Abstract
Variation in levels of phenolic acids and flavonoids in Scrophularia striata Boiss. cells cultured in both shake flask and bioreactor in vitro systems, was studied at different growth phases. Four phenolic acids (cinnamic, salicylic, coumaric, and caffeic acid), one stilbenoid (resveratrol), and seven flavonoids (diosmin, rutin, kaempferol, catechin, myricetin, quercetin, and luteolin) were analyzed by high-performance liquid chromatography with photodiode array detection. Production of phenolics in the bioreactor was higher than in shake flasks. Catechin was the most abundant flavonoid in both culture systems, while quercetin, which was detected only in the bioreactor, was the lowest amount represented (32.82 μg g−1 DW). Resveratrol accumulation in bioreactor cultures was 59.84-fold higher than that in shake flasks. Moreover, hierarchical clustering analysis based on Pearson’s correlation coefficient confirmed a positive correlation between the growth phase and some metabolites. The flavonoid accumulation increased with the cells’ physiological age in the bioreactor. Principal component analysis showed that the time course of induction of phenolic acids, flavonoids, and a stilbenoid (resveratrol) was significantly correlated. These findings highlight the capacity of S. striata for large-scale production of desired phenolics using a bioreactor system.
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Agati G, Azzarello E, Pollastri S, Tattini M (2012) Flavonoids as antioxidants in plants: location and functional significance. Plant Sci 196:67–76
Ahmad S, Hahn EJ, PK Y (2008) Aeration volume and photosynthetic photon flux affect cell growth and secondary metabolite contents in bioreactor cultures of Morinda citrifolia. J Plant Biol 51:209–212
Ahmadi-Sakha S, Sharifi M, Niknam V (2016) Bioproduction of phenylethanoid glycosides by plant cell culture of Scrophularia striata Boiss.: from shake-flasks to bioreactor. Plant Cell Tissue Organ Cult 124:275–281
Akkol EK, Goger F, Kosar M, Baser KH (2008) Phenolic composition and biological activities of Salvia halophila and Salvia virgata from Turkey. Food Chem 108:942–949
Ali M, Abbasi BH, Ul-Haq I (2013) Production of commercially important secondary metabolites and antioxidant activity in cell suspension cultures of Artemisia absinthium L. Ind Crop Prod 49:400–406
Andrade SAL, Silveira APD, Jorge RA, Abreu MF (2008) Cadmium accumulation in sunflower plants influenced by arbuscular mycorrhiza. Int J Phytoremediat 10(1):1–13
Ardeshiry Lajimi A, Rezaei Tavirani M, Mortazavi SA, Barzegr MSH, Rezaee MB (2010) Study of anti-cancer property of Scrophularia striata extract on the human astrocytoma cell line (1321). Iran J Pharm Res 9:403–410
Azadmehr A, Afshari A, Baradaran B, Hajiaghaee R, Rezazadeh S, Monsef-Esfahani H (2009) Suppression of nitric oxide production in activated murine peritoneal macrophages in-vitro and ex-vivo by Scrophularia striata ethanolic extract. J Ethnopharmacol 6:166–169
Bahrami AM, Valadi A (2010) Effect of Scrophularia striata ethanolic leaves extracts on Staphylococcus areus. Int J Pharmacol 6:431–434
Chang CC, Yang MH, Wen HM, Chern JC (2002) Estimation of total flavonoid content in propolis by two complementary colorimetric methods. J Food Drug Anal 10:178–182
Chen WH, Xu CM, Zeng JL, Zhao B, Wang XD, Wang YC (2007) Improvement of echinacoside and acteoside production by two-stage elicitation in cell suspension culture of Cistanche deserticola. World J Microbiol Biotechnol 23:1451–1458
Donnez D, Kim KH, Antoine S, Conreux A, De Luca V, Jeandt P, Clement C, Courot E (2011) Bioproduction of resveratrol and viniferins by an elicited grapevine cell culture in a 2 L stirred bioreactor. Process Biochem 46:1056–1062
Dzialo M, Mierziak J, Korzun U, Preisner M, Szopa J, Kulma A (2016) The potential of plants phenolics in prevention and therapy of skin disorders. Int J Mol Sci 17:160. https://doi.org/10.3390/ijms17020160
Eibl R, Eibl D (2008) Design of bioreactors suitable for plant cell and tissue cultures. Phytochem Rev 7:593–598
Federici E, Touché A, Choquart S, Avanti O, Fay L, Offord E, Courtois D (2003) High isoflavone content and estrogenic activity of 25 year-old Glycine max tissue cultures. Phytochemistry 64:717–724
Georgiev M, Ludwig-Müller J, Weber J, Stancheva N, Bley T (2011) Bioactive metabolite production and stress-related hormones in Devil’s claw cell suspension cultures grown in bioreactors. Appl Microbiol Biotechnol 89:1683–1691
Gill SS, Anjum NA, Hasanuzzaman M, Gil R, Trivedi DK, Ahmad I, Pereira E, Tuteja N (2013) Glutathione and glutathione reductase: a boon in disguise for plant abiotic stress defense operations. Plant Physiol Biochem 70:204–212
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930
Gudej J, Tomczyk M (2004) Determination of flavonoids, tannins and ellagic acid in leaves from Rubus L. species. Arch Pharm Res 27:1114–1119
Hussain MS, Fareed S, Ansari S, Rahman M, Ahmad IZ, Saeed M (2012) Current approaches toward production of secondary plant metabolites. J Pharm Bioall Sci 4(1):10–20
Jang YS, Baque A, Shiragi HK, Moh SH, Lee EJ, Peak KY (2013) CO2-enriched microenvironment induces biosynthesis of anthraquinones, phenolics and flavonoids in bioreactor cell suspension cultures of Morinda citrifolia (L.): the role of antioxidants and enzymes. Aust J Crop Sci 7:1606–1616
Jeandet P, Clement C, Courot E (2014) Resveratrol production at large scale using plant cell suspensions. Eng Life Sci 14:622–632
Keinänen M, Oladham NJ, Baldwin LT (2001) Rapid HPLC screening of jasmonate induced increases in tobacco alkaloids, phenolics and diterpene glycosides in Nicotiana attenuate. J Agric Food Chem 49:3553–3558
Khanpour-Ardestani N, Sharifi M, Behmanesh M (2015) Establishment of callus and cell suspension culture of Scrophularia striata Boiss.: an in vitro approach for acteoside production. Cytotechnology 67:475–485
Li H, Piao XC, Gao R, Jin M, Jiang J, Lian ML (2016) Effect of several physicochemical factors on callus biomass and bioactive compound accumulation of R. sachalinensis bioreactor culture. In Vitro Cell Dev Biol-Plant 52:241–250
Luczkiewicz M, Glod D (2005) Morphogenesis-dependent accumulation of phytoestrogens in Genista tinctoria in-vitro cultures. Plant Sci 168:967–979
Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassay of tobacco tissue culture. Physiol Plantarum 15:473–497
Ouyang J, Wang XD, Zhao B, Wang YC (2005) Enhanced production of phenylethanoid glycosides by precursor feeding to cell culture of Cistanche deserticola. Process Biochemistry 40:3480–3484
Owen RW, Haubner R, Mier W, Giacosa A, Hull WE, Spiegelhalder B, Bartsch H (2003) Isolation, structure elucidation and antioxidant potential of the major phenolic and flavonoid compounds in brined olive drupes. Food Chem Toxicol 41:703–717
Paek KY, Chakrabarty D, Hahn EJ (2005) Application of bioreactor systems for large scale production of horticultural and medicinal plants. Plant Cell Tissue Organ Cult 81:287–300
Petrussa E, Braidot E, Zancani M, Peresson C, Bertolini A, Patui S, Vianello A (2013) Plant flavonoids—biosynthesis, transport and involvement in stress responses. Int J Mol Sci 14:14950–14973
Rao SR, Ravishankar GA (2002) Plant cell cultures: chemical factories of secondary metabolites. Biotechnol Adv 20:101–153
Safavi F, Meighani H, Ebrahimi P, Hafez Ghoran S (2012) Antioxidant and antibacterial activity of Scrophularia striata. Res Pharm Sci 7:S582
Shoohani B, Hemati AA, Taheri Moghadam M (2010) Effects of Scrophularia striata extract on wound healing in rabbit. J Ilam Univ. Med Sci 17:9–16
Sivakumar G (2006) Bioreactor technology: a novel industrial tool for high-tech production of bioactive molecules and biopharmaceuticals from plant roots. Biotechnol J 1:1419–1427
Tanideh N, Haddadi MH, Rokni-Hosseini MH, Hosseinzadeh M, Mehrabani D, Sayehmiri K, Kohhi-Hosseinabadi O (2015) The healing effect of Scrophularia Striata on experimental burn wounds infected to Pseudomonas Aeruginosa in rat. World J Plast Surg 4:16–22
Taveira M, Pereira DM, Sousa C, Ferrers F, Andarde PB, Martins A, Pereira JA, Valentao P (2009) In vitro cultures of Brassica oleracea L. var. costata DC: potential plant bioreactor for antioxidant phenolic compounds. J Agric Food Chem 57:1247–1252
Varsha S, Shaily G, Kishan GR (2011) Increased puerarin biosynthesis during in vitro shoot formation in Pueraria tuberose grown in bioreactor with aeration. Physiol Mol Biol Plants 17:87–92
Vijaya SN, Udayasri PVV, Aswani KY, Ravi BB, Phani KY, Vijay VM (2010) Advancements in the production of secondary metabolites. J Nat Prod 3:112–123
Yansong M, Yu D, Qiao-Yang S, Zeng-Fu X, Liwen J (2008) Plant bioreactors for pharmaceuticals. Biotechnol Genet Eng Rev 25:363–363
Yusuf NA, Annuar MSM, Khalid N (2013) Physical stress for overproduction of biomass and flavonoids in cell suspension cultures of Boesenbergia rotunda. Acta Physiol Plant 35:1713–1719
Zamanian-Azodi M, Ardeshirylajimi A, Ahmadi N, Rezaee MB, Jalilian FA, Khodarahmi R (2013) Antibacterial effects of Scrophularia striata seed aqueous extract on Staphylococcus aureus. J Paramed Sci 4:58–63
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Editor: Neftali Ochoa-Alejo
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Ahmadi-Sakha, S., Sharifi, M., Niknam, V. et al. Phenolic compounds profiling in shake flask and bioreactor system cell cultures of Scrophularia striata Boiss. In Vitro Cell.Dev.Biol.-Plant 54, 444–453 (2018). https://doi.org/10.1007/s11627-018-9899-9
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DOI: https://doi.org/10.1007/s11627-018-9899-9