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Anthocyanins and Flavonols from the Blue Flowers of Six Meconopsis

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Anthocyanins and Flavonols from the Blue Flowers of Six Meconopsis Biochemical Systematics and Ecology 86 (2019) 103925 Contents lists available at ScienceDirect Biochemical Systematics and Ecology journal homepage: www.elsevier.com/locate/biochemsyseco Anthocyanins and flavonols from the blue flowers ofsix Meconopsis species T in Bhutan ∗ Tsukasa Iwashinaa, , Kazutaka Yokoyamab, Rinchen Yangzomc, Takayuki Mizunoa, Hari Prasad Devkotad, Yoshinori Muraia, Kencho Dorjic, Choki Wangmoc, Choki Gyeltshenc a Department of Botany, National Museum of Nature and Science, Amakubo 4-1-1, Tsukuba, Ibaraki, 305-0005, Japan b Graduate School of Agriculture, Ibaraki University, Ami, Ibaraki, 300-0393, Japan c National Biodiversity Centre, Ministry of Agriculture and Forests, Serbithang, Thimpu, 873, Bhutan d Graduate School of Pharmaceutical Sciences, Kumamoto University, Oe-honmachi 5-1, Kumamoto, 862-0973, Japan ARTICLE INFO ABSTRACT Keywords: Blue flowers of six Bhutani Meconopsis species, M. bhutanica, M. bella, M. horridula, M. simplicifolia, M. primulina Meconopsis and M. polygonoides, were surveyed for anthocyanins and other flavonoids. Four anthocyanins were isolated and M. bhutanica identified as cyanidin 3-O-sambubioside-7-O-glucoside (1), cyanidin 3-O-[xylosyl-(1 → 2)-(6″-malonylgluco- Papaveraceae side)]-7-O-glucoside (2), cyanidin 3-O-sambubioside (4) and cyanidin 3-O-[xylosyl-(1 → 2)-(6″-malonylgluco- Bhutan side)] (5). On the other hand, 12 flavonols were isolated from their Meconopsis species with various combination Anthocyanins and characterized as kaempferol 3-O-glycosides (8–12), kaempferol 3,7-O-glycosides (13–16), quercetin 3-O- Flavonols glycosides (17 and 18) and isorhamnetin 3-O-glycoside (19). Of six Meconopsis species which were surveyed in this experiment, anthocyanin and flavonol composition of five species except for M. horridula was clarified for the first time. Their Meconopsis species showed the different flavonoid profiles, respectively, and flavonoid di- versity within the glycosylation level of Meconopsis flowers were indicated. 1. Subject and source Meconopsis polygonoides (Prain) Prain, upper Chorotang, Paro Valley, Bhutan, 3850 m alt., 1 July 2013; between Sol Yaktsa – Thongbula, Mt. The genus Meconopsis (Papaveraceae) consists of ca. 150 species and Jomolhari range, Bhutan. ca. 4500 m alt., 8 July 2015. Voucher spe- is growing in 2000–5000 m alt. of the Himalayan Mountains and ad- cimens were deposited in the Herbarium of National Biodiversity jacent Highland (Grey-Wilson, 2014). In Bhutan, ca. 15 Meconopsis Centre (THIM), Bhutan. species are distributed (Long, 1984). Recently, a new species, Meco- nopsis bhutanica Tosh.Yoshida & Grey-Wilson was found in Bhutan 2. Previous work (Yoshida and Grey-Wilson, 2012). Flowers of six Meconopsis species which were analysed in this survey were collected in following site and Flower colours of Meconopsis species are diversified from white, date: Meconopsis bhutanica Tosh.Yoshida & Grey-Wilson, near Jan- yellow, red, purple to blue. Of their flower colours, blue flowers oftwo gothan, Mt. Jomolhari range, Bhutan, ca. 4400 m alt., 6 July 2015; Meconopsis species, M. horridula Hook.f. & Thomson and M. betonicifolia Meconopsis bella Prain, Paro Valley, Bhutan ca. 4100 m alt., 2 July 2013; Franch. have been surveyed for the pigments (Takeda et al., 1996; near Jangothang, Mt. Jomolhari range, Bhutan ca. 4400 m alt., 6 July Tanaka et al., 2001; Yoshida et al., 2006). Their pigment composition 2015; Meconopsis horridula Hook.f. & Thomson, Paro Valley, Bhutan, ca. was essentially the same and cyanidin 3-O-[xylosyl-(1 → 2)-(6″-mal- 4100 m, 2 July 2013; near Lake Tso Phu, Mt. Jomolhari range, Bhutan, onylglucoside)]-7-O-glucoside (2), and two flavonols, kaempferol 3-O- ca. 4300 m alt., 6 July 2015; Meconopsis simplicifolia (D.Don) Walp., gentiobioside (10) and kaempferol 3-O-xylosylgentiobioside (12), were upper Chorotang, Paro Valley, Bhutan, ca. 4050 and 4200 m alt., 1 and isolated (Takeda et al., 1996). Moreover, cyanidin 3-O-sambubioside-7- 2 July 2013; between Sol Yaktsa – Thongbula, Mt. Jomolhari range, O-glucoside (1) and kaempferol 3-O-glucosyl-(1 → 6)-galactoside were Bhutan, ca. 4500 m alt., 8 July 2015; Meconopsis primulina Prain, upper found in the blue flowers of M. grandis Prain, together with 2 and 10 Chorotang, Paro Valley, Bhutan, 3850 m alt., 1 July 2013; Jangothang, (Takeda et al., 1996; Tanaka et al., 2001; Yoshida et al., 2006). Re- Mt. Jomolhari range, Bhutan, ca. 3900 m alt., 5 July 2015; and cently, anthcyanins of red flowers of Meconopsis wallichii Hook. were ∗ Corresponding author. E-mail address: [email protected] (T. Iwashina). https://doi.org/10.1016/j.bse.2019.103925 Received 5 June 2019; Received in revised form 29 June 2019; Accepted 13 July 2019 0305-1978/ Crown Copyright © 2019 Published by Elsevier Ltd. All rights reserved. T. Iwashina, et al. Biochemical Systematics and Ecology 86 (2019) 103925 reported to be cyanidin 3-O-sambubioside (5), 3-O-glucoside and 3-O- (succcinylsambubioside) without the presence of other flavonoids (Iwashina et al., 2018). Although yellow flower pigment of M. panicu- lata (D.Don) Prain has been characterized as herbacetin (8-hydro- xykaempferol) 3-O-glucoside (Harborne, 1969), it was more recently shown to be the mixture of 6-hyroxykaempferol 3-O-glucoside and 3-O- sophoroside, together with minor kaempferol 3-O-glucoside (9) and 3- O-sophoroside (8)(Yokoyama et al., 2018). Similarly, those of yellow flowers of M. integrifolia were identified as quercetin 3-O-gentiobioside and three 3-O-(acetylgentiobiosides) (Huang et al., 2015; Yokoyama et al., 2018). 3. Present study Dry flowers of M. bhutanica (6.91 g), M. bella (2.44 g), M. horridula (2.14 g), M. simplicifolia (2.45 g), M. primulina (5.13 g) and M. poly- gonoides (0.35 g) were extracted with MeOH/HCOOH (92:8), respec- tively. The concentrated extracts were applied to preparative paper chromatography using solvent systems, BAW (n-BuOH/HOAc/ H2O = 4:1:5, upper phase), 15% HOAc and then re-BAW. Isolated an- thocyanins and flavonols were purified by Sephadex LH-20 column chromatography using solvent systems, MeOH/H2O/HCOOH (70:25:5) for anthocyanins and 70% MeOH for flavonols. Qualitative HPLC of crude extracts, and isolated anthocyanins and flavonols were performed using a Shimadzu HPLC/photodiode array (PDA) system (Shimadzu, Kyoto) with Inertsil ODS-4 column (I.D. 10 × 250 mm, GL Sciences, Co. Ltd., Tokyo) (flow-rate, 1.0 ml min−1, detection wave-length, 530 nm) and elution with H3PO4/HOAc/MeCN/ H2O (3:8:6:83) (solv. I) for anthocyanins, and detection wave-length, 350 nm, and elution with MeCN/H2O/H3PO4 (20:80:0.2) (solv. II) for flavonols. Anthocyanins and flavonols were identified by UV spectral survey according Mabry et al. (1970), LC-MS, acid hydrolysis, NMR and/or HPLC and TLC comparisons with authentic samples from the blue flowers of Meconopsis grandis (Takeda et al., 1996; Tanaka et al., 2001), red flowers of Meconopsis wallichii (Iwashina et al., 2018) and Aeschynanthus spp. (Gesneriaceae) (Iwashina et al., unpublished data). LC-MS was performed on a Shimadzu HPLC/UV–vis/ESI MS system using Inertsil ODS-4 column (I.D. 2.1 × 100 mm, GL Sciences, Co. Ltd.) (flow-rate, 0.2 ml min−1, detection wave-length, 530 or 350 nm) and elution with MeCN/H2O/HCOOH (12:87:1) for anthocyanins, and MeCN/H2O/HCOOH (15:80:5) for flavonols. Acid hydrolysis were performed in 12%HCl, 100 °C, 30 min. After cooling in water and shaking with diethyl ether (flavonols) or isoamyl alcohol (anthocya- nins), aglycones and anthocyanidins were migrated to the organic layer, and sugars were left in aqueous layer. Anthocyanidins and fla- vonol aglycones were identified by HPLC comparisons with authentic samples. On the other hand, sugars were characterized by paper chro- matographic comparisons with authentic samples using solvent sys- tems, BBPW (n-BuOH/benzene/pyridine/H2O = 5:1:3:3) and BTPW (n- BuOH/toluene/pyridine/H2O = 5:1:3:3). Sugar spots were visualized by spraying 1% methanolic aniline hydrochloride on the chromato- grams and heating. TLC was performed with Cellulose Plastic Plate (Merck, Germany) using solvent systems, BAW, BEW (n-BuOH/EtOH Fig. 1. Chemical structures of anthocyanins and flavonols from the blue flowers 1 13 of six Bhutani Meconopsis species. H2O = 4:1:2.2) and 15% HOAc. H and C NMR were recorded on a 1 13 Brucker AV-600 in pyridine-d5 at 600 MHz ( H NMR) and 150 MHz ( C NMR). Seven anthocyanins were found in the blue flowers of six Bhutani species except for M. polygonoides with various combinations. They Meconopsis species, i.e. M. bhutanica, M. bella, M. horridula, M. simpli- were isolated and characterized as kaempferol 3-O-sophoroside (8), cifolia, M. primulina and M. polygonoides by HPLC survey. Of their an- kaempferol 3-O-glucoside (9), kaempfeol 3-O-gentiobioside (10), thocyanins, major four were isolated and identified as cyanidin 3-O- kaempferol 3-O-sambubioside (11), kaempferol 3-O-xylosylgentiobio- sambubioside-7-O-glucoside (1), cyanidin 3-O-[xylosyl-(1 → 2)-(6″- side (12), kaempferol 3,7-di-O-glucoside (13), kaempferol 3-O-gentio- malonylglucoside)]-7-O-glucoside (2), cyanidin 3-O-[xylosyl-(1 → 2)- bioside-7-O-glucoside (14), kaempferol 3-O-sambubioside-7-O-gluco- (6″-malonylglucoside)] (4) and cyanidin 3-O-sambubioside (5)(Fig. 1). side (15), kaempferol 3-O-arabinosylglucoside-7-O-glucoside (16), Other three anthocyanins, 3, 6 and 7, could not be isolated for small quercetin 3-O-sambubioside (17), quercetin 3-O-glucoside (18) and amounts. isorhamnetin 3-O-glycoside (19)(Fig. 1). Twelve flavonol glycosides were found in five Bhutani Meconopsis 2 T. Iwashina, et al. Biochemical Systematics and Ecology 86 (2019) 103925 Table 1 Of twelve flavonols, 10 and 12 have been isolated from the flowers Distribution of anthocyanins in the flowers of six Bhutani Meconopsis species. of M. horridula, M. grandis and M.
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