Antifungal Activities of Propolis and its Main Components with an Emphasis Against Phytopathogenic Fungi

Dudoit, Auriane; Cardinault, Nicolas; Mertz, Christian; Chillet, Marc; Brat, Pierre

doi:10.2478/jas-2021-0013

Figures & Tables

Antifungal activity of propolis extracts against plant pathogens

Geographical origin	Tested extract	Pathogen/Origin	Analysed parameter	Method	Results	References
Turkey	EEP	Aspergillus versicolor Penicillium aurantiogriseum (isolated from Turkish cheese)	Percentage of mycelium growth inhibition	Agar medium dilution method	Mycelium growth inhibition (%)EEP concentration 10%: 100% inhibition on all the samples and the 2 strainsEEP concentration 5%: >30% inhibitionEEP concentration 1%: >15% inhibition	[36]
Hamaraya, Ethiopia	EEP	Fusarium sp.Aspergillus niger (isolated from avocado)	Relative inhibition of mycelium growth	Agar medium dilution method	Significant inhibition at a concentration of 10 mg mL⁻¹ for Aspergillus niger and Fusarium sp.	[30]
5 different regions of Turkey	MEP	Alternaria alternataFusarium oxysporum	Percentage of mycelium growth inhibition	Agar medium dilution method	Mycelium growth inhibition (%) as of D+3F. oxysporum: 100% for 2 regions (at 2% and 5% concentration) >52% for the 3 others (from a 2% concentration)A. alternata. 100% for 2 regions at a 5% concentration	[25]
Temuco, Chile	EEP	Alternaria alternata Fusarium sp. Botrytis cinerea Penicillium expansum	Percentage of mycelium growth inhibition	Agar medium dilution method	100% inhibition for all the fungi at an EEP concentration = 2.5% except for B.cinerea = at 5%Inhibition still better than with the chemical fungicide	[45]
Baoding County, Hebei Province, China	EEPP-FrE-FrB-FrW-Fr	Penicillium italicum (isolated from citrus blue mould)	Percentage of mycelium growth inhibition	Agar medium dilution method	Mycelium growth inhibition (%)EEP extract (1200 mg L⁻¹): 93.20%P-Fr extract (200 mg L⁻¹): 35.40%E-Fr extract (200 mg L⁻¹): 100%B-Fr extract (200 mg L⁻¹): 25%W-Fr extract (200 mg L⁻¹): 6.82%	[46]
Medellin, Antioquia, Colombia	EPEMCH₂Cl₂EtOAcMeOH	Colletotrichum gloeosporioides (isolated from papaya (Carica papaya) and mango (Mangifera indica))Botryodiplodia theobromae (isolated from avocado, Persea americana)	Percentage of mycelium growth inhibition	Agar medium dilution method	Mycelium growth inhibition (%) on C. gloeosporioides (mango), C. gloeosporioides (papaya), B. theobromae, respectivelyEPEM extract: 39.8%, 26.1%, 29%CH₂Cl₂ extract: 47.6%, 38.1, 23.5%EtOAc extract: 6.5%, 11.6%, 5.7%MeOH extract: 9.9%, 5.2%, 4.9%	[49]
Sao Paulo, Brazil	EEP	Colletotrichum gloeosporioides	Percentage of mycelium growth inhibition	Agar medium dilution method	Mycelium growth inhibition (%)EEP concentration 2.5%: total inhibitionEEP concentration 0.5/1.0/1.5/2.0%: partial inhibition	[4]
China	EEP	Colletotrichum capsici (isolated from capsicum)	Percentage of mycelium growth inhibition	Agar medium dilution method	Mycelium growth inhibition (%)EEP concentration 0.25%: 66.1% inhibitionEEP concentration 0.50%: 84.3% inhibitionEEP concentration 0.75%: 89% inhibition	[64]
Tehran-Khojir, northern Iran	EEP	Aspergillus niger	Determination of MIC value	Liquid medium dilution method	MIC value (μg mL⁻¹)Aspergillus niger: 500	[44]
El-Aslogy, Zagazig, Egypt	EEP	Aspergillus flavus (isolated from pealed peanut seed)	Percentage of spore germination	Liquid medium dilution method	For EEP concentrations varying from 3 to 4g L⁻¹: 56 to 76% reduction in spore germination percentage	[57]
San Juan province, Argentina	EEP	Aspergillus flavusApsergillus niger	Determination of MIC value	Liquid medium dilution method	Species of the genus Aspergillus are not susceptible to extracts of urban propolis (MIC > 250 μg mL⁻¹)	[58]
‘El Siambon’ Tucuman, Argentina	PPPE	Aspergillus niger (isolated from citrus)**Fusarium sp. Penicillium notatum**	Determination of MIC value	Liquid medium dilution method	MIC value (μg mL⁻¹)Aspergillus niger: 232 ± 0.12Fusarium sp. (20), (21), (22) : 349 ± 0.15, 310 ± 0.10, 194 ± 0.10Penicillium notatum: 349 ± 0.14	[33]
Sao Paulo, Brazil	EEP	Colletotrichum gloeosporioides	Percentage of spore germination inhibition	Liquid medium dilution method	Spore germination inhibition (%)EEP concentration 0.5%: 1.78% inhibitionEEP concentration 1.0%: 47.3% inhibitionEEP concentration 1.5%: 96.4% inhibitionEEP concentration 2.0%: 100% inhibitionEEP concentration 2.5%: 100% inhibition	[4]
‘El Siambon’ Tucuman, Argentina	PPPE	Aspergillus niger (isolated from citrus)**Fusarium sp. Penicillium notatum**	Percentage of mycelium growth inhibition	Paper disc diffusion method	Mycelium growth inhibition (%)Aspergillus niger: 60.4 ± 0.04Fusarium sp. (20), (21), (22): 63.1 ± 0.03, 59.9 ± 0.03, 59.1 ± 0.04Penicillium notatum: 44.6 ± 0.05	[33]
‘El Siambon’ Tucuman, Argentina	PPPE	Aspergillus niger (isolated from citrus)**Fusarium sp. Penicillium notatum**	Compounds displaying activity potential	TLC bioautography	Discovery of phenolic compounds	[33]
Baoding County, Hebei Province, China	EEPP-FrE-FrB-FrW-Fr	Penicillium italicum (isolated from citrus blue mould)	Compounds displaying activity potential	TLC bioautography	Identification: pinobanksin, pinocembrin, chrysin, galangin	[46]

Chemical composition of propolis extracts depending on geographical origin

Geographical origin	Botanical genus and/or species	Bee type	Majority compounds	References
Turkey (10 different regions)	ns	Apis mellifera	Aromatic alcohol, alcohol, aromatic acid, flavonoid^† (flavone, flavanone, flavonol), ketone, terpene^†, vitamin E, acid	[36]
Medellin, Antioquia, Colombia	ns	Apis mellifera	Isocupressic acid, (+)-agathadiol, epi-13-torulosol	[49]
‘El Siambon’ Tucuman, Argentina	Salix humboldiana, Pinus, Eucalyptus	Apis mellifera	Pinocembrin^, galangin^	[33]
Baoding County, Hebei Province, China	ns	ns	Pinobanksin^, pinocembrin^, chrysin^, galangin^	[46]
Tehran-Khojir, northern Iran	Populus (determined by studying the chemical composition of propolis by GC-MS)	ns	Pinobanksin^, pinobanksin-3-acetate, pinocembrin^, pinostrobin, chrysin^, galangin^	[44]
Haramaya, Ethiopia	ns	Apis mellifera	Benzenamine, N,N-dibutyl-(21.94%), Paromomycin (9.74%), 4-Aminobutyramide,N-methyl-N-[4-(1-pyrrolidinyl)-2-butynyl]-(9.26%) and DL-Tryptophan,5-methoxy(7.43%)	[30]
Northeastern Brazil	Dalbergia ecastophyllum	Apis mellifera	Medicarpin, 3-hydroxy-8.9-dimethoxypterocarpan, quercetin, chrysin^*, ferulic acid, artepillin C^†	[42]
Cabreuva, State of Sao Paulo, Brazil	Baccharis dracunculifolia	Apis mellifera	Artepillin C, p-Coumaric acid, kaempferid	[21, 75]
Temuco, Chile	ns	ns	Pinocembrin^, caffeic acid^, myricetin, quercetin, kaempferol, apigenin, galangin^*, caffeic acid phenyl ester (CAPE)	[39]
State de Parana, Brazil	Baccharis dracunculifolia + Auraucaria spp.	ns	3,5-Diprenyl-4-hydroxycinnamic acid^† (DHCA), 2,2-Dimethyl-6-carboxyethenyl-2H-1-benzopyran (DCBEN), 3-Prenyl-4-hydroxycinnamic acid^† (PHCA), 2,2-Dimethyl-8-prenyl-2H-1-benzopyran-6-propenoic acid (DPB)	[76]
State of Minas Gerais, Brazil	Baccharis dracunculifolia	ns	3,5-Diprenyl-4-hydroxycinnamic acid^† (DHCA), 3-Prenyl-4-hydroxycinnamic acid^† (PHCA), 2,2-Dimethyl-8-prenyl-2H-1-benzopyran-6-propenoic acid (DPB), p-Coumaric acid (PCUM), Caffeic acid^* (CA), caffeoylquinic acid derivates^†	[76], [77]
State of Parana, Brazil	Auraucaria spp.	ns	3-Methoxy-4-hydroxy-benzaldehyde, (VAN), 3-Methoxy-4-hydroxycinnamalde-hyde (G2), 2-[1-hydroxymethyl]vinyl-6-acetyl-5-hidroxycumarane (I)	[76]
Isfahan, central Iran	ns	ns	Pinocembrin^, caffeic acid^, kaempferol, phenethyl caffeate, chrysin^, galangin^	[78]
England and New York State, USA	ns	ns	p-coumaric acid, chrysin^, pinocembrin^	[77]
Hatay region, Turkey	pine forest, eucalyptus, poplar trees	Apis mellifera syriaca, Apis mellifera anatoliaca, Apis mellifera caucasica	Caffeic acid^*, sesquiterpenes^†	[79]
Northeastern Portugal	ns	Apis mellifera	New compound: p-coumaric ester derivative dimer, methylated and/or sterified or hydroxylated derivatives of flavonoids, other compounds found in temperate zones	[80]
Greece	ns	ns	α-pinene	[81]
Temuco, Chile	ns	ns	Caffeic acid^, myricetin, quercetin, kaempferol, apigenin, pinocembrin^, galangin^*, CAPE, rutin	[45]
Sonora, Mexico	ns	ns	Pinocembrin^, pinobanksin 3-acetate, chrysin^, CAPE^†, acacetin, galangin^*	[50]
Kangaroo Island, Australia	Acacia paradoxa	Apis mellifera	2′,3′,4′-trimethoxychalcone 2′-hydroxy-3′,4′-dimethoxychalcone 2′,4′-dihydroxy-3′-methoxychalcone pinobanksin 3-acetate 5,7-dihydroxy-6-methoxy-2,3-dihydroflavonol 3-acetate,	[82]
Montevideo, Uruguay	ns	ns	Pinobanksin 3-(2-methyl)butyrate pinobanksin 3-isobutyrate2-methyl-2-butenyl ferulate	[83]
Okinawa, Japan	Macaranga tanarius	Apis mellifera	Nymphaeol-B, Isonymphaeol-B, Nymphaeol-A, 3′-geranyl-naringenin, Nymphaeol-C	[84]
Waikato, New Zealand	ns	ns	Pinobanksin^, pinocembrin^, chrysin^, galangin^, cinnamic and ferulic acid	[47]

Antifungal Activities of Propolis and its Main Components with an Emphasis Against Phytopathogenic Fungi

Figures & Tables

Antifungal activity of propolis extracts against plant pathogens

Chemical composition of propolis extracts depending on geographical origin

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