Abstract
In this chapter, we cover the new insect control techniques that target the intestinal tract and are not based on chemical insecticides. Crystal (Cry) and Cytolitic (Cyt) protein families from Bacillus thuringiensis (Bt) and related toxins are used worldwide for insect control. Their primary action is to lyse midgut epithelial cells via binding to specific brush border receptors and elicit the formation of pores or trigger a necrotic pathway, which leads to the destruction of the midgut. We discuss in some detail recent findings on their mode of action. The use of proteinaceous inhibitors expressed in transgenic plants directed to enzyme targets, such as endopeptidases, α-amylases, and polygalacturonases, is reviewed. The success of transgenic crop plants expressing Cry toxin genes has paved the way for the development of genetically modified plants expressing double-stranded RNA (dsRNA) and CRISPR/Cas that can suppress the expression of genes coding for selected vital proteins. We discuss the recent developments in dsRNA and CRISPR/Cas technologies for insect pest management focusing on their actions in insect midgut.
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References
Acheuk F, Basiouni S, Shehata AA et al (2022) Status and prospects of botanical biopesticides in Europe and Mediterranean countries. Biomol Ther 12:311. https://doi.org/10.3390/biom12020311
Adang MJ, Crickmore N, Jurat-Fuentes JL (2014) Diversity of Bacillus thuringiensis crystal toxins and mechanism of action. Adv Insect Physiol 47:39–87. https://doi.org/10.1016/B978-0-12-800197-4.00002-6
Banyuls N, Hernández-Rodríguez CS, Van Rie J, Ferré J (2018) Critical amino acids for the insecticidal activity of Vip3Af from Bacillus thuringiensis: inference on structural aspects. Sci Rep 8:1–4. https://doi.org/10.1038/s41598-018-25346-3
Bhatia V, Bhattacharya R, Uniyal PL et al (2012) Host generated siRNAs attenuate expression of serine protease gene in Myzus persicae. PLoS One 12:e46343. https://doi.org/10.1371/journal.pone.0046343
Bretschneider A, Heckel DG, Pauchet Y (2016) Three toxins, two receptors, one mechanism: mode of action of Cry1A toxins from Bacillus thuringiensis in Heliothis virescens. Insect Biochem Mol Biol 76:109–117. https://doi.org/10.1016/j.ibmb.2016.07.008
Broadway RM (1997) Dietary regulation of serine proteinases that are resistant to serine proteinase inhibitors. J Insect Physiol 43:855–874
Byrne MJ, Iadanza MG, Perez MA et al (2021) Cryo-EM structures of an insecticidal Bt toxin reveal its mechanism of action on the membrane. Nat Commun 12:2791. https://doi.org/10.1038/s41467-021-23146-4
Calderón-Cortés N, Quesada M, Watanabe H et al (2012) Endogenous plant cell wall digestion: a key mechanism in insect evolution. Annu Rev Ecol Evol Syst 43:45–71. https://doi.org/10.1146/annurev-ecolsys-110411-160312
Chen WB, Lu GQ, Cheng HM et al (2017) Transgenic cotton coexpressing Vip3A and Cry1Ac has a broad insecticidal spectrum against lepidopteran pests. J Invertebr Pathol 149:59–65. https://doi.org/10.1016/j.jip.2017.08.001
Chiu T, Behari A, Chartron JW, Putman A, Li Y (2021) Exploring the potential of engineering polygalacturonase-inhibiting protein as an ecological, friendly, and nontoxic pest control agent. Biotechnol Bioeng 118:3200–3214. https://doi.org/10.1002/bit.27845
Chotechung S, Somta P, Chen J et al (2016) A gene encoding a polygalacturonase-inhibiting protein (PGIP) is a candidate gene for bruchid (Coleoptera: Bruchidae) resistance in mungbean (Vigna radiata). Theor Appl Genet 129:1673–1683. https://doi.org/10.1007/s00122-016-2731-1
Chrispeels MJ, de Sa MF, Higgins TJ (1998) Genetic engineering with α-amylase inhibitors makes seeds resistant to bruchids. Seed Sci Res 8:257–264
Crickmore N, Berry C, Panneerselvam S et al (2021) A structure-based nomenclature for Bacillus thuringiensis and other bacteria-derived pesticidal proteins. J Invertebr Pathol 186:107438. https://doi.org/10.1016/j.jip.2020.107438
Dang LY, Van Damme EJM (2015) Toxic proteins in plants. Phytochemistry 117:51–64. https://doi.org/10.1016/j.phytochem.2015.05.020
de Sousa-majer M, Hardie DC, Turner NC, Higgins TJ (2007) Bean alpha amylase inhibitor in transgenic peas inhibit the development of pea weevil larvae. J Econ Entomol 100:1416–1422. https://doi.org/10.1093/jee/100.4.1416
Del Valle EMM (2004) Cyclodextrins and their uses: a review. Process Biochem 39:1033–1046. https://doi.org/10.1016/S0032-9592(03)00258-9
Dhatwalia D, Aminedi R, Kalia V et al (2022) Host-mediated attenuation of gut sucrase in mustard aphid Lipaphis erysimi impaired its parthenogenetic reproduction on Indian mustard Brassica juncea. Pest Manag Sci 78:803–811. https://doi.org/10.1002/ps.6694
Divekar P, Majumder S, Halder J et al (2022a) Chapter 8. Trilogy: plants-proteases-insects. In: Banik S, Halder J (eds) Plant protection: present developments and future strategies. Today & Tomorrow’s Printers and Publishers, New Delhi
Divekar PA, Rani V, Majumder S et al (2022b) Protease inhibitors: an induced plant defense mechanism against herbivores. J Plant Growth Regul 28:1–7. https://doi.org/10.1007/s00344-022-10767-2
Drula E, Garron ML, Dogan S et al (2022) The carbohydrate-active enzyme database: functions and literature. Nucleic Acids Res 7:D571–D577. https://doi.org/10.1093/nar/gkab1045
Eghrari K, Oliveira SC, Nascimento AM et al (2022) The implications of homozygous vip3Aa20-and cry1Ab-maize on Spodoptera frugiperda control. J Pest Sci 95:115–127. https://doi.org/10.1007/s10340-021-01362-7
Elden TC (2000) Influence of a cysteine proteinase inhibitor on alfalfa weevil (Coleoptera: Curculionidae) growth and development over successive generations. J Entomol Sci 35:70–76. https://doi.org/10.18474/0749-8004-35.1.70
Estruch JJ, Warren GW, Mullins MA et al (1996) Vip3A, a novel Bacillus thuringiensis vegetative insecticidal protein with a wide spectrum of activities against lepidopteran insects. Proc Natl Acad Sci U S A 93:5389–5394
Franco OL, Rigden DJ, Melo FR, Grossi-de-Sá MF (2002) Plant α-amylase inhibitors and their interaction with insect α-amylases: structure, function and potential for crop protection. Eur J Biochem 269:397–412. https://doi.org/10.1046/j.0014-2956.2001.02656.x
Galdeano DM, Breton MC, Lopes JR et al (2017) Oral delivery of double-stranded RNAs induces mortality in nymphs and adults of the Asian citrus psyllid, Diaphorina citri. PLoS One 12:e0171847. https://doi.org/10.1371/journal.pone.0171847
Gamage SI, Kaewwongwal A, Laosatit K et al (2022) Tandemly duplicated genes encoding polygalacturonase inhibitors are associated with bruchid (Callosobruchus chinensis) resistance in moth bean (Vigna aconitifolia). Plant Sci 323:111402. https://doi.org/10.1016/j.plantsci.2022.111402
Gomis-Cebolla J, de Escudero IR, Vera-Velasco NM et al (2017) Insecticidal spectrum and mode of action of the Bacillus thuringiensis Vip3Ca insecticidal protein. J Invertebr Pathol 142:60–67. https://doi.org/10.1016/j.jip.2016.10.001
Green TR, Ryan CA (1972) Wound-induced proteinase inhibitors in plant leaves: a possible defense mechanism against insects. Science 175:776–777
Guo Z, Kang S, Chen D et al (2015) MAPK signaling pathway alters expression of midgut ALP and ABCC genes and causes resistance to Bacillus thuringiensis Cry1Ac toxin in diamondback moth. PLoS Genet 11:e1005124. https://doi.org/10.1371/journal.pgen.1005124
Guo Z, Kang S, Sun D et al (2020) MAPK-dependent hormonal signaling plasticity contributes to overcoming Bacillus thuringiensis toxin action in an insect host. Nat Commun 11:1–4. https://doi.org/10.1038/s41467-020-16608-8
Haeger W, Henning J, Heckel DG et al (2020) Direct evidence for a new mode of plant defense against insects via a novel polygalacturonase-inhibiting protein expression strategy. J Biol Chem 295:11833–11844. https://doi.org/10.1074/jbc.RA120.014027
Heckel DG (2021) The essential and enigmatic role of ABC transporters in Bt resistance of noctuids and other insect pests of agriculture. Insects 12:389. https://doi.org/10.3390/insects12050389
Hilder VA, Boulter D (1999) Genetic engineering of crop plants for insect resistance - a critical review. Crop Prot 18:177–191
Hilder VA, Gatehouse AMR, Sheerman SE et al (1987) A novel mechanism of insect resistance engineered into tobacco. Nature 330:160–163
Hwang BH, Bae H, Lim HS et al (2010) Overexpression of polygalacturonase-inhibiting protein 2 (PGIP2) of Chinese cabbage (Brassica rapa ssp. pekinensis) increased resistance to the bacterial pathogen Pectobacterium carotovorum ssp. carotovorum. Plant Cell Tissue Organ Cult 103:293–305. https://doi.org/10.1007/s11240-010-9779-4
ISAAA (2019) Global status of commercialized of biotech/GM crops in 2019: biotech crops drive socio-economic development and sustainable environment in the new frontier; International Service for the Acquisition of Agri-biotech applications: ISAAA brief 55-2019, Ithaca, NY, USA
Jayachandran B, Hussain M, Asgari S (2013) An insect trypsin-like serine protease as a target of microRNA: utilization of microRNA mimics and inhibitors by oral feeding. Insect Biochem Mol Biol 43:398–406. https://doi.org/10.1016/j.ibmb.2012.10.004
Jiang K, Hou XY, Tan TT et al (2018) Scavenger receptor-C acts as a receptor for Bacillus thuringiensis vegetative insecticidal protein Vip3Aa and mediates the internalization of Vip3Aa via endocytosis. PLoS Pathog 14:e1007347. https://doi.org/10.1371/journal.ppat.1007347
Jin MH, Tao JH, Qi LI et al (2021) Genome editing of the SfABCC2 gene confers resistance to Cry1F toxin from Bacillus thuringiensis in Spodoptera frugiperda. J Integr Agr 20:815–820. https://doi.org/10.1016/S2095-3119(19)62772-3
Jin M, Shan Y, Peng Y et al (2022) An integrative analysis of transcriptomics and proteomics reveals novel insights into the response in the midgut of Spodoptera frugiperda larvae to Vip3Aa. Toxins 14:55. https://doi.org/10.3390/toxins14010055
Jongsma MA, Bolter C (1997) The adaptation of insects to plant protease inhibitors. J Insect Physiol 43:885–895
Juge N (2006) Plant protein inhibitors of cell wall degrading enzymes. Trends Plant Sci 11:359–367. https://doi.org/10.1016/j.tplants.2006.05.006
Jurat-Fuentes JL, Heckel DG, Ferré J (2021) Mechanisms of resistance to insecticidal proteins from Bacillus thuringiensis. Annu Rev Entomol 66:121–140. https://doi.org/10.1146/annurev-ento-052620-073348
Kaewwongwal A, Chen J, Somta P et al (2017) Novel alleles of two tightly linked genes encoding polygalacturonase-inhibiting proteins (VrPGIP1 and VrPGIP2) associated with the Br locus that confer bruchid (Callosobruchus spp.) resistance to mungbean (Vigna radiata) accession V2709. Front Plant Sci 8:1692. https://doi.org/10.3389/fpls.2017.01692
Kirsch R, Gramzow L, Theißen G et al (2014) Horizontal gene transfer and functional diversification of plant cell wall degrading PGs: key events in the evolution of herbivory in beetles. Insect Biochem Mol Biol 52:33–50. https://doi.org/10.1016/j.ibmb.2014.06.008
Kirsch R, Heckel DG, Pauchet Y (2016) How the rice weevil breaks down the pectin network: enzymatic synergism and sub-functionalization. Insect Biochem Mol Biol 71:72–82. https://doi.org/10.1016/j.ibmb.2016.02.007
Kirsch R, Kunert G, Vogel H, Pauchet Y (2019) Pectin digestion in herbivorous beetles: impact of pseudoenzymes exceeds that of their active counterparts. Front Physiol 10:685. https://doi.org/10.3389/fphys.2019.00685
Kirsch R, Vurmaz E, Schaefer C et al (2020) Plants use identical inhibitors to protect their cell wall pectin against microbes and insects. Ecol Evol 10:3814–3824. https://doi.org/10.1002/ece3.6180
Laskowski M, Qasim MA (2000) What can the structures of enzyme-inhibitor complexes tell us about the structures of enzyme substrate complexes? Biochim Biophys Acta 1477:324–337. https://doi.org/10.1016/S0167-4838(99)00284-8
Lee MK, Walters FS, Hart H et al (2003) The mode of action of the Bacillus thuringiensis vegetative insecticidal protein Vip3A differs from that of Cry1Ab δ-endotoxin. Appl Environ Microbiol 69:4648–4657. https://doi.org/10.1128/AEM.69.8.4648-4657.2003
Li Q, Jin M, Yu S et al (2022a) Knockout of the ABCB1 gene increases susceptibility to emamectin benzoate, beta-cypermethrin and chlorantraniliprole in Spodoptera frugiperda. Insects 13:137. https://doi.org/10.3390/insects13020137
Li X, Liu X, Lu W et al (2022b) Application progress of plant-mediated RNAi in pest control. Front Bioeng Biotechnol 8:1364. https://doi.org/10.3389/fbioe.2022.963026
Los FC, Kao CY, Smitham J et al (2011) RAB-5-and RAB-11-dependent vesicle-trafficking pathways are required for plasma membrane repair after attack by bacterial pore-forming toxin. Cell Host Microbe 9:147–157. https://doi.org/10.1016/j.chom.2011.01.005
Ludvíková M, Griga M (2022) Pea transformation: history, current status and challenges. Czech J Genet Plant Breed 58:127–161. https://doi.org/10.17221/24/2022-CJGPB
Ma X, Shao E, Chen W et al (2022) Bt Cry1Ac resistance in Trichoplusia ni is conferred by multi-gene mutations. Insect Biochem Mol Biol 140:103678. https://doi.org/10.1016/j.ibmb.2021.103678
Manfredini C, Sicilia F, Ferrari S et al (2005) Polygalacturonase-inhibiting protein 2 of Phaseolus vulgaris inhibits BcPG1, a polygalacturonase of Botrytis cinerea important for pathogenicity, and protects transgenic plants from infection. Physiol Mol Plant Pathol 67:108–115. https://doi.org/10.1016/j.pmpp.2005.10.002
Mesén-Porras EA, Dahdouh-Cabia S, Jimenez-Quiros C et al (2020) Soybean protease inhibitors increase Bacillus thuringiensis subs. Israelensis toxicity against Hypothenemus hampei. Agron Mesoam 1:461–478. https://doi.org/10.15517/am.v31i2.36573
Moon TT, Maliha IJ, Khan AA et al (2022) CRISPR-Cas genome editing for insect pest stress management in crop plants. Stress 2:493–514. https://doi.org/10.3390/stresses2040034
Morton RL, Schroeder HE, Bateman KS et al (2000) Bean α-amylase inhibitor 1 in transgenic peas (Pisum sativum) provides complete protection from pea weevil (Bruchus pisorum) under field conditions. Proc Natl Acad Sci U S A 97:3820–3825. https://doi.org/10.1073/pnas.070054597
Núñez-Ramírez R, Huesa J, Bel Y et al (2020) Molecular architecture and activation of the insecticidal protein Vip3Aa from Bacillus thuringiensis. Nat Commun 11:1–9. https://doi.org/10.1038/s41467-020-17758-5
Qiu L, Fan J, Zhang B et al (2017) RNA interference knockdown of aminopeptidase N genes decrease the susceptibility of Chilo suppressalis larvae to Cry1Ab/Cry1Ac and Cry1Ca-expressing transgenic rice. J Invertebr Pathol 145:9–12. https://doi.org/10.1016/j.jip.2017.03.001
Rajagopal R, Sivakumar S, Agrawal N et al (2002) Silencing of midgut aminopeptidase N of Spodoptera litura by double-stranded RNA establishes its role as Bacillus thuringiensis toxin receptor. J Biol Chem 277:46849–46851. https://doi.org/10.1074/jbc.C200523200
Rathinam M, Rao U, Sreevathsa R (2020) Novel biotechnological strategies to combat biotic stresses: Polygalacturonase inhibitor (PGIP) proteins as a promising comprehensive option. Appl Microbiol Biotechnol 104:2333–2342. https://doi.org/10.1007/s00253-020-10396-3
Rauf I, Asif M, Amin I et al (2019) Silencing cathepsin L expression reduces Myzus persicae protein content and the nutritional value as prey for Coccinella septempunctata. Insect Mol Biol 28:785–797. https://doi.org/10.1111/imb.12589
Rawlings ND, Barrett AJ, Thomas PD et al (2018) The MEROPS database of proteolytic enzymes, their substrates and inhibitors in 2017 and a comparison with peptidases in the PANTHER database. Nucleic Acids Res 46:D624–D632. https://doi.org/10.1093/nar/gkx1134
Raza A, Malik HJ, Shafiq M et al (2016) RNA interference based approach to down regulate osmoregulators of whitefly (Bemisia tabaci): Potential technology for the control of whitefly. PLoS One 11:e0153883. https://doi.org/10.1371/journal.pone.0153883
Richardson M (1991) Seed storage proteins: the enzyme inhibitors. In: Rogers LJ (ed) Methods in plant biochemistry, Amino Acids, vol 5. Proteins and Nucleic Acids. Academic Press, London, pp 259–305
Ryan CA (1990) Protease inhibitors in plants: genes for improving defenses against insects and pathogens. Phytopathology 28:425–449
Santos-Ortega Y, Killiny N (2018) Silencing of sucrose hydrolase causes nymph mortality and disturbs adult osmotic homeostasis in Diaphorina citri (Hemiptera: Liviidae). Insect Biochem Mol Biol 101:131–143. https://doi.org/10.1016/j.ibmb.2018.09.003
Sardoy P, Ilina N, Borniego L et al (2021) Proteases inhibitors-insensitive cysteine proteases allow Nezara viridula to feed on growing seeds of field-grown soybean. J Insect Physiol 132:104250. https://doi.org/10.1016/j.jinsphys.2021.104250
Shade RE, Schroeder HE, Pueyo JJ et al (1994) Transgenic pea seeds expressing the α-amylase inhibitor of the common bean are resistant to bruchid beetles. Bio/Technology 12:793–796
Shelomi M, Danchin EG, Heckel D et al (2016) Horizontal gene transfer of pectinases from bacteria preceded the diversification of stick and leaf insects. Sci Rep 23:1–9. https://doi.org/10.1038/srep26388
Silva CP, Samuels RI (2011) Plant defense proteins that inhibit insect peptidases. In: Ecological aspects of nitrogen metabolism in plants. Wiley, West Sussex, pp 280–307
Silva CP, Terra WR, De Sá MG et al (2001a) Induction of digestive α-amylases in larvae of Zabrotes subfasciatus (Coleoptera: Bruchidae) in response to ingestion of common bean α-amylase inhibitor 1. J Insect Physiol 47:1283–1290. https://doi.org/10.1016/S0022-1910(01)00115-9
Silva CP, Terra WR, Xavier-Filho J et al (2001b) Digestion of legume starch granules by larvae of Zabrotes subfasciatus (Coleoptera: Bruchidae) and the induction of α–amylases in response to different diets. Insect Biochem Mol Biol 31:41–50. https://doi.org/10.1016/S0965-1748(00)00103-X
Silva-Filha MH, Romão TP, Rezende TM et al (2021) Bacterial toxins active against mosquitoes: mode of action and resistance. Toxins 13:523. https://doi.org/10.3390/toxins13080523
Singh G, Sachdev B, Sharma N et al (2010) Interaction of Bacillus thuringiensis vegetative insecticidal protein with ribosomal S2 protein triggers larvicidal activity in Spodoptera frugiperda. Appl Environ Microbiol 76:7202–7209. https://doi.org/10.1128/AEM.01552-10
Singh S, Singh A, Kumar S et al (2020) Protease inhibitors: recent advancement in its usage as a potential biocontrol agent for insect pest management. Insect Sci 27:186–201. https://doi.org/10.1111/1744-7917.12641
Sun D, Zhu L, Guo L et al (2022) A versatile contribution of both aminopeptidases N and ABC transporters to Bt Cry1Ac toxicity in the diamondback moth. BMC Biol 20:1–6. https://doi.org/10.1186/s12915-022-01226-1
Syed T, Askari M, Meng Z et al (2020) Current insights on vegetative insecticidal proteins (Vip) as next generation pest killers. Toxins 12:522. https://doi.org/10.3390/toxins12080522
Tabashnik BE, Carrière Y (2019) Global patterns of resistance to Bt crops highlighting pink bollworm in the United States, China, and India. J Econ Entomol 112:2513–2523. https://doi.org/10.1093/jee/toz173
Tabashnik BE, Brévault T, Carrière Y (2013) Insect resistance to Bt crops: lessons from the first billion acres. Nat Biotechnol 31:510–521. https://doi.org/10.1038/nbt.2597
Tanaka S, Miyamoto K, Noda H et al (2013) The ATP-binding cassette transporter subfamily C member 2 in Bombyx mori larvae is a functional receptor for cry toxins from Bacillus thuringiensis. FEBS J 280:1782–1794. https://doi.org/10.1111/febs.12200
Tang R, Li S, Liang J et al (2022) Optimization of the application of the CRISPR/Cas9 system in Mythimna separata. Entomol Exp Appl 170:593–602. https://doi.org/10.1111/eea.13184
Tokuda G (2019) Plant cell wall degradation in insects: recent progress on endogenous enzymes revealed by multi-omics technologies. Adv Insect Physiol 57:97–136. https://doi.org/10.1016/bs.aiip.2019.08.001
Tyagi S, Kesiraju K, Saakre M et al (2020) Genome editing for resistance to insect pests: an emerging tool for crop improvement. ACS Omega 5:20674–20683. https://doi.org/10.1021/acsomega.0c01435
Valencia A, Bustillo AE, Ossa GE, Chrispeels MJ (2000) α-Amylases of the coffee berry borer (Hypothenemus hampei) and their inhibition by two plant amylase inhibitors. Insect Biochem Mol Biol 30:207–213. https://doi.org/10.1016/S0965-1748(99)00115-0
Wang J, Zhang H, Wang H et al (2016) Functional validation of cadherin as a receptor of Bt toxin Cry1Ac in Helicoverpa armigera utilizing the CRISPR/Cas9 system. Insect Biochem Mol Biol 76:11–17. https://doi.org/10.1016/j.ibmb.2016.06.008
Wang J, Wang H, Liu S et al (2017) CRISPR/Cas9 mediated genome editing of Helicoverpa armigera with mutations of an ABC transporter gene HaABCA2 confers resistance to Bacillus thuringiensis Cry2A toxins. Insect Biochem Mol Biol 87:147–153. https://doi.org/10.1016/j.ibmb.2017.07.002
War AR, Paulraj MG, Ahmad T et al (2012) Mechanisms of plant defense against insect herbivores. Plant Signal Behav 7:1306–1320. https://doi.org/10.4161/psb.21663
Wu W, Gu D, Yan S, Li Z (2019) RNA interference of endoglucanases in the formosan subterranean termite Coptotermes formosanus shiraki (Blattodea: Rhinotermitidae) by dsRNA injection or ingestion. J Insect Physiol 112:15–22. https://doi.org/10.1016/j.jinsphys.2018.11.007
Zeng B, Chen FR, Sun H, Liu Y, Wu SF, Bass C et al (2022) Molecular and functional analysis of chitin synthase genes in Chilo suppressalis (Lepidoptera: Crambidae). Insect Sci 30:1–16. https://doi.org/10.1111/1744-7917.13134.3
Zha W, Peng X, Chen R et al (2011) Knockdown of midgut genes by dsRNA-transgenic plant-mediated RNA interference in the hemipteran insect Nilaparvata lugens. PLoS One 6:e20504. https://doi.org/10.1371/journal.pone.0020504
Zhang M, Du MY, Wang GX et al (2020) Identification, mRNA expression, and functional analysis of chitin synthase 2 gene in the rusty grain beetle, Cryptolestes ferrugineus. J Stored Prod Res 87:101622. https://doi.org/10.1016/j.jspr.2020.101622
Zhang D, Jin M, Yang Y et al (2021a) Synergistic resistance of Helicoverpa armigera to Bt toxins linked to cadherin and ABC transporters mutations. Insect Biochem Mol Biol 137:103635. https://doi.org/10.1016/j.ibmb.2021.103635
Zhang Q, Yan Q, Yuan X et al (2021b) Two polygalacturonase-inhibiting proteins (VrPGIP) of Vigna radiata confer resistance to bruchids (Callosobruchus spp.). J Plant Physiol 258:153376. https://doi.org/10.1016/j.jplph.2021.153376
Zheng JC, Yue XR, Kuang WQ et al (2020) NPC1b as a novel target in controlling the cotton bollworm, Helicoverpa armigera. Pest Manag Sci 76:2233–2242. https://doi.org/10.1002/ps.5761
Zhu-Salzman K, Zeng R (2015) Insect response to plant defensive protease inhibitors. Annu Rev Entomol 60:233–252. https://doi.org/10.1146/annurev-ento-010814-020816
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Terra, W.R., Ferreira, C., Silva, C.P. (2023). New Technologies of Insect Control That Act Through the Gut. In: Molecular Physiology and Evolution of Insect Digestive Systems. Entomology in Focus, vol 7. Springer, Cham. https://doi.org/10.1007/978-3-031-39233-7_15
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