Sains Malaysiana 51(2)(2022): 461-472

http://doi.org/10.17576/jsm-2022-5102-11

Current Status of Genetically Modified Baculovirus Insecticide for Pest Control

(Status Terkini Racun Serangga Bakulovirus Terubah Suai Genetik untuk Kawalan Serangga Perosak)

MUHAMMAD AZHARUDDIN AZALI^{1, 2}, SALMAH MOHAMED², AZIAN HARUN³, SHAHARUM SHAMSUDDIN⁴ & MUHAMMAD FARID JOHAN¹*

¹Department of Haematology, School of Medical Sciences, Universiti Sains Malaysia, 16150 Kubang Kerian, Kelantan Darul Naim, Malaysia

²School of Agriculture Science and Biotechnology, Faculty of Bioresources and Food Industry, Universiti Sultan Zainal Abidin, 22200 Besut, Terengganu Darul Iman, Malaysia

³Department of Medical Microbiology and Parasitology, School of Medical Sciences, Universiti Sains Malaysia, 16150 Kubang Kerian, Kelantan Darul Naim, Malaysia

⁴School of Health Sciences, Universiti Sains Malaysia, 16150 Kubang Kerian, Kelantan Darul Naim, Malaysia

Diserahkan: 17 Januari 2021/Diterima: 28 Mei 2021

ABSTRACT

Baculovirus is an insect specific virus which is harmless to human. This feature has made it suitable to be applied as biopesticide. It has been used to control the insect pest particularly in agriculture sector for half a century and several success stories have been shared. Nevertheless, this insecticide still cannot compete with the synthetic pesticides owing to its slow killing speed and deficiency of compatible hosts. Genetically engineered baculovirus has improved pathogenicity against insect by incorporating foreign genes. These foreign genes encode neurotoxin, hormones, enzymes, and antisense DNA. Expression of these genes can enhance the insecticidal activities of the recombinant baculovirus. Nonetheless, the genetically modified baculovirus still has not been commercialised until today. This might be associated with the concern about the release of the genetically modified organism (GMO) into the environment as the environmental impact of the genetically modified virus is not well understood. Furthermore, it has been found to have effect on certain parasitoid. In conclusion, genetic modifications of the baculovirus have successfully improved its insecticidal activities but insufficient knowledge about its safety has limited its use in the field.

Keywords: Baculovirus insecticide; biopesticide; insecticidal gene; neurotoxin

ABSTRAK

Bakulovirus adalah virus khusus terhadap serangga yang tidak berbahaya kepada manusia. Ciri ini menyebabkan ia sesuai digunakan sebagai bio-racun perosak. Ia telah digunakan untuk mengawal serangga perosak terutamanya dalam sektor pertanian selama setengah abad dan beberapa kejayaan telah dikongsikan. Walau bagaimanapun, penggunaan racun serangga ini tidak dapat mengatasi racun serangga sintetik disebabkan kadar pembunuhannya yang perlahan dan kekurangan hos yang bersesuaian. Pengubahsuaian genetik bakulovirus telah menambah baik kepatogenan bakulovirus terhadap serangga dengan memasukkan gen asing ke dalamnya. Gen asing ini mengekodkan neurotoksin, hormon, enzim dan DNA antisens. Pengekspresan gen ini dapat meningkatkan aktiviti insektisid bakulovirus rekombinan. Namun demikian, bakulovirus terubah suai genetik masih tidak dipasarkan sehingga kini. Ini mungkin berpunca daripada kegusaran terhadap pelepasan organisma terubah suai genetik (GMO) ke persekitaran memandangkan kesan virus terubah suai genetik terhadap persekitaran masih belum difahami sepenuhnya. Tambahan pula, ia telah didapati memberi kesan terhadap parasitoid tertentu. Secara kesimpulannya, pengubahsuaian genetik terhadap bakulovirus telah berjaya meningkatkan aktiviti insektisid tetapi kurangnya pengetahuan tentang keselamatan terhadap penggunaannya telah mengehadkan penggunaannya di lapangan.

Kata kunci: Bakulovirus insektisid; Bio-racun perosak; gen insektisid; neurotoksin

RUJUKAN

Ali, M.P., Kato, T. & Park, E.Y. 2015. Improved insecticidal activity of a recombinant baculovirus expressing spider venom cyto-insectotoxin. Applied Microbiology and Biotechnology 99(23): 10261-10269.

Ardisson-Araújo, D.M.P., Morgado, F.D.S., Schwartz, E.F., Corzo, G. & Ribeiro, B.M. 2013. A new theraphosid spider toxin causes early insect cell death by necrosis when expressed in vitro during recombinant baculovirus infection. PloS ONE 8(12): e84404.

Assenga, S.P., You, M., Shy, C.H., Yamagishi, J., Sakaguchi, T., Zhou, J., Kibe, M.K., Xuan, X. & Fujisaki, K. 2006. The use of a recombinant baculovirus expressing a chitinase from the hard tick Haemaphysalis longicornis and its potential application as a bioacaricide for tick control. Parasitology Research 98(2): 111-118.

Beas-Catena, A., Sánchez-Mirón, A., García-Camacho, F., Contreras-Gómez, A. & Molina-Grima, E. 2014. Baculovirus biopesticides: An overview. Journal of Animal and Plant Sciences 24(2): 362-373.

Bel Haj Rhouma, R., Cérutti-Duonor, M., Benkhadir, K., Goudey-Perrière, F., El Ayeb, M., Lopez-Ferber, M. & Karoui, H. 2005. Insecticidal effects of Buthus occitanus tunetanus BotIT6 toxin expressed in Escherichia coli and baculovirus/insect cells. Journal of Insect Physiology 51(12): 1376-1383.

Bonning, B.C. & Nusawardani, T. 2007. Introduction to the use of baculoviruses as biological insecticides. Methods in Molecular Biology 388: 359-366.

Bonning, B.C., Possee, R.D. & Hammock, B.D. 1999. Insecticidal efficacy of a recombinant Baculovirus expressing JHE-KK, a modified juvenile hormone esterase. Journal of Invertebrate Pathology 73(2): 234-236.

Bonning, B.C., Ward, V.K., van Meer, M.M., Booth, T.F. & Hammock, B.D. 1997. Disruption of lysosomal targeting is associated with insecticidal potency of juvenile hormone esterase. Proceedings of the National Academy of Sciences of the United States of America 94(12): 6007-6012.

Bonning, B.C., Hirst, M., Possee, R.D. & Hammock, B.D. 1992. Further development of a recombinant baculovirus insecticide expressing the enzyme juvenile hormone esterase from Heliothis virescens. Insect Biochemistry and Molecular Biology 22(5): 453-458.

Carbonell, L.F., Hodge, M.R., Tomalski, M.D. & Miller, L.K. 1988. Synthesis of a gene coding for an insect-specific scorpion neurotoxin and attempts to express it using baculovirus vectors. Gene 73(2): 409-418.

Chang, J.H., Choi, J.Y., Jin, B.R., Roh, J.Y., Olszewski, J.A., Seo, S.J., O’Reilly, D.R. & Je, Y.H. 2003. An improved baculovirus insecticide producing occlusion bodies that contain Bacillus thuringiensis insect toxin. Journal of Invertebrate Pathology 84(1): 30-37.

Choi, J.Y., Jung, M.P.P., Park, H.H.H., Tao, X.Y., Jin, B.R. & Je, Y.H. 2013. Insecticidal activity of recombinant baculovirus co-expressing Bacillus thuringiensis crystal protein and Kunitz-type toxin isolated from the venom of bumblebee Bombus ignitus. Journal of Asia-Pacific Entomology 16(1): 75-80.

Cory, J.S., Hirst, M.L., Williams, T., Hails, R.S., Goulson, D., Green, B.M., Carty, T.M., Possee, R.D., Cayley, P.J. & Bishop, D.H.L. 1994. Field trial of a genetically improved baculovirus insecticide. Nature 370(6485): 138-140.

Cramer, H.H. 1967. Plant Protection and World Crop Production. Leverkusen: Farbenfabriken Bayer AG.

Deng, S.Q., Chen, J.T., Li, W.W., Chen, M. & Peng, H.J. 2019. Application of the scorpion neurotoxin AaIT against insect pests. International Journal of Molecular Sciences 20(14): 3467-3475.

Dhaliwal, G.S., Jindal, V. & Mohindru, B. 2015. Crop losses due to insect pests: Global and Indian scenario. Indian Journal of Entomology 77(2): 165-168.

Eldridge, R., O’Reilly, D.R. & Miller, L.K. 1992a. Efficacy of a baculovirus pesticide expressing an eclosion hormone gene. Biological Control 2(2): 104-110.

Eldridge, R., O’Reilly, D.R., Hammock, B.D. & Miller, L.K. 1992b. Insecticidal properties of genetically engineered baculoviruses expressing an insect juvenile hormone esterase gene. Applied and Environmental Microbiology 58(5): 1583-1591.

El-Sheikh, E.S.A., Kamita, S.G., Vu, K. & Hammock, B.D. 2011. Improved insecticidal efficacy of a recombinant baculovirus expressing mutated JH esterase from Manduca sexta. Biological Control 58(3): 354-361.

Fu, Y., Li, X., Du, J., Zheng, S. & Liang, A. 2015. Regulation analysis of AcMNPV-mediated expression of a Chinese scorpion neurotoxin under the IE1, P10 and PH promoter in vivo and its use as a potential bio-insecticide. Biotechnology Letters 37(10): 1929-1936.

Gershburg, E., Stockholm, D., Froy, O., Rashi, S., Gurevitz, M. & Chejanovsky, N. 1998. Baculovirus-mediated expression of a scorpion depressant toxin improves the insecticidal efficacy achieved with excitatory toxins. FEBS Letters 422(2): 132-136.

Gramkow, A.W., Perecmanis, S., Sousa, R.L.B., Noronha, E.F., Felix, C.R., Nagata, T. & Ribeiro, B.M. 2010. Insecticidal activity of two proteases against Spodoptera frugiperda larvae infected with recombinant baculoviruses. Virology Journal 7(1): 143-152.

Haase, S., Sciocco-Cap, A. & Romanowski, V. 2015. Baculovirus insecticides in Latin America: Historical overview, current status and future perspectives. Viruses 7(5): 2230-2267.

Hernandez-Crespo, P., Sait, S.M., Hails, R.S. & Cory, J.S. 2001. Behavior of a recombinant baculovirus in lepidopteran hosts with different susceptibilities. Applied and Environmental Microbiology 67(3): 1140-1146.

Hernandez-Crespo, P., Hails, R.S., Sait, S.M., Green, B.M., Carty, T.M. & Cory, J.S. 1999. Response of permissive and semi-permissive hosts to a recombinant baculovirus insecticide in the field. Biological Control 16(2): 119-127.

Iyaniwura, T.T. 1991. Non-target and environmental hazards of pesticides. Reviews on Environmental Health 9(3): 161-176.

Jarvis, D.L., Reilly, L.M., Hoover, K., Schultz, C., Hammock, B.D. & Guarino, L.A. 1996. Construction and characterization of immediate early baculovirus pesticides. Biological Control 7(2): 228-235.

Jinn, T.R., Tu, W.C., Lu, C.I. & Tzen, J.T.C. 2006. Enhancing insecticidal efficacy of baculovirus by early expressing an insect neurotoxin, LqhIT2, in infected Trichoplusia ni larvae. Applied Microbiology and Biotechnology 72(6): 1247-1253.

Kamita, S.G. & Hammock, B.D. 2010. Juvenile hormone esterase: Biochemistry and structure. Journal of Pesticide Science 35(3): 265-274.

Kergunteuil, A., Bakhtiari, M., Formenti, L., Xiao, Z., Defossez, E. & Rasmann, S. 2016. Biological control beneath the feet: A review of crop protection against insect root herbivores. Insects 7(4): 70-91.

Korth, K.L. & Levings III, C.S. 1993. Baculovirus expression of the maize mitochondrial protein URF13 confers insecticidal activity in cell cultures and larvae. Proceedings of the National Academy of Sciences of the United States of America 90(8): 3388-3392.

Kreutzweiser, D., England, L., Shepherd, J., Conklin, J. & Holmes, S. 2001. Comparative effects of a genetically engineered insect virus and a growth-regulating insecticide on microbial communities in aquatic microcosms. Ecotoxicology and Environmental Safety 48(1): 85-98.

Lee, H.H., Moon, E.S., Lee, S.T., Hwang, S.H., Cha, S.C. & Yoo, K.H. 1998. Construction of a baculovirus Hyphantria cunea NPV insecticide containing the insecticidal protein gene of Bacillus thuringiensis subsp. kurstaki HD1. Journal of Microbiology and Biotechnology 8(6): 685-691.

Lee, S.Y., Qu, X., Chen, W., Poloumienko, A., MacAfee, N., Morin, B., Lucarotti, C. & Krause, M. 1997. Insecticidal activity of a recombinant baculovirus containing an antisense c-myc fragment. Journal of General Virology 78(1): 273-281.

Lei, C., Yang, S., Lei, W., Nyamwasa, I., Hu, J. & Sun, X. 2019. Displaying enhancing factors on the surface of occlusion bodies improves the insecticidal efficacy of a baculovirus. Pest Management Science 76(4): 1363-1370.

Li, J., Zhou, Y., Lei, C., Fang, W. & Sun, X. 2015. Improvement in the UV resistance of baculoviruses by displaying nano-zinc oxide-binding peptides on the surfaces of their occlusion bodies. Applied Microbiology and Biotechnology 99(16): 6841-6853.

Maeda, S. 1989. Increased insecticidal effect by a recombinant baculovirus carrying a synthetic diuretic hormone gene. Biochemical and Biophysical Research Communications 165(3): 1177-1183.

Maeda, S., Volrath, S.L., Hanzlik, T.N., Harper, S.A., Majima, K., Maddox, D.W., Hammock, B.D. & Fowler, E. 1991. Insecticidal effects of an insect-specific neurotoxin expressed by a recombinant baculovirus. Virology 184(2): 777-780.

Martens, J.W., Knoester, M., Weijts, F., Groffen, S.J., Hu, Z., Bosch, D. & Vlak, J.M. 1995. Characterization of baculovirus insecticides expressing tailored Bacillus thuringiensis CryIA(b) crystal proteins. Journal of Invertebrate Pathology 66(3): 249-257.

McNitt, L., Espelie, K.E. & Miller, L.K. 1995. Assessing the safety of toxin-producing baculovirus biopesticides to a nontarget predator, the Social Wasp Polistes metricus Say. Biological Control 5(2): 267-278.

Merryweather, A.T., Weyer, U., Harris, M.P., Hirst, M., Booth, T. & Possee, R.D. 1990. Construction of genetically engineered baculovirus insecticides containing the Bacillus thuringiensis subsp. kurstaki HD-73 delta endotoxin. Journal of General Virology 71(7): 1535-1544.

Moscardi, F. 1999. Assessment of the application of baculoviruses for control of lepidoptera. Annual Review of Entomology 44: 257-289.

Nusawardani, T., Ruberson, J.R., Obrycki, J.J. & Bonning, B.C. 2005. Effects of a protease-expressing recombinant baculovirus insecticide on the parasitoid Cotesia marginiventris (Cresson). Biological Control 35(1): 46-54.

O’reilly, D.R. & Miller, L.K. 1991. Improvement of a baculovirus pesticide by deletion of the egt gene. Nature Biotechnology 9(11): 1086-1089.

Pazmiño-Ibarra, V., Mengual-Martí, A., Targovnik, A.M. & Herrero, S. 2019. Improvement of baculovirus as protein expression vector and as biopesticide by CRISPR/Cas9 editing. Biotechnology and Bioengineering 116(11): 2823-2833.

Petrik, D.T., Iseli, A., Montelone, B.A., Van Etten, J.L. & Clem, R.J. 2003. Improving baculovirus resistance to UV inactivation: Increased virulence resulting from expression of a DNA repair enzyme. Journal of Invertebrate Pathology 82(1): 50-56.

Popham, H.J.R., Li, Y. & Miller, L.K. 1997. Genetic improvement of Helicoverpa zea nuclear polyhedrosis virus as a biopesticide. Biological Control 10(2): 83-91.

Rajendra, W., Hackett, K.J., Buckley, E. & Hammock, B.D. 2006. Functional expression of lepidopteran-selective neurotoxin in baculovirus: Potential for effective pest management. Biochimica et Biophysica Acta 1760(2): 158-163.

Ran, Z., Shi, X., Han, F., Li, J., Zhang, Y., Zhou, Y., Yin, J., Li, R. & Zhong, J. 2018. Expressing microRNA bantam sponge drastically improves the insecticidal activity of baculovirus via increasing the level of ecdysteroid hormone in Spodoptera exigua larvae. Frontiers in Microbiology 9: 1824-1834.

Regev, A., Rivkin, H., Gurevitz, M. & Chejanovsky, N. 2006. New measures of insecticidal efficacy and safety obtained with the 39K promoter of a recombinant baculovirus. FEBS Letters 580(30): 6777-6782.

Regev, A., Rivkin, H., Inceoglu, B., Gershburg, E., Hammock, B.D., Gurevitz, M. & Chejanovsky, N. 2003. Further enhancement of baculovirus insecticidal efficacy with scorpion toxins that interact cooperatively. FEBS Letters 537(1-3): 106-110.

Shao, H.L., Dong, D.J., Hu, J.D., Wang, J.X. & Zhao, X.F. 2008. Construction of the recombinant baculovirus AcMNPV with cathepsin B-like proteinase and its insecticidal activity against Helicoverpa armigera. Pesticide Biochemistry and Physiology 91(3): 141-146.

Shen, S., Gan, Y., Wang, M., Hu, Z., Wang, H. & Deng, F. 2012. Incorporation of GP64 into Helicoverpa armigera nucleopolyhedrovirus enhances virus infectivity in vivo and in vitro. Journal of General Virology 93(12): 2705-2711.

Shim, H.J., Choi, J.Y., Wang, Y., Tao, X.Y., Liu, Q., Roh, J.Y., Kim, J.S., Kim, W.J., Woo, S.D., Jin, B.R. & Je, Y.H. 2013. NeuroBactrus, a novel, highly effective, and environmentally friendly recombinant baculovirus insecticide. Applied and Environmental Microbiology 79(1): 141-149.

Stewart, L.M., Hirst, M., López Ferber, M., Merryweather, A.T., Cayley, P.J. & Possee, R.D. 1991. Construction of an improved baculovirus insecticide containing an insect-specific toxin gene. Nature 352(6330): 85-88.

Szolajska, E., Poznanski, J., Ferber, M.L., Michalik, J., Gout, E., Fender, P., Bailly, I., Dublet, B. & Chroboczek, J. 2004. Poneratoxin, a neurotoxin from ant venom. Structure and expression in insect cells and construction of a bio-insecticide. European Journal of Biochemistry 271(11): 2127-2136.

Thompson, C.G., Scott, D.W. & Wickman, B.E. 1981. Long-term persistence of the nuclear polyhedrosis virus of the Douglas-Fir Tussock moth, Orgyia pseudotsugata (Lepidoptera: Lymantriidae), in forest soil. Environmental Entomology 10(2): 254-255.

Tomalski, M.D. & Miller, L.K. 1991. Insect paralysis by baculovirus-mediated expression of a mite neurotoxin gene. Nature 352(6330): 82-85.

Wan, H., Zhang, Y., Zhao, X., Ji, J., You, H. & Li, J. 2015. Enhancing the insecticidal activity of recombinant baculovirus by expressing a growth-blocking peptide from the beet armyworm Spodoptera exigua. Journal of Asia-Pacific Entomology 18(3): 535-539.

Wood, H.A. & Granados, R.R. 1991. Genetically engineered baculoviruses as agents for pest control. Annual Review of Microbiology 45: 69-87.

Yang, S., Zhao, L., Ma, R., Fang, W., Hu, J., Lei, C. & Sun, X. 2017. Improving baculovirus infectivity by efficiently embedding enhancing factors into occlusion bodies. Applied and Environmental Microbiology 83(14): e00595-17.

*Pengarang untuk surat-menyurat; email: faridjohan@usm.my