The Citrus reticulata essential oil: evaluation of antifungal activity against penicillium species related to bakery products spoilage

Authors

  • Veronika Valková AgroBioTech Research Centre, The Slovak University of Agriculture in Nitra, Tr. A. Hlinku 2, 94976 Nitra, Slovakia; Faculty of Horticulture and Landscape Engineering, Department of Fruit Sciences, Viticulture and Enology, Slovak University of Agriculture, Tr. A. Hlinku 2, 94976 Nitra, Slovakia, Tel.: +421376414928 https://orcid.org/0000-0001-7048-6323
  • Hana Ďúranová AgroBioTech Research Centre, The Slovak University of Agriculture in Nitra, Tr. A. Hlinku 2, 94976 Nitra, Slovakia, Tel.: +421376414975 https://orcid.org/0000-0002-7274-6210
  • Lucia Galovičová The Slovak University of Agriculture in Nitra, Faculty of Horticulture and Landscape Engineering, Department of Fruit Sciences, Viticulture and Enology, Tr. A. Hlinku 2, 94976 Nitra, Slovakia, Tel.: +421907260116 https://orcid.org/0000-0002-1203-4115
  • Jana Štefániková AgroBioTech Research Centre, The Slovak University of Agriculture in Nitra, Tr. A. Hlinku 2, 94976 Nitra, Slovakia, Tel.: +421376414911 https://orcid.org/0000-0002-3799-4390
  • Nenad Vukovic Department of Chemistry, Faculty of Science, University of Kragujevac, 34000 Kragujevac, Serbia, Tel.: +38134336223 https://orcid.org/0000-0003-4382-9743
  • Miroslava Kačániová Faculty of Horticulture and Landscape Engineering, Department of Fruit Sciences, Viticulture and Enology, Slovak University of Agriculture, Tr. A. Hlinku 2, 94976 Nitra, Slovakia; Institute of Food Technology and Nutrition, University of Rzeszow, Department of Bioenergy, Food Technology and Microbiology, Zelwerowicza St. 4, 35601 Rzeszow, Poland, Tel.: +421376414715 https://orcid.org/0000-0002-4460-0222

DOI:

https://doi.org/10.5219/1695

Keywords:

Citrus reticulata, volatile compound, DPPH assay, antifungal properties, bread

Abstract

Fungal food spoilage plays a key role in the deterioration of food products, and finding a suitable natural preservative can solve this problem. Therefore, antifungal activity of green mandarin (Citrus reticulata) essential oil (GMEO) in the vapor phase against the growth of Penicillium (P.) expansum and P. chrysogenum inoculated on wheat bread (in situ experiment) was investigated in the current research. The volatile compounds of the GMEO were analyzed by a gas chromatograph coupled to a mass spectrometer (GC–MS), and its antioxidant activity was determined by testing free radical-scavenging capacity (DPPH assay). Moreover, the disc diffusion method was used to analyze the antifungal activity of GMEO in in vitro conditions. The results demonstrate that the Citrus reticulata EO consisted of α-limonene as the most abundant component (71.5%), followed by γ-terpinene (13.9%), and β-pinene (3.5%), and it displayed the weak antioxidant activity with the value of inhibition 5.6 ±0.7%, which corresponds to 103.0 ±6.4 µg TEAC.mL-1. The findings from the GMEO antifungal activity determination revealed that values for the inhibition zone with disc diffusion method ranged from 0.00 ±0.00 (no antifungal effectiveness) to 5.67 ±0.58 mm (moderate antifungal activity). Finally, exposure of Penicillium strains growing on bread to GMEO in vapor phase led to the finding that 250 μL.L-1 of GMEO exhibited the lowest value for mycelial growth inhibition (MGI) of P. expansum (-51.37 ±3.01%) whose negative value reflects even supportive effect of the EO on the microscopic fungus growth. On the other hand, GMEO at this concentration (250 μL.L-1) resulted in the strongest inhibitory action (MGI: 54.15 ±1.15%) against growth of P. chrysogenum. Based on the findings it can be concluded that GMEO in the vapor phase is not an effective antifungal agent against the growth of P. expansum inoculated on bread; however, its antifungal potential manifested against P. chrysogenum suggests GMEO to be an appropriate alternative to the use of chemical inhibitors for bread preservation.

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References

Adams, R. P. 2007. Identification of Essential Oil Components by Gas Chromatography/Mass Spectrometry. USA : Allured Publishing Corporation, Carol Stream, IL. 456 p. ISBN 978-1-932633-11-4.

Badawy, M. E., Lotfy, T. M., Shawir, S. M. 2020. Facile synthesis and characterizations of antibacterial and antioxidant of chitosan monoterpene nanoparticles and their applications in preserving minced meat. International journal of biological macromolecules, vol. 156, p. 127-136. https://doi.org/10.1016/j.ijbiomac.2020.04.044

Badee, A. Z. M., Helmy, S. A., Morsy, N. F. 2011. Utilisation of orange peel in the production of α-terpineol by Penicillium digitatum (NRRL 1202). Food Chemistry, vol. 126, no. 3, p. 849-854. https://doi.org/10.1016/j.foodchem.2010.11.046

Behbahani, B. A., Shahidi, F., Yazdi, F. T., Mortazavi, S. A., Mohebbi, M. 2017. Antioxidant activity and antimicrobial effect of tarragon (Artemisia dracunculus) extract and chemical composition of its essential oil. Journal of Food Measurement and Characterization, vol. 11, no. 2, p. 847-863. https://doi.org/10.1007/s11694-016-9456-3

Boudiba, S., Tamfu, A. N., Berka, B., Hanini, K., Hioun, S., Allaf, K., Boudiba, L., Ceylan, O. 2021. Anti-quorum sensing and antioxidant activity of essential oils extracted from juniperus species, growing spontaneously in Tebessa Region (East of Algeria). Natural Product Communications, vol. 16, no. 6, p. 1-11. https://doi.org/10.1177/1934578X211024039

Boudries, H., Loupassaki, S., Ladjal Ettoumi, Y., Souagui, S., Bachir Bey, M., Nabet, N., Chikhounne, A., Madani, K., Chibane, M. 2017. Chemical profile, antimicrobial and antioxidant activities of Citrus reticulata and Citrus clementina (L.) essential oils. International Food Research Journal, vol. 24, no. 4, p. 1782-1792.

Boughendjioua, H., Mezedjeri, N. E. H., Idjouadiene, I. 2020. Chemical constituents of Algerian mandarin (Citrus reticulata) essential oil by GC-MS and FT-IR analysis. vol. 33, no. 4, p. 197-201. https://doi.org/10.2478/cipms-2020-0032

Burt, S. 2004. Essential oils: their antibacterial properties and potential applications in foods—a review. International journal of food microbiology, vol. 94, no. 3, p. 223-253. https://doi.org/10.1016/j.ijfoodmicro.2004.03.022

Chouhan, S., Sharma, K., Guleria, S. 2017. Antimicrobial activity of some essential oils—present status and future perspectives. Medicines, vol. 4, no. 3, p. 58. https://doi.org/10.3390/medicines4030058

Cox, S. D., Markham, J. L. 2007. Susceptibility and intrinsic tolerance of Pseudomonas aeruginosa to selected plant volatile compounds. Journal of Applied Microbiology, vol. 103, no. 4, p. 930-936. https://doi.org/10.1111/j.1365-2672.2007.03353.x

Demyttenaere, J. C., Van Belleghem, K., De Kimpe, N. 2001. Biotransformation of (R)-(+)-and (S)-(−)-limonene by fungi and the use of solid phase microextraction for screening. Phytochemistry, vol. 57, no. 2, p. 199-208. https://doi.org/10.1016/S0031-9422(00)00499-4

Denkova-Kostova, R., Teneva, D., Tomova, T., Goranov, B., Denkova, Z., Shopska, V., Slavchev, A., Hristova-Ivanova, Y. 2021. Chemical composition, antioxidant and antimicrobial activity of essential oils from tangerine (Citrus reticulata L.), grapefruit (Citrus paradisi L.), lemon (Citrus lemon L.) and cinnamon (Cinnamomum zeylanicum Blume). Zeitschrift für Naturforschung C, vol. 76, no. 5-6, pp. 175-185. https://doi.org/10.1515/znc-2020-0126

Diniz do Nascimento, L., Moraes, A. A. B. D., Costa, K. S. D., Pereira Galúcio, J. M., Taube, P. S., Costa, C. M. L., Cruz, J. N., de Aguiar Andrade, E. H., Faria, L. J. G. D. 2020. Bioactive natural compounds and antioxidant activity of essential oils from spice plants: New findings and potential applications. Biomolecules, vol. 10, no. 7, p. 988. https://doi.org/10.3390/biom10070988

Droby, S. A. M. I. R., Eick, A., Macarisin, D., Cohen, L., Rafael, G. I. N. A. T., Stange, R., Shapira, R. 2008. Role of citrus volatiles in host recognition, germination and growth of Penicillium digitatum and Penicillium italicum. Postharvest Biology and Technology, vol. 49, no. 3, p. 386-396. https://doi.org/10.1016/j.postharvbio.2008.01.016

Espina, L., Somolinos, M., Lorán, S., Conchello, P., García, D., Pagán, R. 2011. Chemical composition of commercial citrus fruit essential oils and evaluation of their antimicrobial activity acting alone or in combined processes. Food control, vol. 22, no. 6, p. 896-902. https://doi.org/10.1016/j.foodcont.2010.11.021

Fayed, S. A. 2009. Antioxidant and anticancer activities of Citrus reticulate (Petitgrain Mandarin) and Pelargonium graveolens (Geranium) essential oils. Research Journal of Agriculture and Biological Sciences, vol. 5, no. 5. p. 740-747.

Galovičová, L., Borotová, P., Valková, V., Vukovic, N. L., Vukic, M., Terentjeva, M., Štefániková, J., Ďúranová, H., Kowalczewski, P. L., Kačániová, M. 2021. Thymus serpyllum Essential Oil and Its Biological Activity as a Modern Food Preserver. Plants, vol. 10, no. 7, p. 1416. https://doi.org/10.3390/plants10071416

Gao, Y., Tao, N., Liu, Y., Ge, F., Feng, B. 2010. Antimicrobial Activity of the Essential Oil from the Peel of Ponkan (Citrus reticulate Blanco). Journal of Essential Oil Bearing Plants, vol. 13, no. 2, p. 230-236. https://doi.org/10.1080/0972060X.2010.10643817

Inouye, S., Abe, S., Yamaguchi, H., Asakura, M. 2003. Comparative study of antimicrobial and cytotoxic effects of selected essential oils by gaseous and solution contacts. International Journal of Aromatherapy, vol. 13, vol. 1, p. 33-41. https://doi.org/10.1016/S0962-4562(03)00057-2

Ishfaq, M., Akhtar, B., Muhammad, F., Sharif, A., Akhtar, M. F., Hamid, I., Sohail, M., Muhammad, H. 2021. Antioxidant and Wound Healing Potential of Essential Oil from Citrus reticulata Peel and Its Chemical Characterization. Medicinal Values of Peels Essential Oil. Current Pharmaceutical Biotechnology, vol. 22, no. 8, pp. 1114-1121. https://doi.org/10.2174/1389201021999200918102123

Kačániová, M., Galovičová, L., Ivanišová, E., Vukovic, N. L., Štefániková, J., Valková, V., Borotová, P., Žiarovská, J., Terentjeva, M., Felšöciová, S., Tvrdá, E. 2020b. Antioxidant, antimicrobial and antibiofilm activity of coriander (Coriandrum sativum L.) essential oil for its application in foods. Foods, vol. 9, p. 3, p. 282. https://doi.org/10.3390/foods9030282

Kačániová, M., Terentjeva, M., Galovičová, L., Ivanišová, E., Štefániková, J., Valková, V., Borotová, P., Kowalczewski, P. L., Kunová, S., Felcosiova, S., Tvrdá, E., Žiarovksá, J., Prokeinová, R. B., Vukovic, N. 2020a. Biological activity and antibiofilm molecular profile of Citrus aurantium essential oil and its application in a food model. Molecules, vol. 25, no. 17, p. 3956. https://doi.org/10.3390/molecules25173956

Salas, M. L, Mounier, J., Valence, F., Coton, M., Thierry, A., Coton, E. 2017. Antifungal microbial agents for food biopreservation—a review. Microorganisms, vol. 5, no. 3, p. 37. https://doi.org/10.3390/microorganisms5030037

Miladinovic, D. L., Ilic, B. S., Matejic, J. S., Randjelovic, V. N., Nikolic, D. M. 2015. Chemical composition of the essential oil of Geum coccineum. Chemistry of Natural Compounds, vol. 51, no. 4, p. 785-786. https://doi.org/10.1007/s10600-015-1412-7

Mondello, F., Girolamo, A., Scaturro, M., Ricci, M. L. 2009. Determination of Legionella pneumophila susceptibility to Melaleuca alternifolia Cheel (tea tree) oil by an improved broth micro-dilution method under vapour controlled conditions. Journal of microbiological methods, vol. 77, no. 2, p. 243-248. https://doi.org/10.1016/j.mimet.2009.02.012

Noipa, T., Srijaranai, S., Tuntulani, T., Ngeontae, W. 2011. New approach for evaluation of the antioxidant capacity based on scavenging DPPH free radical in micelle systems. Food research international, vol. 44, no. 3, p. 798-806. https://doi.org/10.1016/j.foodres.2011.01.034

Raspo, M. A., Vignola, M. B., Andreatta, A. E., Juliani, H. R. 2020. Antioxidant and antimicrobial activities of citrus essential oils from Argentina and the United States. Food Bioscience, vol. 36, p. 100651. https://doi.org/10.1016/j.fbio.2020.100651

Sandeep, I. S., Sanghamitra, N., Sujata, M. 2015. Differential effect of soil and environment on metabolic expression of turmeric (Curcuma longa cv. Roma). Indian Journal of Experimental Biology, vol. 53, p. 406-411.

Schaich, K. M., Tian, X., Xie, J. 2015. Hurdles and pitfalls in measuring antioxidant efficacy: A critical evaluation of ABTS, DPPH, and ORAC assays. Journal of functional foods, vol. 14, p. 111-125. https://doi.org/10.1016/j.jff.2015.01.043

Sempere-Ferre, F., Asamar, J., Castell, V., Roselló, J., Santamarina, M. P. 2021. Evaluating the Antifungal Potential of Botanical Compounds to Control Botryotinia fuckeliana and Rhizoctonia solani. Molecules, vol. 26, no. 9, p. 2472. https://doi.org/10.3390/molecules26092472

Shaaban, H. A. 2020. Essential Oil as Antimicrobial Agents: Efficacy, Stability, and Safety Issues for Food Application. Essential Oils-Bioactive Compounds, New Perspectives and Applications, p. 1-33. https://doi.org/10.5772/intechopen.92305

Sharifi-Rad, J., Sureda, A., Tenore, G. C., Daglia, M., Sharifi-Rad, M., Valussi, M., Tundis, R., Sharifi-Rad, M., Loizzo, M. R., Ademiluyi, Sharifi-Rad, M., Ayatollahi, S. A., Iriti, M. 2017. Biological activities of essential oils: From plant chemoecology to traditional healing systems. Molecules, vol. 22, no. 1, p. 70. https://doi.org/10.3390/molecules22010070

Sharma, N., Tripathi, A. 2006. Fungitoxicity of the essential oil of Citrus sinensis on post-harvest pathogens. World Journal of Microbiology and Biotechnology, vol. 22, no. 6, p. 587-593. https://doi.org/10.1007/s11274-005-9075-3

Sharma, N., Tripathi, A. 2008. Effects of Citrus sinensis (L.) Osbeck epicarp essential oil on growth and morphogenesis of Aspergillus niger (L.) Van Tieghem. Microbiological research, vol. 163, no. 3, p. 337-344.

Sikkema, J., de Bont, J. A., Poolman, B. 1995. Mechanisms of membrane toxicity of hydrocarbons. Microbiological reviews, vol. 59, no. 2, p. 201-222. https://doi.org/10.1128/mr.59.2.201-222.1995

Soylu, E. M., Soylu, S., Kurt, S. 2006. Antimicrobial activities of the essential oils of various plants against tomato late blight disease agent Phytophthora infestans. Mycopathologia, vol. 161, no. 2, 119-128. https://doi.org/10.1007/s11046-005-0206-z

Srinivasan, V., Thankamani, C. K., Dinesh, R., Kandiannan, K., Zachariah, T. J., Leela, N. K., Hamza, S., Ansha, O. 2016. Nutrient management systems in turmeric: Effects on soil quality, rhizome yield and quality. Industrial crops and Products, vol. 85, p. 241-250. https://doi.org/10.1016/j.indcrop.2016.03.027

Tan, Q., Day, D. F., Cadwallader, K. R. 1998. Bioconversion of (R)-(+)-limonene by P. digitatum (NRRL 1202). Process Biochemistry, vol. 33, no. 1, p. 29-37. https://doi.org/10.1016/S0032-9592(97)00048-4

Tao, N. G., Liu, Y. J., Tang, Y. F., Zhang, J. H., Zhang, M. L., Zeng, H. Y. 2009. Essential oil composition and antimicrobial activity of Citrus reticulata. Chemistry of Natural Compounds, vol. 45, no. 3, p. 437-438.

Tullio, V., Nostro, A., Mandras, N., Dugo, P., Banche, G., Cannatelli, M. A., Cuffini, A. M., Alonzo, V., Carlone, N. A. 2007. Antifungal activity of essential oils against filamentous fungi determined by broth microdilution and vapour contact methods. Journal of applied microbiology, vol. 102, no. 6, p. 1544-1550. https://doi.org/10.1111/j.1365-2672.2006.03191.x

Tyagi, A. K., Malik, A. 2010. Antimicrobial action of essential oil vapours and negative air ions against Pseudomonas fluorescens. International journal of food microbiology, vol. 143, no. 3, p. 205-210. https://doi.org/10.1016/j.ijfoodmicro.2010.08.023

Valková, V., Ďúranová, H., Galovičová, L., Vukovic, N. L., Vukic, M., Kačániová, M. 2021. In Vitro Antimicrobial Activity of Lavender, Mint, and Rosemary Essential Oils and the Effect of Their Vapours on Growth of Penicillium spp. in a Bread Model System. Molecules, vol. 26, no. 13, p. 3859. https://doi.org/10.3390/molecules26133859

Van Den Dool, H., Kratz, P. D. 1963. A Generalization of the Retention Index System Including Linear Temperature Programmed Gas-Liquid Partition Chromatography. Journal of Chromatography A, vol. 11, p. 463-471.

Viuda-Martos, M., Ruiz-Navajas, Y., Fernández-López, J., Pérez-Álvarez, J. A. 2009. Chemical composition of mandarin (C. reticulata L.), grapefruit (C. paradisi L.), lemon (C. limon L.) and orange (C. sinensis L.) essential oils. Journal of Essential Oil Bearing Plants, vol. 12, vol. 2, p. 236-243. https://doi.org/10.1080/0972060X.2009.10643716

Viuda-Martos, M., Ruíz-Navajas, Y., Fernández-López, J., Pérez-Álvarez, J. A. 2007. Chemical composition of the essential oils obtained from some spices widely used in Mediterranean region. Acta Chimica Slovenica, vol. 54, no. 4, p. 921-926.

Wang, H., Tao, N., Huang, S., Liu, Y. 2012. Effect of Shatangju (Citrus reticulata Blanco) essential oil on spore germination and mycelium growth of Penicillium digitatum and P. italicum. Journal of Essential Oil Bearing Plants, vol. 15, no. 5, p. 715-723. https://doi.org/10.1080/0972060X.2012.10644111

Yabalak, E., Eliuz, E. A., Nazlı, M. D. 2021. Evaluation of Citrus reticulata essential oil: Chemical composition and antibacterial effectiveness incorporated gelatin on E. coli and S. aureus. International Journal of Environmental Health Research, p. 1-10. https://doi.org/10.1080/09603123.2021.1872059

Published

2021-10-28

How to Cite

Valková, V., Ďúranová, H., Galovičová, L. ., Štefániková, J., Vukovic, N., & Kačániová, M. (2021). The Citrus reticulata essential oil: evaluation of antifungal activity against penicillium species related to bakery products spoilage. Potravinarstvo Slovak Journal of Food Sciences, 15, 1112–1119. https://doi.org/10.5219/1695

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