Advertisement

Plant Molecular Biology

, Volume 56, Issue 6, pp 973–985 | Cite as

A hypersensitive response-induced ATPase associated with various cellular activities (AAA) protein from tobacco plants

  • Megumi Sugimoto
  • Yube Yamaguchi
  • Kimiyo Nakamura
  • Yuko Tatsumi
  • Hiroshi Sano
Article

Abstract

The hypersensitive response (HR) is one of the most critical defense systems in higher plants. In order to understand its molecular basis, we have screened tobacco genes that are transcriptionally activated during the early stage of the HR by the differential display method. Among six genes initially identified, one was found encoding a 57 kDa polypeptide with 497 amino acids not showing significant similarity to any reported proteins except for the AAA domain (ATPase associated with various cellular activities) spanning over 230 amino acids. The bacterially expressed protein exhibited ATP hydrolysis activity, and a green fluorescent protein-fusion protein localized in the cytoplasm of onion epidermis cells. The protein was subsequently designated as NtAAA1 (Nicotiana tabacum AAA1). NtAAA1 transcripts were induced 6 h after HR onset not only by TMV but also by incompatiblePsuedomonas syringae, indicating that NtAAA1 is under the control of the N-gene with a common role in pathogen responses. Expression of NtAAA1 was induced by jasmonic acid and ethylene, but not by salicylic acid (SA). It also occurred at a high level in SA-deficient tobacco plants upon TMV infection. When NtAAA1 was silenced by the RNAi method, accumulation of transcripts for PR-1a significantly increased during the HR. Treatments with SA induced higher expression of PR-1a and acidic PR-2 in RNAi transgenic plants than in wild-type counterparts. These results suggest that NtAAA1 mitigates the SA signaling pathway, and therefore that NtAAA1 modulates the pathogen response of the host plants by adjusting the HR to an appropriate level.

Keywords

AAA-protein ATPase hypersensitive response Nicotiana tabacum salicylic acid 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Abbink, T.E.M., Peart, J.R., Mos, T.N.M., Baulcombe, D.C., Bol, J.F., Linthorst, H.J.M. 2002Silencing of a gene encoding a protein component of the oxygen-evolving complex of photosystem II enhances virus replication in plantsVirology295307319Google Scholar
  2. Barroso, C., Vega, J.M., Gotor, C. 1995A new member of the cytosolic O-acetylserine (thiol) lyase gene family in Arabidopsis thalianaFEBS Lett.36315Google Scholar
  3. Beyer, A. 1997Sequence analysis of the AAA protein familyProtein Sci.620432058Google Scholar
  4. Bradford, M.M. 1976A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of dye-bindingAnal. Biochem.72248254CrossRefPubMedGoogle Scholar
  5. Chomczynski, P., Sacchi, N. 1987Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extractionAnal. Biochem.162156159CrossRefPubMedGoogle Scholar
  6. Dyer, W.E., Henstrand, J.M., Handa, A.K., Herrmann, K.M. 1989Wounding induces the first enzyme of the shikimate pathway in SolanaceaeProc. Natl. Acad. Sci. USA8973707373Google Scholar
  7. Felton, G.W., Korth, K.L. 2000Trade-offs between pathogen and herbivore resistanceCurr. Opin. Plant Biol.3309314Google Scholar
  8. Frohlich, K.-U. 2001An AAA family treeJ. Cell Sci.11416011602Google Scholar
  9. Fu, H., Doelling, J.H., Rubin, D.M., Vierstra, R.D. 1999Structural and functional analysis of the six regulatory particle triple-A ATPase subunits from the Arabidopsis 26S proteasomePlant J.18529539Google Scholar
  10. Hammond-Kosack, K.E., Jones, J.D.G. 1996Resistance gene-dependent plant defense responsesPlant Cell817731791CrossRefPubMedGoogle Scholar
  11. Holmes, F.O. 1938Inheritance of resistance to tobacco-mosaic disease in tobaccoPhytopathology28553561Google Scholar
  12. Iyer, L.M., Leipe, D.D., Koonin, E.V., Aravind, L. 2004Evolutionary history and higher order classification of AAA+ ATPasesJ. Struct. Biol.1461131Google Scholar
  13. Leonhard, K., Stieglar, A., Neupert, W., Langer, T. 1999Chaperone-like activity of the AAA domain of the yeast Yme1 AAA proteaseNature398348351PubMedGoogle Scholar
  14. Lindahl, M., Tabak, S., Cseke, L., Pichersky, E., Andersson, B., Adam, Z. 1996Identification, characterization, and molecular cloning of a homologue of the bacterial FtsH protease in chloroplasts of higher plantsJ. Biol. Chem.2712932929334Google Scholar
  15. Lupas, A.N., Martin, J. 2002AAA proteinsCurr. Opin. Struct. Biol.12746753Google Scholar
  16. Mandujano-Chávez, A., Schoenbeck, M.A., Ralston, L.F., Lozova-Gloria, E., Chappell, J. 2000Differential induction of sesquiterpene metabolism in tobacco cell suspension cultures by methyl jasmonate and fungal elicitorArch. Biochem. Biophys.381285294Google Scholar
  17. Matsuoka, M., Yamamoto, N., Kano-Murakami, Y., Tanaka, Y., Ozeki, Y., Hirano, H., Kagawa, H., Oshima, M., Ohashi, Y. 1987Classification and structural comparison of full-length cDNAs for pathogenesis-related proteinsPlant Physiol.85942946Google Scholar
  18. Murray, M.G., Thompson, W.F. 1980Rapid isolation of high molecular weight plant DNANucleic Acids Res.843214325Google Scholar
  19. Nishiguchi, M., Yoshida, K., Sumizono, T., Tazaki, K. 2002A receptor-like protein kinase with a lectin-like domain from lombardy poplar: gene expression in response to wounding and characterization of phosphorylation activityMol. Gene. Genom.267506514Google Scholar
  20. Olsen, L.J. 1998The surprising complexity of peroxisome biogenesisPlant Mol. Biol.38163189Google Scholar
  21. Patel, S., Latterich, M. 1998The AAA team: related ATPases with diverse functionsTrends Cell Biol.86571Google Scholar
  22. Perlin, D.S., Spanswick, R.M. 1981Characterization of ATPase activity associated with corn leaf plasma membranesPlant Physiol.68521526Google Scholar
  23. Ponstein, A.S., Bres-Vloemans, S.A., Sela-Buurlage, M.B., Elzen, P.J.M., Melchers, L.S., Cornlissen, B.J.C. 1994A novel pathogen- and wound-inducible tobacco (Nicotiana tabacum) protein with antifungal activityPlant Physiol.104109118Google Scholar
  24. Rancour, D.M, Dickey, C.E., Park, S., Bednarek, S.Y. 2002Characterization of AtCDC48. Evidence for multiple membrane fusion mechanisms at the plane of cell division in plantsPlant Physiol.13012411253Google Scholar
  25. Ryals, J.A., Neuenschwander, U.H., Willits, M.G., Molina, A., Steiner, H.Y., Hunt, M.D. 1996Systemic acquired resistancePlant Cell818091819CrossRefPubMedGoogle Scholar
  26. Seo, S., Okamoto, M., Iwai, T., Iwano, M., Fukui, K., Isogai, A., Nakajima, N., Ohashi, Y. 2000Reduced level of chloroplast FtsH protein in tobacco mosaic virus-infected tobacco leaves accelerate the hypersensitive reactionPlant Cell12917932Google Scholar
  27. Ueda, A., Shi, W., Sanmiya, K., Shono, M., Takebe, T. 2001Functional analysis of salt-inducible proline transporter of barley rootsPlant Cell Physiol.4212821289Google Scholar
  28. Vale, R.D. 2000AAA proteins: lords of the ringJ. Cell Biol.150F13F19Google Scholar
  29. Wang, Y., Herrmann, K.M., Weller, S.C., Goldsbrough, P.B. 1991Cloning and nucleotide sequence of a complementary DNA encoding 3-deoxy-D-arabino- heptulosonate 7-phosphate synthase from tobaccoPlant Physiol.97847848Google Scholar
  30. Wesley, S.V., Halliwell, C.A., Smith, N.A., Wang, M., Rouse, D.T., Liu, Q., Gooding, P.S., Singh, S.P., Abbott, D., Stoutjesdijk, P.A., Robinson, S.P., Gleave, A.P., Green, A.G., Waterhouse, P.M. 2001Construct design for efficient, effective and highthroughput gene silencing in plantsPlant J.27581590Google Scholar
  31. Weststeijn, E.A. 1981Lesion growth and virus localization in leaves of Nicotiana tabacum cv. Xanthi nc. after inoculation with tobacco mosaic virus and incubation alternately at 22 °C and 32 °CPhysiol. Plant Pathol.18357368Google Scholar
  32. Yamaguchi, Y., Yoda, H., Akiyama, K., Sano, H. 2003Induction of transcripts encoding a novel seven-transmembrane protein during the hypersensitive response to tobacco mosaic virus infection in tobacco plantsPlanta218249253Google Scholar
  33. Yap, Y.-K., Kakamu, K., Yamaguchi, Y., Koizumi, N., Sano, H. 2002Promoter analysis of WIPK, a gene encoding a tobacco MAP kinase, with reference to wounding and tobacco mosaic virus infectionJ. Plant Physiol.1597783Google Scholar
  34. Yoda, H., Ogawa, M., Yamaguchi, Y., Koizumi, N., Kusano, T., Sano, H. 2002Identification of early-responsive genes associated with the hypersensitive response to tobacco mosaic virus and characterization of a WRKY-type transcription factor in tobacco plantsMol. Genet. Genom.267154161Google Scholar
  35. Yoda, H., Yamaguchi, Y., Sano, H. 2003Induction of hypersensitive cell death by hydrogen peroxide produced through polyamine degradation in tobacco plantsPlant Physiol.13219731981Google Scholar
  36. Yoshida, K.T., Naito, S., Takeda, G. 1994cDNA cloning of regeneration specific genes in rice by differential screening of randomly amplified cDNAs using PAPD primersPlant Cell. Physiol.3510031009Google Scholar

Copyright information

© Springer 2005

Authors and Affiliations

  • Megumi Sugimoto
    • 1
    • 2
  • Yube Yamaguchi
    • 1
    • 3
  • Kimiyo Nakamura
    • 1
  • Yuko Tatsumi
    • 1
  • Hiroshi Sano
    • 1
  1. 1.Research and Education Center for Genetic InformationNara Institute of Science and TechnologyNaraJapan
  2. 2.Research Institute for BioresourcesOkayama UniversityOkayamaJapan
  3. 3.Institute of Biological ChemistryWashington State UniversityPullmanUSA

Personalised recommendations