Azadiraktin Üzerine Genel Bir Değerlendirme

Tarımsal üretimde ürün kayıplarını azaltmak amacıyla, zararlı böceklerle mücadelede pratik ve etkili alternatif yöntemler geliştirilmedikçe pestisitlerin kullanımı günümüzde olduğu gibi gelecekte de devam edecektir. Ancak, sentetik pestisitlerin çevre ve insan sağlığı üzerindeki olumsuz etkileriyle ilgili farkındalığın artması ve zararlı böceklerin kullanılan pestisitlere karşı direnç (özellikle çapraz direnç) geliştirmesi alternatif mücadele yöntemlerine ya da düşük riskli pestisit arayışlarına neden olmaktadır. Çeşitli alternatifler arasında da özellikle allelokimyasallar olarak adlandırılan organik bitki türevi bileşiklere olan ilgi yeniden artmıştır. Günümüzde, Hint neem ağacının neem tohumundan elde edilen bir tetranortriterpenoid olan azadiraktin [Azadirachta indica A. Juss (Meliaceae)], ticarileştirilen önde gelen biyopestisitlerden biridir. Ayrıca zirai mücadelede kullanılan azadiraktin dünya çapında en başarılı botanik pestisit olmaya da devam etmektedir. Azadiraktinin, biyolojik mücadele etmenleri olan predatörlere ve parazitoitlere karşı düşük toksisiteye ve az kalıntı özelliğine sahip olduğu bilinmektedir. Bunun yanı sıra zararlı böcekler üzerinde güçlü bir beslenme engelleyici ve böcek büyüme düzenleyici özellik de göstermektedir. Bu derleme, azadiraktinin kökenli insektisitleri bütün yönleriyle ele almıştır.

Anahtar Kelimeler:

azadiraktin, insektisit, böcek, mücadele

An Overview of Azadiractin

In order to reduce crop losses in agricultural production, the use of pesticides will continue in the future as it is today, unless practical and effective alternative methods are developed to control pests. However, the increasing awareness of the negative effects of conventional pesticides on the environment and human health and the development of resistance (especially cross-resistance) of pests to the pesticides used, lead to the search for alternative control methods or low-risk pesticides. Among the various alternatives, there has been a renewed interest in organic plant-derived compounds, especially so-called allelochemicals. Today, azadirachtin [Azadirachta indica A. Juss (Meliaceae)], a tetranortriterpenoid derived from the neem seed of the Indian neem tree, is one of the leading commercialized biopesticides. It also remains the most successful botanical pesticide used in agricultural control worldwide. Azadirachtin has low toxicity and low residues against biological control agents such as predators and parasitoids. It also exhibits strong antifeedant and insect growth regulator effects on insect pests. This review covers all aspects of azadirachtin-based insecticides.

Keywords:

azadirachtin , insecticide, insect, control,

PDF

___

Aarthy, T., Mulani, F.A., Pandreka, A., Kumar, A., Nandikol, S.S., Haldar, S. and Thulasiram, H.V. (2018). Tracing biosynthetic origin of limonoids and their functional groups through stable isotope labeling and inhibition in neem tree (Azadirachta indica) cell suspension. BMC Plant Biolgy, 18, 230.
Ahmad, S., Ansari, M.S. and Muslim, M. (2015). Toxic effects of neem based insecticides on the fitness of Helicoverpa armigera (Hübner). Crop Protection, 68, 72–78.
Aktar, M.W., Sengupta, D. and Chowdhury, A. (2009). Impact of pesticides use in agriculture their benefits and hazards. Interdisciplinary Toxicology, 2, 1–12.
Aribi, N., Oulhaci, M.C., Kilani-Morakchi, S., Sandoz, J.C., Kaiser, L., Denis, B. and Joly, D. (2017). Azadirachtin impact on mate choice, female sexual receptivity and male activity in Drosophila melanogaster (Diptera: Drosophilidae). Pesticide Biochemistry and Physiology, 143, 95–101.
Aribi, N., Denis, B., Kilani-Morakchi, S. and Joly, D. (2020). L’azadirachtine, un pesticide naturel aux effets multiples. Médecine Sciences, 36, 44–49.
Asaduzzaman, M., Shim, J.K., Lee, S. and Lee, K.Y. (2016). Azadirachtin ingestion is lethal and inhibits expression of ferritin and thioredoxin peroxidase genes of the sweetpotato whitefly Bemissia tabaci. Journal of Asia-Pacific Entomology, 19, 1–4.
Baumler, R. and Potter, D.A. (2007). Knockdown, residual, and antifeedant activity of pyrethroids and home landscape bioinsecticides against japanese beetles (Coleoptera: Scarabaeidae) on linden foliage. Journal of Economic Entomology, 100, 541–548.
Benuzzi, M. and Ladurner, E. (2018). Plant protection tools in organic farming. Handbook of Pest Management in Organic Farming, 24–59.
Bernardes, R.C., Barbosa, W.F., Martins, G.F. and Lima, M.A.P. (2018). The reduced-risk insecticide azadirachtin poses a toxicological hazard to stingless bee Partamona helleri (Friese, 1990) queens. Chemosphere, 201, 550–556.
Bezzar-Bendjazia, R., Kilani-Morakchi, S. and Aribi, N. (2016). Larval exposure to azadirachtin affects fitness and oviposition site preference of Drosophila melanogaster. Pesticide Biochemistry and Physiology, 133, 85–90.
Bezzar-Bendjazia, R., Kilani-Morakchi, S., Ferdenache, M. and Aribi, N. (2017). Azadirachtin induces larval avoidance and antifeeding by disruption of food intake and digestive enzymes in Drosophila melanogaster (Diptera: Drosophilidae). Pesticide Biochemistry and Physiology, 143, 135–140.
Bomford, M.K. and Isman, M.B. (1996). Desensitization of fifth instar Spodoptera litura to azadirachtin and neem. Entomologia Experimentalis et Applicata, 81, 307–313.
Boulahbel, B., Aribi, N., Kilani-Morakchi, S. and Soltani, N. (2015). Insecticidal activity of azadirachtin on Drosophila melanogaster and recovery of normal status by exogenous 20-hydroxyecdysone. African Entomology, 23, 224–233.
Cantrell, C.L., Dayan, F.E. and Duke, S.O. (2012). Natural products as sources for new pesticides. Journal of Natural Products, 75, 1231–1242.
Capinera, J.L. and Froeba, J.G. (2007). Behavioral responses of Schistocerca americana (Orthoptera: Acrididae) to azadirex (neem)-treated host plants. Journal of Economic Entomology, 100, 117–122.
Carson, R. (1962). Silent Spring. Houghton Mifflin, 1st Ed, , 368p.,Boston, USA.
Caubet, Y., Jaisson, P., and Lenoir, A. (1992). Preimaginal induction of adult behaviour in insects. Quarterly Journal of Experimental Psychology, 44, 165–178.
Celestino, D., Braoios, G.I., Ramos, R.G., Gontijo, L.M. and Guedes, R.N.C. (2014). Azadirachtin-mediated reproductive response of the predatory pirate bug Blaptostethus pallescens. Biological Control, 59, 697–705.
Chandler, D., Bailey, A.S., Tatchell, G.M., Davidson, G., Greaves, J. and Grant, W.P. (2011). The development, regulation and use of biopesticides for integrated pest management. Philosophical Transactions of the Royal Society B, 366, 1987–1998.
Charleston, D.S., Kafir, R., Dicke, M. and Vet, L.E.M. (2006). Impact of botanical extracts derived from Melia azedarach and Azadirachta indica on populations of Plutella xylostella and its natural enemies: a field test of laboratory findings. Biological Control, 39, 105–114.
Chaudhary, S., Kanwar, R.K., Sehgal, A., Cahill, D.M., Barrow, C.J., Sehgal, R. and Kanwar, J.R. (2017). Progress on Azadirachta indica based biopesticides in replacing synthetic toxic pesticides. Frontiers in Plant Science, 8, 610.
Chen, J., Fan, X., Zhu, J., Song, L., Li, Z., Lin, F., Yu, R., Xu, H. and Zi, J. (2018). Limonoids from seeds of Azadirachta indica A. Juss. and their cytotoxic activity. Acta Pharmaceutica Sinica B, 8, 639–644.
Cordeiro, E.M.G., Corrêa, A.S., Venzon, M. and Guedes, R.N.C. (2010). Insecticide survival and behavioral avoidance in the laccewings Chrysoperla externa and Ceraeochrysa cubana. Chemosphere, 81, 1352–1357.
Dai, W., Li, Y., Zhu, J., Ge, L.q., Yang, G.Q. and Liu, F. (2019). Selectivityand sublethal effects of some frequently–used biopesticides on the predator Cyrtorhinus lividipennis reuter (Hemiptera: Miridae). Journal of Integrative Agriculture, 18, 124–133.
Damalas, C.A. and Koutroubas, S.D. (2018). Current statuts and recent developments in biopesticide use. Agriculture, 8, 13.
Das, R.K., Sarma, S., Brar, S.K. and Verma, M. (2014). Nanoformulation of insecticides: novel products. Journal of Biofertilizers and Biopesticides, 5, e120.
Dawkar, V.V., Barage, S.H., Barbole, R.S., Fatangare, A., Grimalt, S., Haldar, S., Heckel, D.G., Gupta, V.S., Thulasiram, H.V., Svatoš, A. and Giri, A.P. (2019). Azadirachtin-A from Azadirachta indica ımpacts multiple biological targets in cotton bollworm Helicoverpa armigera. ACS Omega, 4(5), 9531-9541.
Delventhal, R. and Carlson, J. (2016). Bitter taste receptors confer diverse functions to neurons. eLife, 5, e11181. Deravel, J., Krier, F. and Jacques, Ph. (2014). Les biopesticides, alternatives aux produits phytosanitaires chimiques (synthèse bibliographique). Biotechnology, Agronomy and Society and Environment, 18, 220–232.
Dhra, G., Ahmad, M., Kumar, J. and Patanjali, P.K. (2018). Mode of action of azadirachtin: a natural insecticide. International Research Journal, 7, 41–46.
Duarte, J.P., Redaelli, L.R., Silva, C.E. and Jahnke, S.M. (2020). Effect of Azadirachta indica (Sapindales: Meliaceae) oil on the ımmune system of Spodoptera frugiperda (Lepidoptera: Noctuidae) Immatures. Journal of Insect Science, 20, 3-17.
Dubrovsky, E.B. (2005). Hormonal cross talk in insect development. Trends in Endocrinology and Metabolism, 16, 6–11.
Er, A., Taşkiran, D. and Sak, O. (2017). Azadirachtin-induced effects on various life history traits and cellular immune reactions of Galleria mellonella (Lepidoptera: Pyralidae). Archives of Biological Sciences, 69, 35–344.
Feng, R. and Isman, M.B. (1995). Selection for resistance to azadirachtin in the green peach aphid Myzus persicae. Experientia, 51, 831–833.
Ferdenache, M., Bezzar-Bendjezia, R., Marion Poll, F. and Kilani-Morakchi, S. (2019). Transgenerational effects from single larval exposure to azadirachtin on life history and behavior traits of Drosophila melanogaster. Scientific Reports, 9, 17015.
Francesena, N. and Schneider, M.I. (2018). Selectivity assessment of two biorational insecticides, azadirachtin and pyriproxyfen, in comparison to a neonicotinoid, acetamiprid, on pupae and adults of a Neotropical strain Eretmocerus mundus mercet. Chemosphere, 206, 349–358.
Garcia, E.S., Luz, N., Azambuja, P. and Rembold, H. (1990). Azadirachtin depresses the release of prothoracicotropic hormone in Rhodnius prolixus larvae: evidence from head transplantations. Journal of Insect Physiology, 36, 679–682.
Ghazawi, N.A., El-Shranoubi, E.D., El-Shazly, M.M. and Abdel Rahman, K.M. (2007). Effects of azadirachtin on mortality rate and reproductive system of the grasshopper Heteracris littoralis Ramb (Orthoptera: Acrididae). Journal of Orthopaedic Research, 16, 57–65.
Gupta, S.C., Prasad, S., Tyagi, A.K., Kunnumakkara, A.B. and Aggarwal, B.B. (2017). Neem (Azadirachta indica): an indian traditional panacea with modern molecular basis. Phytomedicine, 34, 14–20.
Haddi, K., Turchen, L.M., Viteri Jumbo, L.O., Guedes, R.N.C., Pereira, E.J.G., Aguiar, R.W.S. and Oliveira, E.E. (2020). Rethinking biorational insecticides for pest management: unintended effects and consequences. Pest Management Science, 76, 2286–2293.
Hansen, D.J., Cuomo, J., Khan, M., Gallagher, R.T. and Ellenberge, W.P. (1993). Advances in neem and azadirachtin chemistry and bioactivity. Natural and Engineered Pest Management Agents ACS Symposium Series, 551, 103–129.
Helps, J.C., Paveley, N.D. and Bosch, F. (2017). Identifying circumstances under which high insecticide dose increases or decreases resistance selection. Journal of Theoretical Biology, 7, 153–167.
Hikal, W.M., Baeshen, R.S. and Said-Al, A.H.A. (2017). Botanical insecticide as simple extractives for pest control. Cogent Biology, 3, 1404274.
Huang, Z., Shi, P., Chen, G. and Du, J. (2007). Effects of azadirachtin on hemolymph protein expression in Ostrinia furnacalis (Lepidoptera: Crambidae). Annals of the Entomological Society of America, 100, 245–250.
Iqbal, N., Kumar, N., Saini, M. K., Dubey, S., Agrawal, A. and Kumar, J. (2020). Role of high shear mixing in improving stability and bio-efficacy of botanical oil in water formulation for early stage mosquito eradication. Helion, 6, e03380.
Iqbal, N., Agrawal, A. and Kumar, J. (2021). An effervescent generated tablet for rapid control of mosquito problem in early stages from different breeding sites. Arabian Journal of Chemistry, 14 (4), 103082.
Isman, M.B. (2006). Botanical insecticides, deterrents, and repellents in modern agriculture and an increasingly regulated world. Annual Review of Entomology, 51, 45–66.
Isman, M.B. and Grieneisen, M.L. (2014). Botanical insecticide research: many publications, limited useful data. Trends in Plant Science, 19, 140–145.
Jars, E., Neupane, D. and London, L. (2018). Pesticide poisonings in low- and middle-income countries. Environmental Health Insights, 12, 1–3.
Jauch, J. (2008). Total synthesis of azadirachtin-finally completed after 22 years. Angewandte Chemie International Edition, 47, 34–37.
Jesser, E., Yeguermanb, C., Gilia, V., Santillana, G., Murrayc, A.P., Dominic, C. and Gonzalez, J.O.W. (2020). Optimization and characterization of essential oil nanoemulsions using ultrasound for new ecofriendly insecticides. ACS Sustainable Chemistry and Engineering, 8, 7981–7992.
Kala, S., Naik, S.N., Patanjali, P.K. and Sogan, N. (2019). Neem oil water dispersible tablet as effective larvicide, ovicide and oviposition deterrent against Anopheles culicifacies. South African Journal of Botany, 123, 387–392.
Karuppuchamy, P. and Venugopal, S. (2016). Integrated pest management. Ecofriendly Pest Management for Food Security, Academic Press, 651–684, San Diego.
Kavita, Sharma, S.K. and Sood, A.K. (2023). Repellent and deterrent effects of natural products against diamondback moth, Plutella xylostella (Linnaeus). Research Square, PPR595173.
Khater, H.F. (2012). Prospects of botanical biopesticides in insect pest management. Pharmacologia, 3, 641–656.
Khosravi, R. and Sendi, J.J. (2013). Effect of neem pesticide (achook) on midgut enzymatic activities and selected biological compounds in the hemolymph of lesser mulberry pyralid, Glyphodes pyloalis walker (Lepidoptera: Pyralidae). Journal of Plant Protection, 5, 238–247.
Kilani-Morakchi, S., Bezzar-Bendjazia, R., Ferdenache, M. and Aribi, N. (2017). Preimaginal exposure to azadirachtin affects food selection and digestive enzymes in adults of Drosophila melanogaster (Diptera: Drosophilidae). Pesticide Biochemistry and Physiology, 140, 58–64.
Kraus, W., Bokel, M., Klenk, A. and Pöhn, H. (1985). The structure of azadirachtin and 22,23-dihydro-23β-methoxyazadirachtin. Tetrahedron Leters, 26, 6435–6438.
Kumar, P. and Poehling, H.M. (2007). Effects of azadirachtin, abamectin, and spinosad on sweetpotato white (Homoptera: Aleyrodidae) on tomato plants under laboratory and greenhouse conditions in the humid tropics. Journal of Economic Entomology, 100, 411–420.
Kumar, S. (2015). Biopesticide: an environment friendly pest management strategy. Journal of Biofertilizers and Biopesticides, 6, 1.
Kumar, D., Rahal, A. and Malik, J. K. (2016). Neem extract: nutraceuticals efficcy, safety and toxicity. Academic Press. 585–597, London.
Lee, Y., Kim, S. and Montell, C. (2010). Avoiding DEET through insect gustatory receptors. Neuron 67, 555–561. Lin, S., Li, S., Liu, Z., Zhang, L., Wu, H., Cheng, D. and Zhang, Z. (2021). Using azadirachtin to transform Spodoptera frugiperda from pest to natural enemy. Toxins (Basel), 13(8), 541.
Liu, P.F., Wang, W., Ling, X., Lu, Q., Zhang, J., He, R. and Hang, C. (2019). Regulation hormone-related genes in Ericerus pela (Hemiptera: Coccidae) for dimorphic metamorphosis. Journal of Insect Science, 19, 16. Luo, P., Qin, D., Wu, H., Zheng, Q., Zhau, W., Ye, C., Shen, S., Huang, S., Cheng, D. and Zhang, Z. (2023).
Azadirachtin affected the intestinal structure and microbiota of adult Harmonia axyridis (Coleoptera: Coccinellidae) while controlling Spodoptera frugiperda (Lepidoptera: Noctuidae). Journal of Pest Science, 96, 973–988.
Marco, M. P., Pascual, N., Bellès, X., Camps, F. and Messeguer, A. (1990). Ecdysteroid depletion by azadirachtin in Tenebrio molitor pupae. Pesticide Biochemistry and Physiology, 38, 60–65.
Martinez, S.S. and van Emden, H.F. (1999). Sublethal concentrations of azadirachtin affect food intake, conversion efficiency and feeding behaviour of Spodoptera littoralis (Lepidoptera: Noctuidae). Bulletin of Entomological Research, 89, 65–71.
Mishra, R.K., Bohra, A., Kamaal, N., Kumar, K., Gandhi, K., Sujayanand, G.K., Saabale, P.R., Satheesh Naik, S.J., Sarma, B.K., Kumar, D., Mishra, M., Srivastava, D.K. and Singh, N.P. (2018). Utilization of biopesticides as sustainable solutions for management of pests in legume crops: achievements and prospects. Egyptian Journal of Biological Pest Control, 28(1), 3.
Mordue, L. A. J. and Blackwell, A. (1993). Azadirachtin: an update. Journal of Insect Physiology, 39, 903–924.
Mordue, A.J. and Nisbet, A.J. (2000). Azadirachtin from the neem tree (Azadirachta indica): its actions against insects. Anais da Sociedade Entomológica do Brasil, 29, 615–632.
Mordue, A.J., Morgan, E.D., and Nisbet, A. J. (2010). Azadirachtin, a natural product in insect control, in Insect Control: Biological and synthetic agents. Elsevier BV. All Rights Reserved, 185–203.
Morgan, E.D. (2009). Azadirachtin, a scientific goldmine. Bioorganic and Medicinal Chemistry, 17, 4096–4105.
Nagini, S. (2014). Neem limonoids as anticancer agents: modulation of cancer hallmarks and oncogenic signaling. The Enzymes, 36, 131–147.
Nijhout H.F. (1994). Insect Hormones. Princeton University Press, Princeton, NJ, 280 pp.
Olson, S. (2015). An analysis of the biopesticide market now and where it is going. Outlooks on Pest Management, 26, 203–206.
Oulhaci, M.C., Denis, B., Kilani-Morakchi, S., Sandoz, J. C., Kaiser, L., Joly, D. and Aribi, N. (2018). Azadirachtin effects on mating success, gametic abnormalities and progeny survival in Drosophila melanogaster (Diptera). Pest Management Science, 74,174–180.
Pasquoto-Stigliani, T., Campos, E.V.R., Oliveira, J.L., Silva, C.M.G., Bilesky-José, N., Guilger, M., Trost, J., Oliveira, H.C., Moreira, R.S.M., Fraceto, L.F. and Lima, R. (2017). Nanocapsules containing neem (AzadirachtaIndica) oil: development, characterization, and toxicity evaluation. Scientific Reports, 7, 5929.
Pavela, R. (2016). History, presence and perspective of using plant extracts as commercial botanical insecticides and farm products for protection against insects – a review. Plant Protection Science, 52, 229–241.
Pener, M.P. and Dhadialla, T.S. (2012). An overview of insect growth disruptors; applied aspects. Advances in Insect Physiology, 43, 1–162.
Popp, J., Petö, K. and Nagy, J. (2013). Pesticide productivity and food security: a review. Agronomy for Sustainable Development, 33, 243–255.
Qin, D., Zhang, P., Zhou, Y., Liu, B. and Zhang, Z. (2020). Antifeeding effects of azadirachtin on the fifth instar Spodoptera litura larvae and the analysis of azadirachtin on target sensilla around mouthparts. Archives of Insect Biochemistry and Physiology, 103, 5318.
Riba, M., Marti, J. and Sans, A. (2003). Influence of azadirachtin on development and reproduction of Nezara viridula L, (Het., Pentatomidae). Journal of Applied Entomology, 127, 37–41.
Schmutterer, H. (1990). Properties and potential of natural pesticides from the neem tree, Azadirachta indica. Annual Review of Entomology, 35, 271–297.
Schmutterer, H. (1995). The Neem Tree: Source of Unique Natural Products for Integrated Pest Management, Medicine, Industry and Other Purposes. Wenheim VCH, 1–696.
Schmutterer, H. (2002). The Neem tree and other meliaceous plants. Neem Foundation, 2nd Ed, 719p., Mumbai, India.
Seugling, J., Kuhnen, S., de Barros, G.P., Velerinho, M.B., Mazzarino, L. and Bricarello, P.A. (2019). Development of Baccharis dracunculifolia (Asteraceae) essential oil nanoemulsion and its biological activity on pre-pupae of Cochliomyia hominivorax (Diptera: Calliphoridae). Journal of Pharmacy and Pharmacology, 7, 293–308.
Shanmugapriya, S., Jeya Sundara Sharmila, D., Karthikeyan, G. and Subramanian, K.S. (2019). Bioassay of azadirachtin nanofomulation against bemisia tabaci, the vector of mungbean yellow mosaic virus. Madras Agricultural Journal, 106, 522–527.
Shannag, H.K., Capinera, J.L. and Freihat, N.M. (2015). Effects of neem-based insecticides on consumption and utilization of food in larvae of Spodoptera eridania (Lepidoptera: Noctuidae). Journal of Insect Science, 15:152.
Shu, B., Yu, H., Li, Y., Zhong, H., Li, X., Cao, L. and Lin, Jintian (2020). Identification of azadirachtin responsive genes in Spodoptera frugiperda larvae based on RNA-seq. Pesticide Biochemistry and Physiology, 172, 104745.
Shutterstoc, (2023). Neem ağacı ve moleküler yapısı. https://www.shutterstock.com/. Erişim tarihi: 10.02.2023 Skendžić, S., Zovko, M., Živković, I. P., Lešić, V. and Lemić, D. (2021). The impact of climate change on agricultural ınsect pests. Insects, 12(5), 440.
Smith, S.L. and Mitchell, M.J. (1988). Effects of azadirachtin on insect cytochrome P-450 dependent ecdysone 20-monooxygenase activity. Biochemical and Biophysical Research Communications, 154, 559–563.
Sun, R., Cui, G., Chen, Y., Shu, B., Zhong, G. and Yi, X. (2018). Proteomic profiling analysis of male infertility in Spodoptera litura larvae challenged with azadirachtin and its potential regulated pathways in the following stages. Proteomics, 18, e1800192.
Thakora, Y. (2006). The biopesticide market for global agricultural use. Industrial Biotechnolology, 2, 194–208.
Vivekananthan, T. and Selvisabhanayakam, S.N. (2014). Histopathological observations on testes of adult blister beetle, Mylabris indica (thunberg) (Coleoptera: Meloidae) treated with neem. Journal of the Entomological Research Society, 38, 45–52.
Yu, H., Yang, X., Dai, J., Li, Y., Veeran, S., Lin, J. and Shu, B. (2023). Effects of azadirachtin on detoxification-related gene expression in the fat bodies of the fall armyworm, Spodoptera frugiperda. Environmental Science and Pollution Research, 30, 42587–4259.
Zhao, J., Zhou, Y., Li, X., Cai, W. and Hua, H. (2017). Silencing of juvenile hormone epoxide hydrolase gene (Nljheh) enhances short wing formation in a macropterous strain of the brown planthopper, Nilaparvata lugens. Journal of Insect Physiology, 102, 18–26.