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Plant Cell Reports

, Volume 35, Issue 7, pp 1507–1518 | Cite as

Consumer acceptance of food crops developed by genome editing

  • Tetsuya Ishii
  • Motoko Araki
Opinion Paper

Abstract

One of the major problems regarding consumer acceptance of genetically modified organisms (GMOs) is the possibility that their transgenes could have adverse effects on the environment and/or human health. Genome editing, represented by the CRISPR/Cas9 system, can efficiently achieve transgene-free gene modifications and is anticipated to generate a wide spectrum of plants. However, the public attitude against GMOs suggests that people will initially be unlikely to accept these plants. We herein explored the bottlenecks of consumer acceptance of transgene-free food crops developed by genome editing and made some recommendations. People should not pursue a zero-risk bias regarding such crops. Developers are encouraged to produce cultivars with a trait that would satisfy consumer needs. Moreover, they should carefully investigate off-target mutations in resultant plants and initially refrain from agricultural use of multiplex genome editing for better risk–benefit communication. The government must consider their regulatory status and establish appropriate regulations if necessary. The government also should foster communication between the public and developers. If people are informed of the benefits of genome editing-mediated plant breeding and trust in the relevant regulations, and if careful risk–benefit communication and sincere considerations for the right to know approach are guaranteed, then such transgene-free crops could gradually be integrated into society.

Keywords

Genome editing Crop Food GMO Consumer CRISPR/Cas9 

Notes

Acknowledgments

This work was supported by a Hokkaido University faculty grant to TI.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Ahloowalia B, Maluszynski M, Nichterlein K (2004) Global impact of mutation-derived varieties. Euphytica 135:187–204CrossRefGoogle Scholar
  2. Araki M, Ishii T (2015) Towards social acceptance of plant breeding by genome editing. Trends Plant Sci 20:145–149CrossRefPubMedGoogle Scholar
  3. Araki M, Nojima K, Ishii T (2014) Caution required for handling genome editing technology. Trends Biotechnol 32:234–237CrossRefPubMedGoogle Scholar
  4. Barfoot P, Brookes G (2014) Key global environmental impacts of genetically modified (GM) crop use 1996-2012. GM Crops Food 5:149–160CrossRefPubMedGoogle Scholar
  5. Bartholomaeus A, Parrott W, Bondy G, Walker K (2013) The use of whole food animal studies in the safety assessment of genetically modified crops: limitations and recommendations. Crit Rev Toxicol 43(Suppl 2):1–24CrossRefPubMedPubMedCentralGoogle Scholar
  6. Belhaj K, Chaparro-Garcia A, Kamoun S, Patron NJ, Nekrasov V (2015) Editing plant genomes with CRISPR/Cas9. Curr Opin Biotechnol 32:76–84CrossRefPubMedGoogle Scholar
  7. Brookes G, Barfoot P (2012) GM crops: global socio-economic and environmental impacts 1996–2010. PG Economics Ltd., UKGoogle Scholar
  8. Burgos NR, Singh V, Tseng TM, Black H, Young ND, Huang Z, Hyma KE, Gealy DR, Caicedo AL (2014) The impact of herbicide-resistant rice technology on phenotypic diversity and population structure of United States weedy rice. Plant Physiol 166:1208–1220CrossRefPubMedPubMedCentralGoogle Scholar
  9. Busconi M, Rossi D, Lorenzoni C, Baldi G, Fogher C (2012) Spread of herbicide-resistant weedy rice (red rice, Oryza sativa L.) after 5 years of clearfield rice cultivation in Italy. Plant Biol (Stuttgart, Germany) 14:751–759CrossRefGoogle Scholar
  10. Butler NM, Atkins PA, Voytas DF, Douches DS (2015) Generation and Inheritance of Targeted Mutations in Potato (Solanum tuberosum L.) using the CRISPR/Cas system. PLoS One 10:e0144591CrossRefPubMedPubMedCentralGoogle Scholar
  11. Camacho A, Van Deynze A, Chi-Ham C, Bennett AB (2014) Genetically engineered crops that fly under the US regulatory radar. Nat Biotechnol 32:1087–1091CrossRefPubMedGoogle Scholar
  12. Center_for_Food_Safety (2015) Environmental, Farmer, and Consumer Groups Demand Higher Standards for Genetically Engineered (GE) Crop Regulations. http://www.centerforfoodsafety.org/press-releases/3967/environmental-farmer-and-consumer-groups-demand-higher-standards-for-genetically-engineered-ge-crop-regulations. Accessed 19 Feb 2016
  13. Chen H, Lin Y (2013) Promise and issues of genetically modified crops. Curr Opin Plant Biol 16:255–260CrossRefPubMedGoogle Scholar
  14. Clasen BM, Stoddard TJ, Luo S, Demorest ZL, Li J, Cedrone F, Tibebu R, Davison S, Ray EE, Daulhac A, Coffman A, Yabandith A, Retterath A, Haun W, Baltes NJ, Mathis L, Voytas DF, Zhang F (2015) Improving cold storage and processing traits in potato through targeted gene knockout. Plant Biotechnol J 14:169–176CrossRefPubMedGoogle Scholar
  15. Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, Hsu PD, Wu X, Jiang W, Marraffini LA, Zhang F (2013) Multiplex genome engineering using CRISPR/Cas systems. Science (New York, NY) 339:819–823CrossRefGoogle Scholar
  16. Davidson J (2010) GM plants: science, politics and EC regulations. Plant Sci 178:94–98CrossRefGoogle Scholar
  17. EFSA_GMO_Panel_Working_Group_on_Animal_Feeding_Trials (2008) Safety and nutritional assessment of GM plants and derived food and feed: the role of animal feeding trials. Food Chem Toxicol 46:S2–S70Google Scholar
  18. European_Academies’_Science_Advisory_Council (2015) Statement: New breeding techniques. http://www.easac.eu/fileadmin/PDF_s/reports_statements/Easac_14_NBT.pdf. Accessed 7 Mar 2016
  19. European_Plant_Science_Organisation (2015) Statement: Crop Genetic Improvement Technologies. http://www.epsoweb.org/file/2147. Accessed 7 Mar 2016
  20. European_Seed_Association (2015) Regulatory approaches to modern plant breeding - the case of mutagenesis and new gene editing technologies. https://www.euroseeds.eu/system/files/publications/files/esa_15.0543_0.pdf. Accessed 7 Mar 2015
  21. Friedman M, Rasooly R (2013) Review of the inhibition of biological activities of food-related selected toxins by natural compounds. Toxins 5:743–775CrossRefPubMedPubMedCentralGoogle Scholar
  22. GM_Freeze (2016) The case for regulating Gene Edited crops. http://www.gmfreeze.org/news-releases/266/. Accessed 7 Mar 2016
  23. GMWATCH (2014) “Genome editing”: GM by another name. http://www.gmwatch.org/news/archive/2014/15546-genome-editing-gm-by-another-name. Accessed 19 Feb 2016
  24. Green_Peace (2015) Policy briefing Gene-editing of plants—GM through the back door? http://www.greenpeace.org/eu-unit/Global/eu-unit/reports-briefings/2015/Greenpeace_Gene-editing_30112015%20-%202.pdf. Accessed 4 Mar 2016
  25. Hartung F, Schiemann J (2014) Precise plant breeding using new genome editing techniques: opportunities, safety and regulation in the EU. Plant J Cell Mol Biol 78:742–752CrossRefGoogle Scholar
  26. Hashmi U, Shafqat S, Khan F, Majid M, Hussain H, Kazi AG, John R, Ahmad P (2015) Plant exomics: concepts, applications and methodologies in crop improvement. Plant Signal Behav 10:e976152CrossRefPubMedGoogle Scholar
  27. Haun W, Coffman A, Clasen BM, Demorest ZL, Lowy A, Ray E, Retterath A, Stoddard T, Juillerat A, Cedrone F, Mathis L, Voytas DF, Zhang F (2014) Improved soybean oil quality by targeted mutagenesis of the fatty acid desaturase 2 gene family. Plant Biotechnol J 12:934–940CrossRefPubMedGoogle Scholar
  28. Hsu PD, Lander ES, Zhang F (2014) Development and applications of CRISPR-Cas9 for genome engineering. Cell 157:1262–1278CrossRefPubMedPubMedCentralGoogle Scholar
  29. Huang S, Weigel D, Beachy RN, Li J (2016) A proposed regulatory framework for genome-edited crops. Nat Genet 48:109–111CrossRefPubMedGoogle Scholar
  30. IFOAM_EU (2015) New Plant Breeding Techniques Position paper. http://www.ifoam-eu.org/sites/default/files/ifoameu_policy_npbts_position_final_20151210.pdf. Accessed 4 Mar 2016
  31. Ito Y, Nishizawa-Yokoi A, Endo M, Mikami M, Toki S (2015) CRISPR/Cas9-mediated mutagenesis of the RIN locus that regulates tomato fruit ripening. Biochem Biophys Res Commun 467:76–82CrossRefPubMedGoogle Scholar
  32. Joung JK (2015) Unwanted mutations: standards needed for gene-editing errors. Nature 523:158CrossRefPubMedGoogle Scholar
  33. Joung JK, Sander JD (2013) TALENs: a widely applicable technology for targeted genome editing. Nat Rev Mol Cell Biol 14:49–55CrossRefPubMedGoogle Scholar
  34. Kershen DL (2015) Sustainability Council of New Zealand Trust v The Environmental Protection Authority: gene Editing Technologies and the Law. GM Crops Food. doi: 10.1080/21645698.2015.1122859 PubMedGoogle Scholar
  35. Kim D, Bae S, Park J, Kim E, Kim S, Yu HR, Hwang J, Kim JI, Kim JS (2015) Digenome-seq: genome-wide profiling of CRISPR-Cas9 off-target effects in human cells. Nature methods 12:237–243CrossRefPubMedGoogle Scholar
  36. Kleinstiver BP, Pattanayak V, Prew MS, Tsai SQ, Nguyen NT, Zheng Z, Keith Joung J (2016) High-fidelity CRISPR-Cas9 nucleases with no detectable genome-wide off-target effects. Nature 529:490–495CrossRefPubMedGoogle Scholar
  37. Kling J (2014) Labeling for better or worse. Nat Biotech 32:1180–1183CrossRefGoogle Scholar
  38. Klug A (2010) The discovery of zinc fingers and their applications in gene regulation and genome manipulation. Annu Rev Biochem 79:213–231CrossRefPubMedGoogle Scholar
  39. Lemaire O, Moneyron A, Masson JE (2010) “Interactive technology assessment” and beyond: the field trial of genetically modified grapevines at INRA-Colmar. PLoS Biol 8:e1000551CrossRefPubMedPubMedCentralGoogle Scholar
  40. Li T, Liu B, Spalding MH, Weeks DP, Yang B (2012) High-efficiency TALEN-based gene editing produces disease-resistant rice. Nat Biotechnol 30:390–392CrossRefPubMedGoogle Scholar
  41. Li Y, Hallerman EM, Liu Q, Wu K, Peng Y (2015) The development and status of Bt rice in China. Plant Biotechnol J. doi: 10.1111/pbi.12464 Google Scholar
  42. Lu Y, Wu K, Jiang Y, Xia B, Li P, Feng H, Wyckhuys KA, Guo Y (2010) Mirid bug outbreaks in multiple crops correlated with wide-scale adoption of Bt cotton in China. Science (New York, NY) 328:1151–1154CrossRefGoogle Scholar
  43. Lucht JM (2015) Public acceptance of plant biotechnology and GM crops. Viruses 7:4254–4281CrossRefPubMedPubMedCentralGoogle Scholar
  44. Ma L, Zhu F, Li Z, Zhang J, Li X, Dong J, Wang T (2015) TALEN-Based mutagenesis of lipoxygenase LOX3 enhances the storage tolerance of rice (Oryza sativa) seeds. PLoS One 10:e0143877CrossRefPubMedPubMedCentralGoogle Scholar
  45. Marshall A (2007) GM soybeans and health safety–a controversy reexamined. Nat Biotechnol 25:981–987CrossRefPubMedGoogle Scholar
  46. Nagamangala Kanchiswamy C, Sargent DJ, Velasco R, Maffei ME, Malnoy M (2015a) Looking forward to genetically edited fruit crops. Trends Biotechnol 33:62–64CrossRefPubMedGoogle Scholar
  47. Nagamangala Kanchiswamy C, Malnoy M, Velasco R, Kim JS, Viola R (2015b) Non-GMO genetically edited crop plants. Trends Biotechnol 33:489–491CrossRefGoogle Scholar
  48. Pauwels K, De Keersmaecker SCJ, De Schrijver A, du Jardin P, Roosens NHC, Herman P (2015) Next-generation sequencing as a tool for the molecular characterisation and risk assessment of genetically modified plants: added value or not? Trends Food Sci Technol 45:319–326CrossRefGoogle Scholar
  49. Ramessar K, Capell T, Twyman RM, Quemada H, Christou P (2008) Trace and traceability—a call for regulatory harmony. Nat Biotechnol 26:975–978CrossRefPubMedGoogle Scholar
  50. Ran FA, Hsu PD, Lin CY, Gootenberg JS, Konermann S, Trevino AE, Scott DA, Inoue A, Matoba S, Zhang Y, Zhang F (2013) Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell 154:1380–1389CrossRefPubMedPubMedCentralGoogle Scholar
  51. Romeis J, McLean MA, Shelton AM (2013) When bad science makes good headlines: Bt maize and regulatory bans. Nat Biotechnol 31:386–387CrossRefPubMedGoogle Scholar
  52. Ryffel GU (2014) Transgene flow: facts, speculations and possible countermeasures. GM Crops Food 5:249–258CrossRefPubMedGoogle Scholar
  53. Shan Q, Wang Y, Li J, Zhang Y, Chen K, Liang Z, Zhang K, Liu J, Xi JJ, Qiu JL, Gao C (2013) Targeted genome modification of crop plants using a CRISPR-Cas system. Nat Biotechnol 31:686–688CrossRefPubMedGoogle Scholar
  54. Shan Q, Zhang Y, Chen K, Zhang K, Gao C (2015) Creation of fragrant rice by targeted knockout of the OsBADH2 gene using TALEN technology. Plant Biotechnol J 13:791–800CrossRefPubMedGoogle Scholar
  55. Siegrist M (1999) A Causal model explaining the perception and acceptance of gene technology. J Appl Soc Psychol 29:2093–2106CrossRefGoogle Scholar
  56. Siegrist M, Connor M, Keller C (2012) Trust, confidence, procedural fairness, outcome fairness, moral conviction, and the acceptance of GM field experiments. Risk Anal Off Publ Soc Risk Anal 32:1394–1403CrossRefGoogle Scholar
  57. Tan S, Evans RR, Dahmer ML, Singh BK, Shaner DL (2005) Imidazolinone-tolerant crops: history, current status and future. Pest Manag Sci 61:246–257CrossRefPubMedGoogle Scholar
  58. Tanaka Y (2004) Major psycological facotors affecting acceptance of gene-recombination technology. Risk Anal 24:1575–1583CrossRefPubMedGoogle Scholar
  59. The_Convention_on_Biological_Diversity (2016) The Cartagena Protocol on Biosafety https://bch.cbd.int/protocol/. Accessed 19 Jan 2016
  60. The_New_Zealand_Environmental_Protection_Authority (2015) Consultation on wording of ‘organisms not genetically modified’ regulations in the Hazardous Substances and New Organisms Act. http://www.epa.govt.nz/consultations/new-organisms/Pages/consultation-organisms-not-genetically-modified-regulations.aspx. Accessed 19 Jan 2016
  61. The_US_Library_of_Congress (2014a) Restrictions on Genetically Modified Organisms: New Zealand. http://www.loc.gov/law/help/restrictions-on-gmos/new-zealand.php. Accessed 19 Jan 2016
  62. The_US_Library_of_Congress (2014b ) Restrictions on Genetically Modified Organisms: Japan. http://www.loc.gov/law/help/restrictions-on-gmos/japan.php. Accessed 19 Jan 2016
  63. Tsai SQ, Zheng Z, Nguyen NT, Liebers M, Topkar VV, Thapar V, Wyvekens N, Khayter C, Iafrate AJ, Le LP, Aryee MJ, Joung JK (2015) GUIDE-seq enables genome-wide profiling of off-target cleavage by CRISPR-Cas nucleases. Nat Biotechnol 33:187–197CrossRefPubMedGoogle Scholar
  64. Tsukaya H (2013) Design for controllability. EMBO Rep 14:3CrossRefPubMedGoogle Scholar
  65. Voytas DF, Gao C (2014) Precision genome engineering and agriculture: opportunities and regulatory challenges. PLoS Biol 12:e1001877CrossRefPubMedPubMedCentralGoogle Scholar
  66. Waltz E (2015a) Nonbrowning GM apple cleared for market. Nat Biotechnol 33:326–327CrossRefPubMedGoogle Scholar
  67. Waltz E (2015b) USDA approves next-generation GM potato. Nat Biotechnol 33:12–13CrossRefPubMedGoogle Scholar
  68. Wang Y, Cheng X, Shan Q, Zhang Y, Liu J, Gao C, Qiu JL (2014) Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nat Biotechnol 32:947–951CrossRefPubMedGoogle Scholar
  69. Weeks DP, Spalding MH, Yang B (2015) Use of designer nucleases for targeted gene and genome editing in plants. Plant Biotechnol J. doi: 10.1111/pbi.12448: PubMedGoogle Scholar
  70. Whelan AI, Lema MA (2015) Regulatory framework for gene editing and other new breeding techniques (NBTs) in Argentina. GM Crops Food. doi: 10.1080/21645698.21642015.21114698 PubMedGoogle Scholar
  71. Wolt JD, Wang K, Yang B (2015) The regulatory status of genome-edited crops. Plant Biotechnol J. doi: 10.1111/pbi.12444: PubMedGoogle Scholar
  72. Woo JW, Kim J, Kwon SI, Corvalan C, Cho SW, Kim H, Kim SG, Kim ST, Choe S, Kim JS (2015) DNA-free genome editing in plants with preassembled CRISPR-Cas9 ribonucleoproteins. Nat Biotechnol 33:1162–1164CrossRefPubMedGoogle Scholar
  73. Wunderlich S, Gatto KA (2015) Consumer perception of genetically modified organisms and sources of information. Adv Nutr (Bethesda, Md) 6:842–851CrossRefGoogle Scholar
  74. Zdziarski IM, Edwards JW, Carman JA, Haynes JI (2014) GM crops and the rat digestive tract: a critical review. Environ Int 73:423–433CrossRefPubMedGoogle Scholar
  75. Zetsche B, Gootenberg JS, Abudayyeh OO, Slaymaker IM, Makarova KS, Essletzbichler P, Volz SE, Joung J, van der Oost J, Regev A, Koonin EV, Zhang F (2015) Cpf1 Is a Single RNA-Guided Endonuclease of a Class 2 CRISPR-Cas System. Cell 163:759–771CrossRefPubMedGoogle Scholar
  76. Zhang H, Zhang J, Wei P, Zhang B, Gou F, Feng Z, Mao Y, Yang L, Zhang H, Xu N, Zhu JK (2014) The CRISPR/Cas9 system produces specific and homozygous targeted gene editing in rice in one generation. Plant Biotechnol J 12:797–807CrossRefPubMedGoogle Scholar
  77. Zhou J, Peng Z, Long J, Sosso D, Liu B, Eom JS, Huang S, Liu S, Vera Cruz C, Frommer WB, White FF, Yang B (2015) Gene targeting by the TAL effector PthXo2 reveals cryptic resistance gene for bacterial blight of rice. Plant J Cell Mol Biol 82:632–643CrossRefGoogle Scholar
  78. Zilberman D, Kaplan S, Kim E, Hochman G, Graff G (2013) Continents divided: understanding differences between Europe and North America in acceptance of GM crops. GM Crops Food 4:202–208CrossRefPubMedGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Office of Health and SafetyHokkaido UniversitySapporoJapan

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