1932

Abstract

Genetic engineering is a molecular biology technique that enables a gene or genes to be inserted into a plant's genome. The first genetically engineered plants were grown commercially in 1996, and the most common genetically engineered traits are herbicide and insect resistance. Questions and concerns have been raised about the effects of these traits on the environment and human health, many of which are addressed in a pair of 2008 and 2009 articles. As new science is published and new techniques like genome editing emerge, reanalysis of some of these issues, and a look at emerging issues, is warranted. Herein, an analysis of relevant scientific literature is used to present a scientific perspective on selected topics related to genetic engineering and genome editing.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-081519-035916
2020-04-29
2024-06-18
Loading full text...

Full text loading...

/deliver/fulltext/arplant/71/1/annurev-arplant-081519-035916.html?itemId=/content/journals/10.1146/annurev-arplant-081519-035916&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Adenle AA, Morris EJ, Parayil G 2013. Status of development, regulation and adoption of GM agriculture in Africa: Views and positions of stakeholder groups. Food Policy 43:159–66
    [Google Scholar]
  2. 2. 
    Aguilar J, Gramig GG, Hendrickson JR, Archer DW, Forcella F, Liebig MA 2015. Crop species diversity changes in the United States: 1978–2012. PLOS ONE 10:81–14
    [Google Scholar]
  3. 3. 
    Álvarez-Alfageme F, Bigler F, Romeis J 2011. Laboratory toxicity studies demonstrate no adverse effects of Cry1Ab and Cry3Bb1 to larvae of Adalia bipunctata (Coleoptera: Coccinellidae): the importance of study design. Transgenic Res 20:3467–79
    [Google Scholar]
  4. 4. 
    Aman R, Ali Z, Butt H, Mahas A, Aljedaani F et al. 2018. RNA virus interference via CRISPR/Cas13a system in plants. Genome Biol 19:11–9
    [Google Scholar]
  5. 5. 
    Anderson K, Jackson LA. 2005. Some implications of GM food technology policies for Sub-Saharan Africa. J. Afr. Econ. 14:3385–410
    [Google Scholar]
  6. 6. 
    Andrade PP, Da Silva Ferreira MA, Muniz MS, De Casto Lira-Neto A 2018. GM insect pests under the Brazilian regulatory framework: development and perspectives. BMC Proc 12:1613–18
    [Google Scholar]
  7. 7. 
    Aparicio VC, De Gerónimo E, Marino D, Primost J, Carriquiriborde P, Costa JL 2013. Environmental fate of glyphosate and aminomethylphosphonic acid in surface waters and soil of agricultural basins. Chemosphere 93:91866–73
    [Google Scholar]
  8. 8. 
    Babujia LC, Silva AP, Nakatani AS, Cantão ME, Vasconcelos ATR et al. 2016. Impact of long-term cropping of glyphosate-resistant transgenic soybean [Glycine max (L.) Merr.] on soil microbiome. Transgenic Res 25:4425–40
    [Google Scholar]
  9. 9. 
    Bai YY, Yan RH, Ye GY, Huang F, Wangila DS et al. 2012. Field response of aboveground non-target arthropod community to transgenic Bt-Cry1Ab rice plant residues in postharvest seasons. Transgenic Res 21:51023–32
    [Google Scholar]
  10. 10. 
    Balbuena MS, Tison L, Hahn M-L, Greggers U, Menzel R, Farina WM 2015. Effects of sublethal doses of glyphosate on honeybee navigation. J. Exp. Biol. 218:172799–805
    [Google Scholar]
  11. 11. 
    Barrangou R, Fremaux C, Deveau H, Richards M, Boyaval P et al. 2007. CRISPR provides acquired resistance against viruses in prokaryotes. Science 315:58191709–12
    [Google Scholar]
  12. 12. 
    Barrows G, Sexton S, Zilberman D 2014. Agricultural biotechnology: the promise and prospects of genetically modified crops. J. Econ. Perspect. 28:199–120
    [Google Scholar]
  13. 13. 
    Battaglin WA, Meyer MT, Kuivila KM, Dietze JE 2014. Glyphosate and its degradation product AMPA occur frequently and widely in U.S. soils, surface water, groundwater, and precipitation. J. Am. Water Resour. Assoc. 50:2275–90
    [Google Scholar]
  14. 14. 
    Beckie HJ, Harker KN. 2017. Our top 10 herbicide-resistant weed management practices. Pest Manag. Sci. 73:61045–52
    [Google Scholar]
  15. 15. 
    Beckie HJ, Sikkema PH, Soltani N, Blackshaw RE, Johnson EN 2014. Environmental impact of glyphosate-resistant weeds in Canada. Weed Sci 62:2385–92
    [Google Scholar]
  16. 16. 
    Beckie HJ, Tardif FJ. 2012. Herbicide cross resistance in weeds. Crop Prot 35:15–28
    [Google Scholar]
  17. 17. 
    Benbrook CM. 2016. Trends in glyphosate herbicide use in the United States and globally. Environ. Sci. Eur. 28:11–15
    [Google Scholar]
  18. 18. 
    Boch J, Scholze H, Schornack S, Landgraf A, Hahn S et al. 2009. Breaking the code of DNA binding specificity of TAL-type III effectors. Science 326:59591509–12
    [Google Scholar]
  19. 19. 
    Bolotin A, Quinquis B, Sorokin A, Ehrlich SD 2005. Clustered regularly interspaced short palindrome repeats (CRISPRs) have spacers of extrachromosomal origin. Microbiology 151:82551–61
    [Google Scholar]
  20. 20. 
    Bonas U, Stall RE, Staskawicz B 1989. Genetic and structural characterization of the avirulence gene avrBs3 from Xanthomonas campestris pv. vesicatoria. Mol. Gen. Genet. 218:1127–36
    [Google Scholar]
  21. 21. 
    Bonny S. 2016. Genetically modified herbicide-tolerant crops, weeds, and herbicides: overview and impact. Environ. Manag. 57:131–48
    [Google Scholar]
  22. 22. 
    Bouët A, Gruère GP. 2011. Refining opportunity cost estimates of not adopting GM cotton: an application in seven Sub-Saharan African countries. Appl. Econ. Perspect. Policy 33:2260–79
    [Google Scholar]
  23. 23. 
    Brouns SJJ, Jore MM, Lundgren M, Westra ER, Slijkhuis RJH et al. 2008. Small CRISPR RNAs guide antiviral defense in prokaryotes. Science 321:5891960–64
    [Google Scholar]
  24. 24. 
    Bruckner A, Schmerbauch A, Ruess L, Heigl F, Zaller J 2019. Foliar Roundup application has minor effects on the compositional and functional diversity of soil microorganisms in a short-term greenhouse experiment. Ecotoxicol. Environ. Saf. 174:15506–13
    [Google Scholar]
  25. 25. 
    Can. Food Insp. Agency 2017. Determination of novelty. Directive 94–08 assessment criteria for determining environmental safety of plants with novel traits (revised Dec. 19) http://www.inspection.gc.ca/plants/plants-with-novel-traits/applicants/directive-94-08/eng/1512588596097/1512588596818
    [Google Scholar]
  26. 26. 
    Cao C. 2018. Science, biosafety, and regulations. GMO China: How Global Debates Transformed China's Agricultural Biotechnology Polices76–104 New York: Columbia Univ. Press
    [Google Scholar]
  27. 27. 
    Carrière Y, Crickmore N, Tabashnik BE 2015. Optimizing pyramided transgenic Bt crops for sustainable pest management. Nat. Biotechnol. 33:2161–68
    [Google Scholar]
  28. 28. 
    Catarino R, Ceddia G, Areal FJ, Park J 2015. The impact of secondary pests on Bacillus thuringiensis (Bt) crops. Plant Biotechnol. J. 13:5601–12
    [Google Scholar]
  29. 29. 
    Chakroun M, Banyuls N, Bel Y, Escriche B, Ferré J 2016. Bacterial vegetative insecticidal proteins (Vip) from entomopathogenic bacteria. Microbiol. Mol. Biol. 80:2329–50
    [Google Scholar]
  30. 30. 
    Chandrasegaran S, Carroll D. 2016. Origins of programmable nucleases for genome engineering. J. Mol. Biol. 428:5963–89
    [Google Scholar]
  31. 31. 
    Chatterjee A, Pohit S, Ghose A 2016. Trade and distributional impacts of genetically modified crops in India: a CGE analysis. Margin 10:3381–407
    [Google Scholar]
  32. 32. 
    Chen K, Wang Y, Zhang R, Zhang H, Gao C 2019. CRISPR/Cas genome editing and precision plant breeding in agriculture. Annu. Rev. Plant Biol. 70:667–97
    [Google Scholar]
  33. 33. 
    Chestukhina GG, Kostina LI, Mikhailova AL, Tyurin SA, Klepikova FS, Stepanov VM 1982. The main features of Bacillus thuringiensis δ-endotoxin molecular structure. Arch. Microbiol. 132:2159–62
    [Google Scholar]
  34. 34. 
    Christian M, Cermak T, Doyle EL, Schmidt C, Zhang F et al. 2010. Targeting DNA double-strand breaks with TAL effector nucleases. Genetics 186:2757–61
    [Google Scholar]
  35. 35. 
    Cohen JI, Paarlberg R. 2002. Explaining restricted approval and availability of GM crops in developing countries. AgBiotechNet 4:1–6
    [Google Scholar]
  36. 36. 
    Council Directive 2001/18/EC of the European Parliament and of the Council of 12 March 2001 on the deliberate release into the environment of genetically modified organisms and repealing Council Directive 90/220/EEC, 2001 O.J. (L 106) 17.4.2001
  37. 37. 
    Council Regulation 1829/2003, Genetically modified food and feed, 2003 O.J. (L 268) 1
  38. 38. 
    Coupe RH, Capel PD. 2016. Trends in pesticide use on soybean, corn and cotton since the introduction of major genetically modified crops in the United States. Pest Manag. Sci. 72:51013–22
    [Google Scholar]
  39. 39. 
    Coupe RH, Kalkhoff SJ, Capel PD, Gregoire C 2012. Fate and transport of glyphosate and aminomethylphosphonic acid in surface waters of agricultural basins. Pest Manag. Sci. 68:116–30
    [Google Scholar]
  40. 40. 
    Dai P, Yan Z, Ma S, Yang Y, Wang Q et al. 2018. The herbicide glyphosate negatively affects midgut bacterial communities and survival of honey bee during larvae reared in vitro. J. Agric. Food Chem. 66:297786–93
    [Google Scholar]
  41. 41. 
    Dai PL, Zhou W, Zhang J, Cui HJ, Wang Q et al. 2012. Field assessment of Bt cry1Ah corn pollen on the survival, development and behavior of Apis mellifera ligustica. Ecotoxicol. Environ. Saf 79:232–37
    [Google Scholar]
  42. 42. 
    Dorhout DL, Rice ME. 2010. Intraguild competition and enhanced survival of western bean cutworm (Lepidoptera: Noctuidae) on transgenic Cry1Ab (MON810) Bacillus thuringiensis corn. J. Econ. Entomol. 103:154–62
    [Google Scholar]
  43. 43. 
    Downes S, Mahon RJ, Rossiter L, Kauter G, Leven T et al. 2010. Adaptive management of pest resistance by Helicoverpa species (Noctuidae) in Australia to the Cry2Ab Bt toxin in Bollgard II® cotton. Evol. Appl. 3:5–6574–84
    [Google Scholar]
  44. 44. 
    Duke SO, Lydon J, Koskinen WC, Moorman TB, Chaney RL, Hammerschmidt R 2012. Glyphosate effects on plant mineral nutrition, crop rhizophere microbiota, and plant disease in glyphosate-resistant crops. J. Agric. Food Chem. 60:10375–97
    [Google Scholar]
  45. 45. 
    Ellstrand NC. 2018. “Born to run. ”? Not necessarily: species and trait bias in persistent free-living transgenic plants. Front. Bioeng. Biotechnol. 6:88Reviews instances of transgenes entering wild populations and identifies traits common to persistent free-living transgenic populations.
    [Google Scholar]
  46. 46. 
    Eriksson D, Kershen D, Nepomuceno A, Pogson BJ, Prieto H et al. 2019. A comparison of the EU regulatory approach to directed mutagenesis with that of other jurisdictions, consequences for international trade and potential steps forward. New Phytology 222:41673–84
    [Google Scholar]
  47. 47. 
    Eur. Comm 2015. Communication from the Commission to the European Parliament, The Council, The European Economic and Social Committee and The Committee of the Regions: reviewing the decision-making process on genetically modified organisms (GMOs) Eur. Comm Brussels: https://eur-lex.europa.eu/legal-content/en/TXT/?uri=CELEX%3A52015DC0176
    [Google Scholar]
  48. 48. 
    Eur. Comm 2015. European Commission fact sheet: questions and answers on EU's policies on GMOs. European Commission http://europa.eu/rapid/press-release_MEMO-15-4778_en.htm
    [Google Scholar]
  49. 49. 
    Eur. Comm 2018. Summary record of the appeal committee: genetically modified food and feed Eur. Comm., Oct. 22 Brussels: https://ec.europa.eu/food/sites/food/files/safety/docs/app-comm_gmffer_20181022_sum.pdf
    [Google Scholar]
  50. 50. 
    Eur. Comm. Dir. Gen. Health Food Saf 2016. Final report of an audit carried out in China from 18 November 2015 to 26 November 2015 in order to evaluate the controls systems for genetically modified organisms in respect of food and feed intended for export to the European Union Eur. Comm. Dir. Gen. Health Food Saf Brussels: http://ec.europa.eu/food/fvo/act_getPDF.cfm?PDF_ID=12293
    [Google Scholar]
  51. 51. 
    Eur. Comm. Group Chief Sci. Advis 2018. Statement by the Group of Chief Scientific Advisors: a scientific perspective on the regulatory status of products derived from gene editing and the implications for the GMO directive Eur. Comm. Group Chief Sci Advis: https://ec.europa.eu/info/sites/info/files/2018_11_gcsa_statement_gene_editing_1.pdf
    [Google Scholar]
  52. 52. 
    Eur. Court Justice Grand Chamb 2018. Judgment of the Court (Grand Chamber) in case C-528/16 Eur. Court Justice Grand Chamb., Luxembourg: http://curia.europa.eu/juris/document/document.jsf?text=&docid=204387&pageIndex=0&doclang=EN&mode=req&dir=&occ=first&part=1&cid=317008/
    [Google Scholar]
  53. 53. 
    Exec. Off. Pres. Off. Sci. Technol. Policy 2017. Modernizing the regulatory system for biotechnology products: final version of the 2017 Update to the Coordinated Framework for the Regulation of Biotechnology Off. Sci. Technol. Policy Washington, DC: https://www.epa.gov/sites/production/files/2017-01/documents/2017_coordinated_framework_update.pdf
    [Google Scholar]
  54. 54. 
    Fan C, Wu F, Dong J, Wang B, Yin J, Song X 2019. No impact of transgenic cry1Ie maize on the diversity, abundance and composition of soil fauna in a 2-year field trial. Sci. Rep. 9:110333
    [Google Scholar]
  55. 55. 
    Fang H, Dong B, Yan H, Tang F, Wang B, Yu Y 2012. Effect of vegetation of transgenic Bt rice lines and their straw amendment on soil enzymes, respiration, functional diversity and community structure of soil microorganisms under field conditions. J. Environ. Sci. 24:71259–70
    [Google Scholar]
  56. 56. 
    Fernandez-Cornejo J, Wechsler SJ. 2012. Revisiting the impact of Bt corn adoption by U.S. farmers. Agric. Resour. Econ. Rev. 41:3377–90
    [Google Scholar]
  57. 57. 
    Fernandez-Cornejo J, Wechsler SJ, Livingston M, Mitchell L 2014. Genetically engineered crops in the United States USDA Econ. Res. Rep. 162, US Dep. Agric., Econ. Res. Serv Washington, DC: https://www.ers.usda.gov/webdocs/publications/45179/43668_err162.pdf
    [Google Scholar]
  58. 58. 
    Firko M. 2015. Confirmation that FAD2KO soybean is not a regulated article Letter, US Dep. Agric. Anim. Plant Health Insp. Serv Riverdale, MD: https://www.aphis.usda.gov/biotechnology/downloads/reg_loi/brs_response_cellectis_air_fad2k0_soy_cbidel.pdf
    [Google Scholar]
  59. 59. 
    Food Agric. Organ. U. N., Int. Fund Agric. Dev., World Food Programme 2015. The State of Food Insecurity in the World Rome: World Food Programme https://www.wfp.org/publications/state-food-insecurity-world-2015
    [Google Scholar]
  60. 60. 
    Fraiture M-A, Herman P, De Loose M, Debode F, Roosens NH 2017. How can we better detect unauthorized GMOs in food and feed chains. Trends Biotechnol 35:6508–17
    [Google Scholar]
  61. 61. 
    Gaudelli NM, Komor AC, Rees HA, Packer MS, Badran AH et al. 2017. Programmable base editing of A·T to G·C in genomic DNA without DNA cleavage. Nature 551:768146471 Erratum 2018. Nature 559:7714E8
    [Google Scholar]
  62. 62. 
    Gómez I, Sánchez J, Muñoz-Garay C, Matus V, Gill SS et al. 2014. Bacillus thuringiensis Cry1A toxins are versatile proteins with multiple modes of action: two distinct pre-pores are involved in toxicity. Biochem. J. 459:2383–96
    [Google Scholar]
  63. 63. 
    Gressel J. 2009. Evolving understanding of the evolution of herbicide resistance. Pest Manag. Sci. 65:111164–73
    [Google Scholar]
  64. 64. 
    Gressel J. 2018. Intractable weed problems need innovative solutions using all available technologies. Indian J. Weed Sci. 50:3201–8
    [Google Scholar]
  65. 65. 
    Gressel J, Valverde BE. 2009. A strategy to provide long-term control of weedy rice while mitigating herbicide resistance transgene flow, and its potential use for other crops with related weeds. Pest Manag. Sci. 65:7723–31
    [Google Scholar]
  66. 66. 
    Gruère G, Sengupta D. 2009. GM-free private standards and their effects on biosafety decision-making in developing countries. Food Policy 34:5399–406
    [Google Scholar]
  67. 67. 
    Gruère GP, Bouët A, Mevel S 2011. International trade and welfare effects of biotechnology innovations: GM food crops in Bangladesh, India, Indonesia, and the Philippines. Frontiers of Economics and Globalization, Vol. 10: Genetically Modified Food and Global Welfare C Carter, G Moschini, I Sheldon 283–308 Bingley, UK: Emerald Group
    [Google Scholar]
  68. 68. 
    Guijarro KH, Aparicio V, De Gerónimo E, Castellote M, Figuerola EL et al. 2018. Soil microbial communities and glyphosate decay in soils with different herbicide application history. Sci. Total Environ. 634:974–82
    [Google Scholar]
  69. 69. 
    Hall L, Topinka K, Huffman J, Davis L, Good A 2000. Pollen flow between herbicide-resistant Brassica napus is the cause of multiple-resistant B. napus volunteers. Weed Sci 48:6688–94
    [Google Scholar]
  70. 70. 
    Han H, Yu Q, Owen MJ, Cawthray GR, Powles SB 2016. Widespread occurrence of both metabolic and target-site herbicide resistance mechanisms in Lolium rigidum populations. Pest Manag. Sci. 72:2255–63
    [Google Scholar]
  71. 71. 
    Haney RL, Senseman SA, Hons FM, Zuberer DA 2000. Effect of glyphosate on soil microbial activity and biomass. Weed Sci 48:189–93
    [Google Scholar]
  72. 72. 
    Hanke I, Wittmer I, Bischofberger S, Stamm C, Singer H 2010. Relevance of urban glyphosate use for surface water quality. Chemosphere 81:3422–29
    [Google Scholar]
  73. 73. 
    Heap I. 2014. Herbicide resistant weeds. Integrated Pest Management, Vol. 3: Pesticide Problems D Pimentel, R Peshin 281–301 Dordrecht, Neth: Springer
    [Google Scholar]
  74. 74. 
    Helmer SH, Kerbaol A, Aras P, Jumarie C, Boily M 2015. Effects of realistic doses of atrazine, metolachlor, and glyphosate on lipid peroxidation and diet-derived antioxidants in caged honey bees (Apis mellifera). Environ. Sci. Pollut. Res. 22:118010–21
    [Google Scholar]
  75. 75. 
    Hendriksma HP, Küting M, Härtel S, Näther A, Dohrmann AB et al. 2013. Effect of stacked insecticidal cry proteins from maize pollen on nurse bees (Apis mellifera carnica) and their gut bacteria. PLOS ONE 8:3e59589
    [Google Scholar]
  76. 76. 
    Höss S, Menzel R, Gessler F, Nguyen HT, Jehle JA, Traunspurger W 2013. Effects of insecticidal crystal proteins (Cry proteins) produced by genetically modified maize (Bt maize) on the nematode Caenorhabditis elegans. Environ. Pollut 178:147–51
    [Google Scholar]
  77. 77. 
    Huesing JE, Romeis J, Ellstrand NC, Raybould A, Hellmich RL et al. 2011. Regulatory considerations surrounding the deployment of Bt-expression cowpea in Africa: report of the deliberations of an expert panel. GM Crops 2:3211–24
    [Google Scholar]
  78. 78. 
    Hufford MB, Lubinsky P, Pyhäjärvi T, Devengenzo MT, Ellstrand NC, Ross-Ibarra J 2013. The genomic signature of crop-wild introgression in maize. PLOS Genet 9:5e1003477
    [Google Scholar]
  79. 79. 
    Int. Serv. Acquis. Agri-Biotech Appl 2019. ISAAA's GM Approval Database Updated Oct. 22. http://www.isaaa.org/gmapprovaldatabase/ Database of all genetically engineered crop events approved for food, feed, and/or cultivation around the world.
    [Google Scholar]
  80. 80. 
    Isalan M. 2012. Zinc-finger nucleases: how to play two good hands. Nat. Methods 9:132–34
    [Google Scholar]
  81. 81. 
    James C. 2017. Global status of commercialized biotech/GM crops in 2017: biotech crop adoption surges as economic benefits accumulate in 22 years. ISAAA Briefs 53:1–153Detailed report of the adoption rates of different genetically engineered crops around the world.
    [Google Scholar]
  82. 82. 
    Jayaraman K. 2010. Bt brinjal splits Indian cabinet. Nat. Biotechnol. 28:4296
    [Google Scholar]
  83. 83. 
    Jayaraman K. 2017. Activists bury India's GM mustard hopes. Nat. Biotechnol. 35:121124
    [Google Scholar]
  84. 84. 
    Jin L, Zhang H, Lu Y, Yang Y, Wu K et al. 2015. Large-scale test of the natural refuge strategy for delaying insect resistance to transgenic Bt crops. Nat. Biotechnol. 33:2169–74
    [Google Scholar]
  85. 85. 
    Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E 2012. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337:6096816–21
    [Google Scholar]
  86. 86. 
    Jones HD. 2015. Regulatory uncertainty over genome editing. Nat. Plants 1:114011
    [Google Scholar]
  87. 87. 
    Jung C, Capistrano-Gossmann G, Braatz J, Sashidhar N, Melzer S 2018. Recent developments in genome editing and applications in plant breeding. Plant Breed 137:11–9
    [Google Scholar]
  88. 88. 
    Kay S, Hahn S, Marois E, Hause G, Bonas U 2007. A bacterial effector acts as a plant transcription factor and induces a cell size regulator. Science 318:5850648–51
    [Google Scholar]
  89. 89. 
    Kelly DW, Poulin R, Tompkins DM, Townsend CR 2010. Synergistic effects of glyphosate formulation and parasite infection on fish malformations and survival. J. Appl. Ecol. 47:2498–504
    [Google Scholar]
  90. 90. 
    Kim S, Kim D, Cho S, Kim J, Kim J-S 2014. Highly efficient RNA-guided genome editing in human cells via delivery of purified Cas9 ribonucleoproteins. Genome Res 128:1–32
    [Google Scholar]
  91. 91. 
    Kim YG, Cha J, Chandrasegaran S 1996. Hybrid restriction enzymes: zinc finger fusions to Fok I cleavage domain. PNAS 93:31156–60
    [Google Scholar]
  92. 92. 
    Klümper W, Qaim M. 2014. A meta-analysis of the impacts of genetically modified crops. PLOS ONE 9:11e111629Uses 147 studies to assess the economic and agronomic effects of GE crops internationally.
    [Google Scholar]
  93. 93. 
    Kniss AR. 2017. Long-term trends in the intensity and relative toxicity of herbicide use. Nat. Commun. 8:1–7
    [Google Scholar]
  94. 94. 
    Kniss AR, Coburn CW. 2015. Quantitative evaluation of the Environmental Impact Quotient (EIQ) for comparing herbicides. PLOS ONE 10:61–13
    [Google Scholar]
  95. 95. 
    Komor AC, Kim YB, Packer MS, Zuris JA, Liu DR 2016. Programmable editing of a target base in genomic DNA without double-stranded DNA cleavage. Nature 533:420–24First description of harnessing CRISPR machinery to make a precise single base pair change without homology-directed repair.
    [Google Scholar]
  96. 96. 
    Kovach J, Petzoldt C, Degni J, Tette J 1992. A method to measure the environmental impact of pesticides. N. Y. Food Life Sci. Bull. 139:1–8
    [Google Scholar]
  97. 97. 
    Kudsk P, Streibig JC. 2003. Herbicides—a two-edged sword. Weed Res 43:290–102
    [Google Scholar]
  98. 98. 
    Laitinen P, Rämö S, Siimes K 2007. Glyphosate translocation from plants to soil—does this constitute a significant proportion of residues in soil. Plant Soil 300:1–251–60
    [Google Scholar]
  99. 99. 
    Lemaux PG. 2008. Genetically engineered plants and foods: a scientist's analysis of the issues (Part I). Annu. Rev. Plant Biol. 59:771–812
    [Google Scholar]
  100. 100. 
    Lemaux PG. 2009. Genetically engineered plants and foods: a scientist's analysis of the issues (Part II). Annu. Rev. Plant Biol. 60:511–59
    [Google Scholar]
  101. 101. 
    Lemmon ZH, Reem NT, Dalrymple J, Soyk S, Swartwood KE et al. 2018. Rapid improvement of domestication traits in an orphan crop by genome editing. Nat. Plants 4:766–70
    [Google Scholar]
  102. 102. 
    Li X, Liu B, Cui J, Liu D, Ding S et al. 2011. No evidence of persistent effects of continuously planted transgenic insect-resistant cotton on soil microorganisms. Plant Soil 339:1247–57
    [Google Scholar]
  103. 103. 
    Liao C, Heckel DG, Akhurst R 2002. Toxicity of Bacillus thuringiensis insecticidal proteins for Helicoverpa armigera and Helicoverpa punctigera (Lepidoptera: Noctuidae), major pests of cotton. J. Invertebr. Pathol. 80:155–63
    [Google Scholar]
  104. 104. 
    Lu B-R, Yang X, Ellstrand NC 2016. Fitness correlates of crop transgene flow into weedy populations: a case study of weedy rice in China and other examples. Evol. Appl. 9:857–70
    [Google Scholar]
  105. 105. 
    Lu H, Wu W, Chen Y, Zhang X, Devare M, Thies JE 2010. Decomposition of Bt transgenic rice residues and response of soil microbial community in rapeseed-rice cropping system. Plant Soil 336:1279–90
    [Google Scholar]
  106. 106. 
    Lupwayi NZ, Blackshaw RE. 2013. Soil microbial properties in Bt (Bacillus thuringiensis) corn cropping systems. Appl. Soil Ecol. 63:127–33
    [Google Scholar]
  107. 107. 
    Mabaya E, Fulton J, Simiyu-Wafukho S, Nang'ayo F 2015. Factors influencing adoption of genetically modified crops in Africa. Dev. South Afr. 32:5577–91
    [Google Scholar]
  108. 108. 
    Meihls LN, Higdon ML, Siegfried BD, Miller NJ, Sappington TW et al. 2008. Increased survival of western corn rootworm on transgenic corn within three generations of on-plant greenhouse selection. PNAS 105:4919177–82
    [Google Scholar]
  109. 109. 
    Mijangos I, Becerril JM, Albizu I, Epelde L, Garbisu C 2009. Effects of glyphosate on rhizosphere soil microbial communities under two different plant compositions by cultivation-dependent and -independent methodologies. Soil Biol. Biochem. 41:3505–13
    [Google Scholar]
  110. 110. 
    Mojica FJM, Díez-Villaseñor C, García-Martínez J, Soria E 2005. Intervening sequences of regularly spaced prokaryotic repeats derive from foreign genetic elements. J. Mol. Evol. 60:2174–82
    [Google Scholar]
  111. 111. 
    Moreno-Mateos MA, Fernandez JP, Rouet R, Vejnar CE, Lane MA et al. 2017. CRISPR-Cpf1 mediates efficient homology-directed repair and temperature-controlled genome editing. Nat. Commun. 82024:1–9
    [Google Scholar]
  112. 112. 
    Moscou MJ, Bogdanove AJ. 2009. A simple cipher governs DNA recognition by TAL effectors. Science 326:59591501
    [Google Scholar]
  113. 113. 
    Motta EVS, Raymann K, Moran NA 2018. Glyphosate perturbs the gut microbiota of honey bees. PNAS 115:411–6
    [Google Scholar]
  114. 114. 
    Nat. Acad. Sci. Eng. Med 2016. Genetically Engineered Crops: Experiences and Prospects Washington, DC: Nat. Acad. Press https://doi.org/10.17226/23395 Comprehensive review of the human, environmental, social, and economic effects of genetically engineered crops.
    [Crossref] [Google Scholar]
  115. 115. 
    Nat. Biosaf. Tech. Comm. Braz 2018. National Biosafety Technical Commission normative resolution no. 16, of January 15, 2018 Nat. Biosaf. Tech. Comm. Braz https://agrobiobrasil.org.br/wp-content/uploads/2018/05/Normative-Resolution-16-of-January-15-2018.pdf
    [Google Scholar]
  116. 116. 
    Oberthur S, Gehring T. 2006. Institutional interaction in global environmental governance: the case of the Cartagena Protocol and the World Trade Organization. Glob. Environ. Polit. 6:21–31A detailed analysis of the interactions between the WTO SPS Agreement and the Cartagena Protocol on Biosafety.
    [Google Scholar]
  117. 117. 
    Off. Pestic. Programs 2010. Terms and Conditions for Bt Corn Registrants Washington, DC: Environ. Prot. Agency https://www3.epa.gov/pesticides/chem_search/reg_actions/pip/bt-corn-terms-conditions.pdf
    [Google Scholar]
  118. 118. 
    Onstad DW, Meinke LJ. 2010. Modeling evolution of Diabrotica virgifera virgifera (Coleoptera: Chrysomelidae) to transgenic corn with two insecticidal traits. J. Econ. Entomol. 103:3849–60
    [Google Scholar]
  119. 119. 
    Orloff SB, Putnam DH, Canevari M, Lanini WT 2009. Avoiding weed shifts and weed resistance in Roundup Ready alfalfa systems ANR Publ. 8362, Univ. Calif. Div. Agric. Nat. Resour Davis, CA: https://anrcatalog.ucanr.edu/pdf/8362.pdf
    [Google Scholar]
  120. 120. 
    Paarlberg R. 2010. GMO foods and crops: Africa's choice. N. Biotechnol. 27:5609–13
    [Google Scholar]
  121. 121. 
    Parfitt J, Barthel M, MacNaughton S 2010. Food waste within food supply chains: quantification and potential for change to 2050. Philos. Trans. R. Soc. B 365:15543065–81
    [Google Scholar]
  122. 122. 
    Perry ED, Ciliberto F, Hennessy DA, Moschini G 2016. Genetically engineered crops and pesticide use in U.S. maize and soybeans. Sci. Adv. 2:81–8
    [Google Scholar]
  123. 123. 
    Peterson MA, Collavo A, Ovejero R, Shivrain V, Walsh MJ 2018. The challenge of herbicide resistance around the world: a current summary. Pest Manag. Sci. 74:102246–59
    [Google Scholar]
  124. 124. 
    Peterson RKD, Schleier JJ. 2014. A probabilistic analysis reveals fundamental limitations with the environmental impact quotient and similar systems for rating pesticide risks. PeerJ 2:e364
    [Google Scholar]
  125. 125. 
    Pleasants J. 2017. Milkweed restoration in the Midwest for monarch butterfly recovery: estimates of milkweeds lost, milkweeds remaining and milkweeds that must be added to increase the monarch population. Insect Conserv. Divers. 10:142–53
    [Google Scholar]
  126. 126. 
    Pourcel C, Salvignol G, Vergnaud G 2005. CRISPR elements in Yersinia pestis acquire new repeats by preferential uptake of bacteriophage DNA, and provide additional tools for evolutionary studies. Microbiology 151:3653–63
    [Google Scholar]
  127. 127. 
    Powles SB, Lorraine-Colwill DF, Dellow JJ, Preston C 1998. Evolved resistance to glyphosate in rigid ryegrass (Lolium rigidum) in Australia. Weed Sci 46:5604–7
    [Google Scholar]
  128. 128. 
    Ramesh J. 2010. Bt brinjal: note by Ministry of Environment and Forests. The Hindu, Feb. 9 https://www.thehindu.com/news/national/Bt-Brinjal-Note-by-Ministry-of-Environment-and-Forests/article16578296.ece
    [Google Scholar]
  129. 129. 
    Rashid M, Hasan M, Matin M 2018. Socio-economic performance of Bt eggplant cultivation in Bangladesh. Bangladesh J. Agric. Res. 43:2187–203
    [Google Scholar]
  130. 130. 
    Rendón-Von Osten J, Dzul-Caamal R 2017. Glyphosate residues in groundwater, drinking water and urine of subsistence farmers from intensive agriculture localities: a survey in Hopelchén, Campeche, Mexico. Int. J. Environ. Res. Public Health 14:6595
    [Google Scholar]
  131. 131. 
    Römer P, Hahn S, Jordan T, Strauss T, Bonas U, Lahaye T 2007. Plant pathogen recognition mediated by promoter activation of the pepper Bs3 resistance gene. Science 318:5850645–48
    [Google Scholar]
  132. 132. 
    Römer P, Recht S, Strauß T, Elsaesser J, Schornack S et al. 2010. Promoter elements of rice susceptibility genes are bound and activated by specific TAL effectors from the bacterial blight pathogen, Xanthomonas oryzae pv. oryzae. New Phytol. 187:41048–57
    [Google Scholar]
  133. 133. 
    Rose R, Dively GP. 2007. Effects of insecticide-treated and lepidopteran-active Bt transgenic sweet corn on the abundance and diversity of arthropods. Environ. Entomol. 36:51254–68
    [Google Scholar]
  134. 134. 
    Ryan GF. 1970. Resistance of common groundsel to simazine and atrazine. Weed Sci. Soc. Am. 18:5614–16
    [Google Scholar]
  135. 135. 
    Sanahuja G, Banakar R, Twyman RM, Capell T, Christou P 2011. Bacillus thuringiensis: a century of research, development and commercial applications. Plant Biotechnol. J. 9:3283–300
    [Google Scholar]
  136. 136. 
    Schiemann J, Dietz-Pfeilstetter A, Hartung F, Kohl C, Romeis J, Sprink T 2019. Risk assessment and regulation of plants modified by modern biotechniques: current status and future challenges. Annu. Rev. Plant Biol. 70:699–726
    [Google Scholar]
  137. 137. 
    Schlatter DC, Yin C, Burke I, Hulbert S, Paulitz T 2018. Location, root proximity, and glyphosate-use history modulate the effects of glyphosate on fungal community networks of wheat. Microb. Ecol. 76:1240–57
    [Google Scholar]
  138. 138. 
    Schlatter DC, Yin C, Hulbert S, Burke I, Paulitz T 2017. Impacts of repeated glyphosate use on wheat-associated bacteria are small and depend on glyphosate use history. Appl. Environ. Microbiol. 83:221–16
    [Google Scholar]
  139. 139. 
    Schmidt JEU, Braun CU, Whitehouse LP, Hilbeck A 2009. Effects of activated Bt transgene products (Cry1Ab, Cry3Bb) on immature stages of the ladybird Adalia bipunctata in laboratory ecotoxicity testing. Arch. Environ. Contam. Toxicol. 56:2221–28
    [Google Scholar]
  140. 140. 
    Secr. Conv. Biol. Divers 2000. Cartagena Protocol on Biosafety Convention on Biological Diversity: Texts and Annexes Montreal: Secr. Conv. Biol. Divers https://www.cbd.int/doc/legal/cartagena-protocol-en.pdf
    [Google Scholar]
  141. 141. 
    Shelton AM, Hossain MJ, Paranjape V, Azad AK, Rahman ML et al. 2018. Bt eggplant project in Bangladesh: history, present status, and future direction. Front. Bioeng. Biotechnol. 6:1061–6Description of the deployment of Bt eggplant in Bangladesh.
    [Google Scholar]
  142. 142. 
    Sisterson MS, Biggs RW, Olson C, Carrière Y, Dennehy TJ, Tabashnik BE 2004. Arthropod abundance and diversity in Bt and non-Bt cotton fields. Environ. Entomol. 33:4921–29
    [Google Scholar]
  143. 143. 
    Smyth SJ. 2017. Canadian regulatory perspectives on genome engineered crops. GM Crops Food 8:135–43
    [Google Scholar]
  144. 144. 
    Smyth SJ. 2019. Global status of the regulation of genome editing technologies. CAB Rev 14:0211–6
    [Google Scholar]
  145. 145. 
    Stephens EJ, Losey JE, Allee LL, DiTommaso A, Bodner C, Breyre A 2012. The impact of Cry3Bb Bt-maize on two guilds of beneficial beetles. Agric. Ecosyst. Environ. 156:72–81
    [Google Scholar]
  146. 146. 
    Struger J, Thompson D, Staznik B, Martin P, McDaniel T, Marvin C 2008. Occurrence of glyphosate in surface waters of southern Ontario. Bull. Environ. Contam. Toxicol. 80:4378–84
    [Google Scholar]
  147. 147. 
    Svobodová Z, Shu Y, Habuštová OS, Romeis J, Meissle M 2017. Stacked Bt maize and arthropod predators: exposure to insecticidal Cry proteins and potential hazards. Proc. R. Soc. B 284:185920170440
    [Google Scholar]
  148. 148. 
    Tabashnik BE, Carrière Y. 2017. Surge in insect resistance to transgenic crops and prospects for sustainability. Nat. Biotechnol. 35:10926–35Describes the rising instances of Bt resistance in insects and the necessary steps to delay further resistance.
    [Google Scholar]
  149. 149. 
    Tabashnik BE, Gassmann AJ, Crowder DW, Carriére Y 2008. Insect resistance to Bt crops: evidence versus theory. Nat. Biotechnol. 26:2199–202
    [Google Scholar]
  150. 150. 
    Tabashnik BE, Mota-Sanchez D, Whalon ME, Hollingworth RM, Carrière Y 2014. Defining terms for proactive management of resistance to Bt crops and pesticides. J. Econ. Entomol. 107:2496–507
    [Google Scholar]
  151. 151. 
    Tabashnik BE, Zhang M, Fabrick JA, Wu Y, Gao M et al. 2015. Dual mode of action of Bt proteins: protoxin efficacy against resistant insects. Sci. Rep. 5:115107
    [Google Scholar]
  152. 152. 
    Thompson HM, Levine SL, Doering J, Norman S, Manson P et al. 2014. Evaluating exposure and potential effects on honeybee brood (Apis mellifera) development using glyphosate as an example. Integr. Environ. Assess. Manag. 10:3463–70
    [Google Scholar]
  153. 153. 
    Trump DJ. 2019. Executive order on modernizing the regulatory framework for agricultural biotechnology products Exec. Order, White House Washington, DC: https://www.whitehouse.gov/presidential-actions/executive-order-modernizing-regulatory-framework-agricultural-biotechnology-products/
    [Google Scholar]
  154. 154. 
    US Dep. Agric. Anim. Plant Health Insp. Serv 2019. Regulated Article Letters of Inquiry US Dep. Agric. Anim. Plant Health Insp. Serv Riverdale, MD: https://www.aphis.usda.gov/aphis/ourfocus/biotechnology/am-i-regulated/regulated_article_letters_of_inquiry/regulated_article_letters_of_inquiry
    [Google Scholar]
  155. 155. 
    US Environ. Prot. Agency 2010. Cry1Ab and Cry1F Bacillus thuringiensis (Bt) corn plant-incorporated protectants Biopestic. Regis. Action Doc., US Environ. Prot. Agency, Off. Pestic. Programs, Biopestic. Pollut. Prev. Div Washington, DC: https://www3.epa.gov/pesticides/chem_search/reg_actions/pip/cry1f-cry1ab-brad.pdf
    [Google Scholar]
  156. 156. 
    US Environ. Prot. Agency 2018. White paper on resistance in lepidopteran pests to Bacillus thuringiensis (Bt) plant incorporated protectants (PIPs) in the United States US Environ. Prot. Agency Washington, DC: https://www.epa.gov/sites/production/files/2018-07/documents/position_paper_07132018.pdf
    [Google Scholar]
  157. 157. 
    US Environ. Prot. Agency FIFRA Sci. Advis. Panel 1998. Final report of the subpanel on Bacillus thuringiensis (Bt) plant-pesticides and resistance management US Environ. Prot. Agency Washington, DC: https://archive.epa.gov/scipoly/sap/meetings/web/pdf/finalfeb.pdf
    [Google Scholar]
  158. 158. 
    US Food Drug Admin 2018. Plant and Animal Biotechnology Innovation Action Plan Silver Spring, MD: Food Drug Admin https://www.fda.gov/media/119882/download
    [Google Scholar]
  159. 159. 
    US Food Drug Admin. Center Food Saf. Appl. Nutr 2019. CFSAN note to the file Biotechnol. Notif. File Number 000164, US Food Drug Admin Washington, DC: https://www.fda.gov/media/120708/download
    [Google Scholar]
  160. 160. 
    US Food Drug Admin Off. Food Addit. Saf. 1992. Guidance document: statement of policy—foods derived from new plant varieties. FDA Fed. Regist. 57: https://www.fda.gov/regulatory-information/search-fda-guidance-documents/statement-policy-foods-derived-new-plant-varieties#contents
    [Google Scholar]
  161. 161. 
    van Frankenhuyzen K. 2017. Specificity and cross-order activity of Bacillus thuringiensis pesticidal proteins. Bacillus thuringiensis and Lysinibacillus sphaericus. Characterization and Use in the Field of Biocontrol LM Fiuza, RA Polanczyk, N Crickmore 127–72 Cham, Switz.: Springer
    [Google Scholar]
  162. 162. 
    Velmourougane K, Sahu A. 2013. Impact of transgenic cottons expressing cry1Ac on soil biological attributes. Plant Soil Environ 59:3108–14
    [Google Scholar]
  163. 163. 
    Vera MS, Lagomarsino L, Sylvester M, Pérez GL, Rodríguez P et al. 2010. New evidences of Roundup® (glyphosate formulation) impact on the periphyton community and the water quality of freshwater ecosystems. Ecotoxicology 19:4710–21
    [Google Scholar]
  164. 164. 
    Watrud LS, Lee EH, Fairbrother A, Burdick C, Reichman JR et al. 2004. Evidence for landscape-level, pollen-mediated gene flow from genetically modified creeping bentgrass with CP4 EPSPS as a marker. PNAS 101:4014533–38
    [Google Scholar]
  165. 165. 
    Wei J, Guo Y, Liang G, Wu K, Zhang J et al. 2015. Cross-resistance and interactions between Bt toxins Cry1Ac and Cry2Ab against the cotton bollworm. Sci. Rep. 5:17714
    [Google Scholar]
  166. 166. 
    Wong AY-T, Chan AW-K. 2016. Genetically modified foods in China and the United States: a primer of regulation and intellectual property protection. Food Sci. Hum. Wellness 5:3124–40
    [Google Scholar]
  167. 167. 
    World Trade Organ 2010. World Trade Organization Agreements Series on Sanitary and Phytosanitary Measures 1867 U.N.T.S. 493. Geneva: World Trade Organ https://www.wto.org/english/res_e/booksp_e/agrmntseries4_sps_e.pdf
    [Google Scholar]
  168. 168. 
    Yang F, Kerns D, Huang F 2015. Refuge-in-the-bag strategy for managing insect resistance to BT maize. Outlooks Pest Manag 26:5226–28
    [Google Scholar]
  169. 169. 
    Yaqoob A, Shahid AA, Samiullah TR, Rao AQ, Khan MAU et al. 2016. Risk assessment of Bt crops on the non-target plant-associated insects and soil organisms. J. Sci. Food Agric. 96:82613–19
    [Google Scholar]
  170. 170. 
    Yu Q, Powles S. 2014. Metabolism-based herbicide resistance and cross-resistance in crop weeds: a threat to herbicide sustainability and global crop production. Plant Physiol 166:1106–18
    [Google Scholar]
  171. 171. 
    Zapiola ML, Campbell CK, Butler MD, Mallory-Smith CA 2008. Escape and establishment of transgenic glyphosate-resistant creeping bentgrass Agrostis stolonifera in Oregon, USA: a 4-year study. J. Appl. Ecol. 45:2486–94
    [Google Scholar]
  172. 172. 
    Zapiola ML, Mallory-Smith CA. 2017. Pollen-mediated gene flow from transgenic perennial creeping bentgrass and hybridization at the landscape level. PLOS ONE 12:31–13
    [Google Scholar]
  173. 173. 
    Zetsche B, Gootenberg JS, Abudayyeh OO, Slaymaker IM, Makarova KS et al. 2015. Cpf1 is a single RNA-guided endonuclease of a class 2 CRISPR-Cas system. Cell 163:3759–71
    [Google Scholar]
  174. 174. 
    Zhao J-Z, Cao J, Collins HL, Bates SL, Roush RT et al. 2005. Concurrent use of transgenic plants expressing a single and two Bacillus thuringiensis genes speeds insect adaptation to pyramided plants. PNAS 102:248426–30
    [Google Scholar]
  175. 175. 
    Zhao J-Z, Cao J, Li Y, Collins HL, Roush RT et al. 2003. Transgenic plants expressing two Bacillus thuringiensis toxins delay insect resistance evolution. Nat. Biotechnol. 21:121493–97
    [Google Scholar]
  176. 176. 
    Zsögön A, Čermák T, Naves ER, Notini MM, Edel KH et al. 2018. De novo domestication of wild tomato using genome editing. Nat. Biotechnol. 36:121211–16
    [Google Scholar]
/content/journals/10.1146/annurev-arplant-081519-035916
Loading
  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error