Generation of chromosomal deletions in dicotyledonous plants employing a user-friendly genome editing toolkit

Plant Journal

Volumn 89, Issue 1, 2017, Pages 155-168

  Ordon, Jana ^a   Gantner, Johannes ^a   Kemna, Jan ^a   Schwalgun, Lennart ^a   Reschke, Maik ^a,b   Streubel, Jana ^a,b   Boch, Jens ^a,b   Stuttmann, Johannes ^a  

^a MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^b LEIBNIZ UNIVERSITY HANNOVER   (Germany)

Author keywords

Arabidopsis thaliana; chromosomal deletion; CRISPR Cas; EDS1; Nicotiana benthamiana; plant immunity; technical advance

Indexed keywords

GENES; GROWTH KINETICS; NUCLEIC ACIDS; POPULATION STATISTICS;

ARABIDOPSIS THALIANA; CHROMOSOMAL DELETIONS; CRISPR/CAS; EDS1; NICOTIANA BENTHAMIANA; PLANT IMMUNITIES; TECHNICAL ADVANCES;

PLANTS (BOTANY);

ALLELE; ARABIDOPSIS; BIOLOGICAL MODEL; CHROMOSOME ABERRATION; CRISPR CAS SYSTEM; GENE EDITING; GENETIC POLYMORPHISM; GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; PHENOTYPE; PLANT CHROMOSOME; PLANT GENOME; PROCEDURES; TOBACCO; TRANSGENIC PLANT;

ALLELES; ARABIDOPSIS; BASE SEQUENCE; CHROMOSOME ABERRATIONS; CHROMOSOMES, PLANT; CRISPR-CAS SYSTEMS; GENE EDITING; GENOME, PLANT; MODELS, GENETIC; MUTATION; PHENOTYPE; PLANTS, GENETICALLY MODIFIED; POLYMORPHISM, GENETIC; TOBACCO;

EID: 85003676665     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.13319     Document Type: Article

References (65)

1. Alcazar, R., Garcia, A.V., Parker, J.E. and Reymond, M. (2009) Incremental steps toward incompatibility revealed by Arabidopsis epistatic interactions modulating salicylic acid pathway activation. Proc. Natl Acad. Sci. USA 106, 334–339.
2. Alcazar, R., Garcia, A.V., Kronholm, I., de Meaux, J., Koornneef, M., Parker, J.E. and Reymond, M. (2010) Natural variation at Strubbelig Receptor Kinase 3 drives immune-triggered incompatibilities between Arabidopsis thaliana accessions. Nat. Genet. 42, 1135–1139.
3. Bartsch, M., Gobbato, E., Bednarek, P., Debey, S., Schultze, J.L., Bautor, J. and Parker, J.E. (2006) Salicylic acid-independent ENHANCED DISEASE SUSCEPTIBILITY1 signaling in Arabidopsis immunity and cell death is regulated by the monooxygenase FMO1 and the Nudix hydrolase NUDT7. Plant Cell, 18, 1038–1051.
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.
5. Belhaj, K., Chaparro-Garcia, A., Kamoun, S., Patron, N.J. and Nekrasov, V. (2015) Editing plant genomes with CRISPR/Cas9. Curr. Opin. Biotechnol. 32, 76–84.
6. Boch, J. and Bonas, U. (2010) Xanthomonas AvrBs3 family-type III effectors: discovery and function. Annu. Rev. Phytopathol. 48, 419–436.
7. Boch, J., Scholze, H., Schornack, S., Landgraf, A., Hahn, S., Kay, S., Lahaye, T., Nickstadt, A. and Bonas, U. (2009) Breaking the code of DNA binding specificity of TAL-type III effectors. Science (New York, NY), 326, 1509–1512.
8. Bortesi, L. and Fischer, R. (2015) The CRISPR/Cas9 system for plant genome editing and beyond. Biotechnol. Adv. 33, 41–52.
9. Botella, M.A., Parker, J.E., Frost, L.N., Bittner-Eddy, P.D., Beynon, J.L., Daniels, M.J., Holub, E.B. and Jones, J.D. (1998) Three genes of the Arabidopsis RPP1 complex resistance locus recognize distinct Peronospora parasitica avirulence determinants. Plant Cell, 10, 1847–1860.
10. Brooks, C., Nekrasov, V., Lippman, Z.B. and Van Eck, J. (2014) Efficient gene editing in tomato in the first generation using the clustered regularly interspaced short palindromic repeats/CRISPR-associated9 system. Plant Physiol. 166, 1292–1297.
11. Canver, M.C., Bauer, D.E., Dass, A., Yien, Y.Y., Chung, J., Masuda, T., Maeda, T., Paw, B.H. and Orkin, S.H. (2014) Characterization of genomic deletion efficiency mediated by clustered regularly interspaced palindromic repeats (CRISPR)/Cas9 nuclease system in mammalian cells. J. Biol. Chem. 289, 21312–21324.
12. Chae, E., Bomblies, K., Kim, S.T. et al. (2014) Species-wide genetic incompatibility analysis identifies immune genes as hot spots of deleterious epistasis. Cell, 159, 1341–1351.
13. Christian, M., Cermak, T., Doyle, E.L., Schmidt, C., Zhang, F., Hummel, A., Bogdanove, A.J. and Voytas, D.F. (2010) Targeting DNA double-strand breaks with TAL effector nucleases. Genetics, 186, 757–761.
14. Christian, M., Qi, Y., Zhang, Y. and Voytas, D.F. (2013) Targeted mutagenesis of Arabidopsis thaliana using engineered TAL effector nucleases. G3: Genes - Genomes - Genetics 3, 1697–1705.
15. Clasen, B.M., Stoddard, T.J., Luo, S. et al. (2016) Improving cold storage and processing traits in potato through targeted gene knockout. Plant Biotechnol. J. 14, 169–176.
16. Doench, J.G., Hartenian, E., Graham, D.B., Tothova, Z., Hegde, M., Smith, I., Sullender, M., Ebert, B.L., Xavier, R.J. and Root, D.E. (2014) Rational design of highly active sgRNAs for CRISPR-Cas9-mediated gene inactivation. Nat. Biotechnol. 32, 1262–1267.
17. Doench, J.G., Fusi, N., Sullender, M. et al. (2016) Optimized sgRNA design to maximize activity and minimize off-target effects of CRISPR-Cas9. Nat. Biotechnol. 34, 184–191.
18. Doudna, J.A. and Charpentier, E. (2014) Genome editing. The new frontier of genome engineering with CRISPR-Cas9. Science (New York, NY), 346, 1258096.
19. Engler, C., Youles, M., Gruetzner, R., Ehnert, T.M., Werner, S., Jones, J.D., Patron, N.J. and Marillonnet, S. (2014) A golden gate modular cloning toolbox for plants. ACS Synth. Biol. 3, 839–843.
20. 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.
21. Feng, Z., Zhang, B., Ding, W. et al. (2013) Efficient genome editing in plants using a CRISPR/Cas system. Cell Res. 23, 1229–1232.
22. Feys, B.J., Moisan, L.J., Newman, M.A. and Parker, J.E. (2001) Direct interaction between the Arabidopsis disease resistance signaling proteins, EDS1 and PAD4. EMBO J. 20, 5400–5411.
23. Feys, B.J., Wiermer, M., Bhat, R.A., Moisan, L.J., Medina-Escobar, N., Neu, C., Cabral, A. and Parker, J.E. (2005) Arabidopsis SENESCENCE-ASSOCIATED GENE101 stabilizes and signals within an ENHANCED DISEASE SUSCEPTIBILITY1 complex in plant innate immunity. Plant Cell, 17, 2601–2613.
24. Fu, Y., Foden, J.A., Khayter, C., Maeder, M.L., Reyon, D., Joung, J.K. and Sander, J.D. (2013) High-frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells. Nat. Biotechnol. 31, 822–826.
25. Gao, Y. and Zhao, Y. (2014) Self-processing of ribozyme-flanked RNAs into guide RNAs in vitro and in vivo for CRISPR-mediated genome editing. J. Integr. Plant Biol. 56, 343–349.
26. Gao, Y., Zhang, Y., Zhang, D., Dai, X., Estelle, M. and Zhao, Y. (2015) Auxin binding protein 1 (ABP1) is not required for either auxin signaling or Arabidopsis development. Proc. Natl Acad. Sci. USA 112, 2275–2280.
27. Gao, X., Chen, J., Dai, X., Zhang, D. and Zhao, Y. (2016) An effective strategy for reliably isolating heritable and Cas9-free Arabidopsis mutants generated by CRISPR/Cas9-mediated genome editing. Plant Physiol. 171, 1794–1800.
28. Geissler, R., Scholze, H., Hahn, S., Streubel, J., Bonas, U., Behrens, S.E. and Boch, J. (2011) Transcriptional activators of human genes with programmable DNA-specificity. PLoS ONE, 6, e19509.
29. He, Z., Proudfoot, C., Mileham, A.J., McLaren, D.G., Whitelaw, C.B. and Lillico, S.G. (2015) Highly efficient targeted chromosome deletions using CRISPR/Cas9. Biotechnol. Bioeng. 112, 1060–1064.
30. Hsu, P.D., Scott, D.A., Weinstein, J.A. et al. (2013) DNA targeting specificity of RNA-guided Cas9 nucleases. Nat. Biotechnol. 31, 827–832.
31. Hyun, Y., Kim, J., Cho, S.W., Choi, Y., Kim, J.S. and Coupland, G. (2015) Site-directed mutagenesis in Arabidopsis thaliana using dividing tissue-targeted RGEN of the CRISPR/Cas system to generate heritable null alleles. Planta, 241, 271–284.
32. Jiang, W., Brueggeman, A.J., Horken, K.M., Plucinak, T.M. and Weeks, D.P. (2014a) Successful transient expression of Cas9 and single guide RNA genes in Chlamydomonas reinhardtii. Eukaryot. Cell, 13, 1465–1469.
33. Jiang, W., Yang, B. and Weeks, D.P. (2014b) Efficient CRISPR/Cas9-mediated gene editing in Arabidopsis thaliana and inheritance of modified genes in the T2 and T3 generations. PLoS ONE, 9, e99225.
34. 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 (New York, NY), 337, 816–821.
35. Karimi, M., Inze, D. and Depicker, A. (2002) GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7, 193–195.
36. Kim, Y.G., Cha, J. and Chandrasegaran, S. (1996) Hybrid restriction enzymes: zinc finger fusions to Fok I cleavage domain. Proc. Natl Acad. Sci. USA 93, 1156–1160.
37. Lei, Y., Lu, L., Liu, H.Y., Li, S., Xing, F. and Chen, L.L. (2014) CRISPR-P: a web tool for synthetic single-guide RNA design of CRISPR-system in plants. Mol. Plant 7, 1494–1496.
38. Liang, J., Chao, R., Abil, Z., Bao, Z. and Zhao, H. (2014) FairyTALE: a high-throughput TAL effector synthesis platform. ACS Synth. Biol. 3, 67–73.
39. Lowder, L.G., Zhang, D., Baltes, N.J., Paul, J.W. 3rd, Tang, X., Zheng, X., Voytas, D.F., Hsieh, T.F., Zhang, Y. and Qi, Y. (2015) A CRISPR/Cas9 toolbox for multiplexed plant genome editing and transcriptional regulation. Plant Physiol. 169, 971–985.
40. Ma, X., Zhang, Q., Zhu, Q. et al. (2015) A robust CRISPR/Cas9 system for convenient, high-efficiency multiplex genome editing in monocot and dicot plants. Mol. Plant 8, 1274–1284.
41. Mao, Y., Zhang, Z., Feng, Z., Wei, P., Zhang, H., Botella, J.R. and Zhu, J.K. (2016) Development of germ-line-specific CRISPR-Cas9 systems to improve the production of heritable gene modifications in Arabidopsis. Plant Biotechnol. J. 14, 519–532.
42. Nakagawa, T., Kurose, T., Hino, T., Tanaka, K., Kawamukai, M., Niwa, Y., Toyooka, K., Matsuoka, K., Jinbo, T. and Kimura, T. (2007) Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation. J. Biosci. Bioeng. 104, 34–41.
43. Nielsen, S., Yuzenkova, Y. and Zenkin, N. (2013) Mechanism of eukaryotic RNA polymerase III transcription termination. Science (New York, NY) 340, 1577–1580.
44. Nissim, L., Perli, S.D., Fridkin, A., Perez-Pinera, P. and Lu, T.K. (2014) Multiplexed and programmable regulation of gene networks with an integrated RNA and CRISPR/Cas toolkit in human cells. Mol. Cell 54, 698–710.
45. Rehmany, A.P., Gordon, A., Rose, L.E., Allen, R.L., Armstrong, M.R., Whisson, S.C., Kamoun, S., Tyler, B.M., Birch, P.R.J. and Beynon, J.L. (2005) Differential recognition of highly divergent downy mildew avirulence gene alleles by RPP1 resistance genes from two Arabidopsis lines. Plant Cell, 17, 1839–1850.
46. Richter, A., Streubel, J., Blucher, C., Szurek, B., Reschke, M., Grau, J. and Boch, J. (2014) A TAL effector repeat architecture for frameshift binding. Nat. Commun. 5, 3447.
47. Schiml, S., Fauser, F. and Puchta, H. (2014) The CRISPR/Cas system can be used as nuclease for in planta gene targeting and as paired nickases for directed mutagenesis in Arabidopsis resulting in heritable progeny. Plant J. 80, 1139–1150.
48. Schulze, S., Kay, S., Buttner, D. et al. (2012) Analysis of new type III effectors from Xanthomonas uncovers XopB and XopS as suppressors of plant immunity. New Phytol. 195, 894–911.
49. Shimada, T.L., Shimada, T. and Hara-Nishimura, I. (2010) A rapid and non-destructive screenable marker, FAST, for identifying transformed seeds of Arabidopsis thaliana. Plant J. 61, 519–528.
50. Shirzadian-Khorramabad, R., Jing, H.C., Everts, G.E., Schippers, J.H., Hille, J. and Dijkwel, P.P. (2010) A mutation in the cytosolic O-acetylserine (thiol) lyase induces a genome-dependent early leaf death phenotype in Arabidopsis. BMC Plant Biol. 10, 80.
51. Sinapidou, E., Williams, K., Nott, L., Bahkt, S., Tor, M., Crute, I., Bittner-Eddy, P. and Beynon, J. (2004) Two TIR:NB:LRR genes are required to specify resistance to Peronospora parasitica isolate Cala2 in Arabidopsis. Plant J. 38, 898–909.
52. Sosso, D., Luo, D., Li, Q.B. et al. (2015) Seed filling in domesticated maize and rice depends on SWEET-mediated hexose transport. Nat. Genet. 47, 1489–1493.
53. Stuttmann, J., Peine, N., Garcia, A.V. et al. (2016) Arabidopsis thaliana DM2h (R8) within the Landsberg RPP1-like resistance locus underlies three different cases of EDS1-conditioned autoimmunity. PLoS Genet. 12, e1005990.
54. Tahir, J., Watanabe, M., Jing, H.C., Hunter, D.A., Tohge, T., Nunes-Nesi, A., Brotman, Y., Fernie, A.R., Hoefgen, R. and Dijkwel, P.P. (2013) Activation of R-mediated innate immunity and disease susceptibility is affected by mutations in a cytosolic O-acetylserine (thiol) lyase in Arabidopsis. Plant J. 73, 118–130.
55. Townsend, J.A., Wright, D.A., Winfrey, R.J., Fu, F., Maeder, M.L., Joung, J.K. and Voytas, D.F. (2009) High-frequency modification of plant genes using engineered zinc-finger nucleases. Nature, 459, 442–445.
56. Wagner, S., Stuttmann, J., Rietz, S., Guerois, R., Brunstein, E., Bautor, J., Niefind, K. and Parker, J.E. (2013) Structural basis for signaling by exclusive EDS1 heteromeric complexes with SAG101 or PAD4 in plant innate immunity. Cell Host Microbe, 14, 619–630.
57. Wang, Z.P., Xing, H.L., Dong, L., Zhang, H.Y., Han, C.Y., Wang, X.C. and Chen, Q.J. (2015) Egg cell-specific promoter-controlled CRISPR/Cas9 efficiently generates homozygous mutants for multiple target genes in Arabidopsis in a single generation. Genome Biol. 16, 144.
58. Weber, E., Engler, C., Gruetzner, R., Werner, S. and Marillonnet, S. (2011a) A modular cloning system for standardized assembly of multigene constructs. PLoS ONE, 6, e16765.
59. Weber, E., Gruetzner, R., Werner, S., Engler, C. and Marillonnet, S. (2011b) Assembly of designer TAL effectors by Golden Gate cloning. PLoS ONE, 6, e19722.
60. Wiedenheft, B., Sternberg, S.H. and Doudna, J.A. (2012) RNA-guided genetic silencing systems in bacteria and archaea. Nature, 482, 331–338.
61. Xiao, A., Wang, Z., Hu, Y. et al. (2013) Chromosomal deletions and inversions mediated by TALENs and CRISPR/Cas in zebrafish. Nucleic Acids Res. 41, e141.
62. Xiao, A., Cheng, Z., Kong, L., Zhu, Z., Lin, S., Gao, G. and Zhang, B. (2014) CasOT: a genome-wide Cas9/gRNA off-target searching tool. Bioinformatics, 30, 1180–1182.
63. Xie, K., Minkenberg, B. and Yang, Y. (2015) Boosting CRISPR/Cas9 multiplex editing capability with the endogenous tRNA-processing system. Proc. Natl Acad. Sci. USA 112, 3570–3575.
64. Zhang, Z., Mao, Y., Ha, S., Liu, W., Botella, J.R. and Zhu, J.K. (2015) A multiplex CRISPR/Cas9 platform for fast and efficient editing of multiple genes in Arabidopsis. Plant Cell Rep. 35, 1519–1533.
65. Zhu, S., Jeong, R.D., Venugopal, S.C., Lapchyk, L., Navarre, D., Kachroo, A. and Kachroo, P. (2011) SAG101 forms a ternary complex with EDS1 and PAD4 and is required for resistance signaling against turnip crinkle virus. PLoS Pathog. 7, e1002318.