Engineering plants for aphid resistance: Current status and future perspectives

Theoretical and Applied Genetics

Volumn 127, Issue 10, 2014, Pages 2065-2083

  Yu, Xiudao ^a,b   Wang, Genping ^a   Huang, Siliang ^b   Ma, Youzhi ^a   Xia, Lanqin ^a  

^a INSTITUTE OF PLANT PROTECTION   (China)

^b NANYANG NORMAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CROPS; GENES; INSECTICIDES; METABOLISM; POLLUTION CONTROL; TOXICITY;

AGRICULTURAL PESTS; CURRENT STATUS OF DEVELOPMENT; ENVIRONMENTAL POLLUTIONS; FUTURE PERSPECTIVES; INSECTICIDE RESISTANCE; NON-TARGET ORGANISM; PLANT SECONDARY METABOLISM; POTENTIAL NEGATIVE EFFECTS;

PLANTS (BOTANY);

APHIDIDAE;

BACTERIAL PROTEIN; ENDOTOXIN; HEMOLYSIN; INSECTICIDAL CRYSTAL PROTEIN, BACILLUS THURINGIENSIS; LECTIN; PROTEINASE INHIBITOR;

ANIMAL; APHID; BIOLOGICAL PEST CONTROL; CROP; GENETICS; METABOLISM; PROCEDURES; RNA INTERFERENCE; TRANSGENIC PLANT; TRENDS;

ANIMALS; APHIDS; BACTERIAL PROTEINS; CROPS, AGRICULTURAL; ENDOTOXINS; HEMOLYSIN PROTEINS; LECTINS; METABOLIC NETWORKS AND PATHWAYS; PEST CONTROL, BIOLOGICAL; PLANTS, GENETICALLY MODIFIED; PROTEASE INHIBITORS; RNA INTERFERENCE;

EID: 84919726720     PISSN: 00405752     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00122-014-2371-2     Document Type: Review

References (187)

1. Adio AM, Casteel CL, De Vos M, Kim JH, Joshi V, Li B, Juery C, Daron J, Kliebenstein DJ, Jander G (2011) Biosynthesis and defensive function of Ndelta-acetylornithine, a jasmonate-induced Arabidopsis metabolite. Plant Cell 23:3303–3318
2. Aharoni A, Giri AP, Deuerlein S, Griepink F, de Kogel W, Verstappen FW, Verhoeven HA, Jongsma MA, Schwab W, Bouwmeester HJ (2003) Terpenoid metabolism in wild-type and transgenic Arabidopsis plants. Plant Cell 15:2866–2884
3. Aharoni A, Jongsma MA, Kim T, Ri M, Giri AP, Verstappen FW, Schwab W, Bouwmeester HJ (2006) Metabolic engineering of terpenoid biosynthesis in plants. Phytochem Rev 5:49–58
4. Ahmad S, Veyrat N, Gordon-Weeks R, Zhang Y, Martin J, Smart L, Glauser G, Erb M, Flors V, Frey M (2011) Benzoxazinoid metabolites regulate innate immunity against aphids and fungi in maize. Plant Physiol 157:317–327
5. Aqueel MA, Leather SR (2011) Effect of nitrogen fertilizer on the growth and survival of Rhopalosiphum padi (L.) and Sitobion avenae (F.) (Homoptera: Aphididae) on different wheat cultivars. Crop Prot 30:216–221
6. Auer C, Frederick R (2009) Crop improvement using small RNAs: Applications and predictive ecological risk assessments. Trends Biotechnol 27:644–651
7. 2 affects the interactions between aphid pests and host plant flowering. Agric For Entomol 2:57–61
8. Azzouz H, Cherqui A, Campan E, Rahbé Y, Duport G, Jouanin L, Kaiser L, Giordanengo P (2005) Effects of plant protease inhibitors, oryzacystatin I and soybean Bowman-Birk inhibitor, on the aphid Macrosiphum euphorbiae (Homoptera, Aphididae) and its parasitoid Aphelinusabdominalis (Hymenoptera, Aphididae). J Insect Physiol 51:75–86
9. Bachman PM, Bolognesi R, Moar WJ, Mueller GM, Paradise MS, Ramaseshadri P, Tan J, Uffman JP, Warren J, Wiggins BE (2013) Characterization of the spectrum of insecticidal activity of a double-stranded RNA with targeted activity against Western Corn Rootworm (Diabrotica virgifera virgifera LeConte). Transgenic Res 22:1207–1222
10. Baum JA, Bogaert T, Clinton W, Heck GR, Feldmann P, Ilagan O, Johnson S, Plaetinck G, Munyikwa T, Pleau M (2007) Control of coleopteran insect pests through RNA interference. Nat Biotechnol 25:1322–1326
11. Beale MH, Birkett MA, Bruce TJ, Chamberlain K, Field LM, Huttly AK, Martin JL, Parker R, Phillips AL, Pickett JA (2006) Aphid alarm pheromone produced by transgenic plants affects aphid and parasitoid behavior. Proc Natl Acad Sci USA 103:10509–10513
12. Beckendorf EA, Catangui MA, Riedell WE (2008) Soybean aphid feeding injury and soybean yield, yield components, and seed composition. Agron J 100:237–246
13. Beneteau J, Renard D, Marché L, Douville E, Lavenant L, Rahbé Y, Dupont D, Vilaine F, Dinant S (2010) Binding properties of the N-acetylglucosamine and high-mannose N-glycan PP2-A1 phloem lectin in Arabidopsis. Plant Physiol 153:1345–1361
14. Bhatia V, Bhattacharya R, Uniyal PL, Singh R, Niranjan RS (2012) Host generated siRNAs attenuate expression of serine protease gene in Myzus persicae. PLoS ONE 7:e46343
15. Birch ANE, Geoghegan IE, Majerus ME, McNicol JW, Hackett CA, Gatehouse AM, Gatehouse JA (1999) Tri-trophic interactions involving pest aphids, predatory 2-spot ladybirds and transgenic potatoes expressing snowdrop lectin for aphid resistance. Mol Breeding 5:75–83
16. Blackman RL, Eastop VF (1984) Aphids on the world’s crops. An identification and information guide. Wiley, New York, p 476
17. Bohlmann J, Meyer-Gauen G, Croteau R (1998) Plant terpenoid synthases: Molecular biology and phylogenetic analysis. Proc Natl Acad Sci USA 95:4126–4133
18. Bonning BC, Pal N, Liu S, Wang Z, Sivakumar S, Dixon PM, King GF, Miller WA (2014) Toxin delivery by the coat protein of an aphid-vectored plant virus provides plant resistance to aphids. Nat Biotechnol 32:102–105
19. Bowers WS, Nault LR, Webb RE, Dutky SR (1972) Aphid alarm pheromone: Isolation, identification, synthesis. Science 177:1121–1122
20. Bown DP, Wilkinson HS, Gatehouse JA (1997) Differentially regulated inhibitor-sensitive and insensitive protease genes from the phytophagous insect pest, Helicoverpa armigera, are members of complex multigene families. Insect Biochem Mol Biol 27:625–638
21. Bregitzer P, Mornhinweg DW, Hammon R, Stack M, Baltensperger DD, Hein GL, O’Neill MK, Whitmore JC, Fiedler DJ (2005) Registration of ‘Burton’ barley. Crop Sci 45:1166–1167
22. Burd JD, Burton RL (1992) Characterization of plant damage caused by Russian wheat aphid (Homoptera: Aphididae). J Econ Entomol 85:2017–2022
23. Burgess EP, Malone LA, Christeller JT (1996) Effects of two proteinase inhibitors on the digestive enzymes and survival of honey bees (Apis mellifera). J Insect Physiol 42:823–828
24. Burgueño-Tapia E, Castillo L, González-Coloma A, Joseph-Nathan P (2008) Antifeedant and phytotoxic activity of the sesquiterpene p-benzoquinone perezone and some of its derivatives. J Chem Ecol 34:766–771
25. Carlini CR, Grossi-de-Sá MF (2002) Plant toxic proteins with insecticidal properties. A review on their potentialities as bioinsecticides. Toxicon 40:1515–1539
26. Carrillo L, Martinez M, Álvarez-Alfageme F, Castañera P, Smagghe G, Diaz I, Ortego F (2011) A barley cysteine-proteinase inhibitor reduces the performance of two aphid species in artificial diets and transgenic Arabidopsis plants. Transgenic Res 20:305–319
27. Catangui MA, Beckendorf EA, Riedell WE (2009) Soybean aphid population dynamics, soybean yield loss, and development of stage-specific economic injury levels. Agron J 101:1080–1092
28. Ceci LR, Volpicella M, Rahbé Y, Gallerani R, Beekwilder J, Jongsma MA (2003) Selection by phage display of a variant mustard trypsin inhibitor toxic against aphids. Plant J 33:557–566
29. Chang TJ, Chen L, Chen SB, Cai HY, Liu X, Xiao GF, Zhu Z (2003) Transformation of tobacco with genes encoding Helianthus tuberosus agglutinin (HTA) confers resistance to peach-potato aphid (Myzus persicae). Transgenic Res 12:607–614
30. Chiverton PA (1986) Predator density manipulation and its effects on populations of Rhopalosiphum padi (Horn.: Aphididae) in spring barley. Ann Appl Biol 109:49–60
31. Chougule NP, Bonning BC (2012) Toxins for transgenic resistance to hemipteran pests. Toxins 4:405–429
32. Chougule NP, Li H, Liu S, Linz LB, Narva KE, Meade T, Bonning BC (2013) Retargeting of the Bacillus thuringiensis toxin Cyt2Aa against hemipteran insect pests. Proc Natl Acad Sci USA 110:8465–8470
33. Collins MB, Haley SD, Peairs FB, Rudolph JB (2005) Biotype 2 Russian wheat aphid resistance among wheat germplasm accessions. Crop Sci 45:1877–1880
34. Crock J, Wildung M, Croteau R (1997) Isolation and bacterial expression of a sesquiterpene synthase cDNA clone from peppermint (Mentha x piperita, L.) that produces the aphid alarm pheromone (E)-β-farnesene. Proc Natl Acad Sci USA 94:12833–12838
35. Coeur d’acier A, Pérez-Hidalgo N, Petrović-Obradović O (2010) Aphids (Hemiptera, Aphididae) Chapter 9.2. In: Roques A et al. (eds) Alien terrestrial arthropods of Europe. BioRisk 4:435–474
36. Cunillera N, Boronat A, Ferrer A (1997) The Arabidopsis thaliana FPS1 gene generates a novel mRNA that encodes a mitochondrial farnesyl-diphosphate synthase isoform. J Biol Chem 272:15381–15388
37. de Vos M, Cheng WY, Summers HE, Raguso RA, Jander G (2010) Alarm pheromone habituation in Myzus persicae has fitness consequences and causes extensive gene expression changes. Proc Natl Acad Sci USA 107:14673–14678
38. Delp G, Gradin T, Åhman I, Jonsson LM (2009) Microarray analysis of the interaction between the aphid Rhopalosiphum padi and host plants reveals both differences and similarities between susceptible and partially resistant barley lines. Mol Genet Genomics 281:233–248
39. Dinant S, Clark AM, Zhu Y, Vilaine F, Palauqui J, Kusiak C, Thompson GA (2003) Diversity of the superfamily of phloem lectins (phloem protein 2) in angiosperms. Plant Physiol 131:114–128
40. Dogimont C, Bendahmane A, Chovelon V, Boissot N (2010) Host plant resistance to aphids in cultivated crops: Genetic and molecular bases, and interactions with aphid populations. C R Biol 333:566–573
41. Dogimont C, Bendahmane A, Pitrat M, Burget-Bigeard E,Hagen L, Le Menn A, Pauquet J, Rouselle P, Caboche M, Chovelon V (2009) Gene resistant to Aphis gossypii. US Patent 7576264
42. Down RE, Gatehouse AM, Hamilton W, Gatehouse JA (1996) Snowdrop lectin inhibits development and decrease fecundity of the glasshouse potato aphid (Aulacorthum solani) when administered in vitro and via transgenic plants both in laboratory and glasshouse trials. J Insect Physiol 42:1035–1045
43. Dutta I, Majumder P, Saha P, Ray K, Das S (2005a) 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 169:996–1007
44. Dutta I, Saha P, Majumder P, Sarkar A, Chakraborti D, Banerjee S, Das S (2005b) The efficacy of a novel insecticidal protein, Allium sativum leaf lectin (ASAL), against homopteran insects monitored in transgenic tobacco. Plant Biotechnol J 3:601–611
45. Edwards CA, Sunderland KD, George KS (1979) Studies on polyphagous predators of cereal aphids. J Appl Ecol 16:811–823
46. Escobar CA, Sicker D, Niemeyer HM (1999) Evaluation of DIMBOA analogs as antifeedants and antibiotics towards the aphid Sitobion avenae in artificial diets. J Chem Ecol 25:1543–1554
47. Ewen SW, Pusztai A (1999) Effect of diets containing genetically modified potatoes expressing Galanthus nivalis lectin on rat small intestine. Lancet 354:1353–1354
48. Francis F, Vandermoten S, Verheggen F, Lognay G, Haubruge E (2005) Is the (E)-β-farnesene only volatile terpenoid in aphids? J Appl Entomol 129:6–11
49. Gatehouse A, Ferry N, Edwards MG, Bell HA (2011) Insect-resistant biotech crops and their impacts on beneficial arthropods. Phil Trans R Soc B 366:1438–1452
50. Gatehouse AM, Davison GM, Stewart JN, Gatehouse LN, Kumar A, Geoghegan IE, Birch ANE, Gatehouse JA (1999) Concanavalin A inhibits development of tomato moth (Lacanobiaoleracea) and peach-potato aphid (Myzus persicae) when expressed in transgenic potato plants. Mol Breed 5:153–165
51. Gatehouse AM, Down RE, Powell KS, Sauvion N, Rahbé Y, Newell CA, Merryweather A, Hamilton W, Gatehouse JA (1996) Transgenic potato plants with enhanced resistance to the peach-potato aphid Myzus persicae. Entomol Exp Appl 79:295–307
52. Godard K, Byun-McKay A, Levasseur C, Plant A, Séguin A, Bohlmann J (2007) Testing of a heterologous, wound-and insect-inducible promoter for functional genomics studies in conifer defense. Plant Cell Rep 26:2083–2090
53. Goggin FL, Jia L, Shah G, Hebert S, Williamson VM, Ullman DE (2006) Heterologous expression of the Mi-1.2 gene from tomato confers resistance against nematodes but not aphids in eggplant. Mol Plant Microbe Interact 19:383–388
54. Goławska S, Łukasik I (2012) Antifeedant activity of luteolin and genistein against the pea aphid, Acyrthosiphon pisum. J Pest Sci 85:443–450
55. Gray SM, Banerjee N (1999) Mechanisms of arthropod transmission of plant and animal viruses. Microbiol Mol Biol Rev 63:128–148
56. Gutiérrez C, Fereres A, Reina M, Cabrera R, González-Coloma A (1997) Behavioral and sublethal effects of structurally related lower terpenes on Myzus persicae. J Chem Ecol 23:1641–1650
57. Hakim RS, Baldwin K, Smagghe G (2010) Regulation of midgut growth, development, and metamorphosis. Annu Rev Entomol 55:593–608
58. Halbert SE, Corsini D, Wiebe M, Vaughn SF (2009) Plant-derived compounds and extracts with potential as aphid repellents. Ann Appl Biol 154:303–307
59. Han Y, Wang Y, Bi JL, Yang XQ, Huang Y, Zhao X, Hu Y, Cai QN (2009) Constitutive and induced activities of defense-related enzymes in aphid-resistant and aphid-susceptible cultivars of wheat. J Chem Ecol 35:176–182
60. Harsulkar AM, Giri AP, Patankar AG, Gupta VS, Sainani MN, Ranjekar PK, Deshpande VV (1999) Successive use of non-host plant proteinase inhibitors required for effective inhibition of Helicoverpa armigera gut proteinases and larval growth. Plant Physiol 121:497–506
61. Hilder VA, Boulter D (1999) Genetic engineering of crop plants for insect resistance—a critical review. Crop Prot 18:177–191
62. Hilder VA, Powell KS, Gatehouse A, Gatehouse JA, Gatehouse LN, Shi Y, Hamilton W, Merryweather A, Newell CA, Timans JC (1995) Expression of snowdrop lectin in transgenic tobacco plants results in added protection against aphids. Transgenic Res 4:18–25
63. Hogervorst PA, Wäckers FL, Woodring J, Romeis J (2009) Snowdrop lectin (Galanthus nivalis agglutinin) in aphid honeydew negatively affects survival of a honeydew-consuming parasitoid. Agric For Entomol 11:161–173
64. Hohn TM, Ohlrogge JB (1991) Expression of a fungal sesquiterpene cyclase gene in transgenic tobacco. Plant Physiol 97:460–462
65. Horsch RB, Fraley RT, Rogers SG, Sanders PR, Lloyd A, Hoffmann N (1984) Inheritance of functional foreign genes in plants. Science 223:496–498
66. Hossain MA, Maiti MK, Basu A, Sen S, Ghosh AK, Sen SK (2006) Transgenic expression of onion leaf lectin gene in Indian mustard offers protection against aphid colonization. Crop Sci 46:2022–2032
67. Huang DF, Pan YH, Zhang SX, Cao JP, Yang XM, Zhang J, Yi W (1997) The discovery of insecticidal protein against aphids from Pinellia pedatisecta and P. ternata. Sci Agric Sin 30:94–96
68. Huang HQ, Lin YJ (2007) Cloning and functional analysis of the rice rbcS gene promoter. J Agric Biotechnol 15:451–458
69. Huber DP, Philippe RN, Godard K, Sturrock RN, Bohlmann J (2005) Characterization of four terpene synthase cDNAs from methyl jasmonate-induced Douglas-fir, Pseudotsuga menziesii. Phytochemistry 66:1427–1439
70. Huvenne H, Smagghe G (2010) Mechanisms of dsRNA uptake in insects and potential of RNAi for pest control: A review. J Insect Physiol 56:227–235
71. International Aphid Genomics Consortium (2010) Genome sequence of the pea aphid Acyrthosiphon pisum. PLoS Biol 8:e1000313
72. Jaubert-Possamai S, Le Trionnaire G, Bonhomme J, Christophides GK, Rispe C, Tagu D (2007) Gene knockdown by RNAi in the pea aphid Acyrthosiphon pisum. BMC Biotechnol 7:63
73. Jin S, Zhang X, Daniell H (2012) Pinellia ternata agglutinin expression in chloroplasts confers broad spectrum resistance against aphid, whitefly, Lepidopteran insects, bacterial and viral pathogens. Plant Biotechnol J 10:313–327
74. Jin SX, Kanagaraj A, Verma D, Lange T, Daniell H (2011) Release of hormones from conjugates: Chloroplast expression of β-glucosidase results in elevated phytohormone levels associated with significant increase in biomass and protection from aphids or whiteflies conferred by sucrose esters. Plant Physiol 155:222–235
75. Jinek M, Doudna JA (2008) A three-dimensional view of the molecular machinery of RNA interference. Nature 457:405–412
76. Jongsma MA, Bolter C (1997) The adaptation of insects to plant protease inhibitors. J Insect Physiol 43:885–895
77. Jose AM, Hunter CP (2007) Transport of sequence-specific RNA interference information between cells. Annu Rev Genet 41:305–330
78. Jun T, Mian MR, Michel AP (2012) Genetic mapping revealed two loci for soybean aphid resistance in PI 567301B. Theor Appl Genet 124:13–22
79. Jyoti JL, Michaud JP (2005) Comparative biology of a novel strain of Russian wheat aphid (Homoptera: Aphididae) on three wheat cultivars. J Econ Entomol 98:1032–1039
80. Kanrar S, Venkateswari J, Kirti P, Chopra V (2002) Transgenic Indian mustard (Brassicajuncea) with resistance to the mustard aphid (Lipaphis erysimi Kalt.). Plant Cell Rep 20:976–981
81. Kappers IF, Aharoni A, van Herpen TW, Luckerhoff LL, Dicke M, Bouwmeester HJ (2005) Genetic engineering of terpenoid metabolism attracts bodyguards to Arabidopsis. Science 309:2070–2072
82. Kato T, Hori M, Ogawa T, Muramoto K, Toriyama K (2010) Expression of gene for Dioscorea batatas tuber lectin 1 in transgenic tobacco confers resistance to green-peach aphid. Plant Biotechnol 27:141–145
83. Kettles GJ, Drurey C, Schoonbeek HJ, Maule AJ, Hogenhout SA (2013) Resistance of Arabidopsis thaliana to the green peach aphid, Myzus persicae, involves camalexin and is regulated by microRNAs. New Phytol 198:1178–1190
84. Kim KS, Hill CB, Hartman GL, Hyten DL, Hudson ME, Diers BW (2010) Fine mapping of the soybean aphid-resistance gene Rag2 in soybean PI 200538. Theor Appl Genet 121:599–610
85. Kim Y, Lim S, Kang K, Jung Y, Lee Y, Choi Y, Sano H (2011) Resistance against beet armyworms and cotton aphids in caffeine-producing transgenic chrysanthemum. Plant Biotechnol 28:393–395
86. Klingler J, Creasy R, Gao L, Nair RM, Calix AS, Jacob HS, Edwards OR, Singh KB (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 137:1445–1455
87. Klingler JP, Edwards OR, Singh KB (2007) Independent action and contrasting phenotypes of resistance genes against spotted alfalfa aphid and bluegreen aphid in Medicago truncatula. New Phytol 173:630–640
88. Klingler JP, Nair RM, Edwards OR, Singh KB (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 60:4115–4127
89. Kolbe W, Linke W (1974) Studies of cereal aphids; their occurrence, effect on yield in relation to density levels and their control. Ann Appl Biol 77:85–87
90. Köpke D, Schröder R, Fischer HM, Gershenzon J, Hilker M, Schmidt A (2008) Does egg deposition by herbivorous pine sawflies affect transcription of sesquiterpene synthases in pine? Planta 228:427–438
91. Kovalev OV, Poprawski TJ, Stekolshchikov AV, Vereshchagina AB, Gandrabur SA (1991) Diuraphis Aizenberg (Hom., Aphididae): key to apterous viviparous females, and review of Russian language literature on the natural history of Diuraphis noxia (Kurdjumov, 1913). J Appl Entomol 112:425–436
92. Langridge W, Fitzgerald KJ, Koncz C, Schell J, Szalay AA (1989) Dual promoter of Agrobacterium tumefaciens mannopine synthase genes is regulated by plant growth hormones. Proc Natl Acad Sci USA 86:3219–3223
93. Lecoq H, Wilser G, Pitrat M (1998) Cucurbit viruses: The classics and the emerging. In: McCreight JD (ed) Cucurbitaceae’98. Evaluation and enhancement of cucurbit germplasm. American Society of Horticultural Science, Alexandria, pp 126–142
94. Legeai F, Shigenobu S, Gauthier JP, Colbourne J, Rispe C, Collin O, Richards S, Wilson AC, Murphy T, Tagu D (2010) AphidBase: A centralized bioinformatic resource for annotation of the pea aphid genome. Insect Mol Biol 19:5–12
95. Li H, Chougule NP, Bonning BC (2011) Interaction of the Bacillus thuringiensis delta endotoxins Cry1Ac and Cry3Aa with the gut of the pea aphid, Acyrthosiphon pisum (Harris). J Invertebr Pathol 107:69–78
96. Li Y, Hill CB, Hartman GL (2004) Effect of three resistant soybean genotypes on the fecundity, mortality, and maturation of soybean aphid (Homoptera: Aphididae). J Econ Entomol 97:1106–1111
97. Lord JM, Roberts LM, Robertus JD (1994) Ricin: Structure, mode of action, and some current applications. FASEB J 8:201–208
98. Mahmoud SS, Croteau RB (2002) Strategies for transgenic manipulation of monoterpene biosynthesis in plants. Trends Plant Sci 7:366–373
99. Malone LA, Giacon HA, Burgess EP, Maxwell JZ, Christeller JT, Laing WA (1995) Toxicity of trypsin endopeptidase inhibitors to honey bees (Hymenoptera: Apidae). J Econ Entomol 88:46–50
100. Mao JJ, Zeng FR (2014) Plant-mediated RNAi of a gap gene-enhanced tobacco tolerance against the Myzus persicae. Transgenic Res 23:145–152
101. Mao YB, Cai WJ, Wang JW, Hong GJ, Tao XY, Wang LJ, Huang YP, Chen XY (2007) Silencing a cotton bollworm P450 monooxygenase gene by plant-mediated RNAi impairs larval tolerance of gossypol. Nature Biotechnol 25:1307–1313
102. Maruyama T, Ito M, Honda G (2001) Molecular cloning, functional expression and characterization of (E)-β-farnesene synthase from Citrus junos. Biol Pharm Bull 24:1171–1175
103. McCarville M, Hodgson E, O’Neal M (2012) Soybean aphid-resistant soybean varieties for Iowa. Iowa State University Extension and Outreach, Ames 3023
104. McCreight JD (2008) Potential sources of genetic resistance in Lactuca spp. to the lettuce aphid, Nasanovia ribisnigri (Mosely) (Homoptera:Aphididae). HortScience 43:1355–1358
105. McCreight JD, Kishaba AN, Bohn GW (1984) AR Hale’s Best Jumbo, AR 5, and AR Topmark: Melon aphid-resistant muskmelon breeding lines. HortScience 19:309–310
106. Mehlo L, Gahakwa D, Nghia PT, Loc NT, Capell T, Gatehouse JA, Gatehouse AM, Christou P (2005) An alternative strategy for sustainable pest resistance in genetically enhanced crops. Proc Natl Acad Sci USA 102:7812–7816
107. Meister G, Tuschl T (2004) Mechanisms of gene silencing by double-stranded RNA. Nature 431:343–349
108. Miles PW (1989) Specific responses and damage caused by Aphidoidea. In: Minks AK, Harrewijn P (eds) Aphids: Their biology, natural enemies and control. Elsevier, New York, pp 23–47
109. Mornhinweg DH, Porter DR, Webster JA (1995) Inheritance of Russian wheat aphid resistance in spring barley. Crop Sci 35:1368–1371
110. Morrison WP, Peairs FB (1998) Response model concept and economic impact. Response model for an introduced pest-the Russian wheat aphid. Thomas Say Publications in Entomology, Lanham, pp 1–11
111. Mowry TM (2005) Insecticidal reduction of Potato leafroll virus transmission by Myzus persicae. Ann Appl Biol 146:81–88
112. Murugan M, Khan SA, Cardona PS, Orozco GV, Viswanathan P, Reese J, Starkey S, Smith CM (2010) Variation of resistance in barley against biotypes 1 and 2 of the Russian wheat aphid (Hemiptera: Aphididae). J Econ Entomol 103:938–948
113. Musshoff F, Madea B (2009) Ricin poisoning and forensic toxicology. Drug Test Anal 1:184–191
114. Mutti NS, Park Y, Reese JC, Reeck GR (2006) RNAi knockdown of a salivary transcript leading to lethality in the pea aphid Acyrthosiphon pisum. J Insect Sci 6:38
115. Nault LR (1997) Arthropod transmission of plant viruses: A new synthesis. Ann Entomol Soc Am 90:521–541
116. Neal JJ, Tingey WM, Steffens JC (1990) Sucrose esters of carboxylic acids in glandular trichomes of Solanum berthaultii deter settling and probing by green peach aphid. J Chem Ecol 16:487–497
117. Olsnes S (2004) The history of ricin, abrin and related toxins. Toxicon 44:361–370
118. Pan YH, Zhang SX, Cao JP, Yang XM, Zhang J, Ying WZ, Huang DF (1998) The isolation, purification of Pinellia pedatisecta lectin and its activity on aphid-resistance. Prog Nat Sci 8:502–505
119. Peccoud J, Simon J, McLaughlin HJ, Moran NA (2009) Post-Pleistocene radiation of the pea aphid complex revealed by rapidly evolving endosymbionts. Proc Natl Acad Sci USA 106:16315–16320
120. Picaud S, Brodelius M, Brodelius PE (2005) Expression, purification and characterization of recombinant (E)-β-farnesene synthase from Artemisia annua. Phytochemistry 66:961–967
121. Pickett JA, Griffiths DC (1980) Composition of aphid alarm pheromones. J Chem Ecol 6:349–360
122. Pitino M, Coleman AD, Maffei ME, Ridout CJ, Hogenhout SA (2011) Silencing of aphid genes by dsRNA feeding from plants. PLoS ONE 6:e25709
123. Price DR, Gatehouse JA (2008) RNAi-mediated crop protection against insects. Trends Biotechnol 26:393–400
124. Prosser IM, Adams RJ, Beale MH, Hawkins ND, Phillips AL, Pickett JA, Field LM (2006) Cloning and functional characterisation of a cis-muuroladiene synthase from black peppermint (Mentha × piperita) and direct evidence for a chemotype unable to synthesise farnesene. Phytochemistry 67:1564–1571
125. Qureshi JA, Michaud JP, Martin TJ (2006) Resistance to biotype 2 Russian wheat aphid (Homoptera: Aphididae) in two wheat lines. J Econ Entomol 99:544–550
126. Rabbinge R, Vereyken PH (1980) The effect of diseases or pests upon the host. Z Pflanzenkrankheiten Pflanzenschutz 87:409–422
127. Ragsdale DW, Landis DA, Brodeur J, Heimpel GE, Desneux N (2011) Ecology and management of the soybean aphid in North America. Annu Rev Entomol 56:375–399
128. Ragsdale DW, McCornack BP, Venette RC, Potter BD, MacRae IV, Hodgson EW, O’Neal ME, Johnson KD, O’Neil RJ, DiFonzo CD (2007) Economic threshold for soybean aphid (Hemiptera: Aphididae). J Econ Entomol 100:1258–1267
129. Rahbé Y, Deraison C, Bonadé-Bottino M, Girard C, Nardon C, Jouanin L (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 164:441–450
130. Ramsey JS, Wilson AC, De Vos M, Sun Q, Tamborindeguy C, Winfield A, Malloch G, Smith DM, Fenton B, Gray SM (2007) Genomic resources for Myzus persicae: EST sequencing, SNP identification, and microarray design. BMC Genom 8:423
131. Ribeiro ADO, Pereira E, Galvan TL, Picanco MC, Picoli EDT, Silva DD, Fari MG, Otoni WC (2006) Effect of eggplant transformed with oryzacystatin gene on Myzus persicae and Macrosiphum euphorbiae. J Appl Entomol 130:84–90
132. Rossi M, Goggin FL, Milligan SB, Kaloshian I, Ullman DE, Williamson VM (1998) The nematode resistance gene Mi of tomato confers resistance against the potato aphid. Proc Natl Acad Sci USA 95:9750–9754
133. Rutledge CE, O’Neil RJ (2006) Soybean plant stage and population growth of soybean aphid. J Econ Entomol 99:60–66
134. Ryan CA (1990) Protease inhibitors in plants: Genes for improving defenses against insects and pathogens. Annu Rev Phytopathol 28:425–449
135. Sabater-Muñoz B, Legeai F, Rispe C, Bonhomme J, Dearden P, Dossat C, Duclert A, Gauthier J, Ducray DG, Hunter W, Dang P, Kambhampati S, Martinez-Torres D, Cortes T, Moya A, Nakabachi A, Philippe C, Prunier-Leterme N, Rahbé Y, Simon JC, Stern D, Wincker P, Tagu D (2006) Large-scale gene discovery in the pea aphid Acyrthosiphon pisum (Hemiptera). Genome Biol 7:R21
136. Sadeghi A, Broeders S, De Greve H, Hernalsteens JP, Peumans WJ, Van Damme EJ, Smagghe G (2007) Expression of garlic leaf lectin under the control of the phloem-specific promoter Asus1 from Arabidopsis thaliana protects tobacco plants against the tobacco aphid (Myzus nicotianae). Pest Manag Sci 63:1215–1223
137. Saguez J, Cherqui A, Lehraiki S, Vincent C, Beaujean A, Jouanin L, Laberche J, Giordanengo P (2010) Effects of mti-2 transgenic potato plants on the aphid Myzus persicae (Sternorrhyncha: Aphididae). Intern J Agron. doi:10.1155/2010/653431
138. Saljoqi A (2009) Population dynamics of Myzus persicae (Sulzer) and its associated natural enemies in spring potato crop, Peshawar, Pakistan. Sarhad J Agric 25:451–456
139. Sanmiya K, Ueno O, Matsuoka M, Yamamoto N (1999) Localization of farnesyl diphosphate synthase in chloroplasts. Plant Cell Physiol 40:348–354
140. Schmid A, Schindelholz B, Zinn K (2002) Combinatorial RNAi: A method for evaluating the functions of gene families in Drosophila. Trends Neurosci 25:71–74
141. Senthil-Kumar M, Mysore KS (2011) Caveat of RNAi in plants: The off-target effect. Methods Mol Biol 744:13–25
142. Shahidi-Noghabi S, Van Damme EJ, Smagghe G (2009) Expression of Sambucus nigra agglutinin (SNA-I′) from elderberry bark in transgenic tobacco plants results in enhanced resistance to different insect species. Transgenic Res 18:249–259
143. Shakesby AJ, Wallace IS, Isaacs HV, Pritchard J, Roberts DM, Douglas AE (2009) A water-specific aquaporin involved in aphid osmoregulation. Insect Biochem Mol Biol 39:1–10
144. Sharma HC, Sharma KK, Seetharama N, Ortiz R (2000) Prospects for using transgenic resistance to insects in crop improvement. Electronic J Biotechnol 3:21–22
145. Siomi H, Siomi MC (2009) On the road to reading the RNA-interference code. Nature 457:396–404
146. Smith CM, Belay T, Stauffer C, Stary P, Kubeckova I, Starkey S (2004) Identification of Russian wheat aphid (Homoptera: Aphididae) populations virulent to the Dn4 resistance gene. J Econ Entomol 97:1112–1117
147. Smith CM, Chuang WP (2014) Plant resistance to aphid feeding: Behavioral, physiological, genetic and molecular cues regulate aphid host selection and feeding. Pest Manag Sci 70:528–540
148. Soberón M, Pardo-López L, López I, Gómez I, Tabashnik BE, Bravo A (2007) Engineering modified Bt toxins to counter insect resistance. Science 318:1640–1642
149. Sogorb MA, Vilanova E (2002) Enzymes involved in the detoxification of organophosphorus, carbamate and pyrethroid insecticides through hydrolysis. Toxicol Lett 128:215–228
150. Stary P (1999) Distribution and ecology of the Russian wheat aphid, Diuraphis noxia (Kurdj.), expanded to Central Europe (Hom.: Aphididae). J Pest Sci 72:25–30
151. Stöger E, Williams S, Christou P, Down RE, Gatehouse JA (1999) Expression of the insecticidal lectin from snowdrop (Galanthus nivalis agglutinin; GNA) in transgenic wheat plants: Effects on predation by the grain aphid Sitobion avenae. Mol Breeding 5:65–73
152. Tagu D, Klingler JP, Moya A, Simon J (2008) Early progress in aphid genomics and consequences for plant-aphid interactions studies. Mol Plant Microbe Interact 21:701–708
153. Tiwari S, Mishra DK, Chandrasekhar K, Singh PK, Tuli R (2011) Expression of δ-endotoxin Cry1EC from an inducible promoter confers insect protection in peanut (Arachis hypogaea L.) plants. Pest Manag Sci 67:137–145
154. Van Damme EJ, Lannoo N, Peumans WJ (2008) Plant lectins. Adv Bot Res 48:107–209
155. van Roessel P, Brand AH (2004) Spreading silence with Sid. Genome Biol 5:208
156. Vandenborre G, Smagghe G, Van Damme EJ (2011) Plant lectins as defense proteins against phytophagous insects. Phytochemistry 72:1538–1550
157. Wallaart TE, Bouwmeester HJ, Hille J, Poppinga L, Maijers NC (2001) Amorpha-4, 11-diene synthase: Cloning and functional expression of a key enzyme in the biosynthetic pathway of the novel antimalarial drug artemisinin. Planta 212:460–465
158. Wang EM, Wang R, DeParasis J, Loughrin JH, Gan SS, Wagner GJ (2001) Suppression of a P450 hydroxylase gene in plant trichome glands enhances natural-product-based aphid resistance. Nature Biotechnol 19:371–374
159. Wang YB, Zhang H, Li HC, Miao XX (2011) Second-generation sequencing supply an effective way to screen RNAi targets in large scale for potential application in pest insect control. PLoS ONE 6:e18644
160. Wang ZY, Zhang KW, Sun XF, Tang KX, Zhang JR (2005) Enhancement of resistance to aphids by introducing the snowdrop lectin genegna into maize plants. J Biosci 30:627–638
161. Whangbo JS, Hunter CP (2008) Environmental RNA interference. Trends Genet 24:297–305
162. Whyard S, Singh AD, Wong S (2009) Ingested double-stranded RNAs can act as species-specific insecticides. Insect Biochem Mol Biol 39:824–832
163. Will T, Vilcinskas A (2013) Aphid-proof plants: Biotechnology-based approaches for Aphid control. Adv Biochem Eng Biotechnol 136:179–203
164. Wohlers P (1981) Aphid avoidance of plants contaminated with alarm pheromone (E)-β-farnesene. Z Angew Ent 92:329–336
165. Wroblewski T, Piskurewicz U, Tomczak A, Ochoa O, Michelmore RW (2007) Silencing of the major family of NBS-LRR-encoding genes in lettuce results in the loss of multiple resistance specificities. Plant J 51:803–818
166. Wu J, Luo XL, Guo HN, Xiao J, Tian Y (2006a) Transgenic cotton, expressing Amaranthuscaudatus agglutinin, confers enhanced resistance to aphids. Plant Breeding 125:390–394
167. Wu SQ, Schalk M, Clark A, Miles RB, Coates R, Chappell J (2006b) Redirection of cytosolic or plastidic isoprenoid precursors elevates terpene production in plants. Nature Biotechnol 24:1441–1447
168. Wu ZM, Yan HB, Pan WL, Jiang B, Liu JG, Geng BJ, Sun YT, Wang YH, Dong WQ (2012) Transform of an ectopically expressed bulb lectin gene from ‘Pinellia pedatisecta’ into tobacco plants conferring resistance to aphids (‘Myzusnicotianae’). Aust J Crop Sci 6:904
169. Xia LQ, Ma YZ, He Y, Jones HD (2012) GM wheat development in China: Current status and challenges to commercialization. J Exp Bot 63:1785–1790
170. Xiao Y, Wang K, Ding RX, Zhang HM, Di P, Chen JF, Zhang L, Chen WS (2012) Transgenic tetraploid Isatis indigotica expressing Bt Cry1Ac and Pinellia ternata agglutinin showed enhanced resistance to moths and aphids. Mol Biol Rep 39:485–491
171. Xu LJ, Duan XL, Lv YH, Zhang XH, Nie ZS, Xie CJ, Ni ZF, Liang RQ (2014) Silencing of an aphid carboxylesterase gene by use of plant-mediated RNAi impairs Sitobion avenae tolerance of Phoxim insecticides. Transgenic Res 23:389–396
172. Xu P, Zhang Y, Kang L, Roossinck MJ, Mysore KS (2006) Computational estimation and experimental verification of off-target silencing during posttranscriptional gene silencing in plants. Plant Physiol 142:429–440
173. Xu W, Han Z (2008) Cloning and phylogenetic analysis of sid-1-like genes from aphids. J Insect Sci 8:1–6
174. Yao JH, Pang YZ, Qi HX, Wan BL, Zhao XY, Kong WW, Sun XF, Tang KX (2003) Transgenic tobacco expressing Pinellia ternata agglutinin confers enhanced resistance to aphids. Transgenic Res 12:715–722
175. Ye SH, Chen S, Zhang F, Wang W, Tian Q, Liu JZ, Chen F, Bao JK (2009) Transgenic tobacco expressing Zephyranthes grandiflora agglutinin confers enhanced resistance to aphids. Appl Biochem Biotechnol 158:615–630
176. Yu XD, Jones HD, Ma YZ, Wang GP, Xu ZS, Zhang BM, Zhang YJ, Ren GW, Pickett JA, Xia LQ (2012a) E)-β-Farnesene synthase genes affect aphid (Myzus persicae) infestation in tobacco (Nicotiana tabacum. Funct Integr Genomics 12:207–213
177. Yu XD, Pickett J, Ma YZ, Bruce T, Napier J, Jones HD, Xia LQ (2012b) Metabolic engineering of plant-derived (E)-β-farnesene synthase genes for a novel type of aphid-resistant genetically modified crop plants. J Integr Plant Biol 54:282–299
178. Yu XD, Zhang YJ, Ma YZ, Xu ZS, Wang GP, Xia LQ (2013) Expression of an (E)-β-farnesene synthase gene from Asian peppermint in tobacco affected aphid infestation. Crop J 1:50–60
179. Yu Y, Wei ZM (2008) Increased oriental armyworm and aphid resistance in transgenic wheat stably expressing Bacillus thuringiensis (Bt) endotoxin and Pinellia ternate agglutinin (PTA). Plant Cell Tiss Org Cult 94:33–44
180. Zha W, Peng X, Chen R, Du B, Zhu L, He G (2011) Knockdown of midgut genes by dsRNA-transgenic plant-mediated RNA interference in the hemipteran insect Nilaparvata lugens. PLoS ONE 6:e20504
181. Zhang B, Edwards OR, Kang L, Fuller SJ (2012) Russian wheat aphids (Diuraphis noxia) in China: Native range expansion or recent introduction? Mol Ecol 21:2130–2144
182. Zhang CL, Shi HJ, Chen L, Wang XM, Lü BB, Zhang SP, Liang Y, Liu RX, Qian J, Sun WW (2011) Harpin-induced expression and transgenic overexpression of the phloem protein gene AtPP2-A1 in Arabidopsis repress phloem feeding of the green peach aphid Myzus persicae. BMC Plant Biol 11:11
183. Zhang G, Gu C, Wang D (2010) A novel locus for soybean aphid resistance. Theor Appl Genet 120:1183–1191
184. Zhang M, Zhou YW, Wang H, Jones HD, Gao Q, Wang DH, Ma YZ, Xia LQ (2013) 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 14:560
185. Zhang YJ, Jiang YY, Feng XD, Xia B, Zeng J, Liu Y (2009) Occurring trends of major crop pests in national significances in 2009. China Plant Prot 29:33–36
186. Zhou CC, Qian ZY, Ji Q, Xu H, Chen LL, Luo XQ, Min L, Tang KX, Xiao JB, Kai GY (2011) Expression of the zga agglutinin gene in tobacco can enhance its anti-pest ability for peach-potato aphid (Myzus persica). Acta Physiol Plant 33:2003–2010
187. Zhu-Salzman K, Salzman RA, Ahn J, Koiwa H (2004) Transcriptional regulation of sorghum defense determinants against a phloem-feeding aphid. Plant Physiol 134:420–431