DOI: https://doi.org/10.21498/2518-1017.15.1.2019.162478

CRISPR/Cas technology for crop improvement (review)

Н. Е. Волкова, О. О. Захарова

Abstract


Purpose. To analyze the current state of crop improvement using CRISPR/Cas technology of genome modifications.

Results. The history of the development of genome editing technologies with site-specific endonucleases is presented. The current state of plant varieties creation using these technologies was analyzed. It was shown that CRISPR/Cas technology of gene editing has already been adapted for 20 species of crops, for more than 150 genes associated with important traits. The practical implementation of this technology was presented on the example of rice, for which the greatest progress in the research and use of CRISPR/Cas technology was observed: the largest number of genes has been modified – 78; more than 20 varieties were obtained. Edited rice genes associated with such traits as grain size, grain number, plant height, male sterility, cesium accumulation, tolerance to abiotic and biotic stresses, and resistance to herbicides. The possibility of multiplex editing of a potentially unlimited number of genes was underlined. The situation on the regulation of plants created by genome editing technology was discussed: according to the decision of the European Union (EU) court, all EU regulations and restrictions on the cultivation and sale of products, in particular plant varieties, obtained using genome editing techniques are applied as well as to GMOs, while according to the USDA such plants, except parasitic plants, are not regulated as GMOs. Information on the statement, approved by leading scientists representing more than 90 European research centers and institutes for the study of plants and biological sciences was provided in support of genome editing technology.

Conclusions. Among the genome editing technologies, CRISPR/Cas technology is one of the most powerful approaches, which has become extensively used in plant breeding due to such advantages as high accuracy and quality, efficiency and technical flexibility, relatively low cost compared to other methods. This available method allows obtaining non-transgenic plants with specified modifications, and it is possible to simultaneously “produce” mutations in several targets.


Keywords


genetic modification; genome editing; site-specific endonucleases; gene knockout

References


FAO, IFAD, UNICEF, WFP, & WHO. (2018). The State of food security and nutrition in the world 2018. Building climate resilience for food security and nutrition. Rome: FAO.

Transforming our world: the 2030 Agenda for Sustainable Development. (2015). Retrieved from http://www.un.org/ga/search/view_doc.asp?symbol=A/RES/70/1&Lang=E

Jinek, M., Chylinski, K., Fonfara, I., Hauer, M., Doudna, J., & Charpentier, E. (2012). A programmable dual-RNA–guided DNA endonuclease in adaptive bacterial immunity. Science, 337(6096), 816–821. doi: 10.1126/science.1225829

Govindan, G., & Ramalingam, S. (2016). Programmable site-specific nucleases for targeted genome engineering in higher eukaryotes. J. Cell. Physiol., 231(11), 2380–2392. doi: 10.1002/jcp.25367

Ishino, Y., Shinagawa, H., Makino, K., Amemura, M., & Nakata, A. (1987). Nucleotide sequence of the IAP gene, responsible for alkaline phosphatase isozyme conversion in Escherichia coli, and identification of the gene product. J. Bacteriol., 169(12), 5429–5433. doi: 10.1128/jb.169.12.5429-5433.1987

Jansen, R., Embden, J., Gaastra, W., & Schouls, L. (2002). Identification of genes that are associated with DNA repeats in prokaryotes. Mol. Microbiol., 43(6), 1565–1575. doi: 10.1046/j.1365-2958.2002.02839.x

Sontheimer, E., & Barrangou, R. (2015). The bacterial origins of the CRISPR genome-editing revolution. Hum. Gene Ther., 26(7), 413–424. doi: 10.1089/hum.2015.091

Liu, X., Wu, S., Xu, J., Sui, C., & Wei, J. (2017). Application of CRISPR/Cas9 in plant biology. Acta Pharm. Sin. B., 7(3), 292–302. doi: 10.1016/j.apsb.2017.01.002

Arora, L., & Narula, A. (2017). Gene editing and crop improvement using CRISPR-Cas9 system. Front Plant Sci., 8, 1932. doi: 10.3389/fpls.2017.01932

Langner, T., Kamoun, S., & Belhaj, K. (2018). CRISPR crops: plant genome editing toward disease resistance. Ann. Review Phytopathol., 56, 479–512. doi: 10.1146/annurev-phyto-080417-050158

Lundgren, M., Charpentier, E., & Fineran, P. (Eds.). (2015). CRISPR. Methods and Protocols. New York, USA: Humana Press. doi: 10.1007/978-1-4939-2687-9

Jung, C., Capistrano-Gossmann, G., Braatz, J., Sashidhar, N., & Melzer, S. (2018). Recent developments in genome editing and applications in plant breeding. Plant Breed., 137(1), 1–9. doi: 10.1111/pbr.12526

Osakabe, Y., Watanabe, T., Sugano, S., Ueta, R., Ishihara, R., Shinozaki, K., & Osakabe, K. (2016). Optimization of CRISPR/Cas9 genome editing to modify abiotic stress responses in plants. Sci. Rep., 6, 26685. doi: 10.1038/srep26685

Ricroch, A., Clairand, P., & Harwood, W. (2017). Use of CRISPR systems in plant genome editing: toward new opportunities in agriculture. Emerg. Top. Life Sci., 1(2), 169–182. doi: 10.1042/ETLS20170085

Korotkova, A. M., Gerasimova, S. V., Shumny, V. K., & Khlestkina, E. K. (2017). Crop genes modified using CRISPR/Cas system. Vavilovskii Zhurnal Genetiki i Selekcii [Vavilov Journal of Genetics and Breeding], 21(2), 250–258. doi: 10.18699/VJ17.244

Jaganathan, D., Ramasamy, K., Sellamuthu, G., Jayabalan, S., & Venkataraman, G. (2018). CRISPR for crop improvement: an update review. Front. Plant Sci., 9, 985. doi: 10.3389/fpls.2018.00985

Xu, R., Yang, Y., Qin, R., Li, H., Qiu, C., Li, L., ... Yang, J. (2016). Rapid improvement of grain weight via highly efficient CRISPR/Cas9-mediated multiplex genome editing in rice. J. Genet. Genomics., 43(8), 529–532. doi: 10.1016/j.jgg.2016.07.003

Li, M., Li, X., Zhou, Z., Wu, P., Fang, M., Pan, X., ... Li, H. (2016). Reassessment of the four yield-related genes Gn1a, DEP1, GS3, and IPA1 in rice using a CRISPR/Cas9 system. Front. Plant Sci., 7, 377. doi: 10.3389/fpls.2016.0037

Shen, L., Wang, C., Fu, Y., Wang, J., Liu, Q., Zhang, X., ... Wang, K. (2018). QTL editing confers opposing yield performance in different rice varieties. J. Integr. Plant Biol., 60(2), 89–93. doi: 10.1111/jipb.12501

Lu, Y., & Zhu, J. (2017). Precise editing of a target base in the rice genome using a modified CRISPR/Cas9 system. Mol. Plant., 10(3), 523–525. doi: 10.1016/j.molp.2016.11.013

Zhou, H., He, M., Li, J., Chen, L., Huang, Z., Zheng, S., ... Zhuang, C. (2016). Development of commercial thermosensitive genic male sterile rice accelerates hybrid rice breeding using the CRISPR/Cas9-mediated TMS5 editing system. Sci. Rep., 6, 37395. doi: 10.1038/srep37395

Li, Q., Zhang, D., Chen, M., Liang, W., Wei, J., Qi, Y., & Yuan, Z. (2016). Development of japonica photo-sensitive genic male sterile rice lines by editing carbon starved anther using CRISPR/ Cas9. J. Genet. Genomics., 43(6), 415–419. doi: 10.1016/j.jgg.2016.04.011

Shan, Q., Wang, Y., Li, J., Zhang, Y., Chen, K., Liang, Z., ... Gao, C. (2013). Targeted genome modification of crop plants using a CRISPR-Cas system. Nat. Biotechnol., 31(8), 686–688. doi: 10.1038/nbt.2650

Li, J., Sun, Y., Du, J., Zhao, Y., & Xia, L. (2017). Generation of targeted point mutations in rice by a modified CRISPR/Cas9 system. Mol. Plant., 10(3), 526–529. doi: 10.1016/j.molp.2016.12.001

Xie, K., & Yang, Y. (2013). RNA-guided genome editing in plants using a CRISPR-Cas system. Mol. Plant., 6(6), 1975–1983. doi: 10.1093/mp/sst119

Shen, L., Hua, Y., Fu, Y. Li, J., Liu, Q., Jiao, X., ... Wang, K. (2017). Rapid generation of genetic diversity by multiplex CRISPR/Cas9 genome editing in rice. Sci. China Life Sci., 60(5), 506–515. doi: 10.1007/s11427-017-9008-8

Sun, Y., Zhang, X., Wu, C., He, Y., Ma, Y., Hou, H., ... Xia, L. (2016). Engineering herbicide-resistant rice plants through CRISPR/Cas9-mediated homologous recombination of acetolactate synthase. Mol. Plant., 9(4), 628–631. doi: 10.1016/j.molp.2016.01.001

Shimatani, Z., Kashojiya, S., Takayama, M., Terada, R., Arazoe, T., Ishii, H., ... Kondo, A. (2017). Targeted base editing in rice and tomato using a CRISPR-Cas9 cytidine deaminase fusion. Nat. Biotechnol., 35(5), 441–443. doi: 10.1038/nbt.3833

Nieves-Cordones, M., Mohamed, S., Tanoi, K., Kobayashi, N., Takagi, K., Vernet, A., ... Véry, A. (2017). Production of low-Cs+ rice plants by inactivation of the K+ transporter OsHAK1 with the CRISPR-Cas system. Plant J., 92(1), 43–56. doi: 10.1111/tpj.13632

Mao, X., Zheng, Y., Xiao, K., Wei, Y., Zhu, Y., Cai, Q., ... Zhang, J. (2018). OsPRX2 contributes to stomatal closure and improves potassium deficiency tolerance in rice. Biochem. Biophys. Res. Commun., 495(1), 461–467. doi: 10.1016/j.bbrc.2017.11.045

Liu, D., Chen, X., Liu, J., Ye, J., & Guo, Z. (2012). The rice ERF transcription factor OsERF922 negatively regulates resistance to Magnaporthe oryzae and salt tolerance. J. Exp. Bot., 63(10), 3899–3912. doi: 10.1093/jxb/ers079

Zhou, J., Peng, Z., Long, J., Sosso, D., Liu, B., Eom, J., ... Yang, B. (2015). Gene targeting by the TAL effector PthXo2 reveals cryptic resistance gene for bacterial blight of rice. Plant J., 82(4), 632–643. doi: 10.1111/tpj.12838

Wang, F., Wang, C., Liu, P., Zhang, Q., Li, L., Zhong, C., ... Zhao, K. (2016). Enhanced rice blast resistance by CRISPR/Cas9-targeted mutagenesis of the ERF transcription factor gene OsERF922. PLoS ONE, 11(4), e0154027. doi: 10.1371/journal.pone.0154027

Lowder, L., Zhang, D., Baltes, N., Paul, J., Tang, X., Zheng, X., ... Qi, Y. (2015). A CRISPR/Cas9 toolbox for multiplexed plant genome editing and transcriptional regulation. Plant Physiol., 169(2), 971–985. doi: 10.1104/pp.15.00636

Zhang, Z., Mao, Y., Ha, S., Liu, W., Botella, J., & Zhu, J. (2016). A multiplex CRISPR/Cas9 platform for fast and efficient editing of multiple genes in Arabidopsis. Plant Cell Rep., 35(7), 1519–1533. doi: 10.1007/s00299-015-1900-z

Secretary Perdue Issues USDA Statement on Plant Breeding Innovation. Press Release No 0070.18. (2018). Retrieved from https://www.usda.gov/media/press-releases/2018/03/28/secretary-perdue-issues-usda-statement-plant-breeding-innovation

Court of Justice of the European Union. (2018). Organisms obtained by mutagenesis are GMOs and are, in principle, subject to the obligations laid down by the GMO Directive. Press release No 111/18. Retrieved from https://curia.europa.eu/jcms/upload/docs/application/pdf/2018-07/cp180111en.pdf

Directive 2001/18/EC of the European Parliament and of the Council of 12 March 2001 on the deliberate release into the environment of genetically modified organisms and repealing. Council Directive 90/220/EEC. L 106/2 EN. Retrieved from https://eur-lex.europa.eu/resource.html?uri=cellar:303dd4fa-07a8-4d20-86a8-0baaf0518d22.0004.02/DOC_1&format=PDF

Wight, A. (2018). Strict EU ruling on gene-edited crops squee­zes science. Nature, 56(7729), 15–16. doi: 10.1038/d41586-018-07166-7

Kupferschmidt, K. (2018). EU verdict on CRISPR crops dismays scientists. Science, 361(6401), 435–436. doi: 10.1126/science.361.6401.435

Regulating genome edited organisms as GMOs has negative consequences for agriculture, society and economy (2018). Retrieved from https://www.cnb.csic.es/images/temporal/Position_paper_on_the_ECJ_ruling_on_CRISPR_22_Oct_2018.pdf


GOST Style Citations


The State of food security and nutrition in the world 2018. Building climate resilience for food security and nutrition / FAO, IFAD, UNICEF, WFP and WHO. Rome : FAO, 2018. 202 p.

Transforming our world: the 2030 Agenda for Sustainable Development. URL: http://www.un.org/ga/search/view_doc.asp?symbol=A/RES/70/1&Lang=E

Jinek M., Chylinski K., Fonfara I. et al. A programmable dual-RNA–guided DNA endonuclease in adaptive bacterial immunity. Science. 2012. Vol. 337, Iss. 6096. P. 816–821. doi: 10.1126/science.1225829

Govindan G., Ramalingam S. Programmable site-specific nucleases for targeted genome engineering in higher eukaryotes. J. Cell. Physiol. 2016. Vol. 231, Iss. 11. P. 2380–2392. doi: 10.1002/jcp.25367

Ishino Y., Shinagawa H., Makino K. et al. Nucleotide sequence of the iap gene, responsible for alkaline phosphatase isozyme conversion in Escherichia coli, and identification of the gene product. J. Bacteriol. 1987. Vol. 169, Iss. 12. Р. 5429–5433. doi: 10.1128/jb.169.12.5429-5433.1987

Jansen R., Embden J., Gaastra W., Schouls L. Identification of genes that are associated with DNA repeats in prokaryotes. Mol. Microbiol. 2002. Vol. 43, Iss. 6. P. 1565–1575. doi: 10.1046/j.1365-2958.2002.02839.x

Sontheimer E., Barrangou R. The bacterial origins of the CRISPR genome-editing revolution. Hum. Gene Ther. 2015. Vol. 26, Iss. 7. P. 413–424. doi: 10.1089/hum.2015.091

Liu X., Wu S., Xu J. et al. Application of CRISPR/Cas9 in plant biology. Acta Pharm. Sinica B. 2017. Vol. 7, Iss. 3. Р. 292–302. doi: 10.1016/j.apsb.2017.01.002

Arora L., Narula A. Gene editing and crop improvement using CRISPR-Cas9 system. Front Plant Sci. 2017. Vol. 8: 1932. doi: 10.3389/fpls.2017.01932

Langner T., Kamoun S., Belhaj K. CRISPR crops: plant genome editing toward disease resistance. Ann. Review Phytopathol. 2018. Vol. 56. Р. 479–512. doi: 10.1146/annurev-phyto-080417-050158

CRISPR. Methods and Protocols / M. Lundgren, E. Charpentier, P. Fineran (eds). New York, USA : Humana Press, 2015. doi: 10.1007/978-1-4939-2687-9

Jung C., Capistrano-Gossmann G., Braatz J. et al. Recent deve­lopments in genome editing and applications in plant breeding. Plant Breed. 2018. Vol. 137, Iss. 1. Р. 1–9. doi: 10.1111/pbr.12526

Osakabe Y., Watanabe T., Sugano S. et al. Optimization of CRISPR/Cas9 genome editing to modify abiotic stress responses in plants. Sci. Rep. 2016. Vol. 6: 26685. doi: 10.1038/srep26685

Ricroch A., Clairand P., Harwood W. Use of CRISPR systems in plant genome editing: toward new opportunities in agriculture. Emerg. Top. Life Sci. 2017. Vol. 1, Iss. 2. Р. 169–182. doi: 10.1042/ETLS20170085

Короткова А. М., Герасимова С. В., Шумный В. К., Хлесткина Е. К. Гены сельскохозяйственных растений, модифицированные с помощью системы CRISPR/Cas. Вавиловский журнал генетики и селекции. 2017. Т. 21, № 2. С. 250–258. doi: 10.18699/VJ17.244

JaganathanD., RamasamyK., SellamuthuG. etal. CRISPR for crop improvement: an update review. Front. Plant Sci. 2018. Vol. 9: 985. doi: 10.3389/fpls.2018.00985

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, Iss. 4. Р. 529–532. doi: 10.1016/j.jgg.2016.07.003

Li M., Li X., Zhou Z. et al. Reassessment of the four yield-related genes Gn1a, DEP1, GS3, and IPA1 in rice using a CRISPR/Cas9 system. Front. Plant Sci. 2016. Vol. 7: 377. doi: 10.3389/fpls.2016.0037

Shen L., Wang C., Fu Y. et al. QTL editing confers opposing yield performance in different rice varieties. J. Integr. Plant Biol. 2018. Vol. 60, Iss. 2. Р. 89–93. doi: 10.1111/jipb.12501

Lu Y., Zhu J. Precise editing of a target base in the rice genome using a modified CRISPR/Cas9 system. Mol. Plant. 2017. Vol. 10, Iss. 3. Р. 523–525. doi: 10.1016/j.molp.2016.11.013

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

Li Q., Zhang D., Chen M. et al. Development of japonica photo-sensitive genic male sterile rice lines by editing carbon starved anther using CRISPR/Cas9. J. Genet. Genomics. 2016. Vol. 43, Iss. 6. Р. 415–419. doi: 10.1016/j.jgg.2016.04.011

Shan Q., Wang Y., Li J. et al. Targeted genome modification of crop plants using a CRISPR-Cas system. Nat. Biotechnol. 2013. Vol. 31, Iss. 8. Р. 686–688. doi: 10.1038/nbt.2650

Li J., Sun Y., Du J. et al. Generation of targeted point mu­tations in rice by a modified CRISPR/Cas9 system. Mol. Plant. 2017. Vol. 10, Iss. 3. Р. 526–529. doi: 10.1016/j.molp.2016.12.001

Xie K., Yang Y. RNA-guided genome editing in plants using a CRISPR-Cas system. Mol. Plant. 2013. Vol. 6, Iss. 6. Р. 1975–1983. doi: 10.1093/mp/sst119

Shen L., Hua Y., Fu Y. et al. Rapid generation of genetic diversity by multiplex CRISPR/Cas9 genome editing in rice. Sci. China Life Sci. 2017. Vol. 60, Iss. 5. Р. 506–515. doi: 10.1007/s11427-017-9008-8

Sun Y., Zhang X., Wu C. et al. Engineering herbicide-re­sis­tant rice plants through CRISPR/Cas9-mediated homologous recombination of acetolactate synthase. Mol. Plant. 2016. Vol. 9, Iss. 4. Р. 628–631. doi: 10.1016/j.molp.2016.01.001

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, Iss. 5. Р. 441–443. doi: 10.1038/nbt.3833

Nieves-Cordones M., Mohamed S., Tanoi K. et al. Production of low-Cs+ rice plants by inactivation of the K+ transporter OsHAK1 with the CRISPR-Cas system. Plant J. 2017. Vol. 92, Iss. 1. Р. 43–56. doi: 10.1111/tpj.13632

Mao X., Zheng Y., Xiao K. et al. OsPRX2 contributes to stomatal closure and improves potassium deficiency tolerance in rice. Biochem. Biophys. Res. Commun. 2018. Vol. 495, Iss. 1. Р. 461–467. doi: 10.1016/j.bbrc.2017.11.045

Liu D., Chen X., Liu J. et al. The rice ERF transcription factor OsERF922 negatively regulates resistance to Magnaporthe oryzae and salt tolerance. J. Exp. Bot. 2012. Vol. 63, Iss. 10. Р. 3899–3911. doi: 10.1093/jxb/ers079

Zhou J., Peng Z., Long J. et al. Gene targeting by the TAL effector PthXo2 reveals cryptic resistance gene for bacterial blight of rice. Plant J. 2015. Vol. 82, Iss. 4. Р. 632–643. doi: 10.1111/tpj.12838

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, Iss. 4: e0154027. doi: 10.1371/journal.pone.0154027

Lowder L., Zhang D., Baltes N. et al. A CRISPR/Cas9 toolbox for multiplexed plant genome editing and transcriptional regulation. Plant Physiol. 2015. Vol. 169, Iss. 2. Р. 971–985. doi: 10.1104/pp.15.00636

Zhang Z., Mao Y., Ha S. et al. A multiplex CRISPR/Cas9 platform for fast and efficient editing of multiple genes in Arabidopsis. Plant Cell Rep. 2016. Vol. 35, Iss. 7. Р. 1519–1533. doi: 10.1007/s00299-015-1900-z

Secretary Perdue Issues USDA Statement on Plant Breeding Innovation. Press Release No 0070.18. URL: https://www.usda.gov/media/press-releases/2018/03/28/secretary-perdue-issues-usda-statement-plant-breeding-innovation

Organisms obtained by mutagenesis are GMOs and are, in principle, subject to the obligations laid down by the GMO Directive / Court of Justice of the European Union. Press release No 111/18. URL: https://curia.europa.eu/jcms/upload/docs/application/pdf/2018-07/cp180111en.pdf

Directive 2001/18/EC of the European Parliament and of the Council of 12 March 2001 on the deliberate release into the environment of genetically modified organisms and repealing. Council Directive 90/220/EEC. URL: https://eur-lex.europa.eu/resource.html?uri=cellar:303dd4fa-07a8-4d20-86a8-0baaf0518d22.0004.02/DOC_1&format=PDF

Wight A. Strict EU ruling on gene-edited crops squeezes science. Nature. 2018. Vol. 56, Iss. 7729. P. 15–16. doi: 10.1038/d41586-018-07166-7

Kupferschmidt K. EU verdict on CRISPR crops dismays scientists. Science. 2018. Vol. 361, Iss. 6401. P. 435–436. doi: 10.1126/science.361.6401.435

Regulating genome edited organisms as GMOs has negative consequences for agriculture, society and economy. URL: https://www.cnb.csic.es/images/temporal/Position_paper_on_the_ECJ_ruling_on_CRISPR_22_Oct_2018.pdf







Creative Commons License
This work is licensed under a Creative Commons Attribution-ShareAlike 4.0 International License.

DOI: 10.21498/2518-1017

Flag Counter