An efficient visual screen for CRISPR/CAS9 activity in arabidopsis thaliana

Frontiers in Plant Science

Volumn 8, Issue , 2017, Pages

  Hahn, Florian ^a   Mantegazza, Otho ^a   Greiner, André ^b   Hegemann, Peter ^b   Eisenhut, Marion ^a   Weber, Andreas P M ^a  

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b HUMBOLDT UNIVERSITY   (Germany)

Author keywords

BASTA; CRISPR Cas9; Gene editing; Glabrous1; Glufosinate; Marker; Trichome

Indexed keywords

EID: 85010908942     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2017.00039     Document Type: Article

References (55)

1. Bae, S., Park, J., and Kim, J. S. (2014). Cas-OFFinder: a fast and versatile algorithm that searches for potential off-target sites of Cas9 RNA-guided endonucleases. Bioinformatics 30, 1473-1475. doi:10.1093/bioinformatics/btu048
2. Baltes, N. J., and Voytas, D. F. (2015). Enabling plant synthetic biology through genome engineering. Trends Biotechnol. 33, 120-131. doi:10.1016/j.tibtech.2014.11.008
3. Bayer, E., Gugel, K. H., Hagele, K., Hagenmaier, H., Jessipow, S., Konig, W. A., et al. (1972). Metabolic products of microorganisms. 98. Phosphinothricin and phosphinothricyl-alanyl-analine. Helv. Chim. Acta 55, 224-239. doi:10.1002/hlca.19720550126
4. Belhaj, K., Chaparro-Garcia, A., Kamoun, S., and Nekrasov, V. (2013). Plant genome editing made easy: targeted mutagenesis in model and crop plants using the CRISPR/Cas system. Plant Methods 9:39. doi:10.1186/1746-4811-9-39
5. Bernhardt, K. (2012). The Role of a Peroxisomal NAD+ Carrier in Plants. Düsseldorf: Heinrich-Heine Universität Düsseldorf.
6. Bortesi, L., and Fischer, R. (2015). The CRISPR/Cas9 system for plant genome editing and beyond. Biotechnol. Adv. 33, 41-52. doi:10.1016/j.biotechadv.2014.12.006
7. Carbonari, C. A., Latorre, D. O., Gomes, G. L. G. C., Velini, E. D., Owens, D. K., Pan, Z. Q., et al. (2016). Resistance to glufosinate is proportional to phosphinothricin acetyltransferase expression and activity in LibertyLink (R) and WideStrike (R) cotton. Planta 243, 925-933. doi:10.1007/s00425-015-2457-3
8. Cho, S. W., Kim, S., Kim, Y., Kweon, J., Kim, H. S., Bae, S., et al. (2014). Analysis of off-target effects of CRISPR/Cas-derived RNA-guided endonucleases and nickases. Genome Res. 24, 132-141. doi:10.1101/gr.162339.113
9. Clough, S. J., and Bent, A. F. (1998). Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743. doi:10.1046/j.1365-313x.1998.00343.x
10. Crawford, K. M., and Zambryski, P. C. (2001). Non-targeted and targeted protein movement through plasmodesmata in leaves in different developmental and physiological states. Plant Physiol. 125, 1802-1812. doi:10.1104/pp.125.4.1802
11. Deblock, M., Botterman, J., Vandewiele, M., Dockx, J., Thoen, C., Gossele, V., et al. (1987). Engineering herbicide resistance in plants by expression of a detoxifying enzyme. Embo J. 6, 2513-2518.
12. Doudna, J. A., and Charpentier, E. (2014). Genome editing. The new frontier of genome engineering with CRISPR-Cas9. Science 346:1258096. doi:10.1126/science.1258096
13. Fauser, F., Schiml, S., and Puchta, H. (2014). Both CRISPR/Cas-based nucleases and nickases can be used efficiently for genome engineering in Arabidopsis thaliana. Plant J. 79, 348-359. doi:10.1111/tpj.12554
14. Fendrych, M., Van Hautegem, T., Van Durme, M., Olvera-Carrillo, Y., Huysmans, M., Karimi, M., et al. (2014). Programmed cell death controlled by ANAC033/SOMBRERO determines root cap organ size in Arabidopsis. Curr. Biol. 24, 931-940. doi:10.1016/j.cub.2014.03.025
15. Feng, Z., Mao, Y., Xu, N., Zhang, B., Wei, P., Yang, D. L., et al. (2014). Multigeneration analysis reveals the inheritance, specificity, and patterns of CRISPR/Cas-induced gene modifications in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 111, 4632-4637. doi:10.1073/pnas.1400822111
16. Fu, Y., Foden, J. A., Khayter, C., Maeder, M. L., Reyon, D., Joung, J. K., et al. (2013). High-frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells. Nat. Biotechnol. 31, 822-826. doi:10.1038/nbt.2623
17. Grefen, C., Donald, N., Hashimoto, K., Kudla, J., Schumacher, K., and Blatt, M. R. (2010). A ubiquitin-10 promoter-based vector set for fluorescent protein tagging facilitates temporal stability and native protein distribution in transient and stable expression studies. Plant J. 64, 355-365. doi:10.1111/j.1365-313X.2010.04322.x
18. Hauser, M. T., Harr, B., and Schlotterer, C. (2001). Trichome distribution in Arabidopsis thaliana and its close relative Arabidopsis lyrata: molecular analysis of the candidate gene GLABROUS1. Mol. Biol. Evol. 18, 1754-1763. doi:10.1093/oxfordjournals.molbev.a003963
19. Ishii, T., and Araki, M. (2016). Consumer acceptance of food crops developed by genome editing. Plant Cell Rep. 35, 1507-1518. doi:10.1007/s00299-016-1974-2
20. Jia, L., Clegg, M. T., and Jiang, T. (2004). Evolutionary dynamics of the DNA-binding domains in putative R2R3-MYB genes identified from rice subspecies indica and japonica genomes. Plant Physiol. 134, 575-585. doi:10.1104/pp.103.027201
21. Jiang, W., Yang, B., and Weeks, D. P. (2014). Efficient CRISPR/Cas9-mediated gene editing in Arabidopsis thaliana and inheritance of modified genes in the T2 and T3 generations. PLoS ONE 9:e99225. doi:10.1371/journal.pone.0099225
22. Jinek, M., Chylinski, K., Fonfara, I., Hauer, M., Doudna, J. A., and Charpentier, E. (2012). A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337, 816-821. doi:10.1126/science.1225829
23. Kalve, S., De Vos, D., and Beemster, G. T. (2014). Leaf development: a cellular perspective. Front. Plant Sci. 5:362. doi:10.3389/fpls.2014.00362
24. Koornneef, M., Dellaert, L. W., and Van Der Veen, J. H. (1982). EMS-and radiation-induced mutation frequencies at individual loci in Arabidopsis thaliana (L.) Heynh. Mutat. Res. 93, 109-123. doi:10.1016/0027-5107(82)90129-4
25. Larkin, J. C., Oppenheimer, D. G., Lloyd, A. M., Paparozzi, E. T., and Marks, M. D. (1994). Roles of the GLABROUS1 and TRANSPARENT TESTA GLABRA Genes in Arabidopsis trichome development. Plant Cell 6, 1065-1076. doi:10.2307/3869885
26. Larkin, J. C., Oppenheimer, D. G., Pollock, S., and Marks, M. D. (1993). Arabidopsis GLABROUS1 gene requires downstream sequences for function. Plant Cell 5, 1739-1748. doi:10.1105/tpc.5.12.1739
27. Larkin, J. C., Young, N., Prigge, M., and Marks, M. D. (1996). The control of trichome spacing and number in Arabidopsis. Development 122, 997-1005.
28. Lea, P. J., Joy, K. W., Ramos, J. L., and Guerrero, M. G. (1984). The action of 2-amino-4-(methylphosphinyl)-butanoic acid (phosphinothricin) and its 2-oxo-derivative on the metabolism of cyanobacteria and higher-plants. Phytochemistry 23, 1-6. doi:10.1016/0031-9422(84)83066-6
29. Li, J., Yuan, Y., Lu, Z., Yang, L., Gao, R., Lu, J., et al. (2012). Glabrous rice 1, encoding a homeodomain protein, regulates trichome development in rice. Rice (N Y) 5, 32. doi:10.1186/1939-8433-5-32
30. Li, K., Wang, G., Andersen, T., Zhou, P., and Pu, W. T. (2014). Optimization of genome engineering approaches with the CRISPR/Cas9 system. PLoS ONE 9:e105779. doi:10.1371/journal.pone.0105779
31. Mao, Y., Zhang, H., Xu, N., Zhang, B., Gou, F., and Zhu, J. K. (2013). Application of the CRISPR-Cas system for efficient genome engineering in plants. Mol Plant 6, 2008-2011. doi:10.1093/mp/sst121
32. Marks, M. D. (1994). Plant development. The making of a plant hair. Curr. Biol. 4, 621-623. doi:10.1016/S0960-9822(00)00136-6
33. Miki, B., and McHugh, S. (2004). Selectable marker genes in transgenic plants: applications, alternatives and biosafety. J. Biotechnol. 107, 193-232. doi:10.1016/j.jbiotec.2003.10.011
34. Mullner, H., Eckes, P., and Donn, G. (1993). Engineering crop resistance to the naturally-occurring glutamine-synthetase inhibitor phosphinothricin. ACS Symp. Ser. 524, 38-47. doi:10.1021/bk-1993-0524.ch003
35. Oppenheimer, D. G., Herman, P. L., Sivakumaran, S., Esch, J., and Marks, M. D. (1991). A myb gene required for leaf trichome differentiation in Arabidopsis is expressed in stipules. Cell 67, 483-493. doi:10.1016/0092-8674(91)90523-2
36. Pattanaik, S., Patra, B., Singh, S. K., and Yuan, L. (2014). An overview of the gene regulatory network controlling trichome development in the model plant, Arabidopsis. Front. Plant Sci. 5:259. doi:10.3389/fpls.2014.00259
37. Puchta, H., and Fauser, F. (2014). Synthetic nucleases for genome engineering in plants: prospects for a bright future. Plant J. 78, 727-741. doi:10.1111/tpj.12338
38. Ran, F. A., Hsu, P. D., Wright, J., Agarwala, V., Scott, D. A., and Zhang, F. (2013). Genome engineering using the CRISPR-Cas9 system. Nat. Protoc. 8, 2281-2308. doi:10.1038/nprot.2013.143
39. Salomon, S., and Puchta, H. (1998). Capture of genomic and T-DNA sequences during double-strand break repair in somatic plant cells. EMBO J. 17,6086-6095. doi:10.1093/emboj/17.20.6086
40. Sauer, H., Wild, A., and Ruhle, W. (1987). The effect of phosphinothricin (glufosinate) on photosynthesis.2. The causes of inhibition of photosynthesis. Z. Naturforsch. 42, 270-278. doi:10.1007/BF00032644
41. Semenova, E., Jore, M. M., Datsenko, K. A., Semenova, A., Westra, E. R., Wanner, B., et al. (2011). Interference by clustered regularly interspaced short palindromic repeat (CRISPR) RNA is governed by a seed sequence. Proc. Natl. Acad. Sci. U.S.A. 108, 10098-10103. doi:10.1073/pnas.1104144108
42. Sessions, A., Burke, E., Presting, G., Aux, G., Mcelver, J., Patton, D., et al. (2002). A high-throughput Arabidopsis reverse genetics system. Plant Cell 14,2985-2994. doi:10.1105/tpc.004630
43. Stadler, R., Wright, K. M., Lauterbach, C., Amon, G., Gahrtz, M., Feuerstein, A., et al. (2005). Expression of GFP-fusions in Arabidopsis companion cells reveals non-specific protein trafficking into sieve elements and identifies a novel post-phloem domain in roots. Plant J. 41, 319-331. doi:10.1111/j.1365-313X.2004.02298.x
44. Tachibana, K., Watanabe, T., Sekizawa, Y., and Takematsu, T. (1986). Action mechanism of bialaphos.2. Accumulation of ammonia in plants treated with bialaphos. J. Pestic. Sci. 11, 33-37. doi:10.1584/jpestics.11.33
45. Thompson, C. J., Movva, N. R., Tizard, R., Crameri, R., Davies, J. E., Lauwereys, M., et al. (1987). Characterization of the herbicide-resistance gene bar from Streptomyces-hygroscopicus. Embo J. 6, 2519-2523.
46. Wang, Y., Cheng, X., Shan, Q., Zhang, Y., Liu, J., Gao, C., et al. (2014). Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nat. Biotechnol. 32, 947-951. doi:10.1038/nbt.2969
47. Weigel, D., and Glazebrook, J. (2009). Quick miniprep for plant DNA isolation. Cold Spring Harb. Protoc. 2009:dbrot5179. doi:10.1101/pdb.prot5179
48. Wild, A., Sauer, H., and Ruhle, W. (1987). The effect of phosphinothricin (glufosinate) on photosynthesis.1. Inhibition of photosynthesis and accumulation of ammonia. Z. Naturforsch. 42, 263-269. doi:10.1007/BF00032644
49. Wolt, J. D., Wang, K., and Yang, B. (2016). The regulatory status of genome-edited crops. Plant Biotechnol. J. 14, 510-518. doi:10.1111/pbi.12444
50. Woo, J. W., Kim, J., Kwon, S. I., Corvalan, C., Cho, S. W., Kim, H., et al. (2015). DNA-free genome editing in plants with preassembled CRISPR-Cas9 ribonucleoproteins. Nat. Biotechnol. 33, 1162-1164. doi:10.1038/nbt.3389
51. Xu, R. F., Li, H., Qin, R. Y., Li, J., Qiu, C. H., Yang, Y. C., et al. (2015). Generation of inheritable and “transgene clean” targeted genome-modified rice in later generations using the CRISPR/Cas9 system. Sci. Rep. 5:11491. doi:10.1038/srep11491
52. Yang, C., Li, H., Zhang, J., Luo, Z., Gong, P., Zhang, C., et al. (2011). A regulatory gene induces trichome formation and embryo lethality in tomato. Proc. Natl. Acad. Sci. U.S.A. 108, 11836-11841. doi:10.1073/pnas.1100532108
53. Yang, C., and Ye, Z. (2013). Trichomes as models for studying plant cell differentiation. Cell Mol. Life. Sci. 70, 1937-1948. doi:10.1007/s00018-012-1147-6
54. Yoshimi, K., Kaneko, T., Voigt, B., and Mashimo, T. (2014). Allele-specific genome editing and correction of disease-associated phenotypes in rats using the CRISPR-Cas platform. Nat. Commun. 5:4240. doi:10.1038/ncomms5240
55. Zhang, Y., Liang, Z., Zong, Y., Wang, Y., Liu, J., Chen, K., et al. (2016). Efficient and transgene-free genome editing in wheat through transient expression of CRISPR/Cas9 DNA or RNA. Nat. Commun. 7:12617. doi:10.1038/ncomms12617