BIOINSECTICIDES AS FUTURE MAINSTREAM PEST CONTROL AGENTS: OPPORTUNITIES AND CHALLENGES
Mingbo QU, Hans MERZENDORFER, Bernard MOUSSIAN, Qing YANG
BIOINSECTICIDES AS FUTURE MAINSTREAM PEST CONTROL AGENTS: OPPORTUNITIES AND CHALLENGES
•Wide use of botanical insecticides is limited by the availability of certain plants.
•Studies are needed to improve RNAi efficiency and to assess their safety risk.
•Microbial insecticides are promising, but they only control a narrow range of pests.
•Multitarget approach should be a promising strategy in future pest control.
•Nanoformulation could enhance stability and control the release of bioinsecticides.
Bioinsecticides are naturally-occurring substances from different sources that control insect pests. Ideal bioinsecticides should have low toxicity to non-target organisms. They should also be easily degraded in sewage treatment works and natural environments, highly effective in small quantities and affect target pests only. Public concerns about possible side-effects of synthetic pesticides have accelerated bioinsecticide research and development. However, to develop bioinsecticides into mainstream products, their high production costs, short shelf-life and often uncertain modes of action need to be considered. This review summarizes current progress on bioinsecticides which are categorized as biochemical insecticides and their derivatives, plant-incorporated protectants, and microbial bioinsecticides. The current constraints that prevent bioinsecticides from being widely used are discussed and future research directions are proposed.
biochemical insecticide / bioinsecticide / microbial bioinsecticides / plant-incorporated protectant / RNA insecticide
[1] |
Haddi K, Turchen L M, Viteri Jumbo L O, Guedes R N, Pereira E J, Aguiar R W, Oliveira E E. Rethinking biorational insecticides for pest management: unintended effects and consequences. Pest Management Science, 2020, 76(7): 2286–2293
CrossRef
Pubmed
Google scholar
|
[2] |
Bioinsecticides Market by Organism Type(Bacteria Thuringiensis, Beauveria Bassiana, and Metarhizium Anisopliae), Type (Microbials and Macrobials), Mode of Application, Formulation, Crop Type and Region-Global Trends & Forecast to 2025. MarketsandMarkets, 2020: 1–194
|
[3] |
Seiber J N, Coats J, Duke S O, Gross A D. Biopesticides: state of the art and future opportunities. Journal of Agricultural and Food Chemistry, 2014, 62(48): 11613–11619
CrossRef
Pubmed
Google scholar
|
[4] |
Dhadialla T S, Carlson G R, Le D P. New insecticides with ecdysteroidal and juvenile hormone activity. Annual Review of Entomology, 1998, 43(1): 545–569
CrossRef
Pubmed
Google scholar
|
[5] |
Jindra M, Bittova L. The juvenile hormone receptor as a target of juvenoid “insect growth regulators”. Archives of Insect Biochemistry and Physiology, 2020, 103(3): e21615
CrossRef
Pubmed
Google scholar
|
[6] |
Gregg P C, Del Socorro A P, Landolt P J. Advances in attract-and-kill for agricultural pests: beyond pheromones. Annual Review of Entomology, 2018, 63(1): 453–470
CrossRef
Pubmed
Google scholar
|
[7] |
Liang Y Y, Luo M, Fu X G, Zheng L X, Wei H Y. Mating disruption of chilo suppressalis from sex pheromone of another pyralid rice pest Cnaphalocrocis medinalis (Lepidoptera: Pyralidae). Journal of Insect Science, 2020, 20(3): 19
CrossRef
Pubmed
Google scholar
|
[8] |
Xu L, Xie Y, Na R, Li Q X. Mini-review: recent advances in the identification and application of sex pheromones of gall midges (Diptera: Cecidomyiidae). Pest Management Science, 2020, 76(12): 3905–3910
CrossRef
Pubmed
Google scholar
|
[9] |
Hassemer M J, Borges M, Withall D M, Pickett J A, Laumann R A, Birkett M A, Blassioli-Moraes M C. Development of pull and push-pull systems for management of lesser mealworm, Alphitobius diaperinus, in poultry houses using alarm and aggregation pheromones. Pest Management Science, 2019, 75(4): 1107–1114
CrossRef
Pubmed
Google scholar
|
[10] |
Gries R, Britton R, Holmes M, Zhai H, Draper J, Gries G. Bed bug aggregation pheromone finally identified. Angewandte Chemie International Edition, 2015, 54(4): 1135–1138
CrossRef
Pubmed
Google scholar
|
[11] |
King G F, Hardy M C. Spider-venom peptides: structure, pharmacology, and potential for control of insect pests. Annual Review of Entomology, 2013, 58(1): 475–496
CrossRef
Pubmed
Google scholar
|
[12] |
Gurevitz M, Karbat I, Cohen L, Ilan N, Kahn R, Turkov M, Stankiewicz M, Stühmer W, Dong K, Gordon D. The insecticidal potential of scorpion beta-toxins. Toxicon, 2007, 49(4): 473–489
CrossRef
Pubmed
Google scholar
|
[13] |
Casida J E, Durkin K A. Neuroactive insecticides: targets, selectivity, resistance, and secondary effects. Annual Review of Entomology, 2013, 58(1): 99–117
CrossRef
Pubmed
Google scholar
|
[14] |
Copping L G, Menn J. J. Biopesticides: a review of their action, applications and efficacy. Pest Management Science, 2000, 56(8): 651–676
CrossRef
Google scholar
|
[15] |
Matsuda K. Okaramines and other plant fungal products as new insecticide leads. Current Opinion in Insect Science, 2018, 30: 67–72
CrossRef
Pubmed
Google scholar
|
[16] |
Jouzani G S, Valijanian E, Sharafi R. Bacillus thuringiensis: a successful insecticide with new environmental features and tidings. Applied Microbiology and Biotechnology, 2017, 101(7): 2691–2711
CrossRef
Pubmed
Google scholar
|
[17] |
Pardo-López L, Soberón M, Bravo A. Bacillus thuringiensis insecticidal three-domain Cry toxins: mode of action, insect resistance and consequences for crop protection. FEMS Microbiology Reviews, 2013, 37(1): 3–22
CrossRef
Pubmed
Google scholar
|
[18] |
Then C, Bauer-Panskus A. Possible health impacts of Bt toxins and residues from spraying with complementary herbicides in genetically engineered soybeans and risk assessment as performed by the European Food Safety Authority EFSA. Environmental Sciences Europe, 2017, 29(1): 1
CrossRef
Pubmed
Google scholar
|
[19] |
Bakkali F, Averbeck S, Averbeck D, Idaomar M. Biological effects of essential oils–a review. Food and Chemical Toxicology, 2008, 46(2): 446–475
|
[20] |
da Silva B C, Melo D R, Franco C T, Maturano R, Fabri R L, Daemon E. Evaluation of eugenol and (E)-cinnamaldehyde insecticidal activity against larvae and pupae of Musca domestica (Diptera: Muscidae). Journal of Medical Entomology, 2020, 57(1): 181–186
Pubmed
|
[21] |
Regnault-Roger C, Vincent C, Arnason J T. Essential oils in insect control: low-risk products in a high-stakes world. Annual Review of Entomology, 2012, 57(1): 405–424
CrossRef
Pubmed
Google scholar
|
[22] |
Isman M B. Botanical insecticides, deterrents, and repellents in modern agriculture and an increasingly regulated world. Annual Review of Entomology, 2006, 51(1): 45–66
CrossRef
Pubmed
Google scholar
|
[23] |
Isman M B. Botanical insecticides in the twenty-first century-fulfilling their promise? Annual Review of Entomology, 2020, 65(1): 233–249
CrossRef
Pubmed
Google scholar
|
[24] |
Benelli G, Canale A, Toniolo C, Higuchi A, Murugan K, Pavela R, Nicoletti M. Neem (Azadirachta indica): towards the ideal insecticide? Natural Product Research, 2017, 31(4): 369–386
CrossRef
Pubmed
Google scholar
|
[25] |
Fernandes S R, Barreiros L, Oliveira R F, Cruz A, Prudêncio C, Oliveira A I, Pinho C, Santos N, Morgado J. Chemistry, bioactivities, extraction and analysis of azadirachtin: state-of-the-art. Fitoterapia, 2019, 134: 141–150
CrossRef
Pubmed
Google scholar
|
[26] |
Morgan E D. Azadirachtin, a scientific gold mine. Bioorganic & Medicinal Chemistry, 2009, 17(12): 4096–4105
CrossRef
Pubmed
Google scholar
|
[27] |
Ujvary I. Nicotine and Other Insecticidal Alkaloids. In: Yamamoto I, Casida J E, eds. Nicotinoid Insecticides and the Nicotinic Acetylcholine Receptor.Tokyo: Springer, 1999
|
[28] |
Copping L G, Duke S O. Natural products that have been used commercially as crop protection agents. Pest Management Science, 2007, 63(6): 524–554
CrossRef
Pubmed
Google scholar
|
[29] |
James C. Executive Summary. Global status of commercialized biotech/GM crops. ISAAA Brief, 2015, 51
|
[30] |
Schnepf E, Crickmore N, Van Rie J, Lereclus D, Baum J, Feitelson J, Zeigler D R, Dean D H. Bacillus thuringiensis and its pesticidal crystal proteins. Microbiology and Molecular Biology Reviews, 1998, 62(3): 775–806
CrossRef
Pubmed
Google scholar
|
[31] |
Syed T, Askari M, Meng Z, Li Y, Abid M A, Wei Y, Guo S, Liang C, Zhang R. Current insights on vegetative insecticidal proteins (Vip) as next generation pest killers. Toxins, 2020, 12(8): 522
CrossRef
Pubmed
Google scholar
|
[32] |
Adeyinka O S, Riaz S, Toufiq N, Yousaf I, Bhatti M U, Batcho A, Olajide A A, Nasir I A, Tabassum B. Advances in exogenous RNA delivery techniques for RNAi-mediated pest control. Molecular Biology Reports, 2020, 47(8): 6309–6319
CrossRef
Pubmed
Google scholar
|
[33] |
Liu S, Jaouannet M, Dempsey D A, Imani J, Coustau C, Kogel K H. RNA-based technologies for insect control in plant production. Biotechnology Advances, 2020, 39: 107463
CrossRef
Pubmed
Google scholar
|
[34] |
Kesho A. Microbial bio-pesticides and their use in integrated pest management. Chemical and Biomolecular Engineering, 2020, 5(1): 26–34
CrossRef
Google scholar
|
[35] |
Lacey L A, Grzywacz D, Shapiro-Ilan D I, Frutos R, Brownbridge M, Goettel M S. Insect pathogens as biological control agents: back to the future. Journal of Invertebrate Pathology, 2015, 132: 1–41
CrossRef
Pubmed
Google scholar
|
[36] |
Moscardi F. Assessment of the application of baculoviruses for control of Lepidoptera. Annual Review of Entomology, 1999, 44(1): 257–289
CrossRef
Pubmed
Google scholar
|
[37] |
Sharma A, Sandhi R K, Reddy G V P. A review of interactions between insect biological control agents and semiochemicals. Insects, 2019, 10(12): 439
CrossRef
Pubmed
Google scholar
|
[38] |
Khambay B P S, Jewess P J. Pyrethroids. In: Gilbert L I, Gill S, eds. Insect Control, 1st Edition.London: Academic Press, 2010, 1–29
|
[39] |
Miyazawa M, Fujioka J, Ishikawa Y. Insecticidal compounds from Phellodendron amurense active against Drosophila melanogaster. Journal of the Science of Food and Agriculture, 2002, 82(8): 830–833
CrossRef
Google scholar
|
[40] |
Ainge G D, Lorimer S D, Gerard P J, Ruf L D. Insecticidal activity of huperzine A from the New Zealand clubmoss, Lycopodium varium. Journal of Agricultural and Food Chemistry, 2002, 50(3): 491–494
CrossRef
Pubmed
Google scholar
|
[41] |
Crickmore N, Berry C, Panneerselvam S, Mishra R, Connor T R, Bonning B C. A structure-based nomenclature for Bacillus thuringiensis and other bacteria-derived pesticidal proteins. Journal of Invertebrate Pathology, 2020: 107438
CrossRef
Pubmed
Google scholar
|
[42] |
Campbell P M, Reiner D, Moore A E, Lee R Y, Epstein M M, Higgins T J V. Comparison of the α-amylase inhibitor-1 from common bean (Phaseolus vulgaris) varieties and transgenic expression in other legumes—post-translational modifications and immunogenicity. Journal of Agricultural and Food Chemistry, 2011, 59(11): 6047–6054
CrossRef
Pubmed
Google scholar
|
[43] |
Vandenborre G, Smagghe G, Van Damme E J M. Plant lectins as defense proteins against phytophagous insects. Phytochemistry, 2011, 72(13): 1538–1550
CrossRef
Pubmed
Google scholar
|
[44] |
Gatehouse J A. Prospects for using proteinase inhibitors to protect transgenic plants against attack by herbivorous insects. Current Protein & Peptide Science, 2011, 12(5): 409–416
CrossRef
Pubmed
Google scholar
|
[45] |
Arakane Y, Muthukrishnan S. Insect chitinase and chitinase-like proteins. Cellular and Molecular Life Sciences, 2010, 67(2): 201–216
CrossRef
Pubmed
Google scholar
|
[46] |
Cooper S G, Douches D S, Grafius E J. Combining engineered resistance, avidin, and natural resistance derived from Solanum chacoense bitter to control Colorado potato beetle (Coleoptera: Chrysomelidae). Journal of Economic Entomology, 2009, 102(3): 1270–1280
CrossRef
Pubmed
Google scholar
|
[47] |
Baum J A, Bogaert T, Clinton W, Heck G R, Feldmann P, Ilagan O, Johnson S, Plaetinck G, Munyikwa T, Pleau M, Vaughn T, Roberts J. Control of coleopteran insect pests through RNA interference. Nature Biotechnology, 2007, 25(11): 1322–1326
CrossRef
Pubmed
Google scholar
|
[48] |
Li H, Khajuria C, Rangasamy M, Gandra P, Fitter M, Geng C, Woosely A, Hasler J, Schulenberg G, Worden S, McEwan R, Evans C, Siegfried B, Narva K E. Long dsRNA but not siRNA initiates RNAi in western corn rootworm larvae and adults. Journal of Applied Entomology, 2015, 139(6): 432–445
CrossRef
Google scholar
|
[49] |
Thakur N, Upadhyay S K, Verma P C, Chandrashekar K, Tuli R, Singh P K. Enhanced whitefly resistance in transgenic tobacco plants expressing double stranded RNA of v-ATPase A gene. PLoS One, 2014, 9(3): e87235
CrossRef
Pubmed
Google scholar
|
[50] |
Cruz J, Mané-Padrós D, Bellés X, Martín D. Functions of the ecdysone receptor isoform-A in the hemimetabolous insect Blattella germanica revealed by systemic RNAi in vivo. Developmental Biology, 2006, 297(1): 158–171
CrossRef
Pubmed
Google scholar
|
[51] |
Zhu J Q, Liu S, Ma Y, Zhang J Q, Qi H S, Wei Z J, Yao Q, Zhang W Q, Li S. Improvement of pest resistance in transgenic tobacco plants expressing dsRNA of an insect-associated gene EcR. PLoS One, 2012, 7(6): e38572
CrossRef
Pubmed
Google scholar
|
[52] |
Hussain T, Aksoy E, Çalışkan M E, Bakhsh A. Transgenic potato lines expressing hairpin RNAi construct of molting-associated EcR gene exhibit enhanced resistance against Colorado potato beetle (Leptinotarsa decemlineata, Say). Transgenic Research, 2019, 28(1): 151–164
CrossRef
Pubmed
Google scholar
|
[53] |
Bolognesi R, Ramaseshadri P, Anderson J, Bachman P, Clinton W, Flannagan R, Ilagan O, Lawrence C, Levine S, Moar W, Mueller G, Tan J, Uffman J, Wiggins E, Heck G, Segers G. Characterizing the mechanism of action of double-stranded RNA activity against western corn rootworm (Diabrotica virgifera virgifera LeConte). PLoS One, 2012, 7(10): e47534
CrossRef
Pubmed
Google scholar
|
[54] |
Tan J, Levine S L, Bachman P M, Jensen P D, Mueller G M, Uffman J P, Meng C, Song Z, Richards K B, Beevers M H. No impact of DvSnf7 RNA on honey bee (Apis mellifera L.) adults and larvae in dietary feeding tests. Environmental Toxicology and Chemistry, 2016, 35(2): 287–294
CrossRef
Pubmed
Google scholar
|
[55] |
Mamta , Reddy K R, Rajam M V. Targeting chitinase gene of Helicoverpa armigera by host-induced RNA interference confers insect resistance in tobacco and tomato. Plant Molecular Biology, 2016, 90(3): 281–292
CrossRef
Pubmed
Google scholar
|
[56] |
Mao Y B, Cai W J, Wang J W, Hong G J, Tao X Y, Wang L J, Huang Y P, Chen X Y. Silencing a cotton bollworm P450 monooxygenase gene by plant-mediated RNAi impairs larval tolerance of gossypol. Nature Biotechnology, 2007, 25(11): 1307–1313
CrossRef
Pubmed
Google scholar
|
[57] |
Guo H, Song X, Wang G, Yang K, Wang Y, Niu L, Chen X, Fang R. Plant-generated artificial small RNAs mediated aphid resistance. PLoS One, 2014, 9(5): e97410
CrossRef
Pubmed
Google scholar
|
[58] |
Zotti M, Dos Santos E A, Cagliari D, Christiaens O, Taning C N T, Smagghe G. RNA interference technology in crop protection against arthropod pests, pathogens and nematodes. Pest Management Science, 2018, 74(6): 1239–1250
CrossRef
Pubmed
Google scholar
|
[59] |
San Miguel K, Scott J G. The next generation of insecticides: dsRNA is stable as a foliar-applied insecticide. Pest Management Science, 2016, 72(4): 801–809
CrossRef
Pubmed
Google scholar
|
[60] |
Mehlhorn S G, Geibel S, Bucher G, Nauen R. Profiling of RNAi sensitivity after foliar dsRNA exposure in different European populations of Colorado potato beetle reveals a robust response with minor variability. Pesticide Biochemistry and Physiology, 2020, 166: 104569
CrossRef
Pubmed
Google scholar
|
[61] |
Lü J, Liu Z Q, Guo W, Guo M J, Chen S M, Yang C X, Zhang Y J, Pan H P. Oral delivery of dsHvlwr is a feasible method for managing the pest Henosepilachna vigintioctopunctata (Coleoptera: Coccinellidae). Insect Science, 2021, 28(2): 509–520
CrossRef
Pubmed
Google scholar
|
[62] |
Kwon D H, Park J H, Lee S H. Screening of lethal genes for feeding RNAi by leaf disc-mediated systematic delivery of dsRNA in Tetranychus urticae. Pesticide Biochemistry and Physiology, 2013, 105(1): 69–75
CrossRef
Pubmed
Google scholar
|
[63] |
Kwon D H, Park J H, Ashok P A, Lee U, Lee S H. Screening of target genes for RNAi in Tetranychus urticae and RNAi toxicity enhancement by chimeric genes. Pesticide Biochemistry and Physiology, 2016, 130: 1–7
CrossRef
Pubmed
Google scholar
|
[64] |
Ali M W, Khan M M, Song F, Wu L, He L, Wang Z, Zhang Z Y, Zhang H, Jiang Y. RNA interference-based silencing of the Chitin Synthase 1 gene for reproductive and developmental disruptions in Panonychus citri. Insects, 2020, 11(11): 786
CrossRef
Pubmed
Google scholar
|
[65] |
Camargo R A, Barbosa G O, Possignolo I P, Peres L E, Lam E, Lima J E, Figueira A, Marques-Souza H. RNA interference as a gene silencing tool to control Tuta absoluta in tomato (Solanum lycopersicum). PeerJ, 2016, 4: e2673
CrossRef
Pubmed
Google scholar
|
[66] |
Andrade E C, Hunter W B. RNAi feeding bioassay: development of a non-transgenic approach to control Asian citrus psyllid and other hemipterans. Entomologia Experimentalis et Applicata, 2017, 162(3): 389–396
CrossRef
Google scholar
|
[67] |
Tian H, Peng H, Yao Q, Chen H, Xie Q, Tang B, Zhang W. Developmental control of a lepidopteran pest Spodoptera exigua by ingestion of bacteria expressing dsRNA of a non-midgut gene. PLoS One, 2009, 4(7): e6225
CrossRef
Pubmed
Google scholar
|
[68] |
Xiong Y, Zeng H, Zhang Y, Xu D, Qiu D. Silencing the HaHR3 gene by transgenic plant-mediated RNAi to disrupt Helicoverpa armigera development. International Journal of Biological Sciences, 2013, 9(4): 370–381
CrossRef
Pubmed
Google scholar
|
[69] |
Ganbaatar O, Cao B, Zhang Y, Bao D, Bao W, Wuriyanghan H. Knockdown of Mythimna separata chitinase genes via bacterial expression and oral delivery of RNAi effectors. BMC Biotechnology, 2017, 17(1): 9
CrossRef
Pubmed
Google scholar
|
[70] |
Vatanparast M, Kim Y. Optimization of recombinant bacteria expressing dsRNA to enhance insecticidal activity against a lepidopteran insect, Spodoptera exigua. PLoS One, 2017, 12(8): e0183054
CrossRef
Pubmed
Google scholar
|
[71] |
Ma Z Z, Zhou H, Wei Y L, Yan S, Shen J. A novel plasmid-Escherichia coli system produces large batch dsRNAs for insect gene silencing. Pest Management Science, 2020, 76(7): 2505–2512
CrossRef
Pubmed
Google scholar
|
[72] |
Zhang X, Zhang J, Zhu K Y. Chitosan/double-stranded RNA nanoparticle-mediated RNA interference to silence chitin synthase genes through larval feeding in the African malaria mosquito (Anopheles gambiae). Insect Molecular Biology, 2010, 19(5): 683–693
CrossRef
Pubmed
Google scholar
|
[73] |
Forim M R, Costa E S, da Silva M F, Fernandes J B, Mondego J M, Boiça Junior A L. Development of a new method to prepare nano-/microparticles loaded with extracts of Azadirachta indica, their characterization and use in controlling Plutella xylostella. Journal of Agricultural and Food Chemistry, 2013, 61(38): 9131–9139
CrossRef
Pubmed
Google scholar
|
[74] |
Avila L A, Chandrasekar R, Wilkinson K E, Balthazor J, Heerman M, Bechard J, Brown S, Park Y, Dhar S, Reeck G R, Tomich J M. Delivery of lethal dsRNAs in insect diets by branched amphiphilic peptide capsules. Journal of the Controlled Release Society, 2018, 273: 139–146
CrossRef
Pubmed
Google scholar
|
[75] |
Christiaens O, Tardajos M G, Martinez Reyna Z L, Dash M, Dubruel P, Smagghe G. Increased RNAi efficacy in Spodoptera exigua via the formulation of dsRNA with guanylated polymers. Frontiers in Physiology, 2018, 9: 316
CrossRef
Pubmed
Google scholar
|
[76] |
Lin Y H, Huang J H, Liu Y, Belles X, Lee H J. Oral delivery of dsRNA lipoplexes to German cockroach protects dsRNA from degradation and induces RNAi response. Pest Management Science, 2017, 73(5): 960–966
CrossRef
Pubmed
Google scholar
|
[77] |
Malik H J, Raza A, Amin I, Scheffler J A, Scheffler B E, Brown J K, Mansoor S. RNAi-mediated mortality of the whitefly through transgenic expression of double-stranded RNA homologous to acetylcholinesterase and ecdysone receptor in tobacco plants. Scientific Reports, 2016, 6(1): 38469
CrossRef
Pubmed
Google scholar
|
[78] |
Cordova-Kreylos A L, Fernandez L E, Koivunen M, Yang A, Flor-Weiler L, Marrone P G. Isolation and characterization of Burkholderia rinojensis sp. nov., a non-Burkholderia cepacia complex soil bacterium with insecticidal and miticidal activities. Applied and Environmental Microbiology, 2013, 79(24): 7669–7678
CrossRef
Pubmed
Google scholar
|
[79] |
Glare T R, O’Callaghan M. Microbial biopesticides for control of invertebrates: progress from New Zealand. Journal of Invertebrate Pathology, 2019, 165: 82–88
CrossRef
Pubmed
Google scholar
|
[80] |
Rasmann S, Bennett A, Biere A, Karley A, Guerrieri E. Root symbionts: powerful drivers of plant above- and belowground indirect defenses. Insect Science, 2017, 24(6): 947–960
CrossRef
Pubmed
Google scholar
|
[81] |
Pineda A, Kaplan I, Hannula S E, Ghanem W, Bezemer T M. Conditioning the soil microbiome through plant-soil feedbacks suppresses an aboveground insect pest. New Phytologist, 2020, 226(2): 595–608
CrossRef
Pubmed
Google scholar
|
[82] |
Garzo E, Rizzo E, Fereres A, Gomez S K. High levels of arbuscular mycorrhizal fungus colonization on Medicago truncatula reduces plant suitability as a host for pea aphids (Acyrthosiphon pisum). Insect Science, 2020, 27(1): 99–112
CrossRef
Pubmed
Google scholar
|
[83] |
Vekemans M C, Marchand P A. The fate of biocontrol agents under the European phytopharmaceutical regulation: how this regulation hinders the approval of botanicals as new active substances. Environmental Science and Pollution Research International, 2020, 27(32): 39879–39887
CrossRef
Pubmed
Google scholar
|
[84] |
Chen L, Liu T, Duan Y, Lu X, Yang Q. Microbial secondary metabolite, phlegmacin B1, as a novel inhibitor of insect chitinolytic enzymes. Journal of Agricultural and Food Chemistry, 2017, 65(19): 3851–3857
CrossRef
Pubmed
Google scholar
|
[85] |
Duan Y, Liu T, Zhou Y, Dou T, Yang Q. Glycoside hydrolase family 18 and 20 enzymes are novel targets of the traditional medicine berberine. Journal of Biological Chemistry, 2018, 293(40): 15429–15438
CrossRef
Pubmed
Google scholar
|
[86] |
Enan E E. Molecular response of Drosophila melanogaster tyramine receptor cascade to plant essential oils. Insect Biochemistry and Molecular Biology, 2005, 35(4): 309–321
CrossRef
Pubmed
Google scholar
|
[87] |
Makhoba X H, Viegas C Jr, Mosa R A, Viegas F P D, Pooe O J. Potential Impact of the multi-target drug approach in the treatment of some complex diseases. Drug Design, Development and Therapy, 2020, 14: 3235–3249
CrossRef
Pubmed
Google scholar
|
[88] |
Muthukrishnan S, Merzendorfer H, Arakane Y, Yang Q. Chitin organizing and modifying enzymes and proteins involved in remodeling of the insect cuticle. Advances in Experimental Medicine and Biology, 2019, 1142: 83–114
CrossRef
Pubmed
Google scholar
|
[89] |
Zhu K Y, Merzendorfer H, Zhang W, Zhang J, Muthukrishnan S. Biosynthesis, turnover, and functions of chitin in insects. Annual Review of Entomology, 2016, 61(1): 177–196
CrossRef
Pubmed
Google scholar
|
[90] |
Chen W, Qu M, Zhou Y, Yang Q. Structural analysis of group II chitinase (ChtII) catalysis completes the puzzle of chitin hydrolysis in insects. Journal of Biological Chemistry, 2018, 293(8): 2652–2660
CrossRef
Pubmed
Google scholar
|
[91] |
Qu M, Watanabe-Nakayama T, Sun S, Umeda K, Guo X, Liu Y, Ando T, Yang Q. High-speed atomic force microscopy reveals factors affecting the processivity of chitinases during interfacial enzymatic hydrolysis of crystalline chitin. ACS Catalysis, 2020, 10(22): 13606–13615
CrossRef
Google scholar
|
[92] |
Shahzad K, Manzoor F. Nanoformulations and their mode of action in insects: a review of biological interactions. Drug and Chemical Toxicology, 2021, 44(1): 1–11
CrossRef
Pubmed
Google scholar
|
[93] |
Jampílek J, Kráľová K. Chapter 17-Nanobiopesticides in agriculture: state of the art and future opportunities. In: Koul O, ed. Nano-Biopesticides Today and Future Perspectives. Academic Press, 2019: 397–447
|
[94] |
Jampílek J, Katarína K. 3-Nanopesticides: preparation, targeting, and controlled release. In: Grumezescu A M, eds. New Pesticides and Soil Sensors. Academic Press, 2017, 81–27
|
[95] |
de Oliveira J L, Campos E V R, Bakshi M, Abhilash P C, Fraceto L F. Application of nanotechnology for the encapsulation of botanical insecticides for sustainable agriculture: prospects and promises. Biotechnology Advances, 2014, 32(8): 1550–1561
CrossRef
Pubmed
Google scholar
|
[96] |
Yang F L, Li X G, Zhu F, Lei C L. Structural characterization of nanoparticles loaded with garlic essential oil and their insecticidal activity against Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae). Journal of Agricultural and Food Chemistry, 2009, 57(21): 10156–10162
CrossRef
Pubmed
Google scholar
|
[97] |
Benelli G. Plant-mediated biosynthesis of nanoparticles as an emerging tool against mosquitoes of medical and veterinary importance: a review. Parasitology Research, 2016, 115(1): 23–34
CrossRef
Pubmed
Google scholar
|
[98] |
Pradhan S, Mailapalli D R. Nanopesticides for Pest Control. In: Lichtfouse E, eds. Sustainable Agriculture Reviews 40. Cham: Springer, 2020, 43–74
|
/
〈 | 〉 |