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

Auriane Dudoit
Auriane Dudoit
, 
Nicolas Cardinault
Nicolas Cardinault
, 
Christian Mertz
Christian Mertz
, 
Marc Chillet
Marc Chillet
 y 
Pierre Brat
Pierre Brat
   | 24 jun 2021
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Article Category: Review paper
Publicado en línea: 24 jun 2021
Páginas: 5 - 24
Recibido: 17 jun 2020
Aceptado: 17 mar 2021
DOI: https://doi.org/10.2478/jas-2021-0013
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© 2021 Auriane Dudoit et al., published by Sciendo
This work is licensed under the Creative Commons Attribution 4.0 International License.

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]
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