RNAi-based insecticidal crops: Potential effects on nontarget species

BioScience

Volumn 63, Issue 8, 2013, Pages 657-665

  Lundgren, Jonathan G ^a   Duan, Jian J ^a  

^a U S DEPARTMENT OF AGRICULTURE   (United States)

Author keywords

exposure; GM crops; insecticide; nontarget testing; RNAi

Indexed keywords

EID: 84883200081     PISSN: 00063568     EISSN: None     Source Type: Journal    
DOI: 10.1525/bio.2013.63.8.8     Document Type: Review

References (61)

1. Agrawal N, Dasaradhi PVN, Mohmmed A, Malhotra P, Bhatnagar RK, Mukherjee SK. 2003. RNA interference: Biology, mechanism, and applications. Microbiology and Molecular Biology Reviews 67: 657-685.
2. Alemán LM, Doench J, Sharp PA. 2007. Comparison of siRNA-induced off-target RNA and protein effects. RNA 13: 385-395.
3. Auer C, Frederick R. 2009. Crop improvement using small RNAs: Applications and predictive ecological risk assessments. Trends in Biotechnology 27: 644-651.
4. Baum JA, et al. 2007. Control of coleopteran insect pests through RNA interference. Nature Biotechnology 25: 1322-1326.
5. Bhatti MA, Duan JJ, Head GP, Jiang C, McKee MJ, Nickson TE, Pilcher CL, Pilcher CD. 2005. Field evaluation of the impact of corn rootworm (Coleoptera: Chrysomelidae)-protected Bt corn on foliagedwelling arthropods. Environmental Entomology 34: 1336-1345.
6. Birmingham A, et al. 2006. 3UTR seed matches, but not overall identity, are associated with RNAi off-targets. Nature Methods 3: 199-204.
7. Bøhn T, Traavik T, Primicerio R. 2010. Demographic responses of Daphnia magna fed transgenic Bt-maize. Ecotoxicology 19: 419-430.
8. Davidson BL, McCray PB. 2011. Current prospects for RNA interference-based therapies. Nature Reviews Genetics 12: 329-340.
9. Dillin A. 2003. The specifics of small interfering RNA specificity. Proceedings of the National Academy of Sciences 100: 6289-6291.
10. Dively GP. 2005. Impact of transgenic VIP3a × Cry1Ab lepidopteran-resistant field corn on the nontarget arthropod community. Environmental Entomology 34: 1267-1291.
11. Duan JJ, Marvier M, Huesing J, Dively G[P], Huang ZY. 2008. A metaanalysis of effects of Bt crops on honey bees (Hymenoptera: Apidae). PLOS ONE 3 (art. e1415).
12. Duan JJ, Lundgren JG, Naranjo S[E], Marvier M. 2010. Extrapolating non-target risk of Bt crops from laboratory to field. Biology Letters 6: 74-77.
13. Elbashir SM, Harborth J, Weber K, Tuschl T. 2002. Analysis of gene function in somatic mammalian cells using small interfering RNAs. Methods 26: 199-213.
14. Federov Y, Anderson EM, Birmingham A, Reynolds A, Karpilow J, Robinson K, Leake D, Marshall WS, Khvorova A. 2006. Off-target effects by siRNA can induce toxic phenotype. RNA 12: 1188-1196.
15. Harrap KA. 1982. Assessment of the human and ecological hazards of microbial insecticides. Parasitology 84: 269.
16. Harwood JD, Wallin WG, Obrycki JJ. 2005. Uptake of Bt-endotoxins by non-target herbivores and higher order arthropod predators: Molecular evidence from a transgenic corn agroecosystem. Molecular Ecology 14: 2815-2823.
17. Haussler D, et al. 2009. Genome 10K: A proposal to obtain whole-genome sequence for 10,000 vertebrate species. Journal of Heredity 100: 659-674.
18. Heinemann JA, Agapito-Tenfen SZ, Carman JA. 2013. A comparative evaluation of the regulation of GM crops or products containing dsRNA and suggested improvements to risk assessments. Environment International 55: 43-55.
19. Huvenne H, Smagghe G. 2010. Mechanisms of dsRNA uptake in insects and potential of RNAi for pest control: A review. Journal of Insect Physiology 56: 227-235.
20. Jackson AL, Linsley PS. 2010. Recognizing and avoiding siRNA off-target effects for target identification and therapeutic application. Nature Reviews Drug Discovery 9: 57-67.
21. Jackson AL, Burchard J, Schelter J, Chau BN, Cleary M, Lim L, Linsley PS. 2006. Widespread siRNA "off-target" transcript silencing mediated by seed region sequence complementarity. RNA 12: 1179-1187.
22. Judge AD, Sood V, Shaw JR, Fang D, McClintock K, MacLachlan I. 2005. Sequence-dependent stimulation of the mammalian innate immune response by synthetic siRNA. Nature Biotechnology 23: 457-462.
23. Jurat-Fuentes JL, Jackson TA. 2012. Bacterial entomopathogens. Pages 265-350 in Vega FE, Kaya HK, eds. Insect Pathology, 2nd ed. Academic Press.
24. Kahn AA, Betel D, Miller ML, Sander C, Leslie CS, Marks DS. 2009. Transfection of small RNAs globally perturbs gene regulation by endogenous microRNAs. Nature Biotechnology 27: 549-555.
25. Kulkarni MM, Booker M, Silver SJ, Friedman A, Hong P, Perrimon N, Mathey-Prevot B. 2006. Evidence of off-target effects associated with long dsRNAs in Drosophila melanogaster cell-based assays. Nature Methods 3: 833-838.
26. Levy-Booth DJ, Campbell RG, Gulden RH, Hart MM, Powell JR, Klironomos JN, Pauls KP, Swanton CJ, Trevors JT, Dunfield KE. 2007. Cycling of extracellular DNA in the soil environment. Soil Biology and Biochemistry 39: 2977-2991.
27. Li Y, Romeis J. 2010. Bt maize expressing Cry3Bb1 does not harm the spider mite, Tetranychus urticae, or its ladybird beetle predator, Stethorus punctillum. Biological Control 53: 337-344.
28. Lundgren JG, Fergen JK. 2010. The effects of a winter cover crop on Diabrotica virgifera (Coleoptera: Chrysomelidae) populations and beneficial arthropod communities in no-till maize. Environmental Entomology 39: 1816-1828.
29. Lundgren JG, Jurat-Fuentes JL. 2012. Physiology and ecology of host defense against microbial invaders. Pages 461-480 in Vega FE, Kaya HK, eds. Insect Pathology, 2nd ed. Academic Press.
30. Lundgren JG, Gassmann AJ, Bernal J, Duan J[J], Ruberson J. 2009. Ecological compatibility of GM crops and biological control. Crop Protection 28: 1017-1030.
31. Mansoor S, Amin I, Hussain M, Zafar Y, Briddon RW. 2006. Engineering novel traits in plants through RNA interference. Trends in Plant Science 11: 559-565.
32. Mao Y-B, Tao X-Y, Xue X-Y, Wang L-J, Chen X-Y. 2011. Cotton plants expressing CYP6AE14 double-stranded RNA show enhanced resistance to bollworms. Transgenic Research 20: 665-673.
33. Marvier M, McCreedy C, Regetz J, Kareiva P. 2007. A meta-analysis of effects of Bt cotton and maize on nontarget invertebrates. Science 316: 1475-1477.
34. McLean MA, ed. 2011. Problem Formulation for the Environmental Risk Assessment of RNAi Plants, Conference Proceedings (June 1-3, 2011). Center for Environmental Risk Assessment, International Life Sciences Institute Research Foundation.
35. Metzker ML. 2010. Sequencing technologies: The next generation. Nature Reviews Genetics 11: 31-46.
36. Naranjo SE. 2009. Impacts of Bt crops on non-target organisms and insecticide use patterns. CAB Reviews: Perspectives in Agriculture, Veterinary Science, Nutrition, and Natural Resources 4: 1-23.
37. Nielsen KM, Johnsen PJ, Bensasson D, Daffonchio D. 2007. Release and persistence of extracellular DNA in the environment. Environmental Biosafety Research 6: 37-53.
38. O'Callaghan M, Glare TR, Burgess EPJ, Malone LA. 2005. Effects of plants genetically modified for insect resistance on nontarget organisms. Annual Review of Entomology 50: 271-292.
39. O'Neill MJ, Bourre L, Melgar S, O'Driscoll CM. 2011. Intestinal delivery of non-viral gene therapeutics: Physiological barriers and preclinical models. Drug Discovery Today 16: 203-218.
40. Peterson JA, Lundgren JG, Harwood JD. 2011. Interactions of transgenic Bacillus thuringiensis insecticidal crops with spiders (Araneae). Journal of Arachnology 39: 1-21.
41. Pietramellara G, Ascher J, Borgogni F, Ceccherini MT, Guerri G, Nannipieri P. 2009. Extracellular DNA in soil and sediment: Fate and ecological relevance. Biology and Fertility of Soils 45: 219-235.
42. Qiu S, Adema CM, Lane T. 2005. A computational study of off-target effects of RNA interference. Nucleic Acids Research 33: 1834-1847.
43. Robbins M, Judge A, MacLachlan I. 2009. siRNA and innate immunity. Oligonucleotides 19: 89-102.
44. 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: 1386.
45. Romeis J, Meissle M, Bigler F. 2006. Transgenic crops expressing Bacillus thuringiensis toxins and biological control. Nature Biotechnology 24: 63-71.
46. Saxena S, Jónsson ZO, Dutta A. 2003. Small RNAs with imperfect match to endogenous mRNA repress translation. Journal of Biological Chemistry 278: 44312-44319.
47. Siomi H, Siomi MC. 2009. On the road to reading the RNA-interference code. Nature 457: 396-404.
48. Smith EN, Kruglyak L. 2008. Gene-environment interaction in yeast gene expression. PLOS Biology 6 (art. e83).
49. [USEPA] US Environmental Protection Agency. 1994. Proposed policy: Plant-pesticides subject to the federal insecticide fungicide, and rodenticide act and the Federal Food, Drug, and Cosmetic Act. Federal Register 59: 60496-60518.
50. -. 1998. Guidelines for Ecological Risk Assessment. USEPA.
51. -. 2002. Guidance on Cumulative Risk Assessment of Pesticide Chemicals That Have a Common Mechanism of Toxicity. Office of Pesticide Programs, USEPA. 14 May 2013 www.epa.gov/oppfead1/trac/science/cumulative-guidance.pdf
52. -. 2003. Biopesticides Registration Action Document: Event MON 863 Bacillus thuringiensis Cry3Bb1 corn. Office of Pesticide Programs, USEPA.
53. Van Frankenhuyzen K. 2009. Insecticidal activity of B. thuringiensis crystal proteins. Journal of Invertebrate Pathology 101: 1-16.
54. Wang J, Lu Z, Wientjes MG, Au JL-S. 2010. Delivery of siRNA therapeutics: Barriers and carriers. AAPS Journal 12: 492-503.
55. Wang Y, Morimoto S, Ogawa N, Oomori T, Fujii T. 2009. An improved method to extract RNA from soil with efficient removal of humic acids. Journal of Applied Microbiology 107: 1168-1177.
56. Weber DC, Lundgren JG. 2009. Assessing the trophic ecology of the Coccinellidae: Their roles as predators and prey. Biological Control 51: 199-214.
57. Whyard S, Singh AD, Wong S. 2009. Ingested double-stranded RNAs can act as species-specific insecticides. Insect Biochemistry and Molecular Biology 39: 824-832.
58. Wolfenbarger LL, Naranjo SE, Lundgren JG, Bitzer RJ, Watrud LS. 2008. Bt crop effects on functional guilds of non-target arthropods: A metaanalysis. PLOS ONE 3 (art. e2118).
59. Zha W, Peng X, Chen R, Du B, Zhu L, He G. 2011. Knockdown of midgut genes by dsRNA-transgenic plant-mediated RNA interference in the hemipteran insect Nilaparvata lugens. PLOS ONE 6 (art. e20504).
60. Zhang L, et al. 2012. Exogenous plant MIR168a specifically targets mammalian LDLRAP1: Evidence of cross-kingdom regulation by microRNA. Cell Research 22: 107-126.
61. Zwahlen C, Andow DA. 2005. Field evidence for the exposure of ground beetles to Cry1Ab from transgenic corn. Environmental Biosafety Research 4: 113-117.