    Article  Google Scholar 

  89. Sen J, Sharma AK, Sahu NP, Mahato SB (1992) Production of forskolin in in vitro cultures of Coleus forskohlii. Planta Med 58:324–327

    Article  CAS  PubMed  Google Scholar 

  90. Malathy S, Pap JS (1999) Monitoring of forskolin production from roots and callus by HPTLC in Coleus forskohlii Briq. J Spices Aromat Crops 8:153–157

    Google Scholar 

  91. Jha S, Bandyopadhyay M, Chaudhuri KN, Ghosh S, Ghosh B (2005) Biotechnological approaches for the production of forskolin, withanolides, colchicine and tylophorine. Plant Genet Resour 3:101–115

    Article  CAS  Google Scholar 

  92. Łuczkiewicz M, Głód D (2003) Callus cultures of Genista plants- in vitro material producing high amounts of isoflavones of phytoestrogenic activity. Plant Sci 165:1101–1108

    Article  CAS  Google Scholar 

  93. Sabater-Jara AB, Souliman-Youssef S, Novo-Uzal E, Almagro L, Belchí-Navarro S, Pedreño MA (2013) Biotechnological approaches to enhance the biosynthesis of ginkgolides and bilobalide in Ginkgo biloba. Phytochem Rev 12:191–205

    Article  CAS  Google Scholar 

  94. Mathur A, Mathur AK, Pal M, Uniyal GC (1999) Comparison of qualitative and quantitative in vitro ginsenoside production in callus cultures of three Panax species. Planta Med 65:484–486

    Article  CAS  PubMed  Google Scholar 

  95. Bonfill M, Cusidó RM, Palazón J, Piñol MT, Morales C (2002) Influence of auxins on organogenesis and ginsenoside production in Panax ginseng calluses. Plant Cell Tissue Organ Cult 68:73–78

    Article  CAS  Google Scholar 

  96. Loc NH, Anh NH, Binh DH, Yang MS, Kim TG (2010) Production of glycoalkaloids from callus cultures of Solanum hainanense Hance. J Plant Biotechnol 37:96–101

    Article  Google Scholar 

  97. Mathur M, Jain AK, Dass S, Ramawat KG (2007) Optimization of guggulsterone production in callus cultures of Commiphora wightii (Arnott.) Bhandari. Indian J Biotechnol 6:525–531

    CAS  Google Scholar 

  98. Gopi C, Vatsala TM (2006) In vitro studies on effects of plant growth regulators on callus and suspension culture biomass yield from Gymnema sylvestre R. Br. Afr J Biotechnol 5:1215–1219

    CAS  Google Scholar 

  99. Ahmed AB, Rao AS, Rao MV (2009) In vitro production of gymnemic acid from Gymnema sylvestre (Retz) R. Br. ex Roemer and Schultes through callus culture under abiotic stress conditions. In: Jain SM, Saxena PK (eds) Protocols for in vitro cultures and secondary metabolite analysis of aromatic and medicinal plants, methods in molecular biology (methods and protocols). Humana Press, Totowa, p 547

    Google Scholar 

  100. Nikam TD, Ebrahimi MA, Patil VA (2009) Embryogenic callus culture of Tribulus terrestris L. a potential source of harmaline, harmine and diosgenin. Plant Biotechnol Rep 3:243–250

    Article  Google Scholar 

  101. Zhao DX, Fu CX, Han YS, Lu DP (2005) Effects of elicitation on jaceosidin and hispidulin production in cell suspension cultures of Saussurea medusa. Process Biochem 40(2):739–745

    Article  CAS  Google Scholar 

  102. Biondi S, Scaramagli S, Oksman-Caldentey KM, Poli F (2002) Secondary metabolism in root and callus cultures of Hyoscyamus muticus L.: the relationship between morphological organisation and response to methyl jasmonate. Plant Sci 163:563–569

    Article  CAS  Google Scholar 

  103. Gadzovska S, Maury S, Ounnar S, Righezza M, Kascakova S, Refregiers M, Spasenoski M, Joseph C, Hagège D (2005) Identification and quantification of hypericin and pseudohypericin in different Hypericum perforatum L. in vitro cultures. Plant Physiol Biochem 43:591–601

    Article  CAS  PubMed  Google Scholar 

  104. Ikuta A, Nakamura T, Urabe H (1998) Indolopyridoquinazoline, furoquinoline and canthinone type alkaloids from Phellodendron amurense callus tissues. Phytochemistry 48:285–291

    Article  CAS  Google Scholar 

  105. Thanonkeo S, Panichajakul S (2006) Production of isoflavones, daidzein and genistein in callus cultures of Pueraria candollei Wall. ex Benth. var. mirifica. Songklanakarin J Sci Technol 28:45–53

    Google Scholar 

  106. Tisserat B, Berhow M (2009) Production of pharmaceuticals from Papaver cultivars in vitro. Eng Life Sci 9:190–196

    Article  CAS  Google Scholar 

  107. Praveena C, Veeresham C (2015) Benzophenanthridine alkaloids from callus cutures of Toddalia asiatica. Int J Pharm Sci Nano Technol 8:3003–3008

    CAS  Google Scholar 

  108. Ku KL, Chang PS, Cheng YC, Lien CY (2005) Production of stilbenoids from the callus of Arachis hypogaea: a novel source of the anticancer compound piceatannol. J Agric Food Chem 53:3877–3881

    Article  CAS  PubMed  Google Scholar 

  109. Deshpande J, Labade D, Shankar K, Kata N, Chaudhari M, Wani M, Khetmalas M (2014) In vitro callus induction and estimation of plumbagin content from Plumbago auriculata Lam. Indian J Exp Biol 52:1122–1127

    PubMed  Google Scholar 

  110. Satheeshkumar K, Seeni S (2002) Production of plumbagin (5-hydroxy-2-methyl-1, 4-naphthoquinone) in callus and cell suspension cultures of Plumbago indica Linn. Indian J Biotechnol 1:305–308

    CAS  Google Scholar 

  111. Heyenga AG, Lucas JA, Dewick PM (1990) Production of tumour-inhibitory lignans in callus cultures of Podophyllum hexandrum. Plant Cell Rep 9:382–385

    Article  CAS  PubMed  Google Scholar 

  112. Anrini M, Jha S (2009) Characterization of podophyllotoxin yielding cell lines of Podophyllum hexandrum. Caryologia 62:220–235

    Article  Google Scholar 

  113. Kadkade PG (1982) Growth and podophyllotoxin production in callus tissues of Podophyllum peltatum. Plant Sci Lett 25:107–115

    Article  CAS  Google Scholar 

  114. Guerram M, Jiang Z-Z, Zhang L-Y (2012) Podophyllotoxin, a medicinal agent of plant origin: past, present and future. Chin J Nat Med 10:161–169

    Article  CAS  Google Scholar 

  115. Jayapaul K, Kishor PK, Reddy KJ (2005) Production of pyrroloquinazoline alkaloid from leaf and petiole-derived callus cultures of Adhatoda zeylanica. In Vitro Cell Dev Biol Plant 41:682–685

    Article  CAS  Google Scholar 

  116. Scragg AH, Allan EJ (1986) Production of the triterpenoid quassin in callus and cell suspension cultures of Picrasma quassioides Bennett. Plant Cell Rep 5:356–359

    Article  CAS  PubMed  Google Scholar 

  117. Yamamoto O, Yamada Y (1987) Selection of a reserpine-producing cell strain using UV-light and optimization of reserpine production in the selected cell strain. Plant Cell Tissue Organ Cult 8:125–133

    Article  CAS  Google Scholar 

  118. Nurcahyani N, Solichatun S, Anggarwulan E (2008) The reserpine production and callus growth of Indian snake root (Rauvolfia serpentina (L.) benth. Ex Kurz) culture by addition of Cu2+. Biodiversitas J Biol Divers 9:177–179

    Article  Google Scholar 

  119. Dey A, De JN (2010) Rauvolfia serpentina (L). benth. ex Kurz.-A review. Asian J Plant Sci 9:285–298

    Article  Google Scholar 

  120. Zafar N, Mujib A, Ali M, Tonk D, Gulzar B (2017) Aluminum chloride elicitation (amendment) improves callus biomass growth and reserpine yield in Rauvolfia serpentina leaf callus. Plant Cell Tissue Organ Cult 130:357–368

    Article  CAS  Google Scholar 

  121. Anitha S, Ranjitha BD (2006) Stimulation of reserpine biosynthesis in the callus of Rauvolfia tetraphylla L. by precursor feeding. Afr J Biotechnol 5:659–661

    CAS  Google Scholar 

  122. Rohela GK, Bylla P, Korra R, Reuben C (2016) Phytochemical screening and antimicrobial activity of leaf, stem, root and their callus extracts in Rauwolfia tetraphylla. Int J Agric Biol 18:521–528

    Article  CAS  Google Scholar 

  123. Keskin N, Kunter B (2010) Production of trans-resveratrol in callus tissue of Öküzgözü (Vitis vinifera L.) in response to ultraviolet-C irradiation. J Anim Plant Sci 20:197–200

    Google Scholar 

  124. Liu W, Liu C, Yang C, Wang L, Li S (2010) Effect of grape genotype and tissue type on callus growth and production of resveratrols and their piceids after UV-C irradiation. Food Chem 122:475–481

    Article  CAS  Google Scholar 

  125. Nandagopal K, Halder M, Dash B, Nayak S, Jha S (2018) Biotechnological approaches for production of anti-cancerous compounds resveratrol, podophyllotoxin and zerumbone. Curr Med Chem 25:4693–4717

    Article  CAS  PubMed  Google Scholar 

  126. Xu H, Kim YK, Jin X, Lee SY, Park SU (2008) Rosmarinic acid biosynthesis in callus and cell cultures of Agastache rugosa Kuntze. J Med Plants Res 2:237–241

    Google Scholar 

  127. De-Eknamkul W, Ellis BE (1984) Rosmarinic acid production and growth characteristics of Anchusa officinalis cell suspension cultures. Planta Med 50:346–350

    Article  CAS  PubMed  Google Scholar 

  128. Petersen M (2013) Rosmarinic acid: new aspects. Phytochem Rev 12:207–227

    Article  CAS  Google Scholar 

  129. Kintzios S, Nikolaou A, Skoula M (1999) Somatic embryogenesis and in vitro rosmarinic acid accumulation in Salvia officinalis and S. fruticosa leaf callus cultures. Plant Cell Rep 18:462–426

    Article  CAS  Google Scholar 

  130. Karam NS, Jawad FM, Arikat NA, Shibl RA (2003) Growth and rosmarinic acid accumulation in callus, cell suspension, and root cultures of wild Salvia fruticosa. Plant Cell Tissue Organ Cult 73:117–121

    Article  CAS  Google Scholar 

  131. Tepe B, Sokmen A (2007) Production and optimisation of rosmarinic acid by Satureja hortensis L. callus cultures. Nat Prod Res 21:1133–1144

    Article  CAS  PubMed  Google Scholar 

  132. Furuya T, Yoshikawa T, Ishii T, Kajii K (1983) Effects of auxins on growth and saponin production in callus cultures of Panax ginseng. Planta Med 47:183–187

    Article  CAS  PubMed  Google Scholar 

  133. Mathur A, Shukla YN, Pal M, Ahuja PS, Uniyal GC (1994) Saponin production in callus and cell suspension cultures of Panax quinquefolium. Phytochemistry 35:1221–1225

    Article  CAS  Google Scholar 

  134. Inouye H, Ueda S, Inoue K, Matsumura H (1979) Biosynthesis of shikonin in callus cultures of Lithospermum erythrorhizon. Phytochemistry 18:1301–1308

    Article  CAS  Google Scholar 

  135. Yoshikawa N, Fukui H, Tabata M (1986) Effect of gibberellin A3 on shikonin production in Lithospermum callus cultures. Phytochemistry 25:621–622

    Article  CAS  Google Scholar 

  136. Tůmová L, Tůma J, Megušar K, Doležal M (2010) Substituted pyrazinecarboxamides as abiotic elicitors of flavolignan production in Silybum marianum (L.) gaertn cultures in vitro. Molecules 15:331–340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. Kittipongpatana N, Hock RS, Porter JR (1998) Production of solasodine by hairy root, callus, and cell suspension cultures of Solanum aviculare Forst. Plant Cell Tissue Organ Cult 52:133–143

    Article  CAS  Google Scholar 

  138. Nigra HM, Caso OH, Giulietti AM (1987) Production of solasodine by calli from different parts of Solanum elaeagnifolium Cav. plants. Plant Cell Rep 6:135–137

    CAS  PubMed  Google Scholar 

  139. Nigra HM, Alvarez MA, Giulietti AM (1989) The influence of auxins, light and cell differentiation on solasodine production by Solanum elaeagnifolium Cav. calli. Plant Cell Rep 8:230–233

    Article  CAS  PubMed  Google Scholar 

  140. Hosoda N, Ito H, Yatazawa M (1979) Some accounts on culture conditions of callus tissues of Solanum laciniatum Ait. for producing solasodine. Agric Biol Chem 43:1745–1748

    CAS  Google Scholar 

  141. Chandler SF (1984) Solasodine yield in callus cultures of Solanum laciniatum ait. selected for growth on hormone-free medium. Ann Bot 54:293–296

    Article  CAS  Google Scholar 

  142. Chandler SF, Dodds JH (1983) The effect of phosphate, nitrogen and sucrose on the production of phenolics and solasodine in callus cultures of Solanum laciniatum. Plant Cell Rep 2:205–208

    Article  CAS  PubMed  Google Scholar 

  143. Yogananth N, Bhakyaraj R, Chanthuru A, Parvathi S, Palanivel S (2009) Comparative analysis of solasodine from in vitro and in vivo cultures of Solanum nigrum Linn. Kathmandu University J Sci Eng Technol 5:99–103

    Article  Google Scholar 

  144. Wu CT, Mulabagal V, Nalawade SM, Chen CL, Yang TF, Tsay HS (2003) Isolation and quantitative analysis of cryptotanshinione, an active quinoid diterpene formed in callus of Salvia miltiorrhiza Bunge. Biol Pharm Bull 26:845–848

    Article  CAS  PubMed  Google Scholar 

  145. Krajewska-Patan A, Dreger M, Górska-Paukszta M, Mścisz A, Mielcarek S, Baraniak M, Buchwald W, Marecik R, Grajek W, Mrozikiewicz PM (2007) Salvia miltiorrhiza Bunge in vitro cultivation in callus cultures. Herba Pol 53:88–96

    CAS  Google Scholar 

  146. Deng H, Wang M, Hu S, Mou Q (2010) Effect of irradiating Salvia miltiorrhiza callus on the accumulation of Tanshinone IIA by laser. Med Plant 1:68–72

    CAS  Google Scholar 

  147. Sarmadi M, Karimi N, Palazón J, Ghassempour A, Mirjalili MH (2019) Improved effects of polyethylene glycol on the growth, antioxidative enzymes activity and taxanes production in a Taxus baccata L. callus culture. Plant Cell Tissue Organ Cult 137:319–328

    Article  CAS  Google Scholar 

  148. Majumder A, Jha S (2009) Biotechnological approaches for the production of potential anticancer leads podophyllotoxin and paclitaxel: an overview. J Biol Sci 1:46–69

    Google Scholar 

  149. Wickremesinhe ER, Arteea RN (1993) Taxus callus cultures: initiation, growth optimization, characterization and taxol production. Plant Cell Tissue Organ Cult 35:181–193

    Article  CAS  Google Scholar 

  150. Feng Y, Guo Z (1999) Low ammonium medium used in Taxus ssp. callus inducement and taxol biosynthesis. Nat Prod Res Dev 11:7–13

    CAS  Google Scholar 

  151. Cusidó RM, Palazón J, Navia-Osorio A, Mallol A, Bonfill M, Morales C, Piñol MT (1999) Production of Taxol® and baccatin III by a selected Taxus baccata callus line and its derived cell suspension culture. Plant Sci 146:101–117

    Article  Google Scholar 

  152. Orihara Y, Furuya T (1990) Production of theanine and other γ-glutamyl derivatives by Camellia sinensis cultured cells. Plant Cell Rep 9:65–68

    Article  CAS  PubMed  Google Scholar 

  153. Taniguchi S, Imayoshi Y, Kobayashi E, Takamatsu Y, Ito H, Hatano T, Sakagami H, Tokuda H, Nishino H, Sugita D, Shimura S (2002) Production of bioactive triterpenes by Eriobotrya japonica calli. Phytochemistry 59:315–323

    Article  CAS  PubMed  Google Scholar 

  154. Kalidass C, Mohan VR, Daniel A (2009) Effect of auxin and cytokinin on vincristine production by callus cultures of Catharanthus roseus L. (apocynaceae). Trop Subtrop Agroecosys 12:283–288

    Google Scholar 

  155. Mekky H, Al-Sabahi J, Abdel-Kreem MF (2018) Potentiating biosynthesis of the anticancer alkaloids vincristine and vinblastine in callus cultures of Catharanthus roseus. S Afr J Bot 114:29–31

    Article  CAS  Google Scholar 

  156. Passinho-Soares H, Meira P, David J, Mesquita P, Vale A, de M Rodrigues F, de P Pereira P, de Santana J, de Oliveira F, de Andrade J, David J (2013) Volatile organic compounds obtained by in vitro callus cultivation of Plectranthus ornatus Codd.(Lamiaceae). Molecules 18:10320–10333

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  157. Hwang SJ, Kim YH, Pyo BS (2004) Optimization of aconitine production in suspension cell cultures of Aconitum napellus L. Korean J Med Crop Sci 12:366–371

    Google Scholar 

  158. Baumert A, Maier W, Schumann B, Gröger D (1991) Increased accumulation of acridone alkaloids by cell suspension cultures of Ruta graveolens in response to elicitors. J Plant Physiol 139:224–228

    Article  CAS  Google Scholar 

  159. Zenk MH, El-Shagi H, Arens H, Stöckigt J, Weiler EW, Deus B (1977) Formation of the indole alkaloids serpentine and ajmalicine in cell suspension cultures of Catharanthus roseus. In: Barz W, Reinhard E, Zenk MH (eds) Plant tissue culture and its bio-technological application, proceedings in life sciences. Springer, Berlin/Heidelberg

    Google Scholar 

  160. Schlatmann JE, Nuutila AM, Van Gulik WM, Ten Hoopen HJ, Verpoorte R, J Heijnen J (1993) Scaleup of ajmalicine production by plant cell cultures of Catharanthus roseus. Biotechnol Bioeng 41:253–262

    Article  CAS  PubMed  Google Scholar 

  161. Namdeo A, Patil S, Fulzele DP (2002) Influence of fungal elicitors on production of ajmalicine by cell cultures of Catharanthus roseus. Biotechnol Prog 18:159–162

    Article  CAS  PubMed  Google Scholar 

  162. Nartop P, Akay Ş, Gürel A (2013) Immobilization of Rubia tinctorum L. suspension cultures and its effects on alizarin and purpurin accumulation and biomass production. Plant Cell Tissue Organ Cult 112:123–128

    Article  CAS  Google Scholar 

  163. Kobayashi Y, Akita M, Sakamoto K, Liu H, Shigeoka T, Koyano T, Kawamura M, Furuya T (1993) Large-scale production of anthocyanin by Aralia cordata cell suspension cultures. Appl Microbiol Biotechnol 40:215–218

    Article  CAS  Google Scholar 

  164. Pasqua G, Monacelli B, Mulinacci N, Rinaldi S, Giaccherini C, Innocenti M, Vinceri FF (2005) The effect of growth regulators and sucrose on anthocyanin production in Camptotheca acuminata cell cultures. Plant Physiol Biochem 43:293–298

    Article  CAS  PubMed  Google Scholar 

  165. Narayan MS, Venkataraman LV (2000) Characterisation of anthocyanins derived from carrot (Daucus carota) cell culture. Food Chem 70:361–363

    Article  CAS  Google Scholar 

  166. Zhang W, Seki M, Furusaki S (1997) Effect of temperature and its shift on growth and anthocyanin production in suspension cultures of strawberry cells. Plant Sci 127:207–214

    Article  CAS  Google Scholar 

  167. Chan LK, Koay SS, Boey PL, Bhatt A (2010) Effects of abiotic stress on biomass and anthocyanin production in cell cultures of Melastoma malabathricum. Biol Res 43:127–135

    Article  CAS  PubMed  Google Scholar 

  168. Hirasuna TJ, Shuler ML, Lackney VK, Spanswick RM (1991) Enhanced anthocyanin production in grape cell cultures. Plant Sci 78:107–120

    Article  CAS  Google Scholar 

  169. Saw NM, Riedel H, Cai Z, Kütük O, Smetanska I (2012) Stimulation of anthocyanin synthesis in grape (Vitis vinifera) cell cultures by pulsed electric fields and ethephon. Plant Cell Tissue Organ Cult 108:47–54

    Article  CAS  Google Scholar 

  170. Abdullah MA, Ariff AB, Marziah M, Ali AM, Lajis NH (2000) Growth and anthraquinone production of Morinda elliptica cell suspension cultures in a stirred-tank bioreactor. J Agric Food Chem 48:4432–4438

    Article  CAS  PubMed  Google Scholar 

  171. Thiruvengadam M, Rekha K, Rajakumar G, Lee TJ, Kim SH, Chung IM (2016) Enhanced production of anthraquinones and phenolic compounds and biological activities in the cell suspension cultures of Polygonum multiflorum. Int J Mol Sci 17:1912

    Article  CAS  PubMed Central  Google Scholar 

  172. Perassolo M, Quevedo CV, Giulietti AM, Talou JR (2011) Stimulation of the proline cycle and anthraquinone accumulation in Rubia tinctorum cell suspension cultures in the presence of glutamate and two proline analogs. Plant Cell Tissue Organ Cult 106:153–159

    Article  CAS  Google Scholar 

  173. Baldi A, Dixit VK (2008) Yield enhancement strategies for artemisinin production by suspension cultures of Artemisia annua. Bioresour Technol 99:4609–4614

    Article  CAS  PubMed  Google Scholar 

  174. Sato F, Yamada Y (1984) High berberine-producing cultures of Coptis japonica cells. Phytochemistry 23:281–285

    Article  CAS  Google Scholar 

  175. Hara Y, Yoshioka T, Morimoto T, Fujita Y, Yamada Y (1988) Enhancement of berberine production in suspension cultures of Coptis japonica by gibberellic acid treatment. J Plant Physiol 133:12–15

    Article  CAS  Google Scholar 

  176. Matsubara K, Kitani S, Yoshioka T, Morimoto T, Fujita Y, Yamada Y (1989) High density culture of Coptis japonica cells increases berberine production. J Chem Technol Biotechnol 46:61–69

    Article  CAS  Google Scholar 

  177. Narasimhan S, Nair GM (2004) Release of berberine and its crystallization in liquid medium of cell suspension cultures of Coscinium fenestratum (Gaertn.) Colebr. Curr Sci 86:1369–1371

    CAS  Google Scholar 

  178. Suzuki M, Nakagawa K, Fukui H, Tabata M (1988) Alkaloid production in cell suspension cultures of Thalictrum flavum and T. dipterocarpum. Plant Cell Rep 7:26–29

    Article  CAS  PubMed  Google Scholar 

  179. Nakagawa K, Konagai A, Fukui H, Tabata M (1984) Release and crystallization of berberine in the liquid medium of Thalictrum minus cell suspension cultures. Plant Cell Rep 3:254–257

    Article  CAS  PubMed  Google Scholar 

  180. Nakagawa K, Fukui H, Tabata M (1986) Hormonal regulation of berberine production in cell suspension cultures of Thalictrum minus. Plant Cell Rep 5:69–71

    Article  CAS  PubMed  Google Scholar 

  181. Kobayashi Y, Fukui H, Tabata M (1988) Berberine production by batch and semi-continuous cultures of immobilized Thalictrum cells in an improved bioreactor. Plant Cell Rep 7:249–252

    Article  CAS  PubMed  Google Scholar 

  182. Kobayashi Y, Fukui H, Tabata M (1989) Effect of oxygen supply on berberine production in cell suspension cultures and immobilized cells of Thalictrum minus. Plant Cell Rep 8:255–258

    Article  CAS  PubMed  Google Scholar 

  183. Kobayashi Y, Fukui H, Tabata M (1991) Effect of carbon dioxide and ethylene on berberine production and cell browning in Thalictrum minus cell cultures. Plant Cell Rep 9:496–499

    Article  CAS  PubMed  Google Scholar 

  184. Gügler K, Funk C, Brodelius P (1988) Elicitor-induced tyrosine decarboxylase in berberine-synthesizing suspension cultures of Thalictrum rugosum. Eur J Biochem 170:661–666

    Article  PubMed  Google Scholar 

  185. Kim DI, Pedersen H, Chin CK (1990) Two stage cultures for the production of berberine in cell suspension cultures of Thalictrum rugosum. J Biotechnol 16:297–303

    Article  CAS  PubMed  Google Scholar 

  186. Kim DI, Pedersen H, Chin CK (1991) Cultivation of Thalictrum rugosum cell suspension in an improved airlift bioreactor: stimulatory effect of carbon dioxide and ethylene on alkaloid production. Biotechnol Bioeng 38:331–339

    Article  CAS  PubMed  Google Scholar 

  187. Roberts MF, Strack D, Wink M (2018) Biosynthesis of alkaloids and betalains. Annu Plant Rev 15:20–91

    Article  Google Scholar 

  188. Döring AS, Petersen M (2014) Production of caffeic, chlorogenic and rosmarinic acids in plants and suspension cultures of Glechoma hederacea. Phytochem Lett 10:cxi–vii

    Article  CAS  Google Scholar 

  189. Furuya T, Orihara Y, Tsuda Y (1990) Caffeine and theanine from cultured cells of Camellia sinensis. Phytochemistry 29:2539–2543

    Article  CAS  Google Scholar 

  190. Pan XW, Xu HH, Liu X, Gao X, Lu YT (2004) Improvement of growth and camptothecin yield by altering nitrogen source supply in cell suspension cultures of Camptotheca acuminata. Biotechnol Lett 26:1745–1748

    Article  CAS  PubMed  Google Scholar 

  191. Fulzele DP, Satdive RK, Pol BB (2001) Growth and production of camptothecin by cell suspension cultures of Nothapodytes foetida. Planta Med 67:150–152

    Article  CAS  PubMed  Google Scholar 

  192. Ravishankar GA, Sarma KS, Venkataraman LV, Kadyan AK (1988) Effect of nutritional stress on capsaicin production in immobilized cell cultures of Capsicum annuum. Curr Sci 57:381–383

    CAS  Google Scholar 

  193. Salgado-Garciglia R, Ochoa-Alejo N (1990) Increased capsaicin content in PFP-resistant cells of chili pepper (Capsicum annuum L.). Plant Cell Rep 8:617–620

    Article  CAS  PubMed  Google Scholar 

  194. Islek C, Ustun AS, Koc E (2014) The effects of cellulase on capsaicin production in freely suspended cells and immobilized cell cultures of Capsicum annuum L. Pak J Bot 46:1883–1487

    Google Scholar 

  195. Kehie M, Kumaria S, Tandon P (2012) Osmotic stress induced-capsaicin production in suspension cultures of Capsicum chinense Jacq. cv. Naga King Chili. Acta Physiol Plant 34:2039–2044

    Article  CAS  Google Scholar 

  196. Johnson TS, Ravishankar GA, Venkataraman LV (1991) Elicitation of capsaicin production in freely suspended cells and immobilized cell cultures of Capsicum frutescens Mill. Food Biotechnol 5:197–205

    Article  CAS  Google Scholar 

  197. Sudha G, Ravishankar GA (2003) Putrescine facilitated enhancement of capsaicin production in cell suspension cultures of Capsicum frutescens. J Plant Physiol 160:339–346

    Article  CAS  PubMed  Google Scholar 

  198. Gutiérrez-Carbajal MG, Monforte-González M, Miranda-Ham MD, Godoy-Hernández G, Vázquez-Flota F (2010) Induction of capsaicinoid synthesis in Capsicum chinense cell cultures by salicylic acid or methyl jasmonate. Biol Plant 54:430–434

    Article  CAS  Google Scholar 

  199. Aburjai T, Bernasconi S, Manzocchi LA, Pelizzoni F (1997) Effect of calcium and cell immobilization on the production of choleocalciferol and its derivatives by Solanum malacoxylon cell cultures. Phytochemistry 46:1015–1018

    Article  CAS  Google Scholar 

  200. Tam WJ, Constabel F, Kurz WG (1980) Codeine from cell suspension cultures of Papaver somniferum. Phytochemistry 19:486–487

    Article  CAS  Google Scholar 

  201. Yoshida K, Hayashi T, Sano K (1988) Colchicine precursors and the formation of alkaloids in suspension-cultured Colchicum autumnale. Phytochemistry 27:1375–1378

    Article  CAS  Google Scholar 

  202. Tsutomu N, Hitoshi M, Masao N, Hideko H, Kaisuke Y (1983) Production of cryptotanshinone and ferruginol in cultured cells of Salvia miltiorrhiza. Phytochemistry 22:721–722

    Article  Google Scholar 

  203. Kreis W, Reinhard E (1992) 12β-Hydroxylation of digitoxin by suspension-cultured Digitalis lanata cells: production of digoxin in 20-litre and 300-litre air-lift bioreactors. J Biotechnol 26:257–273

    Article  CAS  PubMed  Google Scholar 

  204. Pawar KD, Thengane SR (2009) Influence of hormones and medium components on expression of dipyranocoumarins in cell suspension cultures of Calophyllum inophyllumL. Process Biochem 44:916–922

    Article  CAS  Google Scholar 

  205. Kouamo K, Creche J, Chénieux JC, Rideau M, Viel C (1985) Alkaloid production by Ochrosia elliptica cell suspension cultures. J Plant Physiol 118:277–283

    Article  CAS  PubMed  Google Scholar 

  206. Jha S, Sahu NP, Sen J, Jha TB, Mahato SB (1991) Production of emetine and cephaeline from cell suspension and excised root cultures of Cephaelis ipecacuanha. Phytochemistry 30:3999–4003

    Article  CAS  Google Scholar 

  207. Mersinger R, Dornauer H, Reinhard E (1988) Formation of forskolin by suspension cultures of Coleus forskohlii1. Planta Med 54:200–204

    Article  CAS  PubMed  Google Scholar 

  208. Kitamura Y, Ikenaga T, Ooe Y, Hiraoka N, Mizukami H (1998) Induction of furanocoumarin biosynthesis in Glehnia littoralis cell suspension cultures by elicitor treatment. Phytochemistry 48:113–117

    Article  CAS  PubMed  Google Scholar 

  209. Park YG, Kim SJ, Kang YM, Jung HY, Prasad DT, Kim SW, Chung YG, Choi MS (2004) Production of ginkgolides and bilobalide from optimized the Ginkgo biloba cell culture. Biotechnol Bioprocess Eng 9:41–46

    Article  CAS  Google Scholar 

  210. 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 

  211. Kang SM, Min JY, Kim YD, Karigar CS, Kim SW, Goo GH, Choi MS (2009) Effect of biotic elicitors on the accumulation of bilobalide and ginkgolides in Ginkgo biloba cell cultures. J Biotechnol 139:84–88

    Article  CAS  PubMed  Google Scholar 

  212. Liu S, Zhong JJ (1997) Simultaneous production of ginseng saponin and polysaccharide by suspension cultures of Panax ginseng: nitrogen effects. Enzym Microb Technol 21:518–524

    Article  CAS  Google Scholar 

  213. Liu S, Zhong JJ (1998) Phosphate effect on production of ginseng saponin and polysaccharide by cell suspension cultures of Panax ginseng and Panax quinquefolium. Process Biochem 33:69–74

    Article  CAS  Google Scholar 

  214. Akalezi CO, Liu S, Li QS, Yu JT, Zhong JJ (1999) Combined effects of initial sucrose concentration and inoculum size on cell growth and ginseng saponin production by suspension cultures of Panax ginseng. Process Biochem 34:639–642

    Article  CAS  Google Scholar 

  215. Hu X, Neill SJ, Cai W, Tang Z (2003) Nitric oxide mediates elicitor-induced saponin synthesis in cell cultures of Panax ginseng. Funct Plant Biol 30:901–907

    Article  CAS  PubMed  Google Scholar 

  216. Zhang YH, Zhong JJ, Yu JT (1996) Effect of nitrogen source on cell growth and production of ginseng saponin and polysaccharide in suspension cultures of Panax notoginseng. Biotechnol Prog 12:567–571

    Article  CAS  Google Scholar 

  217. Zhang YH, Zhong JJ, Yu JT (1996) Enhancement of ginseng saponin production in suspension cultures of Panax notoginseng: manipulation of medium sucrose. J Biotechnol 51:49–56

    Article  CAS  Google Scholar 

  218. Zhong JJ, Chen F, Hu WW (1999) High density cultivation of Panax notoginseng cells in stirred bioreactors for the production of ginseng biomass and ginseng saponin. Process Biochem 35:491–496

    Article  Google Scholar 

  219. Zhong JJ, Zhu QX (1995) Effect of initial phosphate concentration on cell growth and ginsenoside saponin production by suspended cultures of Panax notoginseng. Appl Biochem Biotechnol 55:241–247

    Article  CAS  Google Scholar 

  220. Zhong JJ, Wang SJ (1998) Effects of nitrogen source on the production of ginseng saponin and polysaccharide by cell cultures of Panax quinquefolium. Process Biochem 33:671–675

    Article  CAS  Google Scholar 

  221. Zhong JJ, Bai Y, Wang SJ (1996) Effects of plant growth regulators on cell growth and ginsenoside saponin production by suspension cultures of Panax quinquefolium. J Biotechnol 45:227–234

    Article  CAS  Google Scholar 

  222. Kochan E, Chmiel A (2011) Dynamics of ginsenoside biosynthesis in suspension culture of Panax quinquefolium. Acta Physiol Plant 33:911–915

    Article  CAS  Google Scholar 

  223. Mathur M, Jain AK, Dass S, Ramawat KG (2007) Guggulsterone production in cell suspension cultures of Commiphora wightii grown in shake flask and bioreactors. Biotechnol Lett 29:979–982

    Article  CAS  PubMed  Google Scholar 

  224. Devi CS, Murugesh S, Srinivasan VM (2006) Gymnemic acid production in suspension cell cultures of Gymnema sylvestre. J Appl Sci 6:2263–2268

    Article  CAS  Google Scholar 

  225. Veerashree V, Anuradha CM, Kumar V (2012) Elicitor-enhanced production of gymnemic acid in cell suspension cultures of Gymnema sylvestre R. Br. Plant Cell Tissue Organ Cult 108:27–35

    Article  CAS  Google Scholar 

  226. Chodisetti B, Rao K, Gandi S, Giri A (2015) Gymnemic acid enhancement in the suspension cultures of Gymnema sylvestre by using the signaling molecules- methyl jasmonate and salicylic acid. In Vitro Cell Dev Biol Plant 51:88–92

    Article  CAS  Google Scholar 

  227. Yamada Y, Hashimoto T (1982) Production of tropane alkaloids in cultured cells of Hyoscyamus niger. Plant Cell Rep 1:101–103

    Article  CAS  PubMed  Google Scholar 

  228. Aly UI, El-Shabrawi HM, Hanafy M (2010) Impact of culture conditions on alkaloid production from undifferentiated cell suspension cultures of Egyptian henbane. Aust J Basic Appl Sci 4:4717–4725

    CAS  Google Scholar 

  229. Smith JI, Smart NJ, Kurz WG, Misawa M (1987) Stimulation of indole alkaloid production in cell suspension cultures of Catharanthus roseus by abscisic acid. Planta Med 53:470–474

    Article  CAS  PubMed  Google Scholar 

  230. Bais HP, Walker TS, McGrew JJ, Vivanco JM (2002) Factors affecting growth of cell suspension cultures of Hypericum perforatum L.(St. John’s wort) and production of hypericin. In Vitro Cell Dev Biol Plant 38:58–65

    Article  CAS  Google Scholar 

  231. Xu MJ, Dong JF, Zhu MY (2005) Nitric oxide mediates the fungal elicitor-induced hypericin production of Hypericum perforatum cell suspension cultures through a jasmonic-acid-dependent signal pathway. Plant Physiol 139:991–998

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  232. Pasqua G, Avato P, Monacelli B, Santamaria AR, Argentieri MP (2003) Metabolites in cell suspension cultures, calli, and in vitro regenerated organs of Hypericum perforatum cv. Topas. Plant Sci 165:977–982

    Article  CAS  Google Scholar 

  233. Sharafi E, Khayam Nekoei SM, Fotokian MH, Davoodi D, Hadavand Mirzaei H, Hasanloo T (2013) Improvement of hypericin and hyperforin production using zinc and iron nano-oxides as elicitors in cell suspension culture of St John’s wort (Hypericum perforatum L.). J Med Plants Byprod 2:177–184

    Google Scholar 

  234. Walker TS, Bais HP, Vivanco JM (2002) Jasmonic acid-induced hypericin production in cell suspension cultures of Hypericum perforatum L. (St. John’s wort). Phytochemistry 60:289–293

    Article  CAS  PubMed  Google Scholar 

  235. Murthy HN, Kim YS, Park SY, Paek KY (2014) Hypericins: biotechnological production from cell and organ cultures. Appl Microbiol Biotechnol 98:9187–9198

    Article  CAS  PubMed  Google Scholar 

  236. Cellarova E, Kimakova K, Daxnerova Z, Martonif P (1995) Hypericum perforatum (St. John’s wort): in vitro culture and production of hypericin and other secondary metabolites. In: Bajaj YPS (ed) Biotechnology in agriculture and forestry, medicinal and aromatic plants VIII, vol 33. Springer, Berlin

    Google Scholar 

  237. Kartnig T, Göbel I, Heydel B (1996) Production of hypericin, pseudohypericin and flavonoids in cell cultures of various Hypericum species and their chemotypes. Planta Med 62:51–53

    Article  CAS  PubMed  Google Scholar 

  238. Fu CX, Cheng LQ, Lv XF, Zhao DX, Ma F (2006) Methyl jasmonate stimulates jaceosidin and hispidulin production in cell cultures of Saussurea medusa. Appl Biochem Biotechnol 134:89–96

    Article  CAS  PubMed  Google Scholar 

  239. Yu ZZ, Fu CX, Han YS, Li YX, Zhao DX (2006) Salicylic acid enhances jaceosidin and syringin production in cell cultures of Saussurea medusa. Biotechnol Lett 28:1027–1031

    Article  CAS  PubMed  Google Scholar 

  240. Yogananth N, Bhakyaraj R, Ali MS, Muthezhilan R (2019) Effect of yeast elicitor on the enhancement of kaempferol from in vivo and in vitro callus cultures of Dregea volubilis Benth. Asian J Biol Sci 12:278–283

    Article  Google Scholar 

  241. Yamamoto H, Zhao P, Yazaki K, Inoue K (2002) Regulation of lithospermic acid B and shikonin production in Lithospermum erythrorhizon cell suspension cultures. Chem Pharm Bull 50:1086–1090

    Article  CAS  Google Scholar 

  242. Wiktorowska E, Długosz M, Janiszowska W (2010) Significant enhancement of oleanolic acid accumulation by biotic elicitors in cell suspension cultures of Calendula officinalis L. Enzym Microb Technol 46:14–20

    Article  CAS  Google Scholar 

  243. Gadzovska S, Maury S, Delaunay A, Spasenoski M, Joseph C, Hagège D (2007) Jasmonic acid elicitation of Hypericum perforatum L. cell suspensions and effects on the production of phenylpropanoids and naphtodianthrones. Plant Cell Tissue Organ Cult 89:1–13

    Article  CAS  Google Scholar 

  244. Shinde AN, Malpathak N, Fulzele DP (2009) Studied enhancement strategies for phytoestrogens production in shake flasks by suspension culture of Psoralea corylifolia. Bioresour Technol 100:1833–1839

    Article  CAS  PubMed  Google Scholar 

  245. Nahálka J, Blanárik P, Gemeiner P, Matúsǒvá E, Partlová I (1996) Production of plumbagin by cell suspension cultures of Drosophyllum lusitanicum Link. J Biotechnol 49:153–161

    Article  Google Scholar 

  246. Beigmohammadi M, Movafeghi A, Sharafi A, Jafari S, Danafar H (2019) Cell suspension culture of Plumbago europaea L. towards production of plumbagin. Iran J Biotechnol 17:46–54

    Article  Google Scholar 

  247. Komaraiah P, Kishor PK, Ramakrishna SV (2001) Production of plumbagin from cell cultures of Plumbago rosea L. Biotechnol Lett 23:1269–1272

    Article  CAS  Google Scholar 

  248. Komaraiah P, Amrutha RN, Kishor PK, Ramakrishna SV (2002) Elicitor enhanced production of plumbagin in suspension cultures of Plumbago rosea L. Enzym Microb Technol 31:634–639

    Article  CAS  Google Scholar 

  249. Chattopadhyay S, Srivastava AK, Bhojwani SS, Bisaria VS (2002) Production of podophyllotoxin by plant cell cultures of Podophyllum hexandrum in bioreactor. J Biosci Bioeng 93:215–220

    Article  CAS  PubMed  Google Scholar 

  250. Chattopadhyay S, Srivastava AK, Bisaria VS (2002) Optimization of culture parameters for production of podophyllotoxin in suspension culture of Podophyllum hexandrum. Appl Biochem Biotechnol 102:381–393

    Article  PubMed  Google Scholar 

  251. Majumder A (2012) Influence of an indirect precursor on podophyllotoxin accumulation in cell suspension cultures of Podophyllum hexandrum. Plant Tissue Cult Biotechnol 22:171–177

    Article  Google Scholar 

  252. Anbazhagan VR, Ahn CH, Harada E, Kim YS, Choi YE (2008) Podophyllotoxin production via cell and adventitious root cultures of Podophyllum peltatum. In Vitro Cell Dev Biol Plant 44:494–501

    Article  CAS  Google Scholar 

  253. Ratnadewi D (2017) Alkaloids in plant cell cultures. In: Georgiev V, Pavlov A (eds) Alkaloids: alternatives in synthesis, modification and application. IntechOpen, https://doi.org/10.5772/66288

  254. Ratnadewi D (2013) Enhanced production level of quinine in cell suspension culture of Cinchona Ledgeriana Moens by Paclobutrazol. Biotropia 20:10–18

    Article  Google Scholar 

  255. Yamamoto O, Yamada Y (1986) Production of reserpine and its optimization in cultured Rauwolfia serpentina Benth. cells. Plant Cell Rep 5:50–53

    Article  CAS  PubMed  Google Scholar 

  256. Dubrovina AS, Kiselev KV (2012) Effect of long-term cultivation on resveratrol accumulation in a high-producing cell culture of Vitis amurensis. Acta Physiol Plant 34:1101–1106

    Article  CAS  Google Scholar 

  257. Laura R, Franceschetti M, Ferri M, Tassoni A, Bagni N (2007) Resveratrol production in Vitis vinifera cell suspensions treated with several elicitors. Caryologia 60:169–171

    Article  Google Scholar 

  258. Vuong TV, Franco C, Zhang W (2014) Treatment strategies for high resveratrol induction in Vitis vinifera L. cell suspension culture. Biotechnol Rep 1:15–21

    Article  Google Scholar 

  259. Schripsema J, Ramos-Valdivia A, Verpoorte R (1999) Robustaquinones, novel anthraquinones from an elicited Cinchona robusta suspension culture. Phytochemistry 51:55–60

    Article  CAS  Google Scholar 

  260. Kim HK, Oh SR, Lee HK, Huh H (2001) Benzothiadiazole enhances the elicitation of rosmarinic acid production in a suspension culture of Agastache rugosa O. Kuntze. Biotechnol Lett 23:55–60

    Article  Google Scholar 

  261. Su WW, Lei F (1993) Rosmarinic acid production in perfused Anchusa officinalis culture: effect of inoculum size. Biotechnol Lett 15:1035–1038

    Article  CAS  Google Scholar 

  262. Vogelsang K, Schneider B, Petersen M (2006) Production of rosmarinic acid and a new rosmarinic acid 3′-O-β-d-glucoside in suspension cultures of the hornwort Anthoceros agrestis Paton. Planta 223:369–373

    Article  CAS  PubMed  Google Scholar 

  263. Razzaque A, Ellis BE (1977) Rosmarinic acid production in Coleus cell cultures. Planta 137:287–291

    Article  CAS  PubMed  Google Scholar 

  264. Ulbrich B, Wiesner W, Arens H (1985) Large-scale production of rosmarinic acid from plant cell cultures of Coleus blumei Benth. In: Neumann KH, Barz W, Reinhard E (eds) Primary and secondary metabolism of plant cell cultures, proceedings in life sciences. Springer, Berlin/Heidelberg

    Google Scholar 

  265. Gertlowski C, Petersen M (1993) Influence of the carbon source on growth and rosmarinic acid production in suspension cultures of Coleus blumei. Plant Cell Tissue Organ Cult 34:183–190

    Article  CAS  Google Scholar 

  266. Weremczuk-Jeżyna I, Grzegorczyk-Karolak I, Frydrych B, Hnatuszko-Konka K, Gerszberg A, Wysokińska H (2017) Rosmarinic acid accumulation and antioxidant potential of Dracocephalum moldavica L. cell suspension culture. Notulae Botanicae Horti Agrobotanici Cluj-Napoca 45:215–219

    Article  CAS  Google Scholar 

  267. Ilieva M, Pavlov A (1997) Rosmarinic acid production by Lavandula vera MM cell-suspension culture. Appl Microbiol Biotechnol 47:683–688

    Article  CAS  Google Scholar 

  268. Pavlov AI, Ilieva MP, Panchev IN (2000) Nutrient medium optimization for rosmarinic acid production by Lavandula vera MM cell suspension. Biotechnol Prog 16:668–670

    Article  CAS  PubMed  Google Scholar 

  269. Georgiev M, Pavlov A, Ilieva M (2004) Rosmarinic acid production by Lavandula vera MM cell suspension: the effect of temperature. Biotechnol Lett 26:855–856

    Article  CAS  PubMed  Google Scholar 

  270. Pavlov AI, Georgiev MI, Panchev IN, Ilieva MP (2005) Optimization of rosmarinic acid production by Lavandula vera MM plant cell suspension in a laboratory bioreactor. Biotechnol Prog 21:394–396

    Article  CAS  PubMed  Google Scholar 

  271. Georgiev MI, Kuzeva SL, Pavlov AI, Kovacheva EG, Ilieva MP (2007) Elicitation of rosmarinic acid by Lavandula vera MM cell suspension culture with abiotic elicitors. World J Microbiol Biotechnol 23:301–304

    Article  CAS  Google Scholar 

  272. Ogata A, Tsuruga A, Matsuno M, Mizukami H (2004) Elicitor-induced rosmarinic acid biosynthesis in Lithospermum erythrorhizon cell suspension cultures: activities of rosmarinic acid synthase and the final two cytochrome P450-catalyzed hydroxylations. Plant Biotechnol 21:393–396

    Article  CAS  Google Scholar 

  273. Mizukami H, Tabira Y, Ellis BE (1993) Methyl jasmonate-induced rosmarinic acid biosynthesis in Lithospermum erythrorhizon cell suspension cultures. Plant Cell Rep 12:706–709

    Article  CAS  PubMed  Google Scholar 

  274. 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 108:73–81

    Article  CAS  Google Scholar 

  275. Kintzios S, Makri O, Panagiotopoulos E, Scapeti M (2003) In vitro rosmarinic acid accumulation in sweet basil (Ocimum basilicum L.). Biotechnol Lett 25:405–408

    Article  CAS  PubMed  Google Scholar 

  276. Hakkim FL, Kalyani S, Essa M, Girija S, Song H (2011) Production of rosmarinic acid in Ocimum sanctum (L.) cell suspension cultures by the influence of growth regulators. Int J Biol Med Res 2:1158–1161

    Google Scholar 

  277. Sumaryono W, Proksch P, Hartmann T, Nimtz M, Wray V (1991) Induction of rosmarinic acid accumulation in cell suspension cultures of Orthosiphon aristatus after treatment with yeast extract. Phytochemistry 30:3267–3271

    Article  CAS  Google Scholar 

  278. Hippolyte I, Marin B, Baccou JC, Jonard R (1992) Growth and rosmarinic acid production in cell suspension cultures of Salvia officinalis L. Plant Cell Rep 11:109–112

    Article  CAS  PubMed  Google Scholar 

  279. Sahraroo A, Mirjalili MH, Corchete P, Babalar M, Moghadam MR (2016) Establishment and characterization of a Satureja khuzistanica Jamzad (Lamiaceae) cell suspension culture: a new in vitro source of rosmarinic acid. Cytotechnology 68:1415–1424

    Article  CAS  PubMed  Google Scholar 

  280. Françoise B, Hossein S, Halimeh H, Zahra NF (2007) Growth optimization of Zataria multiflora Boiss. tissue cultures and rosmarinic acid production improvement. Pak J Biol Sci 10:3395–3399

    Article  PubMed  Google Scholar 

  281. Eilert U, Kurz WG, Constabel F (1985) Stimulation of sanguinarine accumulation in Papaver somniferum cell cultures by fungal elicitors. J Plant Physiol 119:65–76

    Article  CAS  Google Scholar 

  282. Wilhelm R, Zenk MH (1997) Biotransformation of thebaine by cell cultures of Papaver somniferum and Mahonia nervosa. Phytochemistry 46:701–708

    Article  CAS  Google Scholar 

  283. Holková I, Bezáková L, Bilka F, Balažová A, Vanko M, Blanáriková V (2010) Involvement of lipoxygenase in elicitor-stimulated sanguinarine accumulation in Papaver somniferum suspension cultures. Plant Physiol Biochem 48:887–892

    Article  CAS  PubMed  Google Scholar 

  284. Cline SD, McHale RJ, Coscia CJ (1993) Differential enhancement of benzophenanthridine alkaloid content in cell suspension cultures of Sanguinaria canadensis under conditions of combined hormonal deprivation and fungal elicitation. J Nat Prod 56:1219–1228

    Article  CAS  PubMed  Google Scholar 

  285. Mahady GB, Schilling AB, Beecher CW (1993) Sanguinaria canadensis L.(Sanguinarius): in vitro culture and the production of benzophenanthridine alkaloids. In: Bajaj YPS (ed) Medicinal and aromatic plants V, Biotechnology in agriculture and forestry, vol 24. Springer, Berlin/Heidelberg

    Chapter  Google Scholar 

  286. Furuya T, Yoshikawa T, Orihara Y, Oda H (1983) Saponin production in cell suspension cultures of Panax ginseng. Planta Med 48:83–87

    Article  CAS  PubMed  Google Scholar 

  287. Lu M, Wong H, Teng W (2001) Effects of elicitation on the production of saponin in cell culture of Panax ginseng. Plant Cell Rep 20:674–677

    Article  CAS  Google Scholar 

  288. Wu JY, Wong K, Ho KP, Zhou LG (2005) Enhancement of saponin production in Panax ginseng cell culture by osmotic stress and nutrient feeding. Enzym Microb Technol 36:133–138

    Article  CAS  Google Scholar 

  289. Thanh NT, Murthy HN, Yu KW, Jeong CS, Hahn EJ, Paek KY (2006) Effect of oxygen supply on cell growth and saponin production in bioreactor cultures of Panax ginseng. J Plant Physiol 163:1337–1341

    Article  CAS  PubMed  Google Scholar 

  290. Merillon JM, Rideau M, Chenieux JC (1984) Influence of sucrose on levels of ajmalicine, serpentine, and tryptamine in Catharanthus roseus cells in vitro. Planta Med 50:497–501

    Article  CAS  PubMed  Google Scholar 

  291. Fu XQ, Lu DW (1999) Stimulation of shikonin production by combined fungal elicitation and in situ extraction in suspension cultures of Arnebia euchroma. Enzym Microb Technol 24:243–246

    Article  CAS  Google Scholar 

  292. Ge F, Yuan X, Wang X, Zhao B, Wang Y (2006) Cell growth and shikonin production of Arnebia euchroma in a periodically submerged airlift bioreactor. Biotechnol Lett 28:525–529

    Article  CAS  PubMed  Google Scholar 

  293. Yazaki K, Fukui H, Kikuma M, Tabata M (1987) Regulation of shikonin production by glutamine in Lithospermum erythrorhizon cell cultures. Plant Cell Rep 6:131–134

    CAS  PubMed  Google Scholar 

  294. Fujita Y (1988) Shikonin: production by plant (Lithospermum erythrorhizon) cell cultures. In: Bajaj YPS (ed) Medicinal and aromatic plants, 4. Springer, Berlin/Heidelberg

    Google Scholar 

  295. Kim DJ, Chang HN (1990) Enhanced shikonin production from Lithospermum erythrorhizon by in situ extraction and calcium alginate immobilization. Biotechnol Bioeng 36:460–466

    Article  CAS  PubMed  Google Scholar 

  296. Kim DJ, Chang HN (1990) Increased shikonin production in Lithospermum erythrorhizon suspension cultures with in situ extraction and fungal cell treatment (elicitor). Biotechnol Lett 12:443–446

    Article  CAS  Google Scholar 

  297. Srinivasan V, Ryu DD (1993) Improvement of shikonin productivity in Lithospermum erythrorhizon cell culture by alternating carbon and nitrogen feeding strategy. Biotechnol Bioeng 42:793–799

    Article  CAS  PubMed  Google Scholar 

  298. Tani M, Takeda K, Yazaki K, Tabata M (1993) Effects of oligogalacturonides on biosynthesis of shikonin in Lithospermum cell cultures. Phytochemistry 34:1285–1290

    Article  CAS  Google Scholar 

  299. Yazaki K, Matsuoka H, Ujihara T, Sato F (1999) Shikonin biosynthesis in Lithospermum erythrorhizon. Plant Biotechnol 16:335–342

    Article  CAS  Google Scholar 

  300. Malik S, Bhushan S, Sharma M, Ahuja PS (2016) Biotechnological approaches to the production of shikonins: a critical review with recent updates. Crit Rev Biotechnol 36:327–340

    Article  CAS  PubMed  Google Scholar 

  301. Liu Z, Qi JL, Chen L, Zhang MS, Wang XQ, Pang YJ, Yang YH (2006) Effect of light on gene expression and shikonin formation in cultured Onosma paniculatum cells. Plant Cell Tissue Organ Cult 84:39–46

    Article  CAS  Google Scholar 

  302. Wu SJ, Qi JL, Zhang WJ, Liu SH, Xiao FH, Zhang MS, Xu GH, Zhao WG, Shi MW, Pang YJ, Shen HG (2008) Nitric oxide regulates shikonin formation in suspension-cultured Onosma paniculatum cells. Plant Cell Physiol 50:118–128

    Article  CAS  PubMed  Google Scholar 

  303. Ashtiani SR, Hasanloo T, Bihamta MR (2010) Enhanced production of silymarin by Ag+ elicitor in cell suspension cultures of Silybum marianum. Pharm Biol 48:708–715

    Article  CAS  PubMed  Google Scholar 

  304. Belchi-Navarro S, Pedreño MA, Corchete P (2011) Methyl jasmonate increases silymarin production in Silybum marianum (L.) Gaernt cell cultures treated with β-cyclodextrins. Biotechnol Lett 33:179–184

    Article  CAS  PubMed  Google Scholar 

  305. Firouzi A, Mohammadi SA, Khosrowchahli M, Movafeghi A, Hasanloo T (2013) Enhancement of silymarin production in cell culture of Silybum marianum (L) Gaertn by elicitation and precursor feeding. J Herbs Spices Med Plant 19:262–274

    Article  CAS  Google Scholar 

  306. Nigra HM, Alvarez MA, Giulietti AM (1990) Effect of carbon and nitrogen sources on growth and solasodine production in batch suspension cultures of Solanum elaeagnifolium Cav. Plant Cell Tissue Organ Cult 21:55–60

    Article  CAS  Google Scholar 

  307. Quadri LE, Giulietti AM (1993) Effect of elicitation on the accumulation of solasodine by immobilized cells of Solanum elaeagnifolium Cav. Enzym Microb Technol 15:1074–1077

    Article  CAS  Google Scholar 

  308. Alvarez MA, Nigra HM, Giulietti AM (1993) Solasodine production by Solanum elaeagnifolium Cav. in vitro cultures: influence of plant growth regulators, age and inoculum size. Large-scale production. Nat Prod Lett 3:9–19

    Article  Google Scholar 

  309. Loc NH (2011) Solasodine production from cell culture of Solanum hainanense Hance. Biotechnol Bioprocess Eng 16:581–586

    Article  CAS  Google Scholar 

  310. Barnabas NJ, David SB (1988) Solasodine production by immobilized cells and suspension cultures of Solanum surattense. Biotechnol Lett 10:593–596

    Article  CAS  Google Scholar 

  311. Malpathak NP, David SB (1992) Stimulation of solasodine production by combining fungal elicitors and immobilized cell suspension cultures of Solanum surattense Burm. Biotechnol Lett 14:965–968

    Article  CAS  Google Scholar 

  312. Villarreal ML, Arias C, Feria-Velasco A, Ramírez OT, Quintero R (1997) Cell suspension culture of Solanum chrysotrichum (Schldl.)-A plant producing an antifungal spirostanol saponin. Plant Cell Tissue Organ Cult 50:39–44

    Article  CAS  Google Scholar 

  313. Gupta P, Sharma S, Saxena S (2014) Effect of salts (NaCl and Na2CO3) on callus and suspension culture of Stevia rebaudiana for steviol glycoside production. Appl Biochem Biotechnol 172:2894–2906

    Article  CAS  PubMed  Google Scholar 

  314. Gupta P, Sharma S, Saxena S (2015) Biomass yield and steviol glycoside production in callus and suspension culture of Stevia rebaudiana treated with proline and polyethylene glycol. Appl Biochem Biotechnol 176:863–874

    Article  CAS  PubMed  Google Scholar 

  315. Mathur S, Shekhawat GS (2013) Establishment and characterization of Stevia rebaudiana (Bertoni) cell suspension culture: an in vitro approach for production of stevioside. Acta Physiol Plant 35:931–939

    Article  CAS  Google Scholar 

  316. 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 Microb Biotechnol 87:137–144

    Article  CAS  Google Scholar 

  317. Onrubia M, Moyano E, Bonfill M et al (2012) Coronatine, a more powerful elicitor for inducing taxane biosynthesis in Taxus media cell cultures than methyl jasmonate. J Plant Physiol 170:211–219

    Article  CAS  PubMed  Google Scholar 

  318. Wickremesinhe ER, Arteca RN (1994) Taxus cell suspension cultures: optimizing growth and production of taxol. J Plant Physiol 144:183–188

    Article  CAS  Google Scholar 

  319. Jha S, Jha TB (1995) A fast-growing cell line of Taxus baccata L. (Himalayan yew) as a potential source of taxol precursor. Curr Sci 69:971–973

    CAS  Google Scholar 

  320. Malik S, Cusidó RM, Mirjalili MH, Moyano E, Palazón J, Bonfill M (2011) Production of the anticancer drug taxol in Taxus baccata suspension cultures: a review. Process Biochem 46:23–34

    Article  CAS  Google Scholar 

  321. Hezari M, Ketchum RE, Gibson DM, Croteau R (1997) Taxol production and taxadiene synthase activity in Taxus canadensis cell suspension cultures. Arch Biochem Biophys 337:185–190

    Article  CAS  PubMed  Google Scholar 

  322. Zhang CH, Fevereiro PS, He G, Chen Z (2007) Enhanced paclitaxel productivity and release capacity of Taxus chinensis cell suspension cultures adapted to chitosan. Plant Sci 172:158–163

    Article  CAS  Google Scholar 

  323. Seki M, Ohzora C, Takeda M, Furusaki S (1997) Taxol (paclitaxel) production using free and immobilized cells of Taxus cuspidata. Biotechnol Bioeng 53:214–219

    Article  CAS  PubMed  Google Scholar 

  324. Jha S, Sanyal D, Ghosh B, Jha TB (1998) Improved taxol yield in cell suspension culture of Taxus wallichiana (Himalayan yew). Planta Med 64:270–272

    Article  CAS  PubMed  Google Scholar 

  325. Ciddi V (2006) Withaferin A from cell cultures of Withania somnifera. Indian J Pharm Sci 68:490–492

    Article  CAS  Google Scholar 

  326. Nagella P, Murthy HN (2010) Establishment of cell suspension cultures of Withania somnifera for the production of withanolide A. Bioresour Technol 101:6735–6739

    Article  CAS  PubMed  Google Scholar 

  327. Sivanandhan G, Dev GK, Jeyaraj M, Rajesh M, Muthuselvam M, Selvaraj N, Manickavasagam M, Ganapathi A (2013) A promising approach on biomass accumulation and withanolides production in cell suspension culture of Withania somnifera (L.) Dunal. Protoplasma 250:885–898

    Article  CAS  PubMed  Google Scholar 

  328. Tocci N, Ferrari F, Santamaria AR, Valletta A, Rovardi I, Pasqua G (2010) Chitosan enhances xanthone production in Hypericum perforatum subsp. angustifolium cell cultures. Nat Prod Res 24:286–293

    Article  CAS  PubMed  Google Scholar 

  329. Holden RR, Holden MA, Yeoman MM (1988) The effects of fungal elicitation on secondary metabolism in cell cultures of Capsicum frutescens. In: Robins RJ, Rhodes MJC (eds) Manipulating secondary metabolism in culture. Cambridge University Press, Cambridge, UK

    Google Scholar 

  330. Bais HP, Walker TS, Schweizer HP, Vivanco JM (2002) Root specific elicitation and antimicrobial activity of rosmarinic acid in hairy root cultures of Ocimum basilicum. Plant Physiol Biochem 40:983–995

    Article  CAS  Google Scholar 

  331. Lee YS, Ju HK, Kim YJ, Lim TG, Uddin MR, Kim YB, Baek JH, Kwon SW, Lee KW, Seo HS, Park SU, Yang TJ (2013) Enhancement of anti-inflammatory activity of Aloe vera adventitious root extracts through the alternation of primary and secondary metabolites via salicylic acid elicitation. PLoS One 8:1–13

    Google Scholar 

  332. Keil M, Hartle B, Guilaume A, Psiorz M (2000) Production of amarogentin in root cultures of Swertia chirata. Planta Med 66:452–457

    Article  CAS  PubMed  Google Scholar 

  333. Praveen N, Manohar SH, Naik PM, Nayeem A, Jeong JH, Murthy HN (2009) Production of andrographolide from adventitious root cultures of Andrographis paniculata. Curr Sci 96:694–697

    CAS  Google Scholar 

  334. Baque MA, Hahn EJ, Paek KY (2010) Growth, secondary metabolite production and antioxidant enzyme response of Morinda citrifolia adventitious root as affected by auxin and cytokinin. Plant Biotechnol Rep 4:109–116

    Article  Google Scholar 

  335. Cui HY, Baque MA, Lee EJ, Paek KY (2013) Scale-up of adventitious root cultures of Echinacea angustifolia in a pilot-scale bioreactor for the production of biomass and caffeic acid derivatives. Plant Biotechnol Rep 7:297–308

    Article  Google Scholar 

  336. Martin KP, Zhang CL, Hembrom ME, Slater A, Madassery J (2008) Adventitious root induction in Ophiorrhiza prostrata: a tool for the production of camptothecin (an anticancer drug) and rapid propagation. Plant Biotechnol Rep 2:163–169

    Article  Google Scholar 

  337. Ghosh B, Mukherjee S, Jha TB, Jha S (2002) Enhanced colchicine production in root cultures of Gloriosa superba by direct and indirect precursors of the biosynthetic pathway. Biotechnol Lett 24:231–234

    Article  CAS  Google Scholar 

  338. Ghosh S, Ghosh B, Jha S (2006) Aluminium chloride enhances colchicine production in root cultures of Gloriosa superba. Biotechnol Lett 28:497–503

    Article  CAS  PubMed  Google Scholar 

  339. Ghosh S, Ghosh B, Jha S (2015) Role of exogenous carbohydrate and amino acid sources on biomass and colchicine production in nontransformed root cultures of Gloriosa superba. Plant Tissue Cult Biotechnol 25:247–256

    Article  Google Scholar 

  340. Zaker A, Sykora C, Gössnitzer F, Abrishamchi P, Asili J, Mousavi SH, Wawrosch C (2015) Effects of some elicitors on tanshinone production in adventitious root cultures of Perovskia abrotanoides Karel. Ind Crop Prod 67:97–102

    Article  CAS  Google Scholar 

  341. Cho JS, Kim JY, Kim IH, Kim DI (2003) Effect of polysaccharide elicitors on the production of decursinol angelate in Angelica gigas Nakai root cultures. Biotechnol Bioprocess Eng 8:158–161

    Article  CAS  Google Scholar 

  342. Rhee HS, Cho HY, Son SY, Yoon SY, Park JM (2010) Enhanced accumulation of decursin and decursinol angelate in root cultures and intact roots of Angelica gigas Nakai following elicitation. Plant Cell Tissue Organ Cult 101:295–302

    Article  CAS  Google Scholar 

  343. Yu KW, Gao WY, Hahn EJ, Paek KY (2001) Effects of macro elements and nitrogen source on adventitious root growth and ginsenoside production in ginseng (Panax ginseng CA Meyer). J Plant Biol 44:179–184

    Article  CAS  Google Scholar 

  344. Kim YS, Hahn EJ, Murthy HN, Paek KY (2004) Adventitious root growth and ginsenoside accumulation in Panax ginseng cultures as affected by methyl jasmonate. Biotechnol Lett 26:1619–1622

    Article  CAS  PubMed  Google Scholar 

  345. Yin S, Zhang Y, Gao W, Wang J, Man S, Liu H (2014) Effect of nitrogen, sucrose and phosphate concentration on biomass and metabolites accumulation in adventitious root culture of Glycyrrhiza uralensis Fisch. Acta Physiol Plant 36:915–921

    Article  CAS  Google Scholar 

  346. Hashimoto T, Yukimune Y, Yamada Y (1986) Tropane alkaloid production in Hyoscyamus root cultures. J Plant Physiol 124:61–75

    Article  CAS  Google Scholar 

  347. Kusakari K, Yokoyama M, Inomata S (2000) Enhanced production of saikosaponins by root culture of Bupleurum falcatum L. using two-step control of sugar concentration. Plant Cell Rep 19:1115–1120

    Article  CAS  PubMed  Google Scholar 

  348. Kusakari K, Yokoyma M, Inomata S, Gozu Y, Katagiri C, Sugimoto Y (2012) Large-scale production of saikosaponins through root culturing of Bupleurum falcatum L. using modified airlift reactors. J Biosci Bioeng 113:99–105

    Article  CAS  PubMed  Google Scholar 

  349. Kim JH, Chang EJ, Oh HI (2005) Saponin production in submerged adventitious root culture of Panax ginseng as affected by culture conditions and elicitors. Asia Pacific J Mol Biol Biotechnol 13:87–91

    Google Scholar 

  350. Kawamura M, Shigeoka T, Akita M, Kobayashi Y (1996) Newly developed apparatus for inoculating plant organ into large-scale fermentor. J Ferment Bioeng 82:618–619

    Article  CAS  Google Scholar 

  351. Reis RV, Borges APPL, Chierrito TPC, Souto ERD, Souza LMD, Iacomini M, Oliveira AJBD, Goncalves RAC (2011) Establishment of adventitious root culture of Stevia rebaudiana Bertoni in roller bottle system. Plant Cell Tissue Organ Cult 106:329–335

    Article  Google Scholar 

  352. Strauss A, Spengel SM, Schaffner W (1995) Saponins from root cultures of Phytolacca acinosa. Phytochemistry 38:861–465

    Article  CAS  Google Scholar 

  353. Wasnik NG, Muthusamy M, Chellappan S, Vaidhyanathan V, Pulla R, Senthil K, Yang DC (2009) Establishment of in vitro root cultures and analysis of secondary metabolites in Indian Ginseng-Withania somnifera. Korean J Plant Res 22:584–591

    Google Scholar 

  354. Praveen N, Murthy HN (2010) Production of withanolide-A from adventitious root cultures of Withania somnifera. Acta Physiol Plant 32:1017–1022

    Article  CAS  Google Scholar 

  355. Sivanandhan G, Arun M, Mayavan S, Rajesh M, Mariashibu TS, Manickavasagam M, Selvaraj N, Ganapathi A (2012) Chitosan enhances withanolides production in adventitious root cultures of Withania somnifera (L.) Dunal. Ind Crop Prod 37:124–129

    Article  CAS  Google Scholar 

  356. Cui L, Wang ZY, Zhou XH (2012) Optimization of elicitors and precursors to enhance valtrate production in adventitious roots of Valeriana amurensis Smir. ex Kom. Plant Cell Tissue Organ Cult 108:411–420

    Article  CAS  Google Scholar 

  357. Ekhteraei Tousi S, Radjabian T, Ebrahimzadeh HA, Niknam V (2012) Enhanced production of valerenic acids and valepotriates by in vitro cultures of Valeriana officinalis L. Int J Plant Prod 4:209–222

    Google Scholar 

  358. Hong ML, Bhatt AR, Ping NS, Keng CL (2012) Detection of elicitation effect on Hyoscyamus niger L. root cultures for the root growth and production of tropane alkaloids. Rom Biotech Lett 17:7340–7351

    CAS  Google Scholar 

  359. Yu KW, Gao W, Hahn EJ, Paek KY (2002) Jasmonic acid improves ginsenoside accumulation in adventitious root culture of Panax ginseng C.A. Meyer. Biochem Eng J 11:211–215

    Article  CAS  Google Scholar 

  360. Kang SM, Jung HY, Kang YM, Yun DJ, Bahk JD, Yang JK, Choi MS (2004) Effects of methyl jasmonate and salicylic acid on the production of tropane alkaloids and the expression of PMT and H6H in adventitious root cultures of Scopolia parviflora. Plant Sci 166:745–751

    Article  CAS  Google Scholar 

  361. Min JY, Jung HY, Kang SM, Kim YD, Kang YM, Park DJ, Prasad DT, Choi MS (2007) Production of tropane alkaloids by small-scale bubble column bioreactor cultures of Scopolia parviflora adventitious roots. Bioresour Technol 98:1748–1753

    Article  CAS  PubMed  Google Scholar 

  362. Ho TT, Lee JD, Jeong CS, Paek KY, Park SY (2018) Improvement of biosynthesis and accumulation of bioactive compounds by elicitation in adventitious root cultures of Polygonum multiflorum. Appl Microbiol Biotechnol 102:199–209

    Article  CAS  PubMed  Google Scholar 

  363. Gaid M, Haas P, Beuerle T, Scholl S, Beerhues L (2016) Hyperforin production in Hypericum perforatum root cultures. J Biotechnol 222:47–55

    Article  CAS  PubMed  Google Scholar 

  364. Murthy HN, Hahn EJ, Paek KY (2008) Adventitious roots and secondary metabolism. Chin J Biotechnol 24:711–716

    Article  CAS  Google Scholar 

  365. Choi SM, Son SH, Yun SR, Kown OW, Seon JH, Paek KY (2000) Pilot scale culture of adventitious roots of ginseng in a bioreactor system. Plant Cell Tissue Organ Cult 62:187–193

    Article  CAS  Google Scholar 

  366. Hahn EJ, Kim YS, Yu KW, Jeong CS, Paek KY (2003) Adventitious root cultures of Panax ginseng C. A. Meyer and ginsenoside production through large scale bioreactor systems. J Plant Biotechnol 5:1–6

    Google Scholar 

  367. Baque MA, Moh SH, Lee EJ, Zhong JJ, Paek KY (2012) Production of biomass and useful compounds from adventitious roots of high-value added medicinal plants using bioreactor. Biotechnol Adv 30:1255–1267

    Article  CAS  PubMed  Google Scholar 

  368. Lulu T, Park SY, Ibrahim R, Paek KY (2015) Production of biomass and bioactive compounds from adventitious roots by optimization of culturing conditions of Eurycoma longifolia in balloon-type bubble bioreactor system. J Biosci Bioeng 119:712–717

    Article  CAS  PubMed  Google Scholar 

  369. Ho TT, Lee KJ, Lee JD, Bhushan S, Paek KY, Park SY (2017) Adventitious root culture of Polygonum multiflorum for phenolic compounds and its pilot-scale production in 500 L-tank. Plant Cell Tissue Organ Cult 130:167–181

    Article  CAS  Google Scholar 

  370. Chaichana N, Dheeranupattana S, Jatisatienr A, Wangkarn S, Pyne SG, Mungkornnasawakul P, Sangthong P, Sastraruji T (2012) Response of stemona alkaloid production in Stemona sp. to chitosan and yeast extract elicitors. Curr Res J Biol Sci 4:449–454

    CAS  Google Scholar 

  371. Rawat JM, Rawat B, Agnihotri RK, Chandra A, Nautiyal S (2013) In vitro propagation, genetic and secondary metabolite analysis of Aconitum violaceum Jacq.: a threatened medicinal herb. Acta Physiol Plant 35:2589–2599

    Article  CAS  Google Scholar 

  372. Satdive RK, Fulzele DP, Eapen S (2003) Studies on production of ajmalicine in shake flasks by multiple shoot cultures of Catharanthus roseus. Biotechnol Prog 19:1071–1075

    Article  CAS  PubMed  Google Scholar 

  373. Anjusha S, Gangaprasad A (2016) In vitro propagation and anthraquinone quantification in Gynochthodes umbellata (L.) Razafim. & B. Bremer (Rubiaceae)- A dye yielding plant. Ind Crop Prod 81:83–90

    Article  CAS  Google Scholar 

  374. Jha S, Jha TB, Mahato SB (1988) Tissue culture of Artemisia annua L. – a potential source of an antimalarial drug. Curr Sci 57:344–346

    Google Scholar 

  375. Woerdenbag HJ, Lüers JF, van Uden W, Pras N, Malingré TM, Alfermann AW (1993) Production of the new antimalarial drug artemisinin in shoot cultures of Artemisia annua L. Plant Cell Tissue Organ Cult 32:247–257

    Article  CAS  Google Scholar 

  376. Kim OT, Kim MY, Hong MH, Ahn JC, Hwang B (2004) Stimulation of asiaticoside accumulation in the whole plant cultures of Centella asiatica (L.) Urban by elicitors. Plant Cell Rep 23:339–344

    Article  CAS  PubMed  Google Scholar 

  377. Sharma M, Ahuja A, Gupta R, Mallubhotla S (2015) Enhanced bacoside production in shoot cultures of Bacopa monnieri under the influence of abiotic elicitors. Nat Prod Res 29:745–749

    Article  CAS  PubMed  Google Scholar 

  378. Naik PM, Manohar SH, Praveen N, Murthy HN (2010) Effects of sucrose and pH levels on in vitro shoot regeneration from leaf explants of Bacopa monnieri and accumulation of bacoside A in regenerated shoots. Plant Cell Tissue Organ Cult 100:235–259

    Article  Google Scholar 

  379. Sharma P, Yadav S, Srivastava A, Shrivastava N (2013) Methyl jasmonate mediates upregulation of bacoside A production in shoot cultures of Bacopa monnieri. Biotechnol Lett 35:1121–1125

    Article  CAS  PubMed  Google Scholar 

  380. Alvarez MA, Eraso NF, Pitta-Alvarez SI, Marconi PL (2009) Two-stage culture for producing berberine by cell suspension and shoot cultures of Berberis buxifolia Lam. Biotechnol Lett 31:457–463

    Article  CAS  PubMed  Google Scholar 

  381. Pèrez-Alonso N, Capote A, Gerth A, Jimènez E (2012) Increased cardenolides production by elicitation of Digitalis lanata shoots cultured in temporary immersion systems. Plant Cell Tissue Organ Cult 110:153–162

    Article  CAS  Google Scholar 

  382. Liu WZ, Wang ZF (2004) Accumulation and localization of camptothecin in young shoot of Camptotheca acuminata. J Plant Physiol Mol Biol 30:405–412

    CAS  Google Scholar 

  383. Roja G (2008) Micropropagation and production of camptothecin from in vitro plants of Ophiorrhiza rugosa var. decumbens. Nat Prod Res 22:1017–1023

    Article  CAS  PubMed  Google Scholar 

  384. Yoshimatsu K, Shimomura K (1993) Cephaelis ipecacuanha A. Richard (Brazilian Ipecac): micropropagation and the production of emetine and cephaeline. In: Bajaj YPS (ed) Medicinal and aromatic plants IV, Biotechnology in agriculture and forestry, 21. Springer, Berli/Heidelberg

    Google Scholar 

  385. Petersen M (1994) Coleus spp.: in vitro culture and the production of forskolin and rosmarinic acid. In: Bajaj YPS (ed) Medicinal and aromatic plants VI, Biotechnology in agriculture and forestry, 26. Springer, Berlin/Heidelberg

    Google Scholar 

  386. Santarem ER, Astarita LV (2003) Multiple shoot formation in Hypericum perforatum L. and hypericin production. Braz J Plant Physiol 15:21–26

    Article  Google Scholar 

  387. Pavlík M, Vacek J, Klejdus B, Kubáň V (2007) Hypericin and hyperforin production in St. John’s wort in vitro culture: influence of saccharose, polyethylene glycol, methyl jasmonate, and Agrobacterium tumefaciens. J Agric Food Chem 55:6147–6153

    Article  CAS  PubMed  Google Scholar 

  388. Coste A, Vlase L, Halmagyi A, Deliu C, Coldea G (2011) Effects of plant growth regulators and elicitors on production of secondary metabolites in shoot cultures of Hypericum hirsutum and Hypericum maculatum. Plant Cell Tissue Organ Cult 106:279–288

    Article  CAS  Google Scholar 

  389. Levieille G, Wilson G (2002) In vitro propagation and iridoid analysis of the medicinal species Harpagophytum procumbens and H. zeyheri. Plant Cell Rep 21:220–225

    Article  CAS  Google Scholar 

  390. Al Khateeb W, Hussein E, Qouta L, Alu’datt M, Al-Shara B, Abuzaiton A (2012) In vitro propagation and characterization of phenolic content along with antioxidant and antimicrobial activities of Cichorium pumilum Jacq. Plant Cell Tissue Organ Cult 110:103–110

    Article  CAS  Google Scholar 

  391. Amoo SO, Van Staden J (2012) Influence of plant growth regulators on shoot proliferation and secondary metabolite production in micropropagated Huernia hystrix. Plant Cell Tissue Organ Cult 112:249–256

    Article  CAS  Google Scholar 

  392. Skrzypczak-Pietraszek E, Słota J, Pietraszek J (2014) The influence of L-phenylalanine, methyl jasmonate and sucrose concentration on the accumulation of phenolic acids in Exacum affine Balf. f. ex Regel shoot culture. Acta Biochim Pol 61:47–53

    Article  PubMed  Google Scholar 

  393. García-Pérez Janet E, Gutiérrez-Uribe Silverio A, García-Lara S (2012) Luteolin content and antioxidant activity in micropropagated plants of Poliomintha glabrescens (Gray). Plant Cell Tissue Organ Cult 108:521–527

    Article  CAS  Google Scholar 

  394. Putalun W, Udomsin O, Yusakul G, Juengwatanatrakul T, Sakamoto S, Tanaka H (2010) Enhanced plumbagin production from in vitro cultures of Drosera burmannii using elicitation. Biotechnol Lett 32:721–724

    Article  CAS  PubMed  Google Scholar 

  395. Panwar GS, Guru SK (2015) Stimulation of reserpine production in the whole plant culture of Rauwolfia serpentina L. by elicitors and precursor feeding. J Plant Biochem Biotechnol 24:49–55

    Article  CAS  Google Scholar 

  396. Santos-Gomes PC, Seabra RM, Andrade PB, Fernandes-Ferreira M (2002) Phenolic antioxidant compounds produced by in vitro shoots of sage (Salvia officinalis L.). Plant Sci 162:981–987

    Article  CAS  Google Scholar 

  397. Touno K, Tamaoka J, Ohashi Y, Shimomura K (2005) Ethylene induced shikonin biosynthesis in shoot culture of Lithospermum erythrorhizon. Plant Physiol Biochem 43:101–115

    Article  CAS  PubMed  Google Scholar 

  398. Touno K, Harada K, Yoshimatsu K, Yazaki K, Shimomura K (2000) Shikonin derivative formation on the stem of cultured shoots in Lithospermum erythrorhizon. Plant Cell Rep 19:1121–1126

    Article  CAS  PubMed  Google Scholar 

  399. Sherif El F, Khattab S, Ibrahim AK, Ahmed SA (2013) Improved silymarin content in elicited multiple shoot cultures of Silybum marianum L. Physiol Mol Biol Plants 19:127–136

    Article  CAS  Google Scholar 

  400. Indrayanto G, Erawati T, Santosa MH (1995) Effect of L-arginine, casein hydrolysate, banana powder and sucrose on growth and solasodine production in shoot cultures of Solanum laciniatum. Plant Cell Tissue Organ Cult 43:237–240

    CAS  Google Scholar 

  401. Bondarev N, Reshetnyak O, Nosov A (2001) Peculiarities of diterpenoid steviol glycoside production in in vitro cultures of Stevia rebaudiana Bertoni. Plant Sci 161:155–163

    Article  CAS  Google Scholar 

  402. Dey A, Kundu S, Bandyopadhyay A, Bhattacharjee A (2013) Efficient micropropagation and chlorocholine chloride induced stevioside production of Stevia rebaudiana Bertoni. C R Biol 336:17–28

    Article  CAS  PubMed  Google Scholar 

  403. Miura Y, Hirata K, Kurano N, Miyamoto K, Uchida K (1988) Formation of vinblastine in multiple shoot culture of Catharanthus roseus. Planta Med 54:18–20

    Article  CAS  PubMed  Google Scholar 

  404. Hirata K, Horiuchi M, Ando T, Miyamoto K, Miura Y (1990) Vindoline and catharanthine production in multiple shoot cultures of Catharanthus roseus. J Ferment Bioeng 70:193–195

    Article  CAS  Google Scholar 

  405. Endo T, Goodbody A, Misawa M (1987) Alkaloid production in root and shoot cultures of Catharanthus roseus. Planta Med 53:479–482

    Article  CAS  PubMed  Google Scholar 

  406. Ray S, Jha S (2001) Production of withaferin A in shoot cultures of Withania somnifera Dunal. Planta Med 67:432–437

    Article  CAS  PubMed  Google Scholar 

  407. Sangwan RS, Chaurasiya NS, Lal P, Misra L, Uniyal GC, Tuli R, Sangwan NS (2007) Withanolide A biogeneration in in vitro shoot cultures of ashwagandha (Withania somnifera Dunal), a main medicinal plant in Ayurveda. Chem Pharm Bull 55:1371–1375

    Article  CAS  Google Scholar 

  408. Brandle JE, Richman A, Swanson AK, Chapman BP (2002) Leaf ESTs from Stevia rebaudiana: a resource for gene discovery in diterpene synthesis. Plant Mol Biol 50:613–622

    Article  CAS  PubMed  Google Scholar 

  409. Brandle JE, Telmer PG (2007) Steviol glycoside biosynthesis. Phytochemistry 68:1855–1863

    Article  CAS  PubMed  Google Scholar 

  410. Singh SD, Rao GP (2005) Stevia: the herbal sugar of 21 st century. Sugar Tech 7:17–24

    Article  CAS  Google Scholar 

  411. Ladygin VG, Bondarev NI, Semenova GA, Smolov AA, Reshetnyak OV, Nosov AM (2008) Chloroplast ultrastructure, photosynthetic apparatus activities and production of steviol glycosides in Stevia rebaudiana in vivo and in vitro. Biol Plant 52:9–16

    Article  CAS  Google Scholar 

  412. Yamazaki T, Flores HE, Shimomura K, Yoshihira K (1991) Examination of steviol glucosides production by hairy root and shoot cultures of Stevia rebaudiana. J Nat Prod 54:986–992

    Article  CAS  Google Scholar 

  413. Pandey H, Pandey P, Pandey SS, Singh S, Banerjee S (2016) Meeting the challenge of stevioside production in the hairy roots of Stevia rebaudiana by probing the underlying process. Plant Cell Tissue Organ Cult 126:511–521

    Article  CAS  Google Scholar 

  414. Sivaram L, Mukundan U (2003) In vitro culture studies on Stevia rebaudiana. In Vitro Cell Dev Biol Plant 39:520–523

    Article  Google Scholar 

  415. Hamill JD, Parr AJ, Robins RJ, Rhodes MJ (1986) Secondary product formation by cultures of Beta vulgaris and Nicotiana rustica transformed with Agrobacterium rhizogenes. Plant Cell Rep 5:111–114

    Article  CAS  PubMed  Google Scholar 

  416. Rhodes MJ, Hilton M, Parr AJ, Hamill JD, Robins RJ (1986) Nicotine production by “hairy root” cultures of Nicotiana rustica: fermentation and product recovery. Biotechnol Lett 8:415–420

    Article  CAS  Google Scholar 

  417. Green KD, Thomas NH, Callow JA (1992) Product enhancement and recovery from transformed root cultures of Nicotiana glauca. Biotechnol Bioeng 39:195–202

    Article  CAS  PubMed  Google Scholar 

  418. Zhao B, Agblevor FA, Ritesh KC, Jelesko JG (2013) Enhanced production of the alkaloid nicotine in hairy root cultures of Nicotiana tabacum L. Plant Cell Tissue Organ Cult 113:121–129

    Google Scholar 

  419. Kinnersley AM, Dougall DK (1980) Correlation between the nicotine content of tobacco plants and callus cultures. Planta 149:205–206

    Article  CAS  PubMed  Google Scholar 

  420. Ohta S, Yatazawa M (1989) Nicotiana tabacum L.(tobacco): in vitro production of nicotine. In: Bajaj YPS (ed) Medicinal and aromatic plants II, Biotechnology in agriculture and forestry, 7. Springer, Berlin/Heidelberg

    Google Scholar 

  421. Yamamoto O, Kamura K (1997) Production of saikosaponin in cultured roots of Bupleurum falcatum L. Plant Tissue Cult Biotechnol 3:138–147

    Google Scholar 

  422. Bulgakov VP, Veselova MV, Tchernoded GK, Kiselev KV, Fedoreyev SA, Zhuravlev YN (2005) Inhibitory effect of the Agrobacterium rhizogenes rolC gene on rabdosiin and rosmarinic acid production in Eritrichium sericeum and Lithospermum erythrorhizon transformed cell cultures. Planta 221:471–478

    Article  CAS  PubMed  Google Scholar 

  423. Mukherjee S, Ghosh B, Jha S (2000) Establishment of forskolin yielding transformed cell suspension cultures of Coleus forskohlii as controlled by different factors. J Biotechnol 76:73–81

    Article  CAS  PubMed  Google Scholar 

  424. 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 rolB and rolC genes. J Biotechnol 97:213–221

    Article  CAS  PubMed  Google Scholar 

  425. Kiselev KV, Dubrovina AS, Veselova MV, Bulgakov VP, Fedoreyev SA, Zhuravlev YN (2007) The rolB gene-induced overproduction of resveratrol in Vitis amurensis transformed cells. J Biotechnol 128:681–692

    Article  CAS  PubMed  Google Scholar 

  426. Shkryl YN, Veremeichik GN, Bulgakov VP, Tchernoded GK, Mischenko NP, Fedoreyev SA, Zhuravlev YN (2008) Individual and combined effects of the rolA, B, and C genes on anthraquinone production in Rubia cordifolia transformed calli. Biotechnol Bioeng 100:118–125

    Article  CAS  PubMed  Google Scholar 

  427. Dubrovina AS, Kiselev KV, Veselova MV, Isaeva GA, Fedoreyev SA, Zhuravlev YN (2009) Enhanced resveratrol accumulation in rolB transgenic cultures of Vitis amurensis correlates with unusual changes in CDPK gene expression. J Plant Physiol 166:1194–1206

    Article  CAS  PubMed  Google Scholar 

  428. Bulgakov VP, Shkryl YN, Veremeichik GN (2010) Engineering high yields of secondary metabolites in Rubia cell cultures through transformation with rol genes. In: Fett-Neto AG (ed) Plant secondary metabolism engineering. Humana Press, Totowa

    Google Scholar 

  429. Dubrovina AS, Manyakhin AY, Zhuravlev YN, Kiselev KV (2010) Resveratrol content and expression of phenylalanine ammonia-lyase and stilbene synthase genes in rolC transgenic cell cultures of Vitis amurensis. Appl Microbiol Biotechnol 88:727–736

    Article  CAS  PubMed  Google Scholar 

  430. Grishchenko OV, Kiselev KV, Tchernoded GK, Fedoreyev SA, Veselova MV, Bulgakov VP, Zhuravlev YN (2013) The influence of the rolC gene on isoflavonoid production in callus cultures of Maackia amurensis. Plant Cell Tissue Organ Cult 113:429–435

    Article  CAS  Google Scholar 

  431. Vereshchagina YV, Bulgakov VP, Grigorchuk VP, Rybin VG, Veremeichik GN, Tchernoded GK, Gorpenchenko TY, Koren OG, Phan NH, Minh NT, Chau LT (2014) The rolC gene increases caffeoylquinic acid production in transformed artichoke cells. Appl Microbiol Biotechnol 98:7773–7780

    Article  CAS  PubMed  Google Scholar 

  432. Grishchenko OV, Kiselev KV, Tchernoded GK, Fedoreyev SA, Veselova MV, Bulgakov VP, Zhuravlev YN (2016) RolB gene-induced production of isoflavonoids in transformed Maackia amurensis cells. Appl Microbiol Biotechnol 100:7479–7489

    Article  CAS  PubMed  Google Scholar 

  433. Kiselev KV, Dubrovina AS, Bulgakov VP (2009) Phenylalanine ammonia-lyase and stilbene synthase gene expression in rolB transgenic cell cultures of Vitis amurensis. Appl Microbiol Biotechnol 82:647–655

    Article  CAS  PubMed  Google Scholar 

  434. Verma P, Sharma A, Khan SA, Shanker K, Mathur AK (2015) Over-expression of Catharanthus roseus tryptophan decarboxylase and strictosidine synthase in rol gene integrated transgenic cell suspensions of Vinca minor. Protoplasma 252:373–381

    Article  CAS  PubMed  Google Scholar 

  435. Chen H, Yuan JP, Chen F, Zhang YL, Song JY (1997) Tanshinone production in Ti-transformed Salvia miltiorrhiza cell suspension cultures. J Biotechnol 58:147–156

    Article  CAS  PubMed  Google Scholar 

  436. 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 

  437. Ibrahim AK, Khalifa S, Khafagi I, Youssef D, Khan I, Mesbah M (2007) Stimulation of oleandrin production by combined Agrobacterium tumefaciens mediated transformation and fungal elicitation in Nerium oleander cell cultures. Enzym Microb Technol 41:331–336

    Article  CAS  Google Scholar 

  438. Yoshimatsu K, Shimomura K (1992) Transformation of opium poppy (Papaver somniferum L.) with Agrobacterium rhizogenes MAFF 03-01724. Plant Cell Rep 11:132–136

    Article  CAS  PubMed  Google Scholar 

  439. Sauerwein M, Ishimaru K, Shimomura K (1991) Indole alkaloids in hairy roots of Amsonia elliptica. Phytochemistry 30:1153–1155

    Article  CAS  Google Scholar 

  440. Ishimaru K, Arakawa H, Yamanaka M, Shimomura K (1994) Polyacetylenes in Lobelia sessilifolia hairy roots. Phytochemistry 35:365–369

    Article  CAS  Google Scholar 

  441. Maldonado-Mendoza IE, Loyola-Vargas VM (1995) Establishment and characterization of photosynthetic hairy root cultures of Datura stramonium. Plant Cell Tissue Organ Cult 40:197–208

    Article  CAS  Google Scholar 

  442. Sauerwein M, Yamazaki T, Shimomura K (1991) Hernandulcin in hairy root cultures of Lippia dulcis. Plant Cell Rep 9:579–581

    CAS  PubMed  Google Scholar 

  443. Bakkali AT, Jaziri M, Foriers A, Vander Heyden Y, Vanhaelen M, Homes J (1997) Lawsone accumulation in normal and transformed cultures of henna, Lawsonia inermis. Plant Cell Tissue Organ Cult 51:83–87

    Article  Google Scholar 

  444. Negi JS, Bisht VK, Bhandari AK, Bisht DS, Singh P, Singh N (2014) Quantification of reserpine content and antibacterial activity of Rauvolfia serpentina (L.) Benth. ex Kurz. Afr J Microbiol Res 8:162–166

    Article  CAS  Google Scholar 

  445. Mehrotra S, Goel MK, Srivastava V, Rahman LU (2015) Hairy root biotechnology of Rauwolfia serpentina: a potent approach for the production of pharmaceutically important terpenoid indole alkaloids. Biotechnol Lett 37:253–263

    Article  CAS  PubMed  Google Scholar 

  446. Krombholz R, Mersinger R, Kreis W, Reinhard E (1992) Production of forskolin by axenic Coleus forskohlii roots cultivated in shake flasks and 20-L glass jar bioreactors. Planta Med 58:328–333

    Article  CAS  PubMed  Google Scholar 

  447. Mersinger R, Dornauer H, Reinhard E (1988) Formation of forskolin by suspension cultures of Coleus forskohlii. Planta Med 54:200–204

    Article  CAS  PubMed  Google Scholar 

  448. Mukherjee S, Ghosh B, Jha S (1996) Forskolin synthesis in in vitro cultures of Coleus forskohlii Briq transformed with Agrobacterium tumefaciens. Plant Cell Rep 15:691–694

    Article  CAS  PubMed  Google Scholar 

  449. Saito K, Murakoshi I, Inzé D, Van Montagu M (1989) Biotransformation of nicotine alkaloids by tobacco shooty teratomas induced by a Ti plasmid mutant. Plant Cell Rep 7:607–610

    Article  CAS  PubMed  Google Scholar 

  450. Spencer A, Hamill JD, Rhodes MJ (1990) Production of terpenes by differentiated shoot cultures of Mentha citrata transformed with Agrobacterium tumefaciens T37. Plant Cell Rep 8:601–604

    Article  CAS  PubMed  Google Scholar 

  451. Alvarez MA, Talou JR, Paniego NB, Giulietti AM (1994) Solasodine production in transformed organ cultures (roots and shoots) of Solanum elaeagnifolium Cav. Biotechnol Lett 16:393–396

    Article  CAS  Google Scholar 

  452. Salem KM, Charlwood BV (1995) Accumulation of essential oils by Agrobacterium tumefaciens-transformed shoot cultures of Pimpinella anisum. Plant Cell Tissue Organ Cult 40:209–215

    Article  CAS  Google Scholar 

  453. Ehmke A, Ohmstede D, Eilert U (1995) Steroidal glycoalkaloids in cell and shoot teratoma cultures of Solanum dulcamara. Plant Cell Tissue Organ Cult 43:191–197

    Article  CAS  Google Scholar 

  454. Subroto MA, Hamill JD, Doran PM (1996) Development of shooty teratomas from several solanaceous plants: growth kinetics, stoichiometry and alkaloid production. J Biotechnol 45:45–57

    Article  CAS  Google Scholar 

  455. Paniego NB, Giulietti AM (1996) Artemisinin production by Artemisia annua L.-transformed organ cultures. Enzym Microb Technol 18:526–530

    Article  CAS  Google Scholar 

  456. Ghosh B, Mukherjee S, Jha S (1997) Genetic transformation of Artemisia annua by Agrobacterium tumefaciens and artemisinin synthesis in transformed cultures. Plant Sci 122:193–199

    Article  CAS  Google Scholar 

  457. Ray S, Jha S (1999) Withanolide synthesis in cultures of Withania somnifera transformed with Agrobacterium tumefaciens. Plant Sci 146:1–7

    Article  CAS  Google Scholar 

  458. Begum F, Nageswara Rao SS, Rao K, Prameela Devi Y, Giri A, Giri CC (2009) Increased vincristine production from Agrobacterium tumefaciens C58 induced shooty teratomas of Catharanthus roseus G. Don. Nat Prod Res 23:973–981

    Article  CAS  PubMed  Google Scholar 

  459. Hong SB, Peebles CA, Shanks JV, San KY, Gibson SI (2006) Terpenoid indole alkaloid production by Catharanthus roseus hairy roots induced by Agrobacterium tumefaciens harboring rol ABC genes. Biotechnol Bioeng 93:386–390

    Article  CAS  PubMed  Google Scholar 

  460. Chen DH, Ye HC, Li GF (2000) Expression of a chimeric farnesyl diphosphate synthase gene in Artemisia annua L. transgenic plants via Agrobacterium tumefaciens-mediated transformation. Plant Sci 155:179–185

    Article  CAS  PubMed  Google Scholar 

  461. Krolicka A, Szpitter A, Stawujak K, Baranski R, Gwizdek-Wisniewska A, Skrzypczak A, Kaminski M, Lojkowska E (2010) Teratomas of Drosera capensis var. alba as a source of naphthoquinone: ramentaceone. Plant Cell Tissue Organ Cult 103:285–292

    Article  CAS  Google Scholar 

  462. Sarkar S, Ghosh I, Roychowdhury D, Jha S (2018) The effects of rol genes of Agrobacterium rhizogenes on morphogenesis and secondary metabolite accumulation in medicinal plants. In: Kumar N (ed) Biotechnological approaches for medicinal and aromatic plants. Springer, Singapore

    Google Scholar 

  463. Christey MC, Sinclair BK, Braun RH, Wyke L (1997) Regeneration of transgenic vegetable brassicas (Brassica oleracea and B. campestris) via Ri-mediated transformation. Plant Cell Rep 16:587–593

    Article  CAS  PubMed  Google Scholar 

  464. Christey MC (2001) Use of Ri-mediated transformation for production of transgenic plants. In Vitro Cell Dev Biol Plant 37:687–700

    Article  CAS  Google Scholar 

  465. Chaudhuri KN, Ghosh B, Tepfer D, Jha S (2006) Spontaneous plant regeneration in transformed roots and calli from Tylophora indica: changes in morphological phenotype and tylophorine accumulation associated with transformation by Agrobacterium rhizogenes. Plant Cell Rep 25:1059–1066

    Article  CAS  PubMed  Google Scholar 

  466. Majumdar S, Garai S, Jha S (2011) Genetic transformation of Bacopa monnieri by wild type strains of Agrobacterium rhizogenes stimulates production of bacopa saponins in transformed calli and plants. Plant Cell Rep 30:941–954

    Article  CAS  PubMed  Google Scholar 

  467. Gangopadhyay M, Chakraborty D, Bhattacharyya S, Bhattacharya S (2010) Regeneration of transformed plants from hairy roots of Plumbago indica. Plant Cell Tiss Org 102:109–114

    Article  Google Scholar 

  468. Sevón N, Dräger B, Hiltunen R, Oksman-Caldentey KM (1997) Characterization of transgenic plants derived from hairy roots of Hyoscyamus muticus. Plant Cell Rep 16:605–611

    Article  PubMed  Google Scholar 

  469. Celma CR, Palazón J, Cusidó RM, Piñol MT, Keil M (2001) Decreased scopolamine yield in field-grown Duboisia plants regenerated from hairy roots. Planta Med 67:249–253

    Article  CAS  Google Scholar 

  470. Misra L, Mishra P, Pandey A, Sangwan RS, Sangwan NS, Tuli R (2008) Withanolides from Withania somnifera roots. Phytochemistry 69:1000–1004

    Article  CAS  PubMed  Google Scholar 

  471. Sen J, Sharma AK (1991) Micropropagation of Withania somnifera from germinating seeds and shoot tips. Plant Cell Tissue Organ Cult 26:71–73

    Article  CAS  Google Scholar 

  472. Kulkarni AA, Thengane SR, Krishnamurthy KV (2000) Direct shoot regeneration from node, internode, hypocotyl and embryo explants of Withania somnifera. Plant Cell Tissue Organ Cult 62:203–209

    Article  Google Scholar 

  473. Sabir F, Sangwan NS, Chaurasiya ND, Misra LN, Sangwan RS (2008) In vitro withanolide production by Withania somnifera L. cultures. Z Naturforsch C 63:409–412

    Article  CAS  PubMed  Google Scholar 

  474. Sivanesan I (2007) Direct regeneration from apical bud explants of Withania somnifera Dunal. Indian J Biotechnol 16:125–127

    Google Scholar 

  475. Roja G, Heble MR, Sipahimalani AT (1991) Tissue cultures of Withania somnifera: morphogenesis and withanolide synthesis. Phytother Res 5:185–187

    Article  CAS  Google Scholar 

  476. Banerjee S, Naqvi AA, Mandal S, Ahuja PS (1994) Transformation of Withania somnifera (L) Dunal by Agrobacterium rhizogenes: infectivity and phytochemical studies. Phytother Res 8:452–455

    Article  CAS  Google Scholar 

  477. Ray S, Ghosh B, Sen S, Jha S (1996) Withanolide production by root cultures of Withania somnifera transformed with Agrobacterium rhizogenes. Planta Med 62:571–573

    Article  CAS  PubMed  Google Scholar 

  478. Das A, Ghose S, Bhattacharyya A, Datta AK (2010) In vitro biogeneration of alkaloids and withanolides in Withania somnifera (L.) Dunal (Solanaceae) var.‘Poshita’and ‘Jawahar 22’. Int J Plant Dev Biol 4:42–46

    Google Scholar 

  479. Chakraborty N, Banerjee D, Ghosh M, Pradhan P, Gupta NS, Acharya K, Banerjee M (2013) Influence of plant growth regulators on callus mediated regeneration and secondary metabolites synthesis in Withania somnifera (L.) Dunal. Physiol Mol Biol Plants 19:117–125

    Article  CAS  PubMed  Google Scholar 

  480. Rani V, Raina SN (2000) Genetic fidelity of organized meristem-derived micropropagated plants: a critical reappraisal. In Vitro Cell Dev Biol Plant 36:319–330

    Article  CAS  Google Scholar 

  481. Bairu MW, Stirk WA, Doležal K, van Staden J (2008) The role of topolins in micropropagation and somaclonal variation of banana cultivars ‘Williams’ and ‘Grand Naine’(Musa spp. AAA). Plant Cell Tissue Organ Cult 95:373–379

    Article  CAS  Google Scholar 

  482. Devi SP, Kumaria S, Rao SR, Tandon P (2014) Single primer amplification reaction (SPAR) methods reveal subsequent increase in genetic variations in micropropagated plants of Nepenthes khasiana Hook. f. maintained for three consecutive regenerations. Gene 538:23–29

    Article  CAS  PubMed  Google Scholar 

  483. Constabel F, Rambold S, Chatson KB, Kurz WG, Kutney JP (1981) Alkaloid production in Catharanthus roseus (L.) G. Don. Plant Cell Rep 1:3–5

    Article  CAS  PubMed  Google Scholar 

  484. Holden PR, Yeoman MM (1994) Variation in the growth and biosynthetic activity of cloned cell cultures of Capsicum frutescens and their response to an exogenously supplied elicitor. Plant Cell Tissue Organ Cult 38:31–37

    Article  CAS  Google Scholar 

  485. Sierra MI, van der Heijden R, van der Leer T, Verpoorte R (1992) Stability of alkaloid production in cell suspension cultures of Tabernaemontana divaricata during long-term subculture. Plant Cell Tissue Organ Cult 28:59–68

    Article  CAS  Google Scholar 

  486. Baebler Š, Hren M, Camloh M, Ravnikar M, Bohanec B, Plaper I, Ucman R, Žel J (2005) Establishment of cell suspension cultures of yew (Taxus× media Rehd.) and assessment of their genomic stability. In Vitro Cell Dev Biol Plant 41:338–343

    Article  CAS  Google Scholar 

  487. Sengupta J, Jha S, Sen S (1988) Karyotype stability in long-term callus derived plants of Crepis tectorum L. Biol Plant 30:247–251

    Article  Google Scholar 

  488. Bhattacharyya P, Kumar V, Van Staden J (2017) Assessment of genetic stability amongst micropropagated Ansellia africana, a vulnerable medicinal orchid species of Africa using SCoT markers. South Afr J Bot 108:294–302

    Article  CAS  Google Scholar 

  489. Salvi ND, George L, Eapen S (2001) Plant regeneration from leaf base callus of turmeric and random amplified polymorphic DNA analysis of regenerated plants. Plant Cell Tissue Organ Cult 66:113–119

    Article  CAS  Google Scholar 

  490. Kaeppler SM, Kaeppler HF, Rhee Y (2000) Epigenetic aspects of somaclonal variation in plants. In: Matzke MA, Matzke AJM (eds) Plant gene silencing. Springer, Dordrecht

    Google Scholar 

  491. Phillips RL, Kaeppler SM, Olhoft P (1994) Genetic instability of plant tissue cultures: breakdown of normal controls. Proc Natl Acad Sci 91:5222–5226

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  492. Bogani P, Simoni A, Lio’ P, Scialpi A, Buiatti M (1996) Genome flux in tomato cell clones cultured in vitro in different physiological equilibria. II. A RAPD analysis of variability. Genome 39:846–853

    Article  CAS  PubMed  Google Scholar 

  493. Linacero R, Alves EF, Vázquez AM (2000) Hot spots of DNA instability revealed through the study of somaclonal variation in rye. Theor Appl Genet 100:506–511

    Article  CAS  Google Scholar 

  494. Keyte AL, Percifield R, Liu B, Wendel JF (2006) Infraspecific DNA methylation polymorphism in cotton (Gossypium hirsutum L.). J Hered 97:444–450

    Article  CAS  PubMed  Google Scholar 

  495. Rival A, Ilbert P, Labeyrie A, Torres E, Doulbeau S, Personne A, Dussert S, Beulé T, Durand-Gasselin T, Tregear JW, Jaligot E (2013) Variations in genomic DNA methylation during the long-term in vitro proliferation of oil palm embryogenic suspension cultures. Plant Cell Rep 32:359–368

    Article  CAS  PubMed  Google Scholar 

  496. Bhattacharyya P, Kumaria S, Diengdoh R, Tandon P (2014) Genetic stability and phytochemical analysis of the in vitro regenerated plants of Dendrobium nobile Lindl., an endangered medicinal orchid. Meta Gene 2:489–504

    Article  PubMed  PubMed Central  Google Scholar 

  497. Devi SP, Kumaria S, Rao SR, Tandon P (2015) Genetic fidelity assessment in micropropagated plants using cytogenetical analysis and heterochromatin distribution: a case study with Nepenthes khasiana Hook f. Protoplasma 252:1305–1312

    Article  PubMed  Google Scholar 

  498. Bhattacharyya P, Kumaria S, Job N, Tandon P (2016) En-masse production of elite clones of Dendrobium crepidatum: a threatened, medicinal orchid used in traditional chinese medicine (TCM). J Appl Res Med Aromat Plants 3:168–176

    Google Scholar 

  499. Bhattacharyya P, Kumaria S, Tandon P (2016) High frequency regeneration protocol for Dendrobium nobile: a model tissue culture approach for propagation of medicinally important orchid species. South Afr J Bot 104:232–243

    Article  CAS  Google Scholar 

  500. Joshi P, Dhawan V (2007) Assessment of genetic fidelity of micropropagated Swertia chirayita plantlets by ISSR marker assay. Biol Plant 51:22–26

    Article  CAS  Google Scholar 

  501. Devarumath RM, Nandy S, Rani V, Marimuthu S, Muraleedharan N (2002) RAPD, ISSR and RFLP fingerprints as useful markers to evaluate genetic integrity of micropropagated plants of three diploid and triploid elite tea clones representing Camellia sinensis (China type) and C. assamica ssp. assamica (Assam-India type). Plant Cell Rep 21:166–173

    Article  CAS  Google Scholar 

  502. Lakshmanan V, Reddampalli Venkataramareddy S, Neelwarne B (2007) Molecular analysis of genetic stability in long-term micropropagated shoots of banana using RAPD and ISSR markers. Electron J Biotechnol 10:106–113

    Article  Google Scholar 

  503. Bhatia R, Singh KP, Jhang T, Sharma TR (2009) Assessment of clonal fidelity of micropropagated gerbera plants by ISSR markers. Sci Hortic 119:208–211

    Article  CAS  Google Scholar 

  504. Bhatia R, Singh KP, Sharma TR, Jhang T (2011) Evaluation of the genetic fidelity of in vitro propagated gerbera (Gerbera jamesonii Bolus) using DNA-based markers. Plant Cell Tissue Organ Cult 104:131–135

    Article  Google Scholar 

  505. Martins M, Sarmento D, Oliveira M (2004) Genetic stability of micropropagated almond plantlets, as assessed by RAPD and ISSR markers. Plant Cell Rep 23:492–496

    Article  CAS  PubMed  Google Scholar 

  506. Rathore NS, Rai MK, Phulwaria M, Rathore N, Shekhawat NS (2014) Genetic stability in micropropagated Cleome gynandra revealed by SCoT analysis. Acta Physiol Plant 36:555–559

    Article  CAS  Google Scholar 

  507. Singh P, Dwivedi P, Atri N (2014) In vitro shoot multiplication of Stevia and assessment of stevioside content and genetic fidelity of the regenerants. Sugar Tech 16:430–439

    Article  CAS  Google Scholar 

  508. Patel KR, Berlyn GP (1982) Genetic instability of multiple buds of Pinus coulteri regenerated from tissue culture. Can J For Res 12:93–101

    Article  Google Scholar 

  509. Alicchio R, Antonioli C, Palenzona D (1984) Karyotypic variability in plants of Solanum melongena regenerated from callus grown in presence of culture filtrate of Verticillium dahliae. Theor Appl Genet 67:267–271

    Article  CAS  PubMed  Google Scholar 

  510. Hao YJ, Deng XX (2002) Occurrence of chromosomal variations and plant regeneration from long-term-cultured citrus callus. In Vitro Cell Dev Biol Plant 38:472–476

    Article  Google Scholar 

  511. Zucchi MI, Arizono H, Morais VA, Fungaro MH, Vieira ML (2002) Genetic instability of sugarcane plants derived from meristem cultures. Genet Mol Biol 25:91–96

    Article  CAS  Google Scholar 

  512. Eshraghi P, Zarghami R, Ofoghi H (2005) Genetic stability of micropropagated plantlets in date palm. J Sci Islam Repub Iran 16:311–315

    CAS  Google Scholar 

  513. Chaudhuri KN, Ghosh B, Tepfer D, Jha S (2005) Genetic transformation of Tylophora indica with Agrobacterium rhizogenes A4: growth and tylophorine productivity in different transformed root clones. Plant Cell Rep 24:25–35

    Article  CAS  PubMed  Google Scholar 

  514. Bandyopadhyay M, Jha S, Tepfer D (2007) Changes in morphological phenotypes and withanolide composition of Ri-transformed roots of Withania somnifera. Plant Cell Rep 26:599–609

    Article  CAS  PubMed  Google Scholar 

  515. Alpizar E, Dechamp E, Lapeyre-Montes F, Guilhaumon C, Bertrand B, Jourdan C, Lashermes P, Etienne H (2008) Agrobacterium rhizogenes-transformed roots of coffee (Coffea arabica): conditions for long-term proliferation and morphological and molecular characterization. Ann Bot 101:929–940

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  516. Roychowdhury D, Basu A, Jha S (2015) Morphological and molecular variation in Ri-transformed root lines are stable in long term cultures of Tylophora indica. Plant Growth Regul 75:443–453

    Article  CAS  Google Scholar 

  517. Halder M, Jha S (2016) Enhanced trans-resveratrol production in genetically transformed root cultures of Peanut (Arachis hypogaea L.). Plant Cell Tissue Organ Cult 124:555–572

    Article  CAS  Google Scholar 

  518. Lipp Joao KH, Brown TA (1994) Long-term stability of root cultures of tomato transformed with Agrobacterium rhizogenes R1601. J Exp Bot 45:641–647

    Article  CAS  Google Scholar 

  519. Geerlings A, Hallard D, Martinez Caballero A, Lopes Cardoso I, van der Heijden R, Verpoorte R (1999) Alkaloid production by a Cinchona officinalis ‘ledgeriana’ hairy root culture containing constitutive expression constructs of tryptophan decarboxylase and strictosidine synthase cDNA from Catharanthus roseus. Plant Cell Rep 19:191–196

    Article  CAS  PubMed  Google Scholar 

  520. Zdravković-Korać S, Ćalić D, Druart PH, Radojević L (2003) The horse chestnut lines harboring the rol genes. Biol Plant 47:487–491

    Article  Google Scholar 

  521. Santos PM, Figueiredo AC, Oliveira MM, Barroso JG, Pedro LG, Deans SG, Younus AKM, Scheffer JJC (1999) Morphological stability of Pimpinella anisum hairy root cultures and time-course study of their essential oils. Biotechnol Lett 21:859–864

    Article  CAS  Google Scholar 

  522. Basu A, Joshi RK, Jha S (2015) Genetic transformation of Plumbago zeylanica with Agrobacterium rhizogenes strain LBA 9402 and characterization of transformed root lines. Plant Tissue Cult Biotechnol 25:21–35

    Article  Google Scholar 

  523. Roychowdhury D, Ghosh B, Chaubey B, Jha S (2013) Genetic and morphological stability of six-year-old transgenic Tylophora indica plants. Nucleus 56:81–89

    Article  Google Scholar 

  524. Paul P, Sarkar S, Jha S (2015) Effects associated with insertion of cryptogein gene utilizing Ri and Ti plasmids on morphology and secondary metabolites are stable in Bacopa monnieri-transformed plants grown in vitro and ex vitro. Plant Biotechnol Rep 9:231–245

    Article  Google Scholar 

  525. Benson EE, Hamill JD (1991) Cryopreservation and post freeze molecular and biosynthetic stability in transformed roots of Beta vulgaris and Nicotiana rustica. Plant Cell Tissue Organ Cult 24:163–172

    Article  CAS  Google Scholar 

  526. Maldonado-Mendoza IE, Ayora-Talavera T, Loyola-Vargas VM (1993) Establishment of hairy root cultures of Datura stramonium characterization and stability of tropane alkaloid production during long periods of subculturing. Plant Cell Tissue Organ Cult 33:321–329

    Article  CAS  Google Scholar 

  527. Baíza AM, Quiroz-Moreno A, Ruíz JA, Loyola-Vargas VM (1999) Genetic stability of hairy root cultures of Datura stramonium. Plant Cell Tissue Organ Cult 59:9–17

    Article  Google Scholar 

  528. Sevón N, Hiltunen R, Oksman-Caldentey KM (1998) Somaclonal variation in transformed roots and protoplast-derived hairy root clones of Hyoscyamus muticus. Planta Med 64:37–41

    Article  PubMed  Google Scholar 

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Acknowledgments

S.J. is thankful to the National Academy of Sciences (NASI, Allahabad, India) for the award of “Senior Scientist, NASI” and providing the financial support to continue the research and to the Head, Department of Botany, University of Calcutta, for facilities provided.

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Halder, M., Jha, S. (2020). Morphogenesis, Genetic Stability, and Secondary Metabolite Production in Untransformed and Transformed Cultures. In: Ramawat, K., Ekiert, H., Goyal, S. (eds) Plant Cell and Tissue Differentiation and Secondary Metabolites. Reference Series in Phytochemistry. Springer, Cham. https://doi.org/10.1007/978-3-030-11253-0_15-1

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  • DOI: https://doi.org/10.1007/978-3-030-11253-0_15-1

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  1. Latest

    Morphogenesis, Genetic Stability, and Secondary Metabolite Production in Untransformed and Transformed Cultures
    Published:
    27 February 2020

    DOI: https://doi.org/10.1007/978-3-030-11253-0_15-2

  2. Original

    Morphogenesis, Genetic Stability, and Secondary Metabolite Production in Untransformed and Transformed Cultures
    Published:
    02 December 2019

    DOI: https://doi.org/10.1007/978-3-030-11253-0_15-1