Is VIP1 important for Agrobacterium-mediated transformation?

Plant Journal

Volumn 79, Issue 5, 2014, Pages 848-860

  Shi, Yong ^a,b   Lee, Lan Ying ^b   Gelvin, Stanton B ^b  

^a NORTHWEST A F UNIVERSITY   (China)

^b PURDUE UNIVERSITY   (United States)

Author keywords

Agrobacterium; Arabidopsis thaliana; Nicotiana benthamiana; Plant transformation; Protein subcellular localization; VirE2; VirE2 interacting protein 1

Indexed keywords

CELLS; CYTOLOGY; PROTEINS; TOBACCO;

AGROBACTERIUM; ARABIDOPSIS THALIANA; NICOTIANA BENTHAMIANA; PLANT TRANSFORMATION; PROTEIN SUBCELLULAR LOCALIZATION; VIRE2; VIRE2 INTERACTING PROTEIN 1;

PLANTS (BOTANY);

AGROBACTERIUM; ARABIDOPSIS; ARABIDOPSIS THALIANA; BENTHAMINA; NICOTIANA BENTHAMIANA; NICOTIANA TABACUM;

ARABIDOPSIS PROTEIN; BACTERIAL PROTEIN; BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR; DNA BINDING PROTEIN; ION CHANNEL; VIP1 PROTEIN, ARABIDOPSIS; VIRE2 PROTEIN, AGROBACTERIUM;

AGROBACTERIUM; ARABIDOPSIS; CELL NUCLEUS; CYTOPLASM; GENETIC TRANSFORMATION; GENETICS; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; PLANT LEAF; PROTEIN TRANSPORT; TOBACCO; TRANSGENIC PLANT;

AGROBACTERIUM; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BACTERIAL PROTEINS; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; CELL NUCLEUS; CYTOPLASM; DNA-BINDING PROTEINS; ION CHANNELS; PLANT LEAVES; PLANTS, GENETICALLY MODIFIED; PROTEIN TRANSPORT; TOBACCO; TRANSFORMATION, GENETIC;

EID: 84906789325     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12596     Document Type: Article

References (64)

1. Abu-Arish, A., Frenkiel-Krispin, D., Fricke, T., Tzfira, T., Citovsky, V., Wolf, S.G., and, Elbaum, M., (2004) Three-dimensional reconstruction of Agrobacterium VirE2 protein with single-stranded DNA. J. Biol. Chem. 279, 25359-25363. (Pubitemid 38756792)
2. Alonso, J. M., Stepanova, A. N., Leisse, T. J., et al,. (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science, 301, 653-657. (Pubitemid 36927950)
3. Ballas, N., and, Citovsky, V., (1997) Nuclear localization signal binding protein from Arabidopsis mediates nuclear import of Agrobacterium VirD2 protein. Proc. Natl Acad. Sci. USA, 94, 10723-10728. (Pubitemid 27430801)
4. Bhattacharjee, S., Lee, L.-Y., Oltmanns, H., Cao, H., Veena, Cuperus, J., and, Gelvin, S.B., (2008) AtImpa-4, an Arabidopsis importin α isoform, is preferentially involved in Agrobacterium-mediated plant transformation. Plant Cell, 20, 2661-2680. (Pubitemid 352844583)
5. Cannone, J., Marino, D., Jauneau, A., Pouzet, C., Briere, C., Roby, D., and, Rivas, S., (2011) The Xanthomonas type III effector XopD targets the Arabidopsis transcription factor MYB30 to sppress plant defense. Plant Cell, 23, 3498-3511.
6. Canonne, J., and, Rivas, S., (2012) Bacterial effectors target the plant cell nucleus to subvert host transcription. Plant Signal. Behav. 7, 217-221.
7. Citovsky, V., Zupan, J., Warnick, D., and, Zambryski, P., (1992) Nuclear localization of Agrobacterium VirE2 protein in plant cells. Science, 256, 1802-1805.
8. Citovsky, V., Warnick, D., and, Zambryski, P., (1994) Nuclear import of Agrobacterium VirD2 and VirE2 proteins in maize and tobacco. Proc. Natl Acad. Sci. USA, 91, 3210-3214. (Pubitemid 24130205)
9. Citovsky, V., Guralnick, B., Simon, M.N., and, Wall, J.S., (1997) The molecular structure of Agrobacterium VirE2-single stranded DNA complexes involved in nuclear import. J. Mol. Biol. 271, 718-727. (Pubitemid 27376049)
10. Citovsky, V., Kapelnikov, A., Oliel, S., Zakai, N., Rojas, M.R., Gilbertson, R.L., Tzfira, T., and, Loyter, A., (2004) Protein interactions involved in nuclear import of the Agrobacterim VirE2 protein in vivo and in vitro. J. Biol. Chem. 279, 29528-29533. (Pubitemid 38915833)
11. Citovsky, V., Lee, L.-Y., Vyas, S., Glick, E., Chen, M.-H., Vainstein, A., Gafni, Y., Gelvin, S.B., and, Tzfira, T., (2006) Subcellular localization of interacting proteins by bimolecular fluorescence complementation in planta. J. Mol. Biol. 362, 1120-1131. (Pubitemid 44353530)
12. Clough, S.J., and, Bent, A.F., (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
13. Deslandes, L., and, Rivas, S., (2011) The plant cell nucleus. A true arena for the fight between plants and pathogens. Plant Signal. Behav. 6, 42-48.
14. Djamei, A., Pitzschke, A., Nakagami, H., Rajh, I., and, Hirt, H., (2007) Trojan horse strategy in Agrobacterium transformation: abusing MAPK defense signaling. Science, 318, 453-456. (Pubitemid 47614531)
15. Frenkiel-Krispin, D., Wolf, S.G., Albeck, S., et al. (2007) Plant transformation by Agrobacterium tumefaciens: modulation of single-stranded DNA-VirE2 complex assembly by VirE1. J. Biol. Chem. 282, 3458-3464. (Pubitemid 47084425)
16. Gelvin, S.B., (1998) Agrobacterium VirE2 proteins can form a complex with T strands in the plant cytoplasm. J. Bacteriol. 180, 4300-4302. (Pubitemid 28373539)
17. Gelvin, S.B., (2003) Agrobacterium-mediated plant transformation: the biology behind the "gene-jockeying" tool. Microbiol. Mol. Biol. Rev. 67, 16-37. (Pubitemid 36314782)
18. Gelvin, S.B., (2009) Agrobacterium in the genomics age. Plant Physiol. 150, 1665-1676.
19. Gelvin, S.B., (2010a) Finding a way to the nucleus. Curr. Opin. Microbiol. 13, 53-58.
20. Gelvin, S.B., (2010b) Plant proteins involved in Agrobacterium-mediated genetic transformation. Annu. Rev. Phytopathol. 48, 45-68.
21. Grange, W., Duckely, M., Husale, S., Jacob, S., Engel, A., and, Hegner, M., (2008) VirE2: a unique ssDNA-compacting molecular machine. PLoS Biol. 6, 343-351.
22. Guralnick, B., Thomsen, G., and, Citovsky, V., (1996) Transport of DNA into the nuclei of Xenopus oocytes by a modified VirE2 protein of Agrobacterium. Plant Cell, 8, 363-373. (Pubitemid 126635913)
23. Herrera-Estrella, A., Van Montagu, M., and, Wang, K., (1990) A bacterial peptide acting as a plant nuclear targeting signal: the amino-terminal portion of Agrobacterium VirD2 protein directs a β-galactosidase fusion protein into tobacco nuclei. Proc. Natl Acad. Sci. USA, 87, 9534-9537. (Pubitemid 120016477)
24. Howard, E., and, Citovsky, V., (1990) The emerging structure of the Agrobacterium T-DNA transfer complex. BioEssays, 12, 103-108. (Pubitemid 120034451)
25. Howard, E.A., Zupan, J.R., Citovsky, V., and, Zambryski, P.C., (1992) The VirD2 protein of A. tumefaciens contains a C-terminal bipartite nuclear localization signal: implications for nuclear uptake of DNA in plant cells. Cell, 68, 109-118.
26. Koncz, C., and, Schell, J., (1986) The promoter of TL-DNA gene 5 controls the tissue-specific expression of chimaeric genes carried by a novel type of Agrobacterium binary vector. Mol. Gen. Genet. 204, 383-396.
27. Koukolikova-Nicola, Z., and, Hohn, B., (1993) How does the T-DNA of Agrobacterium tumefaciens find its way into the plant cell nucleus? Biochimie, 75, 635-638. (Pubitemid 23305228)
28. Koukolikova-Nicola, Z., Raineri, D., Stephens, K., Ramos, C., Tinland, B., Nester, E.W., and, Hohn, B., (1993) Genetic analysis of the virD operon of Agrobacterium tumefaciens: a search for functions involved in transport of T-DNA into the plant cell nucleus and in T-DNA integration. J. Bacteriol. 175, 723-731. (Pubitemid 23046935)
29. Lacroix, B., and, Citovsky, V., (2013a) Characterization of VIP1 activity as a transcriptional regulator in vitro and in planta. Sci. Rep. 3, 2440.
30. Lacroix, B., and, Citovsky, V., (2013b) The roles of bacterial and host plant factors in Agrobacterium-mediated genetic transformation. Int. J. Dev. Biol. 57, 467-481.
31. Lee, L.-Y., Kononov, M.E., Bassuner, B., Frame, B.R., Wang, K., and, Gelvin, S.B., (2007) Novel plant transformation vectors containing the superpromoter. Plant Physiol. 145, 1294-1300. (Pubitemid 350276748)
32. Lee, L.-Y., Fang, M.-J., Kuang, L.-Y., and, Gelvin, S.B., (2008) Vectors for multi-color bimolecular fluorescence complementation to investigate protein-protein interactions in living plant cells. Plant Methods, 4, 24.
33. Lee, L.-Y., Wu, F.-H., Hsu, C.-T., et al. (2012) Screening a cDNA library for protein-protein interactions directly in planta. Plant Cell, 24, 1746-1759.
34. Li, J., Krichevsky, A., Vaidya, M., Tzfira, T., and, Citovsky, V., (2005) Uncoupling of the functions of the Arabidopsis VIP1 protein in transient and stable plant genetic transformation by Agrobacterium. Proc. Natl Acad. Sci. USA, 102, 5733-5738. (Pubitemid 40559628)
35. Li, X., Yang, Q., Tu, H., Lim, Z., and, Pan, S.Q., (2014) Direct visualization of Agrobacterium-delivered VirE2 in recipient cells. Plant J. 77, 487-495.
36. Lichtenstein, C., and, Draper, J., (1986) Genetic engineering of plants. In DNA Cloning. A Practical Approach, Vol. 2 (, Glover, D.M., ed.). Washington, DC: IRL Press, pp. 67-119.
37. Magori, S., and, Citovsky, V., (2012) The role of the ubiquitin-proteosome system in Agrobacterium tumefaciens-mediated genetic transformation of plants. Plant Physiol. 160, 65-71.
38. McCullen, C.A., and, Binns, A.N., (2006) Agrobacterium tumefaciens and plant cell interactions and activities required for interkingdom macromolecular transfer. Annu. Rev. Cell Dev. Biol. 22, 101-127.
39. Mysore, K.S., Bassuner, B., Deng, X.-B., Darbinian, N.S., Motchoulski, A., Ream, W., and, Gelvin, S.B., (1998) Role of the Agrobacterium tumefaciens VirD2 protein in T-DNA transfer and integration. Mol. Plant Microbe Interact. 11, 668-683. (Pubitemid 28417756)
40. Nagai, T., Ibata, K., Park, E.S., Kubota, M., Mikoshiba, K., and, Miyawaki, A., (2002) A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nat. Biotechnol. 20, 87-90. (Pubitemid 34044921)
41. Nam, J., Matthysse, A.G., and, Gelvin, S.B., (1997) Differences in susceptibility of Arabidopsis ecotypes to crown gall disease may result from a deficiency in T-DNA integration. Plant Cell, 9, 317-333. (Pubitemid 27176822)
42. Nam, J., Mysore, K.S., Zheng, C., Knue, M.K., Matthysse, A.G., and, Gelvin, S.B., (1999) Identification of T-DNA tagged Arabidopsis mutants that are resistant to transformation by Agrobacterium. Mol. Gen. Genet. 261, 429-438. (Pubitemid 29185032)
43. Narasimhulu, S.B., Deng, X.-B., Sarria, R., and, Gelvin, S.B., (1996) Early transcription of Agrobacterium T-DNA genes in tobacco and maize. Plant Cell, 8, 873-886. (Pubitemid 126635938)
44. Pitzschke, A., (2013) Agrobacterium infection and plant defense-transformation success hangs by a thread. Front. Plant Sci. 4, 519.
45. Pitzschke, A., and, Hirt, H., (2010) New insights into an old story: Agrobacterium-induced tumour formation in plants by plant transformation. EMBO J. 29, 1021-1032.
46. Pitzschke, A., Djamei, A., Teige, M., and, Hirt, H., (2009) VIP1 response elements mediate mitogen-activated protein kinase 3-induced stress gene expression. Proc. Natl Acad. Sci. USA, 106, 18414-18419.
47. Rossi, L., Hohn, B., and, Tinland, B., (1996) Integration of complete transferred DNA units is dependent on the activity of virulence E2 protein of Agrobacterium tumefaciens. Proc. Natl Acad. Sci. USA, 93, 126-130. (Pubitemid 26038115)
48. Sakalis, P.A., van Heusden, G.P.H., and, Hooykaas, P.J.J., (2013) Visualization of VirE2 protein translocation by the Agrobacterium type IV secretion system into host cells. Microbiologyopen, 3, 104-117.
49. Sambrook, J., and, Russell, D.W., (2001) Molecular Cloning, A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
50. Sen, P., Pazour, G. J., Anderson, D., and, Das, A., (1989) Cooperative binding of Agrobacterium tumefaciens VirE2 protein to single-stranded DNA. J. Bacteriol. 171, 2573-2580.
51. Stachel, S.E., and, Nester, E.W., (1986) The genetic and transcriptional organization of the vir region of the A6 Ti plasmid of Agrobacterium tumefaciens. EMBO J. 5, 1445-1454.
52. Tenea, G.N., Spantzel, J., Lee, L.-Y., Zhu, Y., Lin, K., Johnson, S.J., and, Gelvin, S.B., (2009) Overexpression of several Arabidopsis histone genes increases Agrobacterium-mediated transformation and transgene expression in plants. Plant Cell, 21, 3350-3367.
53. Tsugama, D., Liu, S., and, Takano, T., (2012) A bZIP protein, VIP1, is a regulator of osmosensory signaling in Arabidopsis. Plant Physiol. 159, 144-155.
54. Tsugama, D., Liu, S., and, Takano, T., (2013a) Metal-binding ability of VIP1: a bZIP protein in Arabidopsis thaliana. Protein J. 32, 526-532.
55. Tsugama, D., Liu, S., and, Takano, T., (2013b) A bZIP protein, VIP1, interacts with Arabidopsis heterotrimeric G protein β subunit, AGB1. Plant Physiol. Biochem. 71, 240-246.
56. Tzfira, T., and, Citovsky, V., (2001) Comparison between nuclear localization of nopaline- and octopine-specific Agrobacterium VirE2 proteins in plant, yeast and mammalian cells. Mol. Plant Pathol. 2, 171-176. (Pubitemid 32664955)
57. Tzfira, T., Vaidya, M., and, Citovsky, V., (2001) VIP1, an Arabidopsis protein that interacts with Agrobacterium VirE2, is involved in VirE2 nuclear import and Agrobacterium infectivity. EMBO J., 20, 3596-3607. (Pubitemid 32634366)
58. Tzfira, T., Vaidya, M., and, Citovsky, V., (2002) Increasing plant susceptibility to Agrobacterium infection by over-expression of the Arabidopsis nuclear protein VIP1. Proc. Natl Acad. Sci. USA, 99, 10435-10440.
59. Tzfira, T., Vaidya, M., and, Citovsky, V., (2004) Involvement of targeted proteolysis in plant genetic transformation by Agrobacterium. Nature, 431, 87-92. (Pubitemid 39215113)
60. Veena, Jiang, H., Doerge, R.W., and, Gelvin, S.B., (2003) Transfer of T-DNA and Vir proteins to plant cells by Agrobacterium tumefaciens induces expression of host genes involved in mediating transformation and suppresses host defense gene expression. Plant J. 35, 219-236. (Pubitemid 36901068)
61. Wu, Y., Zhao, Q., Gao, L., Yu, X.-M., Fang, P., Oliver, D.J., and, Xiang, C.-B., (2010) Isolation and characterization of low-sulphur-tolerant mutants of Arabidopsis. J. Exp. Bot., 61, 3407-3422.
62. Yusibov, V.M., Steck, T.R., Gupta, V., and, Gelvin, S.B., (1994) Association of single-stranded transferred DNA from Agrobacterium tumefaciens with tobacco cells. Proc. Natl Acad. Sci. USA, 91, 2994-2998. (Pubitemid 24130161)
63. Zhu, Y., Nam, J., Humara, J.M., et al. (2003) Identification of Arabidopsis rat mutants. Plant Physiol. 132, 494-505. (Pubitemid 36715052)
64. Ziemienowicz, A., Merkle, T., Schoumacher, F., Hohn, B., and, Rossi, L., (2001) Import of Agrobacterium T-DNA into plant nuclei: two distinct functions of VirD2 and VirE2 proteins. Plant Cell, 13, 369-383. (Pubitemid 32207689)