Biochemical response of Mediterranean flour moth, Ephestia kuehniella Zeller (Lep.: Pyralidae) to the toxicity of trans-anethole

Document Type : Research paper-Persian

Authors

1 PhD graduated, Department of Plant Protection, Faculty of Agricultural Sciences, University of Guilan, Rasht. Iran

2 Associate Professor, Department of Plant Protection, Faculty of Agriculture, University of Zabol, Zabol, Iran

3 Associate Professor, Department of Plant Protection, Faculty of Agricultural Sciences, University of Guilan, Rasht. Iran

Abstract

Background and Objectives
Essential oils are a variety of compounds, and their monoterpenoids, as the main constituents may impair insects' physiological and behavioral functions and could thus be applied in pest management. In addition to causing damage to stored products, the Mediterranean flour moth, Ephestia kuehniella Zeller, 1879 (Lep.: Pyralidae), is actually an easy model to grow in the laboratory and is one of the suitable insects to determine toxicity and in vivo interactions of xenobiotics with physiological systems of insects. In the present study, in order to better understand the mechanism of action of trans-anethole as one of the most important secondary metabolites of the Apiaceae family, the oral toxicity of this compound was evaluated on the activities of digestive and detoxifying enzymes, and metabolites involving in intermediate metabolism of the fourth instar of E. kuehniella.
Materials and Methods
Fourth instar larvae of E. kuehniella were randomly selected and separately exposed to 1 g of the artificial diet containing 1, 2, 4, 8, and 16 μL/g of trans-anethole while the control larvae fed on the diet containing acetone. The bioassay test was performed in 3 replicates with 10 larvae per replication. Mortality was determined after 24 h and LC50 value was calculated by POLO-plus software. Ephestia kuehniella larvae were exposed to the LC50 value of trans-anethole to determine its effects on the enzymatic and non-enzymatic components. After 24 of exposure, the larvae hemolymph, midgut, and fat bodies were extracted. Hemolymph samples were immediately centrifuged at 15000 × g at 4°C for 20 min, while samples of midgut and fat bodies were initially homogenized by a glass pestle and then centrifuged under the same conditions. The hemolymph samples were used to assay the detoxifying enzymes and enzymes of intermediary metabolism, while the midgut samples were used to assess the digestive enzymes. Fat body samples and head capsules were also used for energy reserves.
Results
The LC50 value of trans-anethole against the larvae was 7.03 μL g-1. Significant decrease in the digestive enzyme activities (α-amylase, α and β-glucosidase, lipase) and specific proteases (trypsin, chymotrypsin, elastase, amino and carboxy peptidase) were observed. In contrast, the activity of the detoxifying enzymes (esterases, and glutathione S- transferase) increased in the treated insects. The activities of amino transferases (alanine, aspartate, and gamma-glutamyl) significantly increased in the treated larvae by trans-anethole. Significant decreases in lactate dehydrogenase and phosphatase (acid and alkaline) were observed after treatment. Moreover, the amount of storage macromolecules (total protein, glycogen, and triglyceride) in the treated insects was significantly decreased compared to the control.
Discussion
Our research revealed that trans-anethole is a toxic compound to E. kuehniella by reducing the survival and digestive efficiency of the larvae. Moreover, trans-anethole significantly enhanced the detoxifying enzymes activities. When the larvae were exposed to LC50 of trans-anethole, the digestive activity was reduced due to the cytotoxic effects of trans-anethole on epithelial cells of the larval alimentary canal. Our results demonstrated that trans-anethole might have a promising potential to develop as a safe compound to suppress E. kuehniella population. For the practical use of trans-anethole to control E. kuehniella, it is required to determine the accurate mode of action, and using appropriate formulations to increase its efficacy in long-term applications.

References

Athanassiou, C. G., Rani, P. U., & Kavallieratos, N. G. (2014). The use of plant extracts for stored product protection. Singh, D. (ed.), Advances in Plant Biopesticides. New Delhi, India. pp. 131-148.
Bernfeld, P. (1955). Amylases, α and β. Methods in Enzymology, 1, 149-158. https://doi.org/10.1016/0076-6879(55)01021-5
Bessey, O. A. (1954). A method for a rapid determination of alkaline phosphatase with five cubic millimeters of serum. Journal of Biological Chemistry, 207, 19-23.
Chun, Y., & Yin, Z. D. (1993). Glycogen assay for diagnosis of female genital Chlamydia trachomatis infection. Journal of Clinical Microbiology, 36(4), 1081-1082. https://doi.org/10.1128/JCM.36.4.1081-1082.1998
Cruz, G. S., Wanderley-Teixeira, V., Oliveira, J. V., D’assunçã, C. G., Cunha, F. M., Teixeira, A. A. C., et al. (2017). Effect of trans-anethole, limonene and your combination in nutritional components and their reflection on reproductive parameters and testicular apoptosis in Spodoptera frugiperda (Lepidoptera: Noctuidae). Chemico-Biological Interactions, 63, 74-80. https://doi.org/10.1016/j.cbi.2016.12.013
Dias, M. L., Auad, A. M., Magno, M. C., Resende, T. T., Fonseca, M. G., & Silva, S. E. B. (2019). Insecticidal activity of compounds of plant origin on Mahanarva spectabilis (Hemiptera: Cercopidae). Insects, 10(10), 1-11. https://doi.org/10.3390/insects10100360
Fossati, P., & Prencipe, L. (1982). Serum triglycerides determined colorimetrically with an enzyme that produces hydrogen peroxide. Clinical Chemistry, 28(10), 2077-2080. https://doi.org/10.1093/clinchem/28.10.2077
Fournier, D., Cuany, A., Pralavorio, M., Bride, J. M., & Berge, J. B. (1987). Analysis of methidathion resistance mechanisms in Phytoseiulus persimilis A.H. Pesticide Biochemistry and Physiology, 28, 271-278. https://doi.org/10.1016/0048-3575(87)90025-3
Gallego, F.J., Rodríguez-Gómez, A., Carmen Reche, M., Balanza, V., & Bielza P. (2022). Effect of the amount of Ephestia kuehniella eggs for rearing on development, survival, and reproduction of Orius laevigatus. Insects, 13(250), 1-8. https://doi.org/10.3390/insects13030250
Ghanem, I., Audeh, A., Alnaser, A.A., & Tayoub, G. (2013). Chemical constituents and insecticidal activity of the essential oil from fruits of Foeniculum vulgare Miller on larvae of Khapra beetle (Trogoderma granarium Everts). Herba Polonica, 59(4), 86-96. https://doi.org/10.2478/hepo-2013-0026
Goharrostami, M., & Sendi, J.J. (2018). Investigation on endosymbionts of Mediterranean flour moth gut and studying their role in physiology and biology. Journal of Stored Products Research, 75, 10-17. https://doi.org/10.1016/j.jspr.2017.11.003
Han, Z., Moores, G., Devonshire, A., & Denholm, I. (1998). Association between biochemical marks and insecticide resistance in the Cotton Aphid, Aphis gossypii. Pesticide Biochemistry and Physiology, 62, 164-171. https://doi.org/10.1006/pest.1998.2373
Hemingway, J., & Karunatne, S. H. P. (1998). Mosquito carboxylesterases: A review of the molecular biology and biochemistry of a major insecticide resistance mechanism. Medical and Veterinary Entomology, 12(1), 1-12. https://doi.org/10.1046/j.1365-2915.1998. 00082.x 
Isman, M. B. (2006). Botanical insecticides, deterrents and repellents in modern agriculture and an increasingly regulated world. Annual Review of Entomology, 51, 45-66. https://doi.org/10.1146/annurev.ento.51.110104.151146
Isman, M.B. (2020). Botanical insecticides in the twenty-first century-fulfilling their promise?. Annual Review of Entomology, 65, 233-249. https://doi.org/10.1146/annurev-ento-011019-025010
 Kim, S.W., Kang, J., & Park, I.K. (2013). Fumigant toxicity of Apiaceae essential oils and their constituents against Sitophilus oryzae and their acetylcholinesterase inhibitory activity. Journal of Asia Pacific Entomology, 16, 443-447. https://doi.org/10.1016/j.indcrop.2014.09.052
King, J. (1965). The dehydrogenases or oxidoreductases. Lactate dehydrogenase, In King, J. (Ed.). Practical clinical enzymology. London: Van Nostrand, pp. 83-93.
Klowden, M. J. (2007). Physiological systems in insects. Second edition, Academic Press, USA.
Kumrungsee, N., Pluempanupat, W., Koul, O., & Bullangpoti, V. (2014). Toxicity of essential oil compounds against diamondback moth, Plutella xylostella, and their impact on detoxification enzyme activities. Journal of Pest Science, 87(4), 721-729. https://doi.org/10.1007/s10340-014-0602-6
Li, X. C., Schuler, M. A., & Berenbaum, M. R. (2007). Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annual Review of Entomology, 52, 231-253. https://doi.org/10.1146/annurev.ento.51.110104.151104
Lima, F. M., Favero, S., & Lima, J. O. G. (2001). Production of the Mediterranean flour moth, Anagasta kuehniella (Zeller) (Lepidoptera: Pyralidae), on an artificial diet containing corn meal. Neotropical Entomology, 30(1), 37-42. https://doi.org/10.1590/S1519-566X2001000100007
Lowry, O. H., Rosebrough, N. J., Farr, A. L., & Randall, R. J. (1951). Protein measurement with the Folin phenol reagent. Journal of Biological Chemistry, 193(1), 265-75. https://doi.org/10.1016/S0021-9258(19)52451-6
Nation, J. L. (2008). Insect physiology and biochemistry. 2nd edition. CRC Press, New York.
Oppenoorth, F.J., Van der Pas, L., & Houx, N. (1979). Glutathione S-transferase and hydrolytic activity in a tetrachlorvinphos-resistant strain of housefly and their influence on resistance. Pesticide Biochemistry and Physiology, 11, 176-178. https://doi.org/10.1016/0048-3575(79)90057-9
Oppert, B., Kramer, K.J., & McGaughey, W.H. (1997). Rapid microplate assay of proteinase mixtures. Biotechnology, 23(1), 70-72.
Pascual-Villalobos, M. J., Cantó-Tejero, M., Guirao, P., & López, M. D. (2020). Fumigant toxicity in Myzus persicae Sulzer (Hemiptera: Aphididae): Controlled release of (E)-anethole from microspheres. Plants, 9(1), 1-11.  https://doi.org/10.3390/plants9010124
Pavela, R., Maggi, F., Cianfaglione, K., Bruno, M., & Benelli, G. (2018). Larvicidal activity of essential oils of five Apiaceae taxa and some of their main constituents against Culex quinquefasciatus. Chemistry and Biodiversity, 15(1), 1-12. https://doi.org/10.1002/cbdv.201700382
Rajaei, A., Yazdanian, M., & Asadeh, Gh. (2021). Lethal and sublethal effects of low temperature, alone and in combination with eucalyptus essential oil, against adult Mediterranean flour moth, Ephestia kuehniella. Plant Protection (Scientific Journal of Agriculture), 43(4): 91-109. https://doi.org/10.22055/PPR.2021.16769
Rajendran, S., & Sriranjini, V. (2008). Plant products as fumigants for stored-product insect control. Journal of Stored Products Research, 44(2), 126-135. https://doi.org/10.1016/j.jspr.2007.08.003
Ramzi, S., Sahragard, A., & Zibaee, A. (2014). Effects of Citrullus colocynthis agglutinin on intermediary metabolism of Ectomyelois ceratoniae Zeller (Lepidoptera: Pyralidae). Journal of Asia-Pacific Entomology, 17(3), 273-279. https://doi.org/10.1016/j.aspen.2014.01.005
Ramzi, S., Seraji, A., Gonbad, R.A. & Haghighat, S. (2022). Effects of the extract and the essential oil of Allium sativum on tea mealy bug, Pseudococcus viburni Sigornet (Hemiptera: Pseudococcidae). Biocatalysis and Agricultural Biotechnology, 42,102359. https://doi.org/10.1016/j.bcab.2022.102359
Rosa, J.S., Oliveira, L., Sousa, R.M.O.F., Escobar, C.B., & Fernandes-Ferreira, M. (2020). Bioactivity of some Apiaceae essential oils and their constituents against Sitophilus zeamais (Coleoptera: Curculionidae). Bulletin of Entomological Research, 110(3), 406-416. https://doi.org/10.1017/S0007485319000774
Scott, I. M., Jensen, H., Scott, J. G., Isman, M. B., Arnason, J. T., & Philogène, B. J. R. (2003). Botanical insecticides for controlling agricultural pests: Piperamides and the Colorado potato beetle Leptinotarsa decemlineata Say (Coleoptera: Chrysomelidae). Archives of Insect Biochemistry and Physiology, 54(4), 212-225. https://doi.org/10.1002/arch.10118
Senthil-Nathan, S. (2006). Effects of Melia azedarach on nutritional physiology and enzyme activities of the rice leaf folder Cnaphalocrocis medinalis (Guenée) (Lepidoptera: Pyralidae). Pesticide Biochemistry and Physiology, 84, 98-108. https://doi.org/10.1016/j.pestbp.2005.05.006
Shahriari, M., & Sahebzadeh, N. (2017). Effect of diallyl disulfide on physiological performance of Ephestia kuehniella Zeller (Lepidoptera: Pyralidae). Archive of Phytopathology and Plant Protection, 50(1) 33-46. https://doi.org/10.1080/03235408.2016.1253252
Shahriari, M., Sahebzadeh, N., & Zibaee, A. (2017a). Metabolic response of Ephestia kuehniella Zeller (Lepidoptera: Pyralidae) to essential oil of Ajwain and thymol. Toxin Reviews, 36(3), 204-209. https://doi.org/10.1080/15569543.2017.1294605
Shahriari, M., Sahebzadeh, N., & Zibaee, A. (2017b). Effect of Teucrium polium (Lamiaceae) essential oil on digestive enzyme activities and energy reserves of Ephestia kuehniella (Lepidoptera: Pyralidae). Invertebrate Survival Journal, 14(1), 182-189. https://doi.org/10.25431/1824-307X/isj.v14i1.182-189
Shahriari, M., Sahebzadeh, N., Sarabandi, M., & Zibaee, A. (2016). Oral toxicity of thymol, α-Pinene, Diallyl Disulfide and Trans-Anethole, and Their Binary Mixtures against Tribolium castaneum Herbst larvae (Coleoptera: Tenebrionidae). Jordan Journal of Biological Sciences, 9(4), 213-219.
Shahriari, M., Zibaee, A., Sahebzadeh, N., & Shamakhi, L. (2018). Effects of α-pinene, trans-anethole, and thymol as the essential oil constituents on antioxidant system and acetylcholine esterase of Ephestia kuehniella Zeller (Lepidoptera: Pyralidae). Pesticide Biochemistry and Physiology, 150, 40-47. https://doi.org/10.1016/j.pestbp.2018.06.015
Silva, C. P., & Terra, W. R. M. (1995). An α-glucosidase from perimicrovillar membranes of Dysdercus peruvianus (Hemiptera: Pyrrhocoridae) midgut cells: Purification and properties. Insect Biochemistry and Molecular Biology, 25(4), 487-494. https://doi.org/10.1016/0965-1748(94)00088-G
Sousa, R.M.O., Rosa, J.S., Oliveira, L., Cunha, A., & Fernandes-Ferreira, M. (2015). Activities of Apiaceae essential oils and volatile compounds on hatchability, development, reproduction and nutrition of Pseudaletia unipuncta (Lepidoptera: Noctuidae). Industrial Crops and Products, 63, 226-237. https://doi.org/10.1016/j.indcrop.2014.09.052
Szasz, G. (1976). Reaction-rate method for gamma-glutamyltransferase activity in serum. Clinical Chemistry, 22(12), 2051-2055.
Talepour, F., Zibaee, A., Seyahooei, M.A., & Sendi, J.J. (2021). Toxicity and physiological effects of diallyl sulfide and dialyl disulfide on Tuta absoluta Meyrick. Physiological and Molecular Plant Pathology, 116, 101741. https://doi.org/10.1016/j.pmpp.2021.101741
Tavakoli, B., & Ajam Hosni, M. (2018). Effect of palizin, diflubenzuron, chlorpyrifos, deltamethrin and hexaflumuron on bio- demographic characteristic and feeding index of Flour moth, Anagasta kuehniella, (Lep: Pyralidae). Journal of Applied Plant Protection, 6(1), 25-33.
Thomas, L. (1998). Clinical laboratory diagnostic. first ed., TH Books Verlasgesellschaft, Frankfurt.
Tsujita, T., Ninomiya, H., & Okuda, H. (1989). p-nitrophenyl butyrate hydrolyzing activity of hormone-sensitive lipase from bovine adipose tissue. Journal of Lipid Research, 30(7), 997-1004. https://doi.org/10.1016/S0022-2275(20)38302-4
Xavier, V. M., Message, D., Picanco, M. C., Chediak, M., Santana Junior, P. A., Ramos, R. S., et al. (2015). Acute toxicity and sublethal effects of botanical insecticides to honeybees. Journal of Insect Sciences, 15(1), 1-6. https://doi.org/10.1093/jisesa/iev110
Yazdani, E., Sendi, J.J., Aliakbar, A., & Senthil-Nathan, S. (2013). Effect of Lavandula angustifolia essential oil against lesser mulberry pyralid Glyphodes pyloalis Walker (Lep: Pyralidae) and identification of its major derivatives. Pesticide Biochemistry and Physiology, 107(2), 250-257. https://doi.org/10.1016/j.pestbp.2013.08.002
Zhu, Y.C., Guo, Z., Chen, M.S., Zhu, K.Y., Liu, X.F., & Scheffler, B. (2011). Major putative pesticide receptors, detoxification enzymes, and transcriptional profile of the midgut of the tobacco budworm, Heliothis virescens (Lepidoptera: Noctuidae). Journal of Invertebrate Pathology, 106(2), 296-307. https://doi.org/10.1016/j.jip.2010.10.007
Zibaee, A., & Bandani, A. R. (2010). Effects of Artemisia annua L. (Asteracea) on digestive enzymes profiles and cellular immune reactions of sun pest, Eurygaster integriceps (Heteroptera: Scutellaridae), against Beauvaria bassiana. Bulletin of Entomological Research, 100, 185-196.
 © 2022 by the authors. Licensee SCU, Ahvaz, Iran. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution-NonCommercial 4.0 International (CC BY-NC 4.0 license) (http://creativecommons.org/licenses/by-nc/4.0/
Plant Protection (Scientific Journal of Agriculture)
Volume 45, Issue 2
July 2022
Pages 121-136

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