Abstract
Halyomorpha halys (Stål) (Heteroptera: Pentatomidae) has brought about agricultural harm throughout the Eastern Black Sea coastline since 2017. It continues to come to a threat because there are no adequate studies on managing this pest. One of the major rein strategies of insecticides is acetylcholinesterase (ACHE) inhibition. Therefore, this study aims to investigate an alternative way to struggle H. halys by inhibiting ACHE. The ACHE was purified from H. halys using edrophonium-Sepharose 6B affinity chromatography and characterized by examining some kinetic properties. The molecular weight of the purified enzyme was determined by Sodium Dodecyl Sulfate-Polyacrylamide Gel Electrophoresis and natural polyacrylamide gel electrophoresis. In addition, the inhibitory effects of tacrine and edrophonium chloride, and water extracts of olive leaf, walnut leaf and alder leaf on this ACHE were investigated. The acetylcholinesterase was purified 403-fold with an 83.3% yield. H. halys ACHE was found to have six subunits and a molecular weight of approximately 350 kDa. The ACHE’s Km, Vmax, and kcat values were assigned to be 0.02 ± 0.006 mM, 3,333.3 ± 481 EU.mg protein− 1, and 1070.2 ± 184 min− 1, respectively. All inhibitors highly inhibited of activity of h.halys ACHE. Especially, the fact that the water extracts of these plants are effective in ACHE inhibition is significant due to being environmentally amicable pesticides that may be benefited in the struggle with the pest.
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Abbou F, Azzi R, Ouffai K, El Haci IA, Belyagoubi-Benhammou N, Bensouici C, Benamar H (2022). Phenolic profile, antioxidant and enzyme inhibitoryproperties of phenolic-rich fractions from the aerial parts of Menthapulegium L. South African Journal of Botany, 146, 196–204. https://doi.org/10.1016/j.sajb.2021.10.024
Abdellaoui K, Boussadia O, Miladi M, Boughattas I, Omri G, Mhafdhi M, Brahem M (2019) Olive leaf extracts toxicity to the migratory locust, Locusta migratoria: histopathological effects on the alimentary canal and acetylcholinesterase and glutathione S-transferases activity. Neotrop Entomol 48(2):246–259. https://doi.org/10.1007/s13744-018-0628-1
Acheuk F, Lakhdari W, Abdellaoui K, Belaid M, Allouane R, Hallouane F (2017) Phytochemical study and bioinsecticidal effect of the crude ethanolic extract of the algerian plant Artemisia judaica L. (Asteraceae) against the black bean aphid Aphis fabae Scop. Agric For 63:95–104. https://doi.org/10.17707/AgricultForest.63.1.11
Adeyemi Hassan M M (2010). The potential of secondary metabolites in plant materials deterents against insect pests: A review. African Journal of Pure andApplied Chemistry, 4(11), 243–246.http://www.academicjournals.org/journal/AJPAC/article-abstract/B76CE2E2388
Ak K, Uluca M, Aydin Ö, Gokturk T (2019) Important invasive species and its pest status in Turkey: Halyomorpha halys (Stål) (Heteroptera: Pentatomidae), Journal of Plant Diseases and Protection (2019) 126:401–408. https://doi.org/10.1007/s41348-019-00243-7
Askar KA, Kudi AC, Moody AJ (2011) Purification of Soluble Acetylcholinesterase from Sheep Liver by Affinity Chromatography. Appl Biochem Biotechnol 165(1):336–346. https://doi.org/10.1007/s12010-011-9254-7
Bariselli M, Bugiani R, Maistrello L (2016) Distribution and damage caused by Halyomorpha halys in Italy. EPPO Bull 46:332–334
Bosco L, Moraglio ST, Tavella L (2018) Halyomorpha halys, a serious threat for hazelnut in newly invaded areas. J Pest Sci 91:661–670. https://doi.org/10.1007/s10340-017-0937-x
Bughio FM, Wilkins RM (2004) Influence of Malathion Resistance Status on Survival and Growth of Tribolium Castaneum (Coleoptera: Tenebrionidae), when Fed on Flour from İnsect-Resistant and susceptible Grain Rice Cultivars. J Stored Prod Res 40(1):65–75. https://doi.org/10.1016/S0022-474X(02)00077-2
Cavdar H, Senturk M, Guney M, Durdagi S, Kayik G, Supuran CT, Ekinci D (2019) Inhibition of acetylcholinesterase and butyrylcholinesterase with uracil derivatives: kinetic and computational studies. J Enzyme Inhib Med Chem 34(1):429–437. https://doi.org/10.1080/14756366.2018.1543288
Çerçi B, Koçak Ö (2017) Further contribution to the Heteroptera (Hemiptera) fauna of Turkey with a new synonymy. Acta Biologica Turcica 30(4):121–127
Cesari M, Maistrello L, Ganzerli F, Dioli P, Rebecchi L, Guidettı R (2015) A pest alien invasion in progress: potential pathways of origin of the brown marmorated stink bug Halyomorpha halys populations in Italy. J Pest Sci 88(1):1–7
Céspedes CL, Torres P, Marin JC, Arciniegas A, Romo de Vivar A, Pérez-Castorena AL, Aranda E (2004) Insect growth inhibition by Tocotrienols and Hydroquinones from Roldana barba-johannis. Phytochemistry 65:1963–1975. https://doi.org/10.1016/j.phytochem.2004.03.037
Cira TM, Venette RC, Aigner J, Kuhar T, Mullins DE, Gabbert SE, Hutchison WD (2016) Cold tolerance of Halyomorpha halys (Hemiptera: Pentatomidae) across geographic and temporal scales. Environ Entomol 45(2):484–491
Colovic MB, Krstic DZ, Lazarevic-Pasti TD, Bondzic AM, Vasic VM (2013) Acetylcholinesterase inhibitors. Pharmacol Toxicol Curr Neuropharmacol 11(3):315–335
Costi E, Haye T, Maistrello L (2017) Biological parameters of the invasive brown marmorated stink bug, Halyomorpha halys, in southern Europe. J Pest Sci 90:1059–1067. https://doi.org/10.1007/s10340-017-0899-z
Cox PD (2004) Potential for using semiochemicals to protect stored products from İnsect İnfestation. J Stored Prod Res 40(1):1–25. https://www.jstor.org/stable/42552942-474X (02)00078-4
Dinçer B, Kızıl D (2022) Inhibition and purification of acetylcholinesterases from adults and nymphs of Ricania simulans (Walker, 1851)(Hemiptera: Ricaniidae). Int J Trop Insect Sci 42(5):3363–3372
Dong ZH (1995) Purification of cholinesterase from Pseudosciaena Crocea muscle. Chin Biochem J 11(4):487–489
Dudai Y, Silman I (1974) The Molecular Weight and Subunit structure of acetylcholinesterase preparations from the Electric Organ of the Electric Eel. Biochem Biophys Res Commun 59(1):117–124
Duranay S, Anil S, Hasbal G, Özsoy N (2019) Purification of acetylcholinesterase from the Mollusc Mytilus Galloprovincialis Lam. And Investigation of its Kinetic Properties. J Res Pharm 23(4):759–769. https://doi.org/10.12991/jrp.2019.185
Ellman GL, Courtney KD, Andres V, Featherstone RM (1961) A New and Rapid Colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7(2):2–3. https://doi.org/10.1016/0006-2952(61)90145-9
Fournier D, Mutero A (1994) Modification of acetylcholinesterase as a mechanism of resistance to insecticides. Comp Biochem Physiol Part-C: Pharmacology 108(1):9–31. https://doi.org/10.1016/1367-8280(94)90084-1
Gao JR, Rao JV, Wilde GE, Zhu KY (1998) Purification and Kinetic Analysis of Acetylcholinesterase from Western Corn Rootworm, Diabrotica virgifera virgifera (Coleoptera: Chrysomelidae). Arch Insect Biochem Physiol 39(3):118–25. https://doi.org/10.1002/(SICI)1520-6327(1998)39:3<118::AID-ARCH4>3.0.CO;2-6
Gapon DA (2016) First records of the brown marmorated stink bug Halyomorpha halys (Stål, 1855) (Heteroptera, Pentatomidae) in Russia, Abkhazia, and Georgia. Entomol Rev 96:1086–1088
Gü lçinİ, Gören A C, Taslimi P, Alwasel S H, Kılıc O ve Bursal E (2020). Anticholinergic, antidiabetic and antioxidant activities of Anatolianpennyroyal (Mentha pulegium)-analysis of its polyphenol contents byLC-MS/MS. Biocatalysis andAgricultural Biotechnology, 23(November2019). https://doi.org/10.1016/j.bcab.2019.101441
Güncan A, Gümüş E (2019) Brown marmorated stink bug, Halyomorpha halys (Stal, 1855) (Hemiptera:Heteroptera, Pentataomidae), a New and Importand Pest in Turkey. Entomol News 28(2):204–2010
Hamouda AB, Zarrad K, Laarif A, Chaieb I (2015a) Insecticidal Effect of Solanum elaeagnifolium extracts under Laboratory Conditions. J Entomol Zool Stud 3(3):187–190
Hamouda AB, Boussadia O, Khaoula B, Laarif A, Braham M (2015b) Studies on İnsecticidal and Deterrent Effects of Olive Leaf extracts on Myzus persicae and phthorimaea operculella. J Entomol Zool Stud 3(6):294–297
Haye T, Weber DC (2017) Special issue on the brown marmorated stink bug, Halyomorpha halys: an emerging pest of global concern. J Pest Sci 90:987–988. https://doi.org/10.1007/s10340-017-0897-1
Haye T, Gariepy T, Hoelmer K, Rossı JP, Streıto JP, Tassus X, Desneux N (2015) Range expansion of the invasive brown marmorated stinkbug, Halyomorpha halys: an increasing threat to field, fruit and vegetable crops worldwide. J Pest Sci 88(4):665–673
Hedstrom CS, Shearer PW, Miller JC, Walton VM (2014) The effects of kernel feeding by Halyomorpha halys (Hemiptera: Pentatomidae) on commercial hazelnuts. J Econ Entomol 107(5):1858–1865
Hodgson AJ, Chubb IW (1983) Isolation of the secretory form of Soluble Acetylcholinesterase by using Affinity Chromatography on Edrophonium-Sepharose. J Neurochem 41(3):654–662. https://doi.org/10.1111/j.1471-4159.1983
Hoebeke ER, Carter ME (2003) Halyomorpha halys (Stal) (Heteroptera: Pentatomidae): a polyphagous plant pest from Asia newly detected in North America. Proceedings of the Entomological Society of Washington, 105(1): 225–237
Inkley DB (2012) Characteristics of home invasion by the brown marmorated stink bug (Hemiptera: Pentatomidae). J Entomol Sci 47(2):125–130
Jemai H, Feki E, A. and, Sayadi S (2009) Antidiabetic and antioxidant Effects of Hydroxytyrosol and Oleuropein from Olive Leaves in Alloxan-Diabetic rats. J Agric Food Chem 57(19):8798–8804. https://doi.org/10.1021/jf901280r
Jones JR, Lambdin PL (2009) New county and state records for Tennessee of an exotic pest, Halyomorpha halys (Hemiptera: Pentatomidae), with potential economic and ecological implications. Fla Entomol 92(1):177–178
Keane S, Ryan MF (1999) Purification, Characterisation, and Inhibition by Monoterpenes of Acetylcholinesterase from the Waxmoth, Galleria Mellonella (L.). Insect Biochem. Mol. Biol 29(12):1097–1104. https://doi.org/10.1016/S0965-1748(99)00088-0
Kiritani K (2012) The low development threshold temperature and the thermal constant in insects and mites in Japan, vol 31. Bulletin of National Institute for Agro-Environmental Sci, pp 1–74
Kriticos DJ, Kean JM, Phillips CB, Senay SD, Acosta H, Haye T (2017) The potential global distribution of the brown marmorated stink bug, Halyomorpha halys, a critical threat to plant biosecurity. J Pest Sci 90:1033–1043. https://doi.org/10.1007/s10340-017-0869-5
Laemmli UK (1970) Cleavage of structural proteins during the As-Sembly of the Head Bacteriophage T4. Nature 227:680–685. https://doi.org/10.1038/227680a0
Lee DH, Short BD, Joseph SV, Bergh JC, Leskey TC (2013) Review of the biology, ecology, and management of Halyomorpha halys (Hemiptera: Pentatomidae) in China, Japan, and the Republic of Korea. Environ Entomol 42(4):627–641
Li F, Han Z (2002) Purification and characterization of acetylcholinesterase from Cotton Aphid (Aphis gossypii Glover). Arch Insect Biochem Physiol 51(1):37–45. https://doi.org/10.1002/arch.10048
Lineweaver H, Burk D (1934) The determination of enzyme dissociation Constants. J Am Chem Soc 56:658–666
Lingk W (1991) Health Risk Evaluation of Pesticide Contaminations in Drinking Water. Gesunde Pflanzen (Germany, FR)
Liu K, Wang J, Zhao L, Wang Q (2013) Anticancer, antioxidant and antibiotic activities of mushroom Ramaria Flava. Food Chem Toxicol 58:375–380. http://www.ncbi.nlm.nih.gov/pubmed/23684998
Lowry HO, Rosebrouggh JN, Randall RJ, Lewis A (1951) Protein measurement with the Folin Phenol Reagent. J Biol Chem 193:265–275
Lupi D, Dioli P, Limonta L (2017) First evidence of Halyomorpha halys (Stal) (Hemiptera:Heteroptera:Pentatomidae) feeding on rice (Oryza sativa L). J Entomol Acarol Res 9(6679):67–71
Maistrello L, Dioli P, Vaccarı G, Nannıni R, Bortolottıi P, Caruso S, Costi E, Montermını A, Casoli L (2014) Barıselli M (2014) first records in Italy of the asian stinkbug Halyomorpha halys, a new threat for fruit crops. Atti Gte Fitopatol 1:283–288
Mata AT, Proença C, Ferreira AR, Serralheiro ML M, Nogueira JMF, Araújo MEM (2007). Antioxidant and antiacetylcholinesterase activitiesof five plants used as Portuguese food spices. Food Chemistry, 103(3),778–786. https://doi.org/10.1016/j.foodchem.2006.09.017
Meng X, Li C, Xiu C, Zhang J, Li J, Huang L, Zhang Y, Liu Z (2016) Identification and biochemical Properties of two new Acetylcholinesterases in the Pond Wolf Spider (Pardosa pseudoannulata). PLoS ONE 11(16):1–14. https://doi.org/10.1371/journal.pone.0158011
Mishra AK (1990) Fungitoxicity of essential oil of Amomum subulatum against aspergillus flavus. Econ Bot 44(4):530–533. https://www.jstor.org/stable/4255294
Mohamed MA, Amira, Abdel-Gawad S, Abd Elhady MG (2007) Purification and characterization of an acetylcholinesterase from the infective Juveniles of Heterorhabditis bacteriophora. Comp Biochem Physiol Part-C: Toxicology and Pharmacology 146(3):314–324. https://doi.org/10.1016/j.cbpc.2007.04.001
Mohamed MA, Shaalan S, Ghazy AM, Ali AA, Abd-Elaziz AM, Ghanem MME, Abd-Elghany SA (2020) Purification and characterization of acetylcholinesterase in Rhynchophorus ferrugineus (Olivier) (Coleoptera: Curculionidae). Int J Biol Macromol 147:1029–1040. https://doi.org/10.1016/j.ijbiomac.2019.10.071
Mutunga JM, Anderson TD, Wong DM, Carlier PR (2009) Inhibition of Blattella Germanica Acetylcholinesterase by Bis(n)-Tacrines: Prospects for the Molecular Design of a Selective Insecticide for a Household Pest. ACS Symposium Series 1015:41–51
Özdemir İO, Tuncer C (2021) A New Invasive Polyphagous Pest in Turkey, Brown Marmorated Stink bug [Halyomorpha halys (Stål, 1855) (Hemiptera: Pentatomidae)]: identification, similar species and current status. Black Sea Journal of Engineering and Science 4(2):58–67. https://doi.org/10.34248/bsengineering.844095
Prabhakaran SK, Kamble ST (1996) Biochemical characterization and purification of Esterases from three strains of german cockroach, Blattella Germanica (Dictyoptera: Blattellidae). Arch Insect Biochem Physiol 31(1):73–86. https://doi.org/10.1002/(SICI)1520-6327(1996)31:1<73::AID-ARCH5>3.0.CO;2-Y
Rice KB, Bergh CJ, Bergmann EJ, Biddinger DJ, Dieckhoff C, Dively G, Fraser H, Gariepy T, Hamilton G, Haye T, Herbert A, Hoelmer K, Hooks CR, Jones A, Krawczyk G, Kuhar T, Martinson H, Mitchell W, Nielsen AL, Pfeiffer DG, Raupp MJ, Rodriguez-Saona C, Shearer P, Shrewsbury P, Venugopal PD, Whalen J, Wiman NG, Leskey TC, Tooker JF (2014) Biology, Ecology, and management of Brown Marmorated Stink bug (Hemiptera: Pentatomidae). J Integr Pest Manage 5(3):1–13. https://doi.org/10.1603/IPM14002
Scott IM, Jensen H, Scott JG, Isman MB, Arnason JT, Philogene BJR (2003) Botanical insecticides for controlling agricultural pests: piperamides and the Colorado potato beetle Leptinotarsa decemlineata say (Coleoptera: Chrysomelidae). Arch Insect Biochem Physiol 54:212–225. https://doi.org/10.1002/arch.10118
Shi SP, Zhang JY (1981) Purification and some Properties of Cholinesterase from Nebia Albiflora muscle. Acta Biochim Biophys Sin 13(1):10–11
Siegfried BD, Ono M, Swanson JJ (1997) Purification and characterization of a Carboxylesterase Associated with Organophosphate Resistance in the Greenbug, Schizaphis Graminum (Homoptera: Aphididae). Arch Insect Biochem Physiol 36(3):229–240. https://doi.org/10.1002/(SICI)1520-6327(1997)36:3<229::AID-ARCH7>3.0.CO;2-O
Son JY, Shin S, Choi KH, Park K (2002) Purification of Soluble Acetylcholinesterase from Japanese Quail Brain by Affinity Chromatography. Int J Biochem Cell Biol 34(2):204–210. https://doi.org/10.1016/S1357-2725(01)00082-6
Vetek G, Papp V, Haltrich A, Redei D (2014) First record of the brown marmorated stink bug, Halyomorpha halys (Hemiptera: Heteroptera: Pentatomidae), in Hungary, with description of the genitalia of both sexes. Zootaxa 3780:194–200
Wermelinger B, Wyniger D, Forster B (2008) First records of an invasive bug in Europe: Halyomorpha halys Stal (Heteroptera: Pentatomidae), a new pest on woody ornamentals and fruit trees? Mit Sch Ges 81:1–8
Xiwu G, Xuguo Z, Rongjing W, Bingzoneg Z (1998) Distribution and purification of acetylcholinesterase in Cotton Boll Worm (Lepidoptera: Noctuidae). Acta Entomol Sin 41:19–25
Xu T, Li S, Li AJ, Zhao J, Sakamuru S, Huang W, Xia M, Huang R (2023) Identification of potent and selective Acetylcholinesterase/Butyrylcholinesterase inhibitors by virtual screening. J Chem Inf Model 63(8):2321–2330. https://doi.org/10.1021/acs.jcim.3c00230
Zari TA, Al-Attar AM (2011) Therapeutic Effects of Olive Leaves extract on rats treated with a sublethal concentration of Carbendazim. Eur Rev Med Pharmacol Sci 15(4):413–426
Zhu KY, Clark JM (1994) Purification and characterization of Acetyl-Cholinesterase from the Colorado Potato Beetle, Leptinotarsa Decemlineata (say). Insect Biochem Mol Biol 24(5):453–461. https://doi.org/10.1016/0965-1748(94)90040-X
Zhu KY, Brindley WA, Hsiao TH (1991) Isolation and Partial Purification of Acetylcholinesterase from Lygus Hesperus (Hemiptera: Miridae). J Econ Entomol 84(3):790–794. https://doi.org/10.1093/jee/84.3.790
Zhu MC, Xin YB, Sun MJ, Fang YZ (1993) Purification and Properties of Acetylcholinesterase from Human Brain. Sci China Ser B: Chem 36(10):1207–1215 PMID: 8136033
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Dinçer, B., Akpınar, H. Purification of acetylcholinesterase from Halyomorpha halys (Stål) (Heteroptera: Pentatomidae) and management of control of the Pest through inhibition of the enzyme. Int J Trop Insect Sci 43, 1421–1429 (2023). https://doi.org/10.1007/s42690-023-01047-x
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DOI: https://doi.org/10.1007/s42690-023-01047-x