Anticholinesterase Potential of Monoterpenoids on the Whitefly Bemisia tabaci and Their Kinetic Studies

Authors
K. Zarred 1
A. Laarif 2
A. Ben Hamouda 2
I. Chaieb 3
J. Mediouni-Ben Jemaa 4
1 Institut Supérieur Agronomique of Chott Mariem (ISA), University of Sousse, Tunisia.
2 UR13AGR09, Regional Center for Research in Horticulture and Biological Agriculture (CRRHAB), University of Sousse, Tunisia.
3 Laboratory of Plant Protection, National Institute of Agronomic Research of Tunisia (INRAT), University of Carthage, Tunisia.
4 Laboratory of Biotechnology Applied to Agriculture, National Institute of Agronomic Research of Tunisia (INRAT), Tunisia.
Abstract
B-biotype Bemisia tabaci is a severe insect pest worldwide in many ornamental, agricultural, and horticultural crops. Control of this insect is obstructed by resistance to many AcetylCholinEsterase (AChE)-inhibiting insecticides, such as organophosphates and carbamates. In the present work, we evaluated the acetylcholinesterase inhibitory activity of six monoterpenoids namely α-pinene, terpineol, linalool, ß-myrcene, nerol and geraniol in vitro and in vivo. Inhibition of AChE of B. tabaci was measured by colorimetric method. The results showed that all of the monoterpenoids produced AChE inhibitory activity, with IC50 values ranging from 0.96 to 26.85 mM. Alpha-pinene showed the most potent inhibitory activity (IC50= 0.96 mM). Kinetic analysis showed reversible non-competitive type inhibition, revealing that these components might bind both the enzyme alone and the enzyme-substrate. Results demonstrate the AChE inhibitory activity as mode of action of these monoterpenoids at relatively high concentrations. Thus, this could be useful for investigation of new ecofriendly natural insecticidal compounds.

Keywords

1. 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. J. Chem. Ecol., 35: 518-525.
2. Alzogaray, R. A., Sfara, V., Moretti, A. N. and Zerba E. N. 2013. Behavioural and Toxicological Responses of Blattella germanica (Dictyoptera: Blattellidae) to Monoterpenes. Eur. J. Entomol., 2: 247-252.
3. Benner, J. P. 1993. Pesticidal Compounds from Higher Plants. Pestic. Sci., 39: 95-102.
4. Bhadra, S., Mukherjee, P. K., Kumar, N. S. and Bandyopadhyay, A. 2011. Anticholinesterase Activity of Standardized Extract of Illicium verum Hook. f. Fruits, Fitoterapia, 82: 342–346.
5. Byrne, F. J. and Devonshire, A. L. 1997. Kinetics of Insensitive Acetylcholinesterases in Organophosphate- Resistant Tobacco Whitefly, Bemisia tabaci (Gennadius) (Homoptera: Aleyrodidae). Pest Biochem. Physiol., 58: 119–124.
6. Chaubey, M. K. 2011. Fumigant Toxicity of Essential Oils against Rice Weevil Sitophilus oryzae L. (Coleoptera: Curculionidae). J. Biol. Sci. 11: 411-416.
7. Chermiti, B., Braham, M., Cenis, J. L., Alonso, C. and Beitia, F. 1997. Sur la Présence en Tunisie des Biotypes “B” et non B” de Bemisia tabaci (Homoptera : Aleyrodidae) et de leurs Parasitoïdes Associés. Bull. OILB/SROP., 20: 108-113.
8. Dohi, S., Terasaki, M. and Makino, M. 2009. Acetylcholinesterase Inhibitory Activity and Chemical Composition of Commercial Essential Oils. J. Agric. Food Chem., 57: 4313-4318.
9. Dvir, H., Silman, I., Harel, M., Rosenberry, T. L. and Sussman, J. L. 2010. Acetylcholinesterase: From 3D Structure to Function. Chem. Biol. Interact., 187: 10- 22.
10. Ellman, G. L., Courtney, K. D., Valentino, A. J. and Feathertone, R. M. 1961. A New and Rapid Colorimetric Determination of Acetylcholinesterase Activity. Biochem. Pharmacol., 7: 88–95.
11. Finney, D. L. 1971. Probit Analysis. 3rd Edition, Cambridge University Press, UK, 125 PP.
12. Gallardo, A., Picollo, M. I. and Mougabure-Cueto, G. 2015. Lethal Activity of Individual and Mixed Monoterpenoids of Geranium Essential Oil on Musa Domestica. Parasitol. Res., 114: 229-1232.
13. Gonzalez-Zamora, J. E. and Moreno, R. 2011. Model Selection and Averaging in the Estimation of Population Parameters of Bemisia tabaci (Gennadius) from Stage Frequency Data in Sweet Pepper Plants. J. Pest Sci., 84: 165–177.
14. Isman, M. B., Wan, A. J. and Passreiter, C. M. 2001. Insecticidal Activity of Essential Oils to the Tobacco Cutworm, Spodoptera litura. Fitoterapia, 72: 65-8.
15. Isman, M. B. 2000. Plant Essential Oils for Pest and Disease Management. Crop Prot., 19: 603-608.
16. Jukic, M., Politeo, O., Maksimovic, M., Milos, M. and Milos, M. 2007. In Vitro Acetylcholinesterase Inhibitory Properties of Thymol, Carvacrol and Their Derivatives Thymoquinone and Thymohydroquinone. Phytother. Res., 21: 259–261.
17. Kim, S. W., Kang, J. and Park, I. K. 2013. Fumigant Toxicity of Apiaceae Essential Oils and Their Constituents against Sitophilus oryzae and Their Acetylcholinesterase Inhibitory Activity. J. Asia Pac. Entomol., 16: 443-448.
18. Kostyukovsky, M., Rafaeli, A., Gileadi, C., Demchenko, N. and Shaaya, E. 2002. Activation of Octopaminergic Receptors by Essential Oil Constituents Isolated from Aromatic Plants: Possible Mode of Action against Insect Pests. Pest Manag. Sci., 58: 1101–1106.
19. López, M. D. and Pascual-Villalobos, M. J. 2010. Mode of Inhibition of Acetylcholinesterase by Monoterpenoids and Implications for Pest Control. Ind. Crop Prod., 31: 284–288.
20. López, M. D. and Pascual-Villalobos, M. J. 2015a. Are Monoterpenoids and Phenylpropanoids Efficient Inhibitors of Acetylcholinesterase from Stored Product Insect strains?. Flav. Frag. J., 30: 108-112.
21. López, M. D., Campoy, F. J., Pascual-Villalobos, M. J., Muñoz-Delgado, E. and Vidal, C. J. 2015b. Acetylcholinesterase Activity of Electric Eel Is Increased or Decreased by Selected Monoterpenoids and Phenylpropanoids in a Concentration-Dependent Manner. Chem. Biol. Interact., 229: 36-43.
22. Mills, C., Cleary, B. V., Walsh, J. J. and Gilmer, J. F. 2004. Inhibition of Acetylcholinesterase by Tea Tree Oil. J. Pharm. Pharmacol., 56: 375–379.
23. Miyazawa, M., Watanabe, H., Umemoto, K. and Kameoka, H. 1998. Inhibition of Acetylcholinesterase Activity by Essential Oils of Mentha Species. J. Agric. Food Chem., 46: 3431-3434.
24. Miyazawa, M. and Yamafuji, C. 2005. Inhibition of Acetylcholinesterase Activity by Tea Tree Oil and Constituent Terpenoids. Flavour Frag. J., 20: 617-620.
25. Miyazawa, M. and Yamafuji, C. 2006. Inhibition of Acetylcholinesterase Activity by Tea Tree Oil and Constituent Terpenoids. Flavour Frag. J., 21: 198–201.
26. Mukherjee, P. K., Kumar V., Mal M. and Houghton P. J. 2007. Acetylcholinesterase Inhibitors from Plants. Phytomed., 14: 289–300.
27. Oliveira, M. R. V., Henneberry, T. J. and Anderson, P. 2001. History, Current Status, and Collaborative Research Projects for Bemisia tabaci. Crop Prot., 20: 709–723.
28. Orhan I., Aslan, S., Kartal, M., Şener, B. and Hüsnü Can Başer, K. 2008. Inhibitory Effect of Turkish Rosmarinus officinalis L. on Acetylcholinesterase and Butyrylcholinesterase Enzymes. Food Chem., 108: 663-668.
29. Orhan, I., Sener, B., Choudhary, M. I. and Khalid, A. 2004. Acetylcholinesterase and Butyrylcholinesterase Inhibitory Activity of Some Turkish Medicinal Plants. J. Ethnopharmacol., 91: 57–60.
30. Paluch, G., Grodnitzky, J., Bartholomay, L. and Coats, J. 2009. Quantitative Structure-Activity Relationship of Botanical Sesquiterpenes: Spatial and Contact Repellency to the Yellow Fever Mosquito, Aedes aegypti. J. Agric. Food Chem., 57: 7618-25.
31. Palumbo, J. C., Horowitz, A. R. and Prabhaker, N. 2001. Insecticidal Control and Resistance Management for Bemisia tabaci. Crop Prot., 20: 739–765.
32. Park, B. S., Choi, W. S., Kim, K. H. and Lee, S. E. 2005. Monoterpenes from Thyme (Thymus vulgaris) as Potential Mosquito Repellents. J. Am. Mosq Control Assoc., 21: 80-3.
33. Parrella, G., Scassillo, L. and Giorgini, M. 2012. Evidence for a New Genetic Variant in the Bemisia tabaci Species Complex and the Prevalence of the Biotype Q in Southern Italy. J. Pest Sci., 85: 227–238.
34. Perry, N. S. L., Houghton, P. J., Jenner, K. A. and Perry, E. K. 2002. Salvia lavandulaefolia Essential Oil Inhibits Cholinesterase In Vivo. Phytomed., 9: 48–51.
35. Picollo, M. I., Toloza, A. C., Cueto, G. M., Zygadlo, J. and Zerba, E. 2008. Anticholinesterase and Pediculicidal Activities of Monoterpenoids. Fitoterapia, 79: 271-278.
36. Priestley, C. M., Williamson, E. M., Wafford, K. A. and Sattelle, D. B. 2003. Thymol, a Constituent of Thyme Essential Oil, Is a Positive Allosteric Modulator of Human GABAA Receptors and a Homo-Oligomeric GABA Receptor from Drosophila melanogaster. Br. J. Pharmacol., 140: 1363-1372.
37. Roditakis, E., Grispou, M., Morou, E., Kristoffersen, J. B., Roditakis, N., Nauen, R., Vontas, J. and Tsagkarakou, A. 2009. Current Status of Insecticide Resistance in Q Biotype Bemisia tabaci Populations from Crete. Pest Manage. Sci., 65: 313-322.
38. Ryan, M. F. and Bryan, O. 1988. Plant-insect Coevaluation and Inhibition of Acetylcholinesterase. J. Chem. Ecol., 14: 965-1975.
39. Saleh, D., Laarif, A., Clouet, C. and Gauthier, N. 2012. Spatial and host-plant partitioning between coexisting Bemisia tabaci cryptic species in Tunisia. Popul. Ecol., 54: 261–274.
40. Savelev, S., Okello, E., Perry, N. S. L., Wilkins, R. M. and Perry, E. K. 2003. Synergistic and Antagonistic Interactions of Anticholinesterase Terpenoids in Salvia lavandulaefolia Essential Oil. Pharmacol. Biochem. Behav., 75: 661–668.
41. Wilson, M., Moshitzy, P., Laor, E., Ghanim, M., Horowtiz, A. R. and Morin, S. 2007. Reversal of Resistance to Pyriproxyfen in the Q Biotype of Bemisia tabaci (Hemiptera: Aleyrodidae). Pest Manag. Sci., 63: 761-768.
42. Zarrad, K., Ben Hamouda, A., Chaieb, I., Laarif, A. and Mediouni-Ben Jemâa, J. 2015. Chemical Composition, Fumigant and Anti-Acetylcholinesterase Activity of the Tunisian Citrus aurantium L. Essential Oils. Ind. Crop. Prod., 76: 121–127.
Journal of Agricultural Science and Technology
Volume 19, Issue 3
May and June 2017
Pages 643-652