Skip to main content
SpringerLink
Log in

Interaction between Agrobacterium tumefaciens oncoprotein 6b and a tobacco nucleolar protein that is homologous to TNP1 encoded by a transposable element of Antirrhinum majus

  • Regular Paper
  • Published:
Journal of Plant Research Aims and scope Submit manuscript

Abstract

When gene 6b on the T-DNA of Agrobacterium tumefaciens is transferred to plant cells, its expression causes plant hormone-independent division of cells in in vitro culture and abnormal cell growth, which induces various morphological defects in 6b-expressing transgenic Arabidopsis thaliana and Nicotiana tabacum plants. Protein 6b localizes to the nuclei, a requirement for the abnormal cell growth, and binds to a tobacco nuclear protein called NtSIP1 and histone H3. In addition, 6b has histone chaperone-like activity in vitro and affects the expression of various plant genes, including cell division-related genes and meristem-related class 1 KNOX homeobox genes, in transgenic Arabidopsis. Here, we report that 6b binds to a newly identified protein NtSIP2, whose amino acid sequence is predicted to be 30% identical and 51% similar to that of the TNP1 protein encoded by the transposon Tam1 of Antirrhinum majus. Immunolocalization analysis using anti-T7 antibodies showed nucleolar localization of most of the T7 epitope-tagged NtSIP2 proteins. A similar analysis with the T7-tagged 6b protein also showed subnucleolar as well as nuclear localization of the 6b protein. These results suggest the involvement of 6b along with NtSIP2 in certain molecular processes in the nucleolus as well as the nucleoplasm.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Angelov D, Bondarenko VA, Almagro S, Menoni H, Mongelard F, Hans F, Mietton F, Studitsky VM, Hamiche A, Dimitrov S, Bouvet P (2006) Nucleolin is a histone chaperone with FACT-like activity and assists remodeling of nucleosomes. EMBO J 25:1669–1679

    Article  PubMed  CAS  Google Scholar 

  • Banno H, Hirano K, Nakamura T, Irie K, Nomoto S, Matsumoto K, Machida Y (1993) NPK1, a tobacco gene that encodes a protein with a domain homologous to yeast BCK1, STE11, and Byr2 protein kinases. Mol Cell Biol 13:4745–4752

    PubMed  CAS  Google Scholar 

  • Biggiogera M, Fakan S, Kaufmann SH, Black A, Shaper JH, Busch H (1989) Simultaneous immunoelectron microscopic visualization of protein B23 and C23 distribution in the HeLa cell nucleolus. J Histochem Cytochem 37:1371–1374

    PubMed  CAS  Google Scholar 

  • Blanar MA, Rutter WJ (1992) Interaction cloning: identification of a helix-loop-helix zipper protein that interacts with c-Fos. Science 256:1014–1018

    Article  PubMed  CAS  Google Scholar 

  • Brown JW, Shaw PJ, Shaw P, Marshall DF (2005) Arabidopsis nucleolar protein database (AtNoPDB). Nucleic Acids Res 33:D633–636

    Article  PubMed  CAS  Google Scholar 

  • Canaday J, Gerad JC, Crouzet P, Otten L (1992) Organization and functional analysis of three T-DNAs from the vitopine Ti plasmid pTiS4. Mol Gen Genet 235:292–303

    Article  PubMed  CAS  Google Scholar 

  • Chopra S, Brendel V, Zhang J, Axtell JD, Peterson T (1999) Molecular characterization of a mutable pigmentation phenotype and isolation of the first active transposable element from Sorghum bicolor. Proc Natl Acad Sci USA 96:15320–15335

    Article  Google Scholar 

  • Clément B, Pollmann S, Weiler E, Urbanczyk-Wochniak E, Otten L (2006) The Agrobacterium vitis T-6b oncoprotein induces auxin-independent cell expansion in tobacco. Plant J 45:1017–1027

    Article  PubMed  CAS  Google Scholar 

  • Clément B, Perot J, Geoffroy P, Legrand M, Zon J, Otten L (2007) Abnormal accumulation of sugars and phenolics in tobacco roots expressing the Agrobacterium T-6b oncogene and the role of these compounds in 6b-induced growth. Mol Plant Microbe Interact 20:53–62

    Article  PubMed  CAS  Google Scholar 

  • Colombo E, Marine JC, Danovi D, Falini B, Pelicci PG (2002) Nucleophosmin regulates the stability and transcriptional activity of p53. Nat Cell Biol 4:529–533

    Article  PubMed  CAS  Google Scholar 

  • Colombo E, Bonetti P, Lazzerini Denchi E, Martinelli P, Zamponi R, Marine JC, Helin K, Falini B, Pelicci PG (2005) Nucleophosmin is required for DNA integrity and p19Arf protein stability. Mol Cell Biol 25:8874–8886

    Article  PubMed  CAS  Google Scholar 

  • Fatica A, Tollervey D (2002) Making ribosomes. Curr Opin Cell Biol 14:313–318

    Article  PubMed  CAS  Google Scholar 

  • Filipowicz W, Pogacic V (2002) Biogenesis of small nucleolar ribonucleoproteins. Curr Opin Cell Biol 14:319–327

    Article  PubMed  CAS  Google Scholar 

  • Gális I, Simek P, Van Onckelen HA, Kakiuchi Y, Wabiko H (2002) Resistance of transgenic tobacco seedlings expressing the Agrobacterium tumefaciens C58-6b gene, to growth-inhibitory levels of cytokinin is associated with elevated IAA levels and activation of phenylpropanoid metabolism. Plant Cell Physiol 43:939–950

    Article  PubMed  Google Scholar 

  • Garfinkel DJ, Simpson RB, Ream LW, White FF, Gordon MP, Nester EW (1981) Genetic analysis of crown gall: fine structure map of the T-DNA by site-directed mutagenesis. Cell 27:143–153

    Article  PubMed  CAS  Google Scholar 

  • Gierl A (1996) The En/Spm transposable element of maize. Curr Top Microbiol Immunol 204:145–159

    PubMed  CAS  Google Scholar 

  • Ginisty H, Sicard H, Roger B, Bouvet P (1999) Structure and functions of nucleolin. J Cell Sci 112:761–772

    PubMed  CAS  Google Scholar 

  • Grisendi S, Bernardi R, Rossi M, Cheng K, Khandker L, Manova K, Pandolfi PP (2005) Role of nucleophosmin in embryonic development and tumorigenesis. Nature 437:147–153

    Article  PubMed  CAS  Google Scholar 

  • Hooykaas PJJ, der Dulk-Ras H, Schilperoort RA (1988) The Agrobacterium tumefaciens T-DNA gene 6 b is an onc gene. Plant Mol Biol 11:791–794

    Article  CAS  Google Scholar 

  • Ishikawa M, Soyano T, Nishihama R, Machida Y (2002) The NPK1 mitogen-activated protein kinase kinase kinase contains a functional nuclear localization signal at the binding site for the NACK1 kinesin-like protein. Plant J 32:789–798

    Article  PubMed  CAS  Google Scholar 

  • Itahana K, Bhat KP, Jin A, Itahana Y, Hawke D, Kobayashi R, Zhang Y (2003) Tumor suppressor ARF degrades B23, a nucleolar protein involved in ribosome biogenesis and cell proliferation. Mol Cell 12:1151–1164

    Article  PubMed  CAS  Google Scholar 

  • Kakiuchi Y, Galis I, Tamogami S, Wabiko H (2006) Reduction of polar auxin transport in tobacco by the tumorigenic Agrobacterium tumefaciens AK-6b gene. Planta 223:237–247

    Article  PubMed  CAS  Google Scholar 

  • Kiss T (2002) Small nucleolar RNAs: an abundant group of noncoding RNAs with diverse cellular functions. Cell 109:145–148

    Article  PubMed  CAS  Google Scholar 

  • Kitakura S, Fujita T, Ueno Y, Terakura S, Wabiko H, Machida Y (2002) The protein encoded by oncogene 6b from Agrobacterium tumefaciens interacts with a nuclear protein of tobacco. Plant Cell 14:451–463

    Article  PubMed  CAS  Google Scholar 

  • Kojima H, Suzuki T, Kato T, Enomoto K, Sato S, Kato T, Tabata S, Saez-Vasquez J, Echeverria M, Nakagawa T, Ishiguro S, Nakamura K (2007) Sugar-inducible expression of the nucleolin-1 gene of Arabidopsis thaliana and its role in ribosome synthesis, growth and development. Plant J 49:1053–1063

    Article  PubMed  CAS  Google Scholar 

  • Lafontaine DL, Tollervey D (2001) The function and synthesis of ribosomes. Nat Rev 2:514–520

    Article  CAS  Google Scholar 

  • Leemans J, Deblaere R, Willmitzer L, Greve HD, Hernalsteens JP, Montagu MV, Schell J (1982) Genetic Identification of functions of TL-DNA transcripts in octopine crown galls. EMBO J 1:147–152

    PubMed  CAS  Google Scholar 

  • Levesque H, Delepelaire P, Rouzé P, Slightom J, Tepfer D (1988) Common evolutionary origin of the central portions of the Ri TL-DNA of Agrobacterium rhizogenes and the Ti T-DNAs of Agrobacterium tumefaciens. Plant Mol Biol 11:731–744

    Article  CAS  Google Scholar 

  • Morris RO (1986) Genes specifying auxin and cytokinin biosynthesis in phytopathogens. Annu Rev Plant Physiol 37:509–538

    Article  CAS  Google Scholar 

  • Nacken WK, Piotrowiak R, Saedler H, Sommer H (1991) The transposable element Tam1 from Antirrhinum majus shows structural homology to the maize transposon En/Spm and has no sequence specificity of insertion. Mol Gen Genet 228:201–208

    Article  PubMed  CAS  Google Scholar 

  • Nishihama R, Ishikawa M, Araki S, Soyano T, Asada T, Machida Y (2001) The NPK1 mitogen-activated protein kinase kinase kinase is a regulator of cell-plate formation in plant cytokinesis. Genes Dev 15:352–363

    Article  PubMed  CAS  Google Scholar 

  • Okada M, Jang SW, Ye K (2007) Ebp1 association with nucleophosmin/B23 is essential for regulating cell proliferation and suppressing apoptosis. J Biol Chem 282:36744–36754

    Article  PubMed  CAS  Google Scholar 

  • Okuwaki M, Matsumoto K, Tsujimoto M, Nagata K (2001) Function of nucleophosmin/B23, a nucleolar acidic protein, as a histone chaperone. FEBS Lett 506:272–276

    Article  PubMed  CAS  Google Scholar 

  • Olson MO, Dundr M, Szebeni A (2000) The nucleolus: an old factory with unexpected capabilities. Trends Cell Biol 10:189–196

    Article  PubMed  CAS  Google Scholar 

  • Otten L, De Ruffray P (1994) Agrobacterium vitis nopaline Ti plasmid pTiAB4: relationship to other Ti plasmids and T-DNA structure. Mol Gen Genet 245:493–505

    Article  PubMed  CAS  Google Scholar 

  • Petricka JJ, Nelson TM (2007) Arabidopsis nucleolin affects plant development and patterning. Plant Physiol 144:173–186

    Article  PubMed  CAS  Google Scholar 

  • Pontvianne F, Matia I, Douet J, Tourmente S, Medina FJ, Echeverria M, Saez-Vasquez J (2007) Characterization of AtNUC-L1 reveals a central role of nucleolin in nucleolus organization and silencing of AtNUC-L2 gene in Arabidopsis. Mol Biol Cell 18:369–379

    Article  PubMed  CAS  Google Scholar 

  • Raina R, Schlappi M, Karunanandaa B, Elhofy A, Fedoroff N (1998) Concerted formation of macromolecular suppressor–mutator transposition complexes. Proc Natl Acad Sci USA 95:8526–8531

    Article  PubMed  CAS  Google Scholar 

  • Ream LW, Gordon MP, Nester EW (1983) Multiple mutations in the T region of the Agrobacterium tumefaciens tumor-inducing plasmid. Proc Natl Acad Sci USA 80:1660–1664

    Article  PubMed  CAS  Google Scholar 

  • Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, New York, pp 18.48–18.54

    Google Scholar 

  • Scheer U, Hock R (1999) Structure and function of the nucleolus. Curr Opin Cell Biol 11:385–390

    Article  PubMed  CAS  Google Scholar 

  • Schmidt-Zachmann MS, Franke WW (1988) DNA cloning and amino acid sequence determination of a major constituent protein of mammalian nucleoli. Correspondence of the nucleoplasmin-related protein NO38 to mammalian protein B23. Chromosoma 96:417–426

    Article  PubMed  CAS  Google Scholar 

  • Schmidt-Zachmann MS, Hugle-Dorr B, Franke WW (1987) A constitutive nucleolar protein identified as a member of the nucleoplasmin family. EMBO J 6:1881–1890

    PubMed  CAS  Google Scholar 

  • Soyano T, Nishihama R, Morikiyo K, Ishikawa M, Machida Y (2003) NQK1/NtMEK1 is a MAPKK that acts in the NPK1 MAPKKK-mediated MAPK cascade and is required for plant cytokinesis. Genes Dev 17:1055–1067

    Article  PubMed  CAS  Google Scholar 

  • Spanier K, Schell J, Schreier PH (1989) A functional analysis of T-DNA gene 6b: the fine tuning of cytokinin effects on shoot development. Mol Gen Genet 219:209–216

    Article  PubMed  CAS  Google Scholar 

  • Spena A, Schmulling T, Koncz C, Schell JS (1987) Independent and synergistic activity of rol A, B and C loci in stimulating abnormal growth in plants. EMBO J 6:3891–3899

    PubMed  CAS  Google Scholar 

  • Srivastava M, Pollard HB (1999) Molecular dissection of nucleolin’s role in growth and cell proliferation: new insights. FASEB J 13:1911–1922

    PubMed  CAS  Google Scholar 

  • Stieger PA, Meyer AD, Kathmann P, Frundt C, Niederhauser I, Barone M, Kuhlemeier C (2004) The orf13 T-DNA gene of Agrobacterium rhizogenes confers meristematic competence to differentiated cells. Plant Physiol 135:1798–1808

    Article  PubMed  CAS  Google Scholar 

  • Sugimoto M, Kuo ML, Roussel MF, Sherr CJ (2003) Nucleolar Arf tumor suppressor inhibits ribosomal RNA processing. Mol Cell 11:415–424

    Article  PubMed  CAS  Google Scholar 

  • Terakura S, Kitakura S, Ishikawa M, Ueno Y, Fujita T, Machida C, Wabiko H, Machida Y (2006) Oncogene 6b from Agrobacterium tumefaciens induces abaxial cell division at late stages of leaf development and modifies vascular development in petioles. Plant Cell Physiol 47:664–672

    Article  PubMed  CAS  Google Scholar 

  • Terakura S, Ueno Y, Tagami H, Kitakura S, Machida C, Wabiko H, Aiba H, Otten L, Tsukagoshi H, Nakamura K, Machida Y (2007) An oncoprotein from the plant pathogen Agrobacterium has histone chaperone like activity. Plant Cell 19:2855–2865

    Article  PubMed  CAS  Google Scholar 

  • Tinland B, Rohfritsch O, Michler P, Otten L (1990) Agrobacterium tumefaciens T-DNA gene 6b stimulates rol-induced root formation, permits growth at high auxin concentrations and increases root size. Mol Gen Genet 223:1–10

    Article  PubMed  CAS  Google Scholar 

  • Tinland B, Fournier P, Heckel T, Otten L (1992) Expression of a chimaeric heat-shock-inducible Agrobacterium 6b oncogene in Nicotiana rustica. Plant Mol Biol 18:921–930

    Article  PubMed  CAS  Google Scholar 

  • Tuteja R, Tuteja N (1998) Nucleolin: a multifunctional major nucleolar phosphoprotein. Crit Rev Biochem Mol Biol 33:407–436

    Article  PubMed  CAS  Google Scholar 

  • Vojtek AB, Hollenberg SM, Cooper JA (1993) Mammalian Ras interacts directly with the serine/threonine kinase Raf. Cell 74:205–214

    Article  PubMed  CAS  Google Scholar 

  • Wabiko H, Minemura M (1996) Exogenous phytohormone-independent growth and regeneration of tobacco plants transgenic for the 6b gene of Agrobacterium tumefaciens AKE10. Plant Physiol 112:939–951

    Article  PubMed  CAS  Google Scholar 

  • Willmitzer L, Dhaese P, Schreier PH, Schmalenbach W, Van Montagu M, Schell J (1983) Size, location and polarity of T-DNA-encoded transcripts in nopaline crown gall tumors; common transcripts in octopine and nopaline tumors. Cell 32:1045–1056

    Article  PubMed  CAS  Google Scholar 

  • Yu Y, Maggi LB Jr, Brady SN, Apicelli AJ, Dai MS, Lu H, Weber JD (2006) Nucleophosmin is essential for ribosomal protein L5 nuclear export. Mol Cell Biol 26:3798–3809

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Professor Kenzo Nakamura (Nagoya University) for providing GFP-nucleolin and Dr. Yoshihisa Ueno (Nagoya University) for helpful discussion. This work was supported, in part, by a grant from the Program for Promotion of Basic Research Activities for Innovative Biosciences (Japan) and by Grants-in-Aid for Scientific Research on Priority Areas (nos. 10182102, 14036216, and 15028208) from the Ministry of Education, Science, Culture and Sport (Japan). S.T. was supported by a grant of the twenty-first century COE program for Division of Biological Science, Nagoya University, and a research fellowship from the Japan Society for the Promotion of Science for Young Scientists.

Author information

Authors and Affiliations

  1. College of Bioscience and Biotechnology, Chubu University, 1200 Matsumoto-cho, Kasugai, Aichi, 487-8501, Japan

    Saeko Kitakura & Chiyoko Machida

  2. Division of Biological Science, Graduate School of Science, Nagoya University, Furo-cho, Chikusa-ku, Nagoya, Aichi, 464-8602, Japan

    Saeko Kitakura, Shinji Terakura, Yasushi Yoshioka & Yasunori Machida

Authors
  1. Saeko Kitakura
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shinji Terakura
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yasushi Yoshioka
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Chiyoko Machida
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yasunori Machida
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yasunori Machida.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kitakura, S., Terakura, S., Yoshioka, Y. et al. Interaction between Agrobacterium tumefaciens oncoprotein 6b and a tobacco nucleolar protein that is homologous to TNP1 encoded by a transposable element of Antirrhinum majus . J Plant Res 121, 425–433 (2008). https://doi.org/10.1007/s10265-008-0160-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10265-008-0160-1

Keywords

Search

Navigation