Advertisement

Responses of the Colorado Potato Beetle (Coleoptera: Chrysomelidae) to the Chemical Composition of Potato Plant Foliage

  • Guoqi Wen
  • Mohamed KhelifiEmail author
  • Athyna N. Cambouris
  • Noura Ziadi
Article

Abstract

The Colorado potato beetle (CPB), Leptinotarsa decemlineata (Say), is widely considered as the most serious insect defoliator of potato plants (Solanum tuberosum L.). The CPB can completely destroy potato crops and cause tremendous yield losses if left uncontrolled. For decades, CPB populations have been suppressed mainly by chemical insecticides. However, this insect’s diverse and flexible life history, combined with its remarkable adaptability to a variety of stressors, makes the CPB a very challenging pest to control. Potato foliage, which contains high amounts of volatile and non-volatile chemicals, is the CPB’s main food source. Researchers indicated that variations in the feeding performance and abundance of this beetle are attributable to the quality and quantity of chemical components in the host plant foliage. This review investigated the effects of volatile chemicals, carbohydrates, amino acids, glycoalkaloids, and mineral elements in potato foliage on the feeding behaviour and performance of the CPB. In general, the chemical components in potato foliage could enhance or reduce the feeding of the CPB. Altering the chemical composition of potato foliage could be an interesting alternative to reduce the use of insecticides to manage CPB populations in potato crops.

Keywords

Amino acids Carbohydrate Glycoalkaloids Insect control Minerals Volatile chemicals 

Notes

Acknowledgments

The authors wish to thank Xiangru Zhang and Haixiao Li from Agriculture and Agri-Food Canada (AAFC) for their constructive comments on the manuscript. This work was supported by AAFC through the Growing Forward program.

References

  1. Agelopoulos NG, Hooper AM, Maniar SP, Pickett JA, Wadhams LJ (1999) A novel approach for isolation of volatile chemicals released by individual leaves of a plant in situ. J Chem Ecol 25(6):1411–1425.  https://doi.org/10.1023/A:1020939112234 CrossRefGoogle Scholar
  2. Alyokhin A (2009) Colorado potato beetle management on potatoes: current challenges and future prospects. Fruit Veg Cereal Sci Biotechnol 3:10–19Google Scholar
  3. Alyokhin A, Mota-Sanchez D, Baker M, Snyder WE, Menasha S, Whalon M, Dively G, Moarsi WF (2015) The Red Queen in a potato field: integrated pest management versus chemical dependency in Colorado potato beetle control. Pest Manag Sci 71:343–356.  https://doi.org/10.1002/ps.3826 CrossRefPubMedGoogle Scholar
  4. Alyokhin A, Porter G, Groden E, Drummond F (2005) Colorado potato beetle response to soil amendments: a case in support of the mineral balance hypothesis? Agric Ecosyst Environ 109:234–244.  https://doi.org/10.1016/j.agee.2005.03.005 CrossRefGoogle Scholar
  5. Armer CA (2004) Colorado potato beetle toxins revisited: evidence the beetle does not sequester host plant glycoalkaloids. J Chem Ecol 30(4):883–888.  https://doi.org/10.1023/B:JOEC.0000028495.26931.c7 CrossRefPubMedGoogle Scholar
  6. Arrese EL, Soulages JL (2010) Insect fat body: energy, metabolism, and regulation. Annu Rev Entomol 55:207–225.  https://doi.org/10.1146/annurev-ento-112408-085356 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Ballan-Dufrançais C (2002) Localization of metals in cells of pterygote insects. Microsc Res Tech 56:403–420.  https://doi.org/10.1002/jemt.10041 CrossRefPubMedGoogle Scholar
  8. Bejarano L, Mignolet E, Devaux A, Espinola N, Carrasco E, Larondelle Y (2000) Glycoalkaloids in potato tubers: the effect of variety and drought stress on the α-solanine and α-chaconine contents of potatoes. J Sci Food Agric 80:2096–2100.  https://doi.org/10.1002/1097-0010(200011)80:14<2096::AID-JSFA757>3.0.CO;2-6 CrossRefGoogle Scholar
  9. Berge MA, Rosenthal GA, Dahlman DL (1986) Tobacco budworm, Heliothis virescens [Noctuidae] resistance to L-canavanine, a protective allelochemical. Pestic Biochem Physiol 25:319–326.  https://doi.org/10.1016/0048-3575(86)90005-2 CrossRefGoogle Scholar
  10. Boiteau G (2010) Insect pest control on potato: harmonization of alternative and conventional control methods. Am J Potato Res 87:412–419.  https://doi.org/10.1007/s12230-010-9158-z CrossRefGoogle Scholar
  11. Bolter CJ, Dicke M, Van Loon JJ, Visser JH, Posthumus MA (1997) Attraction of Colorado potato beetle to herbivore-damaged plants during herbivory and after its termination. J Chem Ecol 23:1003–1023.  https://doi.org/10.1023/B:JOEC.0000006385.70652.5e CrossRefGoogle Scholar
  12. Braun H, Fontes PCR, Silva TPD, Finger FL, Cecon PR, Ferreira APS (2016) Carbohydrates concentration in leaves of potato plants affected by nitrogen fertilization rates. Revista Ceres 63(2):241–248.  https://doi.org/10.1590/0034-737X201663020016 CrossRefGoogle Scholar
  13. Brouwers EVM, de Kort CAD (1979) Amino acid metabolism during flight in the Colorado potato beetle, Leptinotarsa decemlineata. J Insect Physiol 25:411–414.  https://doi.org/10.1016/0022-1910(79)90008-8 CrossRefGoogle Scholar
  14. Casagrande RA (2014) The Colorado potato beetle: 125 years of mismanagement. Bull Entomol Soc Am 33:142–150.  https://doi.org/10.1093/besa/33.3.142 CrossRefGoogle Scholar
  15. Chowński S, Adamski Z, Marciniak P, Rosiński G, Büyükgüzel E, Büyükgüzel K, Falabella P, Scrano L, Ventrella E, Lelario F, Bufo SA (2016) A review of bioinsecticidal activity of Solanaceae alkaloids. Toxins 8:60.  https://doi.org/10.3390/toxins8030060 CrossRefGoogle Scholar
  16. Cibula AB, Davidson RH, Fisk FW, Lapidus JB (1967) Relationship of free amino acids of some solanaceous plants to growth and development of Leptinotarsa decemlineata (Coleoptera: Chrysomelidae). Ann Entomol Soc Am 60:626–631.  https://doi.org/10.1093/aesa/60.3.626 CrossRefPubMedGoogle Scholar
  17. Cingel A, Savić J, Lazarević J, Ćosić T, Raspor M, Smigocki A, Ninković S (2017) Co-expression of the proteinase inhibitors oryzacystatin I and oryzacystatin II in transgenic potato alters Colorado potato beetle larval development. Insect Sci 24(5):768–780CrossRefGoogle Scholar
  18. de Kort CAD (1990) Thirty five years of diapause research with the Colorado potato beetle. Entomol Exp Appl 56:1–13.  https://doi.org/10.1111/j.1570-7458.1990.tb01376.x CrossRefGoogle Scholar
  19. de Ladurantaye Y, Khelifi M, Cloutier C, Coudron TA (2010) Short-term storage conditions for transport and farm delivery of the stink bug Perillus bioculatus for the biological control of the Colorado potato beetle. Can Biosyst Eng Genie Biosyst Au Can 52:4.1–4.7Google Scholar
  20. Dortland JF, de Kort CAD (1978) Protein synthesis and storage in the fat body of the Colorado potato beetle, Leptinotarsa decemlineata. Insect Biochem 8(2):93–98.  https://doi.org/10.1016/0020-1790(78)90044-6 CrossRefGoogle Scholar
  21. Dickens JC (2002) Behavioural responses of larvae of Colorado potato beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae), to host plant volatile blends attractive to adults. Agric For Entomol 4:309–314.  https://doi.org/10.1046/j.1461-9563.2002.00153.x CrossRefGoogle Scholar
  22. Domek JM, Cantelo WW, Wagner RM, Li BW, Miller-Ihli NJ (1995) Nutritional composition of potato foliage. J Agric Food Chem 43:1512–1515.  https://doi.org/10.1021/jf00054a018 CrossRefGoogle Scholar
  23. Ferro DN, Logan JA, Voss RH, Elkinton JS (1985) Colorado potato beetle (Coleoptera: Chrysomelidae) temperature-dependent growth and feeding rates. Environ Entomol 14:343–348.  https://doi.org/10.1093/ee/14.3.343 CrossRefGoogle Scholar
  24. Friedman M (2004) Analysis of biologically active compounds in potatoes (Solanum tuberosum), tomatoes (Lycopersicon esculentum), and jimson weed (Datura stramonium) seeds. J Chromatogr A 1054:143–155.  https://doi.org/10.1016/j.chroma.2004.04.049 CrossRefPubMedGoogle Scholar
  25. Friedman M (2006) Potato glycoalkaloids and metabolites: roles in the plant and in the diet. J Agric Food Chem 54(23):8655–8681.  https://doi.org/10.1021/jf061471t CrossRefPubMedGoogle Scholar
  26. Friedman M, McDonald GM, Filadelfi-Keszi M (1997) Potato glycoalkaloids: chemistry, analysis, safety, and plant physiology. Crit Rev Plant Sci 16:55–132.  https://doi.org/10.1080/07352689709701946 CrossRefGoogle Scholar
  27. Foyer CH, Parry M, Noctor G (2003) Markers and signals associated with nitrogen assimilation in higher plants. J Exp Bot 54(382):585–593.  https://doi.org/10.1093/jxb/erg053 CrossRefPubMedGoogle Scholar
  28. González-Coloma A, Reina M, Medinaveitia A, Guadaño A, Santana O, Martínez-Díaz R, Ruiz-Mesía L, Alva A, Grandez M, Díaz R, Gavín JA (2004) Structural diversity and defensive properties of norditerpenoid alkaloids. J Chem Ecol 30:1393–1408.  https://doi.org/10.1023/B:JOEC.0000037747.74665.0a CrossRefPubMedGoogle Scholar
  29. Harcourt DG (1971) Population dynamics of Leptinotarsa decemlineata (Say) in eastern Ontario. III. Major population processes. Can Entomol 103:1049–1061.  https://doi.org/10.4039/Ent1031049-7 CrossRefGoogle Scholar
  30. Harrison GD (1987) Host-plant discrimination and evolution of feeding preference in the Colorado potato beetle Leptinotarsa decemlineata. Physiol Entomol 12:407–415.  https://doi.org/10.1111/j.1365-3032.1987.tb00767.x CrossRefGoogle Scholar
  31. Hitchner EM, Kuhar TP, Dickens JC, Youngman RR, Schultz PB, Pfeiffer DG (2008) Host plant choice experiments of Colorado potato beetle (Coleoptera: Chrysomelidae) in Virginia. J Econ Entomol 101:859–865. https://doi.org/10.1603/0022-0493(2008)101[859:HPCEOC]2.0.CO;2Google Scholar
  32. Hollister B, Dickens JC, Perez F, Deahl KL (2001) Differential neurosensory responses of adult Colorado potato beetle, Leptinotarsa decemlineata, to glycoalkaloids. J Chem Ecol 27:1105–1118.  https://doi.org/10.1023/A:1010307827348 CrossRefPubMedGoogle Scholar
  33. Hosie AM, Aronstein K, Sattelle DB, ffrench-Constant RH (1997) Molecular biology of insect neuronal GABA receptors. Trends Neurosci 20:578–583.  https://doi.org/10.1016/S0166-2236(97)01127-2 CrossRefPubMedGoogle Scholar
  34. Hsiao TH, Fraenkel G (1968) The influence of nutrient chemicals on the feeding behavior of the Colorado potato beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae). Ann Entomol Soc Am 61:44–54.  https://doi.org/10.1093/aesa/61.1.44 CrossRefGoogle Scholar
  35. Huang T, Jander G, de Vos M (2011) Non-protein amino acids in plant defense against insect herbivores: representative cases and opportunities for further functional analysis. Phytochemistry 72:1531–1537.  https://doi.org/10.1016/j.phytochem.2011.03.019 CrossRefPubMedGoogle Scholar
  36. Jansson RK, Smilowitz Z (1985) Influence of nitrogen on population parameters of potato insects: abundance, development, and damage of the Colorado potato beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae). Environ Entomol 14:500–506.  https://doi.org/10.1093/ee/14.4.500 CrossRefGoogle Scholar
  37. Jonasson T, Olsson K (1994) The influence of glycoalkaloids, chlorogenic acid and sugars on the susceptibility of potato tubers to wireworm. Potato Res 37:205–216.  https://doi.org/10.1007/BF02360510 CrossRefGoogle Scholar
  38. Karley AJ, Douglas AE, Parker WE (2002) Amino acid composition and nutritional quality of potato leaf phloem sap for aphids. J Exp Biol 205:3009–3018PubMedGoogle Scholar
  39. Khelifi M, Laguë C, de Ladurantaye Y (2007) Physical control of Colorado potato beetle: a review. Appl Eng Agric 23:557–569.  https://doi.org/10.13031/2013.23663 CrossRefGoogle Scholar
  40. Kolbe H, Stephan-Beckmann S (1997) Development, growth and chemical composition of the potato crop (Solanum tuberosum L.). I. Leaf and stem. Potato Res 40:111–129.  https://doi.org/10.1007/BF02407567 CrossRefGoogle Scholar
  41. Kowalski SP, Domek JM, Deahl KL, Sanford LL (1999) Performance of Colorado potato beetle larvae, Leptinotarsa decemlineata (Say), reared on synthetic diets supplemented with Solanum glycoalkaloids. Am J Potato Res 76:305–312.  https://doi.org/10.1007/BF02853629 CrossRefGoogle Scholar
  42. Lafta AM, Lorenzen JH (1995) Effect of high temperature on plant growth and carbohydrate metabolism in potato. Plant Physiol 109(2):637–643.  https://doi.org/10.1104/pp.109.2.637 CrossRefPubMedPubMedCentralGoogle Scholar
  43. Lafta AM, Lorenzen JH (2000) Influence of high temperature and reduced irradiance on glycoalkaloid levels in potato leaves. J Am Soc Hortic Sci 125(5):563–566Google Scholar
  44. Lee KP, Simpson SJ, Wilson K (2008) Dietary protein–quality influences melanization and immune function in an insect. Funct Ecol 22(6):1052–1061.  https://doi.org/10.1111/j.1365-2435.2008.01459.x CrossRefGoogle Scholar
  45. Lefevere KS, Koopmanschap AB, De K (1989) Changes in the concentrations of metabolites in haemolymph during and after diapause in female Colorado potato beetle, Leptinotarsa decemlineata. J Insect Physiol 35:121–128.  https://doi.org/10.1016/0022-1910(89)90045-0 CrossRefGoogle Scholar
  46. Lu Y, Stephen F (2006) On the evolution of the standard amino-acid alphabet. Genome Biol 7:102.  https://doi.org/10.1186/gb-2006-7-1-102 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Lyytinen A, Lindström L, Mappes J, Julkunen–Tiitto R, Fasulati SR, Tiilikkala K (2007) Variability in host plant chemistry: behavioural responses and life-history parameters of the Colorado potato beetle (Leptinotarsa decemlineata). Chemoecology 17(1):51–56.  https://doi.org/10.1007/s00049-006-0361-9 CrossRefGoogle Scholar
  48. Maharijaya A, Vosman B (2015) Managing the Colorado potato beetle; the need for resistance breeding. Euphytica 204:487–501.  https://doi.org/10.1007/s10681-015-1467-3 CrossRefGoogle Scholar
  49. McSweeney CS, Collins EMC, Blackall LL, Seawright AA (2008) A review of anti-nutritive factors limiting potential use of Acacia angustissima as a ruminant feed. Anim Feed Sci Technol 147:158–171.  https://doi.org/10.1016/j.anifeedsci.2007.09.015 CrossRefGoogle Scholar
  50. Miflin BJ, Lea PJ (1977) Amino acid metabolism. Annu Rev Plant Physiol 28:299–329CrossRefGoogle Scholar
  51. Mitchell BK (1974) Behavioural and electrophysiological investigations on the responses of larvae of the Colorado potato beetle (Leptinotarsa decemlineata) to amino acids. Entomol Exp Appl 17:255–264.  https://doi.org/10.1111/j.1570-7458.1974.tb00343.x CrossRefGoogle Scholar
  52. Mitchell BK, Harrison GD (1984) Characterization of galeal chemosensilla in the adult Colorado beetle, Leptinotarsa decemlineata. Physiol Entomol 9:49–56.  https://doi.org/10.1111/j.1365-3032.1984.tb00680.x CrossRefGoogle Scholar
  53. Mitchell BK, McCashin BG (1994) Tasting green leaf volatiles by larvae and adults of Colorado potato beetle, Leptinotarsa decemlineata. J Chem Ecol 20:753–769.  https://doi.org/10.1007/BF02059611 CrossRefPubMedGoogle Scholar
  54. Mondy NI, Munshi CB (1990) Effect of nitrogen fertilization on glycoalkaloid and nitrate content of potatoes. J Agric Food Chem 38(2):565–567.  https://doi.org/10.1021/jf00092a050 CrossRefGoogle Scholar
  55. Muttucumaru N, Powers SJ, Elmore JS, Mottram DS, Halford NG (2013) Effects of nitrogen and sulfur fertilization on free amino acids, sugars, and acrylamide-forming potential in potato. J Agric Food Chem 61(27):6734–6742.  https://doi.org/10.1021/jf401570x CrossRefPubMedPubMedCentralGoogle Scholar
  56. Nakajima N, Hiradate S, Fujii Y (2001) Plant growth inhibitory activity of L-canavanine and its mode of action. J Chem Ecol 27:19–31.  https://doi.org/10.1023/A:1005659714947 CrossRefPubMedGoogle Scholar
  57. Peferoen M, Huybrechts R, De Loof A (1981) Longevity and fecundity in the Colorado potato beetle, Leptinotarsa decemlineata. Entomol Exp Appl 29:321–329.  https://doi.org/10.1111/j.1570-7458.1981.tb03075.x CrossRefGoogle Scholar
  58. Petersson EV, Arif U, Schulzova V, Krtková V, Hajšlová J, Meijer J, Andersson HC, Jonsson L, Sitbon F (2013) Glycoalkaloid and calystegine levels in table potato cultivars subjected to wounding, light, and heat treatments. J Agric Food Chem 61:5893–5902.  https://doi.org/10.1021/jf400318p CrossRefPubMedGoogle Scholar
  59. Prüm B, Florian Bohn H, Seidel R, Rubach S, Speck T (2013) Plant surfaces with cuticular folds and their replicas: influence of microstructuring and surface chemistry on the attachment of a leaf beetle. Acta Biomater 9:6360–6368.  https://doi.org/10.1016/j.actbio.2013.01.030 CrossRefPubMedGoogle Scholar
  60. Rangarajan A, Miller AR, Veilleux RE (2000) Leptine glycoalkaloids reduce feeding by Colorado potato beetle in diploid Solanum sp. hybrids. J Am Soc Hortic Sci 125:689–693Google Scholar
  61. Rivard D, Cloutier C, Michaud D (2004) Colorado potato beetles show differential digestive compensatory responses to host plants expressing distinct sets of defense proteins. Arch Insect Biochem Physiol 55:114–123.  https://doi.org/10.1002/arch.10136 CrossRefPubMedGoogle Scholar
  62. Rosenthal GA (2001) L-Canavanine: a higher plant insecticidal allelochemical. Amino Acids 21:319–330.  https://doi.org/10.1007/s007260170017 CrossRefPubMedGoogle Scholar
  63. Rosenthal GA, Dahlman DL (1986) L-Canavanine and protein synthesis in the tobacco hornworm Manduca sexta. Proc Natl Acad Sci 83:14–18CrossRefGoogle Scholar
  64. Sablon L, Dickens J, Haubruge É, Verheggen F (2013) Chemical ecology of the Colorado potato beetle, Leptinotarsa decemlineata (Say) (Coleoptera: chrysomelidae), and potential for alternative control methods. Insects 4:31–54.  https://doi.org/10.3390/insects4010031 CrossRefGoogle Scholar
  65. Schuetz S, Weissbecker B, Klein A, Hummel H (1997) Host plant selection of the Colorado potato beetle as influenced by damage induced volatiles of the potato plant. Naturwissenschaften 84:212–217.  https://doi.org/10.1007/s001140050381 CrossRefGoogle Scholar
  66. Shepherd T, Griffiths DW (2006) The effects of stress on plant cuticular waxes. New Phytol 171:469–499.  https://doi.org/10.1111/j.1469-8137.2006.01826.x CrossRefPubMedGoogle Scholar
  67. Sinden SL, Sanford LL, Cantelo WW, Deahl KL (1986) Leptine glycoalkaloids and resistance to the Colorado potato beetle (Coleoptera: Chrysomelidae) in Solanum chacoense. Environ Entomol 15:1057–1062.  https://doi.org/10.1093/ee/15.5.1057 CrossRefGoogle Scholar
  68. Singh SK (2018) Explorations of plant’s chemodiversity: role of nitrogen-containing secondary metabolites in plant defense. In: Molecular aspects of plant-pathogen interaction. Springer, Singapore, pp 309–332CrossRefGoogle Scholar
  69. Speijers GJA (1998) Risk assessment of potato-glycoalkaloids. In: AIR NETTOX project seminar report. pp 43–47Google Scholar
  70. Storey KB (1997) Organic solutes in freezing tolerance. Comp Biochem Physiol A 117:319–326.  https://doi.org/10.1016/S0300-9629(96)00270-8 CrossRefGoogle Scholar
  71. Subhani MN, Sahi ST, Ali L, Rehman A, Wakil W (2015) Genotypic variations in potassium contents of potato leaves infested with late blight of potato incited by Phytophthora infestans (Mont.) de Bary. J Environ Agri Sci 2:2313–8629Google Scholar
  72. Szafranek BM, Synak EE (2006) Cuticular waxes from potato (Solanum tuberosum) leaves. Phytochemistry 67(1):80–90.  https://doi.org/10.1016/j.phytochem.2005.10.012 CrossRefPubMedGoogle Scholar
  73. Szafranek BM, Synak EE, Waligóra D, Szafranek J, Nawrot J (2008) Leaf surface compounds of the potato (Solanum tuberosum) and their influence on Colorado potato beetle (Leptinotarsa decemlineata) feeding. Chemoecology 18:205–216.  https://doi.org/10.1007/s00049-008-0407-2 CrossRefGoogle Scholar
  74. Thiery D, Visser JH (1995) Satiation effects on olfactory orientation patterns of Colorado potato beetle females. C R Acad Sci III 318:105–111Google Scholar
  75. Tomlin ES, Sears MK (1992) Indirect competition between the Colorado potato beetle (Coleoptera: Chrysomelidae) and the potato leafhopper (Homoptera: Cicadellidae) on potato: laboratory study. Environ Entomol 21:787–792.  https://doi.org/10.1093/ee/21.4.787 CrossRefGoogle Scholar
  76. Vancanneyt G, Sanz C, Farmaki T, Paneque M, Ortego F, Castañera P, Sánchez-Serrano JJ (2001) Hydroperoxide lyase depletion in transgenic potato plants leads to an increase in aphid performance. Proc Natl Acad Sci 98(14):8139–8144.  https://doi.org/10.1073/pnas.141079498 CrossRefPubMedGoogle Scholar
  77. Visser JH (2011) The design of a low-speed wind tunnel as an instrument for the study of olfactory orientation in the Colorado beetle (Leptinotarsa decemlineata). Entomol Exp Appl 20:275–288.  https://doi.org/10.1111/j.1570-7458.1976.tb02644.x CrossRefGoogle Scholar
  78. Visser JH (1979) Electroantennogram responses of the Colorado beetle, Leptinotarsa decemlineata, to plant volatiles. Entomol Exp Appl 25:86–97.  https://doi.org/10.1111/j.1570-7458.1979.tb02851.x CrossRefGoogle Scholar
  79. Wang M, Zheng Q, Shen Q, Guo S (2013) The critical role of potassium in plant stress response. Int J Mol Sci 14:7370–7390.  https://doi.org/10.3390/ijms14047370 CrossRefPubMedPubMedCentralGoogle Scholar
  80. Weber DC, Ferro DN (1994) Colorado potato beetle: diverse life history poses challenge to management. Adv Potato Pest Biol Manag:54–70Google Scholar
  81. Weeda E, de Kort CAD, Th Beenakkers AM (1979) Fuels for energy metabolism in the Colorado potato beetle, Leptinotarsa decemlineata Say. J Insect Physiol 25:951–955.  https://doi.org/10.1016/0022-1910(79)90108-2 CrossRefGoogle Scholar
  82. Wilde JD, Lambers-Suverkropp KHR, Tol AV (1969) Responses to air flow and airborne plant odour in the Colorado beetle. Neth J Plant Pathol 75:53–57.  https://doi.org/10.1007/BF02137193 CrossRefGoogle Scholar
  83. Wright RJ (1984) Evaluation of crop rotation for control of Colorado potato beetles (Coleoptera: Chrysomelidae) in commercial potato fields on Long Island. J Econ Entomol 77:1254–1259.  https://doi.org/10.1093/jee/77.5.1254 CrossRefGoogle Scholar
  84. Zhang J, Khan SA, Hasse C, Ruf S, Heckel DG, Bock R (2015) Full crop protection from an insect pest by expression of long double-stranded RNAs in plastids. Science 347:991–994.  https://doi.org/10.1126/science.1261680 CrossRefPubMedGoogle Scholar

Copyright information

© European Association for Potato Research 2018

Authors and Affiliations

  • Guoqi Wen
    • 1
    • 2
  • Mohamed Khelifi
    • 1
    Email author
  • Athyna N. Cambouris
    • 2
  • Noura Ziadi
    • 2
  1. 1.Department of Soils and Agri-Food EngineeringUniversité LavalQuebec CityCanada
  2. 2.Quebec Research and Development Centre, Agriculture and Agri-Food CanadaQuebec CityCanada

Personalised recommendations