Targeted mutagenesis in soybean using the CRISPR-Cas9 system

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Sun, Xianjun ^a,b   Hu, Zheng ^b   Chen, Rui ^c   Jiang, Qiyang ^b   Song, Guohua ^b   Zhang, Hui ^b   Xi, Yajun ^a  

^a NORTHWEST A F UNIVERSITY   (China)

^b INSTITUTE OF PLANT PROTECTION   (China)

^c Tianjin Academy of Agricultural Sciences   (China)

Author keywords

[No Author keywords available]

Indexed keywords

SOYBEAN PROTEIN;

ARABIDOPSIS; CRISPR CAS SYSTEM; GENETIC ENGINEERING; GENETICS; MUTAGENESIS; MUTATION; PLANT GENOME; RNA EDITING; SOYBEAN;

ARABIDOPSIS; CRISPR-CAS SYSTEMS; GENETIC ENGINEERING; GENOME, PLANT; MUTAGENESIS; MUTATION; RNA EDITING; SOYBEAN PROTEINS; SOYBEANS;

EID: 84930651072     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep10342     Document Type: Article

References (53)

1. Chen, K. & Gao, C. Targeted genome modification technologies and their applications in crop improvements. Plant Cell Rep. 33, 575-583 (2014).
2. Wyman, C. & Kanaar, R. DNA double-strand break repair: all's well that ends well. Annu. Rev. Genet. 40, 363-383 (2006).
3. Gaj, T., Gersbach, C. A. & Barbas, C. F., 3rd. ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. Trends Biotechnol. 31, 397-405 (2013).
4. Puchta, H. & Fauser, F. Synthetic nucleases for genome engineering in plants: prospects for a bright future. Plant J. 78, 727-741 (2013).
5. Koonin, E. V. & Makarova, K. S. CRISPR-Cas: an adaptive immunity system in prokaryotes. F1000 Biol. Rep. 1, 95 (2009).
6. Makarova, K. S. et al. Evolution and classification of the CRISPR-Cas systems. Nat. Rev. Microbiol. 9, 467-477 (2011).
7. Bhaya, D., Davison, M. & Barrangou, R. CRISPR-Cas systems in bacteria and archaea: versatile small RNAs for adaptive defense and regulation. Annu. Rev. Genet. 45, 273-297 (2011).
8. Barrangou, R. CRISPR-Cas systems and RNA-guided interference. WIREs RNA 4, 267-278 (2013).
9. Deltcheva, E. et al. CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III. Nature 471, 602-607 (2011).
10. Jinek, M. et al. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337, 816-821 (2012).
11. Kuscu, C., Arslan, S., Singh, R., Thorpe, J. & Adli, M. Genome-wide analysis reveals characteristics of off-target sites bound by the Cas9 endonuclease. Nat. Biotechnol. 32, 677-683 (2014).
12. Wu, X. et al. Genome-wide binding of the CRISPR endonuclease Cas9 in mammalian cells. Nat. Biotechnol. 32, 670-676 (2014).
13. Anders, C., Niewoehner, O., Duerst, A. & Jinek, M. Structural basis of PAM-dependent target DNA recognition by the Cas9 endonuclease. Nature 513, 569-573 (2014).
14. Hsu, P.D., Lander, E. S. & Zhang, F. Development and applications of CRISPR-Cas9 for genome engineering. Cell 157, 1262-1278 (2014).
15. 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. 31, 691-693 (2013).
16. Shan, Q. et al. Targeted genome modification of crop plants using a CRISPR-Cas system. Nat. Biotechnol. 31, 686-688 (2013).
17. Li, J. F. et al. Multiplex and homologous recombination-mediated genome editing in Arabidopsis and Nicotiana benthamiana using guide RNA and Cas9. Nat. Biotechnol. 31, 688-691 (2013).
18. Feng, Z. et al. Efficient genome editing in plants using a CRISPR/Cas system. Cell Res. 23, 1229-1232 (2013).
19. Miao, J. et al. Targeted mutagenesis in rice using CRISPR-Cas system. Cell Res. 23, 1233-1236 (2013).
20. Jiang, W. et al. Demonstration of CRISPR/Cas9/sgRNA-mediated targeted gene modification in Arabidopsis, tobacco, sorghum and rice. Nucleic Acids Res. 41, e188 (2013).
21. Jia, H. & Wang, N. Targeted genome editing of sweet orange using Cas9/sgRNA. PLoS One 9, e93806 (2014).
22. Fauser, F., Schiml, S. & Puchta, H. Both CRISPR/Cas-based nucleases and nickases can be used efficiently for genome engineering in Arabidopsis thaliana. Plant J. 79, 348-359 (2014).
23. Xie, K. & Yang, Y. RNA-guided genome editing in plants using a CRISPR-Cas system. Mol. Plant 6, 1975-1983 (2013).
24. Xiao, A. et al. CasOT: a genome-wide Cas9/gRNA off-target searching tool. Bioinformatics 30, 1180-1182 (2014).
25. Bae, S., Park, J. & Kim, J. S. Cas-OFFinder: a fast and versatile algorithm that searches for potential off-target sites of Cas9 RNAguided endonucleases. Bioinformatics 30, 1473-1475 (2014).
26. Xie, S. S., Shen, B., Zhang, C. B., Huang, X. X. & Zhang, Y. L. sgRNAcas9: A Software Package for Designing CRISPR sgRNA and Evaluating Potential Off-Target Cleavage Sites. PLoS One 9, e100448 (2014).
27. Belhaj, K., Chaparro-Garcia, A., Kamoun, S. & Nekrasov, V. Plant genome editing made easy: targeted mutagenesis in model and crop plants using the CRISPR/Cas system. Plant Methods 9, 39 (2013).
28. Feng, Z. et al. Multigeneration analysis reveals the inheritance, specificity, and patterns of CRISPR/Cas-induced gene modifications in Arabidopsis. Proc. Natl Acad. Sci. USA 111, 4632-4637 (2014).
29. Zhang, H. et al. The CRISPR/Cas9 system produces specific and homozygous targeted gene editing in rice in one generation. Plant Biotechnol. J. 12, 797-807 (2014).
30. Jiang, W. Z., Yang, B. & Weeks, D. P. Efficient CRISPR/Cas9-Mediated Gene Editing in Arabidopsis thaliana and Inheritance of Modified Genes in the T2 and T3 Generations. PLoS One 9, e99225 (2014).
31. Wang, Y. et al. Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nat. Biotechnol. 32, 947-951 (2014).
32. Curtin, S. J. et al. Targeted mutagenesis of duplicated genes in soybean with zinc-finger nucleases. Plant Physiol 156, 466-473 (2011).
33. Waibel, F. & Filipowicz, W. U6 snRNA genes of Arabidopsis are transcribed by RNA polymerase III but contain the same two upstream promoter elements as RNA polymerase II-transcribed U-snRNA genes. Nucleic Acids Res. 18, 3451-3458 (1990).
34. Kereszt, A. et al. Agrobacterium rhizogenes-mediated transformation of soybean to study root biology. Nat. Protoc. 2, 948-952 (2007).
35. Hsu, P. D. et al. DNA targeting specificity of RNA-guided Cas9 nucleases. Nat. Biotechnol. 31, 827-832 (2013).
36. Fu, Y. et al. High-frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells. Nat. Biotechnol. 31, 822-826 (2013).
37. Pattanayak, V. et al. High-throughput profiling of off-target DNA cleavage reveals RNA-programmed Cas9 nuclease specificity. Nat. Biotechnol. 31, 839-843 (2013).
38. Li, X., Jiang, D. H., Yong, K. & Zhang, D. B. Varied Transcriptional Efficiencies of Multiple Arabidopsis U6 Small Nuclear RNA Genes. J. Integr. Plant Biol. 49, 222-229 (2007).
39. Ron, M. et al. Hairy Root Transformation Using Agrobacterium rhizogenes as a Tool for Exploring Cell Type-Specific Gene Expression and Function Using Tomato as a Model. Plant Physiol 166, 455-469 (2014).
40. Severin, A. J. et al. RNA-Seq Atlas of Glycine max: a guide to the soybean transcriptome. BMC Plant Biol. 10, 160 (2010).
41. Ran, F. A. et al. Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell 154, 1380-1389 (2013).
42. Fu, Y., Sander, J. D., Reyon, D., Cascio, V. M. & Joung, J. K. Improving CRISPR-Cas nuclease specificity using truncated guide RNAs. Nat. Biotechnol. 32, 279-284 (2014).
43. Xie, K., Zhang, J. & Yang, Y. Genome-wide prediction of highly specific guide RNA spacers for CRISPR-Cas9-mediated genome editing in model plants and major crops. Mol. Plant 7, 923-926 (2014).
44. Cooper, J. L. et al. TILLING to detect induced mutations in soybean. BMC Plant Biol 8, 9 (2008).
45. Bolon, Y. T. et al. Phenotypic and genomic analyses of a fast neutron mutant population resource in soybean. Plant Physiol 156, 240-253 (2011).
46. Anai, T. Potential of a mutant-based reverse genetic approach for functional genomics and molecular breeding in soybean. Breed Sci 61, 462-467 (2012).
47. Fu, F. F., Ye, R., Xu, S. P. & Xue, H. W. Studies on rice seed quality through analysis of a large-scale T-DNA insertion population. Cell Res. 19, 380-391 (2009).
48. Alonso, J. M. et al. Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301, 653-657 (2003).
49. Pattanayak, V. et al. High-throughput profiling of off-target DNA cleavage reveals RNA-programmed Cas9 nuclease specificity. Nat Biotechnol 31, 839-843 (2013).
50. Cui, Y. et al. Tnt1 retrotransposon mutagenesis: a tool for soybean functional genomics. Plant Physiol 161, 36-47 (2013).
51. Mathieu, M. et al. Establishment of a soybean (Glycine max Merr. L) transposon-based mutagenesis repository. Planta 229, 279-289 (2009).
52. Yoo, S. D., Cho, Y. H. & Sheen, J. Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat. Protoc. 2, 1565-1572 (2007).
53. Edgar, R. C. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460-2461 (2010).