Advertisement

Environmental Science and Pollution Research

, Volume 25, Issue 30, pp 29921–29928 | Cite as

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

  • Jérôme Muchembled
  • Caroline Deweer
  • Karin Sahmer
  • Patrice Halama
Chemistry, Activity and Impact of Plant Biocontrol products

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.

Keywords

Biofungicide Essential oils Venturia inaequalis In vitro assay 

Notes

Acknowledgments

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

Funding information

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

References

  1. 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 30:41–50CrossRefGoogle Scholar
  2. 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):440–444CrossRefGoogle Scholar
  3. Alaniz S, Leoni C, Bentancor O, Mondino P (2014) Elimination of summer fungicide sprays for apple scab (Venturia inaequalis) management in Uruguay. Sci Hortic 165:331–335CrossRefGoogle Scholar
  4. 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 51:6158–6164CrossRefGoogle Scholar
  5. 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 723:347–356CrossRefGoogle Scholar
  6. Arslan M, Sibel D (2010) Antifungal activity of essential oils against three vegetative-compatibility groups of Verticillium dahliae. World J Microbiol Biotechnol 26(10):1813–1821CrossRefGoogle Scholar
  7. 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 161:6CrossRefGoogle Scholar
  8. 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 24:279–288CrossRefGoogle Scholar
  9. 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):587–591CrossRefGoogle Scholar
  10. Bakkali F, Averbeck S, Averbeck D, Idaomar M (2008) Biological effects of essential oils—a review. Food Chem Toxicol 46:446–475CrossRefGoogle Scholar
  11. 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):17–21CrossRefGoogle Scholar
  12. 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):238–241CrossRefGoogle Scholar
  13. Bennett R, Wallsgrove R (1994) Secondary metabolites in plant defence mechanisms. New Phytopathol 127:617–633CrossRefGoogle Scholar
  14. Bowen JK, Mesarich CH, Bus VGM, Beresford RM, Plummer KM, Templeton MD (2011) Venturia inaequalis: the causal agent of apple scab. Mol Plant Pathol 12:105–122CrossRefGoogle Scholar
  15. Braun PG, McRae KB (1992) Composition of a population of Venturia inaequalis resistant to myclobutanil. Can J Plant Pathol 14:215–220CrossRefGoogle Scholar
  16. Carisse O, Pelletier JR (1994) Sensitivity distribution of Venturia inaequalis to Fenarimol in Quebec apple orchards. Phytoprotection 75(1):35–43CrossRefGoogle Scholar
  17. Chao SC, Young DG, Oberg CJ (2000) Screening for inhibitory activity of essential oils on selected bacteria, fungi and viruses. J Essent Oil Res 12:639–649CrossRefGoogle Scholar
  18. Chavan PS, Tupe SG (2014) Antifungal activity and mechanism of action of carvacrol and thymol against vineyard and wine spoilage yeasts. Food Control 46:115–120CrossRefGoogle Scholar
  19. Cheng SS, Liu JY, Chang EH, Chang ST (2008) Antifungal activity of cinnamaldehyde and eugenol congeners against wood-rot fungi. Bioresour Technol 99(11):5145–5149CrossRefGoogle Scholar
  20. 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 103:259–261CrossRefGoogle Scholar
  21. 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 166:1–14CrossRefGoogle Scholar
  22. 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 CrossRefGoogle Scholar
  23. 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):3235–3275CrossRefGoogle Scholar
  24. 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):1241–1249CrossRefGoogle Scholar
  25. 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):4836–4850CrossRefGoogle Scholar
  26. 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 110:2023–2032CrossRefGoogle Scholar
  27. Hemaiswarya S, Doble M (2009) Synergistic interaction of eugenol with antibiotics against gram negative bacteria. Phytomedicine 16:997–1005CrossRefGoogle Scholar
  28. 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):133–139CrossRefGoogle Scholar
  29. 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):339–345CrossRefGoogle Scholar
  30. 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):963–967CrossRefGoogle Scholar
  31. Isman MB, Miresmailli S, Machial C (2011) Commercial opportunities for pesticides based on plant essential oils in agriculture, industry and consumer products. Phytochem Rev 10:197–204CrossRefGoogle Scholar
  32. 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 CrossRefGoogle Scholar
  33. Köller W, Parker DM, Reynolds KL (1991) Baseline sensitivities of Venturia inaequalis to sterol demethylation inhibitors. Plant Dis 75(7):726–728CrossRefGoogle Scholar
  34. 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):689–692CrossRefGoogle Scholar
  35. 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 99:8788–8795CrossRefGoogle Scholar
  36. Kunz S, Deising H, Mendgen K (1997) Acquisition of resistance to sterol demethylation inhibitors by populations of Venturia inaequalis. Phytopathology 87(12):1272–1278CrossRefGoogle Scholar
  37. 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 146:231–238CrossRefGoogle Scholar
  38. Lee YS, Kim J, Marshall MR, Wei C (1995) Antibacterial activity of some essential oil components against five foodborne pathogens. J Agric Food Chem 43:2839–2845CrossRefGoogle Scholar
  39. 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 115:144–148CrossRefGoogle Scholar
  40. 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):1–10CrossRefGoogle Scholar
  41. 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):485–491CrossRefGoogle Scholar
  42. 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 154:474–481CrossRefGoogle Scholar
  43. 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):109–114Google Scholar
  44. 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):632–641CrossRefGoogle Scholar
  45. Olaya G, Köller W (1999) Diversity of kresoxim-methyl sensitivities in baseline populations of Venturia inaequalis. Pestic Sci 55:1083–1088CrossRefGoogle Scholar
  46. 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):1518–1523CrossRefGoogle Scholar
  47. 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):411–418CrossRefGoogle Scholar
  48. Ramezani H, Singh HP, Batish DR, Kohli RK (2002) Antifungal activity of the volatile oil of Eucalyptus citriodora. Fitoterapia 73:261–262CrossRefGoogle Scholar
  49. Ritz C, Streibig JC (2008) Nonlinear regression with R. Springer, New YorkGoogle Scholar
  50. 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):433–440CrossRefGoogle Scholar
  51. Schnabel G, Jones AL (2001) The 14α−demethylase (CYP51A1) gene is overexpressed in Venturia inaequalis strains resistant to myclobutanil. Phytopathology 91:102–110CrossRefGoogle Scholar
  52. Shaaban HAE, El-Ghorab AH, Shibamoto T (2012) Bioactivity of essential oils and their volatile aroma components: review. J Essent Oil Res 24(2):203–212CrossRefGoogle Scholar
  53. 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):647–655CrossRefGoogle Scholar
  54. 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):1129–1133CrossRefGoogle Scholar
  55. 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):1301–1308CrossRefGoogle Scholar
  56. Sikkema J, De Bont JAM, Poolman B (1995) Mechanisms of membrane toxicity of hydrocarbons. Microbiol Rev 59:201–222Google Scholar
  57. 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):238–249CrossRefGoogle Scholar
  58. 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):1021–1030CrossRefGoogle Scholar
  59. 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):183–189CrossRefGoogle Scholar
  60. 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 34:32–36CrossRefGoogle Scholar
  61. 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):1544–1550CrossRefGoogle Scholar
  62. 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 8:1561–1568CrossRefGoogle Scholar
  63. 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):1157–1164CrossRefGoogle Scholar
  64. 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 81:204–210CrossRefGoogle Scholar
  65. 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 77:780–786CrossRefGoogle Scholar
  66. Xu XM, Gao LQ, Yang JR (2010) Are insensitivities of Venturia inaequalis to myclobutanil and fenbuconazole correlated? Crop Prot 29:183–189CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  1. 1.Charles Viollette Research Institute, EA 7394, SFR Condorcet FR CNRS 3417, ISA-YncréaLille CedexFrance
  2. 2.Civil and Geo-Environmental Engineering Laboratory (LGCgE), ISA-YncréaLille CedexFrance

Personalised recommendations