Aphid-Proof Plants: Biotechnology-Based Approaches for Aphid Control

  • Torsten Will
  • Andreas Vilcinskas
Part of the Advances in Biochemical Engineering/Biotechnology book series (ABE, volume 136)


Aphid s are economically significant agricultural pests that are responsible for large yield losses in many different crops. Because the use of insecticides is restricted in the context of integrated pest management and aphids develop resistance against them rapidly, new biotechnology-based approaches are required for aphid control. These approaches focus on the development of genetically modified aphid-resistant plants that express protease inhibitor s, dsRNA, antimicrobial peptide s, or repellent s, thus addressing different levels of aphid-plant interactions. However, a common goal is to disturb host plant acceptance by aphid s and to disrupt their ability to take nutrition from plants. The defense agents negatively affect different fitness-associated parameters such as growth, reproduction, and survival, which therefore reduce the impact of infestations. The results from several different studies suggest that biotechnology-based approaches offer a promising strategy for aphid control.


Agro-biotechnology Antimicrobial peptide Aphid Pest control Protease inhibitor Repellent RNAi 



Antimicrobial peptide


Body plan area


Bacillus thuringiensis


Cauliflower mosaic virus


Companion cell


double stranded RNA




Genetically modified




Protease inhibitor


RNA interference


Sieve element


small interfering RNA


Sheath protein



We would like to thank Henrike Schmidtberg (Department of Phytopathology and Applied Zoology, Justus-Liebig-University Giessen), Gregory Walker (Department of Entomology, University of California, Riverside), and Richard M Twyman for reading and editing the manuscript. We also acknowledge generous funding from the Hessian Ministry of Science and Art via the LOEWE research focus “Insect Biotechnology”.


  1. 1.
    Gould N, Thorpe MR, Koroleva O, Minchin PEH (2005) Phloem hydrostatic pressure relates to solute loading rate: a direct test of the Munch hypothesis. Funct Plant Biol 32:1019–1026Google Scholar
  2. 2.
    Münch E (1930) Die Stoffbewegung in der Pflanze. Fischer, JenaGoogle Scholar
  3. 3.
    van Bel AJE (1996) Interaction between sieve element and companion cell and the consequence for photoassimilate distribution. Two structural hardware frames with associated software packages in dicotyledons? J Exp Bot 47:1129–1140Google Scholar
  4. 4.
    Hafke JB, van Amerongen J-K, Kelling F, Furch ACU, Gaupels F, van Bel AJE (2005) Thermodynamic battle for photosynthate acquisition between sieve tubes and adjoining parenchyma in transport phloem. Plant Physiol 138:1527–1537Google Scholar
  5. 5.
    Minchin PEH, Thorpe MR (1987) Measurement of unloading and reloading of photoassimilate within the stem of bean. J Exp Bot 38:211–220Google Scholar
  6. 6.
    Kusnierczyk A, Winge P, Jørstad TS, Troczynska J, Rossiter JT, Bones AM (2008) Towards global understanding of plant defence against aphids—timing and dynamics of early Arabidopsis defence responses to cabbage aphid (Brevicoryne brassicae) attack. Plant, Cell Environ 31:1097–1115Google Scholar
  7. 7.
    Will T, Hewer A, van Bel AJE (2008) A novel perfusion system shows that aphid feeding behavior is altered by decrease of sieve-tube pressure. Ent Exp Appl 127:237–245Google Scholar
  8. 8.
    Tjallingii WF (1995) Regulation of phloem sap feeding by aphids. In: Chapman RF, de Boer G (eds) Regulatory mechanisms in insect feeding. Chapman and Hall, New YorkGoogle Scholar
  9. 9.
    Furch ACU, Zimmermann MR, Will T, Hafke JB, van Bel ACU (2010) Remote-controlled stop of phloem mass flow by biphasic occlusion in Cucurbita maxima. J Exp Bot 61:3697–3708Google Scholar
  10. 10.
    Hao P, Liu C, Wang Y, Chen R, Tang M, Du B, Zhu L, He G (2008) Herbivore-induced callose deposition on the sieve plates of rice: an important mechanism for host resistance. Plant Physiol 146:1810–1820Google Scholar
  11. 11.
    Will T, van Bel AJE (2006) Physical and chemical interactions between aphids and plants. J Exp Bot 57:729–737Google Scholar
  12. 12.
    Ng JCK, Perry KL (2004) Transmission of plant viruses by aphid vectors. Mol Plant Pathol 5:505–511Google Scholar
  13. 13.
    Tjallingii WF (1978) Electrical recording of penetration behavior by aphids. Ent Exp Appl 24:521–530Google Scholar
  14. 14.
    Tjallingii WF (1978) Mechanoreceptors of the aphid labium. Ent Exp Appl 24:731–737Google Scholar
  15. 15.
    Tjallingii WF, Hogen Esch TH (1993) Fine structure of aphid stylet routes in plant tissues in correlation with EPG signals. Physiol Entomol 18:317–328Google Scholar
  16. 16.
    Tjallingii WF (2006) Salivary secretions by aphids interacting with proteins of phloem wound responses. J Exp Bot 57:739–745Google Scholar
  17. 17.
    Hewer A, Will T, van Bel AJE (2010) Plant cues for aphid navigation in vascular tissues. J Exp Biol 213:4030–4042Google Scholar
  18. 18.
    Backus EA (1988) Sensory systems and behaviours which mediate hemipteran plant-feeding: a taxonomic overview. J Insect Physiol 34:151–165Google Scholar
  19. 19.
    Backus EA, McLean DL (1985) Behavioral evidence that the precibarial sensilla of leafhoppers are chemosensory and function in host discrimination. Ent Exp Appl 37:219–228Google Scholar
  20. 20.
    Wensler RJ, Filshie BK (1969) Gustatory sense organs in the food channel of aphids. J Morphology 129:473–492Google Scholar
  21. 21.
    Prado E, Tjallingii WF (1994) Aphid activities during sieve element punctures. Ent Exp Appl 72:157–165Google Scholar
  22. 22.
    Powell G, Tosh CR, Hardie J (2006) Host plant selection by aphids: Behavioral, evolutionary, and applied perspectives. Ann Rev Ent 51:309–330Google Scholar
  23. 23.
    Carolan JC, Fitzroy CIJ, Ashton PD, Douglas AE, Wilkinson TL (2009) The secreted salivary proteome of the pea aphid Acyrthosiphon pisum characterised by mass spectrometry. Proteomics 9:2457–2467Google Scholar
  24. 24.
    Miles PW (1965) Studies on the salivary physiology of plant-bugs: the salivary secretions of aphids. J Insect Physiol 11:1261–1268Google Scholar
  25. 25.
    Will T, Steckbauer K, Hardt M, van Bel AJE (2012) Aphid gel saliva: Sheath structure, protein composition and secretors dependence on stylet-tip milieu. PLoS ONE 7(10):e46903. doi: 10.1371/journal.pone.0046903 Google Scholar
  26. 26.
    Miles PW (1999) Aphid saliva. Biol Rev 74:41–85Google Scholar
  27. 27.
    Moreno A, Garzo E, Fernandez-Mata G, Kassem M, Aranda MA, Fereres A (2011) Aphids secrete watery saliva into plant tissues from the onset of stylet penetration. Ent Exp Appl 139:145–153Google Scholar
  28. 28.
    Martin B, Collar JL, Tjallingii WF, Fereres A (1997) Intracellular ingestion and salivation by aphids may cause the acquisition and inoculation of non-persistently transmitted plant viruses. J Gen Virol 78:2701–2705Google Scholar
  29. 29.
    Carolan JC, Caragea D, Reardon KT, Mutti NS, Dittmer N, Pappan K, Cui F, Castaneto M, Poulain J, Dossat C, Tagu D, Reese JC, Reeck GR, Wilkinson TL, Edwards OR (2011) J Proteom Res 10:1505–1518Google Scholar
  30. 30.
    Will T, Tjallingii WF, Thönnessen A, van Bel AJE (2007) Molecular sabotage of plant defense by aphid saliva. Proc Nat Acad Sci USA 104:10536–10541Google Scholar
  31. 31.
    Wu J, Baldwin IT (2010) New insights into plant responses to the attack from insect herbivores. Ann Rev Gen 44:1–24Google Scholar
  32. 32.
    Bos JIB, Prince D, Pitino M, Maffei ME, Win J, Hogenhout SA (2010) A functional genomics approach identifies candidate effectors from the aphid species Myzus persicae (Green peach aphid). PLoS Gen6 (11):e1001216. doi: 10.1371/journal.pgen.1001216
  33. 33.
    Mutti NS, Louis J, Pappan LK, Pappan K, Begum K, Chen MS, Park Y, Dittmer N, Marshall J, Reese JC, Reeck GR (2008) A protein from the salivary glands of the pea aphid, Acyrtosiphon pisum, is essential in feeding on a host plant. Proc Nat Acad Sci USA 105:9965–9969Google Scholar
  34. 34.
    Webb SE (2010) Insect management of legumes (beans, peas). University of Florida, Gainsville, IFASGoogle Scholar
  35. 35.
    Joshi S, Rabindra RJ, Rajendran TP (2010) Biological control of aphids. J Biol Contr 24:185–202Google Scholar
  36. 36.
    Estruch JJ, Carozzi NB, Desai N, Duck NB, Warren GW, Koziel MG (1997) Transgenic plants: an emerging approach to pest control. Nature Biotech 15:137–141Google Scholar
  37. 37.
    Ferry N, Edwards MG, Gatehouse J, Capell T, Christou P, Gatehouse AMR (2006) Transgenic plants for insect pest control: a forward looking scientific perspective. Transgen Res 15:13–19Google Scholar
  38. 38.
    Kumar S, Chandra A, Pandey KC (2008) Bacillus thuringiensis (Bt) transgenic crop: An environment friendly insect-pest management strategy. J Environ Biol 29:641–653Google Scholar
  39. 39.
    Rahnamaeian M, Langen G, Imani J, Khalifa W, Altincicek B, von Wettstein D, Kogel K-H, Vilcinskas A (2009) Insect peptide metchnikowin confers on barley a selective capacity for resistance to fungal ascomycetes pathogens. J Exp Bot 60:4105–4114Google Scholar
  40. 40.
    Raps A, Kehr J, Gugerli P, Moar WJ, Bigler F, Hilbeck A (2001) Immunological analysis of phloem sap of Bacillus thuringiensis corn and of the non-target herbivore Rhopalosiphum padi (Homoptera: Aphididae) for the presence of Cry1Ab. Mol Ecol 10:525–533Google Scholar
  41. 41.
    Yang N-S, Christou P (1990) Cell type specific expression of a CaMV 35S-Gus gene in transgenic soybean plants. Dev Genet 11:289–293Google Scholar
  42. 42.
    Urwin PE, Troth KM, Zubko EI, Atkinson HJ (2001) Effective transgenic resistance to Globodera pallida in potato field trials. Mol Breed 8:95–101Google Scholar
  43. 43.
    Baum JA, Bogaert T, Clinton W, Heck GR, Feldmann P, Ilagan O, Johnson S, Plaetinck G, Munyikwa T, Pleau M, Vaughn T, Roberts J (2007) Control of coleopteran insect pests through RNA interference. Nat Biotechnol 25:1322–1326Google Scholar
  44. 44.
    Pitino M, Coleman AD, Maffei ME, Ridout CJ, Hogenhout SA (2011) Silencing of aphid genes by dsRNA feeding from plants. PLoS ONE 6(10):e25709. doi: 10.1371/journal.pone.0025709 Google Scholar
  45. 45.
    Truermit E, Sauer N (1995) The promoter of the Arabidopis thaliana SUC2 sucrose-H + symporter gene directs expression of β-glucuroniase to the phloem: Evidence for phloem loading and unloading by SUC2. Planta 196:564–570Google Scholar
  46. 46.
    Imlau A, Truernit E, Sauer N (1999) Cell-to-cell and long-distance trafficking of the green fluorescent protein in the phloem and symplastic unloading of the protein in sink tissues. Plant Cell 11:309–322Google Scholar
  47. 47.
    Kühn C, Hajirezaei MR, Fernie AR, Roessner-Tunali U, Czechowski T, Hierner B (2003) The sucrose transporter StSUT1 localizes to sieve tubes in potato tuber phloem and influences tuber physiology and development. Plant Physiol 131:102–113Google Scholar
  48. 48.
    Langridge WHR, Fitzgerald KJ, Koncz C, Schell J, Szalay AA (1989) Dual promoter of Agrobacterium tumefaciens mannopine synthase genes is regulated by plant growth hormones. Proc Nat Acad Sci USA 86:3219–3223Google Scholar
  49. 49.
    Godard KA, McKay AB, 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. Plan Cell Rep 26:2083–2090Google Scholar
  50. 50.
    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 Management Sci 67:137–145Google Scholar
  51. 51.
    Zhu-Salzmann K, Salzmann RA, Ahn J-E, Koiwa H (2004) Transcriptional regulation of sorghum defense determinants against a phloem-feeding aphid. Plant Physiol 134:420–431Google Scholar
  52. 52.
    Rawlings ND, Tolle DP, Barrett AJ (2004) Evolutionary families of peptidase inhibitors. J Biochem 378:705–716Google Scholar
  53. 53.
    Boulter D (1993) Insect pest control by copying nature using genetically engineered crops. Biochemistry 34:1453–1466Google Scholar
  54. 54.
    Ryan CA (1990) Proteinase inhibitors in plants: genes for improving defenses against insects and pathogens. Ann Rev Phytopathol 28:425–449Google Scholar
  55. 55.
    Dannenhoffer JM, Suhr RC, Thompson GA (2001) Phloem-specific expression of the pumpkin fruit trypsin inhibitor. Planta 212:155–162Google Scholar
  56. 56.
    Kehr J (2006) Phloem sap proteins: their identities and potential roles in the interaction between plants and phloem-feeding insects. J Exp Biol 57:767–774Google Scholar
  57. 57.
    Rhabé Y, Febvay G (1993) Protein toxicity to aphids – an in vitro test on Acyrtosiphon pisum. Ent Exp Appl 67:149–160Google Scholar
  58. 58.
    Rahbé Y, Sauvion N, Febvay G, Peumans WJ, Gatehouse AMR (1995) Toxicity of lectins and processing of ingested proteins in the pea aphid Acyrthosiphon pisum. Ent Exp Appl 76:143–155Google Scholar
  59. 59.
    Corcuera LJ (1993) Biochemical basis for the resistance of barley to aphids. Phytochemistry 33:741–747Google Scholar
  60. 60.
    Casaretto JA, Corcuera LJ (1998) Proteinase inhibitor accumulation in aphid infested barley leaves. Phytochemistry 49:2279–2286Google Scholar
  61. 61.
    Ryan JD, Morgham AT, Richardson PE, Johnson RC, Mort AJ, Eikenbary R (1990) Greenbugs and wheat: a model system for the study of phytotoxic Homoptera. In: Campbell RK, Eikenbary RD (eds) Aphid-Plant Genotype Interactions. Elsevier, AmsterdamGoogle Scholar
  62. 62.
    Broekgaarden C, Poelman EH, Steenhuis G, Voorrips RE, Dicke M, Vosman B (2008) Responses of Brassica oleracea cultivars to infestation by the aphid Brevicoryne brassicae: an ecological and molecular approach. Plant Cell Environ 31:1592–1605Google Scholar
  63. 63.
    Hilder VA, Powell KS, Gatehouse AMR, Gatehouse JA, Gatehouse LN, Shi Y, Hamilton WO, Merryweather A, Newell CA, Timans JC, Peumans WJ, van Damme E, Boulter D (1995) Expression of snowdrop lectin in transgenic tobacco plants results in added protection against aphids. Transgen Res 4:18–25Google Scholar
  64. 64.
    Boulter D, Edwards GA, Gatehouse AMR, Gatehouse JA, Hilder VA (1990) Additive protective effects of different plant-derived insect resistance genes in transgenic tobacco plants. Crop Prot 9:351–354Google Scholar
  65. 65.
    Hilder VA, Brough C, Gatehouse AMR, Gatehouse LN, Powell KS, Shi Y, Hamilton WDO (1992) Genes for protecting transgenic crops from chewing and sap sucking insect pests. In: Proceedings of the Brighton Crop Protection Conference: Pests and Diseases Vol. 2. Lavenham Press, LavenhamGoogle Scholar
  66. 66.
    Powell KS, Gatehouse AMR, Hilder VA, Gatehouse JA (1993) Antimetabolic effects of plant lectins and plant and fungal enzymes on the nymphal stages of two important rice pests, Nilaparva talugens and Nephotettix cinciteps. Ent Exp Appl 66:119–126Google Scholar
  67. 67.
    Rhabé Y, Deraison C, Bonadé-Bottino M, Girard C, Nardon C, Jouanin L (2003) Effects of the cysteine protease inhibitor oryzacystatin (OC-I) of different aphids and reduced performance of Myzus persicae on OC-I expressing transgenic oilseed rape. Plant Sci 164:441–450Google Scholar
  68. 68.
    Ribeiro APO, Pereira EJG, Galvan TL, Picanco MC, Picoli EAT, da Silva DJH, Fári MG, Otoni WC (2006) Effect of eggplant transformed with oryzacystatin gene on Myzus persicae and Macrosiphum euphorbiae. J Appl Entomol 130:84–90Google Scholar
  69. 69.
    Carrillo L, Martinez M, Álvarez-Alfageme F, Castanera 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. Transgen Res 20:305–319Google Scholar
  70. 70.
    Rispe C, Kutsukake M, Doublet V, Hudaverdian S, Legeai F, Simon J-C, Tagu D, Fukatsu T (2008) Large gene family expansion and variable selective pressure for cathepsin B in aphids. Mol Biol Evol 25:5–17Google Scholar
  71. 71.
    Cristofoletti PT, Ribeiro AF, Deraison C, Rahbé Y, Terra WR (2003) Midgut adaptation and digestive enzyme distribution in a phloem feeding insect, the pea aphid Acyrthosiphon pisum. J Insect Physiol 49:11–24Google Scholar
  72. 72.
    Cristofoletti PT, Mendonca de Sousa FA, Rahbé Y, Terra WR (2006) Characterisation of a membrane-bound aminopeptidase purified from Acyrthosiphon pisum midgut cells. FEBS J 273:5574–5598Google Scholar
  73. 73.
    Silva AC, Bacigalupe LD, Luna-Rudloff M, Figueroa CC (2012) Insecticide resistance mechanisms in the green peach aphid Myzus persicae (Hemiptera: Aphididae) II: Costs and benefits. PLoS ONE 7(6):e36810. doi: 10.1371/journal.pone.0036810 Google Scholar
  74. 74.
    Azzouz H, Campan EDM, Cherqui A, Saguez J, Couty A, Jouanin L, Giordanengo P, Kaiser L (2005) Potential effects of plant protease inhibitors, oryzacystatin I and soybean Bowman-Birk inhibitor, on the aphid parasitoid Aphidius ervi Haliday (Hymenoptera, Braconidae). J Insect Physiol 51:941–951Google Scholar
  75. 75.
    Matranga C, Zamore P (2007) Small silencing RNAs. Curr Biol 17:789–793Google Scholar
  76. 76.
    van Rij RP, Berezikov E (2009) Small RNAs and the control of transposons and viruses in Drosophila. Trends Microbiol 17:163–171Google Scholar
  77. 77.
    Ketting R (2011) The many faces of RNAi. Develop Cell 20:148–161Google Scholar
  78. 78.
    Meister G, Tuschl T (2004) Mechanism of gene silencing by double-stranded RNA. Nature 431:343–349Google Scholar
  79. 79.
    Winter J, Jung S, Keller S, Gregory RI, Diederichs S (2009) Many roads to maturity: microRNA biogenesis pathways and their regulation. Nature Cell Biol 11:228–234Google Scholar
  80. 80.
    Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391:806–811Google Scholar
  81. 81.
    Eckhardt NA (2004) Small RNA on the move. Plant Cell 16:1951–1954Google Scholar
  82. 82.
    Nowara D, Gay A, Lacomme C, Shaw J, Ridout C, Douchkov D, Hensel G, Kumlehn J, Schweizer P (2010) HIGS: Host-induced gene silencing in the obligate biotrophic fungal pathogen Blumeria graminis. Plant Cell 22:3130–3141Google Scholar
  83. 83.
    Bellés X (2010) Beyond Drosophila: RNAi in vivo and functional genomics in insects. Annu Rev Ent 55:111–128Google Scholar
  84. 84.
    Mao Y, Cai W, Wang J, Hong G, Tao X, Wang L, Huang Y, Chen X (2007) Silencing a cotton bollworm P450 monooxygenase gene by plant-mediated RNAi impairs larval tolerance of gossypol. Nat Biotechnol 25:1307–1313Google Scholar
  85. 85.
    Whyard S, Singh AD, Wong S (2009) Ingested double-stranded RNAs can act as species-specific insecticides. Insect Biochem Mol Biol 39:824–832Google Scholar
  86. 86.
    Jaubert-Possamai S, Trionnair GL, Bonhomme J, Christophides GK, Rispe C, Tagu D (2007) Gene knockdown by RNAi in the pea aphid Acyrthosiphon pisum. BMC Biotechnol 7:63Google Scholar
  87. 87.
    Mutti NS, Park Y, Reese JC, Reek GR (2006) RNAi knockdown of a salivary transcript leading to lethality in the pea aphid Acyrtosiphon pisum. J Insect Sci 6:38Google Scholar
  88. 88.
    Shakesby AJ, Wallace LS, Isaacs HV, Pritchard J, Roberts DM, Douglas AE (2009) A water-specific aquaporin involved in aphid osmoregulation. Insect Biochem Mol Biol 39:1–10Google Scholar
  89. 89.
    Bucher G, Scholten J, Klingler M (2002) Parental RNAi in Tribolium (Coleoptera). Curr Biol 12:R85–R86Google Scholar
  90. 90.
    The International Aphid Genomics Consortium (2010) Genome sequence of the pea aphid Acyrthosiphon pisum. PLoS Biology 8(2):e1000313. doi: 10.1371/journal.pbio.1000313 Google Scholar
  91. 91.
    Robinson GE, Hackett KJ, Purcell-Miramontes M, Brown SJ, Evans JD, Goldsmith MR, Lawson D, Okamuro J, Robertson HM, Schneider DJ (2011) Creating a buzz about insect genomes. Science 331:1386Google Scholar
  92. 92.
    The International Aphid Genomics Consortium (2010b) Aphid Genomics White Paper II: Proposal to complete development of the aphid modelGoogle Scholar
  93. 93.
    Wiesner J, Vilcinskas A (2010) Antimicrobial peptides – The ancient arm of the human immune system. Virulence 1:440–464Google Scholar
  94. 94.
    Kragol G, Lovas S, Varadi G, Condie BA, Hoffmann R, Otvos L Jr (2001) The antibacterial peptide pyrrhocoricin inhibits the ATPase actions of DnaK and prevents chaperone-assisted protein folding. Biochemistry 40:3016–3026Google Scholar
  95. 95.
    Hancock REW, Scott MG (2000) The role of antimicrobial peptides in animal defenses. Proc Nat Acad Sci USA 97:8856–8861Google Scholar
  96. 96.
    Jiravanichpaisal P, Lee BL, Soderhall K (2006) Cell-mediated immunity in arthropos: Hematopoiesis, coagulation, melanization and opsonization. Immunobiology 211:213–236Google Scholar
  97. 97.
    Bulet P, Stöcklin R (2005) Insect antimicrobial peptides: structures, properties and gene regulation. Protein Peptide Lett 12:3–11Google Scholar
  98. 98.
    Vilcinskas A (2013) Evolutionary plasticity of insect immunity. J Insect Physiol 59:123–129Google Scholar
  99. 99.
    Altincicek B, Gross J, Vilcinskas A (2008) Wounding-mediated gene expression and accelerated viviparous reproduction of the pea aphid Acyrthosiphon pisum. Insect Mol Biol 17:711–716Google Scholar
  100. 100.
    Gerardo NM, Altincicek B, Anselme C, Atamian H, Barribeau SM, de Vos M, Duncan EJ, Evans JD, Gabaldón T, Ghanim M, Heddi A, Kaloshian I, Latorre A, Moya A, Nakabachi A, Parker BJ, Pérez-Brocal V, Pignatelli M, Rahbé Y, Ramsey JS, Spragg CJ, Tamames J, Tamarit D, Tamorindeguy C, Vinsent-Monegat C, Vilcinskas A (2010) Immunity and other defenses in pea aphids, Acyrtosiphon pisum. Gen Biol 11:R21. doi: 10.1186/gb-2010-11-2-r21 Google Scholar
  101. 101.
    Baumann P, Baumann L, Lai C-Y, Rouhbakhsh D (1995) Genetics, physiology, and evolutionary relationships of the genus Buchnera: intracellular symbionts of aphids. Annu Rev Microbiol 49:55–94Google Scholar
  102. 102.
    Moran NA, Russell JA, Koga R, Fukatsu T (2005) Evolutionary relationship of three new species of enterobacteriaceae living as symbionts of aphids and other insects. Appl Environ Microbiol 71:3302–3310Google Scholar
  103. 103.
    Chen D-Q, Campbell BC, Purcell AH (1996) A new rickettsia from a herbivorous insect, the pea aphid Acyrthosiphon pisum (Harris). Curr Microbiol 33:123–128Google Scholar
  104. 104.
    Koga R, Tsuchida T, Fukatsu T (2003) Changing partners in an obligate symbiosis: a facultative endosymbiont can compensate for loss of the essential endosymbiont Buchnera in an aphid. Proc R Soc Lond B 270:2543–2550Google Scholar
  105. 105.
    Tsuchida T, Koga R, Meng X-Y, Matsumoto T, Fukatsu T (2005) Characterization of a facultative endosymbiotic bacterium of the pea aphid Acyrthosiphon pisum. Microbiol Ecol 49:126–133Google Scholar
  106. 106.
    Gündüz EA, Douglas AE (2009) Symbiotic bacteria enable insect to utilize a nutritionally-inadequate diet. Proc R Soc Lond B 276:987–991Google Scholar
  107. 107.
    Oliver KM, Russell JA, Moran NA, Hunter MS (2003) Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc Nat Acad Sci USA 100:1803–1807Google Scholar
  108. 108.
    Lukasik P, van Asch M, Guo H, Ferrari J, Charles H, Godfray J (2012) Unrelated facultative endosymbionts protect aphids against a fungal pathogen. Ecol Lett. doi:  10.1111/ele.12031
  109. 109.
    Scarborough CL, Ferrari J, Godfray HCJ (2005) Aphid protected from pathogen by endosymbiont. Science 310:1781Google Scholar
  110. 110.
    Montllor CB, Maxmen A, Purcell AH (2002) Facultative bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum under heat stress. Ecol Ent 27:189–195Google Scholar
  111. 111.
    Russell JA, Moran NA (2006) Costs and benefits of symbiont infection in aphids: variation among symbionts and across temperatures. Proc R Soc Lond B 273:603–610Google Scholar
  112. 112.
    McLean AHC, van Asch M, Ferrari J, Godfray HCJ (2011) Effects of bacterial secondary symbionts on host plant use in pea aphids. Proc R Soc Lond B 278:760–766Google Scholar
  113. 113.
    Tsuchida T, Koga R, Fukatsu T (2004) Host plant specialization governed by facultative symbiont. Science 303:1989Google Scholar
  114. 114.
    Keymanesh K, Soltani S, Sardari S (2009) Application of antimicrobial peptides in agriculture and food industry. World J Microbiol Biotechnol 25:933–944Google Scholar
  115. 115.
    Koga R, Tsuchida T, Sakurai M, Fikatsu T (2007) Selective elimination of aphid endosymbionts: effects of antibiotic dose and host genotype, and fitness consequences. FEMS Microbiol Ecol 60:229–239Google Scholar
  116. 116.
    Le-Feuvre RR, Ramirez CC, Olea N, Meza-Basso L (2007) Effect of the antimicrobial peptide indolicidin on the green peach aphid Myzus persicae (Sulzer). J Appl Ent 131:71–75Google Scholar
  117. 117.
    Selsted ME, Novotny MJ, Morris WL, Tang YQ, Smith W, Cullor JS (1992) Indolicidin, a novel bactericidal tridecapeptide amide from neutrophils. J Biol Chem 267:4292–4295Google Scholar
  118. 118.
    Ahmad IW, Perkins R, Lupan DM, Selsted ME, Janoff AS (1995) Liposomal entrapment of the neutrophil-derived peptide indolicidin endows it with in vivo antifungal activity. Biochim Biophys Acta 1237:109–114Google Scholar
  119. 119.
    Koch A, Khalifa W, Langen G, Vilcinskas A, Kogel K-H, Imani J (2012) The antimicrobial peptide thanatin reduces fungal infections in Arabidopsis. J Phytopathol 160:606–610Google Scholar
  120. 120.
    Bromley AK, Anderson M (1982) An electrophysiological study of olfaction in the aphid Nasanovia ribisnigri. Ent Exp Appl 32:101–110Google Scholar
  121. 121.
    Dawson GW, Griffiths DS, Pichett JA, Wadhams LJ, Woodcock CM (1987) Plant-derived synergists of aphid alarm pheromone from turnip aphid, Lipaphis (Hyadaphis) erysimi (Homoptera, Aphididae). J Chem Ecol 13:1663–1671Google Scholar
  122. 122.
    Hardie J, Visser JH, Piron PGM (1995) Peripheral odour perception by adult aphid forms with the same genotype but different host-plant preferences. J Insect Physiol 41:91–97Google Scholar
  123. 123.
    Wadhams LJ (1990) The use of coupled gas chromatography: electrophysiological techniques in the identification of insect pheromones. In: McCaffery AR, Wilson AR (eds) Chromatography and isolation of insect hormones and pheromones. Plenum, New York/LondonGoogle Scholar
  124. 124.
    Yan F-S, Visser H (1982) Electroantennogram responses of the cereal aphid Sitobion avenaeto plant volatile components. In: Visser JH, Minks AK (eds) Proceedings of the 5th International Symposium on Insect-Plant Relationships. Pudoc, WageningenGoogle Scholar
  125. 125.
    van Giessen WA, Fescemyer HW, Burrows PM, Peterson JK, Barnett OW (1994) Quantification of electroantennogram responses of the primary rhinaria of Acyrthosiphon pisum (Harris) to C4–C8 primary alcohols and aldehydes. J Chem Ecol 20:909–927Google Scholar
  126. 126.
    Schneider D (1957) Elektrophysiologische Untersuchungen von Chemo- und Mechanorezeptoren der Antenne des Seidenspinners Bombyx mori L. Zeitschift für Vergleichende Physiologie 40:8–41Google Scholar
  127. 127.
    Chapman RF, Bernays EA, Simpson SJ (1990) Attraction and repulsion of the aphid, Cavariella aegopodi, by plant odours. J Chem Ecol 7:881–888Google Scholar
  128. 128.
    Visser JH, Yan F-S (1995) Electroantennogram responses of thegrain aphids Sitobion avenae (F.) and Metopolophium dirhodum (Walk.) (Hom., Aphididae) to plant odour components. J Appl Entomol 119:539–542Google Scholar
  129. 129.
    Visser JH, Piron PGM (1994) Perception of plant odour components by the vetch aphid Megoura viciae: shape characteristics of electroantennogram responses. Proc Exp Appl Entomol 5:85–90Google Scholar
  130. 130.
    Visser JH, Piron PGM (1995) Olactory antennal responses to plant volatiles in apterous virginoparae of the vetch aphid Megoura viciae. Ent Exp Appl 77:37–46Google Scholar
  131. 131.
    Visser JH, Piron PGM, Hardie J (1996) The aphid’s peripheral perception of plant volatiles. Ent Exp Appl 80:35–38Google Scholar
  132. 132.
    Wientjen WH, Lakwijk AC, Vanderma T (1973) Alarm pheromone of grain aphid. Experientia 29:658–660Google Scholar
  133. 133.
    Wohlers P, Tjallingii WF (1983) Electroantennogram responses of aphids to the alarm pheromone (E)-b-farnesene. Ent Exp Appl 33:79–82Google Scholar
  134. 134.
    Calabrese EJ, Sorensen AJ (1978) Dispersal and recolonization by Myzus persicae following aphid alarm pheromone exposure. Ann Entomol Soc Am 71:181–182Google Scholar
  135. 135.
    Montgomery ME, Nault LR (1977) Comparative response of aphids to the alarm pheromone, (E)-β-farnesene. Ent Exp Appl 22:236–242Google Scholar
  136. 136.
    Avé DA, Gregory P, Tingey WM (1987) Aphid repellent sesquiterpenes in glandular trichomes of Solanum berthaultii and Solanum tuberosum. Ent Exp Appl 44:131–138Google Scholar
  137. 137.
    Gibson RW, Pickett JA (1983) Wild potatoe repels aphids by release of aphid alarm pheromone. Nature 302:608–609Google Scholar
  138. 138.
    Kunert G, Otto S, Röse USR, Gershenzon J, Weisser WW (2005) Alarm pheromone mediates production of winged dispersal morphs in aphids. Ecol Lett 8:596–603Google Scholar
  139. 139.
    Hatano E, Kunert G, Weisser WW (2010) Aphid wing induction and ecological costs of alarm pheromone emission under field conditions. PLoS ONE 5(6):e11188. doi: 10.1371/journal.pone.0011188 Google Scholar
  140. 140.
    Sarria E, Palomares-Rius FJ, López-Sesé AI, Heredia A, Gómez-Guillamónt ML (2010) Role of leaf glandular trichomes of melon plants in deterrence of Aphis gossypii Glover. Plant Biol 12:503–511Google Scholar
  141. 141.
    Francis F, Lognay G, Haubruge E (2004) Olfactory responses to aphid and host plant volatile releases: (E)-β-farnesene an effective kairomone for the predator Adalia bipunctata. J Chem Ecol 30:741–755Google Scholar
  142. 142.
    Abassi A, Birkett S, Petterson MA, Pickett JA, Wadhams LJ, Woodcock CM (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 26:1765–1771Google Scholar
  143. 143.
    Zhu JW, Cosse AA, Obrychi JJ, Boo KS, Baker TC (1999) Olfactory reactions of the twelve-spotted lady beetle, Coleomegilla maculata and the green lacewing, Chrysoperla carnea to semiochemicals released from their prey and host plant: Electroantennogram and behavioral responses. J Chem Ecol 25:1163–1177Google Scholar
  144. 144.
    Micha SG, Wyss U (1996) Aphid alarm pheromone (E)-ß-farnesene: a host finding kairomone for the aphid primary parasitoid Aphidius uzbekistanicus (Hymenoptera: Aphidiinae). Chemoecology 7:132–139Google Scholar
  145. 145.
    Du YJ, Poppy GM, Powell W, Pickett JA, Wadhams LJ, Woodcock CM (1998) Identification of semiochemicals released during aphid feeding that attract parasitoid Aphidius ervi. J Chem Ecol 24:1355–1368Google Scholar
  146. 146.
    Verheggen FJ, Haubruge E, De Moraes CM, Mescher MC (2009) Social environment influences aphid production of alarm pheromone. Behav Ecol 20:283–288Google Scholar
  147. 147.
    Braasch J, Kaplan I (2012) Over what distance are plant volatiles bioactive? Estimating the spatial dimensions of attraction in an arthropod assemblage. Ent Exp Appl 145:115–123Google Scholar
  148. 148.
    Beale MH, Birkett MA, Bruce TJA, Chamberlain K, Field LM, Huttly AK, Martin JL, Parker R, Phillips AL, Pickett JA, Prosser IM, Shewry PR, Smart LE, Wadhams LJ, Woodcock CM, Zhang Y (2006) Aphid alarm pheromone produced by transgenic plants affects aphid and parasitoid behavior. Proc Natl Acad Sci USA 103:10509–10513Google Scholar
  149. 149.
    Kunert G, Reinhold C, Gershenzon J (2010) Constitutive emission of the aphid alarm pheromone, (E)-β-farnesene, from plants does not serve as a direct defense against aphids. BMC Ecol 10:23Google Scholar
  150. 150.
    Dixon AFG (1985) Aphid ecology, 2nd edn. Chapman & Hall, LondonGoogle Scholar
  151. 151.
    Dixon AFG (1991) Ecological interactions of aphids and their host plants. In: Campbell RK, Eikenbary RD (eds) Aphid-plant genotype interactions. Elsevier, AmsterdamGoogle Scholar
  152. 152.
    Nevo E, Coll M (2001) Effect of Nitrogen Fertilization on Aphis gossypii (Homoptera: Aphididae): Variation in Size, Color, and Reproduction. J Econ Entomol 94:27–32Google Scholar
  153. 153.
    Mackauer M (1973) Host selection and host suitability in Aphidius smithi. In: Lowe AD (ed) Perspectives in aphid biology. Bull Entomol Soc, New ZealandGoogle Scholar
  154. 154.
    Daniels M, Bale JS, Newbury HJ, Lind RJ, Pritchard J (2009) A sublethal dose of thiamethoxam causes a reduction in xylem feeding by the bird cherry-oat aphid (Rhopalosiphum padi), which is associated with dehydration and reduced performance. J Insect Physiol 55:758–765Google Scholar
  155. 155.
    Bruce TJA, Wadhams LJ, Woodcock CM (2005) Insect host location: a volatile situation. Trends Plant Sci 10:269–274Google Scholar
  156. 156.
    Döring TF, Chittka L (2007) Visual ecology of aphids—a critical review on the role of colours in host finding. Arthropod-Plant Interact 1:3–16Google Scholar
  157. 157.
    Ingwell LL, Eigenbrode SD, Bosque-Pérez NA (2012) Plant viruses alter insect behavior to enhance their spread. Sci Rep 2:578Google Scholar
  158. 158.
    Visser JH, Piron PGM (1998) An open Y-track olfactometer for recording of aphid behavioural responses to plant odours. Proc Exp Appl Entomol 9:41–46Google Scholar
  159. 159.
    Miles PW (1987) Feeding process of Aphidoidea in relation to effects on their food plants. In: Minks AK, Harrewijn P (eds) Aphids: their biology, natural enemies and control, Vol. 2A. World Crop Pests. Elsevier, AmsterdamGoogle Scholar
  160. 160.
    Tjallingii WF, Cherqui A (1999) Aphid saliva and aphid–plant interactions. Proc Sect Exp Appl Entomol Neth Entomol Soc NEV Amst 10:169–174Google Scholar
  161. 161.
    Hewer A, Becker A, van Bel AJE (2011) An aphid’s odyssey—the cortical quest for the vascular bundle. J Exp Biol 214:3868–3879Google Scholar
  162. 162.
    McLean DL, Kinsey MG (1964) A technique for electronically recording aphid feeding and salivation. Nature 202:1358–1359Google Scholar
  163. 163.
    Schaefers GA (1966) The use of direct current for electronically recording of aphid feeding and salivation. Ann Entomol Soc Am 59:1022–1029Google Scholar
  164. 164.
    Backus EA, Bennett WH (2009) The AC-DC correlation monitor: new EPG design with flexible input resistors to detect both R and emf components for any piercing-sucking hemipteran. J Insect Physiol 55:869–884Google Scholar
  165. 165.
    Walker GP (2000) A beginner’s guide to electronic monitoring of homopteran probing behaviour. In: Walker GP, Backus EA (eds) Principles and applications of electronic monitoring and other techniques in the study of homopteran feeding behavior. Thomas Say Publications in Entomology, LanhamGoogle Scholar
  166. 166.
    Caillaud CM, Di Pietro JP, Chaubet B, Pierre JS (2009) Application of discriminant analysis to electrical penetration graphs of the aphid Sitobion avenae feeding on resistant and susceptible wheat. J Appl Ent 119:103–106Google Scholar
  167. 167.
    Klingler J, Powell G, Thompson GA, Isaacs R (1998) Phloem specific aphid resistance in Cucumis melo line AR 5: effects on feeding behavior and performance of Aphis gossypii. Ent Exp Appl 86:79–88Google Scholar
  168. 168.
    van Helden M, Tjallingii WF (1993) Tissue localization of lettuce resistance to the aphid Nasonovia ribisnigri using electrical penetration graphs. Ent Exp Appl 68:269–278Google Scholar
  169. 169.
    Fraley RT, Rogers SG, Horsch RB, Sanders PR, Flick JS, Adams SP, Bittner ML, Brand LA, Fink CL, Fry JS, Galluppi GR, Goldberg SB, Hoffmann NL, Woo SC (1983) Expression of bacterial genes in plant cells. Proc Natl Acad Sci USA 80:4803–4807Google Scholar
  170. 170.
    Mazur BJ, Falco SC (1989) The development of herbicide resistant crops. Ann Rev Plant Physiol Plant Mol Biol 40:441–470Google Scholar
  171. 171.
    Vaeck M, Reynaerts A, Höfte H, Jansens S, De Beuckeleer M, Dean C, Zabeau M, van Montagu M, Leemans J (1987) Nature 328:33–37Google Scholar
  172. 172.
    Ye X, Al-Babili S, Klöti A, Zhang J, Lucca P, Beyer P, Potrykus I (2000) Engineering the provitamin A (β-carotene) biosynthetic pathway into (carotenoid-free) rice endosperm. Science 287:303–305Google Scholar
  173. 173.
    Ahmad P, Ashraf M, Younis M, Hu X, Kumar A, Akram NA, Al-Qurainy F (2012) Role of transgenic plants in agriculture and biopharming. Biotech Adv 30:624–640Google Scholar
  174. 174.
    James C (2011) Global status of commercialized biotech/GM crops. ISAAA Brief No. 43. ISAAA: IthacaGoogle Scholar
  175. 175.
    Food and Agricultural Organisation of the United Nations (2012) Statistical YearbookGoogle Scholar
  176. 176.
    Hoban TJ (2004) Public attitudes towards agricultural biotechnology. ESA Working Paper No. 04–09. Agricultural and Development Economics Division. Food and Agricultural Organisation of the United NationsGoogle Scholar
  177. 177.
    Lynas M (2012) Rothamsted’s aphid-resistant wheat—a turning point for GMOs? Agric Food Sec 1:17Google Scholar

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© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Department of Phytopathology and Applied ZoologyJustus-Liebig-University GiessenGiessenGermany

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