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Crop genes modified using CRISPR/Cas system

https://doi.org/10.18699/VJ17.244

Abstract

The CRISPR/Cas system is the most promising among genome editing tools. It can provide the development of modified nontransgenic plants with the possibility of simultaneous multiple targeted mutations. The purpose of this review is to analyze published papers describing the utilization of the CRISPR/Cas system for crop gene modification in order to assess the potential of this technology as a new plant breeding technique. The search for “CRISPR & crop name” within article titles, abstracts and keywords in the Scopus database was carried out for 45 crops. Among a total of 206 search results, only 88 have been recognized as original articles describing editing crop genes with the CRISPR/Cas system. A total of 145 target genes of 15 crops are described in these 88 articles, including rice with the largest number of genes modified (78 genes). In these studies, the ability to get transgene-free modified plants was widely demonstrated. However, in most cases research was aimed at the approbation of the technology or was to elucidate target gene function, while modification of just 37 target genes was related with crop improvement. We present here a catalogue of these genes. In most of these cases, modifications resulted in knockout of the genes such as negative growth and development regulators or negative regulators of plant resistance. In most cases, the phenotype of modified plants was assessed, and the presence of desired changes was shown. However, since the estimated number of “negative regulators” is limited in plant genomes, the CRISPR-directed gene knockout has a restricted potential for crop improvement. Intensive application of the CRISPR/Cas system for more complicate modifications such as replacement of defect alleles by functional ones or insertion of a desired gene is required (so far reports about such modifications are very rare in crops). In addition, to provide a basis for broad practical application of CRISPR/Cas-based genome editing, more cultivars of crop species should be involved in ongoing studies. Just a few genotypes of crop species have been used for gene modifications thus far. Nevertheless, in spite of the restrictions mentioned, essential success has been achieved over a short period (3.5 years since the first publications on CRISPR/Cas application in plants).

About the Authors

A. M. Korotkova
Institute of Cytology and Genetics SB RAS
Russian Federation
Novosibirsk


S. V. Gerasimova
Institute of Cytology and Genetics SB RAS
Russian Federation
Novosibirsk


V. K. Shumny
Institute of Cytology and Genetics SB RAS; Novosibirsk State University
Russian Federation
Novosibirsk


E. K. Khlestkina
Institute of Cytology and Genetics SB RAS; Novosibirsk State University
Russian Federation
Novosibirsk


References

1. Andersson M., Turesson H., Nicolia A., Fält 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. 2017;36:117-128. DOI 10.1007/s00299-016-2062-3.

2. Butler N.M., Baltes N.J., Voytas D.F., Douches D.S. Geminivirusmediated genome editing in potato (Solanum tuberosum L.) using sequence-specific nucleases. Front Plant Sci. 2016;7:1045. DOI 10.3389/fpls.2016.01045.

3. 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. 2016;17:1140-1153. DOI 10.1111/mpp.12375.

4. Feng Z., Zhang B., Ding W., Liu X., Yang D.L., Wei P., Cao F., Zhu S., Zhang F., Mao Y., Zhu J.K. Efficient genome editing in plants using a CRISPR/Cas system. Cell Res. 2013;23:1229-1232. DOI 10.1038/cr.2013.11.

5. Gerasimova S.V., Khlestkina E.K., Kochetov A.V., Shumny V.K. Genome editing system CRISPR/CAS9 and peculiarities of its application in monocots. Fiziologiya rasteniy = Plant Physiology (Moscow). 2017;64:92-108. DOI 10.7868/S0015330317010079. (in Russian)

6. Jia H., Zhang Y., Orbović V., Xu J., White F.F., Jones J.B., Wang N. Genome editing of the disease susceptibility gene CsLOB1 in citrus confers resistance to citrus canker. Plant Biotechnol. J. 2017. DOI 10.1111/pbi.12677.

7. Khlestkin V.K., Peltek S.E., Kolchanov N.A. Target genes for development of potato (Solanum tuberosum L.) cultivars with desired starch properties (review). Selskokhozyaystvennaya Biologiya = Agricultural Biology. 2017;52(1):25-36. DOI 10.15389/agrobiology.2017.1.25eng. (in Russian)

8. Khlestkina E.K., Shumny V.K. Prospects for application of breakthrough technologies in breeding: The CRISPR/Cas9 system for plant genome editing. Russian Journal of Genetics. 2016;52(7): 676687. DOI 10.7868/S0016675816070055. (in Russian)

9. Klap C., Yeshayahou E., Bolger A.M., Arazi T., Gupta S.K., Shabtai S., Usadel B., Salts Y., Barg R. Tomato facultative parthenocarpy results from Sl AGAMOUS-LIKE 6 loss of function. Plant Biotechnol. J. 2016. DOI 10.1111/pbi.12662.

10. Lawrenson T., Shorinola O., Stacey N., Li C., Østergaard L., Patron N., Uauy C., Harwood W. Induction of targeted, heritable mutations in barley and Brassica oleracea using RNA-guided Cas9 nuclease. Genome Biol. 2015;16:258. DOI 10.1186/s13059-015-0826-7.

11. Li J., Meng X., Zong Y., Chen K., Zhang H., Liu J., Li J., Gao C. Gene replacements and insertions in rice by intron targeting using CRISPRCas9. Nat. Plant. 2016a;2:16139. DOI 10.1038/nplants.2016.139.

12. Li J.F., Norville J.E., Aach J., McCormack M., Zhang D., Bush J., Church G.M., Sheen J. l. Multiplex and homologous recombinationmediated genome editing in Arabidopsis and Nicotiana benthamiana using guide RNA and Cas9. Nat. Biotechnol. 2013;31:688-691. DOI 10.1038/nbt.2654.

13. Li M., Li X., Zhou Z., Wu P., Fang M., Pan X., Lin Q., Luo W., Wu G., Li H. Reassessment of the four yield-related genes Gn1a, DEP1, GS3, and IPA1 in rice using a CRISPR/Cas9 system. Front Plant Sci. Frontiers. 2016b;7:377. DOI 10.3389/fpls.2016.0037.

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

15. Li Z., Liu Z.-B., Xing A., Moon B.P., Koellhoffer J.P., Huang L., Ward R.T., Clifton E., Falco S.C., Cigan A.M. Cas9-guide RNA Directed genome editing in soybean. Plant Physiol. 2015;169:960-970. DOI 10.1104/pp.15.00783.

16. Liang Z., Chen K., Li T., Zhang Y., Wang Y., Zhao Q., Liu J., Zhang H., Liu C., Ran Y., Gao C. Efficient DNA-free genome editing of bread wheat using CRISPR/Cas9 ribonucleoprotein complexes. Nat. Commun. 2017;8:14261. DOI 10.1038/ncomms14261.

17. Lu Y., Zhu J.-K. Precise editing of a target base in the rice genome using a modified CRISPR/Cas9 system. Mol. Plant. 2017. DOI 10.1016/j.molp.2016.11.013.

18. Malnoy M., Viola R., Jung M.-H., Koo O.-J., Kim S., Kim J.-S., Velasco R., Kanchiswamy C.N. DNA-Free genetically edited grapevine and apple protoplast using CRISPR/Cas9 ribonucleoproteins. Frontiers in Plant Sci. 2016;7:1904. DOI 10.3389/fpls.2016.01904.

19. Nekrasov V., Staskawicz B., Weigel D., Jones J.D., Kamoun S. Targeted mutagenesis in the model plant Nicotiana benthamiana using Cas9 RNA-guided endonuclease. Nat. Biotechnol. 2013;31:691693. DOI 10.1038/nbt.2655.

20. Permiakova M.D., Trufanov V.A., Pshenichnikova T.A., Ermakova M.F. Role of lipoxygenase in the determination of wheat grain quality. Prikl. Biokhim. Mikrobiol. = Applied Biochemistry and Microbiology. 2010;46(1):96-102. (in Russian)

21. Sauer N.J., Narváez-Vásquez J., Mozoruk J., Miller R.B., Warburg Z.J., Woodward M.J., Mihiret Y.A., Lincoln T.A., Segami R.E., Sanders S.L., Walker K.A., Beetham P.R., Schöpke C.R., Gocal G.F. Oligonucleotide-mediated genome editing provides precision and function to engineered nucleases and antibiotics in plants. Plant Physiol. 2016;170:1917-1928. DOI 10.1104/pp.15.01696.

22. Shan Q., Wang Y., Li J., Zhang Y., Chen K., Liang Z., Zhang K., Liu J., Xi J.J., Qiu J.L., Gao C. Targeted genome modification of crop plants using a CRISPR-Cas system. Nat. Biotechnol. 2013;31:686688. DOI 10.1038/nbt.2650.

23. Shen L., Wang C., Fu Y., Wang J., Liu Q., Zhang X., Yan C., Qian Q., Wang K. QTL editing confers opposing yield performance in different rice varieties. J. Integr. Plant Biol. 2016. DOI 10.1111/jipb.12501.

24. Shi J., Gao H., Wang H., Lafitte H.R., Archibald R.L., Yang M., Hakimi S.M., Mo H., Habben J.E. ARGOS8 variants generated by CRISPR-Cas9 improve maize grain yield under field drought stress conditions. Plant Biotechnol. J. 2017;15:207-216. DOI 10.1111/pbi.12603.

25. Soyk S., Müller N.A., Park S.J., Schmalenbach I., Jiang K., Hayama R., Zhang L., Van Eck J., Jiménez-Gómez J.M., Lippman Z.B. Variation in the flowering gene SELF PRUNING 5G promotes day-neutrality and early yield in tomato. Nat. Genet. 2016;49:162-168. DOI 10.1038/ng.3733.

26. Sun Y., Zhang X., Wu C., He Y., Ma Y., Hou H., Guo X., Du W., Zhao Y., Xia L. Engineering herbicide-resistant rice plants through CRISPR/ Cas9-mediated homologous recombination of acetolactate synthase. Mol. Plant. 2016;628-631. DOI 10.1016/j.molp.2016.01.001.

27. Svitashev S., Young J.K., Schwartz C., Gao H., Falco S.C., Cigan A.M. Targeted mutagenesis, precise gene editing, and site-specific gene insertion in maize using Cas9 and guide RNA. Plant Physiol. 2015; 169:931-945. DOI 10.1104/pp.15.00793.

28. Tang F., Yang S., Liu J., Zhu H. Rj4, a Gene controlling nodulation specificity in soybeans, encodes a thaumatin-like protein but not the one previously reported. Plant Physiol. 2016;170:26-32. DOI 10.1104/pp.15.01661.

29. Wang F., Wang C., Liu P., Lei C., Hao W., Gao Y., Liu Y.G., Zhao K. Enhanced rice blast resistance by CRISPR/Cas9-targeted mutagenesis of the ERF transcription factor gene OsERF922. PLoS ONE. 2016;11:e0154027. DOI. 10.1371/journal.pone.0154027.

30. Wang Y., Cheng X., Shan Q., Zhang Y., Liu J., Gao C., Qiu J.L. Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nat. Biotechnol. 2014;32:947-951. DOI 10.1038/nbt.2969.

31. Xie K., Yang Y. RNA-guided genome editing in plants using a CRISPR-Cas system. Mol. Plant. 2013;6:1975-1983. DOI 10.1093/mp/sst119.

32. Xu C., Liberatore K.L., MacAlister C.A., Huang Z., Chu Y.-H., Jiang K., Brooks C., Ogawa-Ohnishi M., Xiong G., Pauly M., Van Eck J., Matsubayashi Y., van der Knaap E., Lippman Z.B. A cascade of arabinosyltransferases controls shoot meristem size in tomato. Nat. Genet. 2015;47:784-792. DOI 10.1038/ng.3309.

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

34. Zhang Y., Liang Z., Zong Y., Wang Y., Liu J., Chen K., Qiu J.-L., Gao C. Efficient and transgene-free genome editing in wheat through transient expression of CRISPR/Cas9 DNA or RNA. Nat. Commun. 2016;7:12617. DOI. 10.1038/ncomms12617.

35. Zheng X., Yang S., Zhang D., Zhong Z., Tang X., Deng K., Zhou J., Qi Y., Zhang Y. Effective screen of CRISPR/Cas9-induced mutants in rice by single-strand conformation polymorphism. Plant Cell Rep. 2016;35:1545-1554. DOI 10.1007/s00299-016-1967-1.

36. Zhou H., He M., Li J., Chen L., Huang Z., Zheng S., Zhu L., Ni E., Jiang D., Zhao B., Zhuang C. Development of commercial thermosensitive genic male sterile rice accelerates hybrid rice breeding using the CRISPR/Cas9-mediated TMS5 editing system. Sci. Rep. 2016;6:37395. DOI 10.1038/srep37395.

37. Zlobin N.E., Ternovoy V.V., Grebenkina N.A., Taranov V.V. Making complex things simpler: modern tools to edit the plant genome. Vavilovskii Zhurnal Genetiki i Selektsii = Vavilov Journal of Genetics and Breeding. 2017;21(1):104-111. DOI 10.18699/VJ17.228. (in Russian)


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