1932

Abstract

Enhanced agricultural production through innovative breeding technology is urgently needed to increase access to nutritious foods worldwide. Recent advances in CRISPR/Cas genome editing enable efficient targeted modification in most crops, thus promising to accelerate crop improvement. Here, we review advances in CRISPR/Cas9 and its variants and examine their applications in plant genome editing and related manipulations. We highlight base-editing tools that enable targeted nucleotide substitutions and describe the various delivery systems, particularly DNA-free methods, that have linked genome editing with crop breeding. We summarize the applications of genome editing for trait improvement, development of techniques for fine-tuning gene regulation, strategies for breeding virus resistance, and the use of high-throughput mutant libraries. We outline future perspectives for genome editing in plant synthetic biology and domestication, advances in delivery systems, editing specificity, homology-directed repair, and gene drives. Finally, we discuss the challenges and opportunities for precision plant breeding and its bright future in agriculture.

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2019-04-29
2024-12-03
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Literature Cited

  1. 1.  Abudayyeh OO, Gootenberg JS, Essletzbichler P, Han S, Joung J et al. 2017. RNA targeting with CRISPR-Cas13. Nature 550:280–84
    [Google Scholar]
  2. 2.  Abudayyeh OO, Gootenberg JS, Konermann S, Joung J, Slaymaker IM et al. 2016. C2c2 is a single-component programmable RNA-guided RNA-targeting CRISPR effector. Science 353:aaf5573
    [Google Scholar]
  3. 3.  Ali Z, Abulfaraj A, Idris A, Ali S, Tashkandi M, Mahfouz M 2015. CRISPR/Cas9-mediated viral interference in plants. Genome Biol 16:238
    [Google Scholar]
  4. 4.  Ali Z, Ali S, Tashkandi M, Zaidi SS, Mahfouz MM 2016. CRISPR/Cas9-mediated immunity to geminiviruses: differential interference and evasion. Sci. Rep. 6:26912
    [Google Scholar]
  5. 5.  Andersson M, Turesson H, Nicolia A, Falt AS, 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]
  6. 6.  Andersson M, Turesson H, Olsson N, Falt AS, Ohlsson P et al. 2018. Genome editing in potato via CRISPR-Cas9 ribonucleoprotein delivery. Physiol. Plant. 164:378–84
    [Google Scholar]
  7. 7.  Baltes NJ, Hummel AW, Konecna E, Cegan R, Bruns AN et al. 2015. Conferring resistance to geminiviruses with the CRISPR–Cas prokaryotic immune system. Nat. Plants 1:15145
    [Google Scholar]
  8. 8.  Begemann MB, Gray BN, January E, Singer A, Kelser DC et al. 2017. Characterization and validation of a novel group of type V, class 2 nucleases for in vivo genome editing. bioRxiv 192799. https://doi.org/10.1101/192799
    [Crossref]
  9. 9.  Braatz J, Harloff HJ, Mascher M, Stein N, Himmelbach A, Jung C 2017. CRISPR-Cas9 targeted mutagenesis leads to simultaneous modification of different homoeologous gene copies in polyploid oilseed rape (Brassica napus). Plant Physiol 174:935–42
    [Google Scholar]
  10. 10.  Butler NM, Baltes NJ, Voytas DF, Douches DS 2016. Geminivirus-mediated genome editing in potato (Solanum tuberosum L.) using sequence-specific nucleases. Front. Plant Sci. 7:1045
    [Google Scholar]
  11. 11.  Butt H, Eid A, Ali Z, Atia MAM, Mokhtar MM et al. 2017. Efficient CRISPR/Cas9-mediated genome editing using a chimeric single-guide RNA molecule. Front. Plant Sci. 8:1441
    [Google Scholar]
  12. 12.  Cebrian-Serrano A, Davies B 2017. CRISPR-Cas orthologues and variants: optimizing the repertoire, specificity and delivery of genome engineering tools. Mamm. Genome. 28:247–61
    [Google Scholar]
  13. 13.  Čermák T, Baltes NJ, Čegan R, Zhang Y, Voytas DF 2015. High-frequency, precise modification of the tomato genome. Genome Biol 16:232
    [Google Scholar]
  14. 14.  Čermák T, Curtin SJ, Gil-Humanes J, Čegan R, Kono TJY et al. 2017. A multipurpose toolkit to enable advanced genome engineering in plants. Plant Cell 29:1196–217
    [Google Scholar]
  15. 15.  Chandrasekaran J, Brumin M, Wolf D, Leibman D, Klap C et al. 2016. Development of broad virus resistance in non-transgenic cucumber using CRISPR/Cas9 technology. Mol. Plant Pathol. 17:1140–53
    [Google Scholar]
  16. 16.  Chen B, Gilbert Luke A, Cimini Beth A, 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]
  17. 17.  Chen L, Li W, Katin-Grazzini L, Ding J, Gu X et al. 2018. A method for the production and expedient screening of CRISPR/Cas9-mediated non-transgenic mutant plants. Hortic. Res. 5:13
    [Google Scholar]
  18. 18.  Chen YY, Wang ZP, Ni HW, Xu Y, Chen QJ, Jiang LJ 2017. CRISPR/Cas9-mediated base-editing system efficiently generates gain-of-function mutations in Arabidopsis. Sci. China Life Sci 60:520–23
    [Google Scholar]
  19. 19.  Christian M, Čermák T, Doyle EL, Schmidt C, Zhang F et al. 2010. Targeting DNA double-strand breaks with TAL effector nucleases. Genetics 186:757–61
    [Google Scholar]
  20. 20.  Civáň P, Brown TA 2017. Origin of rice (Oryza sativa L.) domestication genes. Genet. Resour. Crop Evol. 64:1125–32
    [Google Scholar]
  21. 21.  Cong L, Ran FA, Cox D, Lin S, Barretto R, et al 2013. Multiplex genome engineering using CRISPR/Cas systems. Science 339:819–23
    [Google Scholar]
  22. 22.  Cox DBT, Gootenberg JS, Abudayyeh OO, Franklin B, Kellner MJ et al. 2017. RNA editing with CRISPR-Cas13. Science 358:1019–27
    [Google Scholar]
  23. 23.  Cunningham FJ, Goh NS, Demirer GS, Matos JL, Landry MP 2018. Nanoparticle-mediated delivery towards advancing plant genetic engineering. Trends Biotechnol 36:882–97
    [Google Scholar]
  24. 24.  Dahan-Meir T, Filler-Hayut S, Melamed-Bessudo C, Bocobza S, Czosnek H et al. 2018. Efficient in planta gene targeting in tomato using geminiviral replicons and the CRISPR/Cas9 system. Plant J 95:5–16
    [Google Scholar]
  25. 25.  Demirer GS, Zhang H, Matos JL, Goh N, Cunningham F et al. 2019. High aspect ratio nanomaterials enable delivery of functional genetic material without DNA integration in mature plants. Nat. Nanotechnol. https://doi.org/10.1038/s41565-019-0382-5
    [Crossref]
  26. 26.  Dominguez AA, Lim WA, Qi LS 2015. Beyond editing: repurposing CRISPR-Cas9 for precision genome regulation and interrogation. Nat. Rev. Mol. Cell Biol. 17:5–15
    [Google Scholar]
  27. 27.  Dong L, Li L, Liu C, Liu C, Shuaifeng G et al. 2018. Genome editing and double fluorescence proteins enable robust maternal haploid induction and identification in maize. Mol. Plant 11:1214–17
    [Google Scholar]
  28. 28.  Dreissig S, Schiml S, Schindele P, Weiss O, Rutten T et al. 2017. Live-cell CRISPR imaging in plants reveals dynamic telomere movements. Plant J 91:565–73
    [Google Scholar]
  29. 29.  Endo M, Mikami M, Toki S 2016. Biallelic gene targeting in rice. Plant Physiol 170:667–77
    [Google Scholar]
  30. 30.  Esvelt KM, Smidler AL, Catteruccia F, Church GM 2014. Concerning RNA-guided gene drives for the alteration of wild populations. eLife 3:e03401
    [Google Scholar]
  31. 31.  Feng Z, Mao Y, Xu N, Zhang B, Wei P et al. 2014. Multigeneration analysis reveals the inheritance, specificity, and patterns of CRISPR/Cas-induced gene modifications in Arabidopsis. PNAS 111:4632–37
    [Google Scholar]
  32. 32.  Gallego-Bartolomé J, Gardiner J, Liu W, Papikian A, Ghoshal B et al. 2018. Targeted DNA demethylation of the Arabidopsis genome using the human TET1 catalytic domain. PNAS 115:E2125–34
    [Google Scholar]
  33. 33.  Gao L, Cox DBT, Yan WX, Manteiga JC, Schneider MW et al. 2017. Engineered Cpf1 variants with altered PAM specificities. Nat. Biotechnol. 35:789–92
    [Google Scholar]
  34. 34.  Gao X, Chen J, Dai X, Zhang D, Zhao Y 2016. An effective strategy for reliably isolating heritable and Cas9-free Arabidopsis mutants generated by CRISPR/Cas9-mediated genome editing. Plant Physiol 171:1794–800
    [Google Scholar]
  35. 35.  Gao Y, Zhao Y 2013. Self-processing of ribozyme-flanked RNAs into guide RNAs in vitro and in vivo for CRISPR-mediated genome editing. J. Integr. Plant Biol. 56:343–49
    [Google Scholar]
  36. 36.  Gasiunas G, Barrangou R, Horvath P, Siksnys V 2012. Cas9-crRNA ribonucleoprotein complex mediates specific DNA cleavage for adaptive immunity in bacteria. PNAS 109:E2579–86
    [Google Scholar]
  37. 37.  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 551:464–71Explores an adenine base-editor (ABE) system that converts A to G in genomic DNA.
    [Google Scholar]
  38. 38.  Gehrke JM, Cervantes O, Clement MK, Wu Y, Zeng J et al. 2018. An APOBEC3A-Cas9 base editor with minimized bystander and off-target activities. Nat. Biotechnol. 36:977–82
    [Google Scholar]
  39. 39.  Gelvin SB 2010. Plant proteins involved in Agrobacterium-mediated genetic transformation. Annu. Rev. Phytopathol. 48:45–68
    [Google Scholar]
  40. 40.  Gil-Humanes J, Wang Y, Liang Z, Shan Q, Ozuna CV et al. 2017. High-efficiency gene targeting in hexaploid wheat using DNA replicons and CRISPR/Cas9. Plant J 89:1251–62
    [Google Scholar]
  41. 41.  Hamada H, Linghu Q, Nagira Y, Miki R, Taoka N, Imai R 2017. An in planta biolistic method for stable wheat transformation. Sci. Rep. 7:11443
    [Google Scholar]
  42. 42.  He Y, Zhu M, Wang L, Wu J, Wang Q et al. 2018. Programmed self-elimination of the CRISPR/Cas9 construct greatly accelerates the isolation of edited and transgene-free rice plants. Mol. Plant 11:P1210–13
    [Google Scholar]
  43. 43.  Hess GT, Tycko J, Yao D, Bassik MC 2017. Methods and applications of CRISPR-mediated base editing in eukaryotic genomes. Mol. Cell 68:26–43
    [Google Scholar]
  44. 44.  Hu JH, Miller SM, Geurts MH, Tang W, Chen L et al. 2018. Evolved Cas9 variants with broad PAM compatibility and high DNA specificity. Nature 556:57–63
    [Google Scholar]
  45. 45.  Huang J, Li J, Zhou J, Wang L, Yang S et al. 2018. Identifying a large number of high-yield genes in rice by pedigree analysis, whole-genome sequencing, and CRISPR-Cas9 gene knockout. PNAS 115:E7559–67
    [Google Scholar]
  46. 46.  Hummel AW, Chauhan RD, Cermak T, Mutka AM, Vijayaraghavan A et al. 2017. Allele exchange at the EPSPS locus confers glyphosate tolerance in cassava. Plant Biotechnol. J. 16:1275–82
    [Google Scholar]
  47. 47.  Iqbal Z, Sattar MN, Shafiq M 2016. CRISPR/Cas9: a tool to circumscribe cotton leaf curl disease. Front. Plant Sci. 7:475
    [Google Scholar]
  48. 48.  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. 467:76–82
    [Google Scholar]
  49. 49.  Jacobs TB, Zhang N, Patel D, Martin GB 2017. Generation of a collection of mutant tomato lines using pooled CRISPR libraries. Plant Physiol 174:2023–37
    [Google Scholar]
  50. 50.  Ji X, Si X, Zhang Y, Zhang H, Zhang F et al. 2018. Conferring DNA virus resistance with high specificity in plants using a virus-inducible genome editing system. Genome Biol 19:197
    [Google Scholar]
  51. 51.  Ji X, Zhang H, Zhang Y, Wang Y, Gao C 2015. Establishing a CRISPR-Cas-like immune system conferring DNA virus resistance in plants. Nat. Plants 1:15144
    [Google Scholar]
  52. 52.  Jiang F, Doudna JA 2017. CRISPR-Cas9 structures and mechanisms. Annu. Rev. Biophys. 46:505–29
    [Google Scholar]
  53. 53.  Jiang WZ, Henry IM, Lynagh PG, Comai L, Cahoon EB, Weeks DP 2017. Significant enhancement of fatty acid composition in seeds of the allohexaploid, Camelina sativa, using CRISPR/Cas9 gene editing. Plant Biotechnol. J. 15:648–57
    [Google Scholar]
  54. 54.  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 337:816–21Provides first demonstration that dual-transactivating crRNA:crRNA and a single RNA chimera can direct Cas9 to cleave double-strand DNA in vitro.
    [Google Scholar]
  55. 55.  Jusiak B, Cleto S, Perez-Piñera P, Lu TK 2016. Engineering synthetic gene circuits in living cells with CRISPR technology. Trends Biotechnol 34:535–47
    [Google Scholar]
  56. 56.  Kang BC, Yun JY, Kim ST, Shin Y, Ryu J et al. 2018. Precision genome engineering through adenine base editing in plants. Nat. Plants 4:427–431
    [Google Scholar]
  57. 57.  Khanday I, Skinner D, Yang B, Mercier R, Sundaresan V 2018. A male-expressed rice embryogenic trigger redirected for asexual propagation through seeds. Nature 565:91–95
    [Google Scholar]
  58. 58.  Kim D, Lim K, Kim ST, Yoon SH, Kim K et al. 2017. Genome-wide target specificities of CRISPR RNA-guided programmable deaminases. Nat. Biotechnol. 35:475–80
    [Google Scholar]
  59. 59.  Kim H, Kim ST, Ryu J, Kang BC, Kim JS, Kim SG 2017. CRISPR/Cpf1-mediated DNA-free plant genome editing. Nat. Commun. 8:14406
    [Google Scholar]
  60. 60.  Kim K, Ryu SM, Kim ST, Baek G, Kim D et al. 2017. Highly efficient RNA-guided base editing in mouse embryos. Nat. Biotechnol. 35:435–37
    [Google Scholar]
  61. 61.  Kleinstiver BP, Prew MS, Tsai SQ, Topkar VV, Nguyen NT et al. 2015. Engineered CRISPR-Cas9 nucleases with altered PAM specificities. Nature 523:481–85
    [Google Scholar]
  62. 62.  Komatsuda T, Pourkheirandish M, He C, Azhaguvel P, Kanamori H et al. 2007. Six-rowed barley originated from a mutation in a homeodomain-leucine zipper I-class homeobox gene. PNAS 104:1424–29
    [Google Scholar]
  63. 63.  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 533:420–24Explores base-editing technology that converts C to T in the genome without producing double-strand breaks.
    [Google Scholar]
  64. 64.  Koonin EV, Makarova KS, Zhang F 2017. Diversity, classification and evolution of CRISPR-Cas systems. Curr. Opin. Microbiol. 37:67–78
    [Google Scholar]
  65. 65.  Kungulovski G, Jeltsch A 2016. Epigenome editing: state of the art, concepts, and perspectives. Trends Genet 32:101–13
    [Google Scholar]
  66. 66.  Lacroix B, Citovsky V 2016. A functional bacterium-to-plant DNA transfer machinery of Rhizobium etli. PLOS Pathog 12:e1005502
    [Google Scholar]
  67. 67.  Leenay RT, Maksimchuk KR, Slotkowski RA, Agrawal RN, Gomaa AA et al. 2016. Identifying and visualizing functional PAM diversity across CRISPR-Cas systems. Mol. Cell 62:137–47
    [Google Scholar]
  68. 68.  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]
  69. 69.  Li C, Zong Y, Wang Y, Jin S, Zhang D et al. 2018. Expanded base editing in rice and wheat using a Cas9-adenosine deaminase fusion. Genome Biol 19:59
    [Google Scholar]
  70. 70.  Li J, Manghwar H, Sun L, Wang P, Wang G et al. 2018. Whole genome sequencing reveals rare off-target mutations and considerable inherent genetic or/and somaclonal variations in CRISPR/Cas9-edited cotton plants. Plant Biotechnol. J. https://doi.org/10.1111/pbi.13020
    [Crossref] [Google Scholar]
  71. 71.  Li J, Meng X, Zong Y, Chen K, Zhang H et al. 2016. Gene replacements and insertions in rice by intron targeting using CRISPR-Cas9. Nat. Plants 2:16139
    [Google Scholar]
  72. 72.  Li J, Zhang H, Si X, Tian Y, Chen K et al. 2017. Generation of thermosensitive male-sterile maize by targeted knockout of the ZmTMS5 gene. J. Genet. Genom. 44:465–68
    [Google Scholar]
  73. 73.  Li JF, Norville JE, Aach J, McCormack M, Zhang D et al. 2013. Multiplex and homologous recombination-mediated genome editing in Arabidopsis and Nicotiana benthamiana using guide RNA and Cas9. Nat. Biotechnol. 31:688–91
    [Google Scholar]
  74. 74.  Li M, Li X, Zhou Z, Wu P, Fang M et al. 2016. Reassessment of the four yield-related genes gn1a, dep1, gs3, and ipa1 in rice using a CRISPR/Cas9 system. Front. Plant Sci. 7:377
    [Google Scholar]
  75. 75.  Li Q, Zhang D, Chen M, Liang W, Wei J et al. 2016. Development of japonica photo-sensitive genic male sterile rice lines by editing carbon starved anther using CRISPR/Cas9. J. Genet. Genom. 43:415–19
    [Google Scholar]
  76. 76.  Li R, Fu D, Zhu B, Luo Y, Zhu H 2018. CRISPR/Cas9-mediated mutagenesis of lncRNA1459 alters tomato fruit ripening. Plant J 94:513–24
    [Google Scholar]
  77. 77.  Li R, Li R, Li X, Fu D, Zhu B et al. 2018. Multiplexed CRISPR/Cas9-mediated metabolic engineering of γ-aminobutyric acid levels in Solanum lycopersicum. Plant Biotechnol. J. 16:415–27
    [Google Scholar]
  78. 78.  Li S, Gao F, Xie K, Zeng X, Cao Y et al. 2016. The OsmiR396c-OsGRF4-OsGIF1 regulatory module determines grain size and yield in rice. Plant Biotechnol. J. 14:2134–46
    [Google Scholar]
  79. 79.  Li S, Zhang X, Wang W, Guo X, Wu Z et al. 2018. Expanding the scope of CRISPR/Cpf1-mediated genome editing in rice. Mol. Plant 11:995–98
    [Google Scholar]
  80. 80.  Li T, Yang X, Yu Y, Si X, Zhai X et al. 2018. Domestication of wild tomato is accelerated by genome editing. Nat. Biotechnol. 36:1160–63
    [Google Scholar]
  81. 81.  Li W, Ma M, Feng Y, Li H, Wang Y et al. 2015. EIN2-directed translational regulation of ethylene signaling in Arabidopsis. Cell 163:670–83
    [Google Scholar]
  82. 82.  Li X, Wang Y, Chen S, Tian H, Fu D et al. 2018. Lycopene is enriched in tomato fruit by CRISPR/Cas9-mediated multiplex genome editing. Front. Plant Sci. 9:559
    [Google Scholar]
  83. 83.  Li X, Zhou W, Ren Y, Tian X, Lv T et al. 2017. High-efficiency breeding of early-maturing rice cultivars via CRISPR/Cas9-mediated genome editing. J. Genet. Genom. 44:175–78
    [Google Scholar]
  84. 84.  Li Z, Liu ZB, Xing A, Moon BP, Koellhoffer JP et al. 2015. Cas9-guide RNA directed genome editing in soybean. Plant Physiol 169:960–70
    [Google Scholar]
  85. 85.  Li Z, Xiong X, Li J-F 2018. New cytosine base editor for plant genome editing. Sci. China Life Sci. 61:1602–3
    [Google Scholar]
  86. 86.  Li Z, Xiong X, Wang F, Li J-F 2018. Gene disruption through base-editing-induced mRNA mis-splicing in plants. New Phytol https://doi.org/10.1111/nph.15647
    [Crossref] [Google Scholar]
  87. 87.  Li Z, Zhang D, Xiong X, Yan B, Xie W et al. 2017. A potent Cas9-derived gene activator for plant and mammalian cells. Nat. Plants 3:930–36
    [Google Scholar]
  88. 88.  Liang XH, Shen W, Sun H, Migawa MT, Vickers TA, Crooke ST 2016. Translation efficiency of mRNAs is increased by antisense oligonucleotides targeting upstream open reading frames. Nat. Biotechnol. 34:875–80
    [Google Scholar]
  89. 89.  Liang Z, Chen K, Li T, Zhang Y, Wang Y et al. 2017. Efficient DNA-free genome editing of bread wheat using CRISPR/Cas9 ribonucleoprotein complexes. Nat. Commun. 8:14261
    [Google Scholar]
  90. 90.  Liang Z, Chen K, Zhang Y, Liu J, Yin K et al. 2018. Genome editing of bread wheat using biolistic delivery of CRISPR/Cas9 in vitro transcripts or ribonucleoproteins. Nat. Protoc. 13:413–30
    [Google Scholar]
  91. 91.  Lin CS, Hsu CT, Yang LH, Lee LY, Fu JY et al. 2017. Application of protoplast technology to CRISPR/Cas9 mutagenesis: from single cell mutation detection to mutant plant regeneration. Plant Biotechnol. J. 16:1295–310
    [Google Scholar]
  92. 92.  Liu J, Chen J, Zheng X, Wu F, Lin Q et al. 2017. GW5 acts in the brassinosteroid signalling pathway to regulate grain width and weight in rice. Nat. Plants 3:17043
    [Google Scholar]
  93. 93.  Lowder LG, Zhang D, Baltes NJ, Paul JW, Tang X et al. 2015. A CRISPR/Cas9 toolbox for multiplexed plant genome editing and transcriptional regulation. Plant Physiol 169:971–85
    [Google Scholar]
  94. 94.  Lowe K, La Rota M, Hoerster G, Hastings C, Wang N et al. 2018. Rapid genotype “independent” Zea mays L. (maize) transformation via direct somatic embryogenesis. In Vitro Cell. Dev. Biol. 54:240–52
    [Google Scholar]
  95. 95.  Lowe K, Wu E, Wang N, Hoerster G, Hastings C et al. 2016. Morphogenic regulators Baby boom and Wuschel improve monocot transformation. Plant Cell 28:1998–2015
    [Google Scholar]
  96. 96.  Lu HP, Luo T, Fu HW, Wang L, Tan YY et al. 2018. Resistance of rice to insect pests mediated by suppression of serotonin biosynthesis. Nat. Plants 4:338–44
    [Google Scholar]
  97. 97.  Lu K, Wu B, Wang J, Zhu W, Nie H et al. 2018. Blocking amino acid transporter OsAAP3 improves grain yield by promoting outgrowth buds and increasing tiller number in rice. Plant Biotechnol. J. 16:1710–22
    [Google Scholar]
  98. 98.  Lu Y, Ye X, Guo R, Huang J, Wang W et al. 2017. Genome-wide targeted mutagenesis in rice using the CRISPR/Cas9 system. Mol. Plant 10:1242–45
    [Google Scholar]
  99. 99.  Luo M, Gilbert B, Ayliffe M 2016. Applications of CRISPR/Cas9 technology for targeted mutagenesis, gene replacement and stacking of genes in higher plants. Plant Cell Rep 35:1439–50
    [Google Scholar]
  100. 100.  Ma X, Zhang Q, Zhu Q, Liu W, Chen Y et al. 2015. A robust CRISPR/Cas9 system for convenient, high-efficiency multiplex genome editing in monocot and dicot plants. Mol. Plant 8:1274–84
    [Google Scholar]
  101. 101.  Ma Y, Zhang J, Yin W, Zhang Z, Song Y, Chang X 2016. Targeted AID-mediated mutagenesis (TAM) enables efficient genomic diversification in mammalian cells. Nat. Methods 13:1029–35
    [Google Scholar]
  102. 102.  Macovei A, Sevilla NR, Cantos C, Jonson GB, Slamet-Loedin I et al. 2018. Novel alleles of rice eIF4G generated by CRISPR/Cas9-targeted mutagenesis confer resistance to Rice tungro spherical virus. Plant Biotechnol. J. 16:1918–27
    [Google Scholar]
  103. 103.  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]
  104. 104.  Malnoy M, Viola R, Jung MH, Koo OJ, Kim S et al. 2016. DNA-free genetically edited grapevine and apple protoplast using CRISPR/Cas9 ribonucleoproteins. Front. Plant Sci. 7:1904
    [Google Scholar]
  105. 105.  Mateos-Gomez PA, Gong F, Nair N, Miller KM, Lazzerini-Denchi E, Sfeir A 2015. Mammalian polymerase θ promotes alternative-NHEJ and suppresses recombination. Nature 518:254–57
    [Google Scholar]
  106. 106.  McVey M, Khodaverdian VY, Meyer D, Cerqueira PG, Heyer W-D 2016. Eukaryotic DNA polymerases in homologous recombination. Annu. Rev. Genet. 50:393–421
    [Google Scholar]
  107. 107.  Mehta D, Stürchler A, Hirsch-Hoffmann M, Gruissem W, Vanderschuren H 2018. CRISPR-Cas9 interference in cassava linked to the evolution of editing-resistant geminiviruses. bioRxiv 314542. https://doi.org/10.1101/314542
    [Crossref]
  108. 108.  Meng X, Hu X, Liu Q, Song X, Gao C et al. 2018. Robust genome editing of CRISPR-Cas9 at NAG PAMs in rice. Sci. China Life Sci. 61:122–25
    [Google Scholar]
  109. 109.  Meng X, Yu H, Zhang Y, Zhuang F, Song X et al. 2017. Construction of a genome-wide mutant library in rice using CRISPR/Cas9. Mol. Plant 10:1238–41
    [Google Scholar]
  110. 110.  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 115:6058–63
    [Google Scholar]
  111. 111.  Mitter N, Worrall EA, Robinson KE, Li P, Jain RG et al. 2017. Clay nanosheets for topical delivery of RNAi for sustained protection against plant viruses. Nat. Plants 3:16207
    [Google Scholar]
  112. 112.  Morineau C, Bellec Y, Tellier F, Gissot L, Kelemen Z et al. 2017. Selective gene dosage by CRISPR-Cas9 genome editing in hexaploid Camelina sativa. Plant Biotechnol. J. 15:729–39
    [Google Scholar]
  113. 113.  Nakayasu M, Akiyama R, Lee HJ, Osakabe K, Osakabe Y et al. 2018. Generation of α-solanine-free hairy roots of potato by CRISPR/Cas9 mediated genome editing of the St16DOX gene. Plant Physiol. Biochem. 131:70–77
    [Google Scholar]
  114. 114.  Nayak A, Tassetto M, Kunitomi M, Andino R 2013. RNA interference-mediated intrinsic antiviral immunity in invertebrates. Curr. Top. Microbiol. Immunol. 371:183–200
    [Google Scholar]
  115. 115.  Nekrasov V, Staskawicz B, Weigel D, Jones JD, Kamoun S 2013. Targeted mutagenesis in the model plant Nicotiana benthamiana using Cas9 RNA-guided endonuclease. Nat. Biotechnol. 31:691–93
    [Google Scholar]
  116. 116.  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]
  117. 117.  Nemhauser JL, Torii KU 2016. Plant synthetic biology for molecular engineering of signalling and development. Nat. Plants 2:16010
    [Google Scholar]
  118. 118.  Nieves-Cordones M, Mohamed S, Tanoi K, Kobayashi NI, Takagi K et al. 2017. Production of low-Cs+ rice plants by inactivation of the K+ transporter OsHAK1 with the CRISPR-Cas system. Plant J 92:43–56
    [Google Scholar]
  119. 119.  Nishida K, Arazoe T, Yachie N, Banno S, Kakimoto M et al. 2016. Targeted nucleotide editing using hybrid prokaryotic and vertebrate adaptive immune systems. Science 353:aaf8729
    [Google Scholar]
  120. 120.  Nishimasu H, Shi X, Ishiguro S, Gao L, Hirano S et al. 2018. Engineered CRISPR-Cas9 nuclease with expanded targeting space. Science 361:1259–62
    [Google Scholar]
  121. 121.  Nishizawa-Yokoi A, Endo M, Ohtsuki N, Saika H, Toki S 2014. Precision genome editing in plants via gene targeting and piggyBac-mediated marker excision. Plant J 81:160–68
    [Google Scholar]
  122. 122.  Nonaka S, Arai C, Takayama M, Matsukura C, Ezura H 2017. Efficient increase of γ-aminobutyric acid (GABA) content in tomato fruits by targeted mutagenesis. Sci Rep 7:7057
    [Google Scholar]
  123. 123.  Okuzaki A, Ogawa T, Koizuka C, Kaneko K, Inaba M et al. 2018. CRISPR/Cas9-mediated genome editing of the fatty acid desaturase 2 gene in Brassica napus. Plant Physiol. Biochem 131:63–69
    [Google Scholar]
  124. 124.  Østerberg JT, Xiang W, Olsen LI, Edenbrandt AK, Vedel SE et al. 2017. Accelerating the domestication of new crops: feasibility and approaches. Trends Plant Sci 22:373–84
    [Google Scholar]
  125. 125.  Pacher M, Puchta H 2017. From classical mutagenesis to nuclease-based breeding-directing natural DNA repair for a natural end-product. Plant J 90:819–33
    [Google Scholar]
  126. 126.  Paszkowski J, Baur M, Bogucki A, Potrykus I 1988. Gene targeting in plants. EMBO J 7:4021–26
    [Google Scholar]
  127. 127.  Peng A, Chen S, Lei T, Xu L, He Y et al. 2017. Engineering canker-resistant plants through CRISPR/Cas9-targeted editing of the susceptibility gene CsLOB1 promoter in citrus. Plant Biotechnol. J. 15:1509–19
    [Google Scholar]
  128. 128.  Piatek A, Ali Z, Baazim H, Li L, Abulfaraj A et al. 2015. RNA-guided transcriptional regulation in planta via synthetic dCas9-based transcription factors. Plant Biotechnol. J. 13:578–89
    [Google Scholar]
  129. 129.  Prado JR, Segers G, Voelker T, Carson D, Dobert R et al. 2014. Genetically engineered crops: from idea to product. Annu. Rev. Plant Biol. 65:769–90
    [Google Scholar]
  130. 130.  Price AA, Sampson TR, Ratner HK, Grakoui A, Weiss DS 2015. Cas9-mediated targeting of viral RNA in eukaryotic cells. PNAS 112:6164–69
    [Google Scholar]
  131. 131.  Puchta H, Dujon B, Hohn B 1993. Homologous recombination in plant cells is enhanced by in vivo induction of double strand breaks into DNA by a site-specific endonuclease. Nucleic Acids Res 21:5034–40
    [Google Scholar]
  132. 132.  Ran Y, Liang Z, Gao C 2017. Current and future editing reagent delivery systems for plant genome editing. Sci. China Life Sci. 60:490–505
    [Google Scholar]
  133. 133.  Rees HA, Komor AC, Yeh WH, Caetano-Lopes J, Warman M et al. 2017. Improving the DNA specificity and applicability of base editing through protein engineering and protein delivery. Nat. Commun. 8:15790
    [Google Scholar]
  134. 134.  Rodríguez-Leal D, Lemmon ZH, Man J, Bartlett ME, Lippman ZB 2017. Engineering quantitative trait variation for crop improvement by genome editing. Cell 171:470–80Demonstrates targeting cis-regulatory elements in promoters creates a continuum of variation in yield traits.
    [Google Scholar]
  135. 135.  Salsman J, Dellaire G 2016. Precision genome editing in the CRISPR era. Biochem. Cell Biol. 95:187–201
    [Google Scholar]
  136. 136.  Sanchez-Leon S, Gil-Humanes J, Ozuna CV, Gimenez MJ, Sousa C et al. 2018. Low-gluten, nontransgenic wheat engineered with CRISPR/Cas9. Plant Biotechnol. J. 16:902–10
    [Google Scholar]
  137. 137.  Sauer NJ, Narvaez-Vasquez J, Mozoruk J, Miller RB, Warburg ZJ et al. 2016. Oligonucleotide-mediated genome editing provides precision and function to engineered nucleases and antibiotics in plants. Plant Physiol 170:1917–28
    [Google Scholar]
  138. 138.  Scheben A, Wolter F, Batley J, Puchta H, Edwards D 2017. Towards CRISPR/Cas crops—bringing together genomics and genome editing. New Phytol 216:682–98
    [Google Scholar]
  139. 139.  Sedbrook JC, Phippen WB, Marks MD 2014. New approaches to facilitate rapid domestication of a wild plant to an oilseed crop: example pennycress (Thlaspi arvense L.). Plant Sci 227:122–32
    [Google Scholar]
  140. 140.  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. 31:686–88Provides first demonstration of indel-inducing CRISPR/Cas9 system for plants.
    [Google Scholar]
  141. 141.  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. 13:791–800
    [Google Scholar]
  142. 142.  Shen R, Wang L, Liu X, Wu J, Jin W et al. 2017. Genomic structural variation-mediated allelic suppression causes hybrid male sterility in rice. Nat. Commun. 8:1310
    [Google Scholar]
  143. 143.  Shi J, Gao 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]
  144. 144.  Shimatani Z, Kashojiya S, Takayama M, Terada R, Arazoe T et al. 2017. Targeted base editing in rice and tomato using a CRISPR-Cas9 cytidine deaminase fusion. Nat. Biotechnol. 35:441–43
    [Google Scholar]
  145. 145.  Singh M, Kumar M, Albertsen MC, Young JK, Cigan AM 2018. Concurrent modifications in the three homeologs of Ms45 gene with CRISPR-Cas9 lead to rapid generation of male sterile bread wheat (Triticum aestivum L.). Plant Mol. Biol. 97:371–83
    [Google Scholar]
  146. 146.  Subburaj S, Chung SJ, Lee C, Ryu SM, Kim DH et al. 2016. Site-directed mutagenesis in Petunia × hybrida protoplast system using direct delivery of purified recombinant Cas9 ribonucleoproteins. Plant Cell Rep 35:1535–44
    [Google Scholar]
  147. 147.  Sun Y, Jiao G, Liu Z, Zhang X, Li J et al. 2017. Generation of high-amylose rice through CRISPR/Cas9-mediated targeted mutagenesis of starch branching enzymes. Front. Plant Sci. 8:1298
    [Google Scholar]
  148. 148.  Sun Y, Zhang X, Wu C, He Y, Ma Y et al. 2016. Engineering herbicide-resistant rice plants through CRISPR/Cas9-mediated homologous recombination of acetolactate synthase. Mol. Plant 9:628–31
    [Google Scholar]
  149. 149.  Svitashev S, Schwartz C, Lenderts B, Young JK, Mark Cigan A 2016. Genome editing in maize directed by CRISPR-Cas9 ribonucleoprotein complexes. Nat. Commun. 7:13274
    [Google Scholar]
  150. 150.  Svitashev S, Young JK, Schwartz C, Gao H, Falco SC, Cigan AM 2015. Targeted mutagenesis, precise gene editing, and site-specific gene insertion in maize using Cas9 and guide RNA. Plant Physiol 169:931–45
    [Google Scholar]
  151. 151.  Symington LS, Gautier J 2011. Double-strand break end resection and repair pathway choice. Annu. Rev. Genet. 45:247–71
    [Google Scholar]
  152. 152.  Tang L, Mao B, Li Y, Lv Q, Zhang L et al. 2017. Knockout of OsNramp5 using the CRISPR/Cas9 system produces low Cd-accumulating indica rice without compromising yield. Sci. Rep. 7:14438
    [Google Scholar]
  153. 153.  Tang X, Liu G, Zhou J, Ren Q, You Q et al. 2018. A large-scale whole-genome sequencing analysis reveals highly specific genome editing by both Cas9 and Cpf1 (Cas12a) nucleases in rice. Genome Biol 19:84
    [Google Scholar]
  154. 154.  Temme K, Zhao D, Voigt CA 2012. Refactoring the nitrogen fixation gene cluster from Klebsiella oxytoca. PNAS 109:7085–90
    [Google Scholar]
  155. 155.  Teng F, Cui T, Feng G, Guo L, Xu K et al. 2018. Repurposing CRISPR-Cas12b for mammalian genome engineering. Cell Discov 4:63
    [Google Scholar]
  156. 156.  Tian S, Jiang L, Cui X, Zhang J, Guo S et al. 2018. Engineering herbicide-resistant watermelon variety through CRISPR/Cas9-mediated base-editing. Plant Cell Rep 37:1353–56
    [Google Scholar]
  157. 157.  Tilman D, Balzer C, Hill J, Befort BL 2011. Global food demand and the sustainable intensification of agriculture. PNAS 108:20260–64
    [Google Scholar]
  158. 158.  van Kregten M, de Pater S, Romeijn R, van Schendel R, Hooykaas PJJ, Tijsterman M 2016. T-DNA integration in plants results from polymerase-θ-mediated DNA repair. Nat. Plants 2:16164
    [Google Scholar]
  159. 159.  von Arnim AG, Jia Q, Vaughn JN 2014. Regulation of plant translation by upstream open reading frames. Plant Sci 214:1–12
    [Google Scholar]
  160. 160.  von Caemmerer S, Quick WP, Furbank RT 2012. The development of C4 rice: current progress and future challenges. Science 336:1671–72
    [Google Scholar]
  161. 161.  Voth DE, Broederdorf LJ, Graham JG 2012. Bacterial type IV secretion systems: versatile virulence machines. Future Microbiol 7:241–57
    [Google Scholar]
  162. 162.  Waltz E 2016. CRISPR-edited crops free to enter market, skip regulation. Nat. Biotechnol. 34:582
    [Google Scholar]
  163. 163.  Wang C, Liu Q, Shen Y, Hua Y, Wang J et al. 2019. Clonal seeds from hybrid rice by simultaneous genome engineering of meiosis and fertilization genes. Nat. Biotechnol. 37:283–86
    [Google Scholar]
  164. 164.  Wang F, Wang C, Liu P, Lei C, Hao W et al. 2016. Enhanced rice blast resistance by CRISPR/Cas9-targeted mutagenesis of the ERF transcription factor gene OsERF922. PLOS ONE 11:e0154027
    [Google Scholar]
  165. 165.  Wang FZ, Chen MX, Yu LJ, Xie LJ, Yuan LB et al. 2017. OsARM1, an R2R3 MYB transcription factor, is involved in regulation of the response to arsenic stress in rice. Front. Plant Sci. 8:1868
    [Google Scholar]
  166. 166.  Wang H, Studer AJ, Zhao Q, Meeley R, Doebley JF 2015. Evidence that the origin of naked kernels during maize domestication was caused by a single amino acid substitution in tga1. Genetics 200:965–74
    [Google Scholar]
  167. 167.  Wang M, Lu Y, Botella JR, Mao Y, Hua K, Zhu JK 2017. Gene targeting by homology-directed repair in rice using a geminivirus-based CRISPR/Cas9 system. Mol. Plant 10:1007–10
    [Google Scholar]
  168. 168.  Wang M, Mao Y, Lu Y, Tao X, Zhu J-k 2017. Multiplex gene editing in rice using the CRISPR-Cpf1 system. Mol. Plant 10:1011–13
    [Google Scholar]
  169. 169.  Wang X, Li J, Wang Y, Yang B, Wei J et al. 2018. Efficient base editing in methylated regions with a human APOBEC3A-Cas9 fusion. Nat. Biotechnol. 36:946–49
    [Google Scholar]
  170. 170.  Wang Y, Cheng X, Shan Q, Zhang Y, Liu J et al. 2014. Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nat. Biotechnol. 32:947–51Provides first use of genome editing in polyploid wheat to improve crop traits, providing a methodological framework for crop improvement.
    [Google Scholar]
  171. 171.  Woo JW, Kim J, Kwon SI, Corvalan C, Cho SW et al. 2015. DNA-free genome editing in plants with preassembled CRISPR-Cas9 ribonucleoproteins. Nat. Biotechnol. 33:1162–64
    [Google Scholar]
  172. 172.  Wright DA, Townsend JA, Winfrey RJ Jr., Irwin PA, Rajagopal J et al. 2005. High-frequency homologous recombination in plants mediated by zinc-finger nucleases. Plant J 44:693–705
    [Google Scholar]
  173. 173.  Xie K, Minkenberg B, Yang Y 2015. Boosting CRISPR/Cas9 multiplex editing capability with the endogenous tRNA-processing system. PNAS 112:3570–75
    [Google Scholar]
  174. 174.  Xie Y, Niu B, Long Y, Li G, Tang J et al. 2017. Suppression or knockout of SaF/SaM overcomes the Sa-mediated hybrid male sterility in rice. J. Integr. Plant Biol. 59:669–79
    [Google Scholar]
  175. 175.  Xie Y, Xu P, Huang J, Ma S, Xie X et al. 2017. Interspecific hybrid sterility in rice is mediated by OgTPR1 at the S1 locus encoding a peptidase-like protein. Mol. Plant 10:1137–40
    [Google Scholar]
  176. 176.  Xu R, Yang Y, Qin R, Li H, Qiu C et al. 2016. Rapid improvement of grain weight via highly efficient CRISPR/Cas9-mediated multiplex genome editing in rice. J. Genet. Genom. 43:529–32
    [Google Scholar]
  177. 177.  Xue C, Zhang H, Lin Q, Fan R, Gao C 2018. Manipulating mRNA splicing by base editing in plants. Sci. China Life Sci. 61:1293–300
    [Google Scholar]
  178. 178.  Yao L, Zhang Y, Liu C, Liu Y, Wang Y et al. 2018. OsMATL mutation induces haploid seed formation in indica rice. Nat. Plants 4:530–33
    [Google Scholar]
  179. 179.  Ye M, Peng Z, Tang D, Yang Z, Li D et al. 2018. Generation of self-compatible diploid potato by knockout of S-RNase. Nat. Plants 4:651–54
    [Google Scholar]
  180. 180.  Yu QH, Wang B, Li N, Tang Y, Yang S et al. 2017. CRISPR/Cas9-induced targeted mutagenesis and gene replacement to generate long-shelf life tomato lines. Sci. Rep. 7:11874
    [Google Scholar]
  181. 181.  Yu X, Zhao Z, Zheng X, Zhou J, Kong W et al. 2018. A selfish genetic element confers non-Mendelian inheritance in rice. Science 360:1130–32
    [Google Scholar]
  182. 182.  Zaidi SS, Tashkandi M, Mansoor S, Mahfouz MM 2016. Engineering plant immunity: using CRISPR/Cas9 to generate virus resistance. Front. Plant Sci. 7:1673
    [Google Scholar]
  183. 183.  Zetsche B, Gootenberg Jonathan S, Abudayyeh Omar O, Slaymaker Ian M, Makarova Kira S et al. 2015. Cpf1 is a single RNA-guided endonuclease of a class 2 CRISPR-Cas system. Cell 163:759–71Identifies Cpf1, a CRISPR effector that mediates robust DNA interference with features distinct from Cas9.
    [Google Scholar]
  184. 184.  Zhang H, Si X, Ji X, Fan R, Liu J et al. 2018. Genome editing of upstream open reading frames enables translational control in plants. Nat. Biotechnol. 36:894–98Describes how the disruption of uORFs by CRISPR/Cas9 efficiently enhances principal ORF expression at the translational level.
    [Google Scholar]
  185. 185.  Zhang J, Zhang H, Botella JR, Zhu JK 2018. Generation of new glutinous rice by CRISPR/Cas9-targeted mutagenesis of the Waxy gene in elite rice varieties. J. Integr. Plant Biol. 60:369–75
    [Google Scholar]
  186. 186.  Zhang T, Zheng Q, Yi X, An H, Zhao Y et al. 2018. Establishing RNA virus resistance in plants by harnessing CRISPR immune system. Plant Biotechnol. J. 16:1415–23
    [Google Scholar]
  187. 187.  Zhang Y, Li D, Zhang D, Zhao X, Cao X et al. 2018. Analysis of the functions of TaGW2 homoeologs in wheat grain weight and protein content traits. Plant J 94:857–66
    [Google Scholar]
  188. 188.  Zhang Y, Liang Z, Zong Y, Wang Y, Liu J et al. 2016. Efficient and transgene-free genome editing in wheat through transient expression of CRISPR/Cas9 DNA or RNA. Nat. Commun. 7:12617
    [Google Scholar]
  189. 189.  Zhong Z, Zhang Y, You Q, Tang X, Ren Q et al. 2018. Plant genome editing using FnCpf1 and LbCpf1 nucleases at redefined and altered PAM site. Mol. Plant 11:999–1002
    [Google Scholar]
  190. 190.  Zhou H, He M, Li J, Chen L, Huang Z et al. 2016. Development of commercial thermo-sensitive genic male sterile rice accelerates hybrid rice breeding using the CRISPR/Cas9-mediated TMS5 editing system. Sci. Rep. 6:37395
    [Google Scholar]
  191. 191.  Zhou J, Peng Z, Long J, Sosso D, Liu B et al. 2015. Gene targeting by the TAL effector PthXo2 reveals cryptic resistance gene for bacterial blight of rice. Plant J 82:632–43
    [Google Scholar]
  192. 192.  Zhu B, Zhang W, Zhang T, Liu B, Jiang J 2015. Genome-wide prediction and validation of intergenic enhancers in Arabidopsis using open chromatin signatures. Plant Cell 27:2415–26
    [Google Scholar]
  193. 193.  Zong Y, Song Q, Li C, Jin S, Zhang D et al. 2018. Efficient C-to-T base editing in plants using a fusion of nCas9 and human APOBEC3A. Nat. Biotechnol. 36:950–53Explores a new plant cytidine base editor containing a human cytidine deaminase that offers a larger editing window.
    [Google Scholar]
  194. 194.  Zong Y, Wang Y, Li C, Zhang R, Chen K et al. 2017. Precise base editing in rice, wheat and maize with a Cas9-cytidine deaminase fusion. Nat. Biotechnol. 35:438–40
    [Google Scholar]
  195. 195.  Zsögön A, Čermák T, Naves ER, Notini MM, Edel KH et al. 2018. De novo domestication of wild tomato using genome editing. Nat. Biotechnol. 36:1211–16Demonstrates first use of genome editing for de novo domestication of wild species to create novel nutritious crops.
    [Google Scholar]
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