Abstract
In this work an effective method to start axenic cultures of Verbascum thapsus L. was developed. This allowed to obtain a high percentage of callus generation from leaf explants (around 70%) and to start the cultivation of suspension cultured cells rapidly growing in liquid culture medium. Moreover, the production in these materials of the phenylethanoid glycoside compound verbascoside was verified and quantified ascertaining that both calli and cultured cells maintain the ability to accumulate it at levels similar or superior to those found in plant leaves. Moreover, since HPLC–UV chromatograms of extracts of both calli and suspension cultured cells revealed the presence of other relevant peaks close to the verbascoside one, an HPLC–DAD–MS analysis was carried out leading to identify and quantify three further phenylethanoid glycosides i.e. iso-verbascoside, leucosceptoside A and leucosceptoside B, compounds which had been previously detected and identified also in extracts from leaves. On the whole, the above summarized findings confirm and reinforce the attractiveness and reliability of using in vitro cultures as a convenient source of this class of natural plant products, particularly taking into account that a number of biotechnological approaches allowing to increase the yield of the synthesized phytochemicals are currently available and can be applied in plant tissue culture.
Key message
In vitro cultures may represent a convenient source to produce relevant amount of phenylethanoid glycosides, phytochemicals of remarkable importance in the pharmacological as well as in the nutraceutical field.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Alipieva K, Korkina L, Orhan IE, Georgiev MI (2014) Verbascoside—a review of its occurrence, (bio)synthesis and pharmacological significance. Biotechnol Adv 32(6):1065–1076. https://doi.org/10.1016/j.biotechadv.2014.07.001
Bianchini F, Corbetta F (1977) Health plants of the world, Atlas of medicinal plants. Newsweek Books, New York, p 60
Brown D (1995) Encyclopaedia of herbs and their uses. Dorling Kindersley. Brownstein, London
Budzianowska A, Skrzypczak L, Budzianowski J (2004) Phenylethanoid glucosides from in vitro propagated plants and callus cultures of Plantago lanceolata. Planta Med 70(9):834–840. https://doi.org/10.1055/s-2004-827232
Cardinali A, Pati S, Minervini F, D’Antuono I, Linsalata V, Lattanzio V (2012) Verbascoside, isoverbascoside, and their derivatives recovered from olive mill wastewater as possible food antioxidants. J Agric Food Chem 60:1822–1829. https://doi.org/10.1021/jf204001p
Caruso JL (1971) Bud formation in excised stem segments of Verbascum thapsus. Am J Bot 58:429–431. https://doi.org/10.2307/2441135
Conti F, Abbate G, Alessandrini A (2005). Annotated checklist of the italian vascular flora (An) Palomi editore Roma
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(2):279–288. https://doi.org/10.1007/s11240-011-9919-5
Dembitsky VM (2005) Astonishing diversity of natural surfactants: 5. Biologically active glycosides of aromatic metabolites. Lipids 40:869–900. https://doi.org/10.1007/s11745-005-1449-2
Dimitrova P, Kostadinova E, Milanova V, Alipieva K, Georgiev M, Ivanovska N (2012) Antiinflammatory properties of extracts and compounds isolated from Verbascum xanthophoeniceum Griseb. Phytother Res 26(11):1681–1687. https://doi.org/10.1002/ptr.4641
Donnelly SE, Christopher JL (1998) Pollination in Verbascum thapsus (Scrophulariaceae): the advantage of being tall. Am J Bot 85(11):1618–1625. https://doi.org/10.2307/2446490
Endo T, Goodbody A, Misawa M (1987) Alkaloid production in root and shoot cultures of Catharanthus roseus. Planta Med 53(05):479–482. https://doi.org/10.1055/s-2006-962777
Frezza C, Venditti A, Serafini M, Bianco A (2019a) Phytochemistry, chemotaxonomy, ethnopharmacology, and nutraceutics of lamiaceae. Stud Nat Prod Chem 62:125–178. https://doi.org/10.1016/B978-0-444-64185-4.00004-6
Frezza C, Bianco A, Serafini M, Foddai S, Salustri M, Reverberi M, Gelardi L, Bonina A, Bonina FP (2019b) HPLC and NMR analysis of the phenyl-ethanoid glycosides pattern of Verbascum thapsus L. cultivated in the Etnean area. Nat Prod Res 33(9):1310–1316. https://doi.org/10.1080/14786419.2018.1473398
Fu G, Pang H, Wong YH (2008) Naturally occurring phenylethanoid glycosides: potential leads for new therapeutics current medicinal chemistry. Schiphol 15(25):2592–2613. https://doi.org/10.2174/092986708785908996
Gao H, Cui Y, Kang N, Liu X, Liu Y, Zou Y, Zhang Z, Li X, Yang S, Li J et al (2017) Isoacteoside, a dihydroxyphenylethyl glycoside, exhibits anti-inflammatory effects through blocking TLR4 dimerization. Br J Pharmacol 174(17):2880–2896. https://doi.org/10.1111/bph.13912
Grieve M (1981) A modern herbal, vol II. Dover Publications, New York, pp 562–566
Gross KL (1981) Predictions of fate from rosette size in four ‘biennial’ plant species: Verbascum thapsus, Oenothera biennis, Daucus carota, and Tragopogon dubius. Oecol 48(2):209–213. https://doi.org/10.1007/BF00347966
Gross KL, Werner PA (1978) The biology of Canadian weeds. Can J Plant Sci 58(2):401–413
Gyurkovska V, Alipieva K, Maciuk A, Dimitrova P, Ivanovska N, Haas C, Bley T, Georgiev M (2011) Anti-inflammatory activity of Devil’s claw in vitro systems and their active constituents. Food Chem 125(1):171–178. https://doi.org/10.1016/j.foodchem.2010.08.056
Harris BC (1972) The compleat herbal. Barre Publishers, Barre, p 130
HenryM Roussel JL, Andary C (1987) Verbascoside production in callus and suspension cultures of Hygrophila erecta. Phytochemistry 26(7):1961–1963. https://doi.org/10.1016/s0031-9422(00)81738-0
Hoffman D (1988) The herbal handbook: a user’s guide to medicinal herbalism. Healing Arts Press, Rochester, p 67
Hussain H, Aziz S, Miana GA, Ahmad VU, Anwar S, Ahmed I (2009) Minor chemical constituents of Verbascum thapsus. Biochem Syst Ecol 37:124–126. https://doi.org/10.1016/j.bse.2008.12.007
Inagaki N, Nishimura H, Okada M, Mitsuhashi H (1991) Verbascoside production by plant cell cultures. Plant Cell Rep 9(9):484–487. https://doi.org/10.1007/bf00232101
Jiménez C, Riguera R (1994) Phenylethanoid glycosides in plants: structure and biological activity. Nat Prod Rep 11(6):591–606. https://doi.org/10.1039/np9941100591
Kernan MR, Amarquaye A, Chen JL, Chan J, Sesin DF, Parkinson N, Ye Z, Barrett M, Bales C, Stoddart CA et al (1998) Antiviral phenylpropanoid glycosides from the medicinal plant Markhamia lutea. J Nat Prod 61(5):564–570. https://doi.org/10.1021/np9703914
Koua FHM, Babiker HA, Halfawi A, Ibrahim RO, Abbas FM, Elgaali EI, Khlafallah MM (2011) Phytochemical and biological study of Striga hermonthica (Del) Benth callus and intact plant. Res Pharm Biotechnol 3(7):85–92
Lucas R (1969) Common and uncommon uses of herbs for 295 healthful living. Arco Publishing Company, New York, pp 146–147
Mabey R (1988) The new age herbalist. Macmillan Publishing Company, New York, p 113
Macedo AF, Lage CL, Esquibel MA, de Souza MM, da Silva KL, Niero R, Cechinel-Filho V (2004) Preliminary phytochemical and pharmacological studies on plantlets ofAlternanthera brasilianacultured under different spectral quality of lights. Acta Farm Bonaerense 23(4):515–519
Matkowski A (2004) In vitro isoflavonoid production in callus from different organs of Pueraria lobata (Wild.) Ohwi. J Plant Physiol 161(3):343–346. https://doi.org/10.1078/0176-1617-01145
McCutcheon AR, Ellis SM, Hancock REW, Towers GHN (1993) Antibiotic screening of medicinal plants of the British Columbian native peoples. J Ethnopharmacol 37:213–223. https://doi.org/10.1016/0378-8741(92)90036-Q
McCutcheon AR, Ellis SM, Hancock REW, Towers GHN (1994) Antifungal screening of medicinal plants of the British Columbian native peoples. J Ethnopharmacol 44:157–169. https://doi.org/10.1016/0378-8741(94)01183-4
McCutcheon AR, Roberts TE, Gibbons E, Ellis SM, Babiuk LA, Hancock REW, Towers GHN (1995) Antiviral screening of British Columbian medicinal plants. J Ethnopharmacol 49:101–110. https://doi.org/10.1016/0378-8741(95)90037-3
Mehrotra R, Ahmed B, Vishwakarma RA, Thakur RS (1989) Verbascoside. A new luteolin glycoside from Verbascum thapsus. J Nat Prod 52:640–643. https://doi.org/10.1021/np50063a028
Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15(3):473–497
Nielsen E, Temporiti MEE, Cella R (2019) Improvement of phytochemical production by plant cells and organ culture and by genetic engineering. Plant Cell Rep. https://doi.org/10.1007/s00299-019-02415-z
Null G, Null S (1972) Herbs for the seventies. Robert Speller & Sons, New York, p 129
Parc G, Canaguier A, Landré P, Hocquemiller R, Chriqui D, Meyer M (2002) Production of taxoids with biological activity by plants and callus culture from selected Taxus genotypes. Phytochemistry 59(7):725–730. https://doi.org/10.1016/s0031-9422(02)00043-2
Piątczak E, Grąbkowska R, Wysokińska H (2016) Production of iridoid and phenylethanoid glycosides by in vitro systems of plants from the buddlejaceae, orobanchaceae, and scrophulariaceae families. Bioprocess Plant In Vitro Syst. https://doi.org/10.1007/978-3-319-32004-5_3-1
Picerno P, Autore G, Marzocco S, Meloni M, Sanogo R, Aquino RP (2005) Anti-inflammatory activity of verminoside from Kigelia africana and evaluation of cutaneous irritation in cell cultures and reconstituted human epidermis. J Nat Prod 68:1610–1614. https://doi.org/10.1021/np058046z
Pignatti S (1982) Flora d’Italia. Edagricole, Bologna, p 177
Semenza RJ, Young JA, Evans RA (1978) Influence of light and temperature on the germination and seedbed ecology of common mullein (Verbascum thapsus). Weed Sci 26:577–581. https://doi.org/10.1017/S0043174500064584
Skrzypek Z, Wysokińska H (1999) Accumulation of phenylethanoids in suspension cultures of Penstemon serrulatus Menz. Biotechnol Lett 21:691–693. https://doi.org/10.1023/A:1005554224150
Stancheva N, Weber J, Schulze J, Alipieva K, Ludwig-Müller J, Haas C, Georgiev V, Bley T, Georgiev M (2010) Phytochemical and flow cytometric analyses of Devil’s claw cell cultures. Plant Cell Tissue Organ Cult (PCTOC) 105(1):79–84. https://doi.org/10.1007/s11240-010-9844-z
Turker AU, Camper ND, Gurel E (2001) In vitro culture of common mullen (Verbascum thapsus L.). In Vitro Cell Dev Biol Plant 37:40–43. https://doi.org/10.1079/IVP2000111
Venditti A, Frezza C, Serafini M, Bianco A (2016a) Iridoids and phenylethanoid from Pedicularis kerneri Dalla Torre growing in Dolomites, Italy. Nat Prod Res 30(3):327–331. https://doi.org/10.1080/14786419.2015.1060230
Venditti A, Frezza C, Riccardelli M, Foddai S, Nicoletti M, Serafini M, Bianco A (2016b) Secondary metabolites from Scrophularia canina L. Nat Prod Res 30(14):1665–1669. https://doi.org/10.1080/14786419.2015.1122598
Wang P, Kang J, Zheng R, Yang Z, Lu J, Gao J, Jia Z (1996) Scavenging effects of phenylpropanoid glycosides from Pedicularis on superoxide anion and hydroxyl radical by the Spin trapping method. Biochem Pharmacol 51(5):687–691. https://doi.org/10.1016/S0006-2952(95)02255-4
Warashima T, Miyase T, Ueno A (1991) Iridoid glycosides from Verbascum thapsus L. Chem Pharm Bull 39(12):3261–3264. https://doi.org/10.1248/cpb.39.3261
Warashima T, Miyase T, Ueno A (1992) Phenylethanoid and lignan glycosides from Verbascum thapsus. Phytochem 31(3):961–965. https://doi.org/10.1016/0031-9422(92)80048-J
Zhou B, Bahler BD, Hofmann GA, Mattern MR, Johnson RK, Kingston DGI (1998) Phenylethanoid glycosides from Digitalis purpurea and Penstemon linarioides with PKCα-inhibitory activity. J Nat Prod 61(11):1410–1412. https://doi.org/10.1021/np980147s
Author information
Authors and Affiliations
Contributions
MEET carried out all the experiments on cell cultures and the HPLC quantitative analysis of verbascoside. CF and MB performed the HPLC–DAD–MS analysis. LG provided the plant materials, AD, FPB and EN planned and supervised all the experiments. EN, MEET and CF wrote the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by Ali R. Alan.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Temporiti, M.E.E., Frezza, C., Beccaccioli, M. et al. Production of verbascoside and its analogues in in vitro cultures of Verbascum thapsus L.. Plant Cell Tiss Organ Cult 140, 83–93 (2020). https://doi.org/10.1007/s11240-019-01712-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11240-019-01712-5