Sustainable Production of Polyphenols and Antioxidants by Plant In Vitro Cultures

  • Iryna SmetanskaEmail author
Reference work entry
Part of the Reference Series in Phytochemistry book series (RSP)


Phenolic compounds represent big group of plant secondary metabolites that influence flavor, color, and texture and can be used as food additives, nutraceuticals, and pharmaceuticals.

However, there are some limitations in obtaining sufficient amount of these bioactive compounds from plants, because they are rather seldom or occur naturally in plant tissues only at very low concentrations. Alternatively, it is possible to synthesize them chemically, but this way if oft technologically not possible or very sophisticated and economically infeasible.

Plant in vitro cultures provide an attractive route to produce high-value plant-derived products and therefore can be an alternative source of valuable phenolics.

Moreover, compounds synthesized by plant in vitro cultures are natural products and therefore can be more easily accepted by consumers as artificially synthetized substances.

The synthesis of phytochemicals by plant in vitro cultures in contrast to these in plants is not depending on environmental conditions and can be regulated through standard physical and chemical conditions in bioreactor, which helps to avoid qualitative and quantitative fluctuations in product yield.

The process of obtaining valuable phytochemicals can be represented as a multistage technology, each link of which can vary individually in dependence of specific requirements of in vitro cultures (e.g., phytohormones, nutrients, light) or properties of end product (e.g., antioxidative potential, stability).

For the establishment of high-producing and fast-growing cell lines, the parent plants should be selected (Murthy et al. Strategies for enhanced production of plant secondary metabolites from cell and organ cultures. In: Production of biomass and bioactive compounds using bioreactor technology (pp. 471–509). Springer Plus). The expression of synthetic pathways can be influenced by environmental conditions, the supply of precursors, and the application of elicitors (Schreiner, Eur J Nutr 44(2):85–94, 2005) as well as altered by special treatments like biotransformation and immobilization (Georgiev et al., Appl Microbiol Biotechnol 83:809–823, 2009). The efficiency of bioprocessing can be increased by the simplification of methods for product recovery and afterward its stabilization.

This chapter reviews the recent advances in the optimization of environmental factors for production of phenolics by plant in vitro cultures, new developments in bioprocessing of plant cell, hairy root and organ cultures, and emerging technologies on phytochemical recovery.


Plant in vitro cultures Cell cultures Hairy root cultures Organ cultures Phenolic compounds Antioxidants Food additives Cultivation media Precursors Elicitors Exudation Membrane permeabilization Fermentation 



2,4-Dichlorophenoxyacetic acid




Dimethyl sulfoxide


Dry weight


Fresh weight


Indole-3-acetic acid


1-Naphthalene acetic acid



This work would not have been possible without the support of my colleagues, providing together with me long-term research work on plant in vitro cultures. Special thank for the support and discussions to Dr. Ahmed Gabr, Dr. Hoda Mabrok, and Dr. Oksana Sytar as well as for fruitful collaboration of all members of our working group Dr. Dase Hunaefi, Dr. Zhenzhen Cai, Ms. Alexandra Wendt, Ms. Anja Kastell, Dr. Yaroslav Schevchenko, Dr. Heidi Riedel, Dr. Ravichandran Kavitha, Dr. Adel Mohdaly, Dr. Inga Mewis, Dr. Divine Akumo, Ms. Nay Min Saw, and Ms. Irene Hemmerich.


  1. 1.
    Mulabagal V, Tsay H (2004) Plant cell cultures as a source for the production of biologically important secondary metabolites. Int J Appl Sci Eng 2:29–48Google Scholar
  2. 2.
    Namdeo AG (2007) Plant cell elicitation for production of secondary metabolites. Pharmacogn Rev 1:69.
  3. 3.
    Raskin I, Ribnicky DM, Komarnytsky S, Ilic N, Poulev A, Borisjuk N, Brinker A, Moreno DA, Ravichandran K, Ravichandran P, Saw NM, Gabr AMM, Ahmed A, Knorr D, Smetanska I (2012) Effects of different encapsulation agents and drying process on stability of betalain extracts. J Food Sci Technol., ISSN: 0022-1155
  4. 4.
    Alfermann AW, Petersen M (1995) Natural products formation by plant cell biotechnology. Plant Cell Tissue Org Cult 43:199–205CrossRefGoogle Scholar
  5. 5.
    Filova A (2014) Production of some secondary metabolites in plant tissue cultures. Res J Agric Sci 46(1):263–245Google Scholar
  6. 6.
    Vamanu E, Nita S (2013) Antioxidant capacity and the correlation with major phenolic compounds, anthocyanin, and tocopherol content in various extracts from the wild edible Boletus edulis mushroom. Biomed Res Int 2013:313905PubMedGoogle Scholar
  7. 7.
    Bulgakov V, Vereshchagiona YV, Veremeichik GN (2017) Anticancer polyphenols from cultured plant cells: production and new bioengineering strategies. Curr Med Chem.
  8. 8.
    Huang WY, Cai YZ, Zhang YB (2010) Natural phenolic compounds from medicinal herbs and dietary plants: potential use for cancer prevention. Nutr Cancer 62:1–20PubMedCrossRefGoogle Scholar
  9. 9.
    Georgiev MI, Weber J, Maciuk J (2009) Bioprocessing of plant cell cultures for mass production of targeted compounds. Appl Microbiol Biotechnol 83:809–823PubMedCrossRefGoogle Scholar
  10. 10.
    Murthy HN, Dandin VS, Zhong JJ, Paek KY (2014) Strategies for enhanced production of plant secondary metabolites from cell and organ cultures. In: Production of biomass and bioactive compounds using bioreactor technology. Springer Plus, pp 471–509. Scholar
  11. 11.
    Moreno PRH, van der Heijden R, Verpoorte R (1995) Cell and tissue cultures of Catharanthus Roseus: a literature survey. Plant Cell Tissue Organ Cult 42(1):1–25CrossRefGoogle Scholar
  12. 12.
    Weathers PJ, Towler MJ, Xu JF (2010) Bench to batch: advances in plant cell culture for producing useful products. Appl Microbiol Biotechnol 85:1339–1351PubMedCrossRefGoogle Scholar
  13. 13.
    Kim DJ, Chang HN (1990) Enhanced shikonin production from Lithospermum erythrorhizon by in situ extraction and calcium alginate immobilization. Biotechnol Bioeng 36(5):460–466PubMedCrossRefGoogle Scholar
  14. 14.
    King A, Young G (1999) Characteristics and occurrence of phenolic phytochemicals. J Am Diet Assoc 99(2):213–218PubMedCrossRefGoogle Scholar
  15. 15.
    Harris CS, Mo F, Migahed L, Chepelev L, Haddad PS, Wright JS, Willmore WG, Arnason JT, Bennett SAL (2007) Plant phenols regulate neoplastic cell growth and survival: a quantitative structure-activity and biochemical analysis. Can J Physiol Pharmacol 85:1124–1138PubMedCrossRefGoogle Scholar
  16. 16.
    Terao J (2009) Dietary flavonoids as antioxidants. Forum Nutr 61:87–94PubMedCrossRefGoogle Scholar
  17. 17.
    Wu X, Beecher GR, Holden JM, Haytowitz DB, Gebhardt SE, Prior RL (2006) Concentration of anthocyanins in common foods in the United States and estimation of normal consumption. J Agric Food Chem 54:4069–4075PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Huyskens-Keil S, Eichholz I, Kroh LW, Rohn S (2007) UV-B induced changes of phenol composition and antioxidant activity in black currant fruit (Ribes Nigrum L.) J Appl Bot Food Qual 81:140–144Google Scholar
  19. 19.
    Gonzalez-Gallego J, Sanchez-Campos S, Tunon MJ (2007) Anti-inflammatory properties of dietary flavonoids. Nutr Hosp 22:287–293PubMedGoogle Scholar
  20. 20.
    Rohn S, Petzke KJ, Rawel HM, Kroll J (2006) Reactions of chlorogenic acid and quercetin with a soy protein isolate – influence on the in vivo food protein quality in rats. Mol Nutr Food Res 50:696–704; Agarwal M, Kamal R (2007) Studies on flavonoid production using in vitro cultures of Momordica charantia L. Indian J Biotechnol 6:277–279CrossRefGoogle Scholar
  21. 21.
    Maharik N, Elgengaihi S, Taha H (2009) Anthocyanin production in callus cultures of Crataegus sinaica Boiss. Inter J Acad Res 1:30–34Google Scholar
  22. 22.
    Ayabe S, Iida K, Furuya T (1986) Induction of stress metabolites in immobilized Glycyrrhiza echinata cultured cells. Plant Cell Rep 5(3):186–189PubMedCrossRefGoogle Scholar
  23. 23.
    Dixon RA (2005) Engineering of plant natural product pathways. Curr Opin Plant Biol 8(3):329–336PubMedCrossRefGoogle Scholar
  24. 24.
    Bandekar H, Lele SS (2014) Production of flavonol quercetin from cultured plant cells of banyan (Ficus benghalensis L.) Int J Innov Res Sci Eng Technol 3(5):12150–12157Google Scholar
  25. 25.
    Arya D, Patn V, Kant U (2008) In vitro propagation and quercetin quantification in callus cultures of Rasna (Pluchea lanceolata). Indian J Biotechnol 7:383–387Google Scholar
  26. 26.
    Stalikas CD (2007) Extraction, separation, and detection methods for phenolic acids and flavonoids. J Sep Sci 30:3268–3295PubMedCrossRefGoogle Scholar
  27. 27.
    Tsao R, Papadopoulos Y, Yang R, Young JC, McRae K (2006) Isoflavone profiles of red clovers and their distribution in different parts harvested at different growing stages. J Agric Food Chem 54(16):5797–5805PubMedCrossRefGoogle Scholar
  28. 28.
    Ho SC, Chan AS, Ho YP, So EK, Sham A, Zee B, Woo JL (2007) Effects of soy isoflavone supplementation on cognitive function in Chinese postmenopausal women: a double-blind, randomized, controlled trial. Menopause 14(3):489–499PubMedGoogle Scholar
  29. 29.
    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 28:45–53Google Scholar
  30. 30.
    Karuppusamy S (2009) A review on trends in production of secondary metabolites from higher plants by in vitro tissue, organ and cell cultures. J Med Plant Res 3(13):222–1239Google Scholar
  31. 31.
    Ram M, Prasad KV, Kaur C, Singh SK, Arora A, Kumar S (2011) Induction of anthocyanin pigments in callus cultures of Rosa hybrida L. in response to sucrose and ammonical nitrogen levels. Plant Cell Tissue Organ Cult 104:171–179CrossRefGoogle Scholar
  32. 32.
    Curtin C, Zhang W, Franco C (2003) Manipulating anthocyanin composition in Vitis vinifera suspension cultures by elicitation with jasmonic acid and light irradiation. Biotechnol Lett 25(14):1131–1135PubMedCrossRefGoogle Scholar
  33. 33.
    Cai Z, Kastell A, Smetanska I (2014) Chitosan or yeast extract enhance the accumulation of eight phenolic acids in cell suspension cultures of Malus × domestica Borkh. J Hortic Sci Biotechnol 89:93–99. ISSN: 1462-0316CrossRefGoogle Scholar
  34. 34.
    Kiselev KV, Tyunin AP, Manyakhin AY, Zhuravlev YN (2011) Resveratrol content and expression patterns of stilbene synthase genes in Vitis amurensis cells treated with 5-azacytidine. Plant Cell Tissue Organ Cult 105:65–72CrossRefGoogle Scholar
  35. 35.
    Abbott JA, Medina-Bolivar F, Martin EM, Engelberth AS, Villagarcia H, Clausen EC, Carrier DJ (2010) Purification of resveratrol, arachidin-1, and arachidin-3 from hairy root cultures of peanut (Arachis hypogaea) and determination of their antioxidant activity and cytotoxicity. Biotechnol Prog 26:1344–1351PubMedCrossRefGoogle Scholar
  36. 36.
    Cai Z, Kastell A, Speiser C, Smetanska I (2013) Enhanced resveratrol production in Vitis vinifera cell suspension cultures by heavy metals without loss of cell viability. Appl Biochem Biotechnol 171(2):330–340. Scholar
  37. 37.
    Akowuah GA, Ismail Z, Norhayati I, Sadikun A (2005) The effects of different extraction solvents of varying polarities on polyphenols of Orthosiphon stamineus and evaluation of the free radical-scavenging activity. Food Chem 93(2):311–317CrossRefGoogle Scholar
  38. 38.
    Khadeer AMB, Aisha AFA, Nassar ZD, Siddiqui JM, Ismail Z, Omari SMS, Parish CR, Majid AMSA (2011) Cat’s whiskers tea (Orthosiphon stamineus) extract inhibits growth of colon tumor in nude mice and angiogenesis in endothelial cells via suppressing VEGFR phosphorylation. Nutr Cancer 64(1):89–99Google Scholar
  39. 39.
    Kumar J, Gupta PK (2008) Molecular approaches for improvement of medicinal and aromatic plants. Plant Biotechnol Rep 2(2):93–112CrossRefGoogle Scholar
  40. 40.
    Petersen M, Simmonds MS (2003) Rosmarinic acid. Phytochemistry 62(2):121–125PubMedCrossRefGoogle Scholar
  41. 41.
    Kurata H, Achioku T, Okuda N, Furusaki S (1998) Intermittent light irradiation with a second-scale interval enhances caffeine production by Coffea arabica cells. Biotechnol Prog 14(5):797–799PubMedCrossRefGoogle Scholar
  42. 42.
    Begum AN, Nicolle C, Mila I, Lapierre C, Nagano K, Fukushima K, Heinonen SM, Adlercreutz H, Remesy C, Scalbert A (2004) Dietary lignins are precursors of mammalian lignans in rats. J Nutr 134:120–127PubMedCrossRefGoogle Scholar
  43. 43.
    Papandreou D, Zujaja TN, Maitha R (2015) The role of soluble, insoluble fibers and their bioactive compounds in cancer: a mini review. Food Nutr Sci 6:1–11Google Scholar
  44. 44.
    Al-Okbi SY, Mohamed DA, Gabr AMM, Mabrok HB, Hamed TE (2017) Potential hepato- and reno-protective effect of artichoke callus culture and its alcohol extract in galactosamine hydrochloride treated rats. Int J Pharmacogn Phytochem Res 9(3):415–423Google Scholar
  45. 45.
    Mabrok HB, Klopfleisch R, Ghanem KZ, Clavel T, Blaut M, Loh G (2012) Lignan transformation by gut bacteria lowers tumor burden in a gnotobiotic rat model of breast cancer. Carcinogenesis 33(1):203–208PubMedCrossRefGoogle Scholar
  46. 46.
    Gabr AMM, Mabrok HB, Ghanem KZ, Blaut M, Smetanska I (2016) Lignan accumulation in callus and Agrobacterium rhizogenes mediated hairy root cultures of flax (Linum usitatissimum). Plant Cell Tissue Organ Cult 126:255–267CrossRefGoogle Scholar
  47. 47.
    Rates SMK (2001) Plants as sources of drugs. Toxicon 39:603–613PubMedCrossRefGoogle Scholar
  48. 48.
    Yang Y, He F, Yu L, Ji J, Wang Y (2008) Flavonoid accumulation in cell suspension cultures of Glycyrrhiza inflata Batal under optimizing conditions. Z Naturforsch 64:68–72CrossRefGoogle Scholar
  49. 49.
    Zhong JJ (2001) Biochemical engineering of the production of plant-specific secondary metabolites by cell suspension cultures. In: Advances in biochemical engineering/biotechnology, vol 72. Springer, Berlin/Heidelberg, 26 pCrossRefGoogle Scholar
  50. 50.
    Tepe B, Sokmen A (2007) Production and optimisation of rosmarinic acid by Satureja hortensis L. callus cultures. Nat Prod Res 21:1133–1144PubMedCrossRefGoogle Scholar
  51. 51.
    Cai Z, Knorr D, Smetanska I (2012) Enhanced anthocyanins and resveratrol accumulation in Vitis vinifera cell suspension culture by indanoyl-isoleucine, N-linolenoyl-L-glutamine and insect saliva. Enzym Microb Technol 50:29–34. ISSN: 01410229CrossRefGoogle Scholar
  52. 52.
    Konczak-Islam I, Okuno S, Yoshimoto M, Yamakawa O (2013) Composition of phenolics and anthocyanins in a sweet potato cell suspension culture. Biochem Eng J 14:155–161CrossRefGoogle Scholar
  53. 53.
    Rao RS, Ravishankar GA (2002) Plant cell cultures: chemical factories of secondary metabolites. Biotechnol Adv 20:101–153PubMedPubMedCentralCrossRefGoogle Scholar
  54. 54.
    Zenk MH (1977) Plant tissue culture and its bio-technological application. Springer-Verland, Berlin/Heidelberg. 27 pGoogle Scholar
  55. 55.
    Knorr D (1999) Novel approaches in food processing technology: new technologies for preserving foods and modifying function. Curr Opin Biotechnol 10:485–491PubMedPubMedCentralCrossRefGoogle Scholar
  56. 56.
    Riedel H, Cai Z, Kütük O, Smetanska I (2010) Obtaining of phenolic acids from cell cultures of various Artemisia species. Afr J Biotechnol 9(51):8805–8809. ISSN: 1684–5315Google Scholar
  57. 57.
    Szabo E, Thelen A, Petersen M (1999) Fungal elicitor preparations and methyl jasmonate enhance rosmarinic acid accumulation in suspension cultures of Coleus Blumei. Plant Cell Rep 18(6):485–489CrossRefGoogle Scholar
  58. 58.
    Rhodes MJ, Spencer A, Hamill JD (1991) Plant cell culture in the production of flavour compounds. Biochem Soc Trans 19(3):702–706PubMedCrossRefGoogle Scholar
  59. 59.
    Sakamoto K, Iida K, Sawamura K, Hajiro K, Asada Y, Yoshikawa T, Furuya T (1994) Anthocyanin production in cultured cells of Aralia cordata Thunb. Plant Cell Tissue Organ Cult 36(1):1–26CrossRefGoogle Scholar
  60. 60.
    Vasconsuelo A, Giulietti AM, Boland R (2004) Signal transduction events mediating chitosan stimulation of anthraquinone synthesis in Rubia tinctorum. Plant Sci 166:405–413CrossRefGoogle Scholar
  61. 61.
    Kim HK, Sei-Ryang O, 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(1):55–60CrossRefGoogle Scholar
  62. 62.
    Doernenburg H, Knorr D (1996) Production of the phenolic flavour compounds with cultured cells and tissues of Vanilla planifolia species. Food Biotechnol 10:75–92CrossRefGoogle Scholar
  63. 63.
    Ochoa-Villarreal M, Howat S, Hong SM, Jang MO, Jin YW, Lee EK, Loake GJ (2016) Plant cell culture strategies for the production of natural products. BMB Rep 49(3):149–158PubMedPubMedCentralCrossRefGoogle Scholar
  64. 64.
    Zhang HC, Liu JM, Chen HM, Gao CC, HY L, Zhou H, Li Y, Gao SL (2011) Up-regulation of licochalcone A biosynthesis and secretion by Tween 80 in hairy root cultures of Glycyrrhiza uralensis Fisch. Mol Biotechnol 47:50–56PubMedCrossRefGoogle Scholar
  65. 65.
    Shinde AN, Malpathak N, Fulzele D (2010) Impact of nutrient components on production of the phytoestrogens daidzein and genistein by hairy roots of Psoralea corylifolia. J Nat Med 64:346–353PubMedCrossRefGoogle Scholar
  66. 66.
    Condori J, Sivakumar G, Hubstenberger J, Dolan MC, Sobolev VS, Medina-Bolivar F (2010) Induced biosynthesis of resveratrol and the prenylated stilbenoids arachidin-1 and arachidin-3 in hairy root cultures of peanut: effects of culture medium and growth stage. Plant Physiol Biochem 48:310–318PubMedCrossRefGoogle Scholar
  67. 67.
    Bauer N, Kiseljak D, Jelaska S (2009) The effect of yeast extract and methyl jasmonate on rosmarinic acid accumulation in Coleus blumei hairy roots. Biol Plant 53:650–656CrossRefGoogle Scholar
  68. 68.
    Kim YK, Xu H, Park WT, Park NI, Lee SY, Park SU (2010) Genetic transformation of buckwheat (Fagopyrum esculentum M.) with Agrobacterium rhizogenes and production of rutin in transformed root cultures. Aust J Crop Sci 4:485–490Google Scholar
  69. 69.
    Georgieva L, Ivanov I, Marchev A, Aneva I, Denev P, Georgiev V, Pavlov A (2015) Protopine production by fumaria cell suspension cultures: effect of light. Appl Biochem Biotechnol 176(1):287–300. Scholar
  70. 70.
    Georgiev MI, Eibl R, Zhong JJ (2013) Hosting the plant cells in vitro: recent trends in bioreactors. Appl Microbiol Biotechnol 97(9):3787–3800. Scholar
  71. 71.
    Chandra S, Chandra R (2011) Engineering secondary metabolite production in hairy roots. Phytochem Rev 10:371–395CrossRefGoogle Scholar
  72. 72.
    Schreiner M (2005) Vegetable crop management strategies to increase the quantity of phytochemicals. Eur J Nutr 44(2):85–94PubMedCrossRefGoogle Scholar
  73. 73.
    Mohdaly A, Hassanien M, Mahmoud A, Sarhan M, Smetanska I (2013) Phenolics extracted from potato, sugar beet, and sesame processing by-products. Int J Food Prop 16:1148–1168. ISSN: 1094-2912 print/1532-2386 onlineCrossRefGoogle Scholar
  74. 74.
    Ravichandran K, Saw NM, Mohdaly A, Kastell A, Riedel H, Cai Z, Knorr D, Smetanska I (2013) Impact of processing of red beet on betalain content and antioxidant activity. Food Res Int 50(2):670–675. Scholar
  75. 75.
    Hunaefi D, Riedel H, Akumo D, Gruda N, Smetanska I (2013) The effect of lactic acid fermentation on rosmarinic acid and antioxidant properties of in vitro shoot culture of Orthosiphon aristatus as a model study. Food Biotechnol 23:152–177. Scholar
  76. 76.
    Mewis I, Smetanska I, Müller C, Ulrichs C (2011) Specific polyphenolic compounds in cell culture of Vitis Vinifera Gamay Fréaux. Appl Biochem Biotechnol 164:148–161. ISSN: 0273-2289CrossRefPubMedGoogle Scholar
  77. 77.
    Dicosmo F, Misawa M (1995) Plant cell and tissue culture: alternatives for metabolite production. Biotechnol Adv 13:425–435PubMedCrossRefGoogle Scholar
  78. 78.
    Riedel H, Akumo DN, Saw NM, Smetanska I, Neubauer P (2012) Investigation of phenolic acids in suspension cultures of Vitis vinifera stimulated with indanoyl-isoleucine, N-linolenoyl-L-glutamine, malonyl coenzyme A and insect saliva. Metabolites 2:165–177. ISSN: 2218-1989CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Manela N, Oliva M, Ovadia R, Sikron-Persi N, Ayenew B, Fait A, Galili G, Perl A, Weiss D, Oren-Shamir M (2015) Phenylalanine and tyrosine levels are rate-limiting factors in production of health promoting metabolites in Vitis vinifera cv. Gamay Red cell suspension. Front Plant Sci 6:538PubMedPubMedCentralCrossRefGoogle Scholar
  80. 80.
    Shetty K (2001) Biosynthesis and medical applications of rosmarinic acid. J Herbs Spices Med Plants 8(2–3):161–181CrossRefGoogle Scholar
  81. 81.
    Hunaefi D, Gruda N, Smetanska I (2012) In vitro antioxidant activities in sprout culture of Orthosiphon aristatus after treatment with jasmonic acid and yeast extract. Acta Hortic 960:281–288. ISSN: 05677572CrossRefGoogle Scholar
  82. 82.
    Shevchenko Y, Wendt A, Smetanska I (2010) Sprout culture of Stevia rebaudiana Bertoni. In: Geuns J (ed) Stevia science, no fiction. Euprint Heverlee, pp 5–26. ISBN: 978-907-425-307-9Google Scholar
  83. 83.
    Georgiev M, Georgiev V, Weber J, Bley T, Ilieva M, Pavlov A (2008) Agrobacterium rhizogenes-mediated genetic transformations: a powerful tool for the production of metabolites. In: Wolf T, Koch J (eds) Genetically modified plants. Nova Science Publishers, Hauppauge, pp 99–126. ISBN: 978-1-60456-696-3Google Scholar
  84. 84.
    Nermeen MA, Gabr AMM, Ibrahim NM, Shevchenko Y, Smetanska I (2015) Study the effect of hairy root transformation on rapid growth (growth morphology) of Nepeta cataria in vitro cultures. J Innov Pharm Biol Sci, 440–450. ISSN: 2349-2759Google Scholar
  85. 85.
    Gabr A, Ghareeb H, El Shabrawi H, Smetanska I, Bekheet S (2016) Enhancement of silymarin and phenolic compounds accumulation in tissue culture of Milk thistle using elicitors feeding and hairy root cultures. Genet Eng Biotechnol J 14(2):327–333. Scholar
  86. 86.
    Sytar O, Gabr A, Taran N, Smetanska I (2013) Accumulation of phenolic compounds in hairy root culture of Fagopyrum esculentum Moench. Biotechnologica Acta 6(3):75–82. UDK 633.12:631.5:582:581.1CrossRefGoogle Scholar
  87. 87.
    Liu CZ, Guo C, Wang YC, Ouyang F (2002) Effect of light irradiation on hairy root growth and artemisinin biosynthesis of Artemisia annua L. Process Biochem 38:581–585CrossRefGoogle Scholar
  88. 88.
    Sudha CG, Sherina TV, Anu Anand VP, Reji JV, Padmesh P, Soniya EV (2013) Agrobacterium rhizogenes mediated transformation of the medicinal plant Decalepis arayalpathra and production of 2-hydroxy-4-methoxy benzaldehyde. Plant Cell Tiss Organ Cult 112:217–226CrossRefGoogle Scholar
  89. 89.
    Bulgakov VP, Shkryl YN, Veremeichik GN, Gorpenchenko TY, Vereshchagina YV (2013) Recent advances in the understanding of Agrobacterium rhizogenes-derived genes and their effects on stress resistance and plant metabolism. Adv Biochem Eng Biotechnol 134:1–22PubMedGoogle Scholar
  90. 90.
    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 Rubiacordifolia callus cultures transformed with the rolB and rolC genes. J Biotechnol 97:213–221PubMedCrossRefGoogle Scholar
  91. 91.
    Vereshchagina YV, Bulgakov VP, Grigorchuk VP, Rybin VG, Veremeichik GN, Tchernoded GK, Gorpenchenko TY, Koren OG, Phan NHT, Minh NT, Chau LT, Zhuravlev YN (2014) The rolC gene increases caffeoylquinic acid production in transformed artichoke cells. Appl Microbiol Biotechnol 98(18):7773–7780PubMedCrossRefGoogle Scholar
  92. 92.
    Gabr A, Sytar O, Abdelrahman A, Smetanska I (2012) Production of phenolic acids and antioxidant activity in hairy root cultures of different explant sources of common buckwheat (Fagopyrum esculentum M). Aust J Basic Appl Sci 6:577–586. ISSN: 1991-8178Google Scholar
  93. 93.
    Ananga A, Georgiev V, Ochieng J, Phills B, Tsolova V (2013) Production of anthocyanins in grape cell cultures: a potential source of raw material for pharmaceutical, food, and cosmetic industries In: Poljuha D, Sladonja B (eds) The Mediterranean genetic code – grapevine and olive, INTECH Open Access Publisher: Rijeka, Croatia, pp 247–287. ISBN: 978-953-51-1067-5Google Scholar
  94. 94.
    Neumann K-H, Kumar A, Imani J (2009) Plant cell and tissue culture – a tool in biotechnology. Springer, Berlin/HeidelbergGoogle Scholar
  95. 95.
    Zhang ZZ, Li XX, Chu YN, Zhang MX, Wen YQ, Duan CQ, Pan QH (2012) Three types of ultraviolet irradiation differentially promote expression of shikimate pathway genes and production of anthocyanins in grape berries. Plant Physiol Biochem 57:74–83PubMedCrossRefGoogle Scholar
  96. 96.
    Dodds JH, Roberts LW (1985) Experiments in plant tissue culture, 2nd edn. Cambridge University Press, New York. 232 pGoogle Scholar
  97. 97.
    Suzuki M (1995) Enhancement of anthocyanin accumulation by high osmotic stress and low pH in grape cells (Vitis hybrids). J Plant Physiol 147(1):152–155CrossRefGoogle Scholar
  98. 98.
    Do CB, Cormier F (1990) Accumulation of anthocyanins enhanced by a high osmotic potential in grape (Vitis vinifera L.) cell suspensions. Plant Cell Rep 9:143–146PubMedCrossRefGoogle Scholar
  99. 99.
    Kastell A, Smetanska I, Ulrichs C, Cai Z, Mewis I (2013) Effects of phytohormones and jasmonic acid on glucosinolate content in hairy root cultures of Sinapis alba and Brassica rapa. Appl Biochem Biotechnol 169(2):624–635. ISSN: 0273-2289 (print version), ISSN: 1559-0291 (electronic version)PubMedCrossRefGoogle Scholar
  100. 100.
    Tabata H (2006) Production of paclitaxel and the related taxanes by cell suspension cultures of Taxus species. Curr Drug Targets 7(4):453–461PubMedCrossRefGoogle Scholar
  101. 101.
    Zenk MH (1978) The impact of plant cell cultures on industry. In: Thorpe EA (ed) Frontiers of plant tissue culture. The International Association of Plant Tissue Culture, Calgary, pp 1–14Google Scholar
  102. 102.
    Meyer HJ, van Staden J (1995) The in vitro production of an anthocyanin from callus cultures of Oxalis linearis. Plant Cell Tissue Organ Cult 40:55–58CrossRefGoogle Scholar
  103. 103.
    Gan RY, Kuang L, XR X, Zhang YA, Xia EQ, Song FL, Li HB (2010) Screening of natural antioxidants from traditional chinese medicinal plants associated with treatment of rheumatic disease. Molecules 15(9):5988–5997PubMedCrossRefGoogle Scholar
  104. 104.
    Szopa A, Ekiert H (2011) Lignans in Schisandra chinensis in vitro cultures. Pharmazie 66:633–634PubMedGoogle Scholar
  105. 105.
    Havkin-Frenkel D, Podstolski A, Knorr D (1996) Effect of light on vanillin precursors ormation by in vitro cultures of Vanilla planifolia. Plant Cell Tissue Organ Cult 45(2):133–136CrossRefGoogle Scholar
  106. 106.
    Cai Z, Riedel H, Saw NM, Kütük O, Mewis I, Reineke K, Knorr D, Smetanska I (2011) Effects of elicitors and high hydrostatic pressure on secondary metabolism of Vitis vinifera suspension culture. Process Biochem 6(46):1411–1416. Elsevier Science. ISSN: 1359-5113CrossRefGoogle Scholar
  107. 107.
    Sytar O, Cai Z, Marian B, Abhay K, Prasad MNV, Taran N, Smetanska I (2013) Foliar applied nickel on buckwheat (Fagopyrum esculentum) induced phenolic compounds as potential antioxidants. CLEAN – Soil, Air, Water 41(11):1129–1136. Wiley-VCH Verlag, ISSN: 1863-0669CrossRefGoogle Scholar
  108. 108.
    Gabr A, AL-Sayed H, Smetanska I (2012) Effect of drought and salinity stress on total phenolic, flavonoids and flavonols contents and antioxidant activity in in vitro sprout cultures of common buckwheat (Fagopyrum esculentum M.) J Appl Sci Res 8:3934–3942Google Scholar
  109. 109.
    Ahmed AR, Gabr AMM, AL-Sayed HMA, Smetanska I (2012) Effect of drought and salinity stress on total phenolic, flavonoids and flavonols contents and antioxidant activity in in vitro sprout cultures of garden cress (Lepidium sativum). J Appl Sci Res 8:3934–3942. ISSN: 1819-544XGoogle Scholar
  110. 110.
    Hunaefi D, Smetanska I (2013) Tea fermentation effect on rosmarinic acid and antioxidant properties using selected in vitro sprout culture of Orthosiphon aristatus as a model study. 2:167. SpringerPlus
  111. 111.
    Lavola A (1998) Accumulation of flavonoids and related compounds in birch induced by UV-B irradiance. Tree Physiol 18(1):53–58PubMedCrossRefGoogle Scholar
  112. 112.
    Wu J, Lin L (2002) Elicitor-like effects of low-energy ultrasound on plant (Panax ginseng) cells: induction of plant defense responses and secondary metabolite production. Appl Microbiol Biotechnol 59(1):51–57PubMedCrossRefGoogle Scholar
  113. 113.
    Schreiner M, Krumbein A, Knorr D, Smetanska I (2011) Enhancing glucosinolates in root exudates of Brassica rapa ssp. rapa mediated by salicylic acid and methyl jasmonate. J Agric Food Chem 59(4):1400–1405. ISSN: 0021-856123CrossRefPubMedGoogle Scholar
  114. 114.
    Saw NM, Riedel H, Cai Z, Kütük O, Smetanska I (2012) Impact of stress factors on anthocyanin synthesis in grape (Vitis vinifera) cell cultures. Plant Cell Tissue Organ Cult 108:47–54. Springer, ISSN: 1573-5044CrossRefGoogle Scholar
  115. 115.
    Doernenburg H, Knorr D (1997) Challenges and opportunities for metabolite production from plant cell and tissue cultures. Food Technol 51:47–54Google Scholar
  116. 116.
    Gueven A, Knorr D (2011) Isoflavonoid production by soy plant callus suspension culture. J Food Eng 103(3):237–243CrossRefGoogle Scholar
  117. 117.
    Dong J, Wan G, Liang Z (2010) Accumulation of salicylic acid induced phenolic compounds and raised activities of secondary metabolic and antioxidative enzymes in Salvia miltiorrhiza cell culture. J Biotechnol 148:99–104PubMedCrossRefGoogle Scholar
  118. 118.
    Zhang HC, Liu JM, HY L, Gao SL (2009) Enhanced flavonoid production in hairy root cultures of Glycyrrhiza uralensis Fisch by combining the over-expression of chalcone isomerase gene with the elicitation treatment. Plant Cell Rep 28:1205–1213CrossRefPubMedGoogle Scholar
  119. 119.
    Udomsuk L, Jarukamjorn K, Tanaka H, Putalun W (2011) Improved isoflavonoid production in Pueraria candollei hairy root cultures using elicitation. Biotechnol Lett 33:369–374PubMedCrossRefGoogle Scholar
  120. 120.
    Kende H, Zeevaart JAD (1997) The five – classical plant hormones. Plant Cell 9:1197–1210. Scholar
  121. 121.
    Cai Z, Kastell A, Mewis I, Smetanska I (2011) Polysaccharide elicitors enhance anthocyanin and phenolic acid accumulation in cell suspension cultures of Vitis vinifera. Plant Cell Tissue Organ Cult 9:1–9Google Scholar
  122. 122.
    Balasa A (2016) Stress response of plants, metabolite production due to pulsed electric fields. In: Miklavcic D (ed) Handbook of electroporation, pp 1–13., ISBN: 978-3-319-26779-1Google Scholar
  123. 123.
    Abbasi BH, Tian CL, Murch SJ, Saxena PK, Liu CZ (2007) Light enhanced caffeic acid derivatives biosynthesis in hairy root cultures of Echinacea purpurea. Plant Cell Rep 26:1367–1372PubMedCrossRefGoogle Scholar
  124. 124.
    Komaraiah P, Kishor PBK, Carlsson M, Magnusson KE, Mandenius CF (2005) Enhancement of anthraquinone accumulation in Morinda citrifolia suspension cultures. Plant Sci 168:1337–1344CrossRefGoogle Scholar
  125. 125.
    Santamaria AR, Mulinacci N, Valletta A, Innocenti M, Pasqua G (2011) Effects of elicitors on the production of resveratrol and viniferins in cell cultures of Vitis vinifera L. cv Italia. J Agric Food Chem 59:9094–9101PubMedCrossRefGoogle Scholar
  126. 126.
    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 cytochromes P450-catalyzed hydroxylations. Plant Biotechnol 21(5):393–396CrossRefGoogle Scholar
  127. 127.
    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(10):3267–3271CrossRefGoogle Scholar
  128. 128.
    Giner J, Gimeno V, Barbosa-Cánovas GV, Martín O (2016) Effects of pulsed electric field processing on apple and pear polyphenoloxidases. Food Sci Technol Int 7(4):339–345CrossRefGoogle Scholar
  129. 129.
    Toepfl S, Heinz V, Knorr D (2007) History of pulsed electric field application. In: Lelieveld H, Notermans S, De Haan SW (eds) Preservation of food by pulsed electric fields. Woodhead, Cambridge, pp 9–39Google Scholar
  130. 130.
    Ravichandran K, Ahmed A, Knorr D, Smetanska I (2012) The effect of different processing methods on phenolic acids content and antioxidant activity of red beet. Food Res Int 48:16–20. Elsevier, Toronto, ISSN: 0963-9969CrossRefGoogle Scholar
  131. 131.
    Janositz A, Noack AK, Knorr D (2011) Pulsed electric fields and their impact on the diffusion characteristics of potato slices. LWT Food Sci Technol 44:1939–1945CrossRefGoogle Scholar
  132. 132.
    Toepfl S, Siemer C, Heinz V (2014) Effect of high-intensity electric field pulses on solid. In: Sun D (ed) Foods emerging technologies for food processing, Academic Press, UK, pp 147–154. ISBN: 9780124114791CrossRefGoogle Scholar
  133. 133.
    Cai Z, Riedel H, Saw NM, Kütük O, Mewis I, Jäger H, Knorr D, Smetanska I (2010) Effects of pulsed electric field on secondary metabolism of Vitis vinifera L. cv. Gamay Fréaux suspension culture and exudates. Appl Biochem Biotechnol 164:443–453. ISSN: 0273-2289CrossRefPubMedGoogle Scholar
  134. 134.
    Buckow R, Isbarn S, Knorr D, Heinz V, Lehmacher A (2008) Predictive model for inactivation of feline calicivirus, a norovirus surrogate, by heat and high hydrostatic pressure. Appl Environ Microbiol 74:1030–1038PubMedCrossRefGoogle Scholar
  135. 135.
    He X, Zou Y, Yoon WB, Park SJ (2011) Effects of probiotic fermentation on the enhancement of biological and pharmacological activities of Codonopsis lanceolata extracted by high pressure treatment. J Biosci Bioeng 112:188–193PubMedCrossRefGoogle Scholar
  136. 136.
    Balasubramaniam VM, Barbosa-Cánovas GV, Lelieveld HLM (2016) High pressure processing of food: principles, technology and applications. Springer-Verlag New York, 762 pGoogle Scholar
  137. 137.
    Wang JW, Zheng LP, Wu JY, Tan RX (2006) Involvement of nitric oxide in oxidative burst, phenylalanine ammonia-lyase activation and taxol production induced by low-energy ultrasound in Taxus yunnanensis cell suspension cultures. Nitric Oxide Biol Chem 15:351–358CrossRefGoogle Scholar
  138. 138.
    Walker TS, Bais HP, Grotewold E, Vivanco JM (2003) Root exudation and rhizosphere biology. Plant Physiol 132:44–51PubMedPubMedCentralCrossRefGoogle Scholar
  139. 139.
    Cai Zh, Kastell A, Knorr D, Smetanska I. (2011) Exudation: an expanding technique for continuous production and release of secondary metabolites from plant cell suspension and hairy root cultures. Plant Cell Rep., ISSN: 0721-7714 (Print) 1432-203X (Online), Springer, Heidelberg
  140. 140.
    Ye H, Huang LL, Chen SD, Zhong JJ (2004) Pulsed electric field stimulates plant secondary metabolism in suspension cultures of Taxus chinensis. Biotechnol Bioeng 88:788–795PubMedCrossRefGoogle Scholar
  141. 141.
    Zamboni A, Vrhovsek U, Kassemeyer HH, Mattivi F, Velasco R (2006) Elicitor-induced resveratrol production in cell cultures of different grape genotypes (Vitis spp.) Vitis 45:63–68Google Scholar
  142. 142.
    Donnez D, Kim K-H, Antoine S, Conreux A, De Luca V, Jeandet P, Clément C, Courot E (2011) Bioproduction of resveratrol and viniferins by an elicited grapevine cell culture in a 2 L stirred bioreactor. Process Biochem 46:1056–1062CrossRefGoogle Scholar
  143. 143.
    Fornara V, Onelli E, Sparvoli F, Rossoni M, Aina R, Marino G, Citterio S (2008) Localization of stilbene synthase in Vitis vinifera L. during berry development. Protoplasma 233:83–93PubMedCrossRefGoogle Scholar
  144. 144.
    Tassoni A, Fornalè S, Franceschetti M, Musiani F, Michael AJ, Perry B, Bagni N (2005) Jasmonates and Na-orthovanadate promote resveratrol production in Vitis vinifera cv. Barbera cell cultures. New Phytol 166:895–905PubMedCrossRefGoogle Scholar
  145. 145.
    Ferri M, Dipalo SCF, Bagni N, Tassoni A (2011) Chitosan elicits mono-glucosylated stilbene production and release in fed-batch bioreactor cultures of grape cells. Food Chem 124:1473–1479CrossRefGoogle Scholar
  146. 146.
    Hunaefi D, Akumo D, Smetanska I (2013) Effect of fermentation on antioxidant properties of red cabbage. Food Biotechnol 27:66–85. ISSN: 0890-5436 print/1532-4249 onlineCrossRefGoogle Scholar
  147. 147.
    Hunaefi D, Akumo D, Riedel H, Smetanska I (2012) The effect of Lactobacillus plantarum ATCC 8014 and Lactobacillus acidophilus NCFM fermentation on antioxidant properties of selected in vitro sprout culture of Orthosiphon aristatus (Java tea) as a model study. Antioxidants 1:4–32. ISSN: 2076-3921CrossRefPubMedPubMedCentralGoogle Scholar
  148. 148.
    Wu SC, Su YS, Cheng HY (2011) Antioxidant properties of Lactobacillus-fermented and non-fermented Graptopetalum paraguayense E. Walther at different stages of maturity. Food Chem 129:804–809PubMedCrossRefGoogle Scholar
  149. 149.
    Ng CC, Wang CY, Wang YP, Tzeng WS, Shyu YT (2011) Lactic acid bacterial fermentation on the production of functional antioxidant herbal Anoectochilus formosanus Hayata. J Biosci Bioeng 111:289–293PubMedCrossRefGoogle Scholar
  150. 150.
    Katina K, Laitila A, Juvonen R, Liukkonen KH (2007) Bran fermentation as a means to enhance technological properties and bioactivity of rye. Food Microbiol 24:175–186PubMedCrossRefGoogle Scholar
  151. 151.
    Lee IH, Hung LH, Chou CC (2008) Solid-state fermentation with fungi to enhance the antioxidative activity, total phenolic and anthocyanin contents of black bean. Int J Food Microbiol 121(2):150–156PubMedCrossRefGoogle Scholar
  152. 152.
    Cai YZ, Luo Q, Sun M, Corke H (2004) Antioxidant activity and phenolic compounds of 112 traditional Chinese medicinal plants associated with anticancer. Life Sci 74(17):2157–2184PubMedCrossRefGoogle Scholar
  153. 153.
    Halliwell B (2007) Biochemistry of oxidative stress. Biochem Soc Trans 35:1147–1150PubMedCrossRefGoogle Scholar
  154. 154.
    Khlebnikov AI, Schepetkin IA, Domina NG, Kirpotina LN, Quinn MT (2007) Improved quantitative structure-activity relationship models to predict antioxidant activity of flavonoids in chemical, enzymatic, and cellular systems. Bioorg Med Chem 15:1749–1770PubMedCrossRefGoogle Scholar
  155. 155.
    Carocho M, Ferreira ICFR (2013) A review on antioxidants, prooxidants and related controversy: natural and synthetic compounds, screening and analysis methodologies and future perspectives. Food Chem Toxicol 51:15–22PubMedCrossRefGoogle Scholar
  156. 156.
    Furuta S, Nishiba Y, Suda I (1997) Fluorometric assay for screening Antioxidative activity of vegetables. J Food Sci 62:526–528CrossRefGoogle Scholar
  157. 157.
    Mohdaly A, Smetanska I, Ramadan FR, Sarhanb MA, Mahmoud A (2011) Antioxidant potential of sesame (Sesamum indicum) cake extract in stabilization of sunflower and soybean oils. Ind Crop Prod 34:952–959. ISSN: 0926-6690, ElsevierCrossRefGoogle Scholar
  158. 158.
    Ravichandran K, Saw NM, Mohdaly A, Gabr AMM, Kastell A, Riedel H, Cai Zh, Knorr D, Smetanska I (2011) Impact of processing of red beet on betalain content and antioxidant activity. Food Res Int, Special Issue on Stability of Phytochemicals., Elsevier, Toronto, ISSN: 0963-9969
  159. 159.
    Fernandez-Orozco R, Frias J, Muñoz R, Zielinski H (2007) Fermentation as a bio-process to obtain functional soybean flours. J Agric Food Chem 55:8972–8979PubMedCrossRefGoogle Scholar
  160. 160.
    Mohdaly A, Sarhan MA, Mahmoud A, Mohamed FR, Smetanska I (2010) Antioxidant efficacy of potato peels and sugar beet pulp extracts in vegetable oils protection. Food Chem 123:1019–1026. Elsevier, ISSN: 0308-8146CrossRefGoogle Scholar
  161. 161.
    Debnath T, Park PJ, Nath NCD, Samad NB, Park HW, Lim BO (2011) Antioxidant activity of Gardenia jasminoides Ellis fruit extracts. Food Chem 128(3):697–703CrossRefGoogle Scholar
  162. 162.
    Huang D, Ou B, Prior RL (2005) The chemistry behind antioxidant capacity assays. J Agric Food Chem 53(6):1841–1856PubMedCrossRefGoogle Scholar
  163. 163.
    Wang BC, He R, Li ZM (2010) The stability and antioxidant activity of anthocyanins from blueberry. Food Technol Biotechnol 48(1):42–49Google Scholar
  164. 164.
    Sytar O, Borankulova A, ShevchenkoY WA, Smetanska I (2016) Anti-oxidant activity and phenolics composition in Stevia rebaudiana plants of different origin. J Microbiol Biotechnol Food Sci 5(3):221–224CrossRefGoogle Scholar
  165. 165.
    Mohdaly AA, Sarhan MA, Smetanska I, Mahmoud A (2010) Antioxidant properties of various solvent extracts of potato peel, sugar beet pulp and sesame cake. J Sci Food Agric 90:218–226PubMedCrossRefGoogle Scholar
  166. 166.
    Sytar O, Gabr AMM, Smetanska I, Kosyan A (2011) Pigments, phenolic contents and antioxidant activity of buckwheat seedlings under in vivo and in vitro conditions. Agrisafe. Climate change: challenges and opportunities in agriculture, pp 348–352Google Scholar
  167. 167.
    Yu L, Haley S, Perret J, Harris M, Wilson J, Qian M (2002) Free radical properties of wheat extracts. J Agric Food Chem 50(6):1619–1624PubMedCrossRefGoogle Scholar
  168. 168.
    Hunaefi D, Gruda N, Riedel H, Akumo D, Smetanska I (2013d) Improvement in antioxidant activities by lactic acid bacteria. Food Biotechnol 4:279–302. ISSN: 0890-5436 (Print), 1532-4249 (Online)CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Plant Production and Processing, Agricultural Faculty, TriesdorfUniversity of Applied Sciences Weihenstephan-TriesdorfWeidenbachGermany

Personalised recommendations