High frequency targeted mutagenesis in Arabidopsis thaliana using zinc finger nucleases

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 26, 2010, Pages 12028-12033

  Zhang, Feng ^a   Maeder, Morgan L ^b   Unger Wallaced, Erica ^c   Hoshaw, Justin P ^a   Reyon, Deepak ^c   Christian, Michelle ^a   Li, Xiaohong ^a   Pierick, Christopher J ^a   Dobbs, Drena ^c   Peterson, Thomas ^c   Joung, J Keith ^b,d   Voytas, Daniel F ^a  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c IOWA STATE UNIVERSITY   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Alcohol dehydrogenase; Chalcone synthase; Gene knockout; Nonhomologous end joining

Indexed keywords

ALCOHOL DEHYDROGENASE; ALCOHOL DEHYDROGENASE 1; ESTROGEN; NUCLEASE; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN;

ALLELE; ARABIDOPSIS; ARTICLE; CHROMOSOME BREAKAGE; DNA SEQUENCE; DOUBLE STRANDED DNA BREAK; ENZYME ENGINEERING; GENE; GENE DELETION; GENE INSERTION; GENE TARGETING; HOMOZYGOSITY; INDUCED MUTATION; MUTAGENESIS; NONHUMAN; OLIGOMERIZATION; PHENOTYPE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROGENY; PROTEIN EXPRESSION; PROTOPLAST; SCREENING; SEEDLING; SOMATIC MUTATION; TRANSGENIC PLANT; TT4 GENE; YEAST;

ALCOHOL DEHYDROGENASE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BASE SEQUENCE; DEOXYRIBONUCLEASES; DNA REPAIR; DNA, PLANT; GENE TARGETING; GENES, PLANT; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PLANTS, GENETICALLY MODIFIED; PROTEIN ENGINEERING; PROTOPLASTS; SACCHAROMYCES CEREVISIAE; ZINC FINGERS;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 77955395799     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0914991107     Document Type: Article

References (48)

1. Doetschman T, et al. (1987) Targetted correction of a mutant HPRT gene in mouse embryonic stem cells. Nature 330:576-578.
2. Rothstein RJ (1983) One-step gene disruption in yeast. Methods Enzymol 101:202-211.
3. Thomas KR, Capecchi MR (1987) Site-directed mutagenesis by gene targeting in mouse embryo-derived stem cells. Cell 51:503-512.
4. Cathomen T, Joung JK (2008) Zinc-finger nucleases: The next generation emerges. Mol Ther 16:1200-1207.
5. Wyman C, Kanaar R (2006) DNA double-strand break repair: All's well that ends well. Annu Rev Genet 40:363-383.
6. Lloyd A, Plaisier CL, Carroll D, Drews GN (2005) Targeted mutagenesis using zincfinger nucleases in Arabidopsis. Proc Natl Acad Sci USA 102:2232-2237.
7. de Pater S, Neuteboom LW, Pinas JE, Hooykaas PJ, van der Zaal BJ (2009) ZFN-induced mutagenesis and gene-targeting in Arabidopsis through Agrobacterium-mediated floral dip transformation. Plant Biotechnol J 7:821-835.
8. Britt AB, May GD (2003) Re-engineering plant gene targeting. Trends Plant Sci 8:90-95.
9. Bibikova M, Beumer K, Trautman JK, Carroll D (2003) Enhancing gene targeting with designed zinc finger nucleases. Science 300:764.
10. Urnov FD, et al. (2005) Highly efficient endogenous human gene correction using designed zinc-finger nucleases. Nature 435:646-651.
11. Geurts AM, et al. (2009) Knockout rats via embryo microinjection of zinc-finger nucleases. Science 325:433.
12. Doyon Y, et al. (2008) Heritable targeted gene disruption in zebrafish using designed zinc-finger nucleases. Nat Biotechnol 26:702-708.
13. Meng X, Noyes MB, Zhu LJ, Lawson ND, Wolfe SA (2008) Targeted gene inactivation in zebrafish using engineered zinc-finger nucleases. Nat Biotechnol 26:695-701.
14. Shukla VK, et al. (2009) Precise genome modification in the crop species Zea mays using zinc-finger nucleases. Nature 459:437-441.
15. Townsend JA, et al. (2009) High-frequency modification of plant genes using engineered zinc-finger nucleases. Nature 459:442-445.
16. Maeder ML, et al. (2008) Rapid "open-source" engineering of customized zinc-finger nucleases for highly efficient gene modification. Mol Cell 31:294-301.
17. Maeder ML, Thibodeau-Beganny S, Sander JD, Voytas DF, Joung JK (2009) Oligomerized pool engineering (OPEN): an 'open-source' protocol for making customized zinc-finger arrays. Nat Protoc 4:1471-1501.
18. Sander JD, Zaback P, Joung JK, Voytas DF, Dobbs D (2007) Zinc Finger Targeter (ZiFiT): An engineered zinc finger/target site design tool. Nucleic Acids Res 35:W599-W605.
19. Pavletich NP, Pabo CO (1991) Zinc finger-DNA recognition: Crystal structure of a Zif268-DNA complex at 2.1 A. Science 252:809-817.
20. Hoshaw JP, Unger-Wallace E, Zhang F, Voytas DF (2010) A transient assay for monitoring zinc-finger nuclease activity at endogenous plant gene targets. Methods Mol Biol, in press.
21. Gorbunova V, Levy AA (1997) Non-homologous DNA end joining in plant cells is associated with deletions and filler DNA insertions. Nucleic Acids Res 25:4650-4657.
22. Clough SJ, Bent AF (1998) Floral dip: A simplified method for Agrobacteriummediated transformation of Arabidopsis thaliana. Plant J 16:735-743.
23. Zuo J, Niu QW, Chua NH (2000) Technical advance: An estrogen receptor-based transactivator XVE mediates highly inducible gene expression in transgenic plants. Plant J 24:265-273.
24. Curtis MD, Grossniklaus U (2003) A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol 133:462-469.
25. Perez EE, et al. (2008) Establishment of HIV-1 resistance in CD4+ T cells by genome editing using zinc-finger nucleases. Nat Biotechnol 26:808-816.
26. Irish VF, Jenik PD (2001) Cell lineage, cell signaling and the control of plant morphogenesis. Curr Opin Genet Dev 11:424-430.
27. Jacobs M, Dolferus R, Van den Bossche D (1988) Isolation and biochemical analysis of ethyl methanesulfonate-induced alcohol dehydrogenase null mutants of arabidopsis thaliana (L.) Heynh. Biochem Genet 26:105-122.
28. Li J, Ou-Lee TM, Raba R, Amundson RG, Last RL (1993) Arabidopsis flavonoid mutants are hypersensitive to UV-B irradiation. Plant Cell 5:171-179.
29. Shirley BW, et al. (1995) Analysis of Arabidopsis mutants deficient in flavonoid biosynthesis. Plant J 8:659-671.
30. Zou J, et al. (2009) Gene targeting of a disease-related gene in human induced pluripotent stem and embryonic stem cells. Cell Stem Cell 5:97-110.
31. Foley JE, et al. (2009) Rapid mutation of endogenous zebrafish genes using zinc finger nucleases made by Oligomerized Pool ENgineering (OPEN). PLoS One 4:e4348.
32. Pruett-Miller SM, Reading DW, Porter SN, Porteus MH (2009) Attenuation of zinc finger nuclease toxicity by small-molecule regulation of protein levels. PLoS Genet 5:e1000376.
33. Bibikova M, Golic M, Golic KG, Carroll D (2002) Targeted chromosomal cleavage and mutagenesis in Drosophila using zinc-finger nucleases. Genetics 161:1169-1175.
34. Miller JC, et al. (2007) An improved zinc-finger nuclease architecture for highly specific genome editing. Nat Biotechnol 25:778-785.
35. Szczepek M, et al. (2007) Structure-based redesign of the dimerization interface reduces the toxicity of zinc-finger nucleases. Nat Biotechnol 25:786-793.
36. Beumer KJ, et al. (2008) Efficient gene targeting in Drosophila by direct embryo injection with zinc-finger nucleases. Proc Natl Acad Sci USA 105:19821-19826.
37. Masclaux F, Charpenteau M, Takahashi T, Pont-Lezica R, Galaud JP (2004) Gene silencing using a heat-inducible RNAi system in Arabidopsis. Biochem Biophys Res Commun 321:364-369. (Pubitemid 39055755)
38. Kim SY, Hong CB, Lee I (2001) Heat shock stress causes stage-specific male sterility in Arabidopsis thaliana. J Plant Res 114:301-307.
39. Alonso JM, et al. (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301:653-657.
40. Jander G, Barth C (2007) Tandem gene arrays: A challenge for functional genomics. Trends Plant Sci 12:203-210.
41. Lee HJ, Kim E, Kim JS (2010) Targeted chromosomal deletions in human cells using zinc finger nucleases. Genome Res 20:81-89.
42. Halpin C, Cooke SE, Barakate A, El Amrani A, Ryan MD (1999) Self-processing 2A-polyproteins - a system for co-ordinate expression of multiple proteins in transgenic plants. Plant J 17:453-459.
43. Koncz C, Schell J (1986) The promoter of the TL-DNA gene 5 controls the tissue-specific expression of chimeric genes carried by a novel type of Agrobacterium binary vector. Mol Gen Genet 204:383-396.
44. Dong Q, et al. (2005) Comparative plant genomics resources at PlantGDB. Plant Physiol 139:610-618.
45. Swarbreck D, et al. (2008) The Arabidopsis Information Resource (TAIR): Gene structure and function annotation. Nucleic Acids Res 36:D1009-D1014.
46. Olson M, Bostic K, Seltzer M, Berkeley D (1999) Proceedings of the annual conference on USENIX Annual Technical Conference.
47. Stajich JE, et al. (2002) The Bioperl toolkit: Perl modules for the life sciences. Genome Res 12:1611-1618.
48. Fu F, et al. (2009) Zinc Finger Database (ZiFDB): A repository for information on C2H2 zinc fingers and engineered zinc-finger arrays. Nucleic Acids Res 37:D279-D283.