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Screening Effective Antifungal Substances from the Bark and Leaves of Zanthoxylum Avicennae by the Bioactivity-Guided Isolation Method

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Screening Effective Antifungal Substances from the Bark and Leaves of Zanthoxylum Avicennae by the Bioactivity-Guided Isolation Method molecules Article Screening Effective Antifungal Substances from the Bark and Leaves of Zanthoxylum avicennae by the Bioactivity-Guided Isolation Method 1,2, 1,2, 1,2 1,2 1,2 Yongtong Xiong y , Guan Huang y, Zongli Yao , China Zhao , Xiang Zhu , Qinglai Wu 1,2,*, Xudong Zhou 3,* and Junkai Li 1,2,* 1 School of Agriculture, Yangtze University, Jingzhou 434025, China; [email protected] (Y.X.); [email protected] (G.H.); [email protected] (Z.Y.); [email protected] (C.Z.); [email protected] (X.Z.) 2 Institute of Pesticides, Yangtze University, Jingzhou 434025, China 3 TCM and Ethnomedicine Innovation & Development Laboratory, School of Pharmacy, Hunan University of Chinese Medicine, Changsha 410208, China * Correspondence: [email protected] (Q.W.); [email protected] (X.Z.); [email protected] (J.L.); Tel.: +86-716-8066314 (Q.W.) Yongtong Xiong and Guan Huang contributed equally to this study. y Academic Editor: Maria Daglia Received: 25 October 2019; Accepted: 18 November 2019; Published: 20 November 2019 Abstract: To find good antifungal substances by the bioactivity-guided isolation method, we tracked down the effective antifungal substances in the bark and leaves of Zanthoxylum avicennae, and isolated three antifungal compounds 1, 2, and 3. The structures were identified as xanthyletin, luvangetin, and avicennin by 1H-NMR, 13C-NMR, and HRMS spectra. Particularly, compound 2 had several isomers, and the 1H-NMR spectra of 2 in different solvents showed a significant difference. To determine the stereo structure of 2, a single crystal was prepared and identified by X-ray diffraction 1 as Luvangetin. Moreover, the difference of H-NMR data of 2 between in solvent dimethyl sulfoxide-d6 (DMSO-d6) and deuterated chloroform (CDCl3), and other reported isomers were discussed for the first time. The bioassay results indicated that the three compounds 1, 2, and 3 displayed low to high antifungal activities against tested phytopathogenic fungi. In particular, all compounds 1, 2, and 3 showed excellent antifungal activities against Pyricularia oryzae and Z. avicennae, with the values of half maximal effective concentration (EC50) ranging from 31 to 61 mg/L, and compound 3 was also identified as a more potent inhibitor against Fusaium graminearum (EC = 43.26 1.76 mg/L) 50 ± compared with fungicide PCA (phenazine-1-carboxylic acid) (EC = 52.34 1.53 mg/L). The results 50 ± revealed that compounds 1, 2, and 3 were the main antifungal substances of Z. avicennae, and can be used as lead compounds of a fungicide, which has good development value and prospect. Keywords: Zanthoxylum avicennae; bioactivity-guided isolation method; antifungal activity; lead compound; fungicide 1. Introduction Zanthoxylum avicennae belongs to Rutaceae, and is mainly distributed around southern coastal area of China and parts of Southeast Asia, such as Hainan, Fujian, Guangxi, the Philippines, and Vietnam [1]. Z. avicennae has often been used to treat and relieve many illnesses, such as multi-phlegm, rheumatism, sore throat, jaundice, insect and snake bites, vomiting and diarrhea, repel Ascaris, and digestive system diseases in clinical and in traditional Chinese medicine [2–8]. Therefore, Z. avicennae deserves great research value and the bioactive substances from Z. avicennae have Molecules 2019, 24, 4207; doi:10.3390/molecules24234207 www.mdpi.com/journal/molecules Molecules 2019, 24, 4207 2 of 7 Molecules 2019, 24, 4207 2 of 8 attractedmulti-phlegm, researchers’ rheumatism, attention. sore Further throat, studies jaundice, have insect shown and snake that bites,Z. avicennae vomiting mainlyand diarrhea, contains the compoundsrepel ofAscaris triterpenes,, and digestive steroids, system alkaloids, diseases in amides, clinical lignans,and in traditional coumarins, Chinese flavonoids, medicine [2–8]. volatile oils, Therefore, Z. avicennae deserves great research value and the bioactive substances from Z. avicennae and fatty acids [6,9–12], and many compounds have been proven to have various bioactivities, such have attracted researchers’ attention. Further studies have shown that Z. avicennae mainly contains as anti-cancer,the compounds antibacterial of triterpenes, [13], antimildew steroids, alkaloids, activities amides, [14 ],lignans, inhibitory coumarins, activities flavonoids, against volatilePlasmodium vivax [15oils,], and and 1,1-diphenyl-2-picrylhydrazyl fatty acids [6,9–12], and many compounds (DPPH) ha freeve been radical-scavenging proven to have various activity bioactivities, [16]. In China,such asZ. anti-cancer, avicennae isantibacterial distributed [13], abundantly; antimildew however,activities [14], research inhibitory on the activities antifungal against activity of Z. avicennaePlasmodiumis seldom vivax reported. [15], and In1,1-diphenyl-2-picrylhydrazyl order to develop and utilize (DPPH) this plantfree radical-scavenging resource to the bestactivity advantage, [16]. and expand the antifungal application of Z. avicennae, we used the bioassay-guided isolation method In China, Z. avicennae is distributed abundantly; however, research on the antifungal activity of to focus onZ. avicennae exploring is seldom the antifungal reported. compoundsIn order to develop of Z.avicennae and utilize. Thethis resultsplant resource provide to athe research best basis and helpfuladvantage, clues forand the expand discovery the antifungal of novel application antimicrobial of Z. avicennae agents. , we used the bioassay-guided isolation method to focus on exploring the antifungal compounds of Z. avicennae. The results 2. Resultsprovide and Discussiona research basis and helpful clues for the discovery of novel antimicrobial agents. In this2. Results study, and 28.0 Discussion g of bark crude extract were obtained from 120.0 g of bark, and 45.0 g of leave crudeIn extract this study, were 28.0 obtained g of bark crude from extract 170.0 were g of obtained leaves from of 120.0Z. avicennae g of bark,. and The 45.0 extraction g of leave yields were 23.3%crude and extract 26.5%, were respectively.obtained from 170.0 Eight g of fractionsleaves of Z. ( A–Havicennae) were. The isolatedextraction fromyields thewere bark 23.3% crude of Z. avicennaeand 26.5%,and fourrespectively. fractions Eight (I–L fractions) were (A–H isolated) were isolated from the from leave the bark crude. crude Byof Z. the avicennae bioassay-guided and isolationfour method, fractions three (I–L) bioactivewere isolated compounds from the leave1, 2,crude.and By3 werethe bioassay-guided isolated from isolation the fractions, method, and all compoundsthree were bioactive identified compounds by 1 H-NMR,1, 2, and 313 wereC-NMR, isolated and from HRMS the frac spectrations, and (see all details compounds in Supplementary were identified by 1H-NMR, 13C-NMR, and HRMS spectra (see details in Supplementary Materials). Materials).Detailed Detailed analysis analysis indicated indicated that compounds that compounds 1–3 were1–3 xanthyletinwere xanthyletin [17,18], luvangetin [17,18], [19,20], luvangetin and [19,20], and avicenninavicennin [21 [21,22],,22], respectively, respectively, as as shown shown in Figure in Figure 1. 1. FigureFigure 1. The1. The structures structures of of compounds compounds 1–3.1 –3. However, we found that the NMR spectra of three compounds in solvent DMSO-d6 and However, we found that the NMR spectra of three compounds in solvent DMSO-d6 and deuterated deuterated chloroform (CDCl3) showed apparent differences. Particularly, the difference of the chloroform (CDCl ) showed apparent differences. Particularly, the difference of the 1H-NMR spectra 1H-NMR spectra3 of compounds 1 and 2 were especially remarkable. In this research, the 1H and 1 13 of compounds13C-NMR1 andspectra2 wereof compounds especially 1, 2 remarkable. and 3 in solvent In thisDMSO- research,d6, and the differencesH and C-NMRof 1H-NMR spectra of 1 compoundsspectra1, 2inand DMSO-3 ind6 solvent and CDCl DMSO-3 were reportedd6, and thefor the diff firsterences time, ofas shownH-NMR in Table spectra 1. Moreover, in DMSO- d6 and CDCl3 werecompound reported 2 had for several the first natural time, isomers, as shown such in as Table luvangetin1. Moreover, [19,20], compoundalloxanthoxyletin2 had [20], several and natural 1 isomers,xanthoxyletin such as luvangetin [17,23], [shown19,20 ],in alloxanthoxyletin Figure 2, and the H-NMR [20], and spectra xanthoxyletin of these compounds [17,23], shownwere very in Figure2, similar. Particularly, the 1H-NMR spectrum of compound 2 in DMSO-d6 was almost consistent with and the 1H-NMR spectra of these compounds were very similar. Particularly, the 1H-NMR spectrum the reported spectrum of xanthoxyletin in CDCl3 [17]. To determine the stereo structure of 2, a of compoundsingle crystal2 in DMSO- was preparedd6 was by almost slow evaporated consistent in withethyl acetate the reported at room spectrumtemperature, of and xanthoxyletin it was in CDCl3 [17confirmed]. To determine as luvangetin the stereoby X-ray structure diffraction, of as2 ,shown a single in Figure crystal 3. was prepared by slow evaporated in ethyl acetate at room temperature, and it was confirmed as luvangetin by X-ray diffraction, as shown in Figure3. Table 1. 1H-NMR data (J, Hz) of 2 in different deuterium solvents (400 MHz) compared with the isomers reported by the literature. 2 2 2 Location Alloxanthoxyletin Xanthoxyletin (DMSO-d6) (CDCl3) (In Ref.) C2-H 7.92 (d, 9.6, 1 H) 7.59 (d, 9.6, 1 H) 7.57 (d, 9.6, 1 H) 7.96 (d, 10.0, 1 H) 7.85 (d, 10.0, 1 H) C3-H 7.18 (s, 1H) 6.85 (s, 1H) 6.83 (s, 1H) 6.36 (s, 1H) 6.57 (s, 1H) C5-H 6.48 (d, 10.0, 1H) 6.35 (d, 10.0, 1H) 6.33 (d, 10.0, 1 H) 6.62 (d, 10.0, 1H) 6.58 (d, 10.0, 1H) C7-H 6.29 (d, 9.6, 1H) 6.24 (d, 9.6, 1H) 6.24 (d, 9.6 Hz, 1H) 6.16(d, 10.0, 1H) 6.21(d, 10.0, 1H) C8-H 5.88 (d, 10.0, 1H) 5.72 (d, 10.0, 1H) 5.71 (d, 10.0, 1 H) 5.55 (d, 10.0, 1H) 5.71(d, 10.0, 1H) C10 -H 3.86 (s, 3H) 3.99 (s, 3H) 3.98 (s, 3H) 3.87 (s, 3H) 3.87(s, 3H) C20 -H, C30 -H 1.46 (s, 6H) 1.53 (s, 6H) 1.51 (s, 6H) 1.47 (s, 6H) 1.47(s, 6H) Molecules 2019, 24, 4207 3 of 8 Table 1.
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