RNA-Interference-Mediated Aphid Control in Crop Plants: A Review

[en] Crop plants suffer severe yield losses due to the significant damages caused by aphids. RNA interference (RNAi) technology is a versatile and environmentally friendly method for pest management in crop protection. Transgenic plants expressing siRNA/dsRNA and non-transformative methods such as spraying, microinjection, feeding, and a nanocarrier-delivery-mediated RNAi approach have been successfully applied for agricultural insect pest management. In this review, we summarize the application of host-induced gene silencing (HIGS)-mediated RNAi, spray-induced gene silencing (SIGS)-mediated RNAi, and other delivery-method-mediated RNAi methods for aphid control. We further discuss the challenges in RNAi application and propose potential solutions to enhance RNAi efficiency.

Disciplines :

Entomology & pest control

Author, co-author :

Zhang, Jiahui ; Université de Liège - ULiège > TERRA Research Centre

Li, Huiyuan ; Université de Liège - ULiège > TERRA Research Centre

Zhong, Xue ; Université de Liège - ULiège > TERRA Research Centre

Tian, Jinfu ; Université de Liège - ULiège > TERRA Research Centre

Segers, Arnaud ; Université de Liège - ULiège > TERRA Research Centre

Xia, Lanqin

Francis, Frédéric ; Université de Liège - ULiège > TERRA Research Centre > Gestion durable des bio-agresseurs

Language :

English

Title :

RNA-Interference-Mediated Aphid Control in Crop Plants: A Review

Publication date :

09 December 2022

Journal title :

Agriculture

eISSN :

2077-0472

Publisher :

MDPI AG

Volume :

Issue :

Pages :

2108

Peer reviewed :

Peer Reviewed verified by ORBi

Additional URL :

https://www.mdpi.com/2077-0472/12/12/2108/pdf

Funders :

Shennong Laboratory
CAAS - Chinese Academy of Agricultural Sciences
National Engineering Laboratory of Crop Molecular Breeding

Funding text :

This work was funded by the Shennong Laboratory, Zhengzhou Henan 450002, China (SN01-2022-01); the Innovation Program of the Chinese Academy of Agricultural Sciences (ZDXM03 and S2021ZD03); and the National Engineering Laboratory of Crop Molecular Breeding.

Available on ORBi :

since 13 January 2023

Statistics

Number of views

70 (10 by ULiège)

Number of downloads

72 (7 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

OpenAlex citations

Bibliography

Budzinski H. Couderchet M. Environmental and human health issues related to pesticides: From usage and environmental fate to impact Environ. Sci. Pollut. Res. Int. 2018 25 14277 14279 10.1007/s11356-018-1738-3 29569196
Luo K. Zhao H. Wang X. Kang Z. Prevalent pest management strategies for grain aphids: Opportunities and challenges Front. Plant Sci. 2021 12 790919 10.3389/fpls.2021.790919 35082813
Dang Y. Yang Q. Xue Z. Liu Y. RNA interference in fungi: Pathways, functions, and applications Eukaryot. Cell 2011 10 1148 1155 10.1128/EC.05109-11
Li Y. Lu J. Han Y. Fan X. Ding S.-W. RNA interference functions as an antiviral immunity mechanism in mammals Science 2013 342 231 234 10.1126/science.1241911
Nicolás F.E. Ruiz-Vázquez R.M. Functional diversity of RNAi-associated sRNAs in fungi Int. J. Mol. Sci. 2013 14 15348 15360 10.3390/ijms140815348
Bologna N.G. Voinnet O. The diversity, biogenesis, and activities of endogenous silencing small RNAs in Arabidopsis Annu. Rev. Plant Biol. 2014 65 473 503 10.1146/annurev-arplant-050213-035728
Guo Z. Li Y. Ding S.-W. Small RNA-based antimicrobial immunity Nat. Rev. Immunol. 2019 19 31 44 10.1038/s41577-018-0071-x
Song L. Fang Y. Chen L. Wang J. Chen X. Role of non-coding RNAs in plant immunity Plant Commun. 2021 2 100180 10.1016/j.xplc.2021.100180
Jain R.G. Robinson K.E. Asgari S. Mitter N. Current scenario of RNAi-based hemipteran control Pest Manag. Sci. 2021 77 2188 2196 10.1002/ps.6153
Napoli C. Lemieux C. Jorgensen R. Introduction of a chimeric chalcone synthase gene into petunia results in reversible co-suppression of homologous genes in trans Plant Cell 1990 2 279 289 10.2307/3869076
Fire A. Xu S. Montgomery M.K. Kostas S.A. Driver S.E. Mello C.C. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans Nature 1998 391 806 811 10.1038/35888 9486653
Dalakouras A. Wassenegger M. McMillan J.N. Cardoza V. Maegele I. Dadami E. Runne M. Krczal G. Wassenegger M. Induction of silencing in plants by high-pressure spraying of in vitro-synthesized small RNAs Front. Plant Sci. 2016 7 1327 10.3389/fpls.2016.01327 27625678
San Miguel K. Scott J.G. The next generation of insecticides: dsRNA is stable as a foliar-applied insecticide Pest Manag. Sci. 2016 72 801 809 10.1002/ps.4056 26097110
Numata K. Ohtani M. Yoshizumi T. Demura T. Kodama Y. Local gene silencing in plants via synthetic ds RNA and carrier peptide Plant Biotechnol. J. 2014 12 1027 1034 10.1111/pbi.12208
Ghosh S.K.B. Hunter W.B. Park A.L. Gundersen-Rindal D.E. Double strand RNA delivery system for plant-sap-feeding insects PLoS ONE 2017 12 e0171861 10.1371/journal.pone.0171861
Dalakouras A. Jarausch W. Buchholz G. Bassler A. Braun M. Manthey T. Krczal G. Wassenegger M. Delivery of hairpin RNAs and small RNAs into woody and herbaceous plants by trunk injection and petiole absorption Front. Plant Sci. 2018 9 1253 10.3389/fpls.2018.01253
Pitino M. Coleman A.D. Maffei M.E. Ridout C.J. Hogenhout S.A. Silencing of aphid genes by dsRNA feeding from plants PLoS ONE 2011 6 e25709 10.1371/journal.pone.0025709
Xu L. Duan X. Lv Y. Zhang X. Nie Z. Xie C. Ni Z. Liang R. Silencing of an aphid carboxylesterase gene by use of plant-mediated RNAi impairs Sitobion avenae tolerance of Phoxim insecticides Transgenic Res. 2014 23 389 396 10.1007/s11248-013-9765-9
Chung S.H. Jing X. Luo Y. Douglas A.E. Targeting symbiosis-related insect genes by RNAi in the pea aphid-Buchnera symbiosis Insect Biochem. Mol. Biol. 2018 95 55 63 10.1016/j.ibmb.2018.02.004
Koch A. Kogel K.H. New wind in the sails: Improving the agronomic value of crop plants through RNAi-mediated gene silencing Plant Biotechnol. J. 2014 12 821 831 10.1111/pbi.12226
Christiaens O. Niu J. Taning C.N.T. RNAi in insects: A revolution in fundamental research and pest control applications Insects 2020 11 415 10.3390/insects11070415
Santala J. Valkonen J.P. Sensitivity of small RNA-based detection of plant viruses Front. Microbiol. 2018 9 939 10.3389/fmicb.2018.00939
Sang H. Kim J.-I. Advanced strategies to control plant pathogenic fungi by host-induced gene silencing (HIGS) and spray-induced gene silencing (SIGS) Plant Biotechnol. Rep. 2020 14 1 8 10.1007/s11816-019-00588-3
Zand Karimi H. Innes R.W. Molecular mechanisms underlying host-induced gene silencing Plant Cell 2022 34 3183 3199 10.1093/plcell/koac165 35666177
Huang G. Allen R. Davis E.L. Baum T.J. Hussey R.S. Engineering broad root-knot resistance in transgenic plants by RNAi silencing of a conserved and essential root-knot nematode parasitism gene Proc. Natl. Acad. Sci. USA 2006 103 14302 14306 10.1073/pnas.0604698103 16985000
Baum J.A. Bogaert T. Clinton W. Heck G.R. Feldmann P. Ilagan O. Johnson S. Plaetinck G. Munyikwa T. Pleau M. Control of coleopteran insect pests through RNA interference Nat. Biotechnol. 2007 25 1322 1326 10.1038/nbt1359
Nowara D. Gay A. Lacomme C. Shaw J. Ridout C. Douchkov D. Hensel G. Kumlehn J. Schweizer P. HIGS: Host-induced gene silencing in the obligate biotrophic fungal pathogen Blumeria graminis Plant Cell 2010 22 3130 3141 10.1105/tpc.110.077040
Koch A. Kumar N. Weber L. Keller H. Imani J. Kogel K.-H. Host-induced gene silencing of cytochrome P450 lanosterol C14α-demethylase–encoding genes confers strong resistance to Fusarium species Proc. Natl. Acad. Sci. USA 2013 110 19324 19329 10.1073/pnas.1306373110
Govindarajulu M. Epstein L. Wroblewski T. Michelmore R.W. Host-induced gene silencing inhibits the biotrophic pathogen causing downy mildew of lettuce Plant Biotechnol. J. 2015 13 875 883 10.1111/pbi.12307
Jahan S.N. Åsman A.K. Corcoran P. Fogelqvist J. Vetukuri R.R. Dixelius C. Plant-mediated gene silencing restricts growth of the potato late blight pathogen Phytophthora infestans J. Exp. Bot. 2015 66 2785 2794 10.1093/jxb/erv094
Abdellatef E. Will T. Koch A. Imani J. Vilcinskas A. Kogel K.H. Silencing the expression of the salivary sheath protein causes transgenerational feeding suppression in the aphid Sitobion avenae Plant Biotechnol. J. 2015 13 849 857 10.1111/pbi.12322 25586210
Zhang J. Khan S.A. Hasse C. Ruf S. Heckel D.G. Bock R. Full crop protection from an insect pest by expression of long double-stranded RNAs in plastids Science 2015 347 991 994 10.1126/science.1261680 25722411
Pitino M. Hogenhout S.A. Aphid protein effectors promote aphid colonization in a plant species-specific manner Mol. Plant Microbe Interact. 2013 26 130 139 10.1094/MPMI-07-12-0172-FI 23035913
Elzinga D.A. De Vos M. Jander G. Suppression of plant defenses by a Myzus persicae (green peach aphid) salivary effector protein Mol. Plant Microbe Interact. 2014 27 747 756 10.1094/MPMI-01-14-0018-R 24654979
Coleman A.D. Wouters R.H. Mugford S.T. Hogenhout S.A. Persistence and transgenerational effect of plant-mediated RNAi in aphids J. Exp. Bot. 2015 66 541 548 10.1093/jxb/eru450
Faisal M. Abdel-Salam E.M. Alatar A.A. Saquib Q. Alwathnani H.A. Canto T. Genetic transformation and siRNA-mediated gene silencing for aphid resistance in tomato Agronomy 2019 9 893 10.3390/agronomy9120893
Guo H. Zhang Y. Tong J. Ge P. Wang Q. Zhao Z. Zhu-Salzman K. Hogenhout S.A. Ge F. Sun Y. An aphid-secreted salivary protease activates plant defense in phloem Curr. Biol. 2020 30 4826 4836 10.1016/j.cub.2020.09.020
Dong Y. Wu M. Zhang Q. Fu J. Loiacono F.V. Yang Y. Wang Z. Li S. Chang L. Bock R. et al. Control of a sap-sucking insect pest by plastid-mediated RNA interference Mol. Plant 2022 15 1176 1191 10.1016/j.molp.2022.05.008
Xu L. Hou Q. Zhao Y. Lu L. Li B. Ni Z. Liang R. Silencing of a lipase maturation factor 2-like gene by wheat-mediated RNAi reduces the survivability and reproductive capacity of the grain aphid, Sitobion avenae Arch. Insect Biochem. Physiol. 2017 95 e21392 10.1002/arch.21392
Zhao Y. Sui X. Xu L. Liu G. Lu L. You M. Xie C. Li B. Ni Z. Liang R. Plant-mediated RNAi of grain aphid CHS1 gene confers common wheat resistance against aphids Pest Manag. Sci. 2018 74 2754 2760 10.1002/ps.5062
Hou Q. Xu L. Liu G. Pang X. Wang X. Zhang Y. You M. Ni Z. Zhao Z. Liang R. Plant-mediated gene silencing of an essential olfactory-related Gqalpha gene enhances resistance to grain aphid in common wheat in greenhouse and field Pest Manag. Sci. 2019 75 1718 1725 10.1002/ps.5292 30525312
Sun Y. Sparks C. Jones H. Riley M. Francis F. Du W. Xia L. Silencing an essential gene involved in infestation and digestion in grain aphid through plant-mediated RNA interference generates aphid-resistant wheat plants Plant Biotechnol. J. 2019 17 852 854 10.1111/pbi.13067 30582665
Bhatia V. Bhattacharya R. Host-mediated RNA interference targeting a cuticular protein gene impaired fecundity in the green peach aphid Myzus persicae Pest Manag. Sci. 2018 74 2059 2068 10.1002/ps.4900 29493869
Thairu M.W. Skidmore I.H. Bansal R. Novakova E. Hansen T.E. Li-Byarlay H. Wickline S.A. Hansen A.K. Efficacy of RNA interference knockdown using aerosolized short interfering RNAs bound to nanoparticles in three diverse aphid species Insect Mol. Biol. 2017 26 356 368 10.1111/imb.12301
Yan S. Qian J. Cai C. Ma Z. Li J. Yin M. Ren B. Shen J. Spray method application of transdermal dsRNA delivery system for efficient gene silencing and pest control on soybean aphid Aphis glycines J. Pest Sci. 2020 93 449 459 10.1007/s10340-019-01157-x
Biedenkopf D. Will T. Knauer T. Jelonek L. Furch A.C.U. Busche T. Koch A. Systemic spreading of exogenous applied RNA biopesticides in the crop plant Hordeum vulgare ExRNA 2020 2 12 10.1186/s41544-020-00052-3
Liu S. Ladera-Carmona M.J. Poranen M.M. van Bel A.J.E. Kogel K.-H. Imani J. Evaluation of dsRNA delivery methods for targeting macrophage migration inhibitory factor MIF in RNAi-based aphid control J. Plant Dis. Prot. 2021 128 1201 1212 10.1007/s41348-021-00464-9
Zhang Y. Liu X. Francis F. Xie H. Fan J. Wang Q. Liu H. Sun Y. Chen J. The salivary effector protein Sg2204 in the greenbug Schizaphis graminum suppresses wheat defence and is essential for enabling aphid feeding on host plants Plant Biotechnol. J. 2022 20 2187 2201 10.1111/pbi.13900
Ding B.Y. Shang F. Zhang Q. Xiong Y. Yang Q. Niu J.Z. Smagghe G. Wang J.J. Silencing of two insulin receptor genes disrupts nymph-adult transition of alate brown citrus aphid Int. J. Mol. Sci. 2017 18 357 10.3390/ijms18020357
Mou X. Yuan G.R. Jiang H.B. Liu Z. Wang J.J. Functional characterization of two acetylcholinesterase genes in the brown citrus aphid, Aphis (Toxoptera) citricidus (Kirkaldy), using heterologous expression and RNA interference Pestic. Biochem. Physiol. 2017 138 76 83 10.1016/j.pestbp.2017.03.004
Shang F. Niu J.Z. Ding B.Y. Zhang Q. Ye C. Zhang W. Smagghe G. Wang J.J. Vitellogenin and its receptor play essential roles in the development and reproduction of the brown citrus aphid, Aphis (Toxoptera) citricidus Insect Mol. Biol. 2018 27 221 233 10.1111/imb.12366 29226991
Shang F. Ding B.Y. Ye C. Yang L. Chang T.Y. Xie J. Tang L.D. Niu J. Wang J.J. Evaluation of a cuticle protein gene as a potential RNAi target in aphids Pest Manag. Sci. 2020 76 134 140 10.1002/ps.5599 31461217
Ye C. Wang Z.-W. Sheng Y.-L. Wang Z.-G. Smagghe G. Christiaens O. Niu J. Wang J. GNBP1 as a potential RNAi target to enhance the virulence of Beauveria bassiana for aphid control J. Pest Sci. 2021 95 87 100 10.1007/s10340-021-01388-x
Zheng Y. Hu Y. Yan S. Zhou H. Song D. Yin M. Shen J. A polymer/detergent formulation improves dsRNA penetration through the body wall and RNAi-induced mortality in the soybean aphid Aphis glycines Pest Manag. Sci. 2019 75 1993 1999 10.1002/ps.5313
Gong Y.H. Yu X.R. Shang Q.L. Shi X.Y. Gao X.W. Oral delivery mediated RNA interference of a carboxylesterase gene results in reduced resistance to organophosphorus insecticides in the cotton aphid, Aphis gossypii Glover PLoS ONE 2014 9 e102823 10.1371/journal.pone.0102823 25140535
Peng T. Pan Y. Yang C. Gao X. Xi J. Wu Y. Huang X. Zhu E. Xin X. Zhan C. et al. Over-expression of CYP6A2 is associated with spirotetramat resistance and cross-resistance in the resistant strain of Aphis gossypii Glover Pestic. Biochem. Physiol. 2016 126 64 69 10.1016/j.pestbp.2015.07.008 26778436
Rebijith K.B. Asokan R. Hande H.R. Kumar N.K. Krishna V. Vinutha J. Bakthavatsalam N. RNA interference of odorant-binding protein 2 (OBP2) of the cotton aphid, Aphis gossypii (Glover), resulted in altered electrophysiological responses Appl. Biochem. Biotechnol. 2016 178 251 266 10.1007/s12010-015-1869-7
Wu Y. Xu H. Pan Y. Gao X. Xi J. Zhang J. Shang Q. Expression profile changes of cytochrome P450 genes between thiamethoxam susceptible and resistant strains of Aphis gossypii Glover Pestic. Biochem. Physiol. 2018 149 1 7 10.1016/j.pestbp.2018.05.007
Pan Y. Chai P. Zheng C. Xu H. Wu Y. Gao X. Xi J. Shang Q. Contribution of cytochrome P450 monooxygenase CYP380C6 to spirotetramat resistance in Aphis gossypii Glover Pestic. Biochem. Physiol. 2018 148 182 189 10.1016/j.pestbp.2018.04.015
Ullah F. Gul H. Tariq K. Desneux N. Gao X. Song D. Functional analysis of cytochrome P450 genes linked with acetamiprid resistance in melon aphid, Aphis gossypii Pestic. Biochem. Physiol. 2020 170 104687 10.1016/j.pestbp.2020.104687
Ullah F. Gul H. Tariq K. Hafeez M. Desneux N. Gao X. Song D. RNA interference-mediated silencing of ecdysone receptor (EcR) gene causes lethal and sublethal effects on melon aphid, Aphis gossypii Entomol. Gen. 2022 42 791 797 10.1127/entomologia/2022/1434
Shi Y. Liu T.Y. Ding B.Y. Niu J. Jiang H.B. Liu T.X. Wang J.J. Crustacean cardioactive peptide and its receptor modulate the ecdysis behavior in the pea aphid, Acyrthosiphon pisum J. Insect Physiol. 2022 137 104364 10.1016/j.jinsphys.2022.104364 35121009
Mutti N.S. Park Y. Reese J.C. Reeck G.R. RNAi knockdown of a salivary transcript leading to lethality in the pea aphid, Acyrthosiphon pisum J. Insect Sci. 2006 6 38 10.1673/031.006.3801 20233093
Jaubert-Possamai S. Le Trionnaire G. Bonhomme J. Christophides G.K. Rispe C. Tagu D. Gene knockdown by RNAi in the pea aphid Acyrthosiphon pisum BMC Biotechnol. 2007 7 63 10.1186/1472-6750-7-63 17903251
Shakesby A.J. Wallace I.S. Isaacs H.V. Pritchard J. Roberts D.M. Douglas A.E. A water-specific aquaporin involved in aphid osmoregulation Insect Biochem. Mol. Biol. 2009 39 1 10 10.1016/j.ibmb.2008.08.008
Whyard S. Singh A.D. Wong S. Ingested double-stranded RNAs can act as species-specific insecticides Insect Biochem. Mol. Biol. 2009 39 824 832 10.1016/j.ibmb.2009.09.007
Mao J. Zeng F. Feeding-based RNA interference of a gap gene is lethal to the pea aphid, Acyrthosiphon pisum PLoS ONE 2012 7 e48718 10.1371/journal.pone.0048718
Sapountzis P. Duport G. Balmand S. Gaget K. Jaubert-Possamai S. Febvay G. Charles H. Rahbe Y. Colella S. Calevro F. New insight into the RNA interference response against cathepsin-L gene in the pea aphid, Acyrthosiphon pisum: Molting or gut phenotypes specifically induced by injection or feeding treatments Insect Biochem. Mol. Biol. 2014 51 20 32 10.1016/j.ibmb.2014.05.005
Guo K. Wang W. Luo L. Chen J. Guo Y. Cui F. Characterization of an aphid-specific, cysteine-rich protein enriched in salivary glands Biophys. Chem. 2014 189 25 32 10.1016/j.bpc.2014.03.006
Wang W. Luo L. Lu H. Chen S. Kang L. Cui F. Angiotensin-converting enzymes modulate aphid-plant interactions Sci. Rep. 2015 5 8885 10.1038/srep08885
Naessens E. Dubreuil G. Giordanengo P. Baron O.L. Minet-Kebdani N. Keller H. Coustau C. A secreted MIF cytokine enables aphid feeding and represses plant immune responses Curr. Biol. 2015 25 1898 1903 10.1016/j.cub.2015.05.047 26119751
Wang W. Dai H. Zhang Y. Chandrasekar R. Luo L. Hiromasa Y. Sheng C. Peng G. Chen S. Tomich J.M. et al. Armet is an effector protein mediating aphid-plant interactions FASEB J. 2015 29 2032 2045 10.1096/fj.14-266023 25678626
Will T. Vilcinskas A. The structural sheath protein of aphids is required for phloem feeding Insect Biochem. Mol. Biol. 2015 57 34 40 10.1016/j.ibmb.2014.12.005
Zhang Y. Lu Z. Peroxiredoxin 1 protects the pea aphid Acyrthosiphon pisum from oxidative stress induced by Micrococcus luteus infection J. Invertebr. Pathol. 2015 127 115 121 10.1016/j.jip.2015.03.011 25817695
Chen N. Fan Y.L. Bai Y. Li X.D. Zhang Z.F. Liu T.X. Cytochrome P450 gene, CYP4G51, modulates hydrocarbon production in the pea aphid, Acyrthosiphon pisum Insect Biochem. Mol. Biol. 2016 76 84 94 10.1016/j.ibmb.2016.07.006 27425674
Zhang R. Wang B. Grossi G. Falabella P. Liu Y. Yan S. Lu J. Xi J. Wang G. Molecular basis of alarm pheromone detection in aphids Curr. Biol. 2017 27 55 61 10.1016/j.cub.2016.10.013
Webster C.G. Pichon E. van Munster M. Monsion B. Deshoux M. Gargani D. Calevro F. Jimenez J. Moreno A. Krenz B. et al. Identification of plant virus receptor candidates in the stylets of their aphid vectors J. Virol. 2018 92 e00432-18 10.1128/JVI.00432-18
Li X. Qu M.J. Zhang Y. Li J.W. Liu T.X. Expression of neuropeptide F gene and its regulation of feeding behavior in the pea aphid, Acyrthosiphon pisum Front. Physiol. 2018 9 87 10.3389/fphys.2018.00087
Ye C. An X. Jiang Y.D. Ding B.Y. Shang F. Christiaens O. Taning C.N.T. Smagghe G. Niu J. Wang J.J. Induction of RNAi core machinery’s gene expression by exogenous dsRNA and the effects of pre-exposure to dsRNA on the gene silencing efficiency in the pea aphid (Acyrthosiphon pisum) Front. Physiol. 2018 9 1906 10.3389/fphys.2018.01906
Ye C. Jiang Y.D. An X. Yang L. Shang F. Niu J. Wang J.J. Effects of RNAi-based silencing of chitin synthase gene on moulting and fecundity in pea aphids (Acyrthosiphon pisum) Sci. Rep. 2019 9 3694 10.1038/s41598-019-39837-4
Wang Q. Yuan E. Ling X. Zhu-Salzman K. Guo H. Ge F. Sun Y. An aphid facultative symbiont suppresses plant defence by manipulating aphid gene expression in salivary glands Plant Cell Environ. 2020 43 2311 2322 10.1111/pce.13836 32596816
Ding B.Y. Niu J. Shang F. Yang L. Zhang W. Smagghe G. Wang J.J. Parental silencing of a horizontally transferred carotenoid desaturase gene causes a reduction of red pigment and fitness in the pea aphid Pest Manag. Sci. 2020 76 2423 2433 10.1002/ps.5783 32056367
Shahid S. Shi Y. Yang C. Li J. Ali M.Y. Smagghe G. Liu T.X. CCHamide2-receptor regulates feeding behavior in the pea aphid, Acyrthosiphon pisum Peptides 2021 143 170596 10.1016/j.peptides.2021.170596
Zhou X. Ling X. Guo H. Zhu-Salzman K. Ge F. Sun Y. Serratia symbiotica enhances fatty acid metabolism of pea aphid to promote host development Int. J. Mol. Sci. 2021 22 5951 10.3390/ijms22115951
Chang M. Cheng H. Cai Z. Qian Y. Zhang K. Yang L. Ma N. Li D. miR-92a-1-p5 modulated expression of the flightin gene regulates flight muscle formation and wing extension in the pea aphid, Acyrthosiphon pisum (Hemiptera: Aphidoidea) J. Insect Sci. 2022 22 14 10.1093/jisesa/ieac033 35738260
Guo Y. Fan Y. Teng Z. Wang L. Tan X. Wan F. Zhou H. Efficacy of RNA interference using nanocarrier-based transdermal dsRNA delivery system in the woolly apple aphid, Eriosoma lanigerum Arch. Insect Biochem. Physiol. 2022 110 e21888 10.1002/arch.21888
Mulot M. Boissinot S. Monsion B. Rastegar M. Clavijo G. Halter D. Bochet N. Erdinger M. Brault V. Comparative analysis of RNAi-based methods to down-regulate expression of two genes expressed at different levels in Myzus persicae Viruses 2016 8 316 10.3390/v8110316
Gogoi A. Sarmah N. Kaldis A. Perdikis D. Voloudakis A. Plant insects and mites uptake double-stranded RNA upon its exogenous application on tomato leaves Planta 2017 246 1233 1241 10.1007/s00425-017-2776-7
Tariq K. Ali A. Davies T.G.E. Naz E. Naz L. Sohail S. Hou M. Ullah F. RNA interference-mediated knockdown of voltage-gated sodium channel (MpNav) gene causes mortality in peach-potato aphid, Myzus persicae Sci. Rep. 2019 9 5291 10.1038/s41598-019-41832-8
Mahmood I. Afroz A. Malik M.F. Zeeshan N. Khan M.R. Rashid U. Khan M.A.U. Ashraf N.M. Alam S. RNA interference-mediated knockdown of odorant-binding protein 2 and MP58 gene causes mortality in Myzus persicae Int. J. Trop. Insect Sci. 2021 42 315 326 10.1007/s42690-021-00546-z
Zhang Y.H. Ma Z.Z. Zhou H. Chao Z.J. Yan S. Shen J. Nanocarrier-delivered dsRNA suppresses wing development of green peach aphids Insect Sci. 2022 29 669 682 10.1111/1744-7917.12953 34288425
Ding C.Y. Ma Y.M. Li B. Wang Y. Zhao L. Peng J.N. Li M.Y. Liu S. Li S.G. Identification and functional analysis of differentially expressed genes in Myzus persicae (Hemiptera: Aphididae) in response to trans-anethole J. Insect Sci. 2022 22 3 10.1093/jisesa/ieab094 34958664
Wang X.X. Feng Z.J. Chen Z.S. Zhang Z.F. Zhang Y. Liu T.X. Use of tyrosine hydroxylase RNAi to study Megoura viciae (Hemiptera: Aphididae) sequestration of its host’s l-DOPA for body melanism J. Insect Physiol. 2019 114 136 144 10.1016/j.jinsphys.2019.03.007 30904400
Xiao D. Lu Y.H. Shang Q.L. Song D.L. Gao X.W. Gene silencing of two acetylcholinesterases reveals their cholinergic and non-cholinergic functions in Rhopalosiphum padi and Sitobion avenae Pest Manag. Sci. 2015 71 523 530 10.1002/ps.3800
Deng F. Zhao Z. Influence of catalase gene silencing on the survivability of Sitobion avenae Arch. Insect Biochem. Physiol. 2014 86 46 57
Wang D. Liu Q. Li X. Sun Y. Wang H. Xia L. Double-stranded RNA in the biological control of grain aphid (Sitobion avenae F.) Funct. Integr. Genom. 2015 15 211 223 10.1007/s10142-014-0424-x
Yan T. Chen H. Sun Y. Yu X. Xia L. RNA interference of the ecdysone receptor genes EcR and USP in grain aphid (Sitobion avenae F.) affects its survival and fecundity upon feeding on wheat plants Int. J. Mol. Sci. 2016 17 2098 10.3390/ijms17122098
Zhang Y. Fan J. Francis F. Chen J. Molecular characterization and gene silencing of Laccase 1 in the grain aphid, Sitobion avenae Arch. Insect Biochem. Physiol. 2018 97 e21446 10.1002/arch.21446
Ullah R.M.K. Quershi S.R. Adeel M.M. Abdelnabby H. Waris M.I. Duan S.G. Wang M.Q. An odorant binding protein (SaveOBP9) involved in chemoreception of the wheat aphid Sitobion avenae Int. J. Mol. Sci. 2020 21 8331 10.3390/ijms21218331
Ullah R.M.K. Waris M.I. Qureshi S.R. Rasool F. Duan S.G. Zaka S.M. Atiq M.N. Wang M.Q. Silencing of an odorant binding protein (SaveOBP10) involved in the behavioural shift of the wheat aphid Sitobion avenae (Fabricius) Insect Mol. Biol. 2022 31 568 584 10.1111/imb.12780
Zhang Y. Fan J. Sun J.-R. Chen J.-L. Cloning and RNA interference analysis of the salivary protein C002 gene in Schizaphis graminum J. Integr. Agric. 2015 14 698 705 10.1016/S2095-3119(14)60822-4
Zhang B.Z. Ma K.S. Liu J.J. Lu L.Y. Chen X.L. Zhang S.P. Gao X.W. Differential expression of genes in greenbug (Schizaphis graminum Rondani) treated by imidacloprid and RNA interference Pest Manag. Sci. 2019 75 1726 1733 10.1002/ps.5293 30525307
Zhang Y. Liu X. Fu Y. Crespo-Herrera L. Liu H. Wang Q. Zhang Y. Chen J. Salivary effector Sm9723 of grain aphid Sitobion miscanthi suppresses plant defense and is essential for aphid survival on wheat Int. J. Mol. Sci. 2022 23 6909 10.3390/ijms23136909
Whangbo J.S. Hunter C.P. Environmental RNA interference Trends Genet. 2008 24 297 305 10.1016/j.tig.2008.03.007 18450316
Wang M. Weiberg A. Lin F.-M. Thomma B.P. Huang H.-D. Jin H. Bidirectional cross-kingdom RNAi and fungal uptake of external RNAs confer plant protection Nat. Plants 2016 2 16151 10.1038/nplants.2016.151 27643635
Qiao L. Lan C. Capriotti L. Ah-Fong A. Nino Sanchez J. Hamby R. Heller J. Zhao H. Glass N.L. Judelson H.S. et al. Spray-induced gene silencing for disease control is dependent on the efficiency of pathogen RNA uptake Plant Biotechnol. J. 2021 19 1756 1768 10.1111/pbi.13589
Ghosh S.K.B. Hunter W.B. Park A.L. Gundersen-Rindal D.E. Double-stranded RNA oral delivery methods to induce RNA interference in phloem and plant-sap-feeding hemipteran insects J. Vis. Exp. 2018 135 e57390 10.3791/57390
Wang M. Jin H. Spray-induced gene silencing: A powerful innovative strategy for crop protection Trends Microbiol. 2017 25 4 6 10.1016/j.tim.2016.11.011
Hunter W.B. Glick E. Paldi N. Bextine B.R. Advances in RNA interference: dsRNA treatment in trees and grapevines for insect pest suppression Southwest Entomol. 2012 37 85 87 10.3958/059.037.0110
Koch A. Biedenkopf D. Furch A. Weber L. Rossbach O. Abdellatef E. Linicus L. Johannsmeier J. Jelonek L. Goesmann A. An RNAi-based control of Fusarium graminearum infections through spraying of long dsRNAs involves a plant passage and is controlled by the fungal silencing machinery PLoS Pathog. 2016 12 e1005901 10.1371/journal.ppat.1005901
Cagliari D. Dias N.P. Galdeano D.M. Dos Santos E.Á. Smagghe G. Zotti M.J. Management of pest insects and plant diseases by non-transformative RNAi Front. Plant Sci. 2019 10 1319 10.3389/fpls.2019.01319 31708946
Dalakouras A. Wassenegger M. Dadami E. Ganopoulos I. Pappas M.L. Papadopoulou K. Genetically modified organism-free RNA interference: Exogenous application of RNA molecules in plants Plant Physiol. 2020 182 38 50 10.1104/pp.19.00570
Vetukuri R.R. Dubey M. Kalyandurg P.B. Carlsson A.S. Whisson S.C. Ortiz R. Spray-induced gene silencing: An innovative strategy for plant trait improvement and disease control Crop Breed. Appl. Biotechnol. 2021 21 e387921S387911 10.1590/1984-70332021v21sa24
Bilir Ö. Göl D. Hong Y. McDowell J.M. Tör M. Small RNA-based plant protection against diseases Front. Plant Sci. 2022 13 2973 10.3389/fpls.2022.951097 36061762
Zhang X. Zhang J. Zhu K. Chitosan/double-stranded RNA nanoparticle-mediated RNA interference to silence chitin synthase genes through larval feeding in the African malaria mosquito (Anopheles gambiae) Insect Mol. Biol. 2010 19 683 693 10.1111/j.1365-2583.2010.01029.x 20629775
Li-Byarlay H. Li Y. Stroud H. Feng S. Newman T.C. Kaneda M. Hou K.K. Worley K.C. Elsik C.G. Wickline S.A. RNA interference knockdown of DNA methyl-transferase 3 affects gene alternative splicing in the honey bee Proc. Natl. Acad. Sci. USA 2013 110 12750 12755 10.1073/pnas.1310735110
Das S. Debnath N. Cui Y. Unrine J. Palli S.R. Chitosan, carbon quantum dot, and silica nanoparticle mediated dsRNA delivery for gene silencing in Aedes aegypti: A comparative analysis ACS Appl. Mater Interfaces 2015 7 19530 19535 10.1021/acsami.5b05232
Chen J. Tang B. Chen H. Yao Q. Huang X. Chen J. Zhang D. Zhang W. Different functions of the insect soluble and membrane-bound trehalase genes in chitin biosynthesis revealed by RNA interference PLoS ONE 2010 5 e10133 10.1371/journal.pone.0010133
Upadhyay S.K. Chandrashekar K. Thakur N. Verma P.C. Borgio J.F. Singh P.K. Tuli R. RNA interference for the control of whiteflies (Bemisia tabaci) by oral route J. Biosci. 2011 36 153 161 10.1007/s12038-011-9009-1
Kennerdell J.R. Carthew R.W. Use of dsRNA-mediated genetic interference to demonstrate that frizzled and frizzled 2 act in the wingless pathway Cell 1998 95 1017 1026 10.1016/S0092-8674(00)81725-0
Timmons L. Fire A. Specific interference by ingested dsRNA Nature 1998 395 854 10.1038/27579 9804418
Dubrovina A.S. Kiselev K.V. Exogenous RNAs for gene regulation and plant resistance Int. J. Mol. Sci. 2019 20 2282 10.3390/ijms20092282 31072065
Lau S.-E. Schwarzacher T. Othman R.Y. Harikrishna J.A. dsRNA silencing of an R2R3-MYB transcription factor affects flower cell shape in a Dendrobium hybrid BMC Plant Biol. 2015 15 194 10.1186/s12870-015-0577-3 26260631
Ulrich J. Dao V.A. Majumdar U. Schmitt-Engel C. Schwirz J. Schultheis D. Ströhlein N. Troelenberg N. Grossmann D. Richter T. Large scale RNAi screen in Tribolium reveals novel target genes for pest control and the proteasome as prime target BMC Genom. 2015 16 674 10.1186/s12864-015-1880-y
Zhu F. Xu J. Palli R. Ferguson J. Palli S.R. Ingested RNA interference for managing the populations of the Colorado potato beetle, Leptinotarsa decemlineata Pest Manag. Sci. 2011 67 175 182 10.1002/ps.2048
Zhang M. Zhou Y. Wang H. Jones H.D. Gao Q. Wang D. Ma Y. Xia L. Identifying potential RNAi targets in grain aphid (Sitobion avenae F.) based on transcriptome profiling of its alimentary canal after feeding on wheat plants BMC Genom. 2013 14 560 10.1186/1471-2164-14-560
Luo Y. Wang X. Wang X. Yu D. Chen B. Kang L. Differential responses of migratory locusts to systemic RNA interference via double-stranded RNA injection and feeding Insect Mol. Biol. 2013 22 574 583 10.1111/imb.12046
Camargo R.D.A. Herai R.H. Santos L.N. Bento F.M. Lima J.E. Marques-Souza H. Figueira A. De novo transcriptome assembly and analysis to identify potential gene targets for RNAi-mediated control of the tomato leafminer (Tuta absoluta) BMC Genom. 2015 16 635 10.1186/s12864-015-1841-5
Bona A.C.D. Chitolina R.F. Fermino M.L. de Castro Poncio L. Weiss A. Lima J.B.P. Paldi N. Bernardes E.S. Henen J. Maori E. Larval application of sodium channel homologous dsRNA restores pyrethroid insecticide susceptibility in a resistant adult mosquito population Parasites Vectors 2016 9 397 10.1186/s13071-016-1634-y
Li H. Jiang W. Zhang Z. Xing Y. Li F. Transcriptome analysis and screening for potential target genes for RNAi-mediated pest control of the beet armyworm, Spodoptera exigua PLoS ONE 2013 8 e65931 10.1371/journal.pone.0065931
Lomazzo E. Hussmann G.P. Wolfe B.B. Yasuda R.P. Perry D.C. Kellar K.J. Effects of chronic nicotine on heteromeric neuronal nicotinic receptors in rat primary cultured neurons J. Neurochem. 2011 119 153 164 10.1111/j.1471-4159.2011.07408.x 21806615
Wang Y. Zhang H. Li H. Miao X. Second-generation sequencing supply an effective way to screen RNAi targets in large scale for potential application in pest insect control PLoS ONE 2011 6 e18644 10.1371/journal.pone.0018644 21494551
Abbasi R. Heschuk D. Kim B. Whyard S. A novel paperclip double-stranded RNA structure demonstrates clathrin-independent uptake in the mosquito Aedes aegypti Insect Biochem. Mol. Biol. 2020 127 103492 10.1016/j.ibmb.2020.103492 33096213
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 Pestic. Biochem. Physiol. 2016 130 1 7 10.1016/j.pestbp.2015.11.005
Sharath Chandra G. Asokan R. Manamohan M. Krishna Kumar N. Enhancing RNAi by using concatemerized double-stranded RNA Pest Manag. Sci. 2019 75 506 514 10.1002/ps.5149
Silver K. Cooper A.M. Zhu K.Y. Strategies for enhancing the efficiency of RNA interference in insects Pest Manag. Sci. 2021 77 2645 2658 10.1002/ps.6277
Bolognesi R. Ramaseshadri P. Anderson J. Bachman P. Clinton W. Flannagan R. Ilagan O. Lawrence C. Levine S. Moar W. Characterizing the mechanism of action of double-stranded RNA activity against western corn rootworm (Diabrotica virgifera virgifera LeConte) PLoS ONE 2012 7 e47534 10.1371/journal.pone.0047534
Miller S.C. Miyata K. Brown S.J. Tomoyasu Y. Dissecting systemic RNA interference in the red flour beetle Tribolium castaneum: Parameters affecting the efficiency of RNAi PLoS ONE 2012 7 e47431 10.1371/journal.pone.0047431
Clemens J.C. Worby C.A. Simonson-Leff N. Muda M. Maehama T. Hemmings B.A. Dixon J.E. Use of double-stranded RNA interference in Drosophila cell lines to dissect signal transduction pathways Proc. Natl. Acad. Sci. USA 2000 97 6499 6503 10.1073/pnas.110149597
Johnson J.A. Bitra K. Zhang S. Wang L. Lynn D.E. Strand M.R. The UGA-CiE1 cell line from Chrysodeixis includens exhibits characteristics of granulocytes and is permissive to infection by two viruses Insect Biochem. Mol. Biol. 2010 40 394 404 10.1016/j.ibmb.2010.03.005
Pridgeon J.W. Zhao L. Becnel J.J. Strickman D.A. Clark G.G. Linthicum K.J. Topically applied AaeIAP1 double-stranded RNA kills female adults of Aedes aegypti J. Med. Entomol. 2008 45 414 420 10.1093/jmedent/45.3.414 18533434
El-Shesheny I. Hajeri S. El-Hawary I. Gowda S. Killiny N. Silencing abnormal wing disc gene of the Asian citrus psyllid, Diaphorina citri disrupts adult wing development and increases nymph mortality PLoS ONE 2013 8 e65392 10.1371/journal.pone.0065392
Gong L. Chen Y. Hu Z. Hu M. Testing insecticidal activity of novel chemically synthesized siRNA against Plutella xylostella under laboratory and field conditions PLoS ONE 2013 8 e62990 10.1371/journal.pone.0062990
Zhang H. Li H. Guan R. Miao X. Lepidopteran insect species-specific, broad-spectrum, and systemic RNA interference by spraying ds RNA on larvae Entomol. Exp. Appl. 2015 155 218 228
Dias N. Cagliari D. Kremer F.S. Rickes L.N. Nava D.E. Smagghe G. Zotti M. The south American fruit fly: An important pest insect with RNAi-sensitive larval stages Front. Physiol. 2019 10 794 10.3389/fphys.2019.00794 31316391
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 Nat. Biotechnol. 2007 25 1307 1313 10.1038/nbt1352
Avila L. Chandrasekar R. Wilkinson K. Balthazor J. Heerman M. Bechard J. Brown S. Park Y. Dhar S. Reeck G. Delivery of lethal dsRNAs in insect diets by branched amphiphilic peptide capsules J. Control. Release 2018 273 139 146 10.1016/j.jconrel.2018.01.010
Zhang J. Khan S.A. Heckel D.G. Bock R. Next-generation insect-resistant plants: RNAi-mediated crop protection Trends Biotechnol. 2017 35 871 882 10.1016/j.tibtech.2017.04.009
Marques V.V. Angelotti-Mendonça J. Roberto S.R. Advances and challenges in RNA interference technology for citrus Huanglongbing vector control Horticulturae 2021 7 277 10.3390/horticulturae7090277
Allen M.L. Walker W.B. III Saliva of Lygus lineolaris digests double stranded ribonucleic acids J. Insect Physiol. 2012 58 391 396 10.1016/j.jinsphys.2011.12.014
Guan R.-B. Li H.-C. Fan Y.-J. Hu S.-R. Christiaens O. Smagghe G. Miao X.-X. A nuclease specific to lepidopteran insects suppresses RNAi J. Biol. Chem. 2018 293 6011 6021 10.1074/jbc.RA117.001553 29500196
Katoch R. Thakur N. Insect gut nucleases: A challenge for RNA interference mediated insect control strategies Int. J. Biochem. Biotechnol. 2012 1 198 203
Kennedy S. Wang D. Ruvkun G. A conserved siRNA-degrading RNase negatively regulates RNA interference in C. elegans Nature 2004 427 645 649 10.1038/nature02302 14961122
Dias N. Cagliari D. Dos Santos E. Smagghe G. Jurat-Fuentes J. Mishra S. Nava D. Zotti M. Insecticidal gene silencing by RNAi in the neotropical region Neotrop. Entomol. 2020 49 1 11 10.1007/s13744-019-00722-4
Cooper A.M. Silver K. Zhang J. Park Y. Zhu K.Y. Molecular mechanisms influencing efficiency of RNA interference in insects Pest Manag. Sci. 2019 75 18 28 10.1002/ps.5126
Laisney J. Rose V.L. Watters K. Donohue K.V. Unrine J.M. Delivery of short hairpin RNA in the neotropical brown stink bug, Euschistus heros, using a composite nanomaterial Pestic. Biochem. Physiol. 2021 177 104906 10.1016/j.pestbp.2021.104906
Pugsley C.E. Isaac R.E. Warren N.J. Cayre O.J. Recent advances in engineered nanoparticles for RNAi-mediated crop protection against insect pests Front. Agron. 2021 3 652981 10.3389/fagro.2021.652981
Xu P. Zhang Y. Kang L. Roossinck M.J. Mysore K.S. Computational estimation and experimental verification of off-target silencing during posttranscriptional gene silencing in plants Plant Physiol. 2006 142 429 440 10.1104/pp.106.083295
Reddy K. Rajam M. Targeting chitinase gene of Helicoverpa armigera by host-induced RNA interference confers insect resistance in tobacco and tomato Plant Mol. Biol. 2016 90 281 292
Senthil-Kumar M. Mysore K.S. Virus-induced gene silencing can persist for more than 2 years and also be transmitted to progeny seedlings in Nicotiana benthamiana and tomato Plant Biotechnol. J. 2011 9 797 806 10.1111/j.1467-7652.2011.00589.x
Ahmed F. Senthil-Kumar M. Dai X. Ramu V.S. Lee S. Mysore K.S. Zhao P.X. pssRNAit: A web server for designing effective and specific plant siRNAs with genome-wide off-target assessment Plant Physiol. 2020 184 65 81 10.1104/pp.20.00293 32651189
Horn T. Boutros M. E-RNAi: A web application for the multi-species design of RNAi reagents-2010 update Nucleic Acids Res. 2010 38 W332 W339 10.1093/nar/gkq317 20444868
Naito Y. Yamada T. Matsumiya T. Ui-Tei K. Saigo K. Morishita S. dsCheck: Highly sensitive off-target search software for double-stranded RNA-mediated RNA interference Nucleic Acids Res. 2005 33 W589 W591 10.1093/nar/gki419
Altschul S.F. Gish W. Miller W. Myers E.W. Lipman D.J. Basic local alignment search tool J. Mol. Biol. 1990 215 403 410 10.1016/S0022-2836(05)80360-2 2231712
Zhao J.H. Zhang T. Liu Q.Y. Guo H.S. Trans-kingdom RNAs and their fates in recipient cells: Advances, utilization, and perspectives Plant Commun. 2021 2 100167 10.1016/j.xplc.2021.100167 33898979
Yan S. Ren B. Zeng B. Shen J. Improving RNAi efficiency for pest control in crop species BioTechniques 2020 68 283 290 10.2144/btn-2019-0171
Liu S. Geng S. Li A. Mao Y. Mao L. RNAi technology for plant protection and its application in wheat aBIOTECH 2021 2 365 374 10.1007/s42994-021-00036-3
Mitter N. Worrall E.A. Robinson K.E. Li P. Jain R.G. Taochy C. Fletcher S.J. Carroll B.J. Lu G. Xu Z.P. Clay nanosheets for topical delivery of RNAi for sustained protection against plant viruses Nat. Plants 2017 3 16207 10.1038/nplants.2016.207
Mitter N. Worrall E.A. Robinson K.E. Xu Z.P. Carroll B.J. Induction of virus resistance by exogenous application of double-stranded RNA Curr. Opin. Virol. 2017 26 49 55 10.1016/j.coviro.2017.07.009
Huang C.-Y. Wang H. Hu P. Hamby R. Jin H. Small RNAs-big players in plant-microbe interactions Cell Host Microbe 2019 26 173 182 10.1016/j.chom.2019.07.021
Kumar S. Nehra M. Dilbaghi N. Marrazza G. Hassan A.A. Kim K.-H. Nano-based smart pesticide formulations: Emerging opportunities for agriculture J. Control. Release 2019 294 131 153 10.1016/j.jconrel.2018.12.012 30552953
Li J. Qian J. Xu Y. Yan S. Shen J. Yin M. A facile-synthesized star polycation constructed as a highly efficient gene vector in pest management ACS Sustain. Chem. Eng. 2019 7 6316 6322 10.1021/acssuschemeng.9b00004
Fletcher S.J. Reeves P.T. Hoang B.T. Mitter N. A perspective on RNAi-based biopesticides Front. Plant Sci. 2020 11 51 10.3389/fpls.2020.00051
Cai Q. He B. Wang S. Fletcher S. Niu D. Mitter N. Birch P.R. Jin H. Message in a bubble: Shuttling small RNAs and proteins between cells and interacting organisms using extracellular vesicles Annu. Rev. Plant Biol. 2021 72 497 10.1146/annurev-arplant-081720-010616
Zuo Y. Wang H. Xu Y. Huang J. Wu S. Wu Y. Yang Y. CRISPR/Cas9 mediated G4946E substitution in the ryanodine receptor of Spodoptera exigua confers high levels of resistance to diamide insecticides Insect Biochem. Mol. Biol. 2017 89 79 85 10.1016/j.ibmb.2017.09.005 28912111
Wang J. Zhang H. Wang H. Zhao S. Zuo Y. Yang Y. Wu Y. Functional validation of cadherin as a receptor of Bt toxin Cry1Ac in Helicoverpa armigera utilizing the CRISPR/Cas9 system Insect Biochem. Mol. Biol. 2016 76 11 17 10.1016/j.ibmb.2016.06.008 27343383
Ye Z.-F. Liu X.-L. Han Q. Liao H. Dong X.-T. Zhu G.-H. Dong S.-L. Functional characterization of PBP1 gene in Helicoverpa armigera (Lepidoptera: Noctuidae) by using the CRISPR/Cas9 system Sci. Rep. 2017 7 8470 10.1038/s41598-017-08769-2
Dong X.T. Liao H. Zhu G.H. Khuhro S.A. Ye Z.F. Yan Q. Dong S.L. CRISPR/Cas9-mediated PBP1 and PBP3 mutagenesis induced significant reduction in electrophysiological response to sex pheromones in male Chilo suppressalis Insect Sci. 2019 26 388 399 10.1111/1744-7917.12544
Zhu G.-H. Peng Y.-C. Zheng M.-Y. Zhang X.-Q. Sun J.-B. Huang Y. Dong S.-L. CRISPR/Cas9 mediated BLOS2 knockout resulting in disappearance of yellow strips and white spots on the larval integument in Spodoptera litura J. Insect Physiol. 2017 103 29 35 10.1016/j.jinsphys.2017.09.008
Bi H.L. Xu J. Tan A.J. Huang Y.P. CRISPR/Cas9-mediated targeted gene mutagenesis in Spodoptera litura Insect Sci. 2016 23 469 477 10.1111/1744-7917.12341
Zhao Y. Huang G. Zhang W. Mutations in NlInR1 affect normal growth and lifespan in the brown planthopper Nilaparvata lugens Insect Biochem. Mol. Biol. 2019 115 103246 10.1016/j.ibmb.2019.103246 31618682
Lu H.-P. Luo T. Fu H.-W. Wang L. Tan Y.-Y. Huang J.-Z. Wang Q. Ye G.-Y. Gatehouse A.M. Lou Y.-G. Resistance of rice to insect pests mediated by suppression of serotonin biosynthesis Nat. Plants 2018 4 338 344 10.1038/s41477-018-0152-7 29735983
Seni A. Frontier insect pest management technologies for sustainable rice production J. Cereal Res. 2021 13 136 148 10.25174/2582-2675/2021/113113