Nucleases for genome editing in crops

Biocatalysis and Agricultural Biotechnology

Volumn 3, Issue 1, 2014, Pages 14-19

  Kathiria, Palak ^a   Eudes, François ^a  

^a AGRICULTURE AND AGRI FOOD CANADA   (Canada)

Author keywords

CRISPR Cas; Meganuclease; Plant genome engineering; TALENs; Zinc fingers

Indexed keywords

EID: 84894256343     PISSN: 18788181     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcab.2013.12.006     Document Type: Review

References (71)

1. Barrangou R., Fremaux C., Deveau H., Richards M., Boyaval P., Moineau S., Romero D.A., Horvath P. CRISPR provides acquired resistance against viruses in prokaryotes. Science 2007, 315:1709-1712.
2. Beerli R.R., Barbas C.F. Engineering polydactyl zinc-finger transcription factors. Nat. Biotechnol. 2002, 20:135-141.
3. Bhaya D., Davison M., Barrangou R. CRISPR-Cas systems in bacteria and archaea: versatile small RNAs for adaptive defense and regulation. Annu. Rev. Genet. 2011, 45:273-297.
4. Bibikova M., Beumer K., Trautman J.K., Carroll D. Enhancing gene targeting with designed zinc finger nucleases. Science 2003, 300:764.
5. Bitinaite J., Wah D.A., Aggarwal A.K., Schildkraut I. FokI dimerization is required for DNA cleavage. Proc. Natl. Acad. Sci. USA 1998, 95:10570-10575.
6. Boch J., Scholze H., Schornack S., Landgraf A., Hahn S., Kay S., Lahaye T., Nickstadt A., Bonas U. Breaking the code of DNA binding specificity of TAL-type III effectors. Science 2009, 326:1509-1512.
7. Bolotin A., Quinquis B., Sorokin A., Ehrlich S.D. Clustered regularly interspaced short palindrome repeats (CRISPRs) have spacers of extrachromosomal origin. Microbiology 2005, 151:2551-2561.
8. Briggs A.W., Rios X., Chari R., Yang L., Zhang F., Mali P., Church G.M. Iterative capped assembly: rapid and scalable synthesis of repeat-module DNA such as TAL effectors from individual monomers. Nucl. Acids Res. 2012, 40:e117.
9. Brouns S.J., Jore M.M., Lundgren M., Westra E.R., Slijkhuis R.J., Snijders A.P., Dickman M.J., Makarova K.S., Koonin E.V., van der Oost J. Small CRISPR RNAs guide antiviral defense in prokaryotes. Science 2008, 321:960-964.
10. Carte J., Wang R., Li H., Terns R.M., Terns M.P. Cas6 is an endoribonuclease that generates guide RNAs for invader defense in prokaryotes. Genes Dev. 2008, 22:3489-3496.
11. Cermak T., Doyle E.L., Christian M., Wang L., Zhang Y., Schmidt C., Baller J.A., Somia N.V., Bogdanove A.J., Voytas D.F. Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting. Nucl. Acids Res. 2011, 39:e82.
12. Chang N., Sun C., Gao L., Zhu D., Xu X., Zhu X., Xiong J.W., Xi J.J. Genome editing with RNA-guided Cas9 nuclease in zebrafish embryos. Cell Res. 2013, 23:465-472.
13. Chevalier B.S., Stoddard B.L. Homing endonucleases: structural and functional insight into the catalysts of intron/intein mobility. Nucl. Acids Res. 2001, 29:3757-3774.
14. Chugh A., Amundsen E., Eudes F. Translocation of cell-penetrating peptides and delivery of their cargoes in triticale microspores. Plant Cell Rep. 2009, 28:801-810.
15. Chugh A., Eudes F. Study of uptake of cell penetrating peptides and their cargoes in permeabilized wheat immature embryos. FEBS J. 2008, 275:2403-2414.
16. Colleaux L., D'Auriol L., Galibert F., Dujon B. Recognition and cleavage site of the intron-encoded omega transposase. Proc. Natl. Acad. Sci. USA 1988, 85:6022-6026.
17. Curtin S.J., Voytas D.F., Stupar R.M. Genome engineering of crops with designer nucleases. Plant Genome 2012, 5:42-50.
18. Curtin S.J., Zhang F., Sander J.D., Haun W.J., Starker C., Baltes N.J., Reyon D., Dahlborg E.J., Goodwin M.J., Coffman A.P., Dobbs D., Joung J.K., Voytas D.F., Stupar R.M. Targeted mutagenesis of duplicated genes in soybean with zinc-finger nucleases. Plant Physiol. 2011, 156:466-473.
19. Deng D., Yan C., Pan X., Mahfouz M., Wang J., Zhu J.-K., Shi Y., Yan N. Structural basis for sequence-specific recognition of DNA by TAL effectors. Science 2012, 335:720-723.
20. Desjarlais J.R., Berg J.M. Use of a zinc-finger consensus sequence framework and specificity rules to design specific DNA binding proteins. Proc. Natl. Acad. Sci. USA 1993, 90:2256-2260.
21. Deveau H., Garneau J.E., Moineau S. CRISPR/Cas system and its role in phage-bacteria interactions. Annu. Rev. Microbiol. 2010, 64:475-493.
22. Dhar M.K., Kaul S., Kour J. Towards the development of better crops by genetic transformation using engineered plant chromosomes. Plant Cell Rep. 2011, 30:799-806.
23. Elrod-Erickson M., Pabo C.O. Binding studies with mutants of Zif268. Contribution of individual side chains to binding affinity and specificity in the Zif268 zinc finger-DNA complex. J. Biol. Chem. 1999, 274:19281-19285.
24. Fajardo-Sanchez E., Stricher F., Pâques F., Isalan M., Serrano L. Computer design of obligate heterodimer meganucleases allows efficient cutting of custom DNA sequences. Nucl. Acids Res. 2008, 36:2163-2173.
25. Fu Y., Foden J.A., Khayter C., Maeder M.L., Reyon D., Joung J.K., Sander J.D. High-frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells. Nat. Biotechnol. 2013, 31:822-826.
26. Gabriel R., Lombardo A., Arens A., Miller J.C., Genovese P., Kaeppel C., Nowrouzi A., Bartholomae C.C., Wang J., Friedman G., Holmes M.C., Gregory P.D., Glimm H., Schmidt M., Naldini L., von Kalle C. An unbiased genome-wide analysis of zinc-finger nuclease specificity. Nat. Biotechnol. 2011, 29:816-823.
27. Gaj T., Gersbach C.A., Barbas C.F. ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. Trends Biotechnol. 2013, 31:397-405.
28. Gao H., Smith J., Yang M., Jones S., Djukanovic V., Nicholson M.G., West A., Bidney D., Falco S.C., Jantz D., Lyznik L.A. Heritable targeted mutagenesis in maize using a designed endonuclease. Plant J. 2010, 61:176-187.
29. Gimble F.S., Moure C.M., Posey K.L. Assessing the plasticity of DNA target site recognition of the PI-SceI homing endonuclease using a bacterial two-hybrid selection system. J. Mol. Biol. 2003, 334:993-1008.
30. Haber J.E. Mating-type genes and MAT switching in Saccharomyces cerevisiae. Genetics 2012, 191:33-64.
31. Hanin M., Paszkowski J. Plant genome modification by homologous recombination. Curr. Opin. Plant Biol. 2003, 6:157-162.
32. Ishino Y., Shinagawa H., Makino K., Amemura M., Nakata A. Nucleotide sequence of the iap gene, responsible for alkaline phosphatase isozyme conversion in Escherichia coli, and identification of the gene product. J. Bacteriol. 1987, 169:5429-5433.
33. Jacquier A., Dujon B. An intron-encoded protein is active in a gene conversion process that spreads an intron into a mitochondrial gene. Cell 1985, 41:383-394.
34. Jansen R., Embden J.D., Gaastra W., Schouls L.M. Identification of genes that are associated with DNA repeats in prokaryotes. Mol. Microbiol. 2002, 43:1565-1575.
35. Joung J.K., Sander J.D. TALENs: a widely applicable technology for targeted genome editing. Nat. Rev. Mol. Cell Biol. 2013, 14:49-55.
36. Kim Y.G., Cha J., Chandrasegaran S. Hybrid restriction enzymes: zinc finger fusions to Fok I cleavage domain. Proc. Natl. Acad. Sci. USA 1996, 93:1156-1160.
37. Kostriken R., Strathern J.N., Klar A.J., Hicks J.B., Heffron F. A site-specific endonuclease essential for mating-type switching in Saccharomyces cerevisiae. Cell 1983, 35:167-174.
38. Li T., Liu B., Spalding M.H., Weeks D.P., Yang B. High-efficiency TALEN-based gene editing produces disease-resistant rice. Nat. Biotechnol. 2012, 30:390-392.
39. Liu Q., Segal D.J., Ghiara J.B., Barbas C.F. Design of polydactyl zinc-finger proteins for unique addressing within complexgenomes. Proc. Natl. Acad. Sci. USA 1997, 94:5525-5530.
40. Maeder M.L., Thibodeau-Beganny S., Osiak A., Wright D.A., Anthony R.M., Eichtinger M., Jiang T., Foley J.E., Winfrey R.J., Townsend J.A., Unger-Wallace E., Sander J.D., Muller-Lerch F., Fu F., Pearlberg J., Gobel C., Dassie J.P., Pruett-Miller S.M., Porteus M.H., Sgroi D.C., Iafrate A.J., Dobbs D., McCray P.B., Cathomen T., Voytas D.F., Joung J.K. Rapid "open-source" engineering of customized zinc-finger nucleases for highly efficient gene modification. Mol. Cell 2008, 31:294-301.
41. Mak A.N.-S., Bradley P., Cernadas R.A., Bogdanove A.J., Stoddard B.L. The crystal structure of TAL effector PthXo1 bound to its DNA target. Science 2012, 335:716-719.
42. Maliga P., Bock R. Plastid biotechnology: food, fuel, and medicine for the 21st century. Plant Physiol. 2011, 155:1501-1510.
43. Marraffini L.A., Sontheimer E.J. CRISPR interference limits horizontal gene transfer in Staphylococci by targeting DNA. Science 2008, 322:1843-1845.
44. Miller J.C., Tan S., Qiao G., Barlow K.A., Wang J., Xia D.F., Meng X., Paschon D.E., Leung E., Hinkley S.J., Dulay G.P., Hua K.L., Ankoudinova I., Cost G.J., Urnov F.D., Zhang H.S., Holmes M.C., Zhang L., Gregory P.D., Rebar E.J. A TALE nuclease architecture for efficient genome editing. Nat. Biotechnol. 2011, 29:143-148.
45. Mojica F.J., Diez-Villasenor C., Garcia-Martinez J., Soria E. Intervening sequences of regularly spaced prokaryotic repeats derive from foreign genetic elements. J. Mol. Evol. 2005, 60:174-182.
46. Moscou M.J., Bogdanove A.J. A simple cipher governs DNA recognition by TAL effectors. Science 2009, 326:1501.
47. Munoz Bodnar A., Bernal A., Szurek B., Lopez C.E. Tell me a tale of TALEs. Mol. Biotechnol. 2013, 53:228-235.
48. Munoz I.G., Prieto J., Subramanian S., Coloma J., Redondo P., Villate M., Merino N., Marenchino M., D'Abramo M., Gervasio F.L., Grizot S., Daboussi F., Smith J., Chion-Sotinel I., Paques F., Duchateau P., Alibes A., Stricher F., Serrano L., Blanco F.J., Montoya G. Molecular basis of engineered meganuclease targeting of the endogenous human RAG1 locus. Nucl. Acids Res. 2011, 39:729-743.
49. Nickoloff J.A., Chen E.Y., Heffron F. A 24-base-pair DNA sequence from the MAT locus stimulates intergenic recombination in yeast. Proc. Natl. Acad. Sci. USA 1986, 83:7831-7835.
50. Paques F., Duchateau P. Meganucleases and DNA double-strand break-induced recombination: perspectives for gene therapy. Curr. Gene Ther. 2007, 7:49-66.
51. Parry M.A.J., Madgwick P.J., Bayon C., Tearall K., Hernandez-Lopez A., Baudo M., Rakszegi M., Hamada W., Al-Yassin A., Ouabbou H., Labhilili M., Phillips A.L. Mutation discovery for crop improvement. J. Exp. Bot. 2009, 60:2817-2825.
52. Podevin N., Davies H.V., Hartung F., Nogue F., Casacuberta J.M. Site-directed nucleases: a paradigm shift in predictable, knowledge-based plant breeding. Trends Biotechnol. 2013, 31:375-383.
53. Porteus M.H., Baltimore D. Chimeric nucleases stimulate gene targeting in human cells. Science 2003, 300:763.
54. Pourcel C., Salvignol G., Vergnaud G. CRISPR elements in Yersinia pestis acquire new repeats by preferential uptake of bacteriophage DNA, and provide additional tools for evolutionary studies. Microbiology 2005, 151:653-663.
55. Reyon D., Tsai S.Q., Khayter C., Foden J.A., Sander J.D., Joung J.K. FLASH assembly of TALENs for high-throughput genome editing. Nat. Biotechnol. 2012, 30:460-465.
56. Römer P., Hahn S., Jordan T., Strauß T., Bonas U., Lahaye T. Plant pathogen recognition mediated by promoter activation of the pepper Bs3 resistance gene. Science 2007, 318:645-648.
57. Sander J.D., Dahlborg E.J., Goodwin M.J., Cade L., Zhang F., Cifuentes D., Curtin S.J., Blackburn J.S., Thibodeau-Beganny S., Qi Y., Pierick C.J., Hoffman E., Maeder M.L., Khayter C., Reyon D., Dobbs D., Langenau D.M., Stupar R.M., Giraldez A.J., Voytas D.F., Peterson R.T., Yeh J.R., Joung J.K. Selection-free zinc-finger-nuclease engineering by context-dependent assembly (CoDA). Nat. Methods 2011, 8:67-69.
58. Schmid-Burgk J.L., Schmidt T., Kaiser V., Honing K., Hornung V. A ligation-independent cloning technique for high-throughput assembly of transcription activator-like effector genes. Nat. Biotechnol. 2013, 31:76-81.
59. Shukla V.K., Doyon Y., Miller J.C., DeKelver R.C., Moehle E.A., Worden S.E., Mitchell J.C., Arnold N.L., Gopalan S., Meng X., Choi V.M., Rock J.M., Wu Y.-Y., Katibah G.E., Zhifang G., McCaskill D., Simpson M.A., Blakeslee B., Greenwalt S.A., Butler H.J., Hinkley S.J., Zhang L., Rebar E.J., Gregory P.D., Urnov F.D. Precise genome modification in the crop species Zea mays using zinc-finger nucleases. Nature 2009, 459:437-441.
60. Smith J., Bibikova M., Whitby F.G., Reddy A.R., Chandrasegaran S., Carroll D. Requirements for double-strand cleavage by chimeric restriction enzymes with zinc finger DNA-recognition domains. Nucl. Acids Res. 2000, 28:3361-3369.
61. Streubel J., Blucher C., Landgraf A., Boch J. TAL effector RVD specificities and efficiencies. Nat. Biotechnol. 2012, 30:593-595.
62. Sussman D., Chadsey M., Fauce S., Engel A., Bruett A., Monnat R., Stoddard B.L., Seligman L.M. Isolation and characterization of new homing endonuclease specificities at individual target site positions. J. Mol. Biol. 2004, 342:31-41.
63. Thierry A., Dujon B. Nested chromosomal fragmentation in yeast using the meganuclease I-Sce I: a new method for physical mapping of eukaryotic genomes. Nucl. Acids Res. 1992, 20:5625-5631.
64. Townsend J.A., Wright D.A., Winfrey R.J., Fu F., Maeder M.L., Joung J.K., Voytas D.F. High-frequency modification of plant genes using engineered zinc-finger nucleases. Nature 2009, 459:442-445.
65. USDA APHIS BRS, 2013. http://www.aphis.usda.gov.
66. Voytas D.F. Plant genome engineering with sequence-specific nucleases. Annu. Rev. Plant Biol. 2013, 64:327-350.
67. Wang T.L., Uauy C., Robson F., Till B. TILLING in extremis. Plant Biotechnol. J. 2012, 10:761-772.
68. Wendt T., Holm P., Starker C., Christian M., Voytas D., Brinch-Pedersen H., Holme I. TAL effector nucleases induce mutations at a pre-selected location in the genome of primary barley transformants. Plant Mol. Biol. 2013, 83:279-285.
69. Wolfe S.A., Greisman H.A., Ramm E.I., Pabo C.O. Analysis of zinc fingers optimized via phage display: evaluating the utility of a recognition code. J. Mol. Biol. 1999, 285:1917-1934.
70. Wright D.A., Thibodeau-Beganny S., Sander J.D., Winfrey R.J., Hirsh A.S., Eichtinger M., Fu F., Porteus M.H., Dobbs D., Voytas D.F., Joung J.K. Standardized reagents and protocols for engineering zinc finger nucleases by modular assembly. Nat. Protoc. 2006, 1:1637-1652.
71. Xie K., Yang Y. RNA-guided genome editing in plants using a CRISPR-Cas system. Mol. Plant 2013, 6:1975-1983.