CRISPR technology to combat plant RNA viruses: A theoretical model for Potato virus Y (PVY)resistance

[en] RNA viruses are the most diverse phytopathogens which cause severe epidemics in important agricultural crops and threaten the global food security. Being obligatory intracellular pathogens, these viruses have developed fine-tuned evading mechanisms and are non-responsive to most of the prophylactic treatments. Additionally, their sprint ability to overcome host defense demands a broad-spectrum and durable mechanism of resistance. In context of CRISPR-Cas discoveries, some variants of Cas effectors have been characterized as programmable RNA-guided RNases in the microbial genomes and could be reprogramed in mammalian and plant cells with guided RNase activity. Recently, the RNA variants of CRISPR-Cas systems have been successfully employed in plants to engineer resistance against RNA viruses. Some variants of CRISPR-Cas9 have been tamed either for directly targeting plant RNA viruses’ genome or through targeting the host genes/factors assisting in viral proliferation. The new frontiers in CRISPR-Cas discoveries, and more importantly shifting towards RNA targeting will pyramid the opportunities in plant virus research. The current review highlights the probable implications of CRISPR-Cas system to confer the pathogen-derived or host-mediated resistance against phytopathogenic RNA viruses. Furthermore, a multiplexed CRISPR-Cas13a methodology is proposed here to combat Potato virus Y (PVY); a globally diverse phytopathogen infecting multiple crops. © 2019 Elsevier Ltd

Disciplines :

Genetics & genetic processes
Biotechnology
Microbiology
Agriculture & agronomy

Author, co-author :

Hameed, A.; Akhuwat Faisalabad Institute of Research Science and Technology, Faisalabad, Pakistan, Department of Bioinformatics & Biotechnology, Government College University, Allama Iqbal Road, Faisalabad, Pakistan

Syed-Shan-e-Ali, Zaïdi ; Université de Liège - ULiège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Ingénierie des productions végétales et valorisation

Sattar, M. N.; Department of Biotechnology, College of Agriculture and Food Science, King Faisal University, Box 400, Al-Ahsa3192, Saudi Arabia

Iqbal, Z.; Department of Plant Pathology, University of Florida, Gainesville, FL 32611, United States

Tahir, M. N.; Department of Plant Pathology, Bahauddin Zakariya University, Multan, Pakistan

Language :

English

Title :

CRISPR technology to combat plant RNA viruses: A theoretical model for Potato virus Y (PVY)resistance

Publication date :

2019

Journal title :

Microbial Pathogenesis

ISSN :

0882-4010

eISSN :

1096-1208

Publisher :

Academic Press

Volume :

133

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 06 February 2020

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Bibliography

Boualem, A., Dogimont, C., Bendahmane, A., The battle for survival between viruses and their host plants. Curr. Opin. Virol. 17 (2016), 32–38.
Roossinck, M.J., Plants, viruses and the environment: ecology and mutualism. Virology 479–480 (2015), 271–277.
Wylie, S.J., Adams, M., Chalam, C., Kreuze, J., López-Moya, J.J., Ohshima, K., Praveen, S., Rabenstein, F., Stenger, D., Wang, A., ICTV virus taxonomy profile: Potyviridae. J. Gen. Virol. 98 (2017), 352–354.
Rybicki, E.P., A Top Ten list for economically important plant viruses. Arch. Virol. 160 (2015), 17–20.
Whitworth, J.L., Nolte, P., McIntosh, C., Davidson, R., Effect of Potato virus Y on yield of three potato cultivars grown under different nitrogen levels. Plant Dis. 90 (2006), 73–76.
Sevik, M.A., Arli-Sokmen, M., Estimation of the effect of Tomato spotted wilt virus (TSWV)infection on some yield components of tomato. Phytoparasitica 40 (2012), 87–93.
Mahjabeen, Akhtar, K., Sarwar, N., Saleem, M., Asghar, M., Iqbal, Q., Jamil, F., Effect of cucumber mosaic virus infection on morphology, yield and phenolic contents of tomato. Arch. Phytopathol. Plant Prot. 45 (2012), 766–782.
Elena, S., Lalić, J., Plant RNA virus fitness predictability: contribution of genetic and environmental factors. Plant Pathol. 62 (2013), 10–18.
Elena, S.F., Bedhomme, S., Carrasco, P., Cuevas, J.M., de la Iglesia, F., Lafforgue, G., Lalic, J., Prosper, A., Tromas, N., Zwart, M.P., The evolutionary genetics of emerging plant RNA viruses. Mol. Plant Microbe Interact. 24 (2011), 287–293.
Meziadi, C., Blanchet, S., Geffroy, V., Pflieger, S., Genetic resistance against viruses in Phaseolus vulgaris L.: state of the art and future prospects. Plant Sci. 265 (2017), 39–50.
Fuentes, A., Carlos, N., Ruiz, Y., Callard, D., Sánchez, Y., Ochagavía, M.E., Seguin, J., Malpica-Lopez, N., Hohn, T., Lecca, M.R., Field trial and molecular characterization of RNAi-transgenic tomato plants that exhibit resistance to tomato yellow leaf curl geminivirus. Mol. Plant Microbe Interact. 29 (2016), 197–209.
Galvez, L.C., Banerjee, J., Pinar, H., Mitra, A., Engineered plant virus resistance. Plant Sci. 228 (2014), 11–25.
Hameed, A., Tahir, M.N., Asad, S., Bilal, R., Van Eck, J., Jander, G., Mansoor, S., RNAi-mediated simultaneous resistance against three RNA viruses in potato. Mol. Biotechnol. 59 (2017), 73–83.
Jia, R., Zhao, H., Huang, J., Kong, H., Zhang, Y., Guo, J., Huang, Q., Guo, Y., Wei, Q., Zuo, J., Use of RNAi technology to develop a PRSV-resistant transgenic papaya. Sci. Rep., 7, 2017, 12636.
Puchta, H., Applying CRISPR/Cas for genome engineering in plants: the best is yet to come. Curr. Opin. Plant Biol. 36 (2017), 1–8.
Bortesi, L., Fischer, R., The CRISPR/Cas9 system for plant genome editing and beyond. Biotechnol. Adv. 33 (2015), 41–52.
Petolino, J.F., Srivastava, V., Daniell, H., Editing Plant Genomes: a new era of crop improvement. Plant Biotechnol. J 14 (2016), 435–436.
Baltes, N.J., Hummel, A.W., Konecna, E., Cegan, R., Bruns, A.N., Bisaro, D.M., Voytas, D.F., Conferring resistance to geminiviruses with the CRISPR–Cas prokaryotic immune system. Nature Plants, 1, 2015, 15145.
Zaidi, S.S.-e.-A., Mansoor, S., Ali, Z., Tashkandi, M., Mahfouz, M.M., Engineering plants for geminivirus resistance with CRISPR/Cas9 system. Trends Plant Sci. 21 (2016), 279–281.
Lander, E.S., The heroes of CRISPR. Cell 164 (2016), 18–28.
Abudayyeh, O.O., Gootenberg, J.S., Essletzbichler, P., Han, S., Joung, J., Belanto, J.J., Verdine, V., Cox, D.B.T., Kellner, M.J., Regev, A., RNA targeting with CRISPR-Cas13. Nature 550 (2017), 280–284.
Abudayyeh, O.O., Gootenberg, J.S., Konermann, S., Joung, J., Slaymaker, I.M., Cox, D.B., Shmakov, S., Makarova, K.S., Semenova, E., Minakhin, L., C2c2 is a single-component programmable RNA-guided RNA-targeting CRISPR effector. Science, 353, 2016, aaf5573.
Aman, R., Ali, Z., Butt, H., Mahas, A., Aljedaani, F., Khan, M.Z., Ding, S., Mahfouz, M., RNA virus interference via CRISPR/Cas13a system in plants. Genome Biol., 19, 2018, 1.
Mahas, A., Neal Stewart, C. Jr., Mahfouz, M.M., Harnessing CRISPR/Cas systems for programmable transcriptional and post-transcriptional regulation. Biotechnol. Adv. 36 (2018), 295–310.
Yang, L., Chen, L.L., Enhancing the RNA engineering toolkit. Science 358 (2017), 996–997.
Makarova, K.S., Wolf, Y.I., Alkhnbashi, O.S., Costa, F., Shah, S.A., Saunders, S.J., Barrangou, R., Brouns, S.J., Charpentier, E., Haft, D.H., et al. An updated evolutionary classification of CRISPR-Cas systems. Nat. Rev. Microbiol. 13 (2015), 722–736.
Cox, D.B.T., Gootenberg, J.S., Abudayyeh, O.O., Franklin, B., Kellner, M.J., Joung, J., Zhang, F., RNA editing with CRISPR-Cas13. Science 358 (2017), 1019–1027.
Shmakov, S., Smargon, A., Scott, D., Cox, D., Pyzocha, N., Yan, W., Abudayyeh, O.O., Gootenberg, J.S., Makarova, K.S., Wolf, Y.I., et al. Diversity and evolution of class 2 CRISPR-Cas systems. Nat. Rev. Microbiol. 15 (2017), 169–182.
Yan, W.X., Chong, S., Zhang, H., Makarova, K.S., Koonin, E.V., Cheng, D.R., Scott, D.A., Cas13d is a compact RNA-targeting type VI CRISPR effector positively modulated by a WYL-domain-containing accessory protein. Mol. Cell 70 (2018), 327–339 e325.
Price, A.A., Sampson, T.R., Ratner, H.K., Grakoui, A., Weiss, D.S., Cas9-mediated targeting of viral RNA in eukaryotic cells. Proc. Natl. Acad. Sci. U. S. A 112 (2015), 6164–6169.
Sampson, T.R., Saroj, S.D., Llewellyn, A.C., Tzeng, Y.-L., Weiss, D.S., A CRISPR/Cas system mediates bacterial innate immune evasion and virulence. Nature 497 (2013), 254–257.
Zhang, T., Zheng, Q., Yi, X., An, H., Zhao, Y., Ma, S., Zhou, G., Establishing RNA virus resistance in plants by harnessing CRISPR immune system. Plant Biotechnol. J, 2018, 10.1111/pbi.12881.
Smargon, A.A., Cox, D.B., Pyzocha, N.K., Zheng, K., Slaymaker, I.M., Gootenberg, J.S., Abudayyeh, O.A., Essletzbichler, P., Shmakov, S., Makarova, K.S., Cas13b is a type VI-B CRISPR-associated RNA-guided RNase differentially regulated by accessory proteins Csx27 and Csx28. Mol. Cell 65 (2017), 618–630 e617.
Jiang, W., Samai, P., Marraffini, L.A., Degradation of phage transcripts by CRISPR-associated RNases enables type III CRISPR-cas immunity. Cell 164 (2016), 710–721.
Liu, T.Y., Iavarone, A.T., Doudna, J.A., RNA and DNA targeting by a reconstituted Thermus thermophilus Type III-A CRISPR-Cas system. PLoS One, 12, 2017 e0170552.
Samai, P., Pyenson, N., Jiang, W., Goldberg, G.W., Hatoum-Aslan, A., Marraffini, L.A., Co-transcriptional DNA and RNA cleavage during type III CRISPR-cas immunity. Cell 161 (2015), 1164–1174.
O'Connell, M.R., Oakes, B.L., Sternberg, S.H., East-Seletsky, A., Kaplan, M., Doudna, J.A., Programmable RNA recognition and cleavage by CRISPR/Cas9. Nature 516 (2014), 263–266.
East-Seletsky, A., O'Connell, M.R., Burstein, D., Knott, G.J., Doudna, J.A., RNA targeting by functionally orthogonal type VI-a CRISPR-cas enzymes. Mol. Cell 66 (2017), 373–383 e373.
Gootenberg, J.S., Abudayyeh, O.O., Lee, J.W., Essletzbichler, P., Dy, A.J., Joung, J., Verdine, V., Donghia, N., Daringer, N.M., Freije, C.A., et al. Nucleic acid detection with CRISPR-Cas13a/C2c2. Science 356 (2017), 438–442.
East-Seletsky, A., O'Connell, M.R., Knight, S.C., Burstein, D., Cate, J.H., Tjian, R., Doudna, J.A., Two distinct RNase activities of CRISPR-C2c2 enable guide-RNA processing and RNA detection. Nature 538 (2016), 270–273.
Strutt, S.C., Torrez, R.M., Kaya, E., Negrete, O.A., Doudna, J.A., RNA-dependent RNA targeting by CRISPR-Cas9. eLife, 7, 2018 e32724.
Koonin, E.V., Makarova, K.S., Zhang, F., Diversity, classification and evolution of CRISPR-Cas systems. Curr. Opin. Microbiol. 37 (2017), 67–78.
Tamulaitis, G., Venclovas, C., Siksnys, V., Type III CRISPR-cas immunity: major differences brushed aside. Trends Microbiol. 25 (2017), 49–61.
Wright, A.V., Nunez, J.K., Doudna, J.A., Biology and applications of CRISPR systems: harnessing nature's toolbox for genome engineering. Cell 164 (2016), 29–44.
Andersson, M., Turesson, H., Nicolia, A., Falt, A.S., Samuelsson, M., Hofvander, P., Efficient targeted multiallelic mutagenesis in tetraploid potato (Solanum tuberosum)by transient CRISPR-Cas9 expression in protoplasts. Plant Cell Rep. 36 (2017), 117–128.
Peng, A., Chen, S., Lei, T., Xu, L., He, Y., Wu, L., Yao, L., Zou, X., Engineering canker‐resistant plants through CRISPR/Cas9‐targeted editing of the susceptibility gene CsLOB1 promoter in citrus. Plant Biotechnol. J 15 (2017), 1509–1519.
Kanda, Y., Yokotani, N., Maeda, S., Nishizawa, Y., Kamakura, T., Mori, M., The receptor-like cytoplasmic kinase BSR1 mediates chitin-induced defense signaling in rice cells. Biosci. Biotechnol. Biochem. 81 (2017), 1497–1502.
Zhang, Y., Bai, Y., Wu, G., Zou, S., Chen, Y., Gao, C., Tang, D., Simultaneous modification of three homoeologs of TaEDR1 by genome editing enhances powdery mildew resistance in wheat. Plant J. 91 (2017), 714–724.
Iqbal, Z., Sattar, M.N., Shafiq, M., CRISPR/Cas9: a tool to circumscribe cotton leaf curl disease. Front. Plant Sci., 7, 2016, 475.
Khatodia, S., Bhatotia, K., Tuteja, N., Development of CRISPR/Cas9 mediated virus resistance in agriculturally important crops. Bioengineered 8 (2017), 274–279.
Zaidi, S.S.-e.-A., Tashkandi, M., Mansoor, S., Mahfouz, M.M., Engineering plant immunity: using CRISPR/Cas9 to generate virus resistance. Front. Plant Sci., 7, 2016, 1673.
Chandrasekaran, J., Brumin, M., Wolf, D., Leibman, D., Klap, C., Pearlsman, M., Sherman, A., Arazi, T., Gal‐On, A., Development of broad virus resistance in non‐transgenic cucumber using CRISPR/Cas9 technology. Mol. Plant Pathol. 17 (2016), 1140–1153.
Pyott, D.E., Sheehan, E., Molnar, A., Engineering of CRISPR/Cas9-mediated potyvirus resistance in transgene-free Arabidopsis plants. Mol. Plant Pathol. 17 (2016), 1276–1288.
Zhang, Q., Xing, H.L., Wang, Z.P., Zhang, H.Y., Yang, F., Wang, X.C., Chen, Q.J., Potential high-frequency off-target mutagenesis induced by CRISPR/Cas9 in Arabidopsis and its prevention. Plant Mol. Biol. 96 (2018), 445–456.
Chen, S., Yu, X., Guo, D., CRISPR-cas targeting of host genes as an antiviral strategy. Viruses, 10, 2018, 40.
Sanfacon, H., Plant translation factors and virus resistance. Viruses 7 (2015), 3392–3419.
Hyodo, K., Okuno, T., Pathogenesis mediated by proviral host factors involved in translation and replication of plant positive-strand RNA viruses. Curr. Opin. Virol. 17 (2016), 11–18.
Gauffier, C., Lebaron, C., Moretti, A., Constant, C., Moquet, F., Bonnet, G., Caranta, C., Gallois, J.L., A TILLING approach to generate broad‐spectrum resistance to potyviruses in tomato is hampered by eIF4E gene redundancy. Plant J. 85 (2016), 717–729.
Piron, F., Nicolai, M., Minoia, S., Piednoir, E., Moretti, A., Salgues, A., Zamir, D., Caranta, C., Bendahmane, A., An induced mutation in tomato eIF4E leads to immunity to two potyviruses. PLoS One, 5, 2010, e11313.
Bastet, A., Lederer, B., Giovinazzo, N., Arnoux, X., German-Retana, S., Reinbold, C., Brault, V., Garcia, D., Djennane, S., Gersch, S., et al. Trans-species synthetic gene design allows resistance pyramiding and broad-spectrum engineering of virus resistance in plants. Plant Biotechnol. J, 2018, 10.1111/pbi.12896.
Woo, J.W., Kim, J., Kwon, S.I., Corvalan, C., Cho, S.W., Kim, H., Kim, S.G., Kim, S.T., Choe, S., Kim, J.S., DNA-free genome editing in plants with preassembled CRISPR-Cas9 ribonucleoproteins. Nat. Biotechnol. 33 (2015), 1162–1164.
Iyer, V., Boroviak, K., Thomas, M., Doe, B., Ryder, E., Adams, D., No unexpected CRISPR-Cas9 off-target activity revealed by trio sequencing of gene-edited mice. bioRxiv, 2018, 263129.
Ali, Z., Ali, S., Tashkandi, M., Zaidi, S.S.-e.-A., Mahfouz, M.M., CRISPR/Cas9-mediated immunity to geminiviruses: differential interference and evasion. Sci. Rep., 6, 2016, 26912.
Adams, M.J., Zerbini, F.M., French, R., Rabenstein, F., Stenger, D.C., Valkonen, J.P.T., Family - Potyviridae. A.M, Q., Adams, M.J., Carstens, E.B., Lefkowitz, E.J., (eds.)Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses–King, 2012, Elsevier, San Diego, 1069–1089.
Crosslin, J.M., PVY: an old enemy and a continuing challenge. Am. J. Potato Res. 90 (2013), 2–6.
Karasev, A.V., Hu, X., Brown, C.J., Kerlan, C., Nikolaeva, O.V., Crosslin, J.M., Gray, S.M., Genetic diversity of the ordinary strain of Potato virus Y (PVY)and origin of recombinant PVY strains. Phytopathology 101 (2011), 778–785.
Desbiez, C., Moury, B., Lecoq, H., The hallmarks of “green” viruses: do plant viruses evolve differently from the others?. Infect. Genet. Evol. 11 (2011), 812–824.
Funke, C.N., Nikolaeva, O.V., Green, K.J., Tran, L.T., Chikh-Ali, M., Quintero-Ferrer, A., Cating, R.A., Frost, K.E., Hamm, P.B., Olsen, N., Strain-specific resistance to Potato virus Y (PVY)in potato and its effect on the relative abundance of PVY strains in commercial potato fields. Plant Dis. 101 (2017), 20–28.
Green, K.J., Brown, C.J., Gray, S.M., Karasev, A.V., Phylogenetic study of recombinant strains of Potato virus. Y. Virology 507 (2017), 40–52.
Generoso, W.C., Gottardi, M., Oreb, M., Boles, E., Simplified CRISPR-Cas genome editing for Saccharomyces cerevisiae. J. Microbiol. Methods 127 (2016), 203–205.
Hung, S.S., Chrysostomou, V., Li, F., Lim, J.K., Wang, J.H., Powell, J.E., Tu, L., Daniszewski, M., Lo, C., Wong, R.C., et al. AAV-mediated CRISPR/cas gene editing of retinal cells in vivo. Investig. Ophthalmol. Vis. Sci. 57 (2016), 3470–3476.
Ma, X., Wong, A.S.-Y., Tam, H.-Y., Tsui, S.Y.-K., Chung, D.L.-S., Feng, B., In vivo genome editing thrives with diversified CRISPR technologies. Zool. Res., 39, 2018, 58.
Qi, W., Zhu, T., Tian, Z., Li, C., Zhang, W., Song, R., High-efficiency CRISPR/Cas9 multiplex gene editing using the glycine tRNA-processing system-based strategy in maize. BMC Biotechnol., 16, 2016, 58.
Sakuma, T., Nakade, S., Sakane, Y., Suzuki, K.T., Yamamoto, T., MMEJ-assisted gene knock-in using TALENs and CRISPR-Cas9 with the PITCh systems. Nat. Protoc. 11 (2016), 118–133.
Sattar, M.N., Iqbal, Z., Tahir, M.N., Shahid, M.S., Khurshid, M., Al-Khateeb, A.A., Al-Khateeb, S.A., CRISPR/Cas9: a practical approach in date palm genome editing. Front. Plant Sci., 8, 2017, 1469.
Wang, X., Tang, Y., Lu, J., Shao, Y., Qin, X., Li, Y., Wang, L., Li, D., Liu, M., Characterization of novel cytochrome P450 2E1 knockout rat model generated by CRISPR/Cas9. Biochem. Pharmacol. 105 (2016), 80–90.
Plagens, A., Richter, H., Charpentier, E., Randau, L., DNA and RNA interference mechanisms by CRISPR-Cas surveillance complexes. FEMS Microbiol. Rev. 39 (2015), 442–463.
Zetsche, B., Gootenberg, J.S., Abudayyeh, O.O., Slaymaker, I.M., Makarova, K.S., Essletzbichler, P., Volz, S.E., Joung, J., Van Der Oost, J., Regev, A., Cpf1 is a single RNA-guided endonuclease of a class 2 CRISPR-Cas system. Cell 163 (2015), 759–771.
Anantharaman, V., Makarova, K.S., Burroughs, A.M., Koonin, E.V., Aravind, L., Comprehensive analysis of the HEPN superfamily: identification of novel roles in intra-genomic conflicts, defense, pathogenesis and RNA processing. Biol. Direct, 8, 2013, 15.
Kumar, S., Stecher, G., Tamura, K., MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33 (2016), 1870–1874.
Engler, C., Kandzia, R., Marillonnet, S., A one pot, one step, precision cloning method with high throughput capability. PLoS One, 3, 2008 e3647.
Xing, H.L., Dong, L., Wang, Z.P., Zhang, H.Y., Han, C.Y., Liu, B., Wang, X.C., Chen, Q.J., A CRISPR/Cas9 toolkit for multiplex genome editing in plants. BMC Plant Biol., 14, 2014, 327.
Guo, L., Xu, K., Liu, Z., Zhang, C., Xin, Y., Zhang, Z., Assembling the Streptococcus thermophilus clustered regularly interspaced short palindromic repeats (CRISPR)array for multiplex DNA targeting. Anal. Biochem. 478 (2015), 131–133.
Xie, K., Minkenberg, B., Yang, Y., Boosting CRISPR/Cas9 multiplex editing capability with the endogenous tRNA-processing system. Proc. Natl. Acad. Sci. Unit. States Am. 112 (2015), 3570–3575.
Cong, L., Ran, F.A., Cox, D., Lin, S., Barretto, R., Habib, N., Hsu, P.D., Wu, X., Jiang, W., Marraffini, L., Multiplex genome engineering using CRISPR/Cas systems. Science 339 (2013), 819–823.
Liu, L., Li, X., Ma, J., Li, Z., You, L., Wang, J., Wang, M., Zhang, X., Wang, Y., The molecular architecture for RNA-guided RNA cleavage by Cas13a. Cell 170 (2017), 714–726 e710.
Groen, S.C., Wamonje, F.O., Murphy, A.M., Carr, J.P., Engineering resistance to virus transmission. Curr. Opin. Virol. 26 (2017), 20–27.
Zaidi, S.S.-e.-A., Briddon, R.W., Mansoor, S., Engineering dual begomovirus-bemisia tabaci resistance in plants. Trends Plant Sci. 22 (2017), 6–8.
Miller, R.N., Costa Alves, G.S., Van Sluys, M.A., Plant immunity: unravelling the complexity of plant responses to biotic stresses. Ann. Bot. 119 (2017), 681–687.
Gao, Y., Zhao, Y., Specific and heritable gene editing in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 111 (2014), 4357–4358.
Kanchiswamy, C.N., Malnoy, M., Velasco, R., Kim, J.-S., Viola, R., Non-GMO genetically edited crop plants. Trends Biotechnol. 33 (2015), 489–491.
Khatodia, S., Bhatotia, K., Passricha, N., Khurana, S., Tuteja, N., The CRISPR/Cas genome-editing tool: application in improvement of crops. Front. Plant Sci., 7, 2016, 506.
Araki, M., Ishii, T., Towards social acceptance of plant breeding by genome editing. Trends Plant Sci. 20 (2015), 145–149.
Jones, H.D., Regulatory uncertainty over genome editing. Native Plants, 1, 2015, 14011.
Voytas, D.F., Gao, C., Precision genome engineering and agriculture: opportunities and regulatory challenges. PLoS Biol., 12, 2014 e1001877.
Waltz, E., Gene-edited CRISPR mushroom escapes US regulation. Nature, 532, 2016, 293.
Wolt, J.D., Wang, K., Yang, B., The regulatory status of genome‐edited crops. Plant Biotechnology Journal 14 (2016), 510–518.
Kim, H., Kim, J.-S., A guide to genome engineering with programmable nucleases. Nat. Rev. Genet. 15 (2014), 321–334.