Skip to main content
SpringerLink
Log in

Achievements, Challenges, and Prospects in the Production of Nontransgenic, Genome-Edited Plants

  • PROBLEMS AND PROSPECTS
  • Published:
Applied Biochemistry and Microbiology Aims and scope Submit manuscript

Abstract

The review summarizes the problems, achievements, and prospects of various approaches related to the delivery of components of DNA editing systems to plant cells, the regeneration of whole plants with an edited genome, and the development of transgene-free or transgene-clean crops. Here, an attempt was made to systematize the results of various studies describing the successful production of genome-edited (GE) plants with various genome modifications/mutations via the application of nuclease DNA–editing systems (ZFN, TALEN, and CRISPR/Cas). We discuss the main directions for the development of nuclease-based genome-editing methods to obtain GE plants free of foreign sequences from genome-editing tools.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.

Similar content being viewed by others

REFERENCES

  1. Feng, Z.Y., Zhang, B.T., Ding, W.N., et al., Efficient genome editing in plants using a CRISPR/Cas system, Cell Res., 2013, vol. 23, pp. 1229–1232. https://doi.org/10.1038/cr.2013.114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Shan, Q., Wang, Y., Li, J., et al., Targeted genome modification of crop plants using a CRISPR-Cas system, Nat. Biotechnol., 2013, vol. 31, no. 8, pp. 686–688. https://doi.org/10.1038/nbt.2650

    Article  CAS  PubMed  Google Scholar 

  3. Nekrasov, V., Staskawicz, B., Weigel, D., et al., Targeted genome modification of crop plants using a CRISPR-Cas system, Nat. Biotechnol., 2013, vol. 31, no. 8, pp. 686–688. https://doi.org/10.1038/nbt.2650

    Article  CAS  Google Scholar 

  4. Davies, J.P., Kumar, S., and Sastry-Dent, L., Use of Zinc-finger nucleases for crop improvement, Prog. Mol. Biol. Transl. Sci., 2017, vol. 149, pp. 47–63. https://doi.org/10.1016/bs.pmbts.2017.03.006

    Article  PubMed  Google Scholar 

  5. Khan, Z., Khan, S.H., Mubarik, M.S., et al., Use of TALEs and TALEN technology for genetic improvement of plants, Plant Mol. Biol. Rep., 2017, vol. 35, no. 1, pp. 1–19. https://doi.org/10.1007/s11105-016-0997-8

    Article  CAS  Google Scholar 

  6. Belhaj, K., Chaparro-Garcia, A., Kamoun, S., et al., Editing plant genomes with CRISPR/Cas9, Curr. Opin. Biotechnol., 2015, vol. 32, pp. 76–84. https://doi.org/10.1016/j.copbio.2014.11.007

    Article  CAS  PubMed  Google Scholar 

  7. Scheben, A., Wolter, F., Batley, J., et al., Towards CRISPR/Cas crops - bringing together genomics and genome editing, New Phytologist, 2017, vol. 216, pp. 682–698. https://doi.org/10.1111/nph.14702

    Article  CAS  PubMed  Google Scholar 

  8. Jaganathan, D., Ramasamy, K., Sellamuthu, G., et al., CRISPR for crop improvement: an update review, Front. Plant Sci., 2018, vol. 9, p. 985. https://doi.org/10.3389/fpls.2018.00985

    Article  PubMed  PubMed Central  Google Scholar 

  9. Schindele, P., Wolter, F., and Puchta, H., Transforming plant biology and breeding with CRISPR/Cas9, Cas12 and Cas13, FEBS Lett., 2018, vol. 592, no.12, pp. 1954–1967. https://doi.org/10.1002/1873-3468.13073

    Article  CAS  PubMed  Google Scholar 

  10. Romay, G. and Bragard, C., Antiviral defenses in plants through genome editing, Front. Microbiol., 2017, vol. 8, p. 47. https://doi.org/10.3389/fmicb.2017.00047

    Article  PubMed  PubMed Central  Google Scholar 

  11. Zhang, H., Zhang, J., Lang, Z., et al., Genome editing—principles and applications for functional genomics research and crop improvement, Crit. Rev. Plant Sci., 2017, vol. 36, no. 4, pp. 291–309. https://doi.org/10.1080/07352689.2017.1402989

    Article  Google Scholar 

  12. Arora, L. and Narula, A., Gene Editing and crop improvement using CRISPR-Cas9 system. Front. Plant Sci. 2017, vol. 8, pp. 1932. https://doi.org/10.3389/fpls.2017.01932

    Article  PubMed  PubMed Central  Google Scholar 

  13. Mushtaq, M., Bhat, J.A., Mir, Z.A., et al., CRISPR/Cas approach: a new way of looking at plant-abiotic interactions, J. Plant Physiol., 2018, vol. 224–225, pp. 156–162. https://doi.org/10.1016/j.jplph.2018.04.001

    Article  CAS  PubMed  Google Scholar 

  14. Jiang, W.Z., Henry, I.M., Lynagh, P.G., et al., Significant enhancement of fatty acid composition in seeds of the allohexaploid, Camelina sativa, using CRISPR/Cas9 gene editing, Plant Biotechnol. J., 2017, vol. 159, no. 5, pp. 648–657. https://doi.org/10.1111/pbi.12663

    Article  CAS  Google Scholar 

  15. Walts, E., With a free pass, CRISPR-edited plants reach market in record time, Nat. Biotechnol., 2018, vol. 36, no. 1, pp. 6–7. https://doi.org/10.1038/nbt0118-6b

    Article  CAS  Google Scholar 

  16. Jansson, S., Gene-edited plants on the plate: the ‘CRISPR cabbage story,’ Physiol. Plant, 2018, vol. 164, no. 4, pp. 396–495.

    Article  CAS  PubMed  Google Scholar 

  17. Callaway, E., CRISPR plants now subject to tough GM laws in European Union, Nature, 2018, vol. 560, no. 7716, p. 16. https://doi.org/10.1038/d41586-018-05814-6

    Article  CAS  PubMed  Google Scholar 

  18. Lloyd, A., Plaisier, C.L., Carroll, D., and Drews, G.N., Targeted mutagenesis using zinc-finger nucleases in Arabidopsis,Proc. Natl. Acad. Sci. U. S. A, 2005, vol. 102, pp. 2232–2237. https://doi.org/10.1073/pnas.0409339102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Kuluev, B.R., Gerashchenkov, G.A., Rozhnova, N.A., et al., CRISPR/Cas Plant genome editing, Biomika, 2017, vol. 9, no. 3, pp. 155–182.

    Google Scholar 

  20. Yamaguchi, Y.L., Ishida, T., Yoshimura, M., et al., A collection of mutants for CLE-peptide-encoding genes in Arabidopsis generated by CRISPR/Cas9-mediated gene targeting, Plant Cell Physiol., 2017, vol. 58, no. 11, pp. 1848–1856. https://doi.org/10.1093/pcp/pcx13

    Article  CAS  PubMed  Google Scholar 

  21. Zhang, H., Zhang, J.S., Wei, P.L., et al., The CRISPR/Cas9 system produces specific and homozygous targeted gene editing in rice in one generation, Plant Biotechnol. J., 2014, vol. 12, pp. 797–807. https://doi.org/10.1111/pbi.12200

    Article  CAS  PubMed  Google Scholar 

  22. Qi, W., Zhu, T., Tian, Z., et al., High-efficiency CRISPR/ Cas9 multiplex gene editing using the glycine tRNA-processing system-based strategy in maize, BMC Biotechnol., 2016, vol. 16, no. 1, pp. 58. https://doi.org/10.1186/s12896-016-0289-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Kaya, H., Mikami, M., Endo, A., et al., Highly specific targeted mutagenesis in plants using Staphylococcus aureus Cas9, Sci. Rep., 2016, vol. 6, p. 26871. https://doi.org/10.1038/srep26871

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Ma, X.L., Zhang, Q.Y., Zhu, Q.L., et al., A robust CRISPR/ Cas9 system for convenient, high-efficiency multiplex genome editing in monocot and dicot plants, Mol. Plant, 2015, vol. 8, no. 8, pp. 1274–1284. https://doi.org/10.1016/j.molp.2015.04.007

    Article  CAS  PubMed  Google Scholar 

  25. Lowder, L.G., Zhang, D.W., Baltes, N.J., et al., A CRISPR/Cas9 toolbox for multiplexed plant genome editing and transcriptional regulation, Plant Physiol., 2015, vol. 169, pp. 971–985. https://doi.org/10.1104/pp.15.00636

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Shan, Q.W., Wang, Y.P., Li, J., and Gao, C.X., Genome editing in rice and wheat using the CRISPR/Cas system, Nat. Protoc., 2014, vol. 9, pp. 2340–2395. https://doi.org/10.1038/nprot.2014.157

    Article  CAS  Google Scholar 

  27. Xing, H.L., Dong, L., Wang, Z.P., et al., A CRISPR/Cas9 toolkit for multiplex genome editing in plants, BMC Plant Biol., 2014, vol. 14, pp. 327. https://doi.org/10.1186/s12870-014-0327-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Lawrenson, T., Shorinola, O., Stacey, N., et al., Induction of targeted, heritable mutations in barley and Brassica oleracea using RNA-guided Cas9 nuclease, Genome Biol., 2015, vol. 16, pp. 258. https://doi.org/10.1186/s13059-015-0826-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Cigan, A.M., Singh, M., Benn, G., et al., Targeted mutagenesis of a conserved anther-expressed P450 gene confers male sterility in monocots, Plant Biotechnol. J., 2017, vol. 15, pp. 379–389. https://doi.org/10.1111/pbi.12633

    Article  CAS  PubMed  Google Scholar 

  30. Holme, I.B., Wendt, T., Gil-Humanes, J., et al., Evaluation of the mature grain phytase candidate HvPAPhy_a gene in barley (Hordeum vulgare L.) using CRISPR/Cas9 and TALENs. Plant Mol. Biol. 2017, vol. 95 (1–2, pp. 111–121. https://doi.org/10.1007/s11103-017-0640-6

  31. Wang, Y., Cheng, X., Shan, Q., et al., Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew, Nat. Biotechnol., 2014, vol. 32, pp. 947–951. https://doi.org/10.1038/nbt.2969

    Article  CAS  PubMed  Google Scholar 

  32. Curtin, S.J., Xiong, Y., Michno, J.M., et al., CRISPR/Cas9 and TALENs generate heritable mutations for genes involved in small RNA processing of Glycine max and Medicago truncatula,Plant Biotechnol. J., 2018, vol. 16, no. 6, pp. 1125–1137. https://doi.org/10.1111/pbi.12857

    Article  CAS  PubMed  Google Scholar 

  33. Gallego-Bartolome, J., Gardiner, J., Liu, W., et al., Targeted DNA demethylation of the Arabidopsis genome using the human TET1 catalytic domain, Proc. Natl. Acad. Sci. U. S. A., 2018, vol. 115, no. 9, pp. 2125–2134. https://doi.org/10.1073/pnas.1716945115

    Article  CAS  Google Scholar 

  34. Cermak, T., Doyle, E.L., Christian, M., et al., Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting, Nucleic Acids Res., 2011, vol. 39, no. 11. e82. https://doi.org/10.1093/nar/gkr218

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Li, T., Liu, B., Spalding, M.H., et al., High-efficiency TALEN-based gene editing produces disease-resistance, Nat. Biotechnol., 2012, vol. 30, pp. 390–392. https://doi.org/10.1038/nbt.2199

    Article  CAS  PubMed  Google Scholar 

  36. Clasen, B.M., Stoddard, T.J., Luo, S., et al., Improving cold storage and processing traits in potato through targeted gene knockout, Plant Biotechnol. J., 2016, vol. 14, pp. 169–176.

    Article  CAS  PubMed  Google Scholar 

  37. Li, J., Stoddard, T.J., Demorest, Z.L., et al., Multiplexed, targeted gene editing in Nicotiana benthamiana for glyco-engineering and monoclonal antibody production, Plant Biotechnol. J., 2016, vol. 14, pp. 533–542.

    Article  CAS  PubMed  Google Scholar 

  38. Woo, J.W., Kim, J., Kwon, S.I., et al., DNA-free genome editing in plants with preassembled CRISPR-Cas9 ribonucleoproteins, Nat. Biotechnol., 2015, vol. 33, no. 11, pp. 1162–1164. https://doi.org/10.1038/nbt.3389

    Article  CAS  PubMed  Google Scholar 

  39. Sauer, N.J., Narvaez-Vasquez, J., Mozoruk, J., et al., Oligonucleotide-mediated genome editing provides precision and function to engineered nucleases and antibiotics in plants, Plant Physiol., 2016, vol. 170, no. 4, pp. 1917–1928.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Zhang, Q., Xing, H.L., Wang, Z.P., et al., Potential high-frequency off-target mutagenesis induced by CRISPRCas9 in Arabidopsis and its prevention, Plant Mol. Biol., 2018, vol. 96, pp. 445–456. https://doi.org/10.1007/s11103-018-0709-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Zhang, H.Y., Wang, X.H., Dong, L., et al., MISSA 2.0: an updated synthetic biology toolbox for assembly of orthogonal CRISPR/Cas systems, Sci. Rep., 2017, vol. 7, pp. 41993. https://doi.org/10.1038/srep41993

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Xu, R.F., Li, H., Qin, R.Y., et al., Generation of inheritable and “transgene clean” targeted genome-modified rice in later generations using the CRISPR/Cas9 system, Sci. Rep., 2015, vol. 5, pp. 11491. https://doi.org/10.1038/srep11491

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Clough, S.J. and Bent, A.F., Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana,Plant J., 1998, vol. 16, pp. 735–743. https://doi.org/10.1046/j.1365-313x.1998.00343.x

    Article  CAS  PubMed  Google Scholar 

  44. de Pater, S., Neuteboom, L.W., Pinas, J.E., et al., ZFN-induced mutagenesis and gene-targeting in Arabidopsis through Agrobacterium-mediated floral dip transformation, Plant Biotech. J., 2009, vol. 7, pp. 821–835. https://doi.org/10.1111/j.1467-7652.2009.00446.x

    Article  CAS  Google Scholar 

  45. Chandrasekaran, J., Brumin, M., Wolf, D., et al., Development of broad virus resistance in non-transgenic cucumber using CRISPR/Cas9 technology, Mol. Plant Pathol., 2016, vol. 17, no. 7, pp. 1140–1153. https://doi.org/10.1111/mpp.12375

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Gao, Y., Zhang, Y., Zhang, D., et al., Auxin binding protein 1 (ABP1) is not required for either auxin signaling or Arabidopsis development, Proc. Natl. Acad. Sci. U. S. A., 2015, vol. 112, no. 7, pp. 2275–2280. https://doi.org/10.1073/pnas.1500365112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Shi, J., Gao, H., Wang, H., et al., ARGOS8 variants generated by CRISPR/Cas9 improve maize grain yield under field drought stress conditions, Plant Biotechnol. J., 2017, vol. 15, no. 2, pp. 207–216. https://doi.org/10.1111/pbi.12603

    Article  CAS  PubMed  Google Scholar 

  48. Okuzaki, A., Ogawa, T., Koizuka, C., et al., CRISPR/ Cas9-mediated genome editing of the fatty acid desaturase 2 gene in Brassica napus,Plant Physiol. Biochem., 2018, vol. 131, pp. 63–69. https://doi.org/10.1016/j.plaphy.2018.04.025

    Article  CAS  PubMed  Google Scholar 

  49. Klap, C., Yeshayahou, E., Bolger, A.M., et al., Tomato facultative parthenocarpy results from Sl AGAMOUS–LIKE 6 loss of function, Plant Biotechnol. J., 2017, vol. 15 (5, pp. 634–647. https://doi.org/10.1111/pbi.12662

  50. Rodríguez-Leal, D., Lemmon, Z.H., Man, J., et al., Engineering quantitative trait variation for crop improvement by genome editing, Cell, 2017, vol. 171, no. 2, pp. 470–480. e8. https://doi.org/10.1016/j.cell.2017.08.030

  51. Sánchez-Leon S., Gil-Humanes J., Ozuna C.V., et al. Low-gluten, nontransgenic wheat engineered with CRISPR/Cas9, Plant. Biotechnol. J., 2018, vol. 16, no. 4, pp. 902–910. https://doi.org/10.1111/pbi.12837

    Article  CAS  PubMed  Google Scholar 

  52. Ran, Y., Patron, N., Kay, P., et al., Zinc finger nuclease-mediated precision genome editing of an endogenous gene in hexaploid bread wheat (Triticum aestivum) using a DNA repair template, Plant. Biotechnol. J., 2018, vol. 16, no. 12, pp. 2088–2101. https://doi.org/10.1111/pbi.12941

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Li, T., Liu, B., Chen, C.Y., and Yang, B., TALEN-mediated homologous recombination produces site-directed DNA base change and herbicide-resistant rice, J. Genet. Genomics, 2016, vol. 43, pp. 297–305. https://doi.org/10.1016/j.jgg.2016.03

    Article  PubMed  Google Scholar 

  54. Blanvillain-Baufume, S., Reschke, M., Sole, M., et al., Targeted promoter editing for rice resistance to Xanthomonas oryzae pv. oryzae reveals differential activities for SWEET14-inducing TAL effectors, Plant Biotechnol. J., 2017, vol. 15, no. 3, pp. 306–317. https://doi.org/10.1111/pbi.12613

    Article  CAS  PubMed  Google Scholar 

  55. Ambrosio, C., Stigliani, A.L., and Giorio, G., CRISPR/Cas9 editing of carotenoid genes in tomato, Transgenic Res., 2018, pp. 27, no. 4, pp. 367–378. https://doi.org/10.1007/s11248-018-0079-9

  56. Wang, P., Zhang, J., Sun, L., et al., High efficient multisites genome editing in allotetraploid cotton (Gossypium hirsutum) using CRISPR/Cas9 system, Plant Biotechnol. J., 2018, vol. 16, no. 1, pp. 137–150. https://doi.org/10.1111/pbi.12755

    Article  CAS  PubMed  Google Scholar 

  57. Feng, Z., Mao, Y., Xu, N., et al., Multigeneration analysis reveals the inheritance, specificity, and patterns of CRISPR/Cas-induced gene modifications in Arabidopsis,Proc. Natl. Acad. Sci. U. S. A., 2014, vol. 25, no. 12, pp. 4632–4637. https://doi.org/10.1073/pnas.1400822111

    Article  CAS  Google Scholar 

  58. Tsutsui, H. and Higashiyama, T., pKAMA-ITACHI vectors for highly efficient CRISPR/cas9-mediated gene knockout in Arabidopsis thaliana, Plant Cell Physiol., 2017, vol. 58, no. 1, pp., 46–56. https://doi.org/10.1093/pcp/pcw191

  59. Gao, X., Chen, J., Dai, X., et al., An effective strategy for reliably isolating heritable and Cas9-free Arabidopsis mutants generated by CRISPR/Cas9-mediated genome editing, Plant Physiol., 2016, vol. 171, no. 3, pp. 1794–1800. https://doi.org/10.1104/pp.16.00663

    Article  PubMed  PubMed Central  Google Scholar 

  60. Hu, B., Li, D., Liu, X., et al., Engineering non-transgenic gynoecious cucumber using an improved transformation protocol and optimized CRISPR/Cas9 system, Mol. Plant, 2017, vol. 10, no. 12, pp. 1575–1578. https://doi.org/10.1016/j.molp.2017.09.005

    Article  CAS  PubMed  Google Scholar 

  61. Lu, H.P., Liu, S.M., Xu, S.L., et al., CRISPR-S: an active interference element for a rapid and inexpensive selection of genome-edited, transgene-free rice plants, Plant Biotechnol. J., 2017, vol. 15, no. 11, pp. 1371–1373. https://doi.org/10.1111/pbi.12788

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. He, Y., Zhu, M., Wang, L., Wu, J., et al., Programmed self-elimination of the CRISPR/Cas9 construct greatly accelerates the isolation of edited and transgene-free rice plants, Mol. Plant, 2018, vol. 11, no. 9, pp. 1210–1213. https://doi.org/10.1016/j.molp.2018.05.005

    Article  CAS  PubMed  Google Scholar 

  63. Ran, Y., Liang, Z., and Gao, C., Current and future editing reagent delivery systems for plant genome editing, Sci. China Life Sci., 2017, vol. 60, no. 5, pp. 490–505. https://doi.org/10.1007/s11427-017-9022-1

    Article  CAS  PubMed  Google Scholar 

  64. Jiang, W., Zhou, H., Bi, H., et al., Demonstration of CRISPR/Cas9/sgRNA-mediated targeted gene modification in Arabidopsis, tobacco, sorghum and rice. Nucleic Acids Res., 2013, vol. 41, no. 20, pp. e188. https://doi.org/10.1093/nar/gkt780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Lin, C.S., Hsu, C.T., Yang, L.H., et al., Application of protoplast technology to CRISPR/Cas9 mutagenesis: from single-cell mutation detection to mutant plant regeneration, Plant Biotechnol. J., 2018, vol. 16, no. 7, pp. 1295–1310. https://doi.org/10.1111/pbi.12870

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Andersson, M., Turesson, H., Nicolia, A., et al., Efficient targeted multiallelic mutagenesis in tetraploid potato (Solanum tuberosum) by transient CRISPR-Cas9 expression in protoplasts, Plant Cell Rep., 2017, vol. 36, no. 1, pp. 117–128. https://doi.org/10.1007/s00299-016-2062-3

    Article  CAS  PubMed  Google Scholar 

  67. Zhang, Y., Liang, Z., Zong, Y., et al., Efficient and transgene-free genome editing in wheat through transient expression of CRISPR/Cas9 DNA or RNA, Nat. Commun., 2016, vol. 7, p. 12617. https://doi.org/10.1038/ncomms12617

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Zong, Y., Wang, Y., Li, C., et al., Precise base editing in rice, wheat and maize with a Cas9- cytidine deaminase fusion. Nat. Biotechnol. 2017, vol. 35 (5), pp. 438–440. https://doi.org/10.1038/nbt.3811

  69. Li, C., Zong, Y., Wang, Y., et al., Expanded base editing in rice and wheat using a Cas9-adenosine deaminase fusion, Genome Biol., 2018, vol. 19, pp. 59. https://doi.org/10.1186/s13059-018-1443-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Svitashev, S., Young, J.K., Schwartz, C., et al., Targeted mutagenesis, precise gene editing, and site-specific gene insertion in maize using Cas9 and guide RNA, Plant Physiol., 2015, vol. 169, no. 2, pp. 931–945. https://doi.org/10.1104/pp.15.00793

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Luo, S., Li, J., Stoddard, T.J., et al., Non-transgenic plant genome editing using purified sequence-specific nucleases, Mol. Plant, 2015, vol. 8, no. 9, pp. 1425–1427.

    Article  CAS  PubMed  Google Scholar 

  72. Svitashev, S., Schwartz, C., Lenderts, B., et al., Genome editing in maize directed by CRISPR–Cas9 ribonucleoprotein complexes, Nat. Commun., 2016, vol. 7, pp. 13274. https://doi.org/10.1038/ncomms13274

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Liang, Z., Chen, K., Li, T., et al., Efficient DNA-free genome editing of bread wheat using CRISPR/Cas9 ribonucleoprotein complexes, Nat. Commun., 2017, vol. 8, p. 14261. https://doi.org/10.1038/ncomms14261

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Kim, H., Kim, S.T., Ryu, J., et al., CRISPR/Cpf1-mediated DNA-free plant genome editing, Nat. Commun., 2017, vol. 16, no. 8, p. 14406. https://doi.org/10.1038/ncomms14406

    Article  CAS  Google Scholar 

  75. Marton, I., Zuker, A., and Shklarman, E.A., Nontransgenic genome modification in plant cells, Plant Physiol., 2010, vol. 154, no. 3, pp. 1079–1087.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Kumagai, M.H., Donson, J., della-Cioppa, G., et al., Cytoplasmic inhibition of carotenoid biosynthesis with virus-derived RNA, Proc. Natl. Acad. Sci. U. S. A., 1995, vol. 92, pp. 1679–1683.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Ali, Z., Abul-faraj, A., Li, L., et al., Efficient virus-mediated genome editing in plants using the CRISPR/Cas9 system, Mol. Plant, 2015, vol. 8, no. 8, pp. 1288–1291. https://doi.org/10.1016/j.molp.2015.02.011

    Article  CAS  PubMed  Google Scholar 

  78. Zaidi, S.S. and Mansoor, S., Viral vectors for plant genome engineering, Front. Plant Sci., 2017, vol. 8, p. 539. https://doi.org/10.3389/fpls.2017.00539

    Article  PubMed  PubMed Central  Google Scholar 

  79. Baltes, N.J., Gil-Humanes, J., Cermak, T., et al., DNA replicons for plant genome engineering, Plant Cell, 2014, vol. 26, pp. 151–163. https://doi.org/10.1105/tpc.113.119792

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Cermak, T., Baltes, N.J., Cegan, R., et al., High-frequency, precise modification of the tomato genome, Genome Biol., 2015, vol. 16, p. 232. https://doi.org/10.1186/s13059-015-0796-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Hummel, A.W., Chauhan, R.D., Cermak, T., et al., Allele exchange at the EPSPS locus confers glyphosate tolerance in cassava, Plant Biotechnol. J., 2018, vol. 16, pp. 1275–1282. https://doi.org/10.1111/pbi.12868

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Butler, N.M. and Baltes, N.J., Voytas DF., Douches D.S. Geminivirus-mediated genome editing in potato (Solanum tuberosum L.) using sequence-specific nucleases, Front. Plant Sci., 2016, vol. 7, p. 1045. https://doi.org/10.3389/fpls.2016.01045

    Article  PubMed  PubMed Central  Google Scholar 

  83. Dahan-Meir, T., Filler-Hayut, S., Melamed-Bessudo, C., et al., Efficient in planta gene targeting in tomato using geminiviral replicons and the CRISPR/Cas9 system, Plant J., 2018, vol. 95, no. 1, pp. 5–16. https://doi.org/10.1111/tpj.13932

    Article  CAS  PubMed  Google Scholar 

  84. Yin, K., Han, T., Liu, G., et al., A geminivirus-based guide RNA delivery system for CRISPR/Cas9 mediated plant genome editing, Sci. Rep., 2015, vol. 5, p. 14926. https://doi.org/10.1038/srep14926

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Gil-Humanes, J., Wang, Y., Liang, Z., et al., High-efficiency gene targeting in hexaploid wheat using DNA replicons and CRISPR/Cas9, Plant J., 2017, vol. 89, pp. 1251–1262. https://doi.org/10.1111/tpj.13446

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Wang, M., Lu, Y., Botella, J., et al., Gene targeting by homology-directed repair in rice using a geminivirus-based CRISPR/Cas9 system, Mol. Plant., 2017, vol. 10, no. 7, pp. 1007–1010. https://doi.org/10.1016/j.molp.2017.03.002

    Article  CAS  PubMed  Google Scholar 

  87. Iaffaldano, B., Zhang, Y., and Cornish, K., CRISPR/Cas9 genome editing of rubber producing dandelion Taraxacum kok-saghyz using Agrobacterium rhizogenes without selection, Ind. Crops Prod., 2016, vol. 89, pp. 356–362. https://doi.org/10.1016/j.indcrop.2016.05.029

    Article  CAS  Google Scholar 

  88. Jacobs, T.B., Zhang, N., Patel, D., and Martin, G.B., Generation of a collection of mutant tomato lines using pooled CRISPR libraries, Plant. Physiol., 2017, vol. 174, no. 4, pp. 2023–2037. https://doi.org/10.1104/pp.17.00489

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Chen, L., Li, W., Katin-Grazzini, L., et al., A method for the production and expedient screening of CRISPR/ Cas9-mediated non-transgenic mutant plants, Hortic. Res., 2018, vol. 5, p. 13. https://doi.org/10.1038/s41438-018-0023-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Braatz, J., Harloff, H.J., Mascher, M., et al., CRISPR-Cas9 targeted mutagenesis leads to simultaneous modification of different homoeologous gene copies in polyploid oilseed rape (Brassica napus), Plant Physiol., 2017, vol. 174, no. 2, pp. 935–942. https://doi.org/10.1104/pp.17.00426

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Khromov, A.V., Makhotenko, A.V., Snigir’, E.A., et al., Delivery of the CRISPR/Cas9 ribonucleoprotein complex to the apical meristem cells for plasmidless editing of the potato Solanum tuberosum genome, Biotekhnologiya, 2018, vol. 34, no. 6, pp. 51–58. https://doi.org/10.21519/0234-2758-2018-34-6-51-58

    Article  Google Scholar 

  92. Lee, L.Y., Mysore, K., and Gelvin, S., Generation of Agrobacterium strains that efficiently introduce but don’t integrate T-dna into the plant genome, In Vitro Cell Dev. Biol.—Plant, 2018, vol. 54, suppl. 1, p. S88. https://doi.org/10.1007/s11627-018-9923-0

    Article  Google Scholar 

  93. Shukla, V.K., Doyon, Y., Miller, J.C., et al., Precise genome modification in the crop species Zea mays using zinc-finger nucleases, Nature, 2009, vol. 459, no. 7245, pp. 437–441. https://doi.org/10.1038/nature07992

    Article  CAS  PubMed  Google Scholar 

  94. Cai, C.Q., Doyon, Y., Ainley, W.M., et al., Targeted transgene integration in plant cells using designed zinc finger nucleases, Plant Mol. Biol., 2009, vol. 69, no. 9, pp. 699–709. https://doi.org/10.1007/s11103-008-9449-7

    Article  CAS  PubMed  Google Scholar 

  95. Liang, Z., Zhang, K., Chen, K., and Gao, C., Targeted mutagenesis in Zea mays using TALENs and the CRISPR/Cas system, J. Genet Genomics, 2014, vol. 41, no. 2, pp. 63–68. https://doi.org/10.1016/j.jgg.2013.12.001

    Article  CAS  PubMed  Google Scholar 

  96. Sun, Z., Li, N., Huang, G., et al., Site-specific gene targeting using transcription activator-like effector (TALE)- based nuclease in Brassica oleracea,J. Integr. Plant Biol., 2013, vol. 55, no. 11, pp. 1092–1103. https://doi.org/10.1111/jipb.12091

    Article  CAS  PubMed  Google Scholar 

  97. Wendt, T., Holm, P.B., Starker, C.G., et al., TAL effector nucleasesm induce mutations at a pre-selected location in the genome of primary barley transformants, Plant Mol. Biol., 2013, vol. 83, no. 3, pp. 279–285. https://doi.org/10.1007 /s11103-013-0078-4

  98. Johnson, R.A., Gurevich, V., Filler, S., et al., Comparative assessments of CRISPR-Cas nucleases’ cleavage efficiency in planta, Plant Mol. Biol., 2015, vol. 87, nos. 1–2, pp. 143–156. https://doi.org/10.1007/s11103-014-0266-x

    Article  CAS  PubMed  Google Scholar 

  99. Haun, W., Coffman, A., Clasen, B.M., et al., Improved soybean oil quality by targeted mutagenesis of the fatty acid desaturase 2 gene family, Plant Biotechnol. J., 2014, vol. 12, no. 7, pp. 934–940. https://doi.org/10.1111/pbi.12201

    Article  CAS  PubMed  Google Scholar 

  100. Lor, V.S., Starker, C.G., Voytas, D.F., et al., Targeted mutagenesis of the tomato PROCERA gene using transcription activator-like effector nucleases. Plant Physiol., 2014, vol. 166, no. 3, pp. 1288–1291. https://doi.org/10.1104/pp.114.247593

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Brooks, C., Nekrasov, V., Lippman, Z.B., et al., Efficient gene editing in tomato in the first generation using the clustered regularly interspaced short palindromic repeats/CRISPR-associated9 system, Plant Physiol., 2014, vol. 166, no. 3, pp. 1292–1297. https://doi.org/10.1104/pp.114.247577

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Peer, R., Rivlin, G., Golobovitch, S., et al., Targeted mutagenesis using zinc-finger nucleases in perennial fruit trees, Planta, 2015, vol. 241, no. 4, pp. 941–951. https://doi.org/10.1007/s00425-014-2224-x

    Article  CAS  PubMed  Google Scholar 

  103. Jia, H., Orbovic, V., Jones, J.B., and Wang, N., Modification of the PthA4 effector binding elements in Type I CsLOB1 promoter using Cas9/sgRNA to produce transgenic Duncan grapefruit alleviating X-ccΔpthA4:dCsLOB1.3 infection, Plant Biotechnol. J., 2016, vol. 14, pp. 1291–1301. https://doi.org/10.1111/pbi.12495

    Article  CAS  PubMed  Google Scholar 

  104. Butler, N.M., Atkins, P.A., Voytas, D.F., and Douches, D.S., Generation and inheritance of targeted mutations in potato (Solanum tuberosum L.) using the CRISPR/Cas system, PLoS One, 2015, vol. 10, no. 12. e0144591. https://doi.org/10.1371/journal.pone.0144591

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Li, Z.S., Liu, Z.B., Xing, A.Q., et al., Cas9-guide RNA directed genome editing in soybean, Plant Physiol., 2015, vol. 169, pp. 960–970. https://doi.org/10.1104/pp.15.00783

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Hilioti, Z., Ganopoulos, I., Ajith, S., et al., A novel arrangement of zinc finger nuclease system for in vivo targeted genome engineering: the tomato LEC1-LIKE4 gene case, Plant Cell Rep., 2016, vol. 35, no. 11, pp. 2241–2255. https://doi.org/10.1007/s00299-016-2031-x

    Article  CAS  PubMed  Google Scholar 

  107. Tian, S., Jiang, L., Gao, Q., et al., Efficient C-RISPR/Cas9- based gene knockout in watermelon, Plant Cell Rep., 2017, vol. 36, no. 3, pp. 399–406. https://doi.org/10.1007/s00299-016-2089-5

    Article  CAS  PubMed  Google Scholar 

  108. Ren, C., Liu, X., Zhang, Z., et al., CRISPR/Cas9-mediated efficient targeted mutagenesis in Chardonnay (Vitis vinifera L.), Sci. Rep., 2016, vol. 6, p. 32289. https://doi.org/10.1038/srep32289

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Meng, Y., Hou, Y., Wang, H., et al., Targeted mutagenesis by CRISPR/Cas9 system in the model legume Medicago truncatula,Plant Cell Rep., 2017, vol. 36, no. 2, pp. 371–374. https://doi.org/10.1007/s00299-016-2069-9

    Article  CAS  PubMed  Google Scholar 

  110. Wang, L., Wang, L., Tan, Q., et al., Efficient inactivation of symbiotic nitrogen fixation related genes in lotus japonicus using CRISPR-Cas9, Front. Plant Sci., 2016, vol. 7, p. 1333. https://doi.org/10.3389/fpls.2016.013

    Article  PubMed  PubMed Central  Google Scholar 

  111. Alagoz, Y., Gurkok, T., Zhang, B., and Unver, T., Manipulating the biosynthesis of bioactive compound alkaloids for next-generation metabolic engineering in opium poppy using CRISPR-Cas 9 genome editing technology, Sci. Rep., 2016, vol. 6, pp. 30910. https://doi.org/10.1038/srep30910

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Zhang, B., Yang, X., and Yang, C., et al., Exploiting the CRISPR/Cas9 System for targeted genome mutagenesis in petunia, Sci. Rep., 2016, vol. 6, pp. 20315. https://doi.org/10.1038/srep20315

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Nishitani, C., Hirai, N., Komori, S., et al., Efficient genome editing in apple using a CRISPR/Cas9 system, Sci. Rep., 2016, vol. 6, pp. 31481. https://doi.org/10.1038/srep31481

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Jung, J.H. and Altpeter, F., TALEN mediated targeted mutagenesis of the caffeic acid O-methyltransferase in highly polyploid sugarcane improves cell wall composition for production of bioethanol, Plant Mol. Biol., 2016, vol. 92, no. 1, pp. 131–142. https://doi.org/10.1007/s11103-016-0499-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Peng, A., Chen, S., Lei, T., et al., Engineering canker-resistant plants through CRISPR/Cas9-targeted editing of the susceptibility gene CsLOB1 promoter in citrus, Plant Biotechnol. J., 2017, vol. 15, no. 12, pp. 1509–1519. https://doi.org/10.1111/pbi.12733

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Kaur, N. and Alok, A., Shivani, et al., CRISPR/Cas9-mediated efficient editing in phytoene desaturase (PDS) demonstrates precise manipulation in banana cv. Rasthali genome, Funct. Integr. Genomics, 2018, vol. 18, p. 89. https://doi.org/10.1007/s10142-017-0577-5

    Article  CAS  PubMed  Google Scholar 

  117. Watanabe, K., Kobayashi, A., Endo, M., et al., CRI-SPR/Cas9-mediated mutagenesis of the dihydroflavonol-4-reductase-B (DFR-B) locus in the Japanese morning glory Ipomoea (Pharbitis) nil, Sci. Rep., 2017, vol. 7, pp. 10028. https://doi.org/10.1038/s41598-017-10715-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Kui, L., Chen, H., Zhang, W., et al., Building a genetic manipulation tool box for orchid biology: identification of constitutive promoters and application of CRISPR/Cas9 in the orchid, Dendrobium officinale,Front. Plant Sci., 2017, vol. 7, pp. 2036. https://doi.org/10.3389/fpls.2016.02036

    Article  PubMed  PubMed Central  Google Scholar 

  119. Odipio, J., Alicai, T., Ingelbrecht, I., et al., Efficient CRISPR/Cas9 genome editing of phytoene desaturase in cassava, Front. Plant Sci., 2017, vol. 8, p. 1780. https://doi.org/10.3389/fpls.2017.01780

    Article  PubMed  PubMed Central  Google Scholar 

  120. Liu, Y., Merrick, P., Zhang, Z., et al., Targeted mutagenesis in tetraploid switchgrass (Panicum virgatum L.) using CRISPR/Cas9, Plant Biotechnol. J., 2018, vol. 16, no. 2, pp. 381–393. https://doi.org/10.1111/pbi.12778

    Article  CAS  PubMed  Google Scholar 

  121. Zhou, X., Jacobs, T.B., Xue, L.J., et al., Exploiting SNPs for biallelic CRISPR mutations in the outcrossing woody perennial Populus reveals 4-coumarate:CoA ligase specificity and redundancy, New Phytol., 2015, vol. 208, pp. 298–301. https://doi.org/10.1111/nph.13470

    Article  CAS  PubMed  Google Scholar 

  122. Kishi-Kaboshi, M., Aida, R., and Sasaki, K., Generation of gene-edited Chrysanthemum morifolium using multicopy transgenes as targets and markers, Plant Cell Physiol., 2017, vol. 58, no. 2, pp. 216–226. https://doi.org/10.1093/pcp/pcw222

    Article  CAS  PubMed  Google Scholar 

  123. Wen, S., Liu, H., Li, X., et al., TALEN-mediated targeted mutagenesis of fatty acid desaturase 2 (FAD2) in peanut (Arachis hypogaea L.) promotes the accumulation of oleic acid, Plant Mol. Biol., 2018, vol. 97, pp. 177. https://doi.org/10.1007/s11103-018-0731-z

    Article  CAS  PubMed  Google Scholar 

  124. Feng, S., Song, W., Fu, R., et al., Application of the CRISPR/ Cas9 system in Dioscorea zingiberensis,Plant Cell Tiss. Organ Cult., 2018, vol. 135, no. 1, pp. 133–141. https://doi.org/10.1007/s11240-018-1450-5

    Article  CAS  Google Scholar 

  125. Zhou, J., Wang, G., and Liu, Z., Efficient genome editing of wild strawberry genes, vector development and validation, Plant Biotechnol. J., 2018, vol. 16, no. 11, pp. 1868–1877. https://doi.org/10.1111/pbi.12922

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Wang, Z., Wang, S., Li, D., et al., Optimized paired-sgRNA/ Cas9 cloning and expression cassette triggers high-efficiency multiplex genome editing in kiwifruit, Plant Biotechnol. J., 2018, vol. 16, no. 8, pp. 1424–1433. https://doi.org/10.1111/pbi.12884

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Breitler, J.C., Dechamp, E., Campa, C., et al., CRISPR/Cas9-mediated efficient targeted mutagenesis has the potential to accelerate the domestication of Coffea canephora,Plant Cell Tiss. Organ Cult., 2018, vol. 134, no. 3, pp. 383–394. https://doi.org/10.1007/s11240-018-1429-2

    Article  CAS  Google Scholar 

  128. Cai, L., Zhang, L., Fu, Q., and Xu, Z.F., Identification and expression analysis of cytokinin metabolic genes IPTs, CYP735A and CKXs in the biofuel plant Jatropha curcas,Peer J., 2018, vol. 6, pp. e4812. https://doi.org/10.7717/peerj.4812

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. de Pater, S., Pinas, J.E., Hooykaas, P.J.J., and van der Zaal, B.J., ZFN mediated gene targeting of the Arabidopsis protoporphyrinogen oxidase gene through Agrobacterium-mediated floral dip transformation, Plant Biotechnol. J., 2013, vol. 11, pp. 510–515. https://doi.org/10.1111/pbi.12040

    Article  CAS  PubMed  Google Scholar 

  130. Jiang, Y., Juan, WangJ., and Xie, Y., ADF10 shapes the overall organization of apical actin filaments by promoting their turnover and ordering in pollen tubes, J. Cell Sci., 2017, vol. 130, pp. 3988–4001. https://doi.org/10.1242/jcs.207738

    Article  CAS  PubMed  Google Scholar 

  131. Hyun, Y., Kim, J., Cho, S.W., et al., Site-directed mutagenesis in Arabidopsis thaliana using dividing tissue-targeted RGEN of the CRISPR/Cas system to generate heritable null alleles, Planta, 2015, vol. 241, pp. 271–284. https://doi.org/10.1007/s00425-014-2180-5

    Article  CAS  PubMed  Google Scholar 

  132. Yan, L.H., Wei, S.W., Wu, Y.R., et al., High efficiency genome editing in Arabidopsis using Yao promoter-driven CRISPR/Cas9 system, Mol. Plant, 2015, vol. 8, pp. 1820–1823. https://doi.org/10.1016/j.molp.2015.10.00

    Article  CAS  PubMed  Google Scholar 

  133. Pyott, D.E., Sheehan, E., and Molnar, A., Engineering of CRISPR/Cas9–mediated potyvirus resistance in transgene-free Arabidopsis plants, Mol. Plant Pathol., 2016, vol. 17, no. 8, pp. 1276–1288. https://doi.org/10.1111/mpp.12417

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. Jia, Y., Ding, Y., Shi, Y., et al., The cbfs triple mutants reveal the essential functions of CBFs in cold acclimation and allow the definition of CBF regulons in Arabidopsis,New Phytol., 2016, vol. 212, pp. 345–353. https://doi.org/10.1111/nph.14088

    Article  CAS  PubMed  Google Scholar 

  135. Veillet, F., Gaillard, C., Coutos-Thevenot, P., and La Camera, S., Targeting the AtCWIN1 gene to explore the role of invertases in sucrose transport in roots and during Botrytis cinerea infection, Front. Plant Sci., 2016, vol. 7, p. 1899. https://doi.org/10.3389/fpls.2016.01899

    Article  PubMed  PubMed Central  Google Scholar 

  136. Ordon, J., Gantner, J., Kemna, J., et al., Generation of chromosomal deletions in dicotyledonous plants employing a user-friendly genome editing toolkit, Plant J., 2017, vol. 89, no. 1, pp. 155–168. https://doi.org/10.1111/tpj.13319

    Article  CAS  PubMed  Google Scholar 

  137. Steinert, J., Schmidt, C., and Puchta, H., Use of the Cas9 orthologs from Streptococcus thermophilus and Staphylococcus aureus for non-homologous end-joining mediated site-specific mutagenesis in Arabidopsis thaliana,Methods Mol. Biol., 2017, vol. 1669, pp. 365–376. https://doi.org/10.1007/978-1-4939-7286-9_27

    Article  CAS  PubMed  Google Scholar 

  138. Hahn, F., Mantegazza, O., Greiner, A., et al., An efficient visual screen for CRISPR/Cas9 activity in Arabidopsis thaliana,Front. Plant Sci., 2017, vol. 8, pp. 39. https://doi.org/10.3389/fpls.2017.00039

    Article  PubMed  PubMed Central  Google Scholar 

  139. Liang, Y., Zeng, X., Peng, X., et al., Arabidopsis glutamate:glyoxylate aminotransferase 1 (Ler) mutants generated by CRISPR/Cas9 and their characteristics, Transgenic Res., 2018, vol. 27, no. 1, pp. 61–79. https://doi.org/10.1007/s11248-017-0052-z

    Article  CAS  PubMed  Google Scholar 

  140. Saito, M., Kondo, Y., and Fukuda, H., BES1 and BZR1 redundantly promote phloem and xylem differentiation, Plant Cell Physiol., 2018, vol. 59, no. 3, pp. 590–600. https://doi.org/10.1093/pcp/pcy012

    Article  CAS  PubMed  Google Scholar 

  141. Durr, J., Papareddy, R., Nakajima, K., and Gutierrez-Marcos, J., Highly efficient heritable targeted deletions of gene clusters and non-coding regulatory regions in Arabidopsis using CRISPR/Cas9, Sci. Rep., 2018, vol. 8, pp. 4443. https://doi.org/10.1038/s41598-018-22667-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  142. Pauwels, L., De Clercq, R., Goossens, J., et al., A dual sgRNA approach for functional genomics in Arabidopsis thaliana,G3, 2018, vol. 8, no. 8, pp. 2603–2615. https://doi.org/10.1534/g3.118.200046

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  143. Wolter, F., Klemm, J., and Puchta, H., Efficient in planta gene targeting in Arabidopsis using egg cell-specific expression of the Cas9 nuclease of Staphylococcus aureus,Plant J., 2018, vol. 94, no. 4, pp. 735–746. https://doi.org/10.1111/tpj.13893

    Article  CAS  PubMed  Google Scholar 

  144. Kapusi, E., Corcuera-Gomez, M., Melnik, S., and Stoger, E., Heritable genomic fragment deletions and small indels in the putative ENGase gene induced by CRISPR/Cas9 in barley, Front. Plant Sci., 2017, vol. 8, p. 540. https://doi.org/10.3389/fpls.2017.00540

    Article  PubMed  PubMed Central  Google Scholar 

  145. Kumar, N., Galli, M., Ordon, J., et al., Further analysis of barley MORC1 using a highly efficient RNA-guided Cas9 gene-editing system, Plant Biotechnol. J., 2018, vol. 16, no. 11, pp. 1892–1903. https://doi.org/10.1111/pbi.12924

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. Shibuya, K., Watanabe, K., and Ono, M., CRISPR/Cas9-mediated mutagenesis of the EPHEMERAL1 locus that regulates petal senescence in Japanese morning glory, Plant Physiol. Biochem., 2018, vol. 131, pp. 53–57. https://doi.org/10.1016/j.plaphy.2018.04.036

    Article  CAS  PubMed  Google Scholar 

  147. Zhu, J., Song, N., Sun, S., et al., Efficiency and inheritance of targeted mutagenesis in maize using CRISPR-Cas9, J. Genet. Genomics, 2016, vol. 43, no. 1, pp. 25–36. https://doi.org/10.1016/j.jgg.2015.10.006

    Article  PubMed  Google Scholar 

  148. Char, S.N., Neelakandan, A.K., Nahampun, H., et al., An Agrobacterium-delivered CRISPR/Cas9 system for high-frequency targeted mutagenesis in maize, Plant Biotechnol. J., 2017, vol. 15, no. 2, pp. 257–268. https://doi.org/10.1111/pbi.12611

    Article  CAS  PubMed  Google Scholar 

  149. Yang, Y., Zhu, K., Li, H., et al., Precise editing of CLAVATA genes in Brassica napus L. regulates multilocular silique development, Plant Biotechnol. J., 2018, vol. 16, no. 7, pp. 1322–1335. https://doi.org/10.1111/pbi.12872

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  150. Demorest, Z.L., Coffman, A., Baltes, N.J., et al., Direct stacking of sequence-specific nuclease-induced mutations to produce high oleic and low linolenic soybean oil, BMC Plant Biol., 2016, vol. 16, p. 225. https://doi.org/10.1186/s12870-016-0906-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  151. Cai, Y., Chen, L., Liu, X., et al., CRISPR/Cas9-mediated targeted mutagenesis of GmFT2a delays flowering time in soya bean, Plant Biotechnol. J., 2018, vol. 16, no. 1, pp. 176–185. https://doi.org/10.1111/pbi.12758

    Article  CAS  PubMed  Google Scholar 

  152. Kanazashi, Y., Hirose, A., Takahashi, I., et al., Simultaneous site-directed mutagenesis of duplicated loci in soybean using a single guide RNA, Plant Cell Rep., 2018, vol. 37, no. 3, pp. 553–563. https://doi.org/10.1007/s00299-018-2251-3

    Article  CAS  PubMed  Google Scholar 

  153. Gao, J., Zhang, T., Xu, B., et al., CRISPR/Cas9-mediated mutagenesis of carotenoid cleavage dioxygenase 8 (CCD8) in tobacco affects shoot and root architecture, Int. J. Mol. Sci., 2018, vol. 19, no. 4. https://doi.org/10.3390/ijms19041062

  154. Ito, Y., Nishizawa-Yokoi, A., Endo, M., et al., CRISPR/Cas9-mediated mutagenesis of the RIN locus that regulates tomato fruit ripening, Biochem. Biophys. Res. Commun., 2015, vol. 467, no. 1, pp. 76–82. https://doi.org/10.1016/j.bbrc.2015.09.117

    Article  CAS  PubMed  Google Scholar 

  155. Pan, C., Ye, L., Qin, L., et al., CRISPR/Cas9-mediated efficient and heritable targeted mutagenesis in tomato plants in the first and later generations, Sci. Rep., 2016, vol. 6, pp. 24765. https://doi.org/10.1038/srep24765

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  156. Yu, Q.H., Wang, B., Li, N., et al., CRISPR/Cas9-induced targeted mutagenesis and gene replacement to generate long-shelf life tomato lines, Sci. Rep., 2017, vol. 7, no. 1, pp. 11874. https://doi.org/10.1038/s41598-017-12262-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  157. Nekrasov, V., Wang, C., and Win, J., Rapid generation of a transgene-free powdery mildew resistant tomato by genome deletion, Sci. Rep., 2017, vol. 7, no. 1, p. 482. https://doi.org/10.1038/s41598-017-00578-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  158. Shimatani, Z., Kashojiya, S., Takayama, M., et al., Targeted base editing in rice and tomato using a CRISPR-Cas9 cytidine deaminase fusion, Nat. Biotechnol., 2017, vol. 35, no. 5, pp. 441–443. https://doi.org/10.1038/nbt.3833

    Article  CAS  PubMed  Google Scholar 

  159. Deng, L., Wang, H., Sun, C., et al., Efficient generation of pink-fruited tomatoes using CRISPR/Cas9 system, J. Genet. Genomics, 2018, vol. 45, no. 1, pp. 51–54. https://doi.org/10.1016/j.jgg.2017.10.002

    Article  PubMed  Google Scholar 

  160. Wang, M., Liu, Y., Zhang, C., et al., Gene editing by co-transformation of TALEN and chimeric RNA/DNA oligonucleotides on the rice OsEPSPS gene and the inheritance of mutations, PLoS One, 2015, vol. 10, no. 4. e0122755. https://doi.org/10.1371/journal.pone.0122755

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  161. Shan, Q., Zhang, Y., Chen, K., et al., Creation of fragrant rice by targeted knockout of the OsBADH2 gene using TALEN technology, Plant Biotechnol. J., 2015, vol. 13, pp. 791–800. https://doi.org/10.1111/pbi.12312

    Article  CAS  PubMed  Google Scholar 

  162. Wang, F., Wang, C., Liu, P., et al., Enhanced rice blast resistance by CRISPR/Cas9-targeted mutagenesis of the ERF transcription factor gene OsERF922,PLoS One, 2016, vol. 11, no. 4, pp. e0154027. https://doi.org/10.1371/journal.pone.0154027

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  163. Zhou, H., He, M., Li, J., et al., Development of commercial thermo-sensitive genic male sterile rice accelerates hybrid rice breeding using the CRISPR/Cas9-mediated TMS5 editing system, Sci. Rep., 2016, vol. 6, p. 37395. https://doi.org/10.1038/srep37395

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  164. Xu, R., Yang, Y., Qin, R., et al., Rapid improvement of grain weight via highly efficient CRISPR/Cas9-mediated multiplex genome editing in rice, J. Genet. Genomics, 2016, vol. 43, no. 8, pp. 529–532. https://doi.org/10.1016/j.jgg.2016.07.003

    Article  PubMed  Google Scholar 

  165. Xu, R., Qin, R., Li, H., et al., Generation of targeted mutant rice using a CRISPR-Cpf1 system, Plant Biotechnol. J., 2017, vol. 15, pp. 713–717. https://doi.org/10.1111/pbi.12669

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  166. Yin, X., Biswal, A.K., Dionora, J., et al., CRISPR-Cas9 and CRISPR-Cpf1 mediated targeting of a stomatal developmental gene EPFL9 in rice, Plant. Cell Rep., 2017, vol. 36, no. 5, pp. 745–757. https://doi.org/10.1007/s00299-017-2118-z

    Article  CAS  PubMed  Google Scholar 

  167. Minkenberg, B., Xie, K., and Yang, Y., Discovery of rice essential genes by characterizing a CRISPR-edited mutation of closely related rice MAP kinase genes, Plant J., 2017, vol. 89, no. 3, pp. 636–648. https://doi.org/10.1111/tpj.13399

    Article  CAS  PubMed  Google Scholar 

  168. Sun, Y., Jiao, G., Liu, Z., et al., Generation of high-amylose rice through CRISPR/Cas9-mediated targeted mutagenesis of starch branching enzymes, Front. Plant Sci., 2017, vol. 8, p. 298. https://doi.org/10.3389/fpls.2017.00298

    Article  PubMed  PubMed Central  Google Scholar 

  169. Tang, L., Mao, B., Li, Y., et al., Knockout of OsNramp5 using the CRISPR/Cas9 system produces low Cd-accumulating indica rice without compromising yield, Sci. Rep., 2017, vol. 7, no. 1, p. 14438. https://doi.org/10.1038/s41598-017-14832-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  170. Li, D.D., Guan, H., Li, F., et al., Arabidopsis shaker pollen inward K+ channel SPIK functions in SnRK1 complex-regulated pollen hydration on the stigma, J. Integr. Plant Biol., 2017, vol. 59, no. 9, pp. 604–611. https://doi.org/10.1111/jipb.12563

    Article  CAS  PubMed  Google Scholar 

  171. Shimatani, Z., Fujikura, U., Ishii, H., et al., Inheritance of co-edited genes by CRISPR-based targeted nucleotide substitutions in rice, Plant Physiol. Biochem., 2018, vol. 131, pp. 78–83. https://doi.org/10.1016/j.plaphy.2018.04.028

    Article  CAS  PubMed  Google Scholar 

  172. Ye, Y., Wu, K., Chen, J., et al., Ossnd2, a NAC family transcription factor, is involved in secondary cell wall biosynthesis through regulating MYBs expression in rice, Rice (NY), 2018, vol. 11, no. 1, p. 36. https://doi.org/10.1186/s12284-018-0228-z

    Article  PubMed  PubMed Central  Google Scholar 

  173. Liang, Z., Chen, K., Yan, Y., et al., Genotyping genome-edited mutations in plants using CRISPR ribonucleoprotein complexes, Plant Biotechnol. J., 2018, vol. 16, no. 12, pp. 2053–2062.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Funding

The work was supported by the Russian Science Foundation (grant no. 16-16-04019).

Author information

Authors and Affiliations

  1. Shemyakin–Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences, Pushchino Branch, 142290, Pushchino, Moscow oblast, Russia

    D. N. Miroshnichenko, V. R. Timerbaev & S. V. Dolgov

  2. All-Russia Institute of Agricultural Biotechnology, Russian Academy of Sciences, 127550, Moscow, Russia

    D. N. Miroshnichenko, O. A. Shulga, V. R. Timerbaev & S. V. Dolgov

  3. Doka-Gene Technology Ltd, 141880, Rogachevo, Moscow oblast, Russia

    D. N. Miroshnichenko & S. V. Dolgov

Authors
  1. D. N. Miroshnichenko
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. O. A. Shulga
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. V. R. Timerbaev
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. S. V. Dolgov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to S. V. Dolgov.

Ethics declarations

The authors declare that they have no conflicts of interest.

This article does not contain any studies involving animals or human participants performed by any of the authors.

Additional information

Translated by I. Gordon

Abbreviations: CRISPR, clustered regularly interspaced short palindromic repeats; GE, genome-edited; GFP, green fluorescent protein; GMO, genetically modified organism; GMP, genetically modified product; GUS, beta-glucuronidase; RNP, ribonucleoprotein; TALEN, transcription activator-like effector nuclease; TRV, tobacco rattle virus; ZFN, zinc-finger nuclease.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Miroshnichenko, D.N., Shulga, O.A., Timerbaev, V.R. et al. Achievements, Challenges, and Prospects in the Production of Nontransgenic, Genome-Edited Plants. Appl Biochem Microbiol 55, 825–845 (2019). https://doi.org/10.1134/S0003683819090047

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0003683819090047

Keywords:

Search

Navigation