Advertisement

CRISPR-associated nucleases: the Dawn of a new age of efficient crop improvement

  • Rishikesh Ghogare
  • Bruce Williamson-Benavides
  • Fabiola Ramírez-Torres
  • Amit DhingraEmail author
Review

Abstract

The world stands at a new threshold today. As a planet, we face various challenges, and the key one is how to continue to produce enough food, feed, fiber, and fuel to support the burgeoning population. In the past, plant breeding and the ability to genetically engineer crops contributed to increasing food production. However, both approaches rely on random mixing or integration of genes, and the process can be unpredictable and time-consuming. Given the challenge of limited availability of natural resources and changing environmental conditions, the need to rapidly and precisely improve crops has become urgent. The discovery of CRISPR-associated endonucleases offers a precise yet versatile platform for rapid crop improvement. This review summarizes a brief history of the discovery of CRISPR-associated nucleases and their application in genome editing of various plant species. Also provided is an overview of several new endonucleases reported recently, which can be utilized for editing of specific genes in plants through various forms of DNA sequence alteration. Genome editing, with its ever-expanding toolset, increased efficiency, and its potential integration with the emerging synthetic biology approaches hold promise for efficient crop improvement to meet the challenge of supporting the needs of future generations.

Keywords

Gene editing CRISPR Cas endonucleases Plants Crop improvement 

Notes

References

  1. Abudayyeh OO, Gootenberg JS, Konermann S et al (2016) C2c2 is a single-component programmable RNA-guided RNA-targeting CRISPR effector. Science 353(6299):aaf5573CrossRefPubMedPubMedCentralGoogle Scholar
  2. Abudayyeh OO, Gootenberg JS, Essletzbichler P et al (2017) RNA targeting with CRISPR–Cas13. Nature 550(7675):280CrossRefPubMedPubMedCentralGoogle Scholar
  3. Abu-Zaitoon YM, Al Tawaha AR, Alnaimat SM, Al-Rawashdeh IM et al (2019) Investigation of the potential role of aldehyde oxidase in the indole-3-acetic acid synthesis of developing rice grains. Plant Cell Biotechnol Mol Biol 20:6–13Google Scholar
  4. Al Amin N, Ahmad N, Wu N et al (2019) CRISPR-Cas9 mediated targeted the disruption of FAD2–2 microsomal omega-6 desaturase in soybean (Glycine max. L). BMC Biotechnol 19(1):9CrossRefPubMedPubMedCentralGoogle Scholar
  5. Aman R, Ali Z, Butt H et al (2018) RNA virus interference via CRISPR/Cas13a system in plants. Genome Biol 19(1):1CrossRefPubMedPubMedCentralGoogle Scholar
  6. Anders C, Niewoehner O, Duerst A, Jinek M (2014) Structural basis of PAM-dependent target DNA recognition by the Cas9 endonuclease. Nature 513(7519):569CrossRefPubMedPubMedCentralGoogle Scholar
  7. Andersson M, Turesson H, Olsson N et al (2018) Genome editing in potato via CRISPR-Cas9 ribonucleoprotein delivery. Physiol Plant 164(4):378–384CrossRefPubMedPubMedCentralGoogle Scholar
  8. Barrangou R (2015) Diversity of CRISPR-Cas immune systems and molecular machines. Genome Biol 16(1):247CrossRefPubMedPubMedCentralGoogle Scholar
  9. Barrangou R, Fremaux C, Deveau H et al (2007) CRISPR provides acquired resistance against viruses in prokaryotes. Science 315(5819):1709–1712CrossRefPubMedPubMedCentralGoogle Scholar
  10. Begemann M, Gray BN (2018) Compositions and methods for modifying genomes. U.S. Patent No. 9,896,696. U.S. Patent and Trademark Office, Washington, DCGoogle Scholar
  11. Begemann MB, Gray BN, January E, et al (2017a) Characterization and validation of a novel group of type V, class 2 nucleases for in vivo genome editing. BioRxiv 192799Google Scholar
  12. Begemann MB, Gray BN, January E et al (2017b) Precise insertion and guided editing of higher plant genomes using Cpf1 CRISPR nucleases. Sci Rep 7(1):11606CrossRefPubMedPubMedCentralGoogle Scholar
  13. Bertier LD, Ron M, Huo H, Bradford KJ, Britt AB, Michelmore RW (2018) High-resolution analysis of the efficiency, heritability, and editing outcomes of CRISPR/Cas9-induced modifications of NCED4 in lettuce (Lactuca sativa). G3 8(5):1513–1521CrossRefGoogle Scholar
  14. Bolotin A, Quinquis B, Sorokin A et al (2005) Clustered regularly interspaced short palindrome repeats (CRISPRs) have spacers of extrachromosomal origin. Microbiology 151(8):2551–2561CrossRefGoogle Scholar
  15. 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(3):1292–1297CrossRefPubMedPubMedCentralGoogle Scholar
  16. Brouns SJ, Jore MM, Lundgren M et al (2008) Small CRISPR RNAs guide antiviral defense in prokaryotes. Science 321(5891):960–964CrossRefPubMedPubMedCentralGoogle Scholar
  17. Bult CJ, White O, Olsen GJ et al (1996) Complete genome sequence of the methanogenic archaeon, Methanococcus jannaschii. Science 273(5278):1058–1073CrossRefGoogle Scholar
  18. 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(12):e0144591CrossRefPubMedPubMedCentralGoogle Scholar
  19. Cai Y, Chen L, Liu X et al (2015) CRISPR/Cas9-mediated genome editing in soybean hairy roots. PLoS ONE 10(8):e0136064CrossRefPubMedPubMedCentralGoogle Scholar
  20. Cai Y, Chen L, Liu X et al (2018) CRISPR/Cas9-mediated targeted mutagenesis of GmFT2a delays flowering time in soya bean. Plant Biotechnol J 16(1):176–185CrossRefPubMedPubMedCentralGoogle Scholar
  21. Carlson DF, Fahrenkrug SC, Hackett PB (2012) Targeting DNA with fingers and TALENs. Mol Ther Nucleic acids 1Google Scholar
  22. Cebrian-Serrano A, Davies B (2017) CRISPR-Cas orthologues and variants: optimizing the repertoire, specificity, and delivery of genome engineering tools. Mamm Genome 28(7–8):247–261CrossRefPubMedPubMedCentralGoogle Scholar
  23. Čermák T, Baltes NJ, Čegan R, Zhang Y, Voytas DF (2015) High-frequency, precise modification of the tomato genome. Genome Biol 16(1):232CrossRefPubMedPubMedCentralGoogle Scholar
  24. Chandrasekaran J, Brumin M, Wolf D et al (2016) Development of broad virus resistance in non-transgenic cucumber using CRISPR/Cas9 technology. Mol Plant Pathol 17(7):1140–1153CrossRefPubMedPubMedCentralGoogle Scholar
  25. Char SN, Neelakandan AK, Nahampun H et al (2017) An Agrobacterium-delivered CRISPR/Cas9 system for high-frequency targeted mutagenesis in maize. Plant Biotechnol J 15(2):257–268CrossRefGoogle Scholar
  26. Charrier A, Vergne E, Dousset N, Richer A, Petiteau A, Chevreau E (2019) Efficient, targeted mutagenesis in apple and first-time edition of pear using the CRISPR-Cas9 system. Front Plant Sci 10:40CrossRefPubMedPubMedCentralGoogle Scholar
  27. Chavez A, Scheiman J, Vora S et al (2015) Highly efficient Cas9-mediated transcriptional programming. Nat Methods 12(4):326CrossRefPubMedPubMedCentralGoogle Scholar
  28. Chen B, Hu J, Almeida R et al (2016) Expanding the CRISPR imaging toolset with Staphylococcus aureus Cas9 for simultaneous imaging of multiple genomic loci. Nucleic Acids Res 44(8):e75–e75CrossRefPubMedPubMedCentralGoogle Scholar
  29. Cong L, Ran FA, Cox D et al (2013) Multiplex genome engineering using CRISPR/Cas systems. Science 339(6121):819–823CrossRefPubMedPubMedCentralGoogle Scholar
  30. Cook C, Martin L, Bastow R (2014) Opportunities in plant synthetic biology. J Exp Bot 65(8):1921–1926CrossRefGoogle Scholar
  31. Cox DB, Gootenberg JS, Abudayyeh OO, Franklin B, Kellner MJ, Joung J, Zhang F (2017) RNA editing with CRISPR-Cas13. Science 358(6366):1019–1027CrossRefPubMedPubMedCentralGoogle Scholar
  32. Cradick TJ, Fine EJ, Antico CJ et al (2013) CRISPR/Cas9 systems targeting β-globin and CCR32 genes have substantial off-target activity. Nucleic Acids Res 41(20):9584–9592CrossRefPubMedPubMedCentralGoogle Scholar
  33. Curtin SJ, Xiong Y, Michno JM et al (2018) CRISPR/cas9 and talen s generate heritable mutations for genes involved in small RNA processing of glycine max and Medicago truncatula. Plant Biotechnol J 16(6):1125–1137CrossRefPubMedPubMedCentralGoogle Scholar
  34. Dahan-Meir T, Filler-Hayut S, Melamed-Bessudo C, Bocobza S, Czosnek H, Aharoni A, Levy AA (2018) Efficient in planta gene targeting in tomato using geminiviral replicons and the CRISPR/Cas9 system. Plant J 95(1):5–16CrossRefGoogle Scholar
  35. Danilo B, Perrot L, Mara K, Botton E, Nogué F, Mazier M (2019) Efficient and transgene-free gene targeting using Agrobacterium-mediated delivery of the CRISPR/Cas9 system in tomato. Plant Cell Rep 38:459–462CrossRefGoogle Scholar
  36. de Toledo Thomazella DP, Brail Q, Dahlbeck D, Staskawicz B (2016) CRISPR-Cas9 mediated mutagenesis of a DMR6 ortholog in tomato confers broad-spectrum disease resistance. BioRxiv 064824Google Scholar
  37. Deltcheva E, Chylinski K, Sharma CM et al (2011) CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III. Nature 471(7340):602CrossRefPubMedPubMedCentralGoogle Scholar
  38. Deng L, Wang H, Sun C et al (2018) Efficient generation of pink-fruited tomatoes using the CRISPR/Cas9 system. J Genet Genom 45(1):51CrossRefGoogle Scholar
  39. DiCarlo JE, Norville JE, Mali P et al (2013) Genome engineering in Saccharomyces cerevisiae using CRISPR-Cas systems. Nucleic Acids Res 41(7):4336–4343CrossRefPubMedPubMedCentralGoogle Scholar
  40. Ding D, Chen K, Chen Y, Li H, Xie K (2018) Engineering introns to express RNA guides for Cas9-and Cpf1-mediated multiplex genome editing. Mol Plant 11(4):542–552CrossRefGoogle Scholar
  41. Dong D, Ren K, Qiu X et al (2016) The crystal structure of Cpf1 in complex with CRISPR RNA. Nature 532(7600):522CrossRefGoogle Scholar
  42. Doudna JA, Jinek M, Charpentier E, et al (2014) Methods and compositions for RNA-directed target DNA modification and for RNA-directed modulation of transcription. U.S. Patent Application No. 13/842,859Google Scholar
  43. Endo M, Mikami M, Toki S (2015) Multigene knockout utilizing off-target mutations of the CRISPR/Cas9 system in rice. Plant Cell Physiol 56(1):41–47CrossRefPubMedPubMedCentralGoogle Scholar
  44. Endo A, Masafumi M, Kaya H, Toki S (2016) Efficient, targeted mutagenesis of rice and tobacco genomes using Cpf1 from Francisella novicida. Sci Rep 6:38169CrossRefPubMedPubMedCentralGoogle Scholar
  45. Fan D, Liu T, Li C, Jiao B, Li S, Hou Y, Luo K (2015) Efficient CRISPR/Cas9-mediated targeted mutagenesis in Populus in the first generation. Sci Rep 5:12217CrossRefPubMedPubMedCentralGoogle Scholar
  46. Feng Z, Zhang B, Ding W et al (2013) Efficient genome editing in plants using a CRISPR/Cas system. Cell Res 23(10):1229CrossRefPubMedPubMedCentralGoogle Scholar
  47. Feng C, Su H, Bai H et al (2018) High-efficiency genome editing using a dmc1 promoter-controlled CRISPR/Cas9 system in maize. Plant Biotechnol J 16(11):1848–1857CrossRefPubMedPubMedCentralGoogle Scholar
  48. Fister AS, Landherr L, Maximova SN, Guiltinan MJ (2018) Transient expression of CRISPR/Cas9 machinery targeting TcNPR3 enhances defense response in Theobroma cacao. Front Plant Sci 9:268CrossRefPubMedPubMedCentralGoogle Scholar
  49. Friedland AE, Baral R, Singhal P et al (2015) Characterization of Staphylococcus aureus Cas9: a smaller Cas9 for all-in-one adeno-associated virus delivery and paired nickase applications. Genome Biol 16(1):257CrossRefGoogle Scholar
  50. Fu Y, Foden JA, Khayter C et al (2013) High-frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells. Nat Biotechnol 31(9):822CrossRefPubMedPubMedCentralGoogle Scholar
  51. Gao Y, Zhu N, Zhu X, Wu M et al (2019) Diversity and redundancy of the ripening regulatory networks revealed by the fruit ENCODE and the new CRISPR/Cas9 CNR and NOR mutants. Horticult Res 6(1):39CrossRefGoogle Scholar
  52. Garneau JE, Dupuis MÈ, Villion M, Romero DA et al (2010) The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA. Nature 468(7320):67CrossRefPubMedPubMedCentralGoogle Scholar
  53. Gaudelli NM, Komor AC, Rees HA et al (2017) Programmable base editing of A• T to G• C in genomic DNA without DNA cleavage. Nature 551(7681):464CrossRefPubMedPubMedCentralGoogle Scholar
  54. Gilbert LA, Larson MH, Morsut L et al (2013) CRISPR-mediated modular RNA-guided regulation of transcription in eukaryotes. Cell 154(2):442–451CrossRefPubMedPubMedCentralGoogle Scholar
  55. Godfray HCJ, Beddington JR, Crute IR et al (2010) Food security: the challenge of feeding 9 billion people. Science 327(5967):812–818CrossRefGoogle Scholar
  56. Gomez MA, Lin ZD, Moll T et al (2019) Simultaneous CRISPR/Cas9-mediated editing of cassava eIF 4E isoforms nCBP-1 and nCBP-2 reduce cassava brown streak disease symptom severity and incidence. Plant Biotechnol J 17(2):421–434CrossRefGoogle Scholar
  57. Groenen PM, Bunschoten AE, Soolingen DV et al (1993) Nature of DNA polymorphism in the direct repeat cluster of Mycobacterium tuberculosis; application for strain differentiation by a novel typing method. Mol Microbiol 10(5):1057–1065CrossRefGoogle Scholar
  58. Harrington LB, Burstein D, Chen JS et al (2018) Programmed DNA destruction by miniature CRISPR-Cas14 enzymes. Science 362(6416):839–842CrossRefPubMedPubMedCentralGoogle Scholar
  59. Havlicek S, Shen Y, Alpagu Y et al (2017) Re-engineered RNA-guided FokI-nucleases for improved genome editing in human cells. Mol Ther 25(2):342–355CrossRefPubMedPubMedCentralGoogle Scholar
  60. Hayut SF, Bessudo CM, Levy AA (2017) Targeted recombination between homologous chromosomes for precise breeding in tomato. Nat Commun 8:15605CrossRefGoogle Scholar
  61. Holkenbrink C, Dam MI, Kildegaard KR, Beder J, Dahlin J, Doménech Belda D, Borodina I (2018) EasyCloneYALI: CRISPR/Cas9-based synthetic toolbox for engineering of the yeast Yarrowia lipolytica. Biotechnol J 13(9):1700543CrossRefGoogle Scholar
  62. Holme IB, Wendt T, Gil-Humanes J, Deleuran LC, Starker CG, Voytas DF, Brinch-Pedersen H (2017) Evaluation of the mature grain phytase candidate HvPAPhy_a gene in barley (Hordeum vulgare L.) using CRISPR/Cas9 and TALENs. Plant Mol Biol 95(1–2):111–121CrossRefPubMedPubMedCentralGoogle Scholar
  63. Hu X, Wang C, Fu Y et al (2016) Expanding the range of CRISPR/Cas9 genome editing in rice. Mol Plant 9(6):943–945CrossRefGoogle Scholar
  64. Hu X, Wang C, Liu Q, Fu Y, Wang K (2017) Targeted mutagenesis in rice using CRISPR-Cpf1 system. J Genet Genom 44(1):71–73CrossRefGoogle Scholar
  65. Hua K, Tao X, Zhu JK (2019) Expanding the base editing scope in rice by using Cas9 variants. Plant Biotechnol J 17(2):499–504CrossRefPubMedPubMedCentralGoogle Scholar
  66. Hwang SG, Lee CY, Tseng CS (2018) Heterologous expression of rice 9-cis-epoxycarotenoid dioxygenase 4 (OsNCED4) in Arabidopsis confers sugar oversensitivity and drought tolerance. Bot Stud 59(1):2.  https://doi.org/10.1186/s40529-018-0219-9 CrossRefPubMedPubMedCentralGoogle Scholar
  67. Ishino Y, Shinagawa H, Makino K et al (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(12):5429–5433CrossRefPubMedPubMedCentralGoogle Scholar
  68. 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(1):76–82CrossRefGoogle Scholar
  69. Jacobs TB, LaFayette PR, Schmitz RJ, Parrott WA (2015) Targeted genome modifications in soybean with CRISPR/Cas9. BMC Biotechnol 15(1):16CrossRefPubMedPubMedCentralGoogle Scholar
  70. Jia H, Wang N (2014) Targeted genome editing of sweet orange using Cas9/sgRNA. PloS One 9(4):e93806CrossRefPubMedPubMedCentralGoogle Scholar
  71. Jia H, Xu J, Orbović V, Zhang Y, Wang N (2017a) Editing citrus genome via SaCas9/sgRNA system. Front Plant Sci 8:2135CrossRefPubMedPubMedCentralGoogle Scholar
  72. Jia H, Zhang Y, Orbović V, Xu J, White FF, Jones JB, Wang N (2017b) Genome editing of the disease susceptibility gene Cs LOB 1 in citrus confers resistance to citrus canker. Plant Biotechnol J 15(7):817–823CrossRefPubMedPubMedCentralGoogle Scholar
  73. Jia M, Geornaras I, Belk KE, Yang H (2019) Sequence-specific removal of shiga toxin-producing escherichia coli using the crispr-Cas9 system. Meat Muscle Biol 1(3):120–120Google Scholar
  74. Jiang F, Doudna JA (2017) CRISPR–Cas9 structures and mechanisms. Annu Rev Biophys 46:505–529CrossRefGoogle Scholar
  75. Jiang W, Bikard D, Cox D et al (2013a) RNA-guided editing of bacterial genomes using CRISPR-Cas systems. Nat Biotechnol 31(3):233–239CrossRefPubMedPubMedCentralGoogle Scholar
  76. Jiang W, Zhou H, Bi H, Fromm M, Yang B, Weeks DP (2013b) Demonstration of CRISPR/Cas9/sgRNA-mediated targeted gene modification in Arabidopsis, tobacco, sorghum, and rice. Nucleic Acids Res 41(20):e188–e188CrossRefPubMedPubMedCentralGoogle Scholar
  77. Jiang F, Zhou K, Ma L et al (2015) A Cas9–guide RNA complex preorganized for target DNA recognition. Science 348(6242):1477–1481CrossRefGoogle Scholar
  78. Jiang F, Taylor DW, Chen JS et al (2016) Structures of a CRISPR-Cas9 R-loop complex primed for DNA cleavage. Science 351(6275):867–871CrossRefPubMedPubMedCentralGoogle Scholar
  79. 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(6096):816–821CrossRefPubMedPubMedCentralGoogle Scholar
  80. Jinek M, Jiang F, Taylor DW et al (2014) Structures of Cas9 endonucleases reveal RNA-mediated conformational activation. Science 343(6176):1247997CrossRefPubMedPubMedCentralGoogle Scholar
  81. Josephs EA, Kocak DD, Fitzgibbon CJ et al (2015) Structure and specificity of the RNA-guided endonuclease Cas9 during DNA interrogation, target binding, and cleavage. Nucleic Acids Res 43(18):8924–8941CrossRefPubMedPubMedCentralGoogle Scholar
  82. Kawarabayasi Y, Sawada M, Horikawa H et al (1998) Complete sequence and gene organization of the genome of a hyper-thermophilic archaebacterium, Pyrococcus horikoshii OT3. DNA Res 5(2):55–76CrossRefGoogle Scholar
  83. Kawarabayasi Y, Hino Y, Horikawa H et al (1999) Complete genome sequence of an aerobic hyper-thermophilic crenarchaeon, Aeropyrum pernix K1. DNA Res 6(2):83–101CrossRefGoogle Scholar
  84. Kaya H, Mikami M, Endo A, Endo M, Toki S (2016) Highly specific targeted mutagenesis in plants using Staphylococcus aureus Cas9. Sci Rep 6:26871CrossRefPubMedPubMedCentralGoogle Scholar
  85. Kaya H, Ishibashi K, Toki S (2017) A split Staphylococcus aureus Cas9 as a compact genome-editing tool in plants. Plant Cell Physiol 58(4):643–649CrossRefPubMedPubMedCentralGoogle Scholar
  86. Khan MZ, Haider S, Mansoor S, Amin I (2019) Targeting plant ssDNA viruses with engineered miniature CRISPR-Cas14a. Trends Biotechnol 37(8):800–804CrossRefGoogle Scholar
  87. Kim H, Kim ST, Ryu J, Kang BC, Kim JS, Kim SG (2017) CRISPR/Cpf1-mediated DNA-free plant genome editing. Nat Commun 8:14406CrossRefPubMedPubMedCentralGoogle Scholar
  88. Klap C, Yeshayahou E, Bolger AM et al (2017) Tomato facultative parthenocarpy results from Sl AGAMOUS-LIKE 6 loss of function. Plant Biotechnol J 15(5):634–647CrossRefGoogle Scholar
  89. Kleinstiver BP, Prew MS, Tsai SQ et al (2015a) Engineered CRISPR-Cas9 nucleases with altered PAM specificities. Nature 523(7561):481CrossRefPubMedPubMedCentralGoogle Scholar
  90. Kleinstiver BP, Prew MS, Tsai SQ, Nguyen NT, Topkar VV, Zheng Z, Joung JK (2015b) Broadening the targeting range of Staphylococcus aureus CRISPR-Cas9 by modifying PAM recognition. Nat Biotechnol 33(12):1293CrossRefPubMedPubMedCentralGoogle Scholar
  91. Kleinstiver BP, Tsai SQ, Prew MS, Nguyen NT et al (2016) Genome-wide specificities of CRISPR-Cas Cpf1 nucleases in human cells. Nat Biotechnol 34(8):869CrossRefPubMedPubMedCentralGoogle Scholar
  92. Klenk HP, Clayton RA, Tomb JF et al (1998) Corrections: the complete genome sequence of the hyperthermophilic, sulphate-reducing archaeon Archaeoglobus fulgidus. Nature 394(6688):101CrossRefGoogle Scholar
  93. Knott GJ, East-Seletsky A, Cofsky JC, Holton JM, Charles E, O’Connell MR, Doudna JA (2017) Guide-bound structures of an RNA-targeting A-cleaving CRISPR–Cas13a enzyme. Nat struct mol biol 24(10):825CrossRefPubMedPubMedCentralGoogle Scholar
  94. 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(7603):420CrossRefPubMedPubMedCentralGoogle Scholar
  95. Konermann S, Brigham MD, Trevino AE et al (2015) Genome-scale transcriptional activation by an engineered CRISPR-Cas9 complex. Nature 517(7536):583CrossRefGoogle Scholar
  96. Koonin EV, Makarova KS, Zhang F (2017) Diversity, classification, and evolution of CRISPR-Cas systems. Curr Opin Microbiol 37:67–78CrossRefPubMedPubMedCentralGoogle Scholar
  97. Koonin E, Zhang F, Wolf Y, et al (2019) Novel CRISPR enzymes and systems. European patent application no. EP16738253.0AGoogle Scholar
  98. Lander ES (2016) The heroes of CRISPR. Cell 164(1–2):18–28CrossRefGoogle Scholar
  99. Lawrenson T, Shorinola O, Stacey N et al (2015) Induction of targeted, heritable mutations in barley and Brassica oleracea using RNA-guided Cas9 nuclease. Genome Biol 16(1):258CrossRefPubMedPubMedCentralGoogle Scholar
  100. Lee K, Eggenberger AL, Banakar R et al (2019a) CRISPR/Cas9-mediated targeted T-DNA integration in rice. Plant Mol Biol 99(4–5):317–328CrossRefGoogle Scholar
  101. Lee K, Zhang Y, Kleinstiver BP et al (2019b) Activities and specificities of CRISPR/Cas9 and Cas12a nucleases for targeted mutagenesis in maize. Plant Biotechnol J 17(2):362–372CrossRefPubMedPubMedCentralGoogle Scholar
  102. Lemmon ZH, Reem NT, Dalrymple J et al (2018) Rapid improvement of domestication traits in an orphan crop by genome editing. Nat Plants 4(10):766CrossRefGoogle Scholar
  103. Li D, Qiu Z, Shao Y et al (2013a) Heritable gene targeting in the mouse and rat using a CRISPR-Cas system. Nat Biotechnol 31(8):681–683CrossRefGoogle Scholar
  104. Li JF, Norville JE, Aach J et al (2013b) Multiplex and homologous recombination–mediated genome editing in Arabidopsis and Nicotiana benthamiana using guide RNA and Cas9. Nat Biotechnol 31(8):688CrossRefPubMedPubMedCentralGoogle Scholar
  105. Li M, Li X, Zhou Z 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 7:377PubMedPubMedCentralGoogle Scholar
  106. Li C, Zong Y, Wang Y et al (2018a) Expanded base editing in rice and wheat using a Cas9-adenosine deaminase fusion. Genome Biol 19(1):59CrossRefPubMedPubMedCentralGoogle Scholar
  107. Li R, Fu D, Zhu B, Luo Y, Zhu H (2018b) CRISPR/Cas9-mediated mutagenesis of lncRNA1459 alters tomato fruit ripening. Plant J 94(3):513–524CrossRefGoogle Scholar
  108. Li R, Li R, Li X et al (2018c) Multiplexed CRISPR/Cas9-mediated metabolic engineering of γ-aminobutyric acid levels in Solanum lycopersicum. Plant Biotechnol J 16(2):415–427CrossRefPubMedPubMedCentralGoogle Scholar
  109. Li R, Zhang L, Wang L, Chen L, Zhao R, Sheng J, Shen L (2018d) Reduction of tomato-plant chilling tolerance by CRISPR–Cas9-mediated SlCBF1 mutagenesis. J Agric Food Chem 66(34):9042–9051CrossRefGoogle Scholar
  110. Li S, Li J, Zhang J et al (2018e) Synthesis-dependent repair of Cpf1-induced double-strand DNA breaks enables targeted gene replacement in rice. J Exp Bot 69(20):4715–4721CrossRefPubMedPubMedCentralGoogle Scholar
  111. Li S, Zhang X, Wang W et al (2018f) Expanding the scope of CRISPR/Cpf1-mediated genome editing in rice. Mol Plant 11(7):995–998CrossRefGoogle Scholar
  112. Li X, Wang Y, Chen S et al (2018g) Lycopene is enriched in tomato fruit by CRISPR/Cas9-mediated multiplex genome editing. Front Plant Sci 9:559CrossRefPubMedPubMedCentralGoogle Scholar
  113. Li R, Liu C, Zhao R et al (2019) CRISPR/Cas9-Mediated SlNPR1 mutagenesis reduces tomato plant drought tolerance. BMC Plant Biol 19(1):38CrossRefPubMedPubMedCentralGoogle Scholar
  114. Liang Z, Zhang K, Chen K, Gao C (2014) Targeted mutagenesis in Zea mays using TALENs and the CRISPR/Cas system. J Genet Genom 41(2):63–68CrossRefGoogle Scholar
  115. Liang Z, Chen K, Li T et al (2017) Efficient DNA-free genome editing of bread wheat using CRISPR/Cas9 ribonucleoprotein complexes. Nat Commun 8:14261CrossRefPubMedPubMedCentralGoogle Scholar
  116. Liu L, Chen P, Wang M, Li X, Wang J, Yin M, Wang Y (2017) C2c1-sgRNA complex structure reveals RNA-guided DNA cleavage mechanism. Mol cell 65(2):310–322CrossRefGoogle Scholar
  117. Liu JJ, Orlova N, Oakes BL et al (2019) CasX enzymes comprise a distinct family of RNA-guided genome editors. Nature 566(7743):218CrossRefPubMedPubMedCentralGoogle Scholar
  118. Lowder LG, Paul JW, Qi Y (2017) Multiplexed transcriptional activation or repression in plants using CRISPR-dCas9-based systems. In: Kaufmann K, Mueller-Roeber B (eds) Plant gene regulatory networks. Humana Press, New York, pp 167–184CrossRefGoogle Scholar
  119. Lowder LG, Zhou J, Zhang Y et al (2018) Robust transcriptional activation in plants using multiplexed CRISPR-Act2. 0 and mTALE-Act systems. Mol Plant 11(2):245–256CrossRefGoogle Scholar
  120. Lu Y, Zhu JK (2017) Precise editing of a target base in the rice genome using a modified CRISPR/Cas9 system. Mol Plant 10(3):523–525CrossRefPubMedPubMedCentralGoogle Scholar
  121. Ma D, Peng S, Huang W, Cai Z, Xie Z (2018) Rational design of Mini-Cas9 for transcriptional activation. ACS Synth Biol 7(4):978–985CrossRefGoogle Scholar
  122. Ma C, Zhu C, Zheng M et al (2019) CRISPR/Cas9-mediated multiple gene editing in Brassica oleracea var. capitata using the endogenous tRNA-processing system. Horticult Res 6(1):20CrossRefGoogle Scholar
  123. Macovei A, Sevilla NR, Cantos C 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(11):1918–1927CrossRefPubMedPubMedCentralGoogle Scholar
  124. Makarova KS, Grishin NV, Shabalina SA et al (2006) A putative RNA-interference-based immune system in prokaryotes: computational analysis of the predicted enzymatic machinery, functional analogies with eukaryotic RNAi, and hypothetical mechanisms of action. Biol Direct 1(1):7CrossRefPubMedPubMedCentralGoogle Scholar
  125. Makarova KS, Wolf YI, Alkhnbashi OS et al (2015) An updated evolutionary classification of CRISPR–Cas systems. Nat Rev Microbiol 13(11):722CrossRefPubMedPubMedCentralGoogle Scholar
  126. Mali P, Aach J, Stranges PB, Esvelt KM et al (2013) CAS9 transcriptional activators for target specificity screening and paired nickases for cooperative genome engineering. Nat Biotechnol 31(9):833CrossRefPubMedPubMedCentralGoogle Scholar
  127. Malnoy M, Viola R, Jung MH et al (2016) DNA-free genetically edited grapevine and apple protoplast using CRISPR/Cas9 ribonucleoproteins. Front Plant Sci 7:1904CrossRefPubMedPubMedCentralGoogle Scholar
  128. Mao Y, Zhang H, Xu N, Zhang B, Gou F, Zhu JK (2013) Application of the CRISPR–Cas system for efficient genome engineering in plants. Mol Plant 6(6):2008–2011CrossRefPubMedPubMedCentralGoogle Scholar
  129. Martín-Pizarro C, Triviño JC, Posé D (2018) Functional analysis of the TM6 MADS-box gene in the octoploid strawberry by CRISPR/Cas9-directed mutagenesis. J Exp Bot 70(3):885–895CrossRefGoogle Scholar
  130. Marzec M, Hensel G (2018) Targeted base editing systems are available for plants. Trends Plant Sci 23(11):955–957CrossRefGoogle Scholar
  131. Masepohl B, Görlitz K, Böhme H (1996) Long tandemly repeated repetitive (LTRR) sequences in the filamentous cyanobacterium Anabaena sp. PCC 7120. Biochim Biophys Acta BBA Gene Struct Expr 1307(1):26–30CrossRefGoogle Scholar
  132. Miao J, Guo D, Zhang J et al (2013) Targeted mutagenesis in rice using a CRISPR-Cas system. Cell Res 23(10):1233CrossRefPubMedPubMedCentralGoogle Scholar
  133. Michno JM, Wang X, Liu J, Curtin SJ, Kono TJ, Stupar RM (2015) CRISPR/Cas mutagenesis of soybean and Medicago truncatula using a new web-tool and a modified Cas9 enzyme. GM Crops Food 6(4):243–252CrossRefPubMedPubMedCentralGoogle Scholar
  134. Mikami M, Toki S, Endo M (2016) Precision targeted mutagenesis via Cas9 paired nickases in rice. Plant Cell Physiol 57(5):1058–1068CrossRefPubMedPubMedCentralGoogle Scholar
  135. Miller JC, Tan S, Qiao (2011) A TALE nuclease architecture for efficient genome editing. Nat Biotechnol 29(2):143CrossRefGoogle Scholar
  136. Minkenberg B, Xie K, Yang Y (2017) Discovery of rice essential genes by characterizing a CRISPR-edited mutation of closely related rice MAP kinase genes. Plant J 89(3):636–648CrossRefPubMedPubMedCentralGoogle Scholar
  137. Mojica FJM, Ferrer C, Juez G, Rodriguez-Valera F (1995) Long stretches of short tandem repeats are present in the largest replicons of the Archaea Haloferax mediterranei and Haloferax volcanii and could be involved in replicon partitioning. Mol Microbiol 17(1):85–93CrossRefGoogle Scholar
  138. Mojica FJ, Díez-Villaseñor C, García-Martínez J et al (2009) Short motif sequences determine the targets of the prokaryotic CRISPR defense system. Microbiology 155(3):733–740CrossRefPubMedPubMedCentralGoogle Scholar
  139. Murovec J, Pirc Ž, Yang B (2017) New variants of CRISPR RNA-guided genome editing enzymes. Plant Biotechnol J 15(8):917–926CrossRefPubMedPubMedCentralGoogle Scholar
  140. Naim F, Dugdale B, Kleidon J, Brinin A, Shand K, Waterhouse P, Dale J (2018) Gene editing the phytoene desaturase alleles of Cavendish banana using CRISPR/Cas9. Transgenic Res 27(5):451–460CrossRefPubMedPubMedCentralGoogle Scholar
  141. Nakajima I, Ban Y, Azuma A, Onoue N et al (2017) CRISPR/Cas9-mediated targeted mutagenesis in grape. PLoS ONE 12(5):e0177966CrossRefPubMedPubMedCentralGoogle Scholar
  142. Nakayasu M, Akiyama R, Lee HJ 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 131:70–77CrossRefGoogle Scholar
  143. National Research Council (2000) The need for GM technology in agriculture. The National Academies Press, Washington, DC.  https://doi.org/10.17226/9889 CrossRefGoogle Scholar
  144. Nekrasov V, Staskawicz B, Weigel D et al (2013) Targeted mutagenesis in the model plant Nicotiana benthamiana using Cas9 RNA-guided endonuclease. Nat Biotechnol 31(8):691CrossRefPubMedPubMedCentralGoogle Scholar
  145. 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(1):482CrossRefPubMedPubMedCentralGoogle Scholar
  146. Nelson KE, Clayton RA, Gill SR et al (1999) Evidence for lateral gene transfer between Archaea and bacteria from the genome sequence of Thermotoga maritima. Nature 399(6734):323CrossRefGoogle Scholar
  147. Nieves-Cordones M, Mohamed S, Tanoi K et al (2017) Production of low-Cs + rice plants by inactivation of the K + transporter Os HAK 1 with the CRISPR-Cas system. Plant J 92(1):43–56CrossRefGoogle Scholar
  148. Nishimasu H, Ran FA, Hsu PD et al (2014) Crystal structure of Cas9 in complex with guide RNA and target DNA. Cell 156(5):935–949CrossRefPubMedPubMedCentralGoogle Scholar
  149. Nishimasu H, Cong L, Yan WX et al (2015) Crystal structure of Staphylococcus aureus Cas9. Cell 162(5):1113–1126CrossRefPubMedPubMedCentralGoogle Scholar
  150. Noman A, Aqeel M, He S (2016) CRISPR-Cas9: a tool for qualitative and quantitative plant genome editing. Front Plant Sci 7:1740CrossRefPubMedPubMedCentralGoogle Scholar
  151. O’Connell M (2019) Molecular mechanisms of RNA-targeting by Cas13-containing type VI CRISPR-Cas systems. J Mol Biol 431(1):66–87CrossRefGoogle Scholar
  152. Odipio J, Alicai T, Ingelbrecht I, Nusinow DA, Bart R, Taylor NJ (2017) Efficient CRISPR/Cas9 genome editing of phytoene desaturase in cassava. Front Plant Sci 8:1780CrossRefPubMedPubMedCentralGoogle Scholar
  153. Ortigosa A, Gimenez-Ibanez S, Leonhardt N, Solano R (2019) Design of a bacterial speck resistant tomato by CRISPR/Cas9-mediated editing of Sl JAZ 2. Plant Biotechnol J 17(3):665–673CrossRefPubMedPubMedCentralGoogle Scholar
  154. Pan C, Ye L, Qin L et al (2016) CRISPR/Cas9-mediated efficient and heritable targeted mutagenesis in tomato plants in the first and later generations. Sci Rep 6:24765CrossRefPubMedPubMedCentralGoogle Scholar
  155. Park JJ, Dempewolf E, Zhang W et al (2017) RNA-guided transcriptional activation via CRISPR/dCas9 mimics overexpression phenotypes in Arabidopsis. PLoS ONE 12(6):e0179410CrossRefPubMedPubMedCentralGoogle Scholar
  156. Peng A, Chen S, Lei T et al (2017) Engineering canker-resistant plants through CRISPR/Cas9-targeted editing of the susceptibility gene Cs LOB 1 promoter in citrus. Plant Biotechnol J 15(12):1509–1519CrossRefPubMedPubMedCentralGoogle Scholar
  157. Pérez L, Soto E, Farré G et al (2019) CRISPR/Cas9 mutations in the rice Waxy/GBSSI gene induce allele-specific and zygosity-dependent feedback effects on endosperm starch biosynthesis. Plant Cell Rep 38(3):417–433CrossRefGoogle Scholar
  158. Perez-Pinera P, Kocak DD, Vockley CM et al (2013) RNA-guided gene activation by CRISPR-Cas9–based transcription factors. Nat Methods 10(10):973CrossRefPubMedPubMedCentralGoogle Scholar
  159. 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(3):653–663CrossRefGoogle Scholar
  160. Qi LS, Larson MH, Gilbert LA et al (2013) Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression. Cell 152(5):1173–1183CrossRefPubMedPubMedCentralGoogle Scholar
  161. Qin R, Li J, Li H et al (2019) Developing a highly efficient and wildly adaptive CRISPR-SaCas9 toolset for plant genome editing. Plant Biotechnol J 17(4):706CrossRefPubMedPubMedCentralGoogle Scholar
  162. Raitskin O, Schudoma C, West A, Patron NJ (2019) Comparison of efficiency and specificity of CRISPR-associated (Cas) nucleases in plants: an expanded toolkit for precision genome engineering. PLoS ONE 14(2):e0211598CrossRefPubMedPubMedCentralGoogle Scholar
  163. Ran FA, Cong L, Yan WX et al (2015) In vivo genome editing using Staphylococcus aureus Cas9. Nature 520(7546):186CrossRefPubMedPubMedCentralGoogle Scholar
  164. Ron M, Kajala K, Pauluzzi G et al (2014) Hairy root transformation using Agrobacterium rhizogenes as a tool for exploring cell type-specific gene expression and function using tomato as a model. Plant Physiol 166(2):455–469CrossRefPubMedPubMedCentralGoogle Scholar
  165. Sadanandom A, Srivastava AK, Zhang C (2019) Targeted mutagenesis of the SUMO protease, overly tolerant to salt1 in rice through CRISPR/Cas9-mediated genome editing reveals a major role of this SUMO protease in salt tolerance. BioRxiv 555706Google Scholar
  166. Safari F, Zare K, Negahdaripour M, Barekati-Mowahed M, Ghasemi Y (2019) CRISPR Cpf1 proteins: structure, function and implications for genome editing. Cell Biosci 9(1):36CrossRefPubMedPubMedCentralGoogle Scholar
  167. Sánchez-León S, Gil-Humanes J, Ozuna CV, Giménez MJ, Sousa C, Voytas DF, Barro F (2018) Low-gluten, nontransgenic wheat engineered with CRISPR/Cas9. Plant Biotechnol J 16(4):902–910CrossRefPubMedPubMedCentralGoogle Scholar
  168. Sander JD, Joung JK (2014) CRISPR-Cas systems for editing, regulating, and targeting genomes. Nat Biotechnol 32(4):347CrossRefPubMedPubMedCentralGoogle Scholar
  169. Schiml S, Fauser F, Puchta H (2014) The CRISPR/C as the system can be used as nuclease for in planta gene targeting and as paired nickases for directed mutagenesis in Arabidopsis resulting in heritable progeny. Plant J 80(6):1139–1150CrossRefPubMedPubMedCentralGoogle Scholar
  170. Selma S, Bernabe-Orts J, Vazquez-Vilar M et al (2018) Strong gene activation with genome-wide specificity using a new orthogonal CRISPR/Cas9-based programmable transcriptional activator. BioRxiv 486068Google Scholar
  171. Sensen CW, Charlebois RL, Chow C et al (1998) Completing the sequence of the Sulfolobus solfataricus P2 genome. Extremophiles 2(3):305–312CrossRefGoogle Scholar
  172. Severinov K, Zhang F, Wolf Y et al (2017) Novel CRISPR enzymes and systems. U.S. patent application no. US15/482,603Google Scholar
  173. Shan Q, Wang Y, Li J et al (2013) Targeted genome modification of crop plants using a CRISPR-Cas system. Nat Biotechnol 31(8):686CrossRefPubMedPubMedCentralGoogle Scholar
  174. Shen C, Que Z, Xia Y, Tang N, Li D, He R, Cao M (2017a) Knock out of the annexin gene OsAnn3 via CRISPR/Cas9-mediated genome editing decreased cold tolerance in rice. J Plant Biol 60(6):539–547CrossRefGoogle Scholar
  175. Shen L, Hua Y, Fu Y et al (2017b) Rapid generation of genetic diversity by multiplex CRISPR/Cas9 genome editing in rice. Sci China Life Sci 60(5):506–515CrossRefGoogle Scholar
  176. Shi J, Gao H, Wang H et al (2017) ARGOS 8 variants generated by CRISPR-Cas9 improve maize grain yield under field drought stress conditions. Plant Biotechnol J 15(2):207–216CrossRefPubMedPubMedCentralGoogle Scholar
  177. Shiu SH, Bleecker AB (2001) Plant receptor-like kinase gene family: diversity, function, and signaling. Sci STKE 2001(113):re22–re22Google Scholar
  178. Shmakov S, Abudayyeh OO, Makarova KS et al (2015) Discovery and functional characterization of diverse class 2 CRISPR-Cas systems. Mol Cell 60(3):385–397CrossRefPubMedPubMedCentralGoogle Scholar
  179. Shmakov S, Smargon A, Scott D et al (2017) Diversity and evolution of class 2 CRISPR–Cas systems. Nat Rev Microbiol 15:169CrossRefPubMedPubMedCentralGoogle Scholar
  180. Smargon AA, Cox DB, Pyzocha NK et al (2017) Cas13b is a type VI-B CRISPR-associated RNA-guided RNase differentially regulated by accessory proteins Csx27 and Csx28. Mol Cell 65(4):618–630CrossRefPubMedPubMedCentralGoogle Scholar
  181. Smilovic M, Gleeson T, Adamowski J et al (2019) More food with less water—Optimizing agricultural water use. Adv Water Resour 123:256–261CrossRefGoogle Scholar
  182. Songmei L, Jie J, Yang L et al (2019) Characterization and evaluation of OsLCT1 and OsNramp5 mutants generated through CRISPR/Cas9-mediated mutagenesis for breeding low Cd rice. Rice Sci 26(2):88–97CrossRefGoogle Scholar
  183. Soyk S, Müller NA, Park SJ et al (2017) Variation in the flowering gene SELF PRUNING 5G promotes day-neutrality and early yield in tomato. Nat Genet 49(1):162CrossRefGoogle Scholar
  184. Srivastava V, Underwood JL, Zhao S (2017) Dual-targeting by CRISPR/Cas9 for precise excision of transgenes from rice genome. Plant Cell Tissue Organ Cult (PCTOC) 129(1):153–160CrossRefGoogle Scholar
  185. Steinert J, Schiml S, Fauser F, Puchta H (2015) Highly efficient heritable plant genome engineering using Cas9 orthologues from Streptococcus thermophilus and Staphylococcus aureus. Plant J 84(6):1295–1305CrossRefPubMedPubMedCentralGoogle Scholar
  186. Sternberg SH, Redding S, Jinek M et al (2014) DNA interrogation by the CRISPR RNA-guided endonuclease Cas9. Nature 507(7490):62CrossRefPubMedPubMedCentralGoogle Scholar
  187. Strecker J, Jones S, Koopal B et al (2019) Engineering of CRISPR-Cas12b for human genome editing. Nat Commun 10(1):212CrossRefPubMedPubMedCentralGoogle Scholar
  188. Sun X, Hu Z, Chen R, Jiang Q, Song G, Zhang H, Xi Y (2015) Targeted mutagenesis in soybean using the CRISPR-Cas9 system. Sci Rep 5:10342CrossRefPubMedPubMedCentralGoogle Scholar
  189. 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(2):931–945CrossRefPubMedPubMedCentralGoogle Scholar
  190. Svitashev S, Schwartz C, Lenderts B et al (2016) Genome editing in maize directed by CRISPR–Cas9 ribonucleoprotein complexes. Nat Commun 7:13274CrossRefPubMedPubMedCentralGoogle Scholar
  191. Swarts DC, Jinek M (2018) Cas9 versus Cas12a/Cpf1: structure-function comparisons and implications for genome editing. Wiley Interdiscip Rev RNA 9(5):e1481CrossRefGoogle Scholar
  192. Tak YE, Kleinstiver BP, Nuñez JK et al (2017) Inducible and multiplex gene regulation using CRISPR–Cpf1-based transcription factors. Nat Methods 14(12):1163CrossRefPubMedPubMedCentralGoogle Scholar
  193. Tanenbaum ME, Gilbert LA, Qi LS et al (2014) A protein-tagging system for signal amplification in gene expression and fluorescence imaging. Cell 159(3):635–646CrossRefPubMedPubMedCentralGoogle Scholar
  194. Tang L, Mao B, Li Y et al (2017a) Knockout of OsNramp5 using the CRISPR/Cas9 system produces low Cd-accumulating indica rice without compromising yield. Sci Rep 7(1):14438CrossRefPubMedPubMedCentralGoogle Scholar
  195. Tang X, Lowder LG, Zhang T et al (2017b) A CRISPR–Cpf1 system for efficient genome editing and transcriptional repression in plants. Nat Plants 3(3):17018CrossRefPubMedPubMedCentralGoogle Scholar
  196. Teng F, Cui T, Feng G et al (2018) Repurposing CRISPR-Cas12b for mammalian genome engineering. Cell Discov 4(1):63CrossRefPubMedPubMedCentralGoogle Scholar
  197. Tian S, Jiang L, Gao Q et al (2017) Efficient CRISPR/Cas9-based gene knockout in watermelon. Plant Cell Rep 36(3):399–406CrossRefPubMedPubMedCentralGoogle Scholar
  198. Tian S, Jiang L, Cui X et al (2018) Engineering herbicide-resistant watermelon variety through CRISPR/Cas9-mediated base-editing. Plant Cell Rep 37(9):1353–1356CrossRefPubMedPubMedCentralGoogle Scholar
  199. Tomlinson L, Yang Y, Emenecker R et al (2019) Using CRISPR/Cas9 genome editing in tomato to create a gibberellin-responsive dominant dwarf DELLA allele. Plant Biotechnol J 17(1):132–140CrossRefGoogle Scholar
  200. Tripathi JN, Ntui VO, Ron M, Muiruri SK, Britt A, Tripathi L (2019) CRISPR/Cas9 editing of endogenous banana streak virus in the B genome of Musa spp. overcomes a major challenge in banana breeding. Commun Biol 2(1):46CrossRefPubMedPubMedCentralGoogle Scholar
  201. Ueta R, Abe C, Watanabe T et al (2017) Rapid breeding of parthenocarpic tomato plants using CRISPR/Cas9. Sci Rep 7(1):507CrossRefPubMedPubMedCentralGoogle Scholar
  202. Upadhyay SK, Kumar J, Alok A, Tuli R (2013) RNA-guided genome editing for target gene mutations in wheat. G3 3(12):2233–2238CrossRefGoogle Scholar
  203. Van Vu T, Sivankalyani V, Kim EJ, et al (2019) Highly efficient homology-directed repair using transient CRISPR/Cpf1-geminiviral replicon in tomato. BioRxiv 521419Google Scholar
  204. 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(9):947CrossRefPubMedPubMedCentralGoogle Scholar
  205. Wang F, Wang C, Liu P et al (2016) Enhanced rice blast resistance by CRISPR/Cas9-targeted mutagenesis of the ERF transcription factor gene OsERF922. PLoS ONE 11(4):e0154027CrossRefPubMedPubMedCentralGoogle Scholar
  206. Wang L, Chen L, Li R, Zhao R, Yang M, Sheng J, Shen L (2017a) Reduced drought tolerance by CRISPR/Cas9-mediated SlMAPK3 mutagenesis in tomato plants. J Agric Food Chem 65(39):8674–8682CrossRefPubMedPubMedCentralGoogle Scholar
  207. Wang Y, Geng L, Yuan M et al (2017b) Deletion of a target gene in Indica rice via CRISPR/Cas9. Plant Cell Rep 36(8):1333–1343CrossRefGoogle Scholar
  208. Wang M, Mao Y, Lu Y, Wang Z, Tao X, Zhu JK (2018a) Multiplex gene editing in rice with simplified CRISPR-Cpf1 and CRISPR-Cas9 systems. J Integr Plant Biol 60(8):626–631CrossRefGoogle Scholar
  209. Wang W, Pan Q, He F, Akhunova A, Chao S, Trick H, Akhunov E (2018b) Transgenerational CRISPR-Cas9 activity facilitates multiplex gene editing in allopolyploid wheat. CRISPR J 1(1):65–74CrossRefPubMedPubMedCentralGoogle Scholar
  210. Wang X, Tu M, Wang D et al (2018c) CRISPR/Cas9-mediated efficient, targeted mutagenesis in grape in the first generation. Plant Biotechnol J 16(4):844–855CrossRefPubMedPubMedCentralGoogle Scholar
  211. Wang Z, Wang S, Li D et al (2018d) Optimized paired-sgRNA/Cas9 cloning and expression cassette triggers high-efficiency multiplex genome editing in kiwifruit. Plant Biotechnol J 16(8):1424–1433CrossRefPubMedPubMedCentralGoogle Scholar
  212. Wang D, Samsulrizal NH, Yan C et al (2019a) Characterization of CRISPR mutants targeting genes modulating pectin degradation in ripening tomato. Plant Physiol 179(2):544–557PubMedGoogle Scholar
  213. Wang R, da Rocha Tavano EC, Lammers M, Martinelli AP, Angenent GC, de Maagd RA (2019b) Re-evaluation of transcription factor function in tomato fruit development and ripening with CRISPR/Cas9-mutagenesis. Sci Rep 9(1):1696CrossRefPubMedPubMedCentralGoogle Scholar
  214. Wang X, Han Y, Feng X et al (2019c) Breeding of Indica glutinous cytoplasmic male sterile line WX209A via CRISPR/Cas9 mediated genomic editing. Czech J Genet Plant Breed 55:93–100CrossRefGoogle Scholar
  215. Wei L, Qi Z, Teng F (2019) Genome editing system and method based on C2c1 nuclease. CN patent no. 109337904Google Scholar
  216. Wolter F, Klemm J, Puchta H (2018) Efficient in planta gene targeting in Arabidopsis using egg cell-specific expression of the Cas9 nuclease of Staphylococcus aureus. Plant J 94(4):735–746CrossRefGoogle Scholar
  217. Woo JW, Kim J, Kwon SI et al (2015) DNA-free genome editing in plants with preassembled CRISPR-Cas9 ribonucleoproteins. Nat Biotechnol 33(11):1162CrossRefPubMedPubMedCentralGoogle Scholar
  218. Wood AJ, Lo TW, Zeitler B et al (2011) Targeted genome editing across species using ZFNs and TALENs. Science 333(6040):307CrossRefPubMedPubMedCentralGoogle Scholar
  219. Wu D, Guan X, Zhu Y, Ren K, Huang Z (2017) Structural basis of stringent PAM recognition by CRISPR-C2c1 in complex with sgRNA. Cell Res 27(5):705CrossRefPubMedPubMedCentralGoogle Scholar
  220. Xiao B, Huang Y, Tang N, Xiong L (2007) Over-expression of a LEA gene in rice improves drought resistance under the field conditions. Theor Appl Genet 115(1):35–46CrossRefGoogle Scholar
  221. Xie Z, Ma D (2018) Engineering of a minimal SaCas9 CRISPR/Cas system for gene editing and transcriptional regulation optimized by enhanced guide RNA. U.S. Patent Application No. 15/619,518Google Scholar
  222. Xie K, Yang Y (2013) RNA-guided genome editing in plants using a CRISPR–Cas system. Mol Plant 6(6):1975–1983CrossRefPubMedPubMedCentralGoogle Scholar
  223. Xie K, Minkenberg B, Yang Y (2015) Boosting CRISPR/Cas9 multiplex editing capability with the endogenous tRNA-processing system. Proc Natl Acad Sci 112(11):3570–3575CrossRefGoogle Scholar
  224. Xing HL, Dong L, Wang ZP et al (2014) A CRISPR/Cas9 toolkit for multiplex genome editing in plants. BMC Plant Biol 14(1):327CrossRefPubMedPubMedCentralGoogle Scholar
  225. Xu C, Liberatore KL, MacAlister CA, Huang Z et al (2015a) A cascade of arabinosyltransferases controls shoot meristem size in tomato. Nat Genet 47(7):784CrossRefGoogle Scholar
  226. Xu RF, Li H, Qin RY et al (2015b) Generation of inheritable and “transgene clean” targeted genome-modified rice in later generations using the CRISPR/Cas9 system. Sci Rep 5:11491CrossRefPubMedPubMedCentralGoogle Scholar
  227. Xu C, Park SJ, Van Eck J, Lippman ZB (2016) Control of inflorescence architecture in tomato by BTB/POZ transcriptional regulators. Genes Dev 30(18):2048–2061CrossRefPubMedPubMedCentralGoogle Scholar
  228. Xu R, Qin R, Li H, Li D, Li L, Wei P, Yang J (2017) Generation of targeted mutant rice using a CRISPR-Cpf1 system. Plant Biotechnol J 15(6):713–717CrossRefPubMedPubMedCentralGoogle Scholar
  229. Xu ZS, Feng K, Xiong AS (2019) CRISPR/Cas9-mediated multiply targeted mutagenesis in orange and purple carrot plants. Mol Biotechnol 61(3):191–199CrossRefGoogle Scholar
  230. Yamano T, Nishimasu H, Zetsche B et al (2016) Crystal structure of Cpf1 in complex with guide RNA and target DNA. Cell 165(4):949–962CrossRefPubMedPubMedCentralGoogle Scholar
  231. Yamano T, Nishimasu H, Zetsche B et al (2017) Crystal structure of CRISPR Cpf1. European patent no. 3405570A1. European Patent Office, MunichGoogle Scholar
  232. Yang H, Gao P, Rajashankar KR, Patel DJ (2016) PAM-dependent target DNA recognition and cleavage by C2c1 CRISPR-Cas endonuclease. Cell 167(7):1814–1828CrossRefPubMedPubMedCentralGoogle Scholar
  233. Yin X, Biswal AK, Dionora J, Perdigon KM et al (2017) CRISPR-Cas9 and CRISPR-Cpf1 mediated targeting of a stomatal developmental gene EPFL9 in rice. Plant Cell Rep 36(5):745–757CrossRefPubMedPubMedCentralGoogle Scholar
  234. Yu QH, Wang B, Li N et al (2017) CRISPR/Cas9-induced targeted mutagenesis and gene replacement to generate long-shelf-life tomato lines. Sci Rep 7(1):11874CrossRefPubMedPubMedCentralGoogle Scholar
  235. Zetsche B, Gootenberg JS, Abudayyeh OO et al (2015a) Cpf1 is a single RNA-guided endonuclease of class 2 CRISPR-Cas system. Cell 163(3):759–771CrossRefPubMedPubMedCentralGoogle Scholar
  236. Zetsche B, Volz SE, Zhang F (2015b) A split-Cas9 architecture for inducible genome editing and transcription modulation. Nat Biotechnol 33(2):139CrossRefGoogle Scholar
  237. Zhang H, Zhang J, Wei P et al (2014) The CRISPR/C as9 system produces specific and homozygous targeted gene editing in rice in one generation. Plant Biotechnol J 12(6):797–807CrossRefPubMedPubMedCentralGoogle Scholar
  238. Zhang F, Cong L, Fei RAN et al (2016a) U.S. patent application no. 14/970,967Google Scholar
  239. Zhang Y, Liang Z, Zong Y et al (2016b) Efficient and transgene-free genome editing in wheat through transient expression of CRISPR/Cas9 DNA or RNA. Nat Commun 7:12617CrossRefPubMedPubMedCentralGoogle Scholar
  240. Zhang F, LeBlanc C, Irish VF, Jacob Y (2017) Rapid and efficient CRISPR/Cas9 gene editing in citrus using the YAO promoter. Plant Cell Rep 36(12):1883–1887CrossRefPubMedPubMedCentralGoogle Scholar
  241. Zhang J, Zhang H, Botella JR, Zhu JK (2018a) Generation of new glutinous rice by CRISPR/Cas9-targeted mutagenesis of the Waxy gene in elite rice varieties. J Integr Plant Biol 60(5):369–375CrossRefPubMedPubMedCentralGoogle Scholar
  242. Zhang X, Wang W, Shan L et al (2018b) Gene activation in human cells using CRISPR/Cpf1-p300 and CRISPR/Cpf1-SunTag systems. Protein Cell 9(4):380–383PubMedGoogle Scholar
  243. Zhang F, Zetsche B, Gootenberg JS, Abudayyeh OO, Slaymaker I (2019a) Novel CRISPR enzymes and systems. U.S. Patent Application No. 15/844,608Google Scholar
  244. Zhang Y, Zhang Y, Qi Y (2019b) Plant gene knockout and knockdown by CRISPR-Cpf1 (Cas12a) systems. In: Qi Y (ed) Plant genome editing with CRISPR systems, vol 1917. Humana Press, New York, pp 245–256CrossRefGoogle Scholar
  245. Zhou J, Deng K, Cheng Y et al (2017a) CRISPR-Cas9 based genome editing reveals new insights into microRNA function and regulation in rice. Front Plant Sci 8:1598CrossRefPubMedPubMedCentralGoogle Scholar
  246. Zhou X, Zha M, Huang J, Li L, Imran M, Zhang C (2017b) StMYB44 negatively regulates phosphate transport by suppressing the expression of PHOSPHATE1 in potato. J Exp Bot 68(5):1265–1281CrossRefPubMedPubMedCentralGoogle Scholar
  247. Zhu Z, Kang X, Lor VS, Weiss D, Olszewski N (2019) Characterization of a semi-dominant dwarfing PROCERA allele identified in a screen for CRISPR/Cas9-induced suppressors of loss-of-function alleles. Plant Biotechnol J 17(2):319CrossRefGoogle Scholar
  248. Zong Y, Wang Y, Li C et al (2017) Precise base editing in rice, wheat, and maize with a Cas9-cytidine deaminase fusion. Nat Biotechnol 35(5):438CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Washington State UniversityPullmanUSA

Personalised recommendations