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Metabolic Fingerprinting of Leontopodium Species (Asteraceae

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Metabolic Fingerprinting of Leontopodium Species (Asteraceae Phytochemistry 72 (2011) 1379–1389 Contents lists available at ScienceDirect Phytochemistry journal homepage: www.elsevier.com/locate/phytochem Metabolic fingerprinting of Leontopodium species (Asteraceae) by means of 1H NMR and HPLC–ESI-MS Stefan Safer a, Serhat S. Cicek a, Valerio Pieri a, Stefan Schwaiger a, Peter Schneider a, Volker Wissemann b, ⇑ Hermann Stuppner a, a Institute of Pharmacy/Pharmacognosy, Faculty of Chemistry and Pharmacy, Center for Molecular Biosciences Innsbruck (CMBI), University of Innsbruck, Innrain 52c, A-6020 Innsbruck, Austria b Institute of Botany, Systematic Botany Group, Justus-Liebig-University Gießen, Heinrich-Buff-Ring 38, D-35392 Gießen, Germany article info abstract Article history: The genus Leontopodium, mainly distributed in Central and Eastern Asia, consists of ca. 34–58 different Received 30 December 2010 species. The European Leontopodium alpinum, commonly known as Edelweiss, has a long tradition in folk Received in revised form 7 April 2011 medicine. Recent research has resulted in the identification of prior unknown secondary metabolites, Available online 7 May 2011 some of them with interesting biological activities. Despite this, nearly nothing is known about the Asian species of the genus. In this study, we applied proton nuclear magnetic resonance (1H NMR) spectroscopy Keywords: and liquid chromatography–mass spectrometry (LC–MS) metabolic fingerprinting to reveal insights into Leontopodium the metabolic patterns of 11 different Leontopodium species, and to conclude on their taxonomic relation- Asteraceae ship. Principal component analysis (PCA) of 1H NMR fingerprints revealed two species groups. Discrimi- Metabolic fingerprinting 1H NMR nators for these groups were identified as fatty acids and sucrose for group A, and ent-kaurenoic acid and LC–MS derivatives thereof for group B. Five diterpenes together with one sesquiterpene were isolated from Leon- Chemotaxonomy topodium franchetii roots; the compounds were described for the first time for L. franchetii: ent-kaur-16- en-19-oic acid, methyl-15a-angeloyloxy-ent-kaur-16-en-19-oate, methyl-ent-kaur-16-en-19-oate, 8- acetoxymodhephene, 19-acetoxy-ent-kaur-16-ene, methyl-15b–angeloyloxy-16,17-epoxy-ent-kauran- 19-oate. In addition, differences in the metabolic profile between collected and cultivated species could be observed using a partial least squares-discriminant analysis (PLS-DA). PCA of the LC–MS fingerprints revealed three groups. Discriminating signals were compared to literature data and identified as two bisabolane derivatives responsible for discrimination of group A and C, and one ent-kaurenoic acid deriv- ative, discriminating group B. A taxonomic relationship between a previously unidentified species and L. franchetii and Leontopodium sinense could be determined by comparing NMR fingerprints. This finding supports recent molecular data. Furthermore, Leontopodium dedekensii and L. sinense, two closely related species in terms of morphology and DNA-fingerprints, could be distinguished clearly using 1H NMR and LC–MS metabolic fingerprinting. Ó 2011 Elsevier Ltd. All rights reserved. 1. Introduction cies also occur in Europe: The widespread Leontopodium alpinum Cass., and its endemic sister species, Leontopodium nivale (Ten.) The genus Leontopodium R.Br. ex Cassini comprises between 34 Huet. ex Hand.-Mazz., which has a disjunct distribution in the Cen- (Dickoré, unpublished), 41 (Handel-Mazzetti, 1927), and 58 (Wu tral Apennines in Italy and the Pirin Mountains in Bulgaria. For et al., 1994) different species. The main distribution of the genus people living in the European Alps, especially L. alpinum, which is is in Central and Eastern Asia. The centre of diversity is south-wes- known as the Alpine Edelweiss, is a very important part of their tern China, where 15 to 18 different species can be found. Two spe- cultural heritage. The Alpine Edelweiss (L. alpinum Cass. or L. nivale subsp. alpinum (Cass.) Greuter) has a long tradition in folk medicine. References ⇑ Corresponding author. Address: Leopold-Franzens-Universität Innsbruck, Inn- from the year 1582 already mentioned the use of Edelweiss for the rain 52c, Josef-Moeller-Haus, A-6020 Innsbruck, Austria. Tel.: +43 512 507 5300; treatment of diarrhoea and dysentery (Tabernaemontanus, 1582). fax: +43 512 507 2939. Several other applications in traditional medicine for extracts and E-mail addresses: [email protected] (S. Safer), [email protected] (S.S. plant parts of Edelweiss were described throughout the years. Re- Cicek), [email protected] (V. Pieri), [email protected] (S. Schwaiger), [email protected] (P. Schneider), [email protected] cent phytochemical research on L. alpinum has resulted in the detec- (V. Wissemann), [email protected] (H. Stuppner). tion of almost 50 different, partly uncommon secondary 0031-9422/$ - see front matter Ó 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.phytochem.2011.04.006 1380 S. Safer et al. / Phytochemistry 72 (2011) 1379–1389 metabolites, including sesquiterpenes (Dobner et al., 2003a; Gray In our study, we used both 1H NMR spectroscopy and LC–MS in et al., 2000; Schwaiger et al., 2004; Stuppner et al., 2002), diterpenes combination with multivariate statistics as an approach to detect (e.g., Schwaiger et al., 2004), lignanes (Dobner et al., 2003a; Schwai- metabolic fingerprints of species within the genus Leontopodium. ger et al., 2004), benzofurans (e.g., Dobner et al., 2003a), and phenolic We investigated roots of 11 different species, which were collected compounds, such as the novel described leontopodic acids (Schwai- in the field, and the roots of 12 different cultivated species (Ta- ger et al., 2005). Some of these compounds are highly bioactive, ble 1). The main aim of this study was to reveal information about which was demonstrated in several different pharmacological mod- similarities and differences between the species of the genus Leon- els. Hence, antibacterial (Dobner et al., 2003b), antioxidative and topodium by comparing their metabolic fingerprints, and to con- DNA-protecting (Schwaiger et al., 2005), and anti-inflammatory clude on their relationship to each other. (Schwaiger et al., 2004) properties were observed, as well as an enhancement of cholinergic transmission in the brain (Hornick 2. Results and discussion et al., 2008) and an inhibition of intimal hyperplasia of venous by- pass grafts (Reisinger et al., 2009). Despite these results, nearly noth- 2.1. 1H NMR spectroscopy ing is known about bioactive compounds in other Leontopodium species. Until now, only a few phytochemical and pharmacological 2.1.1. Extraction of plant material and acquisition of NMR spectra investigations have been conducted on these species (e.g., Leontopo- Powdered plant material was extracted directly with DMSO-d . dium longifolium Ling: Li et al., 2006; Leontopodium leontopodioides 6 This is adequate for qualitative purposes and simplifies the extrac- Beauverd: Li et al., 1994; Leontopodium andersonii C.B. Clarke: Sch- tion process. DMSO was the most appropriate solvent for our sam- waiger et al., 2010; Leontopodium nanum Hand.-Mazz.: Wang et al., ples; both apolar and polar compounds were extracted, resulting in 2002), although many species were used in Traditional Asian Medi- a broad range of metabolites. The extraction method used was sim- cine, e.g., in Tibet (Kletter and Kriechbaum, 2001). ple and convenient, requiring just a small amount of plant material Whereas the metabolome is clearly defined as the ‘complete suspended in the solvent and extracted on a flat-bed shaker for complement of small molecules present in an organism’ (Hall, 24 h. After centrifugation, an aliquot of the supernatant was ana- 2006), there are different approaches to detect and investigate lysed directly by 1H NMR spectroscopy. Due the use of an auto the metabolome. Throughout the years, various terms were de- sampler, NMR experiments were also accomplished overnight, fined, such as metabonomics, metabolomics, metabolic profiling which was additionally time-saving. Three sample replicates (and and metabolic fingerprinting. A metabolic fingerprinting approach accordingly only two sample replicates for Leontopodium himalaya- is defined as a ‘high-throughput qualitative screening of an organ- num due to a lack of plant material) were used to test the precision ism or tissue with the primary aim of sample comparison and dis- of the method. crimination analysis’ (Hall, 2006). Commonly used techniques for metabolic fingerprinting are LC– MS (liquid chromatography–mass spectrometry) and 1H NMR 2.1.2. Multivariate statistical analysis and pattern recognition (proton nuclear magnetic resonance) spectroscopy. LC–MS as a fin- The spectra were imported into AMIX and pre-processed using gerprinting technique was applied successfully in various fields of the bucketing function. By generating a number of integrated re- plant research, such as chemotaxonomy (Urbain et al., 2009), plant gions for each dataset, complexity of the NMR spectra was reduced. biochemistry (Kim and Park, 2009), food chemistry (Pongsuwan Here, we found a bucket width of d 0.04 suitable for our data. A ta- et al., 2008), and for the quality control of medicinal plants (e.g., ble of bucket-integrated spectra was exported as a spreadsheet. Tianniam et al., 2008). The main advantage of mass spectrometry Principal component analysis (PCA) was performed in SIMCA-P. is its high sensitivity, which allows the detection of low molecular PCA is
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