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In Vitro Cultures of Cyclopia Plants (Honeybush) As a Source Of In vitro Cultures of Cyclopia Plants (Honeybush) as a Source of Bioactive Xanthones and Flavanones Adam Kokotkiewicza, Malgorzata Wnukb, Adam Bucinskib, and Maria Luczkiewicza,* a The Chair and Department of Pharmacognosy, Faculty of Pharmacy, Medical University of Gdansk, al. gen. J. Hallera 107, 80-416 Gdan´ sk, Poland. Fax: +4 85 83 49 31 60. E-mail: [email protected] b The Chair and Department of Biopharmacy, Faculty of Pharmacy, Ludwig Rydygier Collegium Medicum in Bydgoszcz, Nicolaus Copernicus University in Torun, ul. M. Sklodowskiej-Curie 9, 85-094 Bydgoszcz, Poland * Author for correspondence and reprint requests Z. Naturforsch. 64 c, 533 – 540 (2009); received February 5/March 12, 2009 In vitro shoot and callus cultures of the endemic South-African shrubs: Cyclopia inter- media E. Mey., Cyclopia subternata Vogel, and Cyclopia genistoides (L.) Vent. (Fabaceae) were established and examined for the presence of polyphenolic compounds. The xanthones mangiferin and isomangiferin, as well as the fl avanones hesperidin and eriocitrin were iden- tifi ed by LC-ESI-MS and LC-DAD, and analyzed quantitatively by HPLC. The respective intact plants were analyzed for comparison. From all in vitro cultures, the highest levels of mangiferin (1.55%) and isomangiferin (0.56%) were recorded in C. subternata microshoots, compared to 1.31% and 0.49% found in the intact plant. Callus cultures of all species syn- thesized only trace amounts of mangiferin and isomangiferin. Hesperidin and eriocitrin con- tents were signifi canly lower in all in vitro cultures, in comparison to the respective intact plants. Among the obtained in vitro biomasses, the highest hesperidin content was recorded in C. intermedia (0.9%) and C. subternata (0.87%) microshoots, whereas C. subternata callus was characterized by the best growth parameters and highest hesperidin content (0.69%) from all examined Cyclopia calli. Key words: Honeybush, Plant in vitro Culture, LC-ESI-MS Analysis Introduction highly limited, for example to hilltops or marshy areas (Kokotkiewicz and Luczkiewicz, 2009). The genus Cyclopia (Fabaceae family, Podalyr- Since the early 19th century, the herb of a ieae tribe) comprises over 20 species of shrubs, number of Cyclopia species has been used to endemic to the Cape Floristic Region of South produce honeybush herbal tea, traditionally ob- Africa (Joubert et al., 2008a; Kokotkiewicz and tained by the fermentation process, but more re- Luczkiewicz, 2009). Cyclopia plants are character- cently available also in an unfermented version ized by trifoliate leaves and yellow, sweet-scented (the so called “green honeybush”) (Joubert et al., fl owers. The distribution of some species, due 2008a, b; Kokotkiewicz and Luczkiewicz, 2009). to their peculiar environmental requirements, is The commercially most exploited species in- clude C. intermedia E. Mey., C. subternata Vogel, C. genistoides (L.) Vent., and C. sessilifl ora Eckl. & Zeyh. Honeybush infusions have a distinctive Abbreviations: 4-CPPU, N-(2-chloro-4-pyridyl)-N’-phe- sweet, honey-like fl avour, low tannin content, and nyl urea; 2,4-D, 2,4-dichlorophenoxyacetic acid; 2iP, are coffeine-free. In recent years, they are gain- 6-(γ,γ-dimethylallylamino)purine; DW, dry weight; Gi, growth index; HPLC, high-performance liquid chroma- ing popularity as a beverage for everyday use and tography; IBA, indole-3-butyric acid; KN, kinetin; LC- a substitute for tea. Signifi cant amounts of plant DAD, liquid chromatography-diode array detection; material are also exported (Joubert et al., 2008a; LC-ESI-MS, liquid chromatography-electrospray ion- Kokotkiewicz and Luczkiewicz, 2009). ization-mass spectrometry; MS, Murashige and Skoog; NAA, α-naphthaleneacetic acid; PVP, polyvinylpyrro- Apart from a characteristic honey-like taste lidone; SH, Schenk and Hildebrandt; TDZ, thidiazuron; and aroma, honeybush extracts may exert numer- 2,4,5-T, 2,4,5-trichlorophenoxyacetic acid. ous health-promoting activities. Research showed 0939 – 5075/2009/0700 – 0533 $ 06.00 © 2009 Verlag der Zeitschrift für Naturforschung, Tübingen · http://www.znaturforsch.com · D NNC_7_8_2009.indbC_7_8_2009.indb 533533 113.08.20093.08.2009 117:51:467:51:46 534 A. Kokotkiewicz et al. · Xanthones and Flavanones Accumulation in Cyclopia that extracts obtained from Cyclopia plants have Material and Methods substantial antioxidant and antimutagenic po- Seeds and intact plant material tential demonstrated in various in vitro, ex vivo and in vivo models, and thus may be potentially Seeds of C. intermedia, C. subternata, and C. benefi cial in cancer prevention. Moreover, some genistoides were obtained from Silverhill Seeds, honeybush extracts exhibit signifi cant phytoestro- Kenilworth, Cape Town, South Africa. Herbs genic activity (Joubert et al., 2008a; Kokotkiewicz of the respective intact plants were obtained and Luczkiewicz, 2009). from Cape Honeybush Tea, Mossel Bay, South The main chemical components of Cyclopia Africa. plants are polyphenols, represented by xantho- nes, fl avanones, fl avones, fl avonols, isofl avones In vitro cultures and coumestans (Joubert et al., 2008a; Kokotkie- General procedures wicz and Luczkiewicz, 2009). The most important All Cyclopia cultures were cultivated on Schenk compounds, present in highest amount, include and Hildebrandt (SH) (Schenk and Hildebrandt, the xanthones mangiferin and isomangiferin, as 1972) and Murashige and Skoog (MS) (Mu- well as the fl avanone hesperidin (Joubert et al., rashige and Skoog, 1962) media supplemented 2003, 2008b). with growth regulators (Table I) and 3.0% w/v The aim of the present study was to establish, sucrose, and solidifi ed with 0.6% w/v (SH medi- for the fi rst time, in vitro cultures of three Cy- um) or 0.7% w/v (MS medium) of agar. The pH of clopia species (C. subternata, C. intermedia, and the media was adjusted to 5.80 prior to autoclav- C. genistoides) and to evaluate their potential to ing (0.1 MPa, 121 ºC, 20 min). The cultures were produce xanthones and fl avanones. The reason maintained in baby food jars (Sigma-Aldrich, for this is the endemic character of Cyclopia to- USA) in a growth chamber at (24 ± 1) ºC under gether with its chemical uniqueness, manifested continuous light [Phillips white fl uorescent lamps, by the presence of the xanthones mangiferin and 36 W, (88 ± 8) μmol m–2 s–1 light intensity]. isomangiferin, which are rarely recorded in the Fabaceae family (De Nysschen et al., 1996). Until Germination now, in vitro cultures of legume plants have been Prior to sterilization, the seeds were scarifi ed extensively studied in terms of isofl avone produc- with fi ne (P120) sand paper. Next, they were sur- tion (Dixon, 1999), whereas little is known about face-sterilized in 70% ethanol for 1 min, followed the xanthone metabolism within the Fabaceae by 0.5% NaOCl for 30 min. After sterilization, the family. At present, most experiments concerning seeds were rinsed three times with sterile, dou- the xanthone accumulation in plant cell cultures ble distilled water, and put into Petri dishes lined are conducted with the use of plants from the with wet fi lter paper. The seeds were germinated genera Hypericum (Clusiaceae) and Centaurium in the dark at (24 ± 1) ºC. After germination, the (Gentianaceae) (Dias et al., 2000, 2001; Pasqua seeds were moved to a growth chamber for 10 d et al., 2003; Mulinacci et al., 2008). Previous in and the obtained seedlings were then used in fur- vitro experiments concerning Genista plants (Fa- ther experiments. Germination rates and time of baceae) showed that the isofl avonoid content in germination were determined by repeating the the plant biomass can be substantially elevated experiment twice. by establishing in vitro cultures, and further selec- tion of the medium and culture type (Luczkiewicz Callus cultures and Glod, 2003, 2005). Due to positive results (in For callus initiation, cotyledone, hypocotyl and terms of the biofl avonoid content) observed in root fragments of Cyclopia seedlings (0.5 – 1.0 cm) the case of Genista cell lines, it was decided to were placed on solid SH and MS media supple- examine in vitro cultures of legume plants rep- mented with growth regulators alone [0.5 mg/l resenting a non-standard, xanthone-oriented sec- kinetin (KN) and 5.0 mg/l 2,4-dichlorophenoxy- ondary metabolism, namely those of Cyclopia, for acetic acid (2,4-D)] or together with antioxidants: the presence of polyphenolic derivatives, and to 100.0 mg/l L-cysteine or 1000.0 mg/l polyvinylpyr- compare the results with those of the respective rolidone (PVP) (6 media modifi cations). The cul- intact plants. tures were subcultured 6 times onto fresh media NNC_7_8_2009.indbC_7_8_2009.indb 534534 113.08.20093.08.2009 117:51:467:51:46 A. Kokotkiewicz et al. · Xanthones and Flavanones Accumulation in Cyclopia 535 with the same growth regulators and antioxidants Preparation of extracts every 4 weeks. 1000.0-mg portions of pulverized, freeze-dried After 6 passages, the initial calli were trans- plant materials (herbs of the intact plants and in ferred onto solid SH and MS media supplement- vitro biomasses) were extracted with two portions ed with various growth regulators (Table I) and of methanol (2 × 100 ml, 2 × 3.0 h, 40 ºC) and one grown for 6 months (6 subsequent passages), in portion of 90% aqueous methanol (100 ml, 3.0 h, order to determine the conditions for continu- 40 ºC) with the use of a hotplate magnetic stir- ous callus growth. After that period, the in vitro rer. The methanolic extracts were concentrated biomasses were evaluated for growth, structure under reduced pressure (40 ºC). The dry residues and morphological tendencies (Table I). The cal- were diluted in water and partioned into chloro- lus growth indices (Gi) were evaluated after 30 d form and aqueous fractions. The aqueous phases using the Klein formula: Gi = [(Fw – Fo)/Fo]·100, were then vacuum-concentrated (40 ºC), and the where Fw is the fresh weight after 30 d and Fo resulting dry residues were dissolved in 10 ml of is the fresh weight of the inoculum (Zenkteler, methanol (HPLC grade) and stored at – 20 ºC.
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