Transgenic approaches for sterile insect control of dipteran livestock pests and lepidopteran crop pests

Transgenic Insects: Techniques and Applications

Volumn , Issue , 2014, Pages 152-167

  Scott, Maxwell J ^a   Morrison, Neil I ^b   Simmons, Gregory S ^c  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

^b OXITEC LIMITED   (United Kingdom)

^c Animal Plant Health and Inspection Service Plant Protection and Quarantine Centers for Plant Health Science and Technology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84927976286     PISSN: None     EISSN: None     Source Type: Book    
DOI: None     Document Type: Chapter

References (91)

1. Alexander, J.L. (2006) Screwworms. Journal of the American Veterinary Medicine Association 228, 357-367.
2. Allen, M.L., Handler, A.M., Berkebile, D.R. and Skoda, S.R. (2004) piggyBac transformation of the New World screwworm, Cochliomyia hominivorax, produces multiple distinct mutant strains. Medical and Veterinary Entomology 18, 1-9.
3. Alphey, L. (2002) Re-engineering the sterile insect technique. Insect Biochemistry and Molecular Biology 32, 1243-1247.
4. Ant, T., Koukidou, M., Rempoulakis, P., Gong, H.F., Economopoulos, A., Vontas, J. and Alphey, L. (2012) Control of the olive fruit fly using genetics-enhanced sterile insect technique. BMC Biology 10, 51.
5. APHIS (2009) Use of Genetically Engineered Fruit Fly and Pink Bollworm in APHIS Plant Pest Control Programs; Record of Decision. Federal Register 74, 21314-21316.
6. Benedict, M.Q., Eckerstorfer, M., Franz, G., Gaugitsch, H., Greiter, A., Heissenbergera, A., Knols, B.G., Kumschickc, S., Nentwigc, W. and Rabitsch, W. (2010) Defining Environmental Risk Assessment Criteria for Genetically Modified Insects to be placed on the EU Market. Technical report submitted to EFSA.
7. Benedict, M.Q. and Robinson, A.S. (2003) The first releases of transgenic mosquitoes: an argument for the sterile insect technique. Trends in Parasitology 19, 349-355.
8. Berghammer, A.J., Klingler, M. and Wimmer, E.A. (1999) A universal marker for transgenic insects. Nature 402, 370-371.
9. Bloem, K.A. and Bloem, S. (2000) SIT for codling moth eradication in British Columbia, Canada. In: Tan, K.H. (ed.) Area-wide Control of Fruit Flies and Other Insect Pests. Pernebit Universiti Sains Malaysia, Pulau Pinang, Malaysia, pp. 207-214.
10. Bloem, K.A., Bloem, S. and Carpenter, J.E. (2005) Impact of moth suppression/eradication programmes using the sterile insect technique or inherited sterility. In: Dyck, V.A., Hendrichs, J. and Robinson, A.S. (eds) Sterile Insect Technique. Principles and Practice in Area-Wide Integrated Pest Management. Springer, Dordrecht, the Netherlands, pp. 677-700.
11. Bloem, S., Bloem, K.A., Carpenter, J.E. and Calkins, C.O. (1999) Inherited sterility in codling moth (Lepidoptera: Tortricidae): effect of substerilizing doses of radiation on insect fecundity, fertility, and control. Annals of the Entomological Society of America 92, 222-229.
12. Bushland, R.C., Lindquist, A.W. and Knipling, E.F. (1955) Eradication of Screw-Worms through Release of Sterilized Males. Science 122, 287-288.
13. Carpenter, J.E., Bloem, S. and Marec, F. (2005) Inherited sterility in insects. In: Dyck, V.A., Hendrichs, J. and Robinson, A.S. (eds) Sterile Insect Technique. Principles and Practice in Area-Wide Integrated Pest Management. Springer, Dordrecht, the Netherlands, pp. 115-146.
14. Carpenter, J.E.H., Nelley, N. and Mullinix, B.G. (1997) Effect of substerilizing doses of radiation on sperm precedence in fall armyworm (Lepidoptera: Noctuidae). Journal of Economic Entomology 90, 444-448.
15. Catteruccia, F., Benton, J.P. and Crisanti, A. (2005) An Anopheles transgenic sexing strain for vector control. Nature Biotechnology 23, 1414-1417.
16. Chen, P., Ho, S.I., Shi, Z. and Abrams, J.M. (2004) Bifunctional killing activity encoded by conserved reaper proteins. Cell Death and Differentiation 11, 704-713.
17. Coates, C.J., Jasinskiene, N., Miyashiro, L. and James, A.A. (1998) Mariner transposition and transformation of the yellow fever mosquito, Aedes aegypti. Proceedings of the National Academy of Sciences USA 95, 3748-3751.
18. Concha, C. and Scott, M.J. (2009) Sexual development in Lucilia cuprina (Diptera, Calliphoridae) is controlled by the transformer gene. Genetics 182, 785-798.
19. Concha, C., Belikoff, E.J., Carey, B.L., Li, F., Schiemann, A.H. and Scott, M.J. (2011) Efficient germ-line transformation of the economically important pest species Lucilia cuprina and Lucilia sericata (Diptera, Calliphoridae). Insect Biochemistry and Molecular Biology 41, 70-75.
20. Crystal, M.M. (1979) Sterilization of screwworm flies (Diptera: Calliphoridae) with gamma rays: restudy after two decades. Journal of Medical Entomology 15, 103-108.
21. Dafa'alla, T.H., Condon, G.C., Condon, K.C., Phillips, C.E., Morrison, N.I., Jin, L., Epton, M.J., Fu, G. and Alphey, L. (2006) Transposon-free insertions for insect genetic engineering. Nature Biotechnology 24, 820-821.
22. Enkerlin, W.R. (2005) Impact of fruit fly programmes using the sterile insect technique. In: Dyck, V.A., Hendrichs, J. and Robinson, A.S. (eds) Sterile Insect Technique. Principles and Practice in Area-Wide Integrated Pest Management. Springer, Dordrecht, the Netherlands, pp. 651-676.
23. FAO/IAEA (2006) Status and risk assessment of the use of transgenic arthropods in plant protection. FAO/IAEA technical meeting, 8-12 April 2002.
24. Feldman, U., Dyck, V.A., Mattioli, R.C. and Jannin, J. (2005) Potential impact of tsetse fly control involving the sterile insect technique. In; Dyck, V.A., Hendrichs, J. and Robinson, A.S. (eds) Sterile Insect Technique. Principles and Practice in Area-Wide Integrated Pest Management. Springer, Dordrecht, the Netherlands, pp. 701-723.
25. Foster, G.G., Weller, G.L., James, W.J., Paschalidis, K.M. and McKenzie, L.J. (1993) Advances in sheep blowfly genetic control in Australia. In: Management of Insect Pests: Nuclear and Related Molecular and Genetic Techniques. International Atomic Energy Agency, Vienna, pp. 299-312.
26. Franz, G. (2005) Genetic sexing strains in Mediterranean fruit fly, an example for other species amenable to large scale rearing for the sterile insect technique. In: Dyck, V.A., Hendrichs, J. and Robinson, A.S. (eds) Sterile Insect Technique. Principles and Practice in Area-Wide Integrated Pest Management. Springer, Dordrecht, the Netherlands, pp. 427-451.
27. Fu, G., Condon, K.C., Epton, M.J., Gong, P., Jin, L., Condon, G.C., Morrison, N.I., Dafa'alla, T.H. and Alphey, L. (2007) Female-specific insect lethality engineered using alternative splicing. Nature Biotechnology 25, 353-357.
28. Gong, P., Epton, M.J., Fu, G., Scaife, S., Hiscox, A., Condon, K.C., Condon, G.C., Morrison, N.I., Kelly, D.W., Dafa'alla, T., Coleman, P.G. and Alphey, L. (2005) A dominant lethal genetic system for autocidal control of the Mediterranean fruitfly. Nature Biotechnology 23, 453-456.
29. Gossen, M. and Bujard, H. (1992) Tight control of gene expression in mammalian cells by tetracycline-responsive promoters. Proceedings of the National Academy of Sciences USA 89, 5547-5551.
30. Grether, M.E., Abrams, J.M., Agapite, J., White, K. and Steller, H. (1995) The head involution defective gene of Drosophila melanogaster functions in programmed cell death. Genes and Development 9, 1694-1708.
31. Handler, A.M. and Harrell, R.A., 2nd (2001) Transformation of the Caribbean fruit fly, Anastrepha suspensa , with a piggyBac vector marked with polyubiquitin-regulated GFP. Insect Biochemistry and Molecular Biology 31, 199-205.
32. Handler, A.M., McCombs, S.D., Fraser, M.J. and Saul, S.H. (1998) The lepidopteran transposon vector, piggyBac , mediates germ-line transformation in the Mediterranean fruit fly. Proceedings of the National Academy of Sciences USA 95, 7520-7525.
33. Handler, A.M., Zimowska, G.J. and Horn, C. (2004) Post-integration stabilization of a transposon vector by terminal sequence deletion in Drosophila melanogaster . Nature Biotechnology 22, 1150-1154.
34. Handler, A.M., Allen, M.L. and Skoda, S.R. (2009) Development and utilization of transgenic New World screwworm, Cochliomyia hominivorax . Medical and Veterinary Entomology 23 (Suppl. 1), 98-105.
35. Heath, A.C. and Bishop, D.M. (2006) Flystrike in New Zealand: An overview based on a 16-year study, following the introduction and dispersal of the Australian sheep blowfly, Lucilia cuprina Wiedemann (Diptera: Calliphoridae). Veterinary Parasitology 137, 333-344.
36. Heinrich, J.C. and Scott, M.J. (2000) A repressible female-specific lethal genetic system for making transgenic insect strains suitable for a sterilerelease program. Proceedings of the National Academy of Sciences USA 97, 8229-8232.
37. Heinrich, J.C., Li, X., Henry, R.A., Haack, N., Stringfellow, L., Heath, A.C. and Scott, M.J. (2002) Germ-line transformation of the Australian sheep blowfly Lucilia cuprina . Insect Molecular Biology 11, 1-10.
38. Heinrichs, V., Ryner, L.C. and Baker, B.S. (1998) Regulation of sex-specific selection of fruitless 5' splice sites by transformer and transformer-2. Molecular and Cell Biology 18, 450-458.
39. Henneberry, T.J. and Naranjo, S.E. (1998) Integrated management approaches for pink bollworm in the southwestern United States. International Pest Management Review 3, 31-52.
40. Horn, C. and Wimmer, E.A. (2003) A transgenebased, embryo-specific lethality system for insect pest management. Nature Biotechnology 21, 64-70.
41. Hoshijima, K., Inoue, K., Higuchi, I., Sakamoto, H. and Shimura, Y. (1991) Control of doublesex alternative splicing by transformer and transformer-2 in Drosophila . Science 252, 833-836.
42. Jin, L., Walker, A.S., Fu, G., Harvey-Samuel, T., Dafa'alla, T.H., Miles, A., Marubbi, T., Granville, D., Humphrey-Jones, N., O'Connell, S., Morrison, N.I. and Alphey, L. (2013) Engineered female-specific lethality for control of pest Lepidoptera. ACS Synthetic Biology 2, 160-166.
43. Kimura, K., Harada, C. and Aoki, H. (1971) Studies on the W translocation of yellow blood gene in the silkworm (Bombyx mori ). Japanese Journal of Breeding 21, 199-203.
44. Klassen, W. and Curtis, C.F. (2005) History of the sterile insect technique. In: Dyck, V.A., Hendrichs, J. and Robinson, A.S. (eds) Sterile Insect Technique. Principles and Practice in Area-Wide Integrated Pest Management. Springer, Dordrecht, the Netherlands, pp. 3-36.
45. Knipling, E.F. (1960) The eradication of the screwworm fly. Scientific American 203, 54-61.
46. Koval, T.M. (1996) Moths: myths and mysteries of stress resistance. BioEssays 18, 149-156.
47. Krafsur, E.S., Whitten, C.J. and Novy, J.E. (1987) Screwworm eradication in North and Central America. Parasitology Today 3, 131-137.
48. LaChance, L.E. (1967) The induction of dominant lethal mutations in insects by ionizing radiation and chemicals- as related to the sterile-male technique of insect control. In: Wright, J.W. and Pal, R. (eds) Genetics of Insect Vectors of Disease. Elsevier, Amsterdam, the Netherlands, pp. 617-650.
49. Li, F., Vensko, S.P., 2nd, Belikoff, E.J. and Scott, M.J. (2013) Conservation and Sex-Specific Splicing of the transformer Gene in the Calliphorids Cochliomyia hominivorax , Cochliomyia macellaria and Lucilia sericata. PLoS One 8, e56303.
50. Li, F., Wantuch, H.A., Linger, R.J., Belikoff, E.J. and Scott, M.J. (2014) Transgenic sexing system for genetic control of the Australian sheep blow fly Lucilia cuprina . Insect Biochemistry and Molecular Biology 51, 80-88.
51. Loukeris, T.G., Livadaras, I., Arca, B., Zabalou, S. and Savakis, C. (1995) Gene transfer into the medfly, Ceratitis capitata , with a Drosophila hydei transposable element. Science 270, 2002-2005.
52. Marec, F. (1991) Genetic control of pest Lepidoptera: construction of a balanced lethal strain in Ephestia kuehniella . Entomologia Experimentalis et Applicata 61, 271-283.
53. Marec, F., Kollárová, I. and Pavelka, J. (1999) Radiation-Induced Inherited Sterility Combined with a Genetic Sexing System in Ephestia kuehniella (Lepidoptera: Pyralidae). Annals of the Entomological Society of America 92, 250-259.
54. Marec, F., Neven, L.G., Robinson, A.S., Vreysen, M., Goldsmith, M.R., Nagaraju, J. and Franz, G. (2005) Development of genetic sexing strains in Lepidoptera: from traditional to transgenic approaches. Journal of Economic Entomology 98, 248-259.
55. Mazumdar, A. and Mazumdar, M. (2002) How one becomes many: blastoderm cellularization in Drosophila melanogaster . BioEssays 24, 1012-1022.
56. McDonagh, L.M. and Stevens, J.R. (2011) The molecular systematics of blowflies and screwworm flies (Diptera: Calliphoridae) using 28S rRNA, COX1 and EF-1alpha: insights into the evolution of dipteran parasitism. Parasitology 138, 1760-1777.
57. McInnis, D.O., Tam, S., Grace, C. and Miyashita, D. (1994) Population suppression and sterility induced by variable sex ratio, sterile insect releases of Ceratitis capitata (Diptera: Tephritidae) in Hawaii. Annals of the Entomological Society of America 87, 231-240.
58. Morrison, N.I., Franz, G., Koukidou, M., Miller, T.A., Saccone, G., Alphey, L.S., Beech, C.J., Nagaraju, J., Simmons, G.S. and Polito, L.C. (2011) Genetic improvements to the Sterile Insect Technique for agricultural pests. Asian-Pacific Journal of Molecular Biology and Biotechnology 18, 275-295.
59. Morrison, N.I., Simmons, G.S., Fu, G., O'Connell, S., Walker, A.S., Dafa'alla, T., Walters, M., Claus, J., Tang, G., Jin, L., Marubbi, T., Epton, M.J., Harris, C.L., Staten, R.T., Miller, E., Miller, T.A. and Alphey, L. (2012) Engineered repressible lethality for controlling the pink bollworm, a lepidopteran pest of cotton. PLoS One 7, e50922.
60. Murakami, A. and Imai, H.T. (1974) Cytological evidence for holocentric chromosomes of the silkworms, Bombyx mori and B. mandarina, (Bombycidae, Lepidoptera). Chromosoma 47, 167-178.
61. Nagaraju, J. (2002) Application of genetic principles for improving silk production. Current Science 83, 409-414.
62. Ogaugwu, C.E., Schetelig, M.F. and Wimmer, E.A. (2013) Transgenic sexing system for Ceratitis capitata (Diptera: Tephritidae) based on femalespecific embryonic lethality. Insect Biochemistry and Molecular Biology 43, 1-8.
63. Pane, A., Salvemini, M., Delli Bovi, P., Polito, C. and Saccone, G. (2002) The transformer gene in Ceratitis capitata provides a genetic basis for selecting and remembering the sexual fate. Development 129, 3715-3725.
64. Parker, A.G. (2005) Mass-rearing for sterile insect release. In: Dyck, V.A., Hendrichs, J. and Robinson, A.S. (eds) Sterile Insect Technique. Principles and Practice in Area-Wide Integrated Pest Management. Springer, Dordrecht, the Netherlands, pp. 209-232.
65. Peloquin, J.J., Thibault, S.T., Staten, R. and Miller, T.A. (2000) Germ-line transformation of pink bollworm (Lepidoptera: Gelechiidae) mediated by the piggyBac transposable element. Insect Molecular Biology 9, 323-333.
66. Rendon, P., McInnis, D., Lance, D. and Stewart, J. (2004) Medfly (Diptera: Tephritidae) genetic sexing: large-scale field comparison of malesonly and bisexual sterile fly releases in Guatemala. Journal of Economic Entomology 97, 1547-1553.
67. Schetelig, M.F. and Handler, A.M. (2012) A transgenic embryonic sexing system for Anastrepha suspensa (Diptera: Tephritidae). Insect Biochemistry and Molecular Biology 42, 790-795.
68. Schetelig, M.F., Caceres, C., Zacharopoulou, A., Franz, G. and Wimmer, E.A. (2009) Conditional embryonic lethality to improve the sterile insect technique in Ceratitis capitata (Diptera: Tephritidae). BMC Biology 7, 4.
69. Schliekelman, P. and Gould, F. (2000) Pest control by the release of insects carrying a femalekilling allele on multiple loci. Journal of Economic Entomology 93, 1566-1579.
70. Scolari, F., Schetelig, M.F., Bertin, S., Malacrida, A.R., Gasperi, G. and Wimmer, E.A. (2008) Fluorescent sperm marking to improve the fight against the pest insect Ceratitis capitata (Wiedemann; Diptera: Tephritidae). Nature Biotechnology 25, 76-84.
71. Scott, M.J., Atapattu, A., Schiemann, A.H., Concha, C., Henry, R., Carey, B.L., Belikoff, E.J., Heinrich, J.C. and Sarkar, A. (2011) Organisation and expression of a cluster of yolk protein genes in the Australian sheep blowfly, Lucilia cuprina . Genetica 139, 63-70.
72. Simmons, G.S., Alphey, L.S., Vasquez, T., Morrison, N.I., Epton, M.J., Miller, E., Miller, T.A. and Staten, R.T. (2007) Potential use of a conditional lethal transgenic pink bollworm Pectinophora gossypiella in area-wide eradication or suppression programmes. In: Vreysen, M.J.B., Robinson, A.S. and Hendrichs, J. (eds) Area-Wide Control of Insect Pests. Springer, Dordrecht, the Netherlands, pp. 119-123.
73. Simmons, G.S., Suckling, D.M., Carpenter, J.E., Addison, M.F., Dyck, V.A. and Vreysen, M.J.B. (2010) Improved quality management to enhance the efficacy of the sterile insect technique for lepidopteran pests. Journal of Applied Entomology 134, 261-273.
74. Simmons, G.S., McKemey, A.R., Morrison, N.I., O'Connell, S., Tabashnik, B.E., Claus, J., Fu, G., Tang, G., Sledge, M., Walker, A.S., Phillips, C.E., Miller, E.D., Rose, R.I., Staten, R.T., Donnelly, C.A. and Alphey, L. (2011) Field performance of a genetically engineered strain of pink bollworm. PLoS One 6, e24110.
75. Spradling, A.C. and Rubin, G.M. (1982) Transposition of cloned P elements into Drosophila germ line chromosomes. Science 218, 341-347.
76. Strunnikov, V. (1975) Sex control in silkworms. Nature 255, 111-113.
77. Suckling, D., Barrington, A., Chhagan, A., Stephens, A., Burnip, G., Charles, J. and Wee, S. (2007) Eradication of the Australian painted apple moth Teia anartoides in New Zealand: Trapping, inherited sterility, and male competitiveness. In: Vreysen, M., Robinson, A. and Hendrichs, J. (eds) Area-Wide Control of Insect Pests. Springer, Dordrecht, the Netherlands, pp. 603-615.
78. Suzuki, M.G., Ohbayashi, F., Mita, K. and Shimada, T. (2001) The mechanism of sex-specific splicing at the doublesex gene is different between Drosophila melanogaster and Bombyx mori. Insect Biochemistry and Molecular Biology 31, 1201-1211.
79. Sze, S.H., Dunham, J.P., Carey, B., Chang, P.L., Li, F., Edman, R.M., Fjeldsted, C., Scott, M.J., Nuzhdin, S.V. and Tarone, A.M. (2012) A denovo transcriptome assembly of Lucilia sericata (Diptera: Calliphoridae) with predicted alternative splices, singlenucleotide polymorphisms and transcript expression estimates. Insect Molecular Biology 21, 205-221.
80. Tabashnik, B.E., Sisterson, M.S., Ellsworth, P.C., Dennehy, T.J., Antilla, L., Liesner, L., Whitlow, M., Staten, R.T., Fabrick, J.A., Unnithan, G.C., Yelich, A.J., Ellers-Kirk, C., Harpold, V.S., Li, X. and Carriere, Y. (2010) Suppressing resistance to Bt cotton with sterile insect releases. Nature Biotechnology 28, 1304-1307.
81. Tan, A., Fu, G., Jin, L., Guo, Q., Li, Z., Niu, B., Meng, Z., Morrison, N.I., Alphey, L. and Huang, Y. (2013) A transgene-based, female-specific lethality system for genetic sexing of the silkworm, Bombyx mori . Proceedings of the National Academy of Sciences USA, doi: 10.1073/pnas.1221700110.
82. Tazima, Y., Ohta, N. and Harada, C. (1951) On the sex determinating method by colouring genes of silkworm eggs. I. Induction of translocation between the W and the tenth chromosomes. Japanese Journal of Breeding 1, 47-50.
83. Thomas, D.D., Donnelly, C.A., Wood, R.J. and Alphey, L.S. (2000) Insect population control using a dominant, repressible, lethal genetic system. Science 287, 2474-2476.
84. Vargas-Teran, M., Hofmann, H.C. and Tweddle, N.E. (2005) Impact of screwworm eradication programmes using the sterile insect technique. In: Dyck, V.A., Hendrichs, J. and Robinson, A.S. (eds) Sterile Insect Technique. Principles and Practice in Area-Wide Integrated Pest Management. Springer, Dordrecht, the Netherlands, pp. 629-650.
85. Verhulst, E.C., van de Zande, L. and Beukeboom, L.W. (2010) Insect sex determination: it all evolves around transformer. Current Opinion in Genetics and Development 20, 376-383.
86. Vreysen, M.J.B. (2005) Monitoring sterile and wild insects in area-wide integrated pest management programmes. In: Dyck, V.A., Hendrichs, J. and Robinson, A.S. (eds) Sterile Insect Technique. Principles and Practice in Area-Wide Integrated Pest Management. Springer, Dordrecht, the Netherlands, pp. 325-361.
87. Walters, M., Morrison, N.I., Claus, J., Tang, G., Phillips, C.E., Young, R., Zink, R.T. and Alphey, L. (2012) Field longevity of a fluorescent protein marker in an engineered strain of the pink bollworm, Pectinophora gossypiella (Saunders). PLoS One 7, e38547.
88. Watts, J.E., Murray, M.D. and Graham, N.P. (1979) The blowfly strike problem of sheep in New South Wales. Australian Veterinary Journal 55, 325-334.
89. Whitten, M.J. and Foster, G.G. (1975) Genetical methods of pest control. Annual Review of Entomology 20, 461-476.
90. Wolf, K.W. (1994) The unique structure of lepidopteran spindles. International Review of Cytology 152, 1-48.
91. Wyss, J.H. (2000) Screwworm eradication in the Americas. Annals of the New York Academy of Sciences 916, 186-193.