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Chemical constituents from Bupleurum chinese and their chemotaxonomic significance
Biochemical Systematics and Ecology 86 (2019) 103929
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Chemical constituents from Bupleurum chinese and their chemotaxonomic significance
T
Danqi Lia, Dandan Yuea,b, Da Liua,c, Xuegui Liua,c,∗∗, Shaojiang Songd,∗ a
Institute of Functional Molecules, Shenyang University of Chemical Technology, Shenyang, Liaoning, 110142, PR China College of Applied Chemistry, Shenyang University of Chemical Technology, Shenyang, Liaoning, 110142, PR China c College of Pharmaceutical and Biological Engineering, Shenyang University of Chemical Technology, Shenyang, Liaoning, 110142, PR China d School of Traditional Chinese Materia Medica, Key Laboratory of Structure-Based Drug Design and Discovery, Ministry of Education, Shenyang Pharmaceutical University, Shenyang, Liaoning, 110016, PR China b
ARTICLE INFO
ABSTRACT
Keywords: Bupleurum chinense DC Apiaceae Chemotaxonomy Phytochemical constituents
A phytochemical investigation of the roots of Bupleurum chinese DC. led to the isolation of eighteen compounds, including three chromones (1–3), seven flavonoids (4–10), one dihydrochalcone (11), two phenylpropanoid glycosides (12–13), one lignan (14), three sterols (15–17) and one stilbenoid (18). Their structures were elucidated on the basis of NMR spectroscopic analysis and comparison with literature data. Compounds 6–7, 11–14 and 18 were firstly reported from the genus Bupleurum and the family Apiaceae. Moreover, the chemotaxonomic value of the isolates was also discussed.
1. Subject and source The genus of Bupleurum, belonging to the family Apiaceae, is represented by 200 species in the world, which is widely distributed in the Northern Hemisphere, North Africa and Eurasia (Yao et al., 2013). The genus comprises annual and perennial species with bisexual flowers, containing five stamens, cremocarps, simple, long, and slender leaves (Neves and Watson, 2004). Bupleurum species are commonly used as medicinal plants with a variety of bioactive constituents and abundant pharmacological activities (Ashour and Wink, 2011). The roots of Bupleurum chinense DC., a well-known Traditional Chinese Medicine, was primarily used to treat cold fevers, chills, congestion and stuffiness in the chest and hypochondria in the form of pharmaceutical preparations for more than 2000 years (Tan et al., 2008). According to the Chinese Pharmacopoeia of 2015, Bupleurum chinense DC. and Bupleurum scorzonerifolium Willd. were regarded as the standard medical plants (Zhu et al., 2009). With the development of modern pharmacology, recent studies have indicated that the roots of B. chinense possesses a wide range of effcts, such as anti-inflammatory, antitumor, antidepressant, antipyretic, antiviral, antihepatitis, anticonvlsive, hepatoprotective and immunostimulant activities and so on (B.C. Yuan et al., 2017; Kuang et al., 2009; Ashour and Wink, 2011). In order to clarify the taxonomic characters of B. chinense, the systematic phytochemical investigation and
chemotaxonomic relationship were carried out. The roots of B. chinense were purchased from Tong-ren Pharmaceutical Company (Co. Ltd, Shenyang, China) and were authenticated by Prof. Jin-Cai Lu, Department of Pharmaceutical Botany, School of Traditional Chinese Materia Medica, Shenyang Pharmaceutical University. A voucher specimen (No. 1012002) was maintained at the School of Traditional Chinese Materia Medica, Shenyang Pharmaceutical University (see Fig. 1). 2. Previous work Previous phytochemical investigations on genus Bupleurum revealed the presence of various active constituents, including triterpene saponins (Kok et al., 1995; Lin et al., 2013), lignans (Estevez-Braun et al., 1996), flavonoids and related chromones (Zhu et al., 2017), sterols (Pistelli et al., 2005), coumarins (Pistelli et al., 1996), polyacetylenes (Huang et al., 2009), volatile oils (Bertoli et al., 2004) and polysaccharides (Tong et al., 2014). Our group had identified numerous compounds from the roots of B. chinense, including seven new oleanane triterpenoids and one new lignan (Li et al., 2015, 2016). The chemotaxonomy of the flavonoids from aerial part of B. chinense had been investigated (Zhang et al., 2007). But, there are less reports about the constitutes in the roots of B. chinense, which one also have important chemotaxonomical significance.
Corresponding author. Corresponding author. Institute of Functional Molecules, College of Pharmaceutical and Biological Engineering, Shenyang University of Chemical Technology, Shenyang, Liaoning, 110142, PR China. E-mail addresses: [email protected] (X. Liu), [email protected] (S. Song). ∗
∗∗
https://doi.org/10.1016/j.bse.2019.103929 Received 1 July 2019; Received in revised form 5 August 2019; Accepted 10 August 2019 Available online 28 August 2019 0305-1978/ © 2019 Published by Elsevier Ltd.
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Fig. 1. Compounds 1–18 from B. chinense.
3. Present work
(1.3 g) and Fr. 3-2-4-4 (0.8 g) were further purifed by semi-preparative HPLC with MeOH/H2O (v/v = 60 : 40) to give compounds 6 (15 mg), 7 (9 mg), 8 (13 mg) and 9 (11 mg), respectively. Fr. 3-3 (28.1 g) was fractionated using silica gel (200–300 mesh) column chromategraphy (CC) with CH2Cl2/MeOH (v/v = 20 : 1, 15 : 1, 10 : 1, 8 : 1, 5 : 1 and 0 : 1) to obtain subfractions (Fr. 3-3-1-Fr. 3-4-4), respectively. Fr. 3-3-2 was repeatedly subjected to Sephadex LH-20 column chromategraphy (CC) with MeOH/H2O (v/v = 60 : 40), and isolated by semipreparative HPLC (35% MeOH/H2O) to yield compounds 17 (11 mg) and 18 (10 mg). Similarly, compounds 10 (9 mg), 12 (8 mg) and 13 (17 mg) were obtained from Fr. 3-3-2 by Sephadex LH-20 column chromategraphy (CC) with MeOH/H2O (v/v = 60 : 40) and semipreparative HPLC (40% MeOH/H2O). In addition, Fr. 3-3-4 yielded one compound 14 (12 mg), each of which was purified by semipreparative HPLC with MeOH/H2O (v/v = 60 : 40). Based on spectroscopic analysis (1H NMR, 13C NMR, HRESIMS and CD) and comparison with the published data (Supporting materials), the isolated compounds were identified as eugenin (1) (Anh et al., 2014), 2, 5-dimethyl-7-hydroxycheomone (2) (Hang et al., 2008), saikochrome-A (3) (Kobayashi et al., 1990), isorhamnetin (4) (Ashour et al., 2018), luteolin (5) (Lin et al., 2014), vitexin-2-O-rhamnoside (6) (Jhoo et al., 2007), kaempferol-3-β-D-(6-O-trans-p-coumaroyl) glucopyranoside (7) (Tsukamoto et al., 2004), isorhamnetin-3-O-β-D-rutinoside (8) (Kuang et al., 2009), kaempferol-3-O-β-D-glucopyranoside (9) (Bencheraiet et al., 2012), apigenin-6, 8-di-C-β-D-glucopyranoside
The air-dried roots (9.5 kg) of B. chinense was extracted using homogenate extraction with 75% ethanol at room temperature for three times. The combined extract solution was evaporated under reduced pressure by a rotary evaporator to obtain 800.0 g residue. The brown residue was fractionated on silica gel (200–300 mesh) column chromategraphy (CC) and eluted with CH2Cl2/MeOH (v/v = 100:1, 50:1, 30:1, 20:1, 10:1 and 0:1) to obtain five fractions (Fr. 1–5). Fr. 3 (88 g) was further separated by polyamide (200–300 mesh) column chromatography (CC) eluting with a stepwise gradient system of MeOH/H2O (v/v = 30 : 70, 50 : 50, 70 : 30 and 100 : 0) to give four fractions (Fr. 31-Fr. 3–4). Fr. 3–2 (21.2 g) was chromatographed over a silica gel (200–300 mesh) column with CH2Cl2/MeOH (v/v = 30 : 1, 20 : 1, 15 : 1, 10 : 1, 8 : 1, 5 : 1 and 0 : 1) to afford four fractions (Fr. 3-2-1-Fr. 3-24). Fr. 3-2-3 (5.4 g) was passed over reversed phase C-18 silica gel column chromatography (CC) with MeOH/H2O mixtures (v/v = 60 : 40) and further purified by semi-preparative HPLC using MeOH/H2O (v/v = 70 : 30) as mobile phase to get compounds 1 (9 mg), 2 (10 mg), 3 (8 mg), 4 (8 mg), 5 (9 mg) and 11 (12 mg). Similarly, the purification of Fr. 3-2-2 (1.5 g) by semi-preparative HPLC with MeOH/H2O (v/ v = 65 : 35) afforded compounds 16 (9 mg). Fr. 3-2-4 (6.8 g) was subjected to reversed phase C-18 silica gel column chromatography (CC) and washed with MeOH/H2O (v/v = 30 : 70, 60 : 40 and pure MeOH) to afford eight subfractions (Fr. 3-2-4-1-Fr. 3-2-4-8). Fr. 3-2-4-3 2
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(10) (Zhang et al., 2008), 1-(2, 4-dihydroxyphenyl)-3-hydroxy-3-(4′hydroxyphenyl)- 1-propanone (11) (Rafi et al., 2002), isoacteoside (12) (Chae et al., 2005), martynoside (13) (E. Fuji et al., 2018), 7R, 8Sdehydrodiconiferyl alcohol (14) (Deyama et al., 1987), β-amyrin (15) (Zhang et al., 2016), α-spinasterol (16) (Li et al., 1997), α-spinasterol-3O-β-D-glucoside (17) (Ashour et al., 2012), α-viniferin (18) (GonalezSarrías et al., 2011).
L. (Verbenaceae) (Saidi et al., 2018), Lagotis brevituba Maxim. (Scrophulariaceae) (X. Yuan et al., 2017), Roylea cinerea (D. Don) Baillon (Lamiaceae) (Sharma et al., 2017), Marrubium vulgare L. (Lamiaceae) (Masoodi et al., 2015), Strobilanthes cusia (Nees) Kuntze (Acanthaceae) (Gu et al., 2014), Calceolaria talcana Grau & C. Ehrhart (Scrophulariaceae) (Muñoz et al., 2013), Salvia viridis L. (Lamiaceae) (Rungsimakan and Rowan, 2014). These findings provided new information on the chemical aspects of B. chinense, and compounds 12 and 13 might serve as a chemotaxonomic marker for distinguishing B. chinense. Lignans are ubiquitously distributed throughout the plant kingdom and have many biological activities. The major subclasses of lignans in this genus are dibenzylbutyrolactone, arylnaphthalenes, aryltetralinelactones and tetrahydrofurofuranes derivatives, depending on the pattern of additional bridging between the two β-linked phenylpropanoid units (Yang et al., 2017). Compound 14 was acquired from Prunus tomentosa Thunb. (Rosaceae) (Liu et al., 2014), Sambucus williamsii Hance (Adoxaceae) (Xiao et al., 2014), Viburnum erosum Thunb. (Caprifoliaceae) (In et al., 2015), Tribulus terrestris L. (Zygophyllaceae) (Hong et al., 2013), Euonymus alatus (Thunb.) Sieb.(Celastraceae) (Jeong et al., 2011). The study exhibited the taxonomic relationships between Apiaceae and other families. Furthermore, compound 14 could be considered as specific markers of B. chinense. Stilbenoids are very rarely reported from other species of genus Bupleurum. This is the first report of a stilbenoid obtained from a species of genus Bupleurum. According to previous research, compound 18 was discovered from Shorea roxburghii G. Don (Dipterocarpaceae) (Kiyofumi et al., 2017), Caragana sinica (Buc'hoz) Rehder (Fabaceae) (Jeong et al., 2017), Dipterocarpus tuberculatus Roxb (Dipterocarpaceae) (Surapinit et al., 2014), Carex humilis Leyss (Cyperaceae) (Seo et al., 2017). Therefore, compound 18 may be of vital importance as the chemotaxonomic marker of B. chinense. In conclusion, the results of this study enriched the phytochemical diversity and added the knowledge about the chemistry of B. chinense. In addition, the presence of compounds 1, 9, 17 demonstrated that B. chinense has a close chemotaxonomic relationship with other Bupleurum species. Compound 6–7, 11–14, 18 had not been found in this genus Bupleurum or in the family Apiaceae. Therefore, These constituents might have chemotaxonomic significance for the identification of B. chinense. However, further studies about the chemical makeup of other Bupleurum species are required.
4. Chemotaxonomic significance In the present phytochemical study, eighteen compounds were obtained from the roots of B. chinense, including three chromones (1–3), seven flavonoids (4–10), one dihydrochalcone (11), two phenylpropanoid glycosides (12–13), one lignan (14), three sterols (15–17), one stilbenoid (18). The findings would enrich chemical diversity of B. chinense and provide evidences for further chemotaxonomic studies. To the best of our knowledge, compounds eugenin (1), 2,5-dimethyl-7-hydroxycheomone (2), saikochrome-A (3), isorhamnetin (4), luteolin (5), isorhamnetin-3-O-β-D-rutinoside (8), kaempferol-3-O-β-Dglucopyranoside (9), apigenin-6, 8-di-C-β-D-glucopyranoside (10), βamyrin (15), α-spinasterol (16), α-spinasterol-β-D-glucoside (17) have been previously reported from B. chinense and the genus Bupleurum. Among them, compounds 1, 9, 17 were previously reported from different species of the same genus. In brief, compounds 1, 9, 17 were previously isolated from Bupleurum scorzonerifolium Willd. (Chang et al., 2003), Bupleurum fruticosum L. (Bencheraiet et al., 2012), Bupleurum marginatum Wall. ex DC. (Ashour et al., 2012), respectively. Thus, the presence of compounds 1, 9, 17 indicated the close phylogenetic relationship among these species of Bupleurum. Significantly, vitexin-2-O-rhamnoside (6), kaempferol-3-β-D-(6-O-trans-p-coumaroyl) glucopyranoside (7), 1-(2,4- dihydroxyphenyl)-3-hydroxy-3-(4′-hydroxyphenyl)-1-propanone (11), isoacteoside (12), martynoside (13), 7R, 8S-dehydrodiconiferyl alcohol (14), α-viniferin (18) were new findings in the genus Bupleurum and the family of Apiaceae. Flavonoids are widely distributed in the genus Bupleurum as the characteristic constituents, which were widely used as vital chemotaxonomical markers to distinguish between different Bupleurum species (Zhang et al., 2007). The flavonoids in the genus Bupleurum are derivatives of the flavonol aglycones, such as kaempferol, isorhamnetin, quercetin, apigenin, acacetin, chrysin, luteolin and tamarixetin (Ashour et al., 2012). Compouds 6 and 7 are flavonoids which have never been found in other plants of Apiaceae family. In addition, compounds 6 and 7 were both obtained from Crataegus pinnatifida Bge. Var. Major N. E. Br. (Rosaceae) (Luo et al., 2015) and Fragaria ananassa Duch. cv. Tochiotome. (Rosaceae) (Tsukamoto et al., 2004). Compoud 6 was also previously isolated from Beta vulgaris var. cicla L. (Amaranthaceae) (Ninfali et al., 2017), Neptunia oleracea Lour. (Fabaceae) (Lee et al., 2016), Tetrastigma hemsleyanum Diels et Gilg (Vitaceae) (Sun et al., 2013), and compoud 7 had been reported from Croton gratissimus Burch. (Euphorbiaceae) (Pudumo et al., 2018). Therefore, the isolation of compouds 6 and 7 could be considered to be the chemotaxonomic signifcance and serve as valuable chemotaxonomic markers for distinguishing B. chinense. Compound 11 was isolated from Glycyrrhiza glabra L. (Fabaceae) (Rafi et al., 2002) and Pisum sativum L. (Fabaceae) (Evidente et al., 2010). Collectively, all of the above facts indicated some genetic relationship between Apiaceae and Fabaceae family. The phenylpropanoid glycosides isolated herein are broadly distributed among some plant families. The literatures revealed that compounds 12 and 13 were both recorded from Sesamum indicum L. (Pedaliaceae) (Y. Fuji et al., 2018), Adansonia digitata L. (Malvaceae) (Li et al., 2017). In addition, compound 12 was isolated from Lathraea squamaria L. (Orobanchaceae) (Dankova et al., 2016), Gynura cusimbua (Asteraceae) (Ma et al., 2017.), Incarvillea compacta Maxim. (Bignoniaceae) (Zhao et al., 2017), Syringa vulgaris L. (Oleaceae) (Tóth et al., 2016), Amphilophium paniculatum (L.) Kunth (Bignoniaceae) (Samy et al., 2015). Compound 13 was discovered from Citharexylum spinosum
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Chemical constituents from Bupleurum chinese and their chemotaxonomic significance
T
Danqi Lia, Dandan Yuea,b, Da Liua,c, Xuegui Liua,c,∗∗, Shaojiang Songd,∗ a
Institute of Functional Molecules, Shenyang University of Chemical Technology, Shenyang, Liaoning, 110142, PR China College of Applied Chemistry, Shenyang University of Chemical Technology, Shenyang, Liaoning, 110142, PR China c College of Pharmaceutical and Biological Engineering, Shenyang University of Chemical Technology, Shenyang, Liaoning, 110142, PR China d School of Traditional Chinese Materia Medica, Key Laboratory of Structure-Based Drug Design and Discovery, Ministry of Education, Shenyang Pharmaceutical University, Shenyang, Liaoning, 110016, PR China b
ARTICLE INFO
ABSTRACT
Keywords: Bupleurum chinense DC Apiaceae Chemotaxonomy Phytochemical constituents
A phytochemical investigation of the roots of Bupleurum chinese DC. led to the isolation of eighteen compounds, including three chromones (1–3), seven flavonoids (4–10), one dihydrochalcone (11), two phenylpropanoid glycosides (12–13), one lignan (14), three sterols (15–17) and one stilbenoid (18). Their structures were elucidated on the basis of NMR spectroscopic analysis and comparison with literature data. Compounds 6–7, 11–14 and 18 were firstly reported from the genus Bupleurum and the family Apiaceae. Moreover, the chemotaxonomic value of the isolates was also discussed.
1. Subject and source The genus of Bupleurum, belonging to the family Apiaceae, is represented by 200 species in the world, which is widely distributed in the Northern Hemisphere, North Africa and Eurasia (Yao et al., 2013). The genus comprises annual and perennial species with bisexual flowers, containing five stamens, cremocarps, simple, long, and slender leaves (Neves and Watson, 2004). Bupleurum species are commonly used as medicinal plants with a variety of bioactive constituents and abundant pharmacological activities (Ashour and Wink, 2011). The roots of Bupleurum chinense DC., a well-known Traditional Chinese Medicine, was primarily used to treat cold fevers, chills, congestion and stuffiness in the chest and hypochondria in the form of pharmaceutical preparations for more than 2000 years (Tan et al., 2008). According to the Chinese Pharmacopoeia of 2015, Bupleurum chinense DC. and Bupleurum scorzonerifolium Willd. were regarded as the standard medical plants (Zhu et al., 2009). With the development of modern pharmacology, recent studies have indicated that the roots of B. chinense possesses a wide range of effcts, such as anti-inflammatory, antitumor, antidepressant, antipyretic, antiviral, antihepatitis, anticonvlsive, hepatoprotective and immunostimulant activities and so on (B.C. Yuan et al., 2017; Kuang et al., 2009; Ashour and Wink, 2011). In order to clarify the taxonomic characters of B. chinense, the systematic phytochemical investigation and
chemotaxonomic relationship were carried out. The roots of B. chinense were purchased from Tong-ren Pharmaceutical Company (Co. Ltd, Shenyang, China) and were authenticated by Prof. Jin-Cai Lu, Department of Pharmaceutical Botany, School of Traditional Chinese Materia Medica, Shenyang Pharmaceutical University. A voucher specimen (No. 1012002) was maintained at the School of Traditional Chinese Materia Medica, Shenyang Pharmaceutical University (see Fig. 1). 2. Previous work Previous phytochemical investigations on genus Bupleurum revealed the presence of various active constituents, including triterpene saponins (Kok et al., 1995; Lin et al., 2013), lignans (Estevez-Braun et al., 1996), flavonoids and related chromones (Zhu et al., 2017), sterols (Pistelli et al., 2005), coumarins (Pistelli et al., 1996), polyacetylenes (Huang et al., 2009), volatile oils (Bertoli et al., 2004) and polysaccharides (Tong et al., 2014). Our group had identified numerous compounds from the roots of B. chinense, including seven new oleanane triterpenoids and one new lignan (Li et al., 2015, 2016). The chemotaxonomy of the flavonoids from aerial part of B. chinense had been investigated (Zhang et al., 2007). But, there are less reports about the constitutes in the roots of B. chinense, which one also have important chemotaxonomical significance.
Corresponding author. Corresponding author. Institute of Functional Molecules, College of Pharmaceutical and Biological Engineering, Shenyang University of Chemical Technology, Shenyang, Liaoning, 110142, PR China. E-mail addresses: [email protected] (X. Liu), [email protected] (S. Song). ∗
∗∗
https://doi.org/10.1016/j.bse.2019.103929 Received 1 July 2019; Received in revised form 5 August 2019; Accepted 10 August 2019 Available online 28 August 2019 0305-1978/ © 2019 Published by Elsevier Ltd.
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Fig. 1. Compounds 1–18 from B. chinense.
3. Present work
(1.3 g) and Fr. 3-2-4-4 (0.8 g) were further purifed by semi-preparative HPLC with MeOH/H2O (v/v = 60 : 40) to give compounds 6 (15 mg), 7 (9 mg), 8 (13 mg) and 9 (11 mg), respectively. Fr. 3-3 (28.1 g) was fractionated using silica gel (200–300 mesh) column chromategraphy (CC) with CH2Cl2/MeOH (v/v = 20 : 1, 15 : 1, 10 : 1, 8 : 1, 5 : 1 and 0 : 1) to obtain subfractions (Fr. 3-3-1-Fr. 3-4-4), respectively. Fr. 3-3-2 was repeatedly subjected to Sephadex LH-20 column chromategraphy (CC) with MeOH/H2O (v/v = 60 : 40), and isolated by semipreparative HPLC (35% MeOH/H2O) to yield compounds 17 (11 mg) and 18 (10 mg). Similarly, compounds 10 (9 mg), 12 (8 mg) and 13 (17 mg) were obtained from Fr. 3-3-2 by Sephadex LH-20 column chromategraphy (CC) with MeOH/H2O (v/v = 60 : 40) and semipreparative HPLC (40% MeOH/H2O). In addition, Fr. 3-3-4 yielded one compound 14 (12 mg), each of which was purified by semipreparative HPLC with MeOH/H2O (v/v = 60 : 40). Based on spectroscopic analysis (1H NMR, 13C NMR, HRESIMS and CD) and comparison with the published data (Supporting materials), the isolated compounds were identified as eugenin (1) (Anh et al., 2014), 2, 5-dimethyl-7-hydroxycheomone (2) (Hang et al., 2008), saikochrome-A (3) (Kobayashi et al., 1990), isorhamnetin (4) (Ashour et al., 2018), luteolin (5) (Lin et al., 2014), vitexin-2-O-rhamnoside (6) (Jhoo et al., 2007), kaempferol-3-β-D-(6-O-trans-p-coumaroyl) glucopyranoside (7) (Tsukamoto et al., 2004), isorhamnetin-3-O-β-D-rutinoside (8) (Kuang et al., 2009), kaempferol-3-O-β-D-glucopyranoside (9) (Bencheraiet et al., 2012), apigenin-6, 8-di-C-β-D-glucopyranoside
The air-dried roots (9.5 kg) of B. chinense was extracted using homogenate extraction with 75% ethanol at room temperature for three times. The combined extract solution was evaporated under reduced pressure by a rotary evaporator to obtain 800.0 g residue. The brown residue was fractionated on silica gel (200–300 mesh) column chromategraphy (CC) and eluted with CH2Cl2/MeOH (v/v = 100:1, 50:1, 30:1, 20:1, 10:1 and 0:1) to obtain five fractions (Fr. 1–5). Fr. 3 (88 g) was further separated by polyamide (200–300 mesh) column chromatography (CC) eluting with a stepwise gradient system of MeOH/H2O (v/v = 30 : 70, 50 : 50, 70 : 30 and 100 : 0) to give four fractions (Fr. 31-Fr. 3–4). Fr. 3–2 (21.2 g) was chromatographed over a silica gel (200–300 mesh) column with CH2Cl2/MeOH (v/v = 30 : 1, 20 : 1, 15 : 1, 10 : 1, 8 : 1, 5 : 1 and 0 : 1) to afford four fractions (Fr. 3-2-1-Fr. 3-24). Fr. 3-2-3 (5.4 g) was passed over reversed phase C-18 silica gel column chromatography (CC) with MeOH/H2O mixtures (v/v = 60 : 40) and further purified by semi-preparative HPLC using MeOH/H2O (v/v = 70 : 30) as mobile phase to get compounds 1 (9 mg), 2 (10 mg), 3 (8 mg), 4 (8 mg), 5 (9 mg) and 11 (12 mg). Similarly, the purification of Fr. 3-2-2 (1.5 g) by semi-preparative HPLC with MeOH/H2O (v/ v = 65 : 35) afforded compounds 16 (9 mg). Fr. 3-2-4 (6.8 g) was subjected to reversed phase C-18 silica gel column chromatography (CC) and washed with MeOH/H2O (v/v = 30 : 70, 60 : 40 and pure MeOH) to afford eight subfractions (Fr. 3-2-4-1-Fr. 3-2-4-8). Fr. 3-2-4-3 2
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(10) (Zhang et al., 2008), 1-(2, 4-dihydroxyphenyl)-3-hydroxy-3-(4′hydroxyphenyl)- 1-propanone (11) (Rafi et al., 2002), isoacteoside (12) (Chae et al., 2005), martynoside (13) (E. Fuji et al., 2018), 7R, 8Sdehydrodiconiferyl alcohol (14) (Deyama et al., 1987), β-amyrin (15) (Zhang et al., 2016), α-spinasterol (16) (Li et al., 1997), α-spinasterol-3O-β-D-glucoside (17) (Ashour et al., 2012), α-viniferin (18) (GonalezSarrías et al., 2011).
L. (Verbenaceae) (Saidi et al., 2018), Lagotis brevituba Maxim. (Scrophulariaceae) (X. Yuan et al., 2017), Roylea cinerea (D. Don) Baillon (Lamiaceae) (Sharma et al., 2017), Marrubium vulgare L. (Lamiaceae) (Masoodi et al., 2015), Strobilanthes cusia (Nees) Kuntze (Acanthaceae) (Gu et al., 2014), Calceolaria talcana Grau & C. Ehrhart (Scrophulariaceae) (Muñoz et al., 2013), Salvia viridis L. (Lamiaceae) (Rungsimakan and Rowan, 2014). These findings provided new information on the chemical aspects of B. chinense, and compounds 12 and 13 might serve as a chemotaxonomic marker for distinguishing B. chinense. Lignans are ubiquitously distributed throughout the plant kingdom and have many biological activities. The major subclasses of lignans in this genus are dibenzylbutyrolactone, arylnaphthalenes, aryltetralinelactones and tetrahydrofurofuranes derivatives, depending on the pattern of additional bridging between the two β-linked phenylpropanoid units (Yang et al., 2017). Compound 14 was acquired from Prunus tomentosa Thunb. (Rosaceae) (Liu et al., 2014), Sambucus williamsii Hance (Adoxaceae) (Xiao et al., 2014), Viburnum erosum Thunb. (Caprifoliaceae) (In et al., 2015), Tribulus terrestris L. (Zygophyllaceae) (Hong et al., 2013), Euonymus alatus (Thunb.) Sieb.(Celastraceae) (Jeong et al., 2011). The study exhibited the taxonomic relationships between Apiaceae and other families. Furthermore, compound 14 could be considered as specific markers of B. chinense. Stilbenoids are very rarely reported from other species of genus Bupleurum. This is the first report of a stilbenoid obtained from a species of genus Bupleurum. According to previous research, compound 18 was discovered from Shorea roxburghii G. Don (Dipterocarpaceae) (Kiyofumi et al., 2017), Caragana sinica (Buc'hoz) Rehder (Fabaceae) (Jeong et al., 2017), Dipterocarpus tuberculatus Roxb (Dipterocarpaceae) (Surapinit et al., 2014), Carex humilis Leyss (Cyperaceae) (Seo et al., 2017). Therefore, compound 18 may be of vital importance as the chemotaxonomic marker of B. chinense. In conclusion, the results of this study enriched the phytochemical diversity and added the knowledge about the chemistry of B. chinense. In addition, the presence of compounds 1, 9, 17 demonstrated that B. chinense has a close chemotaxonomic relationship with other Bupleurum species. Compound 6–7, 11–14, 18 had not been found in this genus Bupleurum or in the family Apiaceae. Therefore, These constituents might have chemotaxonomic significance for the identification of B. chinense. However, further studies about the chemical makeup of other Bupleurum species are required.
4. Chemotaxonomic significance In the present phytochemical study, eighteen compounds were obtained from the roots of B. chinense, including three chromones (1–3), seven flavonoids (4–10), one dihydrochalcone (11), two phenylpropanoid glycosides (12–13), one lignan (14), three sterols (15–17), one stilbenoid (18). The findings would enrich chemical diversity of B. chinense and provide evidences for further chemotaxonomic studies. To the best of our knowledge, compounds eugenin (1), 2,5-dimethyl-7-hydroxycheomone (2), saikochrome-A (3), isorhamnetin (4), luteolin (5), isorhamnetin-3-O-β-D-rutinoside (8), kaempferol-3-O-β-Dglucopyranoside (9), apigenin-6, 8-di-C-β-D-glucopyranoside (10), βamyrin (15), α-spinasterol (16), α-spinasterol-β-D-glucoside (17) have been previously reported from B. chinense and the genus Bupleurum. Among them, compounds 1, 9, 17 were previously reported from different species of the same genus. In brief, compounds 1, 9, 17 were previously isolated from Bupleurum scorzonerifolium Willd. (Chang et al., 2003), Bupleurum fruticosum L. (Bencheraiet et al., 2012), Bupleurum marginatum Wall. ex DC. (Ashour et al., 2012), respectively. Thus, the presence of compounds 1, 9, 17 indicated the close phylogenetic relationship among these species of Bupleurum. Significantly, vitexin-2-O-rhamnoside (6), kaempferol-3-β-D-(6-O-trans-p-coumaroyl) glucopyranoside (7), 1-(2,4- dihydroxyphenyl)-3-hydroxy-3-(4′-hydroxyphenyl)-1-propanone (11), isoacteoside (12), martynoside (13), 7R, 8S-dehydrodiconiferyl alcohol (14), α-viniferin (18) were new findings in the genus Bupleurum and the family of Apiaceae. Flavonoids are widely distributed in the genus Bupleurum as the characteristic constituents, which were widely used as vital chemotaxonomical markers to distinguish between different Bupleurum species (Zhang et al., 2007). The flavonoids in the genus Bupleurum are derivatives of the flavonol aglycones, such as kaempferol, isorhamnetin, quercetin, apigenin, acacetin, chrysin, luteolin and tamarixetin (Ashour et al., 2012). Compouds 6 and 7 are flavonoids which have never been found in other plants of Apiaceae family. In addition, compounds 6 and 7 were both obtained from Crataegus pinnatifida Bge. Var. Major N. E. Br. (Rosaceae) (Luo et al., 2015) and Fragaria ananassa Duch. cv. Tochiotome. (Rosaceae) (Tsukamoto et al., 2004). Compoud 6 was also previously isolated from Beta vulgaris var. cicla L. (Amaranthaceae) (Ninfali et al., 2017), Neptunia oleracea Lour. (Fabaceae) (Lee et al., 2016), Tetrastigma hemsleyanum Diels et Gilg (Vitaceae) (Sun et al., 2013), and compoud 7 had been reported from Croton gratissimus Burch. (Euphorbiaceae) (Pudumo et al., 2018). Therefore, the isolation of compouds 6 and 7 could be considered to be the chemotaxonomic signifcance and serve as valuable chemotaxonomic markers for distinguishing B. chinense. Compound 11 was isolated from Glycyrrhiza glabra L. (Fabaceae) (Rafi et al., 2002) and Pisum sativum L. (Fabaceae) (Evidente et al., 2010). Collectively, all of the above facts indicated some genetic relationship between Apiaceae and Fabaceae family. The phenylpropanoid glycosides isolated herein are broadly distributed among some plant families. The literatures revealed that compounds 12 and 13 were both recorded from Sesamum indicum L. (Pedaliaceae) (Y. Fuji et al., 2018), Adansonia digitata L. (Malvaceae) (Li et al., 2017). In addition, compound 12 was isolated from Lathraea squamaria L. (Orobanchaceae) (Dankova et al., 2016), Gynura cusimbua (Asteraceae) (Ma et al., 2017.), Incarvillea compacta Maxim. (Bignoniaceae) (Zhao et al., 2017), Syringa vulgaris L. (Oleaceae) (Tóth et al., 2016), Amphilophium paniculatum (L.) Kunth (Bignoniaceae) (Samy et al., 2015). Compound 13 was discovered from Citharexylum spinosum
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