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Chemical Composition and Antifungal Activity of Chelidonium Majus Extracts – Antagonistic Action of Chelerythrine and Sanguinarine Against Botrytis Cinerea

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Chemical Composition and Antifungal Activity of Chelidonium Majus Extracts – Antagonistic Action of Chelerythrine and Sanguinarine Against Botrytis Cinerea Chemistry and Ecology ISSN: 0275-7540 (Print) 1029-0370 (Online) Journal homepage: http://www.tandfonline.com/loi/gche20 Chemical composition and antifungal activity of Chelidonium majus extracts – antagonistic action of chelerythrine and sanguinarine against Botrytis cinerea D. Wianowska, S. Garbaczewska, A. Cieniecka–Roslonkiewicz, R. Typek & A. L. Dawidowicz To cite this article: D. Wianowska, S. Garbaczewska, A. Cieniecka–Roslonkiewicz, R. Typek & A. L. Dawidowicz (2018): Chemical composition and antifungal activity of Chelidonium majus extracts – antagonistic action of chelerythrine and sanguinarine against Botrytis cinerea, Chemistry and Ecology, DOI: 10.1080/02757540.2018.1462345 To link to this article: https://doi.org/10.1080/02757540.2018.1462345 Published online: 09 Apr 2018. Submit your article to this journal View related articles View Crossmark data Full Terms & Conditions of access and use can be found at http://www.tandfonline.com/action/journalInformation?journalCode=gche20 CHEMISTRY AND ECOLOGY, 2018 https://doi.org/10.1080/02757540.2018.1462345 RESEARCH ARTICLE Chemical composition and antifungal activity of Chelidonium majus extracts – antagonistic action of chelerythrine and sanguinarine against Botrytis cinerea D. Wianowskaa, S. Garbaczewskab, A. Cieniecka–Roslonkiewiczb, R. Typeka and A. L. Dawidowicza aDepartment of Chromatographic Methods, Faculty of Chemistry, Maria Curie-Sklodowska University, Lublin, Poland; bDepartment of Synthesis, Technology and Biotechnology of Biologically Active Products, Institute of Industrial Organic Chemistry, Warsaw, Poland ABSTRACT ARTICLE HISTORY This study discusses the similarities and differences between the Received 4 November 2017 antifungal activity of Chelidonium majus L. extracts and Final Version Received 28 chelerythrine/sanguinarine, the main alkaloids in these extracts, March 2018 against the plant pathogenic fungus, Botrytis cinerea.Theobtained KEYWORDS data show that the Ch. majus L. extracts inhibit the growth of Natural fungicide; enhancing B. cinerea very effectively. The extracts activity is significantly antifungal activity; synergistic greater than that of chelerythrine/sanguinarine standard solutions action; celandine alkaloids alone and it does not always reflect the total content of alkaloids in the extracts. It has been proved that B. cinerea exhibits very diverse resistance to chelerythrine and sanguinarine. The IC50 values for chelerythrine and sanguinarine equal 5.41 mg/mL and 1.76 mg/mL, respectively. In the mixture the antifungal activity of chelerythrine and sanguinarine is antagonistic in the concentration dependent way. Based on the presented data it is not clear, however, which alkaloids present in the Ch, majus extracts at significantly lower concentration levels enhance the activity of chelerythrine and sanguinarine so that the extracts activity is considerably greater than that of both main alkaloids mixtures. Introduction Chelidonium majus L., commonly known as greater celandine, is a herbaceous perennial plant of the family Papaveraceae, that is native to Europe and Asia but has spread through- out the world. The main constituents of this plant are alkaloids such as benzophenanthri- dines (e.g. chelidonine, chelerythrine and sanguinarine) and protoberberines (e.g. coptisine and berberine) [1–4]. These compounds exhibit numerous biological properties, including choleretic, colagogue, spasmolytic, antitumour, antiinflammatory, antibacterial, antiviral and fungicidal effects, both in vitro and in vivo [5–9]. Of the above mentioned, fun- gicidal activity of benzophenanthridines deserves special attention since in the aspect of rapid development of pathogens resistance to the commonly used synthetic fungicides there is a great demand for alternative and effective natural antifungal agents. CONTACT D. Wianowska [email protected] Department of Chromatographic Methods, Faculty of Chemistry, Maria Curie-Sklodowska University, Pl. Maria Curie-Sklodowska 3, Lublin 20-031, Poland © 2018 Informa UK Limited, trading as Taylor & Francis Group 2 D. WIANOWSKA ET AL. Botrytis cinerea (teleomorph: Botryotinia fuckeliana) is an airborne plant pathogen with a necrotrophic lifestyle that affects many plant species worldwide. This fungus causes the grey mold in vegetables, ornamentals and fruits, that is responsible for great damage in crops in the field or after the harvest period [10]. In addition, B. cinerea is not indifferent to humans since it can cause a respiratory allergic reaction in predisposed individuals [11]. In view of this, many attempts were undertaken to develop fungicidal agents inhibit- ing effectively the growth of this fungus. There are many fungicides for B. cinerea control, most of them are the synthetic agents. Yet due to the genetic plasticity of this fungus at present many of these agents are ineffective [11]. Therefore new fungicides are constantly being looked for, particularly among therapeutic plants and compounds isolated from them as they are considered to be non-toxic to mammals and non-target organisms [12]. They also are regarded to be safer for the environment, which is important taking into account the negative environmental impact of the majority of synthetic fungicides. In the past decade the fungicidal activity of alkaloids from Ch. majus attracted attention of the researchers. It was proved that they are equally active against resistant clinical yeast isolates as well as plant pathogens [13–16]. The Pârvu research team proved in [15,16] that Ch. majus extracts cause ultrastructural changes in B. cinerea conidia and B. tulipae hyphae. In [16] the ultrastructural changes were combined with the chemical composition of Ch. majus extracts. However, until now the activity of alkaloids alone and their mixture was not compared to that of the Ch. majus extracts. Sanguinarine and chelerythrine are the main alkaloids of Ch. majus extracts. The high content of chelerythrine and sanguinarine is also characteristic of the pink plume poppy extract (Macleaya cordata R. Br.). The extract was registered for the use as a fungicide with the trade name Qwel (this extract has the CAS registry number [112 025-60-2]) [12]. This fact additionally develops the scien- tists’ interest in research on the correlation between the activity of sanguinarine and che- lerythrine alone, their mixture and, the fungicidal properties of Ch. majus extracts. Hence the purpose of this study is to present similarities and differences in the antifun- gal properties of the Ch. majus extracts and the sanguinarine and chelerythrine solutions of the same concentrations as those in the plant extracts. In the experiments the effect of different extraction conditions i.e. maceration or extraction in the Soxhlet apparatus using chloroform, ethyl acetate, acetone or methanol as extractants on the antifungal activity of the Ch. majus extracts against B. cinerea was tested in vitro. Materials and methods Materials and reagents Chloroform, ethyl acetate, methanol and acetone (all of analytical grade), acetonitrile (HPLC), were supplied by the Polish Chemical Plant POCh S.A (Gliwice, Poland). Sanguinar- ine and chelerythrine standard (98%) and formic acid were purchased from Sigma-Aldrich (Poznan, Poland). Sabouraud Dextrose Agar was supplied by Argenta, CM0139 Oxoid, (Poznan, Poland). The plant pathogenic fungus (B. cinerea Persoon) was obtained from the Department of Phytopathology and Entomology, University of Warmia and Mazury in Olsztyn, Poland. Water was purified on a Milli-Q system (Millipore, Bedford, MA, USA). Ch. majus was collected in July 2015 near Warsaw (Poland). Overground parts of celan- dine were air-dried at room temperature for 2 weeks. A sufficiently large representative CHEMISTRY AND ECOLOGY 3 sample of the material was pre-cut and then ground with a Braun cutting mill to obtain particle size of 0.2–0.4 mm. Exactly weighted portions of the material (40 g) were sub- jected to extraction. Extraction in the Soxhlet apparatus A sample of the celandine herb (40 g) was submitted to the exhaustive extraction process with 200 mL of chloroform or ethyl acetate or methanol or acetone for 6 h using the Soxhlet apparatus. After cooling, the extract was removed and the same plant material was soaked with a fresh portion of the extractant and again extracted in the Soxhlet appar- atus. The obtained extracts were pooled together and evaporated to dryness using a rotary vacuum evaporator (Buchi R II rotavapor; 40°C). For statistical purposes three inde- pendent extractions were performed. Maceration A 40 g portion of the walnut green husks was soaked with 400 mL of chloroform or ethyl acetate or methanol or ethyl acetate for 24 h at room temperature. After this time the extract was removed, filtered through Whatman no. 4 paper and evaporated to dryness using a rotary vacuum evaporator (Buchi R II rotavapor; 40°C). For statistical purposes three independent extractions were performed. Assay of antifungal activity The activities of the extracts of celandine as well as the chelerythrine and sanguinarine sol- utions against B. cinerea were tested in vitro. Acetone solutions of dry extracts (with the concentration 20.0 mg/mL) and chelerythrine/sanguinarine standards (with the concen- tration from 0.010 to 6.0 mg/mL) were used in the study. A 1 mL aliquot of the solution was uniformly distributed on the surface of Sabouraud dextrose agar and acetone was allowed to evaporate aseptically. The mycelial discs with a diameter of 5 mm were cut from
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