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Physiological Function of NbRanBP1 in Nicotiana benthamiana  

Cho, Hui-Kyung (Department of Biology, Yonsei University)
Park, Jong-A (Department of Biology, Yonsei University)
Pai, Hyun-Sook (Department of Biology, Yonsei University)
Publication Information
Molecules and Cells / v.26, no.3, 2008 , pp. 270-277 More about this Journal
Abstract
This study addresses the physiological functions of the Ran-binding protein homolog NbRanBP1 in Nicotiana benthamiana. Virus-induced gene silencing (VIGS) of NbRanBP1 caused stunted growth, leaf yellowing, and abnormal leaf morphology. The NbRanBP1 gene was constitutively expressed in diverse tissues and an NbRanBP1:GFP fusion protein was primarily localized to the nuclear rim and the cytosol. BiFC analysis revealed in vivo interaction between NbRanBP1 and NbRan1 in the nuclear envelope and the cytosol. Depletion of NbRanBP1 or NbRan1 reduced nuclear accumulation of a NbBTF3:GFP marker protein. In the later stages of development, NbRanBP1 VIGS plants showed stress responses such as reduced mitochondrial membrane potential, excessive production of reactive oxygen species, and induction of defense-related genes. The molecular role of RanBP1 in plants is discussed in comparison with RanBP1 function in yeast and mammals.
Keywords
bimolecular fluorescence complementation; NbBTF3:GFP; NbRan1; nuclear envelope; stress symptoms; virus-induced gene silencing;
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Times Cited By KSCI : 3  (Citation Analysis)
Times Cited By Web Of Science : 6  (Related Records In Web of Science)
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1 Apel, K., and Hirt, H. (2004). Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 55, 373-399   DOI   ScienceOn
2 Battistoni, A., Guarguaglini, G., Degrassi, F., Pittoggi, C., Palena, A., Di Matteo, G., Pisano, C., Cundari, E., and Lavia, P. (1997). Deregulated expression of the RanBP1 gene alters cell cycle progression in murine fibroblasts. J. Cell Sci. 110, 2345-2357
3 Beers, E.P., Woffenden, B.J., and Zhao, C. (2000). Plant proteolytic enzymes: possible roles during programmed cell death. Plant Mol. Biol. 44, 399-415   DOI   ScienceOn
4 Cho, K.H., Jun, S.E., Lee, Y.K., Jeong, S.J., and Kim, G.T. (2006). Developmental processes of leaf morphogenesis in Arabidopsis. J. Plant Biol. 50, 282-290   과학기술학회마을   DOI
5 Chook, Y.M., and Blobel, G. (2001). Karyopherins and nuclear import. Curr. Opin. Struct. Biol. 11, 703-715   DOI   ScienceOn
6 Ciciarello, M., Mangiacasale, R., and Lavia, P. (2007). Spatial control of mitosis by the GTPase Ran. Cell Mol. Life. Sci. 64, 1891-1914   DOI
7 Dasso, M. (2001). Running on Ran: nuclear transport and the mitotic spindle. Cell 104, 321-324   DOI   ScienceOn
8 Di Fiore, B., Ciciarello, M., Mangiacasale, R., Palena, A., Tassin, A.M., Cundari, E., and Lavia, P. (2003). Mammalian RanBP1 regulates centrosome cohesion during mitosis. J. Cell Sci. 116, 3399-3411   DOI   ScienceOn
9 Green, D.R., and Kroemer, G. (2004). The pathophysiology of mitochondrial cell death. Science 305, 627-629
10 Guarguaglini, G., Renzi, L., D'Ottavio, F., Di Fiore, B., Casenghi, M., Cundari, E., and Lavia, P. (2000). Regulated Ran-binding protein 1 activity is required for organization and function of the mitotic spindle in mammalian cells in vivo. Cell Growth Differ. 11, 455-465
11 Kim, M., Lim, J.H., Ahn, C.S, Park, K., Kim, G.-T., Kim, W.T., and Pai, H.-S. (2006). Mitochondria-associated hexokinases play a role in the control of programmed cell death in Nicotiana benthamiana. Plant Cell 18, 2341-2355   DOI   ScienceOn
12 Rose, A., and Meier, I. (2001). A domain unique to plant RanGAP is responsible for its targeting to the plant nuclear rim. Proc. Natl. Acad. Sci. USA 98, 15377-15382
13 Yaseen, N.R., and Blobel, G. (1999). Two distinct classes of Ranbinding sites on the nucleoporin Nup-358. Proc. Natl. Acad.Sci. USA 96, 5516-5521
14 Zhang, H., Huang, H.M., Carson, R.C., Mahmood, J., Thomas, H.M., and Gibson, G.E. (2001). Assessment of membrane potentials of mitochondrial populations in living cells. Anal. Biochem. 298, 170-180   DOI   ScienceOn
15 Schlenstedt, G., Wong, D.H., Koepp, D.M., and Silver, P.A. (1995). Mutants in a yeast Ran binding protein are defective in nuclear transport. EMBO J. 14, 5367-5378
16 Kim, S.H., and Roux, S.J. (2003). An Arabidopsis Ran-binding protein, AtRanBP1c, is a co-activator of Ran GTPase-activating protein and requires the C-terminus for its cytoplasmic localization. Planta 216, 1047-1052
17 Sazer, S., and Dasso, M. (2000). The ran decathlon: multiple roles of Ran. J. Cell Sci. 113, 1111-1118
18 Azevedo, C., Sadanandom, A., Kitagawa, K., Freialdenhoven, A., Shirasu, K., and Schulze-Lefert, P. (2002). The RAR1 interactor SGT1, an essential component of R gene-triggered disease resistance. Science 295, 2073-2076   DOI   ScienceOn
19 Kim, S.H., Arnold, D., Lloyd, A., and Roux, S.J. (2001). Antisense expression of an Arabidopsis ran binding protein renders transgenic roots hypersensitive to auxin and alters auxin-induced root growth and development by arresting mitotic progress. Plant Cell 13, 2619-2630   DOI
20 Aslanukov, A., Bhowmick, R., Guruju, M., Oswald, J., Raz, D., Bush, R.A., Sieving, P.A., Lu, X., Bock, C.B., and Ferreira, P.A. (2006). RanBP2 modulates Cox11 and hexokinase I activities and haploinsufficiency of RanBP2 causes deficits in glucose metabolism. PLoS Genet. 2, e177   DOI   ScienceOn
21 Walter, M., Chaban, C., Schütze, K., Batistic, O., Weckermann, K., Näke, C., Blazevic, D., Grefen, C., Schumacher, K., Oecking, C., et al. (2004). Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. Plant J. 40, 428-438   DOI   ScienceOn
22 Steggerda, S.M., and Paschal, B.M. (2002). Regulation of nuclear import and export by the GTPase Ran. Int. Rev. Cytol. 217, 41-91   DOI
23 Kahana, J.A., and Cleveland, D.W. (1999). Beyond nuclear transport. Ran-GTP as a determinant of spindle assembly. J. Cell Biol. 146, 1205-1210   DOI
24 Lam, E., Kato, N., and Lawton, M. (2001). Programmed cell death, mitochondria and the plant hypersensitive response. Nature 411, 848-853   DOI   ScienceOn
25 Richards, S.A., Lounsbury, K.M., Carey, K.L., and Macara, I.G. (1996). A nuclear export signal is essential for the cytosolic localization of the Ran binding protein, RanBP1. J. Cell Biol. 134, 1157-1168   DOI
26 Stewart, M. (2007). Molecular mechanism of the nuclear protein import cycle Nat. Rev. Mol. Cell. Biol. 8, 195-208   DOI   ScienceOn
27 Bischoff, F.R., Krebber, H., Smirnova, E., Dong, W., and Ponstingl, H. (1995). Co-activation of RanGTPase and inhibition of GTP dissociation by Ran-GTP binding protein RanBP1. EMBO J. 14, 705-715
28 Ma, L., Hong, Z., and Zhang, Z. (2007). Perinuclear and nuclear envelope localizations of Arabidopsis Ran proteins. Plant Cell Rep. 26, 1373-1382   DOI
29 Yang, K.S., Kim, H.S., Jin, U.H., Lee, S.S., Park, J.A., Lim, Y.P., and Pai, H.S. (2007). Silencing of NbBTF3 results in developmental defects and disturbed gene expression in chloroplasts and mitochondria of higher plants. Planta 225, 1459-1469   DOI
30 Yi, R., Bogerd, H.P., Wiegand, H.L., and Cullen, B.R. (2002). Both ran and importins have the ability to function as nuclear mRNA export factors. RNA 8, 180-187   DOI
31 Pemberton, L.F., and Paschal, B.M. (2005). Mechanisms of receptor- mediated nuclear import and nuclear export. Traffic 6, 187-198   DOI   ScienceOn
32 Austin, M.J., Muskett, P., Kahn, K., Feys, B.J., Jones, J.D., and Parker, J.E. (2002), Regulatory role of SGT1 in early R genemediated plant defenses. Science 295, 2077-2080   DOI   ScienceOn
33 Zenklusen, D., and Stutz, F. (2001). Nuclear export of mRNA. FEBS Lett. 498, 150-156   DOI   ScienceOn
34 Haizel, T., Merkle, T., Pay, A., Fejes, E., and Nagy, F. (1997). Characterization of proteins that interact with the GTP-bound form of the regulatory GTPase Ran in Arabidopsis. Plant J. 11, 93-103   DOI   ScienceOn
35 Lee, K.H., Kim, Y.S., Park, C.M., and Kim, H.J. (2008). Proteomic identification of differentially expressed proteins in Arabidopsis mutant ntm1-D with disturbed cell division. Mol. Cells 25, 70-77
36 Cho, H.S., Lee, S.S., Kim, K.D., Hwang, I., Lim, J.-S., Park, Y.-I., and Pai, H.-S. (2004). DNA gyrase is involved in chloroplast nucleoid partitioning. Plant Cell 16, 2665-2682   DOI   ScienceOn
37 Kunzler, M., Gerstberger, T., Stutz, F., Bischoff, F.R., and Hurt, E. (2000). Yeast Ran-binding protein 1 (Yrb1) shuttles between the nucleus and cytoplasm and is exported from the nucleus via a CRM1 (XPO1)-dependent pathway. Mol. Cell. Biol. 20, 4295-4308   DOI
38 Voinnet, O., Rivas, S., Mestre, P., and Baulcombe, D. (2003). An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J. 33, 949-956   DOI   ScienceOn
39 Bethke, P.C., and Jones, R.L. (2001). Cell death of barley aleurone protoplasts is mediated by reactive oxygen species. Plant J. 25, 19-29   DOI   ScienceOn
40 Heath, M.C. (2000). Hypersensitive response-related death. Plant Mol. Biol. 44, 321-324   DOI   ScienceOn
41 Gorlich, D., and Kutay, U. (1999). Transport between the cell nucleus and the cytoplasm. Annu. Rev. Cell Dev. Biol. 15, 607-660   DOI   ScienceOn
42 Ahn, J.-W., Kim, M., Lim, J.H., Kim, G.-T., and Pai, H.-S. (2004). Phytocalpain controls the proliferation and differentiation fates of cells in plant organ development. Plant J. 38, 969-981   DOI   ScienceOn
43 Cullen, B.R. (2003). Nuclear RNA export. J. Cell Sci. 116, 587-597   DOI   ScienceOn
44 Kunzler, M., Trueheart, J., Sette, C., Hurt, E., and Thorner, J. (2001). Mutations in the YRB1 gene encoding yeast ran-bindingprotein- 1 that impair nucleocytoplasmic transport and suppress yeast mating defects. Genetics 157, 1089-1105
45 Bischoff, F.R., and Görlich, D. (1997). RanBP1 is crucial for the release of RanGTP from importin beta-related nuclear transport factors. FEBS Lett. 419, 249-254   DOI   ScienceOn
46 Forler, D., Rabut, G., Ciccarelli, F.D., Herold, A., Köcher, T., Niggeweg, R., Bork, P., Ellenberg, J., and Izaurralde, E. (2004). RanBP2/Nup358 provides a major binding site for NXF1-p15 dimers at the nuclear pore complex and functions in nuclear mRNA export. Mol. Cell. Biol. 24, 1155-1167   DOI
47 Park, J.M., and Paek, K.H. (2006). Recognition and response in plant-pathogen interactions. J. Plant Biol. 50, 132-138   과학기술학회마을   DOI