Synthetic TAL effectors for targeted enhancement of transgene expression in plants

Plant Biotechnology Journal

Volumn 12, Issue 4, 2014, Pages 436-446

  Liu, Wusheng ^a   Rudis, Mary R ^a   Peng, Yanhui ^a   Mazarei, Mitra ^a   Millwood, Reginald J ^a   Yang, Jian Ping ^b   Xu, Wenzhi ^a   Chesnut, Jonathan D ^b   Stewart, Charles Neal ^a,b  

^a UNIVERSITY OF TENNESSEE   (United States)

^b Life Technologies   (United States)

Author keywords

Additive effects; AtPAP1; pporRFP; Synthetic TALEs; Targeted transgene activation; Transgenic plants

Indexed keywords

ARABIDOPSIS; BACTERIA (MICROORGANISMS); NICOTIANA TABACUM; XANTHOMONAS;

ARABIDOPSIS PROTEIN; PAP1 PROTEIN, ARABIDOPSIS; PLANT DNA; PROTEIN BINDING; TRANSACTIVATOR PROTEIN; TRANSCRIPTION FACTOR;

BINDING SITE; CHEMISTRY; GENE EXPRESSION REGULATION; GENETIC ENGINEERING; GENETICS; METABOLISM; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PIGMENTATION; PLANT LEAF; PROCEDURES; PROMOTER REGION; PROTEIN TERTIARY STRUCTURE; REPORTER GENE; TOBACCO; TRANSCRIPTION INITIATION; TRANSGENE; TRANSGENIC PLANT;

ARABIDOPSIS PROTEINS; BASE SEQUENCE; BINDING SITES; DNA, PLANT; GENE EXPRESSION REGULATION, PLANT; GENES, REPORTER; GENETIC ENGINEERING; PIGMENTATION; PLANT LEAVES; PLANTS, GENETICALLY MODIFIED; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; TOBACCO; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TRANSCRIPTIONAL ACTIVATION; TRANSGENES;

EID: 84899063623     PISSN: 14677644     EISSN: 14677652     Source Type: Journal    
DOI: 10.1111/pbi.12150     Document Type: Article

References (47)

1. Alieva, N.O., Konzen, A.K.A., Field, S.F., Meleshkevitch, E.A., Hunt, M.E., BeltranRamirez, V., Miller, D.J., Wiedenmann, J., Salih, A. and Matz, M.V. (2008) Diversity and evolution of coral fluorescent proteins. PLoS ONE, 3, e2680.
2. Beerli, R.R., Segal, D.J., Dreier, B. and Barbas, C.F. 3rd. (1998) Toward controlling gene expression at will: specific regulation of the erbB-2/HER-2 promoter by using polydactyl zinc finger proteins constructed from modular building blocks. Proc. Natl Acad. Sci. USA, 95, 14628-14633.
3. Benfey, P.N., Ren, L. and Chua, N.H. (1990) Tissue-specific expression from CaMV 35S enhancer subdomains in early stages of plant development. EMBO J. 9, 1677-1684.
4. Boch, J. and Bonas, U. (2010) Xanthomonas AvrBs3 family-type III effectors: discovery and function. Ann. Rev. Phytopathol. 48, 419-436.
5. 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, 326, 1509-1512.
6. Bogdanove, A.J. and Voytas, D.F. (2011) TAL effectors: customizable proteins for DNA targeting. Science, 333, 1843-1846.
7. Borevitz, J., Xia, Y., Blount, J.W., Dixon, R.A. and Lamb, C. (2000) Activation tagging identifies a conserved MYB regulator of phenylpropanoid biosynthesis. Plant Cell, 12, 2383-2393.
8. Bultmann, S., Morbitzer, R., Schmidt, C.S., Thanisch, K., Spada, F., Elsaesser, J., Lahaye, T. and Leonhardt, H. (2012) Targeted transcriptional activation of silent oct4 pluripotency gene by combining designer TALEs and inhibition of epigenetic modifiers. Nucleic Acids Res. 40, 5368-5377.
9. Curtin, S.J., Zhang, F., Sander, J.D., Haun, W.J., Starker, C., Baltes, N.J., Revon, D., Dahlborg, E.J., Goodwin, M.J., Coffman, A.P., Dobbs, D., Joung, J.K., Voyats, D.F. and Stupar, R.M. (2011) Targeted mutagenesis of duplicated genes in soybean with zinc-finger nucleases. Plant Physiol. 156, 466-473.
10. Curtis, M.D. and Grossniklaus, U. (2003) A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol. 133, 462-469.
11. Deng, D., Yan, C., Pan, X., Mahfouz, M., Wang, J., Zhu, J.-K., Shi, Y. and Yan, N. (2012) Structural basis for sequence-specific recognition of DNA by TAL effectors. Science, 335, 720-723.
12. Fischer, J.A., Giniger, E., Maniatis, T. and Ptashne, M. (1988) GAL4 activates transcription in Drosophila. Nature, 332, 853-865.
13. Gao, H., Wu, X., Chai, J. and Han, Z. (2012) Crystal structure of a TALE protein reveals an extended N-terminal DNA binding region. Cell Res. 22, 1716-1720.
14. Geibler, 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.
15. Hagmann, M., Georgiev, O. and Schaffner, W. (1997) The VP16 paradox: herpes simplex virus VP16 contains a long-range activation domain but within the natural multiprotein complex activates only from promoter-proximal positions. J. Virol. 71, 5952-5962.
16. Hajdukiewicz, P., Svab, Z. and Maliga, P. (1994) The small, versatile PZP family of Agrobacterium binary vectors for plant transformation. Plant Mol. Biol. 25, 989-994.
17. Hirai, H., Tani, T. and Kikyo, N. (2010) Structure and functions of powerful transactivators: VP16, MyoO and FoxA. Int. J. Dev. Biol. 54, 1589-1596.
18. Horsch, R.B., Frv, J.E., Hoffmann, N.L., Eichholtz, D., Rogers, S.G. and Fralev, R.T. (1985) A simple and general-method for transferring genes into plants. Science, 227, 1229-1231.
19. Huang, P., Xiao, A., Zhou, M., Zhu, Z., Lin, S. and Zhang, B. (2011) Heritable gene targeting in zebrafish using customized TALENs. Nat. Biotechnol. 29, 699-700.
20. Kay, S., Hahn, S., Marois, E., Hause, G. and Bonas, U. (2007) A bacterial effector acts as a plant transcription factor and induces a cell size regulator. Science, 318, 648-651.
21. Kim, J.S., Lee, H.J. and Carroll, D. (2010) Genome editing with modularly assembled zinc-finger nucleases. Nat. Methods, 7, 91-92.
22. Li, T., Huang, S., Zhao, X., Wright, D.A., Carpenter, S., Spalding, M.H., Weeks, D.P. and Yang, B. (2011) Modularly assembled designer TAL effector nucleases for targeted gene knockout and gene replacement in eukaryotes. Nucleic Acids Res. 39, 6315-6325.
23. Liu, X., Miller, C.W., Koeffler, P.H. and Berk, A.J. (1993) The p53 activation domain binds the TATA box-binding polypeptide in Holo-TFIID, and a neighboring p53 domain inhibits transcription. Mol. Cell. Biol. 13, 3291-3300.
24. Liu, W., Mazarei, M., Rudis, M.R., Fethe, M.H. and Stewart, C.N. Jr. (2011) Rapid in vivo analysis of synthetic promoters for plant pathogen phytosensing. BMC Biotechnol. 11, 108.
25. Liu, W., Yuan, J.S. and Stewart, C.N. Jr. (2013a) Advanced genetic tools for plant biotechnology. Nat. Rev. Genet. 14, 781-793.
26. Liu, W., Mazarei, M., Rudis, M.R., Fethe, M.H., Peng, Y., Millwood, R., Shoene, G., Burris, J.N. and Stewart, C.N. Jr. (2013b) Bacterial pathogen phytosensing in transgenic tobacco and Arabidopsis. Plant Biotechnol. J. 11, 43-52.
27. Mak, A.N., Bradley, P., Cernadas, R.A., Bogdanove, A.J. and Stoddard, B.L. (2012) The crystal structure of TAL effector PthXo1 bound to its DNA target. Science, 335, 716-719.
28. Mann, D.G.J., Abercrombie, L.L., Rudis, M.R., Millwood, R.J., Dunlap, J.R. and Stewart, C.N. Jr. (2012) Very bright orange fluorescent plants: endoplasmic reticulum targeting of orange fluorescent proteins as visual reporters in transgenic plants. BMC Biotechnol. 12, 17.
29. Mazarei, M., Teplova, I., Hajimorad, M.R. and Stewart, C.N. Jr. (2008) Pathogen phytosensing: plants to report plant pathogens. Sensors, 8, 2628-2641.
30. Millwood, R.J., Halfhill, M.D., Harkins, D., Rusotti, R. and Stewart, C.N. Jr. (2003) Instrumentation and methodology for quantifying GFP fluorescence in intact plant organs. Biotechniques, 34, 638-643.
31. Morbitzer, R., Romer, P., Boch, J. and Lahaye, T. (2010) Regulation of selected genome loci using de novo-engineered transcription activator-like effector (TALE)-type transcription factors. Proc. Natl Acad. Sci. USA, 107, 21617-21622.
32. Moscou, M.J. and Bogdanove, A.J. (2009) A simple cipher governs DNA recognition by TAL effectors. Science, 326, 1501.
33. Mussolino, C., Morbitzer, R., Lutge, F., Dannemann, N., Lahaye, T. and Cathomen, T. (2011) A novel TALE nuclease scaffold enables high genome editing activity in combination with low toxicity. Nucleic Acids Res. 39, 9283-9293.
34. Ramirez, C.L., Foley, J.E., Wright, D.A., Muller-Lerch, F., Rahman, S.H., Cornu, T.I., Windrey, R.J., Sander, J.D., Fu, F., Townsend, J.A., Cathomen, T., Voytas, D.F. and Joung, J.K. (2008) Unexpected failure rates for modular assembly of engineered zinc fingers. Nat. Methods, 5, 374-375.
35. Romer, P., Hahn, S., Jordan, T., Straub, T. and Lahaye, T. (2007) Plant-pathogen recognition mediated by promoter activation of the pepper Bs3 resistance gene. Science, 318, 645-648.
36. Romer, P., Recht, S. and Lahaye, T. (2009) A single plant resistance gene promoter engineered to recognize multiple TAL effectors from disparate pathogens. Proc. Natl Acad. Sci. USA, 106, 20526-20531.
37. Schmidt, G.W. and Delaney, S.K. (2010) Stable internal reference genes for normalization of real-time RT-PCR in tobacco (Nicotiana tabacum) during development and abiotic stress. Mol. Genet. Genomics, 283, 233-241.
38. Tesson, L., Usal, C., Menoret, S., Leung, E., Niles, B.J., Remy, S., Santiago, Y., Vincent, A.I., Meng, X., Zhang, L., Gregory, P.D., Anegon, I. and Cost, G.J. (2011) Knockout rats generated by embryo microinjection of TALENs. Nat. Biotechnol. 29, 695-696.
39. Tohge, T., Nishiyama, Y., Hirai, M.Y., Nakajima, J., Awazuhara, M., Inoue, E., Takahashi, H., Goodenowe, D.B., Kitayama, M., Noji, M., Yamazaki, M. and Saito, K. (2005) Functional genomics by integrated analysis of metabolome and transcriptome of Arabidopsis plants over-expressing an MYB transcription factor. Plant J. 42, 218-235.
40. 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.
41. Triezenberg, S.J., LaMarco, K.L. and McKnight, S.L. (1988) Functional dissection of VP16, the trans-activator of herpes simplex virus immediate early gene expression. Genes Dev. 2, 718-729.
42. Urnov, F.D. and Rebar, E.J. (2002) Designed transcription factors as tools for therapeutics and functional genomics. Biochem. Pharmacol. 64, 919-923.
43. Urnov, F.D., Rebar, E.J., Holmes, M.C., Zhang, H.S. and Gregory, P.D. (2010) Genome editing with engineered zinc finger nucleases. Nature, 11, 636-646.
44. Xie, D.Y., Sharma, S.B., Wright, E., Wang, Z.Y. and Dixon, R.A. (2006) Metabolic engineering of proanthocyanidins through co-expression of anthocyanidin reductase and the PAP1 MYB transcription factor. Plant J. 45, 895-907.
45. Yang, B., Zhu, W., Johnson, L.B. and White, F.F. (2000) The virulence factor AvrXa7 of Xanthomonas oryzae pv. oryzae is a type III secretion pathway-dependent nuclear-localized double-stranded DNA-binding protein. Proc. Natl Acad. Sci. USA, 97, 9807-9812.
46. Zhang, F., Cong, L., Lodato, S., Kosuri, S., Church, G.M. and Arlotta, P. (2011) Efficient construction of sequence-specific TAL effectors for modulating mammalian transcription. Nat. Biotechnol. 29, 149-154.
47. Zhang, Y., Zhang, F., Li, X., Baller, J.A., Qi, Y., Starker, C.G., Bogdanove, A.J. and Voytas, D.F. (2013) Transcription activator-like effector nucleases enable efficient plant genome engineering. Plant Physiol. 161, 20-27.