Colorado Potato Beetle Control: Comparison
Please note this is a comparison between Version 2 by Catherine Yang and Version 1 by Martina Kadoić Balaško.

The Colorado potato beetle (CPB) is one of the most important potato pest worldwide. It is native to U.S. but during the 20th century it has dispersed through Europe, Asia and western China. It continues to expand in an east and southeast direction. Damages are caused by larvae and adults. Their feeding on potato plant leaves can cause complete defoliation and lead to a large yield loss. After the long period of using only chemical control measures, the emergence of resistance increased and some new and different methods come to the fore. The main focus of this review is on new approaches to the old CPB control problem. We describe the use of Bacillus thuringiensis and RNA interference (RNAi) as possible solutions for the future in CPB management. RNAi has proven successful in controlling many pests and shows great potential for CPB control. Better understanding of the mechanisms that affect efficiency will enable the development of this technology and boost potential of RNAi to become part of integrated plant protection in the future. We described also the possibility of using single nucleotide polymorphisms (SNPs) as a way to go deeper into our understanding of resistance and how it influences genotypes.

  • Colorado potato beetle
  • resistance problem
  • control strategies
  • GM potato
  • RNAi
  • SNPs
Please wait, diff process is still running!

References

  1. Food and Agriculture Organization of the United Nations FAO STAT. Available online: http://www.fao.org/faostat/en/#data/QC/visualize (accessed on 31 March 2020).
  2. James, C. Global Status of Commercialized Biotech/GM Crops; ISAAA: Ithaca, NY, USA, 2011; Volume 44.
  3. Oerke, E.C. Crop losses to pests. J. Agric. Sci. 2006 144, 31–43.
  4. Radcliffe, E.B.; Lagnaoui, A. Pests and Diseases. In Potato Biology and Biotechnology: Advances and Perspectives, 1st ed.; Vreugdenhil, D., Bradshaw, J., Gebhardt, C., Govers, F., Taylor, M.A., MacKerron, D.K., Ross, H.A., Eds.; Elsevier: Oxford, UK, 2007; pp. 545–554.
  5. Weber, D. Colorado beetle: Pest on the move. Pestic. Outlook 2003, 14, 256–259.
  6. Alyokhin, A. Colorado potato beetle management on potatoes: Current challenges and future prospects. Fruit Veg. Cereal Sci. Biotechnol. 2009, 3, 10–19.
  7. Riley, C.V. Seventh Annual Report on the Noxious, Beneficial, and Other Insects of the State of Missouri, 1st ed.; Regan & Carter: Jefferson City, MO, USA, 1875; pp. 1–50.
  8. Casagrande, R.A. The Colorado potato beetle: 125 years of mismanagement. Bull. Entomol. Soc. Am. 1987, 33, 142–150.
  9. Alyokhin, A.; Baker, M.; Mota-Sanchez, D.; Dively, G.; Grafius, E. Colorado potato beetle resistance to insecticides. Am. J. Potato Res. 2008, 85, 395–413.
  10. Cong, W.A.N.G.; Han, X.U.; Pan, X.B. Management of Colorado potato beetle in invasive frontier areas. J. Integr. Agric. 2020, 19, 360–366.
  11. Ferro, D.N.; Logan, J.A.; Voss, R.H.; Elkinton, J.S. Colorado potato beetle (Coleoptera: Chrysomelidae) temperature-dependent growth and feeding rates. Environ. Entomol. 1985, 14, 343–348.
  12. Kennedy, G.G. Colorado potato beetle. In Encyclopedia of Insects, 1st ed.; Academic Press: Cambridge, MA, USA, 2009; pp. 212–213.
  13. Alyokhin, A.; Udalov, M.; Benkovskaya, G. The Colorado potato beetle. Insect Pests of Potato. Glob. Perspect. Biol. Manag. 2013, 2, 11.
  14. Maharijaya, A.; Vosman, B. Managing the Colorado potato beetle; the need for resistance breeding. Euphytica 2015, 204, 487–501.
  15. Kiss, J.; Komaromi, J.; Bayar, K.; Edwards, C.R.; Hatala-Zseller, I. Western corn rootworm (Diabrotica virgifera virgifera LeConte) and the crop rotation systems in Europe. In Western Corn Rootworm: Ecology and Management, 1st ed.; Vidal, S., Kuhlmann, U., Edwards, C.R., Eds.; CAB International: Wallingford, UK, 2005; pp. 189–220.
  16. Grafius, E.J.; Douches, D.S. The present and future role of insect-resistant genetically modified potato cultivars in IPM. In Integration of Insect-Resistant Genetically Modified Crops within IPM Programs, 1st ed.; Springer: Dordrecht, The Netherlands, 2008; pp. 195–221.
  17. Gauthier, N.L.; Hofmaster, R.N.; Semel, M. History of Colorado potato beetle control. Adv. Potato Pest Manag. 1981, 23, 13–33.
  18. Grafius, E. Economic impact of insecticide resistance in the Colorado potato beetle (Coleoptera: Chrysomelidae) on the Michigan potato industry. J. Econ. Entomol. 1997, 90, 1144–1151.
  19. Stanković, S.; Zabel, A.; Kostic, M.; Manojlovic, B.; Rajkovic, S. Colorado potato beetle [Leptinotarsa decemlineata (Say)] resistance to organophosphates and carbamates in Serbia. J. Pest Sci. 2004, 77, 11–15.
  20. Sladan, S.; Miroslav, K.; Ivan, S.; Snezana, J.; Petar, K.; Goran, T.; Jevdovic, R. Resistance of Colorado potato beetle (Coleoptera: Chrysomelidae) to neonicotinoids, pyrethroids and nereistoxins in Serbia. Rom. Biotechnol. Lett. 2012, 17, 7599–7609.
  21. Szendrei, Z.; Grafius, E.; Byrne, A.; Ziegler, A. Resistance to neonicotinoid insecticides in field populations of the Colorado potato beetle (Coleoptera: Chrysomelidae). Pest Manag. Sci. 2012, 68, 941–946.
  22. Scott, I.M.; Tbeetle Leptinotaolman, J.H.; MacArthur, D.C. Insecticide resistance and cross‐resistance development in Colorado potato rsa decemlineata Say (Coleoptera: Chrysomelidae) populations in Canada 2008–2011. Pest Manag. Sci. 2015, 71, 712–721.
  23. Arthropod Pesticide Resistance Database (APRD). Leptinotarsa decemlineata-Shown Resistance to Active Ingredient(s). Available online: https://www.pesticideresistance.org/display.php?page=species&arId=141 (accessed on 26 February 2020).
  24. Hellmich, R.L.; Albajes, R.; Bergvinson, D.; Prasifka, J.R.; Wang, Z.Y.; Weiss, M.J. The present and future role of insect-resistant genetically modified maize in IPM. In Integration of Insect-Resistant Genetically Modified Crops within IPM Programs, 1st ed.; Springer: Dordrecht, The Netherlands, 2008; pp. 119–158.
  25. Abbas, M.S.T. Genetically engineered (modified) crops (Bacillus thuringiensis crops) and the world controversy on their safety. Egypt. J. Biol. Pest Control 2018, 28, 1–12.
  26. SPUDsmart. Potato Breeding: A European Approach, Part III. Available online: https://spudsmart.com/potato-breeding-a-european-approach-part-iii/ (accessed on 20 May 2020).
  27. European Food Safety Authority (EFSA). Available online: http://www.efsa.europa.eu/ (accessed 30 March 2020).
  28. Thompson, A.L.; Farnsworth, B.L.; Gudmestad, N.C.; Secor, G.A.; Preston, D.A.; Sowokinos, J.R.; Glynn, M.; Hatterman-Valenti, H. Dakota diamond: An exceptionally high yielding, cold chipping potato cultivar with long-term storage potential. Am. J. Potato Res. 2008, 85, 171.
  29. Dik, A.; Ceglarska, E.; Ilovai, Z. Sweet pepper: Development in plant pathology. In Integrated Pest and Disease Management in Greenhouse Crops; Springer: Dodrecht, The Netherlands, 2000; pp. 473–485.
  30. Walker, K.; Mendelsohn, M.; Matten, S.; Alphin, M.; Ave, D. The role of microbial Bt products in US crop protection. J. New Seeds 2003, 5, 31–51.
  31. Perlak, F.J.; Stone, T.B.; Muskopf, Y.M.; Petersen, L.J.; Parker, G.B.; McPherson, S.A.; Wyman, J.; Love, S.; Reed, G.; Biever, D.; et al. Genetically improved potatoes: Protection from damage by Colorado potato beetles. Plant Mol. Biol. 1993, 22, 313–321.
  32. Whalon, M.E.; Wingerd, B.A. Bt: Mode of action and use. Arch. Insect Biochem. Physiol. Publ. Collab. Entomol. Soc. Am. 2003, 54, 200–211.
  33. Sexson, D.L.; Wyman, J.A. Effect of crop rotation distance on populations of Colorado potato beetle (Coleoptera: Chrysomelidae): Development of areawide Colorado potato beetle pest management strategies. J. Econ. Entomol. 2005, 98, 716–724.
  34. Christou, P.; Capell, T.; Kohli, A.; Gatehouse, J.A.; Gatehouse, A.M. Recent developments and future prospects in insect pest control in transgenic crops. Trends Plant Sci. 2006, 11, 302–308.
  35. Fischhoff, D.A.; Fuchs, R.L.; Lavrik, P.B.; McPherson, S.A.; Perlak, F.J. Insect Resistant Tomato and Potato Plants. U.S. Patent No. 5,495,071, 27 February 1996.
  36. Thomas, P.E.; Kaniewski, W.K.; Lawson, E.C. Reduced field spread of potato leafroll virus in potatoes transformed with the potato leafroll virus coat protein gene. Plant Dis. 1997, 81, 1447–1453.
  37. Adang, M.J.; Brody, M.S.; Cardineau, G.; Eagan, N.; Roush, R.T.; Shewmaker, C.K.; Jones, A.; Oakes, J.V.; McBride, K.E. The reconstruction and expression of a Bacillus thuringiensis cryIIIA gene in protoplasts and potato plants. Plant Mol. Biol. 1993, 21, 1131–1145.
  38. Haffani, Y.Z.; Overney, S.; Yelle, S.; Bellemare, G.; Belzile, F.J. Premature polyadenylation contributes to the poor expression of the Bacillus thuringiensis cry3Ca1 gene in transgenic potato plants. Mol. Gen. Genet. Mgg 2000, 264, 82–88.
  39. Naimov, S.; Weemen-Hendriks, M.; Dukiandjiev, S.; de Maagd, R.A. Bacillus thuringiensis delta-endotoxin Cry1 hybrid proteins with increased activity against the Colorado potato beetle. Appl. Environ. Microbiol. 2001, 67, 5328–5330.
  40. Meissle, M.; Romeis, J. Insecticidal activity of Cry3Bb1 expressed in Bt maize on larvae of the Colorado potato beetle, Leptinotarsa Decemlineata. Entomol. Exp. Appl. 2009, 131, 308–319.
  41. Reed, G.L.; Jensen, A.S.; Riebe, J.; Head, G.; Duan, J.J. Transgenic Bt potato and conventional insecticides for Colorado potato beetle management: Comparative efficacy and non‐target impacts. Entomol. Exp. Appl. 2001, 100, 89–100.
  42. Keller, B.; Langenbruch, G.A. Control of coleopteran pests by Bacillus thuringiensis. In Bacillus Thuringiensis, an Environmental Biopesticide: Theory and Practice; John Wiley & Sons: New York, NY, USA, 1993; pp.171–191.
  43. Kaniewski, W.K.; Thomas, P.E. The potato story. J. Agrobiotechnol. Manag. Econ. 2004, 7, 8.
  44. Alyokhin, A.V.; Ferro, D.N. Relative fitness of Colorado potato beetle (Coleoptera: Chrysomelidae) resistant and susceptible to the Bacillus thuringiensis Cry3A toxin. J. Econ. Entomol. 1999, 92, 510–515.
  45. Hoy, C.W. Colorado potato beetle resistance management strategies for transgenic potatoes. Am. J. Potato Res. 1999, 76, 215–219.
  46. Whalon, M.E.; Ferro, D.N. Bt-potato resistance management. In Now or Never: Serious New Plans to Save a Natural Pest Control; Union of Concerned Scientists: Cambridge, MA, USA, 1998.
  47. Thornton, M. The rise and fall of NewLeaf potatoes. NABC Rep. 2003, 15, 235–243.
  48. Zhao, J.Z.; Bishop, B.A.; Grafius, E.J. Inheritance and synergism of resistance to imidacloprid in the Colorado potato beetle (Coleoptera: Chrysomelidae). J. Econ. Entomol. 2000, 93, 1508–1514.
  49. Olson, E.R.; Dively, G.P.; Nelson, J.O. Baseline susceptibility to imidacloprid and cross resistance patterns in Colorado potato beetle (Coleoptera: Chrysomelidae) populations. J. Econ. Entomol. 2000, 93, 447–458.
  50. Mota‐Sanchez, D.; Hollingworth, R.M.; Grafius, E.J.; Moyer, D.D. Resistance and cross‐resistance to neonicotinoid insecticides and spinosad in the Colorado potato beetle, Leptinotarsa decemlineata (Say)(Coleoptera: Chrysomelidae). Pest Manag. Sci. 2006, 62, 30–37.
  51. Alyokhin, A.; Dively, G.; Patterson, M.; Castaldo, C.; Rogers, D.; Mahoney, M.; Wollam, J. Resistance and cross‐resistance to imidacloprid and thiamethoxam in the Colorado potato beetle Leptinotarsa Decemlineata. Pest Manag. Sci. 2007, 63, 32–41.
  52. Spooner, D.M.; Bamberg, J.B. Potato genetic resources: Sources of resistance and systematics. Am. Potato J. 1994, 71, 325–337.
  53. Balbyshev, N.F.; Lorenzen, J.H. Hypersensitivity and egg drop: A novel mechanism of host plant resistance to Colorado potato beetle (Coleoptera: Chrysomelidae). J. Econ. Entomol. 1997, 90, 652–657.
  54. Lorenzen, J.H.; Balbyshev, N.F.; Lafta, A.M.; Casper, H.; Tian, X.; Sagredo, B. Resistant potato selections contain leptine and inhibit development of the Colorado potato beetle (Coleoptera: Chrysomelidae). J. Econ. Entomol. 2001, 94, 1260–1267.
  55. Coombs, J.J.; Douches, D.S.; Li, W.; Grafius, E.J.; Pett, W.L. Combining engineered (Bt-cry3A) and natural resistance mechanisms in potato for control of Colorado potato beetle. J. Am. Soc. Hortic. Sci. 2002, 127, 62–68.
  56. Mansoor, S.; Amin, I.; Hussain, M.; Zafar, Y.; Briddon, R.W. Engineering novel traits in plants through RNA interference. Trends Plant Sci. 2006, 11, 559–565.
  57. He, W.W.; Xu, S.J.; Xu, L.T.; Zhang, J. RNA interference in Colorado potato beetle (Leptinotarsa decemlineata): A potential strategy for pest control. J. Integr. Agric. 2020, 19, 428–437.
  58. Zhang, J.; Khan, S.A.; Heckel, D.G.; Bock, R. Next-generation insect-resistant plants: RNAi-mediated crop protection. Trends Biotechnol. 2017, 35, 871–882.
  59. Zhang, H.; Li, H.C.; Miao, X.X. Feasibility, limitation and possible solutions of RNAi‐based technology for insect pest control. Insect Sci. 2013, 20, 15–30.
  60. Dowling, D.P.; Miles, Z.D.; Köhrer, C.; Maiocco, S.J.; Elliott, S.J.; Bandarian, V.; Drennan, C.L. Molecular basis of cobalamin-dependent RNA modification. Nucleic Acids Res. 2016, 44, 9965–9976.
  61. Baum, J.A.; Bogaert, T.; Clinton, W.; Heck, G.R.; Feldmann, P.; Ilagan, O.; Johnson, S.; Plaetinck, G.; Munyikwa, T.; Pleau, M.; et al. Control of coleopteran insect pests through RNA interference. Nat. Biotechnol. 2007, 25, 1322–1326.
  62. Swevers, L.; Smagghe, G. Use of RNAi for control of insect crop pests. In Arthropod-Plant Interactions, 1st ed.; Smagghe, G., Diaz, I., Eds.; Springer: Dordrecht, The Netherlands, 2012; pp. 177–197.
  63. Kumar, A.; Congiu, L.; Lindström, L.; Piiroinen, S.; Vidotto, M.; Grapputo, A. Sequencing, de novo assembly and annotation of the Colorado potato beetle, Leptinotarsa decemlineata, transcriptome. PLoS ONE 2014, 9, e86012.
  64. Schoville, S.D.; Chen, Y.H.; Andersson, M.N.; Benoit, J.B.; Bhandari, A.; Bowsher, J.H.; Brevik, K.; Cappelle, K.; Chen, M.J.M.; Childers, A.K.; et al. A model species for agricultural pest genomics: The genome of the Colorado potato beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae). Sci. Rep. 2018, 8, 1–18.
  65. Zhu, F.; Xu, J.; Palli, R.; Ferguson, J.; Palli, S.R. Ingested RNA interference for managing the populations of the Colorado potato beetle, Leptinotarsa Decemlineata. Pest Manag. Sci. 2011, 67, 175–182.
  66. Zhou, L.T.; Jia, S.; Wan, P.J.; Kong, Y.; Guo, W.C.; Ahmat, T.; Li, G.Q. RNA interference of a putative S-adenosyl-L-homocysteine hydrolase gene affects larval performance in Leptinotarsa decemlineata (Say). J. Insect Physiol. 2013, 59, 1049–1056.
  67. Wan, Y.; Qu, K.; Zhang, Q.C.; Flynn, R.A.; Manor, O.; Ouyang, Z.; Zhang, J.; Spitale, R.C.; Snyder, M.P.; Segal, E.; et al. Landscape and variation of RNA secondary structure across the human transcriptome. Nature 2014, 505, 706–709.
  68. Gaddelapati, S.C.; Kalsi, M.; Roy, A.; Palli, S.R. Cap’n’collar C regulates genes responsible for imidacloprid resistance in the Colorado potato beetle, Leptinotarsa decemlineata. Insect Biochem. Mol. Biol. 2018, 99, 54–62.
  69. Kong, Y.; Liu, X.P.; Wan, P.J.; Shi, X.Q.; Guo, W.C.; Li, G.Q. The P450 enzyme Shade mediates the hydroxylation of ecdysone to 20‐hydroxyecdysone in the Colorado potato beetle, Leptinotarsa decemlineata. Insect Mol. Biol. 2014, 23, 632–643.
  70. Ochoa-Campuzano, C.; Martínez-Ramírez, A.C.; Contreras, E.; Rausell, C.; Real, M.D. Prohibitin, an essential protein for Colorado potato beetle larval viability, is relevant to Bacillus thuringiensis Cry3Aa toxicity. Pestic. Biochem. Physiol. 2013, 107, 299–308.
  71. Liu, X.P.; Fu, K.Y.; Lü, F.G.; Meng, Q.W.; Guo, W.C.; Li, G.Q. Involvement of FTZ-F1 in the regulation of pupation in Leptinotarsa decemlineata (Say). Insect Biochem. Mol. Biol. 2014, 55, 51–60.
  72. Fu, K.Y.; Guo, W.C.; Ahmat, T.; Li, G.Q. Knockdown of a nutrient amino acid transporter gene LdNAT1 reduces free neutral amino acid contents and impairs Leptinotarsa decemlineata pupation. Sci. Rep. 2015, 5, 18124.
  73. Zhang, J.; Khan, S.A.; Hasse, C.; Ruf, S.; Heckel, D.G.; Bock, R. Full crop protection from an insect pest by expression of long double-stranded RNAs in plastids. Science 2015, 347, 991–994.
  74. Lü, F.G.; Fu, K.Y.; Guo, W.C.; Li, G.Q. Characterization of two juvenile hormone epoxide hydrolases by RNA interference in the Colorado potato beetle. Gene 2015, 570, 264–271.
  75. Wan, P.J.; Fu, K.Y.; Lü, F.G.; Guo, W.C.; Li, G.Q. Knockdown of a putative alanine aminotransferase gene affects amino acid content and flight capacity in the Colorado potato beetle Leptinotarsa decemlineata. Amino Acids 2015, 47, 1445–1454.
  76. Wan, P.J.; Fu, K.Y.; Lü, F.G.; Wang, X.X.; Guo, W.C.; Li, G.Q. Knocking down a putative Δ1‐pyrroline‐5‐carboxylate dehydrogenase gene by RNA interference inhibits flight and causes adult lethality in the Colorado potato beetle Leptinotarsa decemlineata (Say). Pest Manag. Sci. 2015, 71, 1387–1396.
  77. Guo, W.C.; Liu, X.P.; Fu, K.Y.; Shi, J.F.; Lü, F.G.; Li, G.Q. Functions of nuclear receptor HR3 during larval-pupal molting in Leptinotarsa decemlineata (Say) revealed by in vivo RNA interference. Insect Biochem. Mol. Biol. 2015, 63, 23–33.
  78. Shi, J.F.; Fu, J.; Mu, L.L.; Guo, W.C.; Li, G.Q. Two Leptinotarsa uridine diphosphate N-acetylglucosamine pyrophosphorylases are specialized for chitin synthesis in larval epidermal cuticle and midgut peritrophic matrix. Insect Biochem. Mol. Biol. 2016, 68, 1–12.
  79. Shi, J.F.; Mu, L.L.; Chen, X.; Guo, W.C.; Li, G.Q. RNA interference of chitin synthase genes inhibits chitin biosynthesis and affects larval performance in Leptinotarsa decemlineata (Say). Int. J. Biol. Sci. 2016, 12, 1319.
  80. Shi, J.F.; Xu, Q.Y.; Sun, Q.K.; Meng, Q.W.; Mu, L.L.; Guo, W.C.; Li, G.Q. Physiological roles of trehalose in Leptinotarsa larvae revealed by RNA interference of trehalose-6-phosphate synthase and trehalase genes. Insect Biochem. Mol. Biol. 2016, 77, 52–68.
  81. Guo, W.C.; Liu, X.P.; Fu, K.Y.; Shi, J.F.; Lü, F.G.; Li, G.Q. Nuclear receptor ecdysone‐induced protein 75 is required for larval–pupal metamorphosis in the Colorado potato beetle Leptinotarsa decemlineata (Say). Insect Mol. Biol. 2016, 25, 44–57.
  82. Fu, K.Y.; Li, Q.; Zhou, L.T.; Meng, Q.W.; Lü, F.G.; Guo, W.C.; Li, G.Q. Knockdown of juvenile hormone acid methyl transferase severely affects the performance of Leptinotarsa decemlineata (Say) larvae and adults. Pest Manag. Sci. 2016, 72, 1231–1241.
  83. Fu, K.Y.; Zhu, T.T.; Guo, W.C.; Ahmat, T.; Li, G.Q. Knockdown of a putative insulin-like peptide gene LdILP2 in Leptinotarsa decemlineata by RNA interference impairs pupation and adult emergence. Gene 2016, 581, 170–177.
  84. Xu, L.; Zhang, Y.; Zhang, S.; Deng, J.; Lu, M.; Zhang, L.; Zhang, J. Comparative analysis of the immune system of an invasive bark beetle, Dendroctonus valens, infected by an entomopathogenic fungus. Dev. Comp. Immunol. 2018, 88, 65–69.
  85. Hussain, T.; Aksoy, E.; Çalışkan, M.E.; Bakhsh, A. Transgenic potato lines expressing hairpin RNAi construct of molting-associated EcR gene exhibit enhanced resistance against Colorado potato beetle (Leptinotarsa decemlineata, Say). Transgenic Res. 2019, 28, 151–164.
  86. Petek, M.; Coll, A.; Razinger, J.; Gruden, K. Validating the potential of double-stranded RNA targeting Colorado potato beetle mesh gene in laboratory and field trials. bioRxiv 2020, doi:10.1101/2020.02.13.945097.
  87. Gui, S.; Taning, C.N.T.; Wei, D.; Smagghe, G. First report on CRISPR/Cas9-targeted mutagenesis in the Colorado potato beetle, Leptinotarsa Decemlineata. J. Insect Physiol. 2020, 121, 104013.
  88. Palli, S.R. RNA interference in Colorado potato beetle: Steps toward development of dsRNA as a commercial insecticide. Curr. Opin. Insect Sci. 2014, 6, 1–8.
  89. Whitten, M.M.; Facey, P.D.; Del Sol, R.; Fernández-Martínez, L.T.; Evans, M.C.; Mitchell, J.J.; Bodger, O.G.; Dyson, P.J. Symbiont-mediated RNA interference in insects. Proc. R. Soc. B Biol. Sci. 2016, 283, 20160042.
  90. Taning, C.N.; Christiaens, O.; Li, X.; Swevers, L.; Casteels, H.; Maes, M.; Smagghe, G. Engineered flock house virus for targeted gene suppression through RNAi in fruit flies (Drosophila melanogaster) in vitro and in vivo. Front. Physiol. 2018, 9, 805.
  91. Cagliari, D.; Avila dos Santos, E.; Dias, N.; Smagghe, G.; Zotti, M. Nontransformative strategies for RNAi in crop protection. In Modulating Gene Expression-Abridging the RNAi and CRISPR-Cas9 Technologies; IntechOpen: Rijeka, Croatia, 2019.
  92. Christiaens, O.; Dzhambazova, T.; Kostov, K.; Arpaia, S.; Joga, M.R.; Urru, I.; Sweet, J.; Smagghe, G.; Literature review of baseline information on RNAi to support the environmental risk assessment of RNAi‐based GM plants. EFSA Supporting Publ. 2018, 15, 1424E.
  93. Burand, J.P.; Hunter, W.B. RNAi: Future in insect management. J. Invertebr. Pathol. 2013, 112, S68–S74.
  94. Katoch, R.; Sethi, A.; Thakur, N.; Murdock, L.L. RNAi for insect control: Current perspective and future challenges. Appl. Biochem. Biotechnol. 2013, 171, 847–873.
  95. Clark, J.M.; Lee, S.H.; Kim, H.J.; Yoon, K.S.; Zhang, A. DNA‐based genotyping techniques for the detection of point mutations associated with insecticide resistance in Colorado potato beetle Leptinotarsa Decemlineata. Pest Manag. Sci. 2001, 57, 968–974.
  96. Udalov, M.B.; Benkovskaya, G.V. Population genetics of the Colorado potato beetle: From genotype to phenotype. Russ. J. Genet. Appl. Res. 2011, 1, 321.
  97. Grapputo, A.; Boman, S.; Lindstroem, L.; Lyytinen, A.; Mappes, J. The voyage of an invasive species across continents: Genetic diversity of North American and European Colorado potato beetle populations. Mol. Ecol. 2005, 14, 4207–4219.
  98. Sakai, A.K.; Allendorf, F.W.; Holt, J.S.; Lodge, D.M.; Molofsky, J.; With, K.A.; Baughman, S.; Cabin, R.J.; Cohen, J.E.; Ellstrand, N.C.; et al. The population biology of invasive species. Annu. Rev. Ecol. Syst. 2001, 32, 305–332.
  99. Xing, C.; Schumacher, F.R.; Xing, G.; Lu, Q.; Wang, T.; Elston, R.C. December. Comparison of microsatellites, single-nucleotide polymorphisms (SNPs) and composite markers derived from SNPs in linkage analysis. BMC Genet. 2005, 6, S29.
  100. Genissel, A.; Pastinen, T.; Dowell, A.; Mackay, T.F.; Long, A.D. No evidence for an association between common nonsynonymous polymorphisms in Delta and bristle number variation in natural and laboratory populations of Drosophila melanogaster. Genetics 2004, 166, 291–306.
  101. Coates, B.S.; Sumerford, D.V.; Miller, N.J.; Kim, K.S.; Sappington, T.W.; Siegfried, B.D.; Lewis, L.C. Comparative performance of single nucleotide polymorphism and microsatellite markers for population genetic analysis. J. Hered. 2009, 100, 556–564.
  102. Kotsakiozi, P.; Evans, B.R.; Gloria‐Soria, A.; Kamgang, B.; Mayanja, M.; Lutwama, J.; Le Goff, G.; Ayala, D.; Paupy, C.; Badolo, A.; et al. Population structure of a vector of human diseases: Aedes aegypti in its ancestral range, Africa. Ecol. Evol. 2018, 8, 7835–7848.
  103. Saarman, N.P.; Opiro, R.; Hyseni, C.; Echodu, R.; Opiyo, E.A.; Dion, K.; Johnson, T.; Aksoy, S.; Caccone, A. The population genomics of multiple tsetse fly (Glossina fuscipes fuscipes) admixture zones in Uganda. Mol. Ecol. 2019, 28, 66–85.
  104. Francischini, F.J.; Cordeiro, E.M.; de Campos, J.B.; Alves-Pereira, A.; Viana, J.P.G.; Wu, X.; Wei, W.; Brown, P.; Joyce, A.; Murua, G.; et al. Diatraea saccharalis history of colonization in the Americas. The case for human-mediated dispersal. PLoS ONE 2019, 14, e0220031.
  105. Yadav, S.; Stow, A.J.; Dudaniec, R.Y. Detection of environmental and morphological adaptation despite high landscape genetic connectivity in a pest grasshopper (Phaulacridium vittatum). Mol. Ecol. 2019, 8, 3395–3412.
  106. Brumfield, R.T.; Beerli, P.; Nickerson, D.A.; Edwards, S.V. The utility of single nucleotide polymorphisms in inferences of population history. Trends Ecol. Evol. 2003, 18, 249–256.
  107. Morin, P.A.; Luikart, G.; Wayne, R.K. SNPs in ecology, evolution and conservation. Trends Ecol. Evol. 2004, 19, 208–216.
  108. Jaccoud, D.; Peng, K.; Feinstein, D.; Kilian, A. Diversity arrays: A solid state technology for sequence information independent genotyping. Nucleic Acids Res. 2001, 29, e25.
  109. Nantoume, A.D.; Andersen, S.B.; Jensen, B.D. Genetic differentiation of watermelon landrace types in Mali revealed by microsatellite (SSR) markers. Genet. Resour. Crop Evol. 2013, 60, 2129–2141.
More
ScholarVision Creations