[en] Medicinal plants play important roles in traditional medicine, and numerous compounds among them have been recognized for their antimicrobial activity. However, little is known about the potential of Vietnamese medicinal plants for antifungal activity. In this study, we examined the antagonistic activity of twelve medicinal plant species collected in Northern Vietnam against Penicillium digitatum, Aspergillus flavus, Aspergillus fumigatus, and Candida albicans. The results showed that the antifungal activities of the crude extracts from Mahonia bealei, Ficus semicordata, and Gnetum montanum were clearly detected with the citrus postharvest pathogen P. digitatum. These extracts could fully inhibit the growth of P. digitatum on the agar medium, and on the infected citrus fruits at concentrations of 300-1000 µg/mL. Meanwhile, the other tested fungi were less sensitive to the antagonistic activity of the plant extracts. In particular, we found that the ethanolic extract of M. bealei displayed a broad-spectrum antifungal activity against all four pathogenic fungi. Analysis of this crude extract by enrichment coupled with high-performance liquid chromatography revealed that berberine and palmatine are major metabolites. Additional inspections indicated berberine as the key compound responsible for the antifungal activity of the M. bealei ethanolic extract. Our study provides a better understanding of the potential of Vietnamese medicinal plant resources for combating fungal pathogens. This work also highlights that the citrus pathogen P. digitatum can be employed as a model fungus for screening the antifungal activity of botanicals.
Research Center/Unit :
GIGA I3-Laboratory for Organogenesis and Regeneration -ULiège
Disciplines :
Microbiology Pharmacy, pharmacology & toxicology
Author, co-author :
Tran My Hanh ; Université de Liège - ULiège > Faculté des Sciences > Form. doct. sc. (bioch., biol. mol. cel., bioinf. - paysage) ; Université de Liège - ULiège > Faculté des Sciences > Doct. sc. (bioch., biol. mol. cel., bioinf. - paysage) ; ULiège - Université de Liège [BE] > Sciences de la Vie > Lab. Organogenèse et Régénération, GIGA-I3
Le, Diep Hong; Faculty of Biology, University of Science, Vietnam National University, Hanoi (VNU), 334 Nguyen Trai, Thanh Xuan, Hanoi 100000, Vietnam
Nguyen, Van-Anh Thi ; Faculty of Biology, University of Science, Vietnam National University, Hanoi (VNU), 334 Nguyen Trai, Thanh Xuan, Hanoi 100000, Vietnam
Vu, Tao Xuan; Center for Experimental Biology, National Center for Technological Progress, Ministry of Science and Technology, C6 Thanh Xuan Bac, Thanh Xuan, Hanoi 100000, Vietnam
Thanh, Nguyen Thi Kim; Faculty of Biology, University of Science, Vietnam National University, Hanoi (VNU), 334 Nguyen Trai, Thanh Xuan, Hanoi 100000, Vietnam
Giang, Do Hoang; Center for Research and Technology Transfer, Vietnam Academy of Science and Technology, 18 Hoang Quoc Viet, Cau Giay, Hanoi 100000, Vietnam
Dat, Nguyen Tien; Center for Research and Technology Transfer, Vietnam Academy of Science and Technology, 18 Hoang Quoc Viet, Cau Giay, Hanoi 100000, Vietnam
Pham, Hai The; Faculty of Biology, University of Science, Vietnam National University, Hanoi (VNU), 334 Nguyen Trai, Thanh Xuan, Hanoi 100000, Vietnam
Muller, Marc ; Université de Liège - ULiège > GIGA > GIGA I3 - Laboratory for Organogenesis and Regeneration
Nguyen, Huy Quang; Faculty of Biology, University of Science, Vietnam National University, Hanoi (VNU), 334 Nguyen Trai, Thanh Xuan, Hanoi 100000, Vietnam ; National Key Laboratory of Enzyme and Protein Technology, University of Science, Vietnam National University, Hanoi (VNU), 334 Nguyen Trai, Thanh Xuan, Hanoi 100000, Vietnam
Tran, Van-Tuan ; Faculty of Biology, University of Science, Vietnam National University, Hanoi (VNU), 334 Nguyen Trai, Thanh Xuan, Hanoi 100000, Vietnam ; National Key Laboratory of Enzyme and Protein Technology, University of Science, Vietnam National University, Hanoi (VNU), 334 Nguyen Trai, Thanh Xuan, Hanoi 100000, Vietnam
Language :
English
Title :
Penicillium digitatum as a Model Fungus for Detecting Antifungal Activity of Botanicals: An Evaluation on Vietnamese Medicinal Plant Extracts.
This research was funded by ARES (Académie de Recherche et d’Enseignement Supérieur) through the project “Exploring the Medical and (Eco)-toxicological Potential of Natural Extracts in North Vietnam”.
Kurnaz M.L. Kurnaz I.A. Commercialization of medicinal bioeconomy resources and sustainability Sustain. Chem. Pharm. 2021 22 100484 10.1016/j.scp.2021.100484
Astutik S. Pretzsch J. Kimengsi J.N. Asian medicinal plants’ production and utilization potentials: A review Sustainability 2019 11 5483 10.3390/su11195483
Patra J.K. Das G. Lee S. Kang S.S. Shin H.S. Selected commercial plants: A review of extraction and isolation of bioactive compounds and their pharmacological market value Trends Food Sci. Technol. 2018 82 89 109 10.1016/j.tifs.2018.10.001
Azmir J. Zaidul I.S.M. Rahman M.M. Sharif K.M. Mohamed A. Sahena F. Jahurul M.H.A. Ghafoor K. Norulaini N.A.N. Omar A.K.M. Techniques for extraction of bioactive compounds from plant materials: A review J. Food Eng. 2013 117 426 436 10.1016/j.jfoodeng.2013.01.014
Yusoff I.M. Taher Z.M. Rahmat Z. Chua L.S. A review of ultrasound-assisted extraction for plant bioactive compounds: Phenolics, flavonoids, thymols, saponins and proteins Food Res. Int. 2022 157 111268 10.1016/j.foodres.2022.111268
Yang L. Yang C. Li C. Zhao Q. Liu L. Fang X. Chen X.Y. Recent advances in biosynthesis of bioactive compounds in traditional Chinese medicinal plants Sci. Bull. 2016 61 3 17 10.1007/s11434-015-0929-2
Porras G. Chassagne F. Lyles J.T. Marquez L. Dettweiler M. Salam A.M. Samarakoon T. Shabih S. Farrokhi D.R. Quave C.L. Ethnobotany and the role of plant natural products in antibiotic drug discovery Chem. Rev. 2020 121 3495 3560 10.1021/acs.chemrev.0c00922
Geddes-McAlister J. Shapiro R.S. New pathogens, new tricks: Emerging, drug-resistant fungal pathogens and future prospects for antifungal therapeutics Ann. N. Y. Acad. Sci. 2019 1435 57 78 10.1111/nyas.13739
Bhatta U.K. Alternative management approaches of citrus diseases caused by Penicillium digitatum (green mold) and Penicillium italicum (blue mold) Front. Plant Sci. 2022 12 833328 10.3389/fpls.2021.833328
Fisher M.C. Alastruey-Izquierdo A. Berman J. Bicanic T. Bignell E.M. Bowyer P. Bromley M. Brüggemann R. Garber G. Cornely O.A. et al. Tackling the emerging threat of antifungal resistance to human health Nat. Rev. Microbiol. 2022 20 557 571 10.1038/s41579-022-00720-1
Ali-Shtayeh M.S. Yaghmour R.M.R. Faidi Y.R. Salem K. Al-Nuri M.A. Antimicrobial activity of 20 plants used in folkloric medicine in the Palestinian area J. Ethnopharmacol. 1998 60 265 271 10.1016/S0378-8741(97)00153-0
Giordani C. Simonetti G. Natsagdorj D. Choijamts G. Ghirga F. Calcaterra A. Quaglio D. De Angelis G. Toniolo C. Pasqua G. Antifungal activity of Mongolian medicinal plant extracts Nat. Prod. Res. 2019 34 449 455 10.1080/14786419.2019.1610960 31135192
Webster D. Taschereau P. Belland R.J. Sand C. Rennie R.P. Antifungal activity of medicinal plant extracts; preliminary screening studies J. Ethnopharmacol. 2008 115 140 146 10.1016/j.jep.2007.09.014
Hoffman B.R. DelasAlas H. Blanco K. Wiederhold N. Lewis R.E. Williams L. Screening of antibacterial and antifungal activities of ten medicinal plants from Ghana Pharm. Biol. 2008 42 13 17 10.1080/13880200490504925
Dabur R. Singh H. Chhillar A.K. Ali M. Sharma G.L. Antifungal potential of Indian medicinal plants Fitoterapia 2004 75 389 391 10.1016/j.fitote.2004.01.015 15159003
Imanshahidi M. Hosseinzadeh H. Pharmacological and therapeutic effects of Berberis vulgaris and its active constituent, berberine Phytother. Res. 2008 22 999 1012 10.1002/ptr.2399
Tillhon M. Ortiz L.G. Lombardi P. Scovassi A.I. Berberine: New perspectives for old remedies Biochem. Pharmacol. 2012 84 1260 1267 10.1016/j.bcp.2012.07.018
Aldholmi M. Marchand P. Ourliac-Garnier I. Le Pape P. Ganesan A. A decade of antifungal leads from natural products: 2010–2019 Pharmaceuticals 2019 12 182 10.3390/ph12040182
Corkley I. Fraaije B. Hawkins N. Fungicide resistance management: Maximizing the effective life of plant protection products Plant Pathol. 2021 71 150 169 10.1111/ppa.13467
Khetabi A.E. Lahlali R. Ezrari S. Radouane N. Lyousfi N. Banani H. Askarne L. Tahiri A. Ghadraoui L.E. Belmalha S. et al. Role of plant extracts and essential oils in fighting against postharvest fruit pathogens and extending fruit shelf life: A review Trends Food Sci. Technol. 2022 120 402 417 10.1016/j.tifs.2022.01.009
Makhuvele R. Naidu K. Gbashi S. Thipe V.C. Adebo O.A. Njobeh P.B. The use of plant extracts and their phytochemicals for control of toxigenic fungi and mycotoxins Heliyon 2020 6 e05291 10.1016/j.heliyon.2020.e05291 33134582
Wu Y. Ren D. Gao C. Li J. Du B. Wang Z. Qian S. Recent advances for alkaloids as botanical pesticides for use in organic agriculture Int. J. Pest Manag. 2021 1 11 10.1080/09670874.2021.1917723
Seepe H.A. Nxumalo W. Amoo S.O. Natural products from medicinal plants against phytopathogenic Fusarium species: Current research endeavours, challenges and prospects Molecules 2021 26 6539 10.3390/molecules26216539 34770948
Costa J.H. Bazioli J.M. de Moraes Pontes J.G. Fill T.P. Penicillium digitatum infection mechanisms in citrus: What do we know so far? Fungal Biol. 2019 123 584 593 10.1016/j.funbio.2019.05.004
Sánchez-Torres P. Molecular mechanisms underlying fungicide resistance in citrus postharvest green mold J. Fungi 2021 7 783 10.3390/jof7090783
Matrose N.A. Obikeze K. Belay Z.A. Caleb O.J. Plant extracts and other natural compounds as alternatives for post-harvest management of fruit fungal pathogens: A review Food Biosci. 2021 41 100840 10.1016/j.fbio.2020.100840
Ngegba P.M. Cui G. Khalid M.Z. Zhong G. Use of botanical pesticides in agriculture as an alternative to synthetic pesticides Agriculture 2022 12 600 10.3390/agriculture12050600
Do T.L. Nguyen X.D. Native drugs of Vietnam: Which traditional and scientific approaches? J. Ethnopharmacol. 1991 32 51 56 10.1016/0378-8741(91)90103-k
Hoang S.V. Baas P. Keßler P.J.A. Traditional medicinal plants in Ben En National Park, Vietnam Blumea 2008 53 569 601 10.3767/000651908x607521
On T.V. Quyen D. Bich L.D. Jones B. Wunder J. Russell-Smith J. A survey of medicinal plants in BaVi National Park, Vietnam: Methodology and implications for conservation and sustainable use Biol. Conserv. 2001 97 295 304 10.1016/s0006-3207(00)00125-7
Giang P.M. Otsuka H. New compounds and potential candidates for drug discovery from medicinal plants of Vietnam Chem. Pharm. Bull. 2018 66 493 505 10.1248/cpb.c17-00628 29710046
Lee C. Kim S.Y. Eum S. Paik J.H. Bach T.T. Darshetkar A.M. Choudhary R.K. Hai D.V. Quang B.H. Thanh N.T. et al. Ethnobotanical study on medicinal plants used by local Van Kieu ethnic people of Bac Huong Hoa nature reserve, Vietnam J. Ethnopharmacol. 2019 231 283 294 10.1016/j.jep.2018.11.006 30412749
Nguyen X.M.A. Bun S.S. Ollivier E. Dang T.P.T. Ethnobotanical study of medicinal plants used by K’Ho-Cil people for treatment of diarrhea in Lam Dong Province, Vietnam J. Herb. Med. 2020 19 100320 10.1016/j.hermed.2019.100320
Banskota A.H. Tezuka Y. Le Tran Q. Kadota S. Chemical constituents and biological activities of Vietnamese medicinal plants Curr. Top. Med. Chem. 2003 3 227 248 10.2174/1568026033392516 12570775
Ueda J.Y. Tezuka Y. Banskota A.H. Tran Q.L. Tran Q.K. Harimaya Y. Saiki I. Kadota S. Antiproliferative activity of Vietnamese medicinal plants Biol. Pharm. Bull. 2002 25 753 760 10.1248/bpb.25.753
Nguyen M.T.T. Awale S. Tezuka Y. Tran Q.L. Watanabe H. Kadota S. Xanthine oxidase inhibitory activity of Vietnamese medicinal plants Biol. Pharm. Bull. 2004 27 1414 1421 10.1248/bpb.27.1414
Nguyen-Pouplin J. Tran H. Tran H. Phan T.A. Dolecek C. Farrar J. Tran T.H. Caron P. Bodo B. Grellier P. Antimalarial and cytotoxic activities of ethnopharmacologically selected medicinal plants from South Vietnam J. Ethnopharmacol. 2007 109 417 427 10.1016/j.jep.2006.08.011
Nguyen Q.V. Nguyen V.B. Eun J.B. Wang S.L. Nguyen D.H. Tran T.N. Nguyen A.D. Anti-oxidant and antidiabetic effect of some medicinal plants belong to Terminalia species collected in Dak Lak Province, Vietnam Res. Chem. Intermed. 2016 42 5859 5871 10.1007/s11164-015-2409-3
Vu T.T. Kim H. Tran V.K. Dang Q.L. Nguyen H.T. Kim H. Kim I.S. Choi G.J. Kim J.C. In vitro antibacterial activity of selected medicinal plants traditionally used in Vietnam against human pathogenic bacteria BMC Complementary Altern. Med. 2016 16 32 10.1186/s12906-016-1007-2
Nguyen-Vo T.H. Le T. Pham D. Nguyen T. Le P. Nguyen A. Nguyen T. Nguyen T.N. Nguyen V. Do H. et al. VIETHERB: A database for Vietnamese herbal species J. Chem. Inf. Modeling 2018 59 1 9 10.1021/acs.jcim.8b00399
Vu X.T. Ngo T.T. Mai T.D.L. Bui T.T. Le H.D. Bui T.V.H. Nguyen Q.H. Ngo X.B. Tran V.T. A highly efficient Agrobacterium tumefaciens-mediated transformation system for the postharvest pathogen Penicillium digitatum using DsRed and GFP to visualize citrus host colonization J. Microbiol. Methods 2018 144 134 144 10.1016/j.mimet.2017.11.019 29175534
Nierman W.C. Yu J. Fedorova-Abrams N.D. Losada L. Cleveland T.E. Bhatnagar D. Bennett J.W. Dean R. Payne G.A. Genome sequence of Aspergillus flavus NRRL 3357, a strain that causes aflatoxin contamination of food and feed Genome Announc. 2015 3 e00168-15 10.1128/genomeA.00168-15 25883274
Balouiri M. Sadiki M. Ibnsouda S.K. Methods for in vitro evaluating antimicrobial activity: A review J. Pharm. Anal. 2016 6 71 79 10.1016/j.jpha.2015.11.005 29403965
Huang Y. Wang T. Jiang Z. Fast analysis of alkaloids from different parts of Mahonia bealei (Fort.) Carr. studied for their anti-Alzheimer’s activity using supercritical fluid chromatography J. Sep. Sci. 2021 44 2006 2014 10.1002/jssc.202001079
He J.M. Mu Q. The medicinal uses of the genus Mahonia in traditional Chinese medicine: An ethnopharmacological, phytochemical and pharmacological review J. Ethnopharmacol. 2015 175 668 683 10.1016/j.jep.2015.09.013
Gurib-Fakim A. Medicinal plants: Traditions of yesterday and drugs of tomorrow Mol. Asp. Med. 2006 27 1 93 10.1016/j.mam.2005.07.008
Liu Q. Luyten W. Pellens K. Wang Y. Wang W. Thevissen K. Liang Q. Cammue B.P.A. Schoofs L. Luo G. Antifungal activity in plants from Chinese traditional and folk medicine J. Ethnopharmacol. 2012 143 772 778 10.1016/j.jep.2012.06.019
Shi Y. Mon A.M. Fu Y. Zhang Y. Wang C. Yang X. Wang Y. The genus Ficus (Moraceae) used in diet: Its plant diversity, distribution, traditional uses and ethnopharmacological importance J. Ethnopharmacol. 2018 226 185 196 10.1016/j.jep.2018.07.027
Wan C. Chen C. Li M. Yang Y. Chen M. Chen J. Chemical constituents and antifungal activity of Ficus hirta Vahl. fruits Plants 2017 6 44 10.3390/plants6040044
Martin F. Grkovic T. Sykes M.L. Shelper T. Avery V.M. Camp D. Quinn R.J. Davis R.A. Alkaloids from the Chinese Vine Gnetum montanum J. Nat. Prod. 2011 74 2425 2430 10.1021/np200700f
Xiang W. Jiang B. Li X.M. Zhang H.J. Zhao Q.S. Li S.H. Sun H.D. Constituents of Gnetum montanum Fitoterapia 2002 73 40 42 10.1016/S0367-326X(01)00370-7
Chen J. Shen Y. Chen C. Wan C. Inhibition of key citrus postharvest fungal strains by plant extracts in vitro and in vivo: A review Plants 2019 8 26 10.3390/plants8020026 30678206
Hu W. Yu L. Wang M.H. Antioxidant and antiproliferative properties of water extract from Mahonia bealei (Fort.) Carr. leaves Food Chem. Toxicol. 2011 49 799 806 10.1016/j.fct.2010.12.001 21130829
Hu W. Wu L. Qiang Q. Ji L. Wang X. Luo H. Wu H. Jiang Y. Wang G. Shen T. The dichloromethane fraction from Mahonia bealei (Fort.) Carr. leaves exerts an anti-inflammatory effect both in vitro and in vivo J. Ethnopharmacol. 2016 188 134 143 10.1016/j.jep.2016.05.013
Wu L. Shen T. Zhou Y. Wu J. Ji X.Y. Si C.L. Hu W.C. Secondary metabolites of Mahonia bealei branches Chem. Nat. Compd. 2018 54 564 566 10.1007/s10600-018-2408-x
Singh I.P. Mahajan S. Berberine and its derivatives: A patent review (2009–2012) Expert Opin. Ther. Pat. 2012 23 215 231 10.1517/13543776.2013.746314
