Induction of targeted, heritable mutations in barley and Brassica oleracea using RNA-guided Cas9 nuclease

Genome Biology

Volumn 16, Issue 1, 2015, Pages

  Lawrenson, Tom ^a   Shorinola, Oluwaseyi ^a   Stacey, Nicola ^a   Li, Chengdao ^b   Østergaard, Lars ^a   Patron, Nicola ^c   Uauy, Cristobal ^a   Harwood, Wendy ^a  

^a JOHN INNES CENTRE   (United Kingdom)

^b MURDOCH UNIVERSITY   (Australia)

^c SAINSBURY LABORATORY   (United Kingdom)

Author keywords

Barley; Brassica; Breeding; CRISPR Cas9; Crops; GA4; Genome editing; Mutations; Off target; PM19

Indexed keywords

DNA; NUCLEASE; PROTEIN CAS9; RNA; UNCLASSIFIED DRUG; GUIDE RNA;

ARTICLE; BARLEY; BASE MISPAIRING; BRASSICA OLERACEA; CAS9 GENE; CONTROLLED STUDY; DNA MODIFICATION; GENE INDUCTION; GENE LOCUS; GENE MUTATION; GENE SEQUENCE; GENE TARGETING; HEREDITY; NONHUMAN; PHENOTYPE; PLANT GENE; RNA EDITING; TRANSGENIC PLANT; BRASSICA; CRISPR CAS SYSTEM; GENETICS; HORDEUM; MUTATION; PLANT GENOME;

BRASSICA; CRISPR-CAS SYSTEMS; GENE TARGETING; GENOME, PLANT; HORDEUM; MUTATION; PHENOTYPE; RNA EDITING; RNA, GUIDE;

EID: 84948761978     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/s13059-015-0826-7     Document Type: Article

References (50)

1. Voytas DF, Gao C. Precision genome engineering and agriculture: opportunities and regulatory challenges. PLoS Biol. 2014;12:e1001877.
2. Hsu Patrick D, Lander Eric S, Zhang F. Development and applications of CRISPR-Cas9 for genome engineering. Cell. 2014;157:1262-78.
3. Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, et al. Multiplex genome engineering using CRISPR/Cas systems. Science. 2013;339:819-23.
4. Mali P, Yang L, Esvelt KM, Aach J, Guell M, DiCarlo JE, et al. RNA-guided human genome engineering via Cas9. Science. 2013;339:823-6.
5. Belhaj K, Chaparro-Garcia A, Kamoun S, Patron NJ, Nekrasov V. Editing plant genomes with CRISPR/Cas9. Curr Opin Biotechnol. 2015;32:76-84.
6. Li J-F, Norville JE, Aach J, McCormack M, Zhang D, Bush J, et al. Multiplex and homologous recombination-mediated genome editing in Arabidopsis and Nicotiana benthamiana using guide RNA and Cas9. Nat Biotech. 2013;31:688-91.
7. Nekrasov V, Staskawicz B, Weigel D, Jones JDG, Kamoun S. Targeted mutagenesis in the model plant Nicotiana benthamiana using Cas9 RNA-guided endonuclease. Nat Biotech. 2013;31:691-3.
8. Shan Q, Wang Y, Li J, Zhang Y, Chen K, Liang Z, et al. Targeted genome modification of crop plants using a CRISPR-Cas system. Nat Biotech. 2013;31:686-8.
9. Feng Z, Mao Y, Xu N, Zhang B, Wei P, Yang D-L, et al. Multigeneration analysis reveals the inheritance, specificity, and patterns of CRISPR/Cas-induced gene modifications in Arabidopsis. Proc Natl Acad Sci. 2014;111:4632-7.
10. Zhang H, Zhang J, Wei P, Zhang B, Gou F, Feng Z, et al. The CRISPR/Cas9 system produces specific and homozygous targeted gene editing in rice in one generation. Plant Biotechnol J. 2014;12:797-807.
11. Zhou H, Liu B, Weeks DP, Spalding MH, Yang B. Large chromosomal deletions and heritable small genetic changes induced by CRISPR/Cas9 in rice. Nucleic Acids Res. 2014;42:10903-14.
12. Wang Y, Cheng X, Shan Q, Zhang Y, Liu J, Gao C, et al. Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nat Biotech. 2014;32:947-51.
13. Arnaud N, Girin T, Sorefan K, Fuentes S, Wood TA, Lawrenson T, et al. Gibberellins control fruit patterning in Arabidopsis thaliana. Genes Dev. 2010;24:2127-32.
14. Chiang H-H, Hwang I, Goodman HM. Isolation of the Arabidopsis GA4 locus. Plant Cell. 1995;7:195-201.
15. Ranford JC, Bryce JH, Morris PC. PM19, a barley (Hordeum vulgare L.) gene encoding a putative plasma membrane protein, is expressed during embryo development and dormancy. J Exp Bot. 2002;53:147-8.
16. Barrero JM, Cavanagh C, Verbyla KL, Tibbits JFG, Verbyla AP, Huang BE, et al. Transcriptomic analysis of wheat near-isogenic lines identifies PM19-A1 and A2 as candidates for a major dormancy QTL. Genome Biol. 2015;16:93.
17. Bortesi L, Fischer R. The CRISPR/Cas9 system for plant genome editing and beyond. Biotechnol Adv. 2015;33:41-52.
18. Jiang W, Zhou H, Bi H, Fromm M, Yang B, Weeks DP. Demonstration of CRISPR/Cas9/sgRNA-mediated targeted gene modification in Arabidopsis, tobacco, sorghum and rice. Nucleic Acids Res. 2013;41(20):e188.
19. Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E. A programmable dual-RNA-guided DNA Endonuclease in adaptive bacterial immunity. Science. 2012;337:816-21.
20. Hartung F, Schiemann J. Precise plant breeding using new genome editing techniques: opportunities, safety and regulation in the EU. Plant J. 2014;78:742-52.
21. Xu R-F, Li H, Qin R-Y, Li J, Qiu C-H, Yang Y-C, et al. Generation of inheritable and "transgene clean" targeted genome-modified rice in later generations using the CRISPR/Cas9 system. Sci Rep. 2015;5:11491.
22. Sparrow P, Dale P, Irwin J. Brassica oleracea. In: Wang K, editor. Agrobacterium Protocols, vol. 343. New York: Humana Press; 2006. p. 417-26.
23. Mitchum MG, Yamaguchi S, Hanada A, Kuwahara A, Yoshioka Y, Kato T, et al. Distinct and overlapping roles of two gibberellin 3-oxidases in Arabidopsis development. Plant J. 2006;45:804-18.
24. Brooks C, Nekrasov V, Lippman ZB, Van Eck J. Efficient gene editing in tomato in the first generation using the clustered regularly interspaced short palindromic repeats/CRISPR-associated9 system. Plant Physiol. 2014;166:1292-7.
25. Mikami M, Toki S, Endo M. Parameters affecting frequency of CRISPR/Cas9 mediated targeted mutagenesis in rice. Plant Cell Rep. 2015;34:1807-15.
26. Endo M, Mikami M, Toki S. Multi-gene knockout utilizing off-target mutations of the CRISPR/Cas9 system in rice. Plant Cell Physiol. 2015;56:41-7.
27. Jiang W, Bikard D, Cox D, Zhang F, Marraffini LA. RNA-guided editing of bacterial genomes using CRISPR-Cas systems. Nat Biotech. 2013;31:233-9.
28. Cradick TJ, Fine EJ, Antico CJ, Bao G. CRISPR/Cas9 systems targeting β-globin and CCR5 genes have substantial off-target activity. Nucleic Acids Res. 2013;41:9584-92.
29. Lin Y, Cradick TJ, Brown MT, Deshmukh H, Ranjan P, Sarode N, et al. CRISPR/Cas9 systems have off-target activity with insertions or deletions between target DNA and guide RNA sequences. Nucleic Acids Res. 2014;42:7473-85.
30. Fu Y, Sander JD, Reyon D, Cascio VM, Joung JK. Improving CRISPR-Cas nuclease specificity using truncated guide RNAs. Nat Biotechnol. 2014;32:279-84.
31. Ran FA, Hsu Patrick D, Lin C-Y, Gootenberg Jonathan S, Konermann S, Trevino AE, et al. Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell. 2013;154:1380-9.
32. Shen B, Zhang W, Zhang J, Zhou J, Wang J, Chen L, et al. Efficient genome modification by CRISPR-Cas9 nickase with minimal off-target effects. Nat Meth. 2014;11:399-402.
33. Guilinger JP, Thompson DB, Liu DR. Fusion of catalytically inactive Cas9 to FokI nuclease improves the specificity of genome modification. Nat Biotech. 2014;32:577-82.
34. Tsai SQ, Wyvekens N, Khayter C, Foden JA, Thapar V, Reyon D, et al. Dimeric CRISPR RNA-guided FokI nucleases for highly specific genome editing. Nat Biotech. 2014;32:569-76.
35. Borrill P, Adamski N, Uauy C. Genomics as the key to unlocking the polyploid potential of wheat. New Phytol. 2015;208:1008-22.
36. Adams KL, Wendel JF. Polyploidy and genome evolution in plants. Curr Opin Plant Biol. 2005;8:135-41.
37. The International Wheat Genome Sequencing Consortium. A chromosome-based draft sequence of the hexaploid bread wheat (Triticum aestivum) genome. Science. 2014;345:1251788.
38. Girin T, Stephenson P, Goldsack CMP, Kempin SA, Perez A, Pires N, et al. Brassicaceae INDEHISCENT genes specify valve margin cell fate and repress replum formation. Plant J. 2010;63:329-38.
39. Spence J, Vercher Y, Gates P, Harris N. 'Pod shatter' in Arabidopsis thaliana, Brassica napus and B. juncea. J Microsc. 1996;181:195-203.
40. The Brassica Database. [ http://brassicadb.org/brad/blastPage.php ].
41. International Barley Sequencing Consortium Database [ http://webblast.ipk-gatersleben.de/barley/ ]
42. Weber E, Engler C, Gruetzner R, Werner S, Marillonnet S. A modular cloning system for standardized assembly of multigene constructs. PLoS One. 2011;6:e16765.
43. Engler C, Youles M, Gruetzner R, Ehnert T-M, Werner S, Jones JDG, et al. A golden gate modular cloning toolbox for plants. ACS Synthetic Biol. 2014;3:839-43.
44. Harwood W. A Protocol for High-Throughput Agrobacterium-Mediated Barley Transformation. In: Henry RJ, Furtado A, editors. Cereal Genomics, vol. 1099. New York: Humana Press; 2014. p. 251-60.
45. Hundleby PAC, Irwin J. Brassica oleracea and B. napus. In: Wang K, editor. Agrobacterium Protocols, vol. 1223. New York: Springer; 2015. p. 287-97.
46. Voytas DF. Plant genome engineering with sequence-specific nucleases. Annu Rev Plant Biol. 2013;64:327-50.
47. Edwards K, Johnstone C, Thompson C. A simple and rapid method for the preparation of plant genomic DNA for PCR analysis. Nucleic Acids Res. 1991;19:1349.
48. Smyth DR, Bowman JL, Meyerowitz EM. Early flower development in Arabidopsis. Plant Cell. 1990;2:755-67.
49. Østergaard L, Kempin SA, Bies D, Klee HJ, Yanofsky MF. Pod shatter-resistant Brassica fruit produced by ectopic expression of the FRUITFULL gene. Plant Biotechnol J. 2006;4:45-51.
50. Weng H, Pan A, Yang L, Zhang C, Liu Z, Zhang D. Estimating number of transgene copies in transgenic rapeseed by real-time PCR assay with HMG I/Y as an endogenous reference gene. Plant Mol Biol Rep. 2004;22:289-300.