Insecticidal and antifungal effects of lemon, orange, and grapefruit peel essential oils from Argentina
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Abstract
The aim of the present work was to study the bioactivity of lemon, orange, and grapefruit peel essential oils (EOs) obtained from Argentinian plantations on different agronomically important insect and fungal species. The chemical profile of EOs was determined by Gas Chromatography-Mass Spectrometry (GC/MS); the insecticidal activity was studied through contact and fumigant assays; the antifungal activity was evaluated with fumigant tests. Orange EO was the most effective against Rhyzopertha dominica, Oryzaephilus spp. and Sitophilus granarius in fumigation tests (LC50= 89.39, 94.50, and 163.64 µL/L air, respectively); while the insecticidal effect of EOs was species-dependent in contact toxicity assays. Regarding antifungal activity, Rhizoctonia solanii was more susceptible than Sclerotium rolfsii to the tested EOs, with lemon from Industry 1 and orange being the most toxic EOs (MIC=10.77 µL/plate and 11.02 µL/plate, respectively). Conversely, S. rolfsii was strongly inhibited by lemon EO from Industry 2 (MIC= 52.40 µL/plate). Besides limonene, other compounds that could be responsible for these bioactivities were: linalool, carvone, α-pinene, β-pinene, β-myrcene, α-terpineol, terpinen-4-ol, limonene oxide, β-phellandrene, γ-terpinene, sabinene, neral, neryl acetate, β-caryophyllene and p-cymene. Citrus peel EOs can be used against different pests, contributing to the valorization of citrus residues.
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Abdelgaleil, S. A. M., Mohamed, M. I. E., Badawy, M. E. I. and El-Arami, S. A. A. (2009). Fumigant and Contact Toxicities of Monoterpenes to Sitophilus oryzae (L.) and Tribolium castaneum (Herbst) and their Inhibitory Effects on Acetylcholinesterase Activity. Journal of Chemical Ecology, 35(5), 518–525. https://doi.org/10.1007/s10886-009-9635-3
Achimón, F., Brito, V. D., Pizzolitto, R. P., Ramirez Sanchez, A., Gómez, E. A. and Zygadlo, J. A. (2021). Chemical composition and antifungal properties of commercial essential oils against the maize phytopathogenic fungus Fusarium verticillioides. Revista Argentina de Microbiologia, 53(4), 292–303. https://doi.org/10.1016/j.ram.2020.12.001
Achimón, F., Dambolena, J. S., Zygadlo, J. A. and Pizzolitto, R. P. (2019). Carbon sources as factors affecting the secondary metabolism of the maize pathogen Fusarium verticillioides. LWT, 115, 108470. https://doi.org/10.1016/j.lwt.2019.108470
Achimón, F., Krapacher, C. R., Jacquat, A. G., Pizzolitto, R. P. and Zygadlo, J. A. (2021). Carbon sources to enhance the biosynthesis of useful secondary metabolites in Fusarium verticillioides submerged cultures. World Journal of Microbiology and Biotechnology, 37, 78. https://doi.org/10.1007/s11274-021-03044-z
Alarcón, R., Ocampos, S., Pacciaroni, A. and Sosa, V. (2012). Chemical Composition, Antifungal and Herbicidal Effects of Essential Oil Isolated from Chersodoma argentina (Asteraceae). Natural Product Communications, 7(1), 125–128. https://doi.org/10.1177/1934578X1200700140
Arena, J. S., Merlo, C., Defagó, M. T. and Zygadlo, J. A. (2020). Insecticidal and antibacterial effects of some essential oils against the poultry pest Alphitobius diaperinus and its associated microorganisms. Journal of Pest Science, 93, 403–414. https://doi.org/10.1007/s10340-019-01141-5
Bravim dos Santos, A. T., Zanuncio Junior, J. S., Parreira Alves, L., Pedra de Abreu, K. M., de Oliveira Bernardes, C., de Carvalho, J. R. and
Menini, L. (2021). Chemical identification and insecticidal effect of Tephrosia vogelii essential oil against Cerosipha forbesi in strawberry crop. Crop Protection, 139, 105405. https://doi.org/10.1016/j.cropro.2020.105405
Brito, V. D., Achimón, F., Dambolena, J. S., Pizzolitto, R. P. and Zygadlo, J. A. (2019). Trans-2-hexen-1-ol as a tool for the control of Fusarium verticillioides in stored maize grains. Journal of Stored Products Research, 82, 123–130. https://doi.org/10.1016/j.jspr.2019.05.002
Brito, V. D., Achimón, F., Pizzolitto, R. P., Ramírez Sánchez, A., Gómez Torres, E. A., Zygadlo, J. A. and Zunino, M. P. (2021). An alternative to reduce the use of the synthetic insecticide against the maize weevil Sitophilus zeamais through the synergistic action of Pimenta racemosa and Citrus sinensis essential oils with chlorpyrifos. Journal of Pest Science, 94(2), 409-421. https://doi.org/10.1007/s10340-020-01264-0
Chavan, P., Singh, A. K. and Kaur, G. (2018). Recent progress in the utilization of industrial waste and by-products of citrus fruits: A review. Journal of Food Process Engineering, 41(8), e12895. https://doi.org/10.1111/jfpe.12895
da Silva, A. C. R., Monteiro Lopes, P., Barros de Azevedo, M. M., Machado Costa, D. C., Sales Alviano, C. and Sales Alviano, D. (2012). Biological Activities of α-Pinene and β-Pinene Enantiomers. Molecules, 17(6), 6305–6316. https://doi.org/10.3390/molecules17066305
de Macêdo Andrade, A. C., Rosalen, P. L., Freires, I. A., Scotti, L., Scotti, M. T., Aquino, S. G. and de Castro, R. D. (2018). Antifungal Activity, Mode of Action, Docking Prediction and Anti-biofilm Effects of (+)-β-pinene Enantiomers against Candida spp. Current Topics in Medicinal Chemistry, 18(29), 2481–2490. https://doi.org/10.2174/1568026618666181115103104
Di Rienzo J. A., Casanoves F., Balzarini M. G., González L., Tablada M. and Robledo C. W. InfoStat (versión 2017) [Software]. Córdoba, Argentina: Grupo InfoStat, FCA, Universidad Nacional de Córdoba. http://www.infostat.com.ar
Dosoky, N. S. and Setzer, W. N. (2018). Biological Activities and Safety of Citrus spp. Essential Oils. International Journal of Molecular Sciences, 19(7), 1966. https://doi.org/10.3390/ijms19071966
Dutta, S., Kundu, A., Saha, S., Prabhakaran, P. and Mandal, A. (2020). Characterization, antifungal properties and in silico modelling perspectives of Trachyspermum ammi essential oil. LWT, 131, 109786. https://doi.org/10.1016/j.lwt.2020.109786
Espinosa-García, F. J. and Langenheim, J. H. (1991). Effects of sabinene and γ-terpinene from coastal redwood leaves acting singly or in mixtures on the growth of some of their fungus endophytes. Biochemical Systematics and Ecology, 19(8), 643–650. https://doi.org/10.1016/0305-1978(91)90080-J
Feng, J., Wang, R., Chen, Z., Zhang, S., Yuan, S., Cao, H., Jafari, S. M. and Yang, W. (2020). Formulation optimization of D-limonene-loaded nanoemulsions as a natural and efficient biopesticide. Colloids and Surfaces A: Physicochemical and Engineering Aspects, 596, 124746. https://doi.org/10.1016/j.colsurfa.2020.124746
Finney, D. J. (1971). Probit analysis (3rd ed.). Cambridge University Press.
Herrera, J. M., Zunino, M. P., Dambolena, J. S., Pizzolitto, R. P., Gañan, N. A., Lucini, E. I. and Zygadlo, J. A. (2015). Terpene ketones as natural insecticides against Sitophilus zeamais. Industrial Crops and Products, 70, 435–442. https://doi.org/10.1016/j.indcrop.2015.03.074
Jing, L., Lei, Z., Li, L., Xie, R., Xi, W., Guan, Y., Sumner, L. W. and Zhou, Z. (2014). Antifungal activity of citrus essential oils. Journal of Agricultural and Food Chemistry, 62(14), 3011–3033. https://doi.org/10.1021/jf5006148
Justino, J., Rauter, A. P., Canda, T., Wilkins, R. and Matthews, E. (2005). Sugar derivatives containing oxiranes and α,β-unsaturated γ-lactones as potential environmentally friendly insecticides. Pest Management Science, 61(10), 985–990. https://doi.org/10.1002/ps.1064
Kordali, Ş., Aslan, I., Çalmaşur, O. and Çakir, A. (2006). Toxicity of essential oils isolated from three Artemisia species and some of their major components to granary weevil, Sitophilus granarius (L.) (Coleoptera: Curculionidae). Industrial Crops and Products, 23(2), 162–170. https://doi.org/10.1016/j.indcrop.2005.05.005
Kordali, Ş., Kotan, R. and Çakir, A. (2007). Screening of antifungal activities of 21 oxygenated monoterpenes in-vitro as plant disease control agents. Allelopathy Journal, 19(2), 373–392. http://supersol.com.tr/Files/FUNGUSIT/2007_21oxygenated.pdf
Kordali, Ş., Usanmaz, A., Bayrak, N. and Çakır, A. (2017). Fumigation of Volatile Monoterpenes and Aromatic Compounds Against Adults of Sitophilus granarius (L.) (Coleoptera: Curculionidae). Records of Natural Products, 11(4), 362–373. https://www.acgpubs.org/doc/2018080514551846-RNP-1701-020.pdf
Liu, T. T., Chao, L. K. P., Hong, K. S., Huang, Y. J. and Yang, T. S. (2020). Composition and Insecticidal Activity of Essential Oil of Bacopa caroliniana and Interactive Effects of Individual Compounds on the Activity. Insects, 11(1), 23. https://doi.org/10.3390/insects11010023
López, M. D., Contreras, J. and Pascual-Villalobos, M. J. (2010). Selection for tolerance to volatile monoterpenoids in Sitophilus oryzae (L.), Rhyzopertha dominica (F.) and Cryptolestes pusillus (Schönherr). Journal of Stored Products Research, 46(1), 52–58. https://doi.org/10.1016/j.jspr.2009.09.003
Ložienė, K., Švedienė, J., Paškevičius, A., Raudonienė, V., Sytar, O. and Kosyan, A. (2018). Influence of plant origin natural α-pinene with different enantiomeric composition on bacteria, yeasts and fungi. Fitoterapia, 127, 20–24. https://doi.org/10.1016/j.fitote.2018.04.013
Marei, G. I. K., Abdel Rasoul, M. A. and Abdelgaleil, S. A. M. (2012). Comparative antifungal activities and biochemical effects of monoterpenes on plant pathogenic fungi. Pesticide Biochemistry and Physiology, 103(1), 56–61. https://doi.org/10.1016/j.pestbp.2012.03.004
Margni, M., Rossier, D., Crettaz, P. and Jolliet, O. (2002). Life cycle impact assessment of pesticides on human health and ecosystems. Agriculture, Ecosystems and Environment, 93(1–3), 379–392. https://doi.org/10.1016/S0167-8809(01)00336-X
Nguyen, H., Campi, E. M., Jackson, W. R. and Patti, A. F. (2009). Effect of oxidative deterioration on flavour and aroma components of lemon oil. Food Chemistry, 112(2), 388–393. https://doi.org/10.1016/j.foodchem.2008.05.090
Oboh, G., Ademosun, A. O., Olumuyiwa, T. A., Olasehinde, T. A., Ademiluyi, A. O. and Adeyemo, A. C. (2017). Insecticidal activity of essential oil from orange peels (Citrus sinensis) against Tribolium confusum, Callosobruchus maculatus and Sitophilus oryzae and its inhibitory effects on acetylcholinesterase and Na+/K+-ATPase activities. Phytoparasitica, 45(4), 501–508. https://doi.org/10.1007/s12600-017-0620-z
Park, M. J., Gwak, K. S., Yang, I., Kim, K. W., Jeung, E. B., Chang, J. W. and Choi, I. G. (2009). Effect of citral, eugenol, nerolidol and α-terpineol on the ultrastructural changes of Trichophyton mentagrophytes. Fitoterapia, 80(5), 290–296. https://doi.org/10.1016/j.fitote.2009.03.007
Pavela, R. (2014). Acute, synergistic and antagonistic effects of some aromatic compounds on the Spodoptera littoralis Boisd. (Lep., Noctuidae) larvae. Industrial Crops and Products, 60, 247–258. https://doi.org/10.1016/j.indcrop.2014.06.030
Plata-Rueda, A., Campos, J. M., da Silva Rolim, G., Martínez, L. C., Dos Santos, M. H., Fernandes, F. L., Serrão, J. E. and Zanuncio, J. C. (2018). Terpenoid constituents of cinnamon and clove essential oils cause toxic effects and behavior repellency response on granary weevil, Sitophilus granarius. Ecotoxicology and Environmental Safety, 156, 263–270. https://doi.org/10.1016/j.ecoenv.2018.03.033
Praveena, A. and Sanjayan, K. P. (2011). Inhibition of Acetylcholinesterase in three insects of economic importance by linalool, a monoterpene phytochemical. Insect Pest Management, A Current Scenario, 240–345. https://www.researchgate.net/profile/Purushothaman-Sanjayan/publication/235898957_INHIBITION_OF_ACETYLCHOLINESTERASE_IN_THREE_INSECTS_OF_ECONOMIC_IMPORTANCE_BY_LINALOOL_A_MONOTERPENE_PHYTOCHEMICAL/links/00463513f15719df05000000/INHIBITION-OF-ACETYLCHOLINESTERASE-IN-THREE-INSECTS-OF-ECONOMIC-IMPORTANCE-BY-LINALOOL-A-MONOTERPENE-PHYTOCHEMICAL.pdf
Rahimmalek, M., Heidari, E. F., Ehtemam, M. H. and Mohammadi, S. (2017). Essential oil variation in Iranian Ajowan (Trachyspermum ammi (L.) Sprague) populations collected from different geographical regions in relation to climatic factors. Industrial Crops and Products, 95, 591–598. https://doi.org/10.1016/j.indcrop.2016.11.017
Rozman, V., Kalinovic, I. and Korunic, Z. (2007). Toxicity of naturally occurring compounds of Lamiaceae and Lauraceae to three stored-product insects. Journal of Stored Products Research, 43(4), 349–355. https://doi.org/10.1016/j.jspr.2006.09.001
Salazar, M. O., Pisano, P. L., González Sierra, M. and Furlan, R. L. E. (2018). NMR and multivariate data analysis to assess traceability of argentine citrus. Microchemical Journal, 141, 264–270. https://doi.org/10.1016/j.microc.2018.05.037
Satari, B. and Karimi, K. (2018). Citrus processing wastes: Environmental impacts, recent advances, and future perspectives in total valorization. Resources, Conservation and Recycling, 129, 153–167. https://doi.org/10.1016/j.resconrec.2017.10.032
Simas, D. L. R., de Amorim, S. H. B. M., Goulart, F. R. V., Alviano, C. S., Alviano, D. S., and da Silva, A. J. R. (2017). Citrus species essential oils and their components can inhibit or stimulate fungal growth in fruit. Industrial Crops and Products, 98, 108–115. https://doi.org/10.1016/j.indcrop.2017.01.026
Singh, B., Singh, J. P., Kaur, A. and Yadav, M. P. (2021). Insights into the chemical composition and bioactivities of citrus peel essential oils. Food Research International, 143, 110231. https://doi.org/10.1016/j.foodres.2021.110231
Stein, S., Mirokhin, Y., Tchekhovskoi D. and Mallard, G. (2008). The NIST Mass Spectral Program for the NIST/EPA/NIH Mass Spectral Library (version 2.0) [Software]. United States of America. https://www.nist.gov/
Sun, J., Feng, Y., Wang, Y., Li, J., Zou, K., Liu, H., Hu, Y., Xue, Y., Yang, L., Du, S. and Wu, Y. (2020). Investigation of Pesticidal Effects of Peucedanum terebinthinaceum Essential Oil on Three Stored-Product Insects. Records of Natural Products, 14(3), 177–189. http://doi.org/10.25135/rnp.149.19.05.1287
Tripathi, A. K., Prajapati, V. and Kumar, S. (2003). Bioactivities of l-Carvone, d-Carvone, and Dihydrocarvone Toward Three Stored Product Beetles. Journal of Economic Entomology, 96(5), 1594–1601. https://doi.org/10.1093/jee/96.5.1594
Velázquez-Nuñez, M. J., Avila-Sosa, R., Palou, E. and López-Malo, A. (2013). Antifungal activity of orange (Citrus sinensis var. valencia) peel essential oil applied by direct addition or vapor contact. Food Control, 31(1), 1–4. https://doi.org/10.1016/j.foodcont.2012.09.029
Vilela, G. R., de Almeida, G. S., D’Arce, M. A. B. R., Moraes, M. H. D., Brito, J. O., da Silva, M. F. das G. F., Silva, S. C., de Stefano Piedade, S. M., Calori-Domingues, M. A. and da Gloria, E. M. (2009). Activity of essential oil and its major compound, 1,8-cineole, from Eucalyptus globulus Labill., against the storage fungi Aspergillus flavus Link and Aspergillus parasiticus Speare. Journal of Stored Products Research, 45(2), 108–111. https://doi.org/10.1016/j.jspr.2008.10.006
Wang, C. F., Yang, K., Zhang, H. M., Cao, J., Fang, R., Liu, Z. L., Du, S. S., Wang, Y. Y., Deng, Z. W. and Zhou, L. (2011). Components and Insecticidal Activity against the Maize Weevils of Zanthoxylum schinifolium fruits and leaves. Molecules, 16(4), 3077–3088. https://doi.org/10.3390/molecules16043077
Wuryatmo, E., Klieber, A. and Scott, E. S. (2003). Inhibition of Citrus Postharvest Pathogens by Vapor of Citral and Related Compounds in Culture. Journal of Agricultural and Food Chemistry, 51(9), 2637–2640. https://doi.org/10.1021/jf026183l
Yildirim, E., Emsen, B. and Kordali, S. (2013). Insecticidal Effects of Monoterpenes on Sitophilus zeamais Motschulsky (Coleoptera: Curculionidae). Journal of Applied Botany and Food Quality, 86, 198–204. https://doi.org/10.5073/JABFQ.2013.086.027
Zema, D. A., Calabrò, P. S., Folino, A., Tamburino, V., Zappia, G. and Zimbone, S. M. (2018). Valorisation of citrus processing waste: A review. Waste Management, 80, 252–273. https://doi.org/10.1016/j.wasman.2018.09.024