Skip to main content
SpringerLink
Log in

Antifungal activity of essential oils on two Venturia inaequalis strains with different sensitivities to tebuconazole

  • Chemistry, Activity and Impact of Plant Biocontrol products
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

The antifungal activity of seven essential oils (eucalyptus, clove, mint, oregano, savory, tea tree, and thyme) was studied on Venturia inaequalis, the fungus responsible for apple scab. The composition of the essential oils was checked by gas chromatography-mass spectrometry. Each essential oil had its main compound. Liquid tests were performed to calculate the IC50 of essential oils as well as their majority compounds. The tests were made on two strains with different sensitivities to tebuconazole: S755, the sensitive strain, and rs552, the strain with reduced sensitivity. Copper sulfate was selected as the reference mineral fungicidal substance. IC50 with confidence intervals were calculated after three independent experiments. The results showed that all essential oils and all major compounds had in vitro antifungal activities. Moreover, it was highlighted that the effectiveness of four essential oils (clove, eucalyptus, mint, and savory) was higher than copper sulfate on both strains. For each strain, the best activity was obtained using clove and eucalyptus essential oils. For clove, the IC50 obtained on the sensitive strain (5.2 mg/L [4.0–6.7 mg/L]) was statistically lower than the IC50 of reduced sensitivity strain (14 mg/L [11.1–17.5 mg/L]). In contrast, for eucalyptus essential oil, the IC50 were not different with respectively 9.4–13.0 and 12.2–17.9 mg/L for S755 and rs552 strains. For mint, origano, savory, tea tree, and thyme, IC50 were always the best on rs552 strain. The majority compounds were not necessarily more efficient than their corresponding oils; only eugenol (for clove) and carvacrol (for oregano and savory) seemed to be more effective on S755 strain. On the other hand, rs552 strain seemed to be more sensitive to essential oils than S755 strain. In overall, it was shown that essential oils have different antifungal activities but do not have the same antifungal activities depending on the fungus strain used.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Ahmad A, Khan A, Akhtar F, Yousuf S, Xess I, Khan LA (2011) Fungicidal activity of thymol and carvacrol by disrupting ergosterol biosynthesis and membrane integrity against Candida. Eur J Clin Microbiol Infect Dis 30:41–50

    Article  CAS  Google Scholar 

  • Aiko V, Mehta A (2013) Inhibitory effect of clove (Syzygium aromaticum) on the growth of Penicillium citrinum and citrinin production. J Food Safety 33(4):440–444

    Article  Google Scholar 

  • Alaniz S, Leoni C, Bentancor O, Mondino P (2014) Elimination of summer fungicide sprays for apple scab (Venturia inaequalis) management in Uruguay. Sci Hortic 165:331–335

    Article  CAS  Google Scholar 

  • Angelini LG, Carpanese G, Cioni PL, Morelli I, Macchia M, Flamini G (2003) Essential oils from Mediterranean Lamiaceae as weed germination inhibitors. J Agric Food Chem 51:6158–6164

    Article  CAS  Google Scholar 

  • Arminante F, De Falco E, De Feo V, De Martino L, Mancini E, Quaranta E (2006) Allelopathic activity of essential oils from Mediterranean Labiatae. Acta Hortic 723:347–356

    Article  CAS  Google Scholar 

  • Arslan M, Sibel D (2010) Antifungal activity of essential oils against three vegetative-compatibility groups of Verticillium dahliae. World J Microbiol Biotechnol 26(10):1813–1821

    Article  CAS  Google Scholar 

  • Arslan U, Ilhan K, Karabulut OA (2013) Evaluation of the use of ammonium bicarbonate and oregano (Origanum vulgare Ssp. Hirtum ) extract on the control of apple scab. J Phytopathol 161:6

    Article  Google Scholar 

  • Attia S, Grissa KL, Ghrabi ZG, Mailleux AC, Lognay G, Hance T (2012) Acaricidal activity of 31 essential oils extracted from plants collected in Tunisia. J Essent Oil Res 24:279–288

    Article  CAS  Google Scholar 

  • Azaz AD, Kürkcüoglu M, Satil F, Can Baser KH, Tümen G (2005) In vitro antimicrobial activity and chemical composition of some Satureja essential oils. Flavour Fragr J 20(6):587–591

    Article  CAS  Google Scholar 

  • Bakkali F, Averbeck S, Averbeck D, Idaomar M (2008) Biological effects of essential oils—a review. Food Chem Toxicol 46:446–475

    Article  CAS  Google Scholar 

  • Barrera-Necha LL, Garduno-Pizana C, Garcia-Barrera LJ (2009) In vitro antifungal activity of essential oils and their compounds on mycelial growth of Fusarium oxysporum f. sp. gladioli (Massey) Snyder and Hansen. Plant Pathol 8(1):17–21

    Article  Google Scholar 

  • Basilico MZ, Basilico JC (1999) Inhibitory effects of some spice essential oils on Aspergillus ochraceus NRRL 3174 growth and ochratoxin A production. Lett Appl Microbiol 29(4):238–241

    Article  CAS  Google Scholar 

  • Bennett R, Wallsgrove R (1994) Secondary metabolites in plant defence mechanisms. New Phytopathol 127:617–633

    Article  CAS  Google Scholar 

  • Bowen JK, Mesarich CH, Bus VGM, Beresford RM, Plummer KM, Templeton MD (2011) Venturia inaequalis: the causal agent of apple scab. Mol Plant Pathol 12:105–122

    Article  Google Scholar 

  • Braun PG, McRae KB (1992) Composition of a population of Venturia inaequalis resistant to myclobutanil. Can J Plant Pathol 14:215–220

    Article  CAS  Google Scholar 

  • Carisse O, Pelletier JR (1994) Sensitivity distribution of Venturia inaequalis to Fenarimol in Quebec apple orchards. Phytoprotection 75(1):35–43

    Article  Google Scholar 

  • Chao SC, Young DG, Oberg CJ (2000) Screening for inhibitory activity of essential oils on selected bacteria, fungi and viruses. J Essent Oil Res 12:639–649

    Article  CAS  Google Scholar 

  • Chavan PS, Tupe SG (2014) Antifungal activity and mechanism of action of carvacrol and thymol against vineyard and wine spoilage yeasts. Food Control 46:115–120

    Article  CAS  Google Scholar 

  • Cheng SS, Liu JY, Chang EH, Chang ST (2008) Antifungal activity of cinnamaldehyde and eugenol congeners against wood-rot fungi. Bioresour Technol 99(11):5145–5149

    Article  CAS  Google Scholar 

  • Coskun S, Girisgin O, Kürkcüoglu M, Malyer H, Girisgin AO, Kırımer N, Baser KH (2008) Acaricidal efficacy of Origanum onites L. essential oil against Rhipicephalus turanicus (Ixodidae). Parasitol Res 103:259–261

    Article  Google Scholar 

  • Da Cruz Cabral L, Fernández Pinto V, Patriarca A (2013) Application of plant derived compounds to control fungal spoilage and mycotoxin production in foods. Int J Food Microbiol 166:1–14

    Article  Google Scholar 

  • Davidson P, Taylor T, Schmidt S (2013) Chemical preservatives and natural antimicrobial compounds. In: Doyle M, Buchanan R (eds) Food microbiology. ASM Press, Washington, DC, pp 765–801. https://doi.org/10.1128/9781555818463.ch30

    Chapter  Google Scholar 

  • EFSA (2013) Conclusion on the peer review of the pesticide risk assessment of confirmatory data submitted for the active substance copper (I), copper (II) variants namely copper hydroxide, copper oxychloride, tribasic copper sulphate, copper (I) oxide, Bordeaux mixture. EFSA J 11(6):3235–3275

    Article  Google Scholar 

  • Gao L, Berrie A, Yang J, Xu X (2009) Within- and between-orchard variability in the sensitivity of Venturia inaequalis to myclobutanil, a DMI fungicide, in the UK. Pest Manag Sci 65(11):1241–1249

    Article  CAS  Google Scholar 

  • Giweli A, Džamić AM, Soković M, Ristić MS, Marin PD (2012) Antimicrobial and antioxidant activities of essential oils of Satureja thymbra growing wild in Libya. Molecules 17(12):4836–4850

    Article  CAS  Google Scholar 

  • Govindarajan M, Sivakumar R, Rajeswari M, Yogalakshmi K (2012) Chemical composition and larvicidal activity of essential oil from Mentha spicata (Linn.) against three mosquito species. Parasitol Res 110:2023–2032

    Article  CAS  Google Scholar 

  • Hemaiswarya S, Doble M (2009) Synergistic interaction of eugenol with antibiotics against gram negative bacteria. Phytomedicine 16:997–1005

    Article  CAS  Google Scholar 

  • Hossain MB, Piotrowski M, Lensing J, Gau AE (2009) Inhibition of conidial growth of Venturia inaequalis by the extracellular protein fraction from the antagonistic bacterium Pseudomonas fluorescens Bk3. Biol Control 48(2):133–139

    Article  Google Scholar 

  • Ibrahim L, Karaky M, Ayoub P, El Ajouz N, Ibrahim S (2012) Chemical composition and antimicrobial activities of essential oil and its components from Lebanese Origanum syriacum L. J Essent Oil Res 24(4):339–345

    Article  CAS  Google Scholar 

  • Ilhan K, Arslan U, Karabulut OA (2006) The effect of sodium bicarbonate alone or in combination with a reduced dose of tebuconazole on the control of apple scab. Crop Prot 25(9):963–967

    Article  CAS  Google Scholar 

  • Isman MB, Miresmailli S, Machial C (2011) Commercial opportunities for pesticides based on plant essential oils in agriculture, industry and consumer products. Phytochem Rev 10:197–204

    Article  CAS  Google Scholar 

  • Jha G, Thakur K, Thakur P (2009) The Venturia apple pathosystem: pathogenicity mechanisms and plant defence responses. J Biomed Biotechnol 2009: 1–10. https://doi.org/10.1155/2009/680160

    Article  Google Scholar 

  • Köller W, Parker DM, Reynolds KL (1991) Baseline sensitivities of Venturia inaequalis to sterol demethylation inhibitors. Plant Dis 75(7):726–728

    Article  Google Scholar 

  • Köller W, Smith FD, Reynolds JKL, Wilcox WF, Burri JA (1995) Seasonal changes of sensitivities to sterol demethylation inhibitors in Venturia inaequalis populations. Mycol Res 99(6):689–692

    Article  Google Scholar 

  • Kordali S, Cakir A, Ozer H, Cakmakci R, Kesdek M, Mete E (2008) Antifungal, phytotoxic and insecticidal properties of essential oil isolated from Turkish Origanum acutidens and its three components, carvacrol, thymol and p-cymene. Bioresour Technol 99:8788–8795

    Article  CAS  Google Scholar 

  • Kunz S, Deising H, Mendgen K (1997) Acquisition of resistance to sterol demethylation inhibitors by populations of Venturia inaequalis. Phytopathology 87(12):1272–1278

    Article  CAS  Google Scholar 

  • Kunz S, Lutz B, Deising H, Mendgen K (1998) Assessment of sensitivities to anilopyrimidine and strobilurin-fungicides in populations of the apple scab fungus Venturia inaequalis. J Phytopathol 146:231–238

    Article  CAS  Google Scholar 

  • Lee YS, Kim J, Marshall MR, Wei C (1995) Antibacterial activity of some essential oil components against five foodborne pathogens. J Agric Food Chem 43:2839–2845

    Article  Google Scholar 

  • Martinez-Romero D, Guillen F, Valverde JM, Bailen G, Zapata PJ, Serrano M (2007) Influence of carvacrol on survival of Botrytis cinerea inoculated in table grapes. Int J Food Microbiol 115:144–148

    Article  CAS  Google Scholar 

  • Mondino P, Casanova L, Celio A, Bentancur O, Leoni C, Alaniz S (2015) Sensitivity of Venturia Inaequalis to trifloxystrobin and difenoconazole in Uruguay. J Phytopathol 163(1):1–10

    Article  CAS  Google Scholar 

  • Montag J, Schreiber L, Schönherr J (2005) An in vitro study on the post infection activities of hydrated lime and lime sulphur against apple scab (Venturia inaequalis). J Phytopathol 153(7–8):485–491

    Article  CAS  Google Scholar 

  • Montag J, Schreiber L, Schönherr J (2006) An in vitro study of the nature of protective activities of copper sulphate, copper hydroxide and copper oxide against conidia of Venturia inaequalis. J Phytopathol 154:474–481

    Article  CAS  Google Scholar 

  • Nagy G, Hochbaum T, Sarosi S, Ladanyi M (2014) In vitro and in planta activity of some essential oils against Venturia inaequalis (Cooke) G. Winter Not Bot Horti Agrobot Cluj Napoca 42(1):109–114

    CAS  Google Scholar 

  • Nana WL, Eke P, Fokom R, Via IB, Begoude D, Tchana T, Tchameni NS, Kuate J, Menut C, Boyom FF (2015) Antimicrobial activity of Syzygium aromaticum and Zanthoxylum xanthoxyloides essential oils against Phytophthora megakarya. J Phytopathol 163(7–8):632–641

    Article  CAS  Google Scholar 

  • Olaya G, Köller W (1999) Diversity of kresoxim-methyl sensitivities in baseline populations of Venturia inaequalis. Pestic Sci 55:1083–1088

    Article  CAS  Google Scholar 

  • Omidbeygi M, Barzegar M, Hamidi Z, Naghdibadi H (2007) Antifungal activity of thyme, summer savory and clove essential oils against Aspergillus flavus in liquid medium and tomato paste. Food Control 18(12):1518–1523

    Article  CAS  Google Scholar 

  • Perumal AB, Sellamuthu PS, Nambiar RB, Sadiku ER (2016) Antifungal activity of five different essential oils in vapour phase for the control of Colletotrichum gloeosporioides and Lasiodiplodia theobromae in vitro and on mango. Int J Food Sci Technol 51(2):411–418

    Article  CAS  Google Scholar 

  • Ramezani H, Singh HP, Batish DR, Kohli RK (2002) Antifungal activity of the volatile oil of Eucalyptus citriodora. Fitoterapia 73:261–262

    Article  CAS  Google Scholar 

  • Ritz C, Streibig JC (2008) Nonlinear regression with R. Springer, New York

    Google Scholar 

  • Sameza ML, Mabou LCN, Tchameni SN, Bedine MAB, Tchoumbougnang F, Dongmo PMJ, Boyom Fekam F (2016) Evaluation of clove essential oil as a mycobiocide against Rhizopus stolonifer and Fusarium solani, tuber rot causing fungi in yam (Dioscorea Rotundata Poir.) J Phytopathol 164(7–8):433–440

    Article  CAS  Google Scholar 

  • Schnabel G, Jones AL (2001) The 14α−demethylase (CYP51A1) gene is overexpressed in Venturia inaequalis strains resistant to myclobutanil. Phytopathology 91:102–110

    Article  CAS  Google Scholar 

  • Shaaban HAE, El-Ghorab AH, Shibamoto T (2012) Bioactivity of essential oils and their volatile aroma components: review. J Essent Oil Res 24(2):203–212

    Article  CAS  Google Scholar 

  • Sharma N, Gruszewski HA, Park SW, Holm DG, Vivanco JM (2004) Purification of an isoform of patatin with antimicrobial activity against Phytophthora infestans. Plant Physiol Bioch 42(7–8):647–655

    Article  CAS  Google Scholar 

  • Shimoni M, Putievsky E, Ravid U, Reuveni R (1993) Antifungal activity of volatile fractions of essential oils from four aromatic wild plants in Israel. J Chem Ecol 19(6):1129–1133

    Article  CAS  Google Scholar 

  • Shirane N, Takenaka H, Ueda K, Hashimoto Y, Katoh K, Ishii H (1996) Sterol analysis of DMI-resistant and -sensitive strains of Venturia inaequalis. Phytochemistry 41(5):1301–1308

    Article  CAS  Google Scholar 

  • Sikkema J, De Bont JAM, Poolman B (1995) Mechanisms of membrane toxicity of hydrocarbons. Microbiol Rev 59:201–222

    CAS  Google Scholar 

  • Soković MD, Vukojević J, Marin PD, Brkić DD, Vajs V, Van Griensven LJLD (2009) Chemical composition of essential oils of thymus and mentha species and their antifungal activities. Molecules 14(1):238–249

    Article  Google Scholar 

  • Soylu S, Yigitbas H, Soylu EM, Kurt S (2007) Antifungal effects of essential oils from oregano and fennel on Sclerotinia sclerotiorum. J Appl Microbiol 103(4):1021–1030

    Article  CAS  Google Scholar 

  • Soylu EM, Kurt S, Soylu S (2010) In vitro and in vivo antifungal activities of the essential oils of various plants against tomato grey mould disease agent Botrytis cinerea. Int J Food Microbiol 143(3):183–189

    Article  CAS  Google Scholar 

  • Stammler G, Taher K, Koch A, Haber J, Liebmann B, Bouagila A, Yahyaoui A, Nasraoui B (2012) Sensitivity of Mycosphaerella graminicola isolates from Tunisia to epoxiconazole and pyraclostrobin. Crop Prot 34:32–36

    Article  CAS  Google Scholar 

  • Tullio V, Nostro A, Mandras N, Dugo P, Banche G, Cannatelli MA, Cuffini AM, Alonzo V, Carlone NA (2006) Antifungal activity of essential oils against filamentous fungi determined by broth microdilution and vapour contact methods. J Appl Microbiol 102(6):1544–1550

    Article  Google Scholar 

  • Ultee A, Bennik MHJ, Moezelaar R (2002) The phenolic hydroxyl group of carvacrol is essential for action against the food borne pathogen Bacillus cereus. Appl Environ Microbiol 8:1561–1568

    Article  Google Scholar 

  • Vijaya Palani P, Lalithakumari D (1999) Resistance of Venturia inaequalis to the sterol biosynthesis inhibiting fungicide, penconazole [1-(2-(2,4-dichlorophenyl) pentyl)-1H-1,2,4-triazole]. Mycol Res 103(9):1157–1164

    Article  Google Scholar 

  • Wilson CL, Solar JM, Ghaouth AE, Wisniewski ME (1998) Rapid evaluation of plant extracts and essential oils for antifungal activity against Botrytis cinerea. Plant Dis 81:204–210

    Article  Google Scholar 

  • Xie Y, Yang Z, Cao D, Rong F, Ding H, Zhang D (2015) Antitermitic and antifungal activities of eugenol and its congeners from the flower buds of Syzygium aromaticum (clove). Ind Crop Prod 77:780–786

    Article  CAS  Google Scholar 

  • Xu XM, Gao LQ, Yang JR (2010) Are insensitivities of Venturia inaequalis to myclobutanil and fenbuconazole correlated? Crop Prot 29:183–189

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Dr. Christophe Waterlot (ISA-Yncréa, LGCgE) for his assistance and suggestions.

Funding

The authors would like to thank the Ministry of Agriculture, Agri-Food and Forestry for the co-financing of this study (CASDAR).

Author information

Authors and Affiliations

  1. Charles Viollette Research Institute, EA 7394, SFR Condorcet FR CNRS 3417, ISA-Yncréa, 48 boulevard Vauban, 59014, Lille Cedex, France

    Jérôme Muchembled, Caroline Deweer & Patrice Halama

  2. Civil and Geo-Environmental Engineering Laboratory (LGCgE), ISA-Yncréa, 48 boulevard Vauban, 59014, Lille Cedex, France

    Karin Sahmer

Authors
  1. Jérôme Muchembled
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Caroline Deweer
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Karin Sahmer
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Patrice Halama
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jérôme Muchembled.

Additional information

Responsible editor: Philippe Garrigues

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Muchembled, J., Deweer, C., Sahmer, K. et al. Antifungal activity of essential oils on two Venturia inaequalis strains with different sensitivities to tebuconazole. Environ Sci Pollut Res 25, 29921–29928 (2018). https://doi.org/10.1007/s11356-017-0507-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-017-0507-z

Keywords

Search

Navigation