Determination of antifungal effects of some plant essential oils and their mixtures on brown spot disease caused by Alternaria alternata on mandarin

Year 2024, Volume: 28 Issue: 4, 570 - 583, 15.12.2024

Mehmet Atay , Meltem Avan , Memet İnan

https://doi.org/10.29050/harranziraat.1556160

Abstract

Alternaria alternata, an important phytopathogenic fungus worldwide, is a fungus that causes serious crop losses in many plant species both during cultivation and post-harvest period. This pathogen, which causes brown spot disease on leaves and fruits of different citrus species, produces black or central gray rots on mandarin (Citrus reticulata) fruits. In this study, different doses of mixtures of two thyme species (Thymbra spicata L. and Origanum onites L.) and sage (Salvia officinalis L.) essential oils in single and double combinations were investigated in volatile phase and in vitro conditions for their antifungal effects against A. alternata, isolated from mandarin fruits. In case of single use of oils, T. spicata (4.0 µl petri-1) essential oil showed the highest antifungal effect against fungal isolates at minimum inhibitory concentration (MIC). After using the oils as mixtures, the highest inhibition was determined in the essential oil mixtures of T. vulgaris + O. onites and T. spicata + S. officinalis (8.0 µl petri-1). As a result, the plant essential oils and their mixtures used in the study showed antifungal effects against A. alternata isolate in a dose-dependent manner. Especially considering that mandarin fruits are a product that is stored and preserved, these essential oils obtained from different plants can be easily applied as fumigants in stored product.

Keywords

Synergistic effect, Alternaria alternata, Salvia officinalis L., Origanum onites L., Thynbra spicata L.

Bazı bitki uçucu yağ ve karışımlarının mandarinde Alternaria alternata’nın neden olduğu kahverengi leke hastalığı üzerine olan antifungal etkilerinin belirlenmesi

Abstract

Dünya çapında önemli bir fitopatojen fungus türü olan Alternaria alternata, çok sayıda bitki türünde gerek yetiştiricilik sırasında gerekse hasat sonrası dönemde ciddi ürün kayıplarına neden olan bir fungustur. Farklı turunçgil türlerinin yaprak ve meyvelerinde kahverengi leke hastalığına neden olan bu patojen, mandarin (Citrus reticulata) meyveleri üzerinde siyah veya merkezi gri renkte çürüklükler meydana getirir. Bu çalışmada, iki kekik türü (Thymbra spicata L. ve Origanum onites L.) ve adaçayı (Salvia officinalis L.) uçucu yağlarının tekli ve ikili kombinasyonlar halindeki karışımlarının farklı dozları, buhar fazında ve in vitro şartlarda mandarin meyvesinden izole edilen patojen A. alternata’ya karşı antifungal etkileri araştırılmıştır. Yağların tekli olarak kullanımı durumunda fungal izolata karşı en düşük uygulama dozundaki (MIC) en yüksek antifungal etkiyi T. spicata (4.0 µl petri-1) uçucu yağı göstermiştir. Yağların karışımlar şeklinde kullanılmaları sonrası en yüksek engelleme ise T. spicata + O. onites ve T. spicata + S. officinalis (8.0 µl petri-1) uçucu yağ karışımlarında saptanmıştır. Sonuç olarak, çalışmada kullanılan bitki uçucu yağları ve karışımları doza bağlı bir şekilde A. alternata izolatına karşı antifungal etkiler göstermişlerdir. Özellikle mandarin meyvelerinin depolanarak muhafaza edilebilen bir ürün olduğu göz önünde bulundurulduğunda, farklı bitkilerden elde edilmiş bu uçucu yağların, depolanmış ürünlerde fumigant olarak ümitvar olduğu sonucuna varılmıştır.

Keywords

Sinerjistik etki, Alternaria alternata, Salvia officinalis L., Origanum onites L., Thymbra spicata l.

References

• Abbott, W.S. (1925). A method of computing the effectiveness of an insecticide. Journal of Economic Entomology, 18, 265-267.
• Arlotta, C., Ciacciulli, A., Strano, M.C., Cafaro, V., Salonia, F., Caruso, P., Licciardello C, Russo G, Smith, M.W., & Cuenca, J. (2020.) Disease resistant citrus breeding using newly developed high resolution melting and CAPS protocols for Alternaria brown spot marker assisted selection. Agronomy, 10(9), 1368. https://doi.org/10.3390/agronomy10091368.
• Atay, M., & Soylu, S. (2023). Kurutmalık biber meyvelerinde iç çürüklüğüne neden olan bazı fungal etmenlere karşı bitki uçucu yağlarının in vitro antifungal etkileri. Kahramanmaraş Sütçü İmam Üniversitesi Tarım ve Doğa Dergisi, 26(1), 76-89. https://doi.org/10.18016/ksutarimdoga.vi.1085859.
• Avcı, A.B., & İnan, M. (2020). Comparing of Cultivated Annual and Perennial Calendula officinalis L. Species. Kahramanmaraş Sütçü İmam Üniversitesi Tarım ve Doğa Dergisi, 24(3), 579-585.
• Bassimba, D., Mira, J.L., & Vicent, A. (2014). Inoculum sources, infection periods, and effects of environmental factors on Alternaria brown spot of mandarin in Mediterranean climate conditions. Plant Disease, 98(3), 409-417. https://doi.org/10.1094/PDIS-09-13-0956-RE
• Dang, H.X., Pryor, B., Peever, T., & Lawrence, C.B. (2015). The Alternaria genomes database: a comprehensive resource for a fungal genus comprised of saprophytes, plant pathogens, and allergenic species. BMC Genomics 16(1), 1-9. https://doi.org/10.1186/s12864-015-1430-7
• De-Miguel, M.D., Caballero, P., & Fernández-Zamudio, M.A. (2019). Varietal change dominates adoption of technology in Spanish citrus production. Agronomy, 9(10), 631. https://doi.org/10.3390/agronomy9100631
• Elena, K. (2006). Alternaria brown spot of Minneola in Greece; evaluation of citrus species susceptibility. European Journal of Plant Pathology, 115, 259–262. https://doi.org/10.1007/s10658-006-9005-8
• FAO, (2024). Food and Agriculture Organization of the United Nations Official Website. Citrus fruit production data. http://www.fao.org/faostat/en/#data (Erişim Tarihi: 24.08.2024)
• Felipini, R.B., Brito, R.A.S, Azevedo, F.A., Massola, & Júnior. N.S. (2023). Alternaria alternata f. sp. citri tangerine pathotype induces reactive oxygen species accumulation in susceptible citrus leaves. Physiological and Molecular Plant Pathology, 126, 102040. https://doi.org/10.1016/j.pmpp.2023.102040
• Garganese, F., Schena, L., Siciliano, I., Prigigallo, M.I., Spadaro, D., De Grassi, A., Ippolito, A., & Sanzani, S.M. (2016). Characterization of citrus-associated Alternaria species in Mediterranean areas. PloS One 11(9), e0163255. https://doi.org/10.1371/journal.pone.0163255
• Garganese, F., Ippolito, A., Di Rienzo, V., Lotti, C., Montemurro, C., & Sanzani, S.M. (2018). A new high resolution melting assay for genotyping Alternaria species causing citrus brown spot. Journal of the Science of Food and Agriculture, 98(12), 4578–4583. https://doi.org/10.1002/jsfa.8986
• Garganese, F., Sanzani, S.M., Di Rella, D., Schena, L., & Ippolito, A. (2019). Pre-and postharvest application of alternative means to control Alternaria Brown spot of citrus. Crop Protection, 121, 73–79. https://doi.org/10.1016/j.cropro.2019.03.014.
• Gedikoğlu, A., Sökmen, M., & Çivit, A. (2019). Evaluation of Thymus vulgaris and Thymbra spicata essential oils and plant extracts for chemical composition, antioxidant, and antimicrobial properties. Food science & nutrition, 7(5), 1704-1714.
• Ghooshkhaneh, N.G., Golzarian, M. R., & Mamarabadi, M. (2022). Withdrawn: Spectral pattern study of citrus black rot caused by Alternaria alternata and selecting optimal wavelengths for decay detection. Food Science & Nutrition, 10(6), 1694. https://doi.org/10.1002/fsn3.2739
• Golmohammadi, M., & Rahimian, H., (2004). First report of brown spot caused by Alternaria alternata on tangrine in Iran. In Proceedings of 16th Iranian plant protection congress, (Vol. 28, p. 461). https://doi.org/10.22059/ijpps.2017.233507.1006787
• González-Lamothe, R., Mitchell, G., Gattuso, M., Diarra, M.S., Malouin, F., & Bouarab, K. (2009). Plant antimicrobial agents and their effects on plant and human pathogens. International Journal of Molecular Sciences, 10(8), 3400-3419. https://doi.org/10.3390/ijms10083400
• Grati, Affes., T., Chenenaoui, S., Zemni, H., Hammami, M., Bachkouel, S., Aidi Wannes, W. & Lasram, S. (2022). Biological control of Citrus brown spot pathogen, “Alternaria alternata” by different essential oils. International Journal of Environmental Health Research, 33(8), 823-836. https://doi.org/10.1080/09603123.2022.2055748
• Güney, İ. G., Tekin, F., Günen, T. U., Özer, G., & Derviş, S. (2023). Alternaria alternata causing inner black rot of lemon (Citrus limon) fruits in Turkey: Genetic diversity and characterisation. Physiological and Molecular Plant Pathology, 125, 101998. https://doi.org/10.1016/j.pmpp.2023.101998
• Han, J., Fan, Y., Sun, T., An, J., Ding, Y., Zhang, W., Liu, F., & Wang, C. (2023). Sodium nitroprusside (SNP) treatment increases the postharvest resistance of apple fruit to Alternaria alternata by enhancing antioxidant enzyme activity. Physiological and Molecular Plant Pathology, 129, 102199. https://doi.org/10.1016/j.pmpp.2023.102199
• He, J.Z., Shao, P., Liu, J. H., & Ru, Q.M. (2012). Supercritical carbon dioxide extraction of flavonoids from pomelo (Citrus grandis (L.) Osbeck) peel and their antioxidant activity. International journal of molecular sciences, 13(10), 13065-13078. https://doi.org/10.3390%2Fijms131013065
• Kachur, K., & Suntres, Z. (2020). The Antibacterial Properties of Phenolic Isomers, Carvacrol and Thymol. Critical Reviews in Food Science and Nutrition, 60, 3042-3053. https://doi.org/10.1080/10408398.2019.1675585
• Kara, M., Türkmen, M., & Soylu, S. (2022). Rezene ve defne uçucu yağ karışımlarının kimyasal bileşenlerinin ve Pestalotiopsis funerea’ya karşı antifungal etkinliklerinin belirlenmesi. Kahramanmaraş Sütçü İmam Üniversitesi Tarım ve Doğa Dergisi, 25 (1), 113-126. https://doi.org/10.18016/ksutarimdoga.vi.904966
• Kizil, S., Toncer, O., Diraz, E., & Karaman, S. (2015). Variation of agronom-ical characteristics and essential oil components of Zahter (Thymbra spicata L. var. spicata) populations in semi-arid climatic conditions. Turkish Journal of Field Crops, 20(2), 242–251.
• Kotan, R., Sahin, F., Ala, A. (2005). Identification and pathogenicity of bacteria isolated from pome fruits trees in eastern Anatolia region of Turkey. J. Plant Dis. Prot., 113, 8–13.
• Kotan, R., Cakir, A., Dadasoglu, F., Aydin, T., Cakmakci, R., Ozer, H., ... & Dikbas, N. (2010). Antibacterial activities of essential oils and extracts of Turkish Achillea, Satureja and Thymus species against plant pathogenic bacteria. Journal of the Science of Food and Agriculture, 90(1), 145-160.
• Lee, S.B., Taylor, J.W. (1990). Isolation of DNA from fungal mycelia and single spores. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications, pp 282–287.
• Lucas, G.C., Alves, E., Pereira, R.B., Perina, F.J. & de Souza, R.M. (2012). Antibacterial activity of essential oils on Xanthomonas vesicatoria and control of bacterial spot in tomato. Pesquisa Agropecuária Brasileira, 47, 351-359. http:// dx.doi.org/10.1590/S0100-204X2012000300006
• Morales, H., Marín, S., Ramos, A.J, & Sanchis, V. (2010). Influence of post-harvest technologies applied during cold storage of apples in Penicillium expansum growth and patulin accumulation: a review. Food Control, 21(7), 953-962. https://doi.org/10.1016/j.foodcont.2009.12.016
• Perina, F.J., de Andrade, C.C.L., Moreira, S.I., Nery, E.M., Ogoshi, C., & Alves, E. (2019). Cinnamomun zeylanicum oil and trans-cinnamaldehyde against Alternaria brown spot in tangerine: direct effects and induced resistance. Phytoparasitica, 47, 575-589. https://doi.org/10.1007/s12600-019-00754-x
• Raveau, R., Fontaine, J., & Lounès-Hadj, S.A. (2020). Essential oils as potential alternative biocontrol products against plant pathogens and weeds: a review. Foods, 9(3):365. https://doi.org/10.3390/foods9030365
• Scora, R.W. (1975). On the history and origin of Citrus. Bulletin of the Torrey Botanical Club, (Nov.-Dec. 1975), 369-375.
• Silalahi, J. (2002). Anticancer and health protective properties of citrus fruit components. Asia Pacific journal of clinical nutrition, 11(1), 79-84. https://doi.org/10.1046/j.1440-6047.2002.00271.x
• Soylu, E.M., & Kose, F. (2015). Antifungal activities of essential oils against citrus black rot disease agent Alternaria alternata. Journal of Essential Oil Bearing Plants, 18(4), 894-903. https://doi.org/10.1080/0972060X.2014.895158
• 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, 161, 119-128. https://doi.org/ 10.1007/s11046-005-0206-z
• Tripathi, P., Dubey, N.K. & Shukla, A.K. (2008). Use of Some Essential Oils as Post-Harvest Botanical Fungicides in the management of Grey Mould of Grapes Caused by Botrytis cinerea. World Journal of Microbiology and Biotechnology, 24, 39–46. https://doi.org/10.1007/s11274-007-9435-2
• Türkmen, M. (2015). Farklı Yöntemlerle Elde Edilen Uçucu Yağ Karışımlarının Antifungal Etkinliklerinin Belirlenmesi. Mustafa Kemal Üniversitesi Fen Bilimleri Enstitüsü Tarla Bitkileri Ana Bilim Dalı. Yüksek Lisans Tezi, 55 sayfa.
• Vega, B., & Dewdney, M.M. (2014). QoI-resistance stability in relation to pathogenic and saprophytic fitness components of Alternaria alternata from citrus. Plant Disease, 98(10), 1371-1378. https://doi.org/10.1094/PDIS-01-14-0078-RE
• Vicent, A., Armengol, J., Sales, R., García-Jiménez, J., & Alfaro-Lassala, F. (2000). First report of Alternaria brown spot of citrus in Spain. Plant Disease, 84(9), 1044-1044. https://doi.org/10.1094/PDIS.2000.84.9.1044B
• Villaverde, J.J., Sevilla, Morán. B., Sandín España, P., López-Goti, C., & Alonso Prados, J.L. (2014). Biopesticides in the framework of the European Pesticide Regulation (EC) No. 1107/2009. Pest Management Science, 70(1), 2-5. https://doi.org/10.1002/ps.3663
• Wang, Y., Qian, J., Cao, J., Wang, D., Liu, C., Yang, R., & Sun, C. (2017). Antioxidant capacity, anticancer ability and flavonoids composition of 35 citrus (Citrus reticulata Blanco) varieties. Molecules, 22(7), 1114. https://doi.org/10.3390/molecules22071114.
• White, T.J., Bruns, T, Lee, S.J.W.T., & Taylor, J. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protoc A Guide To Methods Appl 18(1):315–3. Wichtl, (1971). Die pharmakogostich-Chemisehe Analys Band, 12, Franfurt/M.
• Xu, S.X., Yan, F.J., Ni, Z.D., Chen, Q.R., Zhang, H. & Zheng, X.D. (2014). In vitro and in vivo control of Alternaria alternata in cherry tomato by essential oil from Laurus nobilis of Chinese Origin. Journal of the Science of Food and Agriculture 94, 1403-1408. https://doi.org/ 10.1002/jsfa.6428
• Zhang, Y.M., Sun, Y., Xi, W.P., Shen, Y., Qiao, L.P., Zhong, L.Z., Ye, X.Q., & Zhou, Z.Q. (2014). Phenolic compositions and antioxidant capacities of Chinese wild mandarin (Citrus reticulata Blanco) fruits. Food Chemistry, 145, 674-680. https://doi.org/10.1016/j.foodchem.2013.08.012
• Zou, Z, Xi, W.P., Hu, Y., Nie, C., & Zhou, Z.Q. (2016). Antioxidant activity of Citrus fruits. Food Chemistry, 196, 885–896. http://dx.doi.org/10.1016/j.foodchem.2015.09.072
• Zhou, T., Wang, X., Ye, B., Shi, L., Bai, X., & Lai, T. (2018). Effects of essential oil decanal on growth and transcriptome of the postharvest fungal pathogen Penicillium expansum. Postharvest Biology and Technology, 145, 203-212. https://doi.org/10.1016/j.postharvbio.2018.07.015