Brassica-aphid interaction: Challenges and prospects of genetic engineering for integrated aphid management

Abassi, 2000, Response of the seven-spot ladybird to an aphid alarm pheromone and an alarm pheromone inhibitor is mediated by paired olfactory cells, J. Chem. Ecol., 26, 1765, 10.1023/A:1005555300476 Afzal, 2008, Plant receptor-like serine threonine kinases: roles in signaling and plant defense, Mol. Plant Microbe Interact., 21, 507, 10.1094/MPMI-21-5-0507 Agarwala, 2007, Phenotypic plasticity in aphids (Homoptera: Insecta): components of variation and causative factors, Curr. Sci. Bangalore, 93, 308 Aharoni, 2003, Terpenoid metabolism in wild-type and transgenic Arabidopsis plants, Plant Cell, 15, 2866, 10.1105/tpc.016253 Ahemad, 2012, Effects of pesticides on plant growth promoting traits of Mesorhizobium strain MRC4, J. Saudi Soc. Agric. Sci., 11, 63 Ahuja, 2010, Defence mechanisms of Brassicaceae: implications for plant-insect interactions and potential for integrated pest management. A review, Agron. Sustain. Dev., 30, 311, 10.1051/agro/2009025 Antolín-Llovera, 2012, Receptor kinase signalling in plant–microbe interactions, Annu. Rev. Phytopathol., 50, 451, 10.1146/annurev-phyto-081211-173002 Atamian, 2013, In planta expression or delivery of potato aphid Macrosiphum euphorbiae effectors Me10 and Me23 enhances aphid fecundity, Mol. Plant Microbe Interact., 26, 67, 10.1094/MPMI-06-12-0144-FI Azzouz, 2005, Effects of plant protease inhibitors, oryzacystatin I and soybean Bowman–Birk inhibitor, on the aphid Macrosiphum euphorbiae (Homoptera, Aphididae) and its parasitoid Aphelinus abdominalis (Hymenoptera, Aphelinidae), J. Insect Physiol., 51, 75, 10.1016/j.jinsphys.2004.11.010 Bachman, 2013, Characterization of the spectrum of insecticidal activity of a double-stranded RNA with targeted activity against western corn rootworm (Diabrotica virgifera virgifera Le Conte), Transgenic Res., 22, 1207, 10.1007/s11248-013-9716-5 Bahlai, 2010, Choosing organic pesticides over synthetic pesticides may not effectively mitigate environmental risk in soybeans, PLoS One, 5, 10.1371/journal.pone.0011250 Bakhetia, 1991, Insect pests, 211 Baldwin, 2010, Plant volatiles, Curr. Biol., 20, R392, 10.1016/j.cub.2010.02.052 Bale, 2008, Biological control and sustainable food production, Philos. Trans. R. Soc. Biol. Sci., 363, 761, 10.1098/rstb.2007.2182 Beale, 2006, Aphid alarm pheromone produced by transgenic plants affects aphid and parasitoid behavior, Proc. Natl. Acad. Sci., 103, 10509, 10.1073/pnas.0603998103 Bhatia, 2012, Host generated siRNAs attenuate expression of serine protease gene in Myzus persicae, PLoS One, 7, 10.1371/journal.pone.0046343 Bhatia, 2011, Aphid resistance in Brassica crops: challenges, biotechnological progress and emerging possibilities, Biotechnol. Adv., 29, 879, 10.1016/j.biotechadv.2011.07.005 Bhattacharya, 2012, Production of nutritionally desirable fatty acids in seed oil of Indian mustard (Brassica juncea L.) by metabolic engineering, Phytochem. Rev., 11, 197, 10.1007/s11101-012-9228-6 Birch, 1999, Tri-trophic interactions involving pest aphids, predatory 2-spot ladybirds and transgenic potatoes expressing snowdrop lectin for aphid resistance, Mol. Breed., 5, 75, 10.1023/A:1009659316170 Blackman, 2000, 466 Bonning, 2014, Toxin delivery by the coat protein of an aphid-vectored plant virus provides plant resistance to aphids, Nat. Biotechnol., 32, 102, 10.1038/nbt.2753 Bos, 2010, A functional genomics approach identifies candidate effectors from the aphid species Myzus persicae (green peach aphid), PLoS Genet., 6, 10.1371/journal.pgen.1001216 Bravo, 2004, Oligomerization triggers binding of a Bacillus thuringiensis Cry1Ab pore-forming toxin to aminopeptidase N receptor leading to insertion into membrane microdomains, Biochem. Biophys. Acta, 1667, 38, 10.1016/j.bbamem.2004.08.013 Campbell, 1990, The role of plant matrix polysaccharides in aphid-plant interactions, 149 Carlini, 2002, Plant toxic proteins with insecticidal properties. A review on their potentialities as bioinsecticides, Toxicon, 40, 1515, 10.1016/S0041-0101(02)00240-4 Carrillo, 2011, A barley cysteine-proteinase inhibitor reduces the performance of two aphid species in artificial diets and transgenic Arabidopsis plants, Transgenic Res., 20, 305, 10.1007/s11248-010-9417-2 Ceci, 2003, Selection by phage display of a variant mustard trypsin inhibitor toxic against aphids, Plant J., 33, 557, 10.1046/j.1365-313X.2003.01645.x Chang, 2003, Transformation of tobacco with genes encoding Helianthus tuberosus Agglutinin (HTA) confers resistance to peach-potato aphid (Myzus persicae), Transgenic Res., 12, 607, 10.1023/A:1025810213869 Cherqui, 2000, Salivary proteins of aphids, a pilot study on identification, separation and immunolocalisation, J. Insect Physiol., 46, 1177, 10.1016/S0022-1910(00)00037-8 Chougule, 2012, Toxins for transgenic resistance to hemipteran pests, Toxins, 4, 405, 10.3390/toxins4060405 Chougule, 2013, Retargeting of the Bacillus thuringiensis toxin Cyt2Aa against hemipteran insect pests, Proc. Natl. Acad. Sci., 110, 8465, 10.1073/pnas.1222144110 Cintas, 2002, A new pathovar, Pseudomonas syringae pv. alisalensis pv. nov., proposed for the causal agent of bacterial blight of broccoli and broccoli raab, Plant Dis., 86, 992, 10.1094/PDIS.2002.86.9.992 Collins, 2005, Biotype 2 Russian wheat aphid resistance among wheat germplasm accessions, Crop Sci., 45, 1877, 10.2135/cropsci2004.0730 Conrad Dixon, 1985, Structure of aphid populations, Annu. Rev. Entomol., 30, 155, 10.1146/annurev.en.30.010185.001103 Dixon, 2005 Dogimont, 2014, The Vat locus encodes for a CC-NBS-LRR protein that confers resistance to Aphis gossypii infestation and A. gossypii-mediated virus resistance, Plant J., 80, 993, 10.1111/tpj.12690 Du, 1998, Identification of semiochemicals released during aphid feeding that attract parasitoid Aphidius ervi, J. Chem. Ecol., 24, 1355, 10.1023/A:1021278816970 Dutta, 2005, Constitutive and phloem specific expression of Allium sativum leaf agglutinin (ASAL) to engineer aphid (Lipaphis erysimi) resistance in transgenic Indian mustard (Brassica juncea), Plant Sci., 169, 996, 10.1016/j.plantsci.2005.05.016 Elzinga, 2014, Suppression of plant defenses by a Myzus persicae (green peach aphid) salivary effector protein, Mol. Plant Microbe Interact., 27, 747, 10.1094/MPMI-01-14-0018-R Elzinga, 2013, The role of protein effectors in plant–aphid interactions, Curr. Opin. Plant Biol., 16, 451, 10.1016/j.pbi.2013.06.018 Esen, 1993, β-Glucosidases: overview chapter 1, 1 FAOSTAT Felton, 1999, Herbivore saliva and its effects on plant defense against herbivores and pathogens, 19 Fire, 1998, Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans, Nature, 391, 806, 10.1038/35888 Foster, 2005, Reduced response of insecticide-resistant aphids and attraction of parasitoids to aphid alarm pheromone; a potential fitness trade-off, Bull. Entomol. Res., 95, 37, 10.1079/BER2004336 Foyer, 2015, Systematic analysis of phloem-feeding insect-induced transcriptional reprogramming in Arabidopsis highlights common features and reveals distinct responses to specialist and generalist insects, J. Exp. Bot., 66, 495, 10.1093/jxb/eru491 Gao, 2010, Identification of potential early regulators of aphid resistance in Medicago truncatula via transcription factor analysis, New Phytol., 186, 980, 10.1111/j.1469-8137.2010.03229.x Gatehouse, 1999, Concanavalin A inhibits development of tomato moth (Lacanobia oleracea) and peach-potato aphid (Myzus persicae) when expressed in transgenic potato plants, Mol. Breed., 5, 153, 10.1023/A:1009681705481 Gatehouse, 1996, Transgenic potato plants with enhanced resistance to the peach-potato aphid Myzus persicae, Entomol. Exp. Appl., 79, 295, 10.1111/j.1570-7458.1996.tb00837.x Giordanengo, 2010, Compatible plant–aphid interactions: how aphids manipulate plant responses?, Comptes Rendus Biol., 333, 516, 10.1016/j.crvi.2010.03.007 Godard, 2007, Testing of a heterologous, wound-and insect-inducible promoter for functional genomics studies in conifer defense, Plant Cell Rep., 26, 2083, 10.1007/s00299-007-0417-5 Guerena, 2006, 1 Hannon, 2002, RNA interference, Nature, 418, 244, 10.1038/418244a Hardie, 1999, 227 Hilder, 1995, Expression of snowdrop lectin in transgenic tobacco plants results in added protection against aphids, Transgenic Res., 4, 18, 10.1007/BF01976497 Hogervorst, 2009, Snowdrop lectin (Galanthus nivalis agglutinin) in aphid honeydew negatively affects survival of a honeydew‐consuming parasitoid, Agric. For. Entomol., 11, 161, 10.1111/j.1461-9563.2008.00412.x Hossain, 2006, Transgenic expression of onion leaf lectin gene in Indian mustard offers protection against aphid colonization, Crop Sci., 46, 2022, 10.2135/cropsci2005.11.0418 Jaouannet, 2014, Plant immunity in plant–aphid interactions, Front. Plant Sci., 5, 663, 10.3389/fpls.2014.00663 Jaubert-Possamai, 2007, Gene knockdown by RNAi in the pea aphid Acyrthosiphon pisum, BMC Biotechnol., 7, 1, 10.1186/1472-6750-7-63 Jin, 2012, Pinellia ternata agglutinin expression in chloroplasts confers broad spectrum resistance against aphid, whitefly, Lepidopteran insects, bacterial and viral pathogens, Plant Biotechnol. J., 10, 313, 10.1111/j.1467-7652.2011.00663.x Jun, 2012, Genetic mapping revealed two loci for soybean aphid resistance in PI 567301B, Theor. Appl. Genet., 124, 13, 10.1007/s00122-011-1682-9 Kanrar, 2002, Transgenic Indian mustard (Brassica juncea) with resistance to the mustard aphid (Lipaphis erysimi Kalt.), Plant Cell Rep., 20, 976, 10.1007/s00299-001-0422-z Kato, 2010, Expression of gene for Dioscorea batatas tuber lectin 1 in transgenic tobacco confers resistance to green-peach aphid, Plant Biotechnol., 27, 141, 10.5511/plantbiotechnology.27.141 Kettles, 2016, The potato aphid salivary effector Me47 is a glutathione-S-transferase involved in modifying plant responses to aphid infestation, Front. Plant Sci., 7, 10.3389/fpls.2016.01142 Kim, 2010, Fine mapping of the soybean aphid-resistance gene Rag2 in soybean PI 200538, Theor. Appl. Genet., 121, 599, 10.1007/s00122-010-1333-6 Kim, 2011, Resistance against beet armyworms and cotton aphids in caffeine-producing transgenic chrysanthemum, Plant Biotechnol., 28, 393, 10.5511/plantbiotechnology.11.0510a Kleczkowski, 1995, Phytohormone conjugates: nature and function, Crit. Rev. Plant Sci., 14, 283, 10.1080/07352689509382361 Klingler, 2005, Aphid resistance in Medicago truncatula involves antixenosis and phloem-specific, inducible antibiosis, and maps to a single locus flanked by NBS-LRR resistance gene analogs, Plant Physiol., 137, 1445, 10.1104/pp.104.051243 Klingler, 2007, Independent action and contrasting phenotypes of resistance genes against spotted alfalfa aphid and bluegreen aphid in Medicago truncatula, New Phytol., 173, 630, 10.1111/j.1469-8137.2006.01939.x Klingler, 2009, A single gene, AIN, in Medicago truncatula mediates a hypersensitive response to both bluegreen aphid and pea aphid, but confers resistance only to bluegreen aphid, J. Exp. Bot., 60, 4115, 10.1093/jxb/erp244 Köpke, 2008, Does egg deposition by herbivorous pine sawflies affect transcription of sesquiterpene synthases in pine?, Planta, 228, 427, 10.1007/s00425-008-0747-8 Kumar, 2011, Screening of wild crucifers for resistance to mustard aphid, Lipaphis erysimi (Kaltenbach) and attempt at introgression of resistance gene (s) from Brassica fruticulosa to Brassica juncea, Euphytica, 179, 461, 10.1007/s10681-011-0351-z Kunert, 2005, Alarm pheromone mediates production of winged dispersal morphs in aphids, Ecol. Lett., 8, 596, 10.1111/j.1461-0248.2005.00754.x Lam, 1996, Use of trichosanthin to reduce infection by turnip mosaic virus, Plant Sci., 114, 111, 10.1016/0168-9452(95)04310-1 Langridge, 1989, Dual promoter of Agrobacterium tumefaciens mannopine synthase genes is regulated by plant growth hormones, Proc. Natl. Acad. Sci., 86, 3219, 10.1073/pnas.86.9.3219 Le Coz, 2011, Plants and plant products, 873 Li, 2011, A comprehensive assessment of the effects of Bt cotton on Coleomegilla maculata demonstrates no detrimental effects by Cry1Ac and Cry2Ab, PLoS One, 6, 10.1371/journal.pone.0022185 Lodge, 1993, Broad-spectrum virus resistance in transgenic plants expressing pokeweed antiviral protein, Proc. Natl. Acad. Sci., 90, 7089, 10.1073/pnas.90.15.7089 Louis, 2012, Arabidopsis thaliana—aphid interaction, Arabidopsis Book, 10, 10.1199/tab.0159 Mao, 2014, Plant-mediated RNAi of a gap gene-enhanced tobacco tolerance against the Myzus persicae, Transgenic Res., 23, 145, 10.1007/s11248-013-9739-y McCarville, 2012, Measuring the benefit of biological control for single gene and pyramided host plant resistance for Aphis glycines (Hemiptera: Aphididae) management, J. Econ. Entomol., 105, 1835, 10.1603/EC12043 McCreight, 2008, Potential sources of genetic resistance in Lactuca spp. to the lettuce aphid, Nasanovia ribisnigri (Mosely) (Homoptera: Aphididae), Hortscience, 43, 1355, 10.21273/HORTSCI.43.5.1355 McCreight, 1984, AR Hale's Best Jumbo, AR 5, and AR Topmark: melon aphid-resistant muskmelon breeding lines, Hortscience, 19, 309, 10.21273/HORTSCI.19.2.309 McHale, 2006, Plant NBS-LRR proteins: adaptable guards, Genome Biol., 7, 212, 10.1186/gb-2006-7-4-212 Mehlo, 2005, An alternative strategy for sustainable pest resistance in genetically enhanced crops, Proc. Natl. Acad. Sci., 102, 7812, 10.1073/pnas.0502871102 Micha, 1996, Aphid alarm pheromone (E)-β-farnesene: a host finding kairomone for the aphid primary parasitoid Aphidius uzbekistanicus (Hymenoptera: aphidiinae), Chemoecology, 7, 132, 10.1007/BF01245965 Miles, 1999, Aphid saliva, Biol. Rev. Camb. Philos. Soc., 74, 41, 10.1017/S0006323198005271 Miles, 1993, The significance of antioxidants in the aphid‐plant interaction: the redox hypothesis, Entomol. Exp. Appl., 67, 275, 10.1111/j.1570-7458.1993.tb01678.x Moon, 1997, Expression of a cDNA encoding Phytolacca insularis antiviral protein confers virus resistance on transgenic potato plants, Mol. Cells, 7, 807 Moran, 1992, The evolution of aphid life cycles, Annu. Rev. Entomol., 37, 321, 10.1146/annurev.en.37.010192.001541 Morkunas, 2011, Phytohormonal signaling in plant responses to aphid feeding, Acta Physiol. Plant., 33, 2057, 10.1007/s11738-011-0751-7 Mornhinweg, 1995, Inheritance of Russian wheat aphid resistance in spring barley, Crop Sci., 35, 1368, 10.2135/cropsci1995.0011183X003500050018x Mutti, 2008, A protein from the salivary glands of the pea aphid, Acyrthosiphon pisum, is essential in feeding on a host plant, Proc. Natl. Acad. Sci., 105, 9965, 10.1073/pnas.0708958105 Mutti, 2006, RNAi knockdown of a salivary transcript leading to lethality in the pea aphid, Acyrthosiphon pisum, J. Insect Sci., 6, 38 Nagaharu, 1935, Genome analysis in Brassica with special reference to the experimental formation of B. napus and peculiar mode of fertilization, J. Jpn. Bot., 7, 389 Oerke, 2006, Crop losses to pests, J. Agric. Sci., 144, 31, 10.1017/S0021859605005708 Pitino, 2011, Silencing of aphid genes by dsRNA feeding from plants, PLoS One, 6, 10.1371/journal.pone.0025709 Pitino, 2013, Aphid protein effectors promote aphid colonization in a plant species-specific manner, Mol. Plant Microbe Interact., 26, 130, 10.1094/MPMI-07-12-0172-FI Powell, 2005, Intracellular salivation is the aphid activity associated with inoculation of non-persistently transmitted viruses, J. Gen. Virol., 86, 469, 10.1099/vir.0.80632-0 Prashar, 2016, Impact of fertilizers and pesticides on soil microflora in agriculture, Sustain. Agric. Rev., 19, 331, 10.1007/978-3-319-26777-7_8 Rahbé, 2003, Effects of the cysteine protease inhibitor oryzacystatin (OC-I) on different aphids and reduced performance of Myzus persicae on OC-I expressing transgenic oilseed rape, Plant Sci., 164, 441, 10.1016/S0168-9452(02)00402-8 Ram, 2017, Dentification and comprehensive evaluation of reference genes for RT-qPCR analysis of host gene-expression in Brassica juncea-aphid interaction using microarray data, Plant Physiol. Biochem., 116, 57, 10.1016/j.plaphy.2017.05.004 Raymer, 2002, Canola: an emerging oilseed crop Ribeiro, 2006, Effect of eggplant transformed with oryza cystatin gene on Myzus persicae and Macrosiphum euphorbiae, J. Appl. Entomol., 130, 84, 10.1111/j.1439-0418.2005.01021.x Roberts, 1986, Plant proteins that inactivate foreign ribosomes, Biosci. Rep., 6, 19, 10.1007/BF01145175 Rodriguez, 2013, Toward understanding the role of aphid effectors in plant infestation, Mol. Plant Microbe Interact., 26, 25, 10.1094/MPMI-05-12-0119-FI Rossi, 1998, The nematode resistance gene Mi of tomato confers resistance against the potato aphid, Proc. Natl. Acad. Sci., 95, 9750, 10.1073/pnas.95.17.9750 Sampaio, 2017, Brassica aphid (Hemiptera: Aphididae) populations are conditioned by climatic variables and parasitism level: a study case of Triângulo Mineiro, Brazil, Bull. Entomol. Res., 107, 410, 10.1017/S0007485317000220 Schmid, 2002, Combinatorial RNAi: a method for evaluating the functions of gene families in Drosophila, Trends Neurosci., 25, 71, 10.1016/S0166-2236(02)02034-9 Schnee, 2006, The products of a single maize sesquiterpene synthase form a volatile defense signal that attracts natural enemies of maize herbivores, Proc. Natl. Acad. Sci., 103, 1129, 10.1073/pnas.0508027103 Schnepf, 1998, Bacillus thuringiensis and its pesticidal crystal proteins, Microbiol. Mol. Biol. Rev., 62, 775, 10.1128/MMBR.62.3.775-806.1998 Shahidi-Noghabi, 2008, Carbohydrate-binding activity of the type-2 ribosome-inactivating protein SNA-I from elderberry (Sambucus nigra) is a determining factor for its insecticidal activity, Phytochemistry, 69, 2972, 10.1016/j.phytochem.2008.09.012 Shakesby, 2009, A water-specific aquaporin involved in aphid osmoregulation, Insect Biochem. Mol. Biol., 39, 1, 10.1016/j.ibmb.2008.08.008 Sharma, 2000, Prospects for using transgenic resistance to insects in crop improvement, Electron. J. Biotechnol., 3, 21, 10.2225/vol3-issue2-fulltext-3 Sharma, 2017, Evaluation the potentiality of some parameters to probe the elevated levels of resistance in Brassica sp. at the early period of aphid infestation in open field condition, J. Entomol. Zool. Stud., 5, 1356 Soufbaf, 2018, Finish line plant-insect interactions mediated by insect feeding mode and plant interference: a case study of Brassica interactions with diamondback moth and turnip aphid, Insect Sci., 25, 690, 10.1111/1744-7917.12439 Stern Thorpe, 2016, Comparative transcriptomics and proteomics of three different aphid species identifies core and diverse effector sets, BMC Genomics, 17, 172, 10.1186/s12864-016-2496-6 Timmons, 2001, Ingestion of bacterially expressed dsRNAs can produce specific and potent genetic interference in Caenorhabditis elegans, Gene, 263, 103, 10.1016/S0378-1119(00)00579-5 Timmons, 1998, Specific interference by ingested dsRNA, Nature, 395, 10.1038/27579 Tiwari, 2011, Expression of delta-endotoxin cry1EC from wound inducible promoter confers insect protection in peanut (Arachis hypogea L.) plants, Pest Manag. Sci., 67, 137, 10.1002/ps.2041 Tran, 1997, Plant proteinase inhibitors are potential anticereal aphid compounds, J. Econ. Entomol., 90, 1672, 10.1093/jee/90.6.1672 Vandenborre, 2011, Plant lectins as defense proteins against phytophagous insects, Phytochemistry, 72, 1538, 10.1016/j.phytochem.2011.02.024 Verhoeven, 1997, A review of mechanisms underlying anticarcinogenicity by Brassica vegetables, Chem. Biol. Interact., 103, 79, 10.1016/S0009-2797(96)03745-3 Wang, 2001, Suppression of a P450 hydroxylase gene in plant trichome glands enhances natural-product-based aphid resistance, Nat. Biotechnol., 19, 371, 10.1038/86770 Wang, 2015, Armet is an effector protein mediating aphid–plant interactions, FASEB J., 29, 2032, 10.1096/fj.14-266023 Wang, 2015, Angiotensin-converting enzymes modulate aphid–plant interactions, Sci. Rep., 5, 8885, 10.1038/srep08885 Wang, 2005, Enhancement of resistance to aphids by introducing the snowdrop lectin genegna into maize plants, J. Biosci., 30, 627, 10.1007/BF02703563 Whyard, 2009, Ingested double-stranded RNAs can act as species-specific insecticides, Insect Biochem. Mol. Biol., 39, 824, 10.1016/j.ibmb.2009.09.007 Will, 2009, Aphid watery saliva counteracts sieve-tube occlusion: a universal phenomenon?, J. Exp. Biol., 212, 3305, 10.1242/jeb.028514 Will, 2007, Molecular sabotage of plant defense by aphid saliva, Proc. Natl. Acad. Sci., 104, 10536, 10.1073/pnas.0703535104 Will, 2006, Physical and chemical interactions between aphids and plants, J. Exp. Bot., 57, 729, 10.1093/jxb/erj089 Will, 2013, Aphid-proof plants: biotechnology-based approaches for Aphid control, 179 Wroblewski, 2007, Silencing of the major family of NBS–LRR‐encoding genes in lettuce results in the loss of multiple resistance specificities, Plant J., 51, 803, 10.1111/j.1365-313X.2007.03182.x Wu, 2014, Innate immune sensing and signaling of cytosolic nucleic acids, Annu. Rev. Immunol., 32, 461, 10.1146/annurev-immunol-032713-120156 Wu, 2006, Transgenic cotton, expressing Amaranthus caudatus agglutinin, confers enhanced resistance to aphids, Plant Breed., 125, 390, 10.1111/j.1439-0523.2006.01247.x Wulff, 2019, Neonicotinoid insecticides alter the transcriptome of soybean and decrease plant resistance, Int. J. Mol. Sci., 20, 783, 10.3390/ijms20030783 Xu, 2014, Silencing of an aphid carboxylesterase gene by use of plant-mediated RNAi impairs Sitobion avenae tolerance of Phoxim insecticides, Transgenic Res., 23, 389, 10.1007/s11248-013-9765-9 Yao, 2003, Transgenic tobacco expressing Pinellia ternata agglutinin confers enhanced resistance to aphids, Transgenic Res., 12, 715, 10.1023/B:TRAG.0000005146.05655.7d Ye, 2009, Transgenic tobacco expressing Zephyranthes grandiflora agglutinin confers enhanced resistance to aphids, Appl. Biochem. Biotechnol., 158, 615, 10.1007/s12010-008-8418-6 Yu, 2014, Engineering plants for aphid resistance: current status and future perspectives, Theor. Appl. Genet., 127, 2065, 10.1007/s00122-014-2371-2 Yu, 2012, E)-β-farnesene synthase genes affect aphid (Myzus persicae) infestation in tobacco (Nicotiana tabacum), Funct. Integr. Genom., 12, 207, 10.1007/s10142-011-0244-1 Yu, 2008, Increased oriental armyworm and aphid resistance in transgenic wheat stably expressing Bacillus thuringiensis (Bt) endotoxin and Pinellia ternata agglutinin (PTA), Plant Cell Tissue Organ Cult., 94, 33, 10.1007/s11240-008-9384-y Zhang, 2010, A novel locus for soybean aphid resistance, Theor. Appl. Genet., 120, 1183, 10.1007/s00122-009-1245-5 Zhang, 2006, Genetic analyses of agronomic and seed quality traits of synthetic oilseed Brassica napus produced from interspecific hybridization of B. campestris and B. oleracea, J. Genet., 85, 45, 10.1007/BF02728969 Zhang, 2013, Feasibility, limitation and possible solutions of RNAi‐based technology for insect pest control, Insect Sci., 20, 15, 10.1111/j.1744-7917.2012.01513.x Zhang, 2011, Arabidopsis Argonaute 2 Regulates innate immunity via miRNA393(∗)-mediated silencing of a Golgi-localized snare gene, MEMB12. Mol. cell, 42, 356, 10.1016/j.molcel.2011.04.010 Zhou, 2001, Oilseed rape, 78