1932

Abstract

The food industry faces a 2050 deadline for the advancement and expansion of the food supply chain to support the world's growing population. Improvements are needed across crops, livestock, and microbes to achieve this goal. Since 2005, researchers have been attempting to make the necessary strides to reach this milestone, but attempts have fallen short. With the introduction of clustered regularly interspaced short palindromic repeats (CRISPRs) and CRISPR-associated (Cas) proteins, the food production field is now able to achieve some of its most exciting advancements since the Green Revolution. This review introduces the concept of applying CRISPR-Cas technology as a genome-editing tool for use in the food supply chain, focusing on its implementation to date in crop, livestock, and microbe production, advancement of products to market, and regulatory and societal hurdles that need to be overcome.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-food-032818-121204
2019-03-25
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/food/10/1/annurev-food-032818-121204.html?itemId=/content/journals/10.1146/annurev-food-032818-121204&mimeType=html&fmt=ahah

Literature Cited

  1. Acquaah G 2009. Principles of Plant Genetics and Breeding Hoboken, NJ: Wiley-Blackwell
  2. Altenbuchner J 2016. Editing of the Bacillus subtilis genome by the CRISPR-Cas9 System. Appl. Environ. Microbiol. 82:5421–27
    [Google Scholar]
  3. Andersson AF, Banfield JF 2008. Virus population dynamics and acquired virus resistance in natural microbial communities. Science 320:1047–50
    [Google Scholar]
  4. Andersson M, Turesson H, Nicolia A, Fält A-S, Samuelsson M, Hofvander P 2017. Efficient targeted multiallelic mutagenesis in tetraploid potato (Solanum tuberosum) by transient CRISPR-Cas9 expression in protoplasts. Plant Cell Rep 36:117–28
    [Google Scholar]
  5. Araki M, Ishii T 2015. Towards social acceptance of plant breeding by genome editing. Trends Plant Sci 20:145–49
    [Google Scholar]
  6. Armin S, Felix W, Jacqueline B, Holger P, David E 2017. Towards CRISPR/Cas crops: bringing together genomics and genome editing. New Phytol 216:682–98
    [Google Scholar]
  7. Barrangou R 2015. Diversity of CRISPR-Cas immune systems and molecular machines. Genome Biol 16:247
    [Google Scholar]
  8. Barrangou R, Coûté-Monvoisin A-C, Stahl B, Chavichvily I, Damange F et al. 2013. Genomic impact of CRISPR immunization against bacteriophages. Biochem. Soc. Trans. 41:1383–91
    [Google Scholar]
  9. Barrangou R, Doudna JA 2016. Applications of CRISPR technologies in research and beyond. Nat. Biotechnol. 34:933–41
    [Google Scholar]
  10. Barrangou R, Fremaux C, Deveau H, Richards M, Boyaval P et al. 2007. CRISPR provides acquired resistance against viruses in prokaryotes. Science 315:1709–12
    [Google Scholar]
  11. Barrangou R, Horvath P 2012. CRISPR: new horizons in phage resistance and strain identification. Annu. Rev. Food Sci. Technol. 3:143–62
    [Google Scholar]
  12. Barrangou R, Horvath P 2017. A decade of discovery: CRISPR functions and applications. Nat. Microbiol. 2:17092
    [Google Scholar]
  13. Beisel CL, Gomaa AA, Barrangou R 2014. A CRISPR design for next-generation antimicrobials. Genome Biol 15:516
    [Google Scholar]
  14. Biot-Pelletier D, Martin VJJ 2016. Seamless site-directed mutagenesis of the Saccharomyces cerevisiae genome using CRISPR-Cas9. J. Biol. Eng. 10:6
    [Google Scholar]
  15. Bomgardner MM 2017. A new toolbox for better crops. Chem. Eng. News 95:30–34
    [Google Scholar]
  16. Bortesi L, Fischer R 2015. The CRISPR/Cas9 system for plant genome editing and beyond. Biotechnol. Adv. 33:41–52
    [Google Scholar]
  17. Brooks C, Nekrasov V, Lippman ZB, Van Eck J 2014. Efficient gene editing in tomato in the first generation using the clustered regularly interspaced short palindromic repeats/CRISPR-associated9 system. Plant Physiol 166:1292–97
    [Google Scholar]
  18. Brouns SJJ, Jore MM, Lundgren M, Westra ER, Slijkhuis RJH et al. 2008. Small CRISPR RNAs guide antiviral defense in prokaryotes. Science 321:960–64
    [Google Scholar]
  19. Carlson DF, Lancto CA, Zang B, Kim E-S, Walton M et al. 2016. Production of hornless dairy cattle from genome-edited cell lines. Nat. Biotechnol. 34:479–81
    [Google Scholar]
  20. Carte J, Christopher RT, Smith JT, Olson S, Barrangou R et al. 2014. The three major types of CRISPR-Cas systems function independently in CRISPR RNA biogenesis in Streptococcus thermophilus. Mol. Microbiol 93:98–112
    [Google Scholar]
  21. Chen B, Gilbert LA, Cimini BA, Schnitzbauer J, Zhang W et al. 2013. Dynamic imaging of genomic loci in living human cells by an optimized CRISPR/Cas system. Cell 155:1479–91
    [Google Scholar]
  22. Cleto S, Jensen JVK, Wendisch VF, Lu TK 2016. Corynebacterium glutamicum metabolic engineering with CRISPR interference (CRISPRi). ACS Synth. Biol. 5:375–85
    [Google Scholar]
  23. Cong L, Ran FA, Cox D, Lin S, Barretto R et al. 2013. Multiplex genome engineering using CRISPR/Cas systems. Science 339:6121819–23
    [Google Scholar]
  24. Crawley AB, Henriksen ED, Stout E, Brandt K, Barrangou R 2018. Characterizing the activity of abundant, diverse and active CRISPR-Cas systems in lactobacilli. Sci. Rep. 8:11544
    [Google Scholar]
  25. Cui K, Shoemaker SP 2018. Public perception of genetically-modified (GM) food: a Nationwide Chinese Consumer Study. npj Sci. Food 2:10
    [Google Scholar]
  26. Davis V 2018. GMO labeling makes public more likely to trust food companies. Science362
  27. Deltcheva E, Chylinski K, Sharma CM, Gonzales K, Chao Y et al. 2011. CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III. Nature 471:602–7
    [Google Scholar]
  28. Deveau H, Barrangou R, Garneau JE, Labonté J, Fremaux C et al. 2008. Phage response to CRISPR-encoded resistance in Streptococcus thermophilus. J. Bacteriol 190:1390–400
    [Google Scholar]
  29. Doudna JA, Charpentier E 2014. The new frontier of genome engineering with CRISPR-Cas9. Science 346:62131258096
    [Google Scholar]
  30. Edvardsen RB, Leininger S, Kleppe L, Skaftnesmo KO, Wargelius A 2014. Targeted mutagenesis in Atlantic salmon (Salmo salar L.) using the CRISPR/Cas9 system induces complete knockout individuals in the F0 generation. PLOS ONE 9:e108622
    [Google Scholar]
  31. Fletcher R 2017. Norwegian legislative debate offers hope for gene editing in aquaculture. The Fish Site Dec. 6. https://thefishsite.com/articles/norwegian-legislative-debate-offers-hope-for-gene-editing-in-aquaculture
  32. Funk C, Kennedy B 2016. The New Food Fights: U.S. Public Divides Over Food Science Washington, DC: Pew Research Center
  33. Gaj T, Gersbach CA, Barbas CF 2013. ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. Trends Biotechnol 31:397–405
    [Google Scholar]
  34. Gao Y, Wu H, Wang Y, Liu X, Chen L et al. 2017. Single Cas9 nickase induced generation of NRAMP1 knockin cattle with reduced off-target effects. Genome Biol 18:13
    [Google Scholar]
  35. Gilbert LA, Horlbeck MA, Adamson B, Villalta JE, Chen Y et al. 2014. Genome-scale CRISPR-mediated control of gene repression and activation. Cell 159:647–61
    [Google Scholar]
  36. Gomaa AA, Klumpe HE, Luo ML, Selle K, Barrangou R, Beisel CL 2014. Programmable removal of bacterial strains by use of genome-targeting CRISPR-Cas systems. mBio 5:e00928–13
    [Google Scholar]
  37. Gomez MA, Lin ZD, Moll T, Luebbert C, Chauhan RD et al. 2018. Simultaneous CRISPR/Cas9-mediated editing of cassava eIF4E isoforms nCBP-1 and nCBP-2 reduces cassava brown streak disease symptom severity and incidence. Plant Biotechnol. J In press
  38. Hale CR, Zhao P, Olson S, Duff MO, Graveley BR et al. 2009. RNA-guided RNA cleavage by a CRISPR RNA-Cas protein complex. Cell 139:945–56
    [Google Scholar]
  39. Hilton IB, D'Ippolito AM, Vockley CM, Thakore PI, Crawford GE et al. 2015. Epigenome editing by a CRISPR-Cas9-based acetyltransferase activates genes from promoters and enhancers. Nat. Biotechnol. 33:510
    [Google Scholar]
  40. Horvath P, Barrangou R 2010. CRISPR/Cas, the immune system of Bacteria and Archaea. Science 327:167–70
    [Google Scholar]
  41. Horvath P, Romero DA, Coûté-Monvoisin A-C, Richards M, Deveau H et al. 2008. Diversity, activity, and evolution of CRISPR loci in Streptococcus thermophilus.J. Bacteriol 190:1401–12
    [Google Scholar]
  42. Hsu PD, Scott DA, Weinstein JA, Ran FA, Konermann S et al. 2013. DNA targeting specificity of RNA-guided Cas9 nucleases. Nat. Biotechnol. 31:827–32
    [Google Scholar]
  43. Ishii T, Araki M 2016. Consumer acceptance of food crops developed by genome editing. Plant Cell Rep 35:1507–18
    [Google Scholar]
  44. Ishino Y, Shinagawa H, Makino K, Amemura M, Nakata A 1987. Nucleotide sequence of the iap gene, responsible for alkaline phosphatase isozyme conversion in Escherichia coli, and identification of the gene product. J. Bacteriol. 169:5429–33
    [Google Scholar]
  45. Jiang W, Zhou H, Bi H, Fromm M, Yang B, Weeks DP 2013. Demonstration of CRISPR/Cas9/sgRNA-mediated targeted gene modification in Arabidopsis, tobacco, sorghum and rice. Nucleic Acids Res. 41:e188
    [Google Scholar]
  46. Jiang Y, Chen B, Duan C, Sun B, Yang J, Yang S 2015. Multigene editing in the Escherichia coli genome via the CRISPR-Cas9 system. Appl. Environ. Microbiol. 81:2506–14
    [Google Scholar]
  47. 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]
  48. Karkute SG, Singh AK, Gupta OP, Singh PM, Singh B 2017. CRISPR/Cas9 mediated genome engineering for improvement of horticultural crops. Front. Plant Sci. 8:1635
    [Google Scholar]
  49. Khalil K, Elayat M, Khalifa E, Daghash S, Elaswad A et al. 2017. Generation of myostatin gene-edited channel catfish (Ictalurus punctatus) via zygote injection of CRISPR/Cas9 system. Sci. Rep. 7:7301
    [Google Scholar]
  50. Khan MHU, Khan SU, Muhammad A, Hu L, Yang Y, Fan C 2018. Induced mutation and epigenetics modification in plants for crop improvement by targeting CRISPR/Cas9 technology. J. Cell. Physiol. 233:4578–94
    [Google Scholar]
  51. Koonin EV, Makarova KS, Zhang F 2017. Diversity, classification and evolution of CRISPR-Cas systems. Curr. Opin. Microbiol. 37:67–78
    [Google Scholar]
  52. LaManna CM, Barrangou R 2018. Enabling the rise of a CRISPR world. CRISPR J 1:205–8
    [Google Scholar]
  53. Larson MH, Gilbert LA, Wang X, Lim WA, Weissman JS, Qi LS 2013. CRISPR interference (CRISPRi) for sequence-specific control of gene expression. Nat. Protoc. 8:2180
    [Google Scholar]
  54. Ledford H 2015. Salmon is first transgenic animal to win US approval for food. Nature http://doi.org/10.1038/nature.2015.18838
    [Crossref]
  55. Liu J, Zhou Y, Qi X, Chen J, Chen W et al. 2017. CRISPR/Cas9 in zebrafish: an efficient combination for human genetic diseases modeling. Hum. Genet. 136:1–12
    [Google Scholar]
  56. Liu Q, Gao R, Li J, Lin L, Zhao J et al. 2017. Development of a genome-editing CRISPR/Cas9 system in thermophilic fungal Myceliophthora species and its application to hyper-cellulase production strain engineering. Biotechnol. Biofuels 10:1
    [Google Scholar]
  57. Liu SJ, Horlbeck MA, Cho SW, Birk HS, Malatesta M et al. 2017. CRISPRi-based genome-scale identification of functional long noncoding RNA loci in human cells. Science 355:6320aah7111
    [Google Scholar]
  58. Lucht JM 2015. Public acceptance of plant biotechnology and GM crops. Viruses 7:4254–81
    [Google Scholar]
  59. Ma X, Mau M, Sharbel TF 2018. Genome editing for global food security. Trends Biotechnol 36:123–27
    [Google Scholar]
  60. Makarova KS, Aravind L, Wolf YI, Koonin EV 2011.a Unification of Cas protein families and a simple scenario for the origin and evolution of CRISPR-Cas systems. Biol. Direct 6:38
    [Google Scholar]
  61. Makarova KS, Haft DH, Barrangou R, Brouns SJJ, Charpentier E et al. 2011.b Evolution and classification of the CRISPR–Cas systems. Nat. Rev. Microbiol. 9:467–77
    [Google Scholar]
  62. Makarova KS, Wolf YI, Alkhnbashi OS, Costa F, Shah SA et al. 2015. An updated evolutionary classification of CRISPR–Cas systems. Nat. Rev. Microbiol. 13:722–36
    [Google Scholar]
  63. Mali P, Yang L, Esvelt KM, Aach J, Guell M et al. 2013. RNA-guided human genome engineering via Cas9. Science 339:823–26
    [Google Scholar]
  64. Malyska A, Bolla R, Twardowski T 2016. The role of public opinion in shaping trajectories of agricultural biotechnology. Trends Biotechnol 34:530–34
    [Google Scholar]
  65. Marraffini LA, Sontheimer EJ 2008. CRISPR interference limits horizontal gene transfer in staphylococci by targeting DNA. Science 322:1843–45
    [Google Scholar]
  66. Marraffini LA, Sontheimer EJ 2010. Self versus non-self discrimination during CRISPR RNA-directed immunity. Nature 463:568
    [Google Scholar]
  67. Maurer A 2017. Syngenta acquires non-exclusive license to use CRISPR-Cas9 gene-editing for agriculture applications Press Release, Novemb. 3. https://www.ncbiotech.org/news/syngenta-acquires-non-exclusive-license-use-crispr-cas9-gene-editing-agriculture-applications
  68. McCaughey T, Sanfilippo PG, Gooden GE, Budden DM, Fan L et al. 2016. A global social media survey of attitudes to human genome editing. Cell Stem Cell 18:569–72
    [Google Scholar]
  69. McFadden BR 2017. The unknowns and possible implications of mandatory labeling. Trends Biotechnol 35:1–3
    [Google Scholar]
  70. Miao C, Xiao L, Hua K, Zou C, Zhao Y et al. 2018. Mutations in a subfamily of abscisic acid receptor genes promote rice growth and productivity. PNAS 115:236058–63
    [Google Scholar]
  71. Nagaraju S, Davies NK, Walker DJF, Köpke M, Simpson SD 2016. Genome editing of Clostridium autoethanogenum using CRISPR/Cas9. Biotechnol. Biofuels 9:219
    [Google Scholar]
  72. Nekrasov V, Wang C, Win J, Lanz C, Weigel D, Kamoun S 2017. Rapid generation of a transgene-free powdery mildew resistant tomato by genome deletion. Sci. Rep. 7:482
    [Google Scholar]
  73. Nishitani C, Hirai N, Komori S, Wada M, Okada K et al. 2016. Efficient genome editing in apple using a CRISPR/Cas9 system. Sci. Rep. 6:31481
    [Google Scholar]
  74. Nødvig CS, Hoof JB, Kogle ME, Jarczynska ZD, Lehmbeck J et al. 2018. Efficient oligo nucleotide mediated CRISPR-Cas9 gene editing in Aspergilli. Fungal Genet. Biol. 115:78–89
    [Google Scholar]
  75. Nødvig CS, Nielsen JB, Kogle ME, Mortensen UH 2015. A CRISPR-Cas9 system for genetic engineering of filamentous fungi. PLOS ONE 10:e0133085
    [Google Scholar]
  76. Oh J-H, van Pijkeren J-P 2014. CRISPR–Cas9-assisted recombineering in Lactobacillus reuteri. Nucleic Acids Res 42:e131
    [Google Scholar]
  77. Oishi I, Yoshii K, Miyahara D, Kagami H, Tagami T 2016. Targeted mutagenesis in chicken using CRISPR/Cas9 system. Sci. Rep. 6:23980
    [Google Scholar]
  78. Pennisi E 2013. The CRISPR craze. Science 341:833–36
    [Google Scholar]
  79. Pohl C, Kiel JAKW, Driessen AJM, Bovenberg RAL, Nygård Y 2016. CRISPR/Cas9 based genome editing of Penicillium chrysogenum. ACS Synth. Biol 5:754–64
    [Google Scholar]
  80. Ramessar K, Capell T, Twyman RM, Quemada H, Christou P 2008. Trace and traceability—a call for regulatory harmony. Nat. Biotechnol. 26:975–78
    [Google Scholar]
  81. Ray DK, Mueller ND, West PC, Foley JA 2013. Yield trends are insufficient to double global crop production by 2050. PLOS ONE 8:e66428
    [Google Scholar]
  82. Rosenblum A 2018. Meet the woman using CRISPR to breed all-male “terminator cattle. MIT Technol. Rev https://www.technologyreview.com/s/609699/meet-the-woman-using-crispr-to-breed-all-male-terminator-cattle/
  83. Schuster M, Schweizer G, Reissmann S, Kahmann R 2016. Genome editing in Ustilago maydis using the CRISPR–Cas system. Fungal Genet. Biol. 89:3–9
    [Google Scholar]
  84. Selle K, Barrangou R 2015. CRISPR-based technologies and the future of food science. J. Food Sci. 80:R2367–72
    [Google Scholar]
  85. Selle K, Klaenhammer TR, Barrangou R 2015. CRISPR-based screening of genomic island excision events in bacteria. PNAS 112:8076–81
    [Google Scholar]
  86. Shan Q, Wang Y, Li J, Zhang Y, Chen K et al. 2013. Targeted genome modification of crop plants using a CRISPR-Cas system. Nat. Biotechnol. 31:686–88
    [Google Scholar]
  87. Shi J, Guo H, Wang H, Lafitte HR, Archibald RL et al. 2017. ARGOS8 variants generated by CRISPR‐Cas9 improve maize grain yield under field drought stress conditions. Plant Biotechnol. J. 15:207–16
    [Google Scholar]
  88. Sternberg SH, Redding S, Jinek M, Greene EC, Doudna JA 2014. DNA interrogation by the CRISPR RNA-guided endonuclease Cas9. Nature 507:62–67
    [Google Scholar]
  89. Stokstad E 2018. European court ruling raises hurdles for CRISPR crops. Science. https://doi.org/10.1126/science.aau8986
    [Crossref]
  90. Teater B 2018. Five company success stories highlighted at CED Conference Press Release, Febr. 18. https://www.ncbiotech.org/news/five-company-success-stories-highlighted-ced-conference
  91. Telugu BP, Park KE, Park CH 2017. Genome editing and genetic engineering in livestock for advancing agricultural and biomedical applications. Mamm. Genome 28:338–47
    [Google Scholar]
  92. Tilman D, Balzer C, Hill J, Befort BL 2011. Global food demand and the sustainable intensification of agriculture. PNAS 108:20260–64
    [Google Scholar]
  93. Tsai SQ, Wyvekens N, Khayter C, Foden JA, Thapar V et al. 2014. Dimeric CRISPR RNA-guided FokI nucleases for highly specific genome editing. Nat. Biotechnol. 32:569
    [Google Scholar]
  94. Tyson GW, Banfield JF 2008. Rapidly evolving CRISPRs implicated in acquired resistance of microorganisms to viruses. Environ. Microbiol. 10:200–07
    [Google Scholar]
  95. Upadhyay SK, Kumar J, Alok A, Tuli R 2013. RNA-guided genome editing for target gene mutations in wheat. Genes Genomes Genet 3:2233–38
    [Google Scholar]
  96. USDA (US Dep. Agric.). 2018.a Secretary Perdue issues USDA statement on plant breeding innovation Press Release 0070.18, March 28. https://www.usda.gov/media/press-releases/2018/03/28/secretary-perdue-issues-usda-statement-plant-breeding-innovation
  97. USDA (US Dep. Agric.). 2018.b Agricultural projections to 2027 Rep. OCE-2018–1, Interag. Agric. Proj. Comm Washington, DC:
  98. Van Eenennaam AL 2018. The importance of a novel product risk-based trigger for gene-editing regulation in food animal species. CRISPR J 1:101–06
    [Google Scholar]
  99. Vigentini I, Gebbia M, Belotti A, Foschino R, Roth FP 2017. CRISPR/Cas9 system as a valuable genome editing tool for wine yeasts with application to decrease urea production. Front. Microbiol. 8:2194
    [Google Scholar]
  100. Vyas VK, Barrasa MI, Fink GR 2015. A Candida albicans CRISPR system permits genetic engineering of essential genes and gene families. Sci. Adv. 1:3e1500248
    [Google Scholar]
  101. Waltz E 2016. Gene-edited CRISPR mushroom escapes US regulation. Nature 532:293
    [Google Scholar]
  102. Waltz E 2018. With a free pass, CRISPR-edited plants reach market in record time. Nat. Biotechnol. 36:6–7
    [Google Scholar]
  103. Wang B 2015. Disruptive CRISPR gene therapy is 150 times cheaper than zinc fingers and CRISPR is faster and more precise. Next Big Future https://www.nextbigfuture.com/2015/06/disruptive-crispr-gene-therapy-is-150.html
  104. Wolt JD, Yang B, Wang K, Spalding MH 2016. Regulatory aspects of genome-edited crops. In Vitro Cell. Dev. Biol. Plant 52:349–53
    [Google Scholar]
  105. Yang L, Güell M, Niu D, George H, Lesha E et al. 2015. Genome-wide inactivation of porcine endogenous retroviruses (PERVs). Science 350:62641101–4
    [Google Scholar]
  106. Yupeng C, Li C, Xiujie L, Chen G, Shi S et al. 2018. CRISPR/Cas9‐mediated targeted mutagenesis of GmFT2a delays flowering time in soya bean. Plant Biotechnol. J. 16:176–85
    [Google Scholar]
  107. Zheng Q, Lin J, Huang J, Zhang H, Zhang R et al. 2017. Reconstitution of UCP1 using CRISPR/Cas9 in the white adipose tissue of pigs decreases fat deposition and improves thermogenic capacity. PNAS 114:E9474–82
    [Google Scholar]
  108. Zoephel J, Randau L 2013. RNA-Seq analyses reveal CRISPR RNA processing and regulation patterns. Biochem. Soc. Trans. 41:1459–63
    [Google Scholar]
/content/journals/10.1146/annurev-food-032818-121204
Loading
/content/journals/10.1146/annurev-food-032818-121204
Loading

Data & Media 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