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.
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T.E.M. Abbink J.R. Peart T.N.M. Mos D.C. Baulcombe J.F. Bol H.J.M. Linthorst (2002) ArticleTitleSilencing of a gene encoding a protein component of the oxygen-evolving complex of photosystem II enhances virus replication in plants Virology 295 307–319
C. Barroso J.M. Vega C. Gotor (1995) ArticleTitleA new member of the cytosolic O-acetylserine (thiol) lyase gene family in Arabidopsis thaliana FEBS Lett. 363 1–5
A. Beyer (1997) ArticleTitleSequence analysis of the AAA protein family Protein Sci. 6 2043–2058
M.M. Bradford (1976) ArticleTitleA rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of dye-binding Anal. Biochem. 72 248–254 Occurrence Handle10.1006/abio.1976.9999 Occurrence Handle1:CAS:528:DyaE28XksVehtrY%3D Occurrence Handle942051
P. Chomczynski N. Sacchi (1987) ArticleTitleSingle-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction Anal. Biochem. 162 156–159 Occurrence Handle10.1006/abio.1987.9999 Occurrence Handle1:CAS:528:DyaL2sXitFSns7Y%3D Occurrence Handle2440339
W.E. Dyer J.M. Henstrand A.K. Handa K.M. Herrmann (1989) ArticleTitleWounding induces the first enzyme of the shikimate pathway in Solanaceae Proc. Natl. Acad. Sci. USA 89 7370–7373
G.W. Felton K.L. Korth (2000) ArticleTitleTrade-offs between pathogen and herbivore resistance Curr. Opin. Plant Biol. 3 309–314
K.-U. Frohlich (2001) ArticleTitleAn AAA family tree J. Cell Sci. 114 1601–1602
H. Fu J.H. Doelling D.M. Rubin R.D. Vierstra (1999) ArticleTitleStructural and functional analysis of the six regulatory particle triple-A ATPase subunits from the Arabidopsis 26S proteasome Plant J. 18 529–539
K.E. Hammond-Kosack J.D.G. Jones (1996) ArticleTitleResistance gene-dependent plant defense responses Plant Cell 8 1773–1791 Occurrence Handle10.1105/tpc.8.10.1773 Occurrence Handle1:CAS:528:DyaK28Xmsl2mtbY%3D Occurrence Handle8914325
F.O. Holmes (1938) ArticleTitleInheritance of resistance to tobacco-mosaic disease in tobacco Phytopathology 28 553–561
L.M. Iyer D.D. Leipe E.V. Koonin L. Aravind (2004) ArticleTitleEvolutionary history and higher order classification of AAA+ ATPases J. Struct. Biol. 146 11–31
K. Leonhard A. Stieglar W. Neupert T. Langer (1999) ArticleTitleChaperone-like activity of the AAA domain of the yeast Yme1 AAA protease Nature 398 348–351 Occurrence Handle1:CAS:528:DyaK1MXitlCkuro%3D Occurrence Handle10192337
M. Lindahl S. Tabak L. Cseke E. Pichersky B. Andersson Z. Adam (1996) ArticleTitleIdentification, characterization, and molecular cloning of a homologue of the bacterial FtsH protease in chloroplasts of higher plants J. Biol. Chem. 271 29329–29334
A.N. Lupas J. Martin (2002) ArticleTitleAAA proteins Curr. Opin. Struct. Biol. 12 746–753
A. Mandujano-Chávez M.A. Schoenbeck L.F. Ralston E. Lozova-Gloria J. Chappell (2000) ArticleTitleDifferential induction of sesquiterpene metabolism in tobacco cell suspension cultures by methyl jasmonate and fungal elicitor Arch. Biochem. Biophys. 381 285–294
M. Matsuoka N. Yamamoto Y. Kano-Murakami Y. Tanaka Y. Ozeki H. Hirano H. Kagawa M. Oshima Y. Ohashi (1987) ArticleTitleClassification and structural comparison of full-length cDNAs for pathogenesis-related proteins Plant Physiol. 85 942–946
M.G. Murray W.F. Thompson (1980) ArticleTitleRapid isolation of high molecular weight plant DNA Nucleic Acids Res. 8 4321–4325
M. Nishiguchi K. Yoshida T. Sumizono K. Tazaki (2002) ArticleTitleA receptor-like protein kinase with a lectin-like domain from lombardy poplar: gene expression in response to wounding and characterization of phosphorylation activity Mol. Gene. Genom. 267 506–514
L.J. Olsen (1998) ArticleTitleThe surprising complexity of peroxisome biogenesis Plant Mol. Biol. 38 163–189
S. Patel M. Latterich (1998) ArticleTitleThe AAA team: related ATPases with diverse functions Trends Cell Biol. 8 65–71
D.S. Perlin R.M. Spanswick (1981) ArticleTitleCharacterization of ATPase activity associated with corn leaf plasma membranes Plant Physiol. 68 521–526
A.S. Ponstein S.A. Bres-Vloemans M.B. Sela-Buurlage P.J.M. Elzen Particlevan den L.S. Melchers B.J.C. Cornlissen (1994) ArticleTitleA novel pathogen- and wound-inducible tobacco (Nicotiana tabacum) protein with antifungal activity Plant Physiol. 104 109–118
D.M Rancour C.E. Dickey S. Park S.Y. Bednarek (2002) ArticleTitleCharacterization of AtCDC48. Evidence for multiple membrane fusion mechanisms at the plane of cell division in plants Plant Physiol. 130 1241–1253
J.A. Ryals U.H. Neuenschwander M.G. Willits A. Molina H.Y. Steiner M.D. Hunt (1996) ArticleTitleSystemic acquired resistance Plant Cell 8 1809–1819 Occurrence Handle10.1105/tpc.8.10.1809 Occurrence Handle1:CAS:528:DyaK28Xmsl2murw%3D Occurrence Handle12239363
S. Seo M. Okamoto T. Iwai M. Iwano K. Fukui A. Isogai N. Nakajima Y. Ohashi (2000) ArticleTitleReduced level of chloroplast FtsH protein in tobacco mosaic virus-infected tobacco leaves accelerate the hypersensitive reaction Plant Cell 12 917–932
A. Ueda W. Shi K. Sanmiya M. Shono T. Takebe (2001) ArticleTitleFunctional analysis of salt-inducible proline transporter of barley roots Plant Cell Physiol. 42 1282–1289
R.D. Vale (2000) ArticleTitleAAA proteins: lords of the ring J. Cell Biol. 150 F13–F19
Y. Wang K.M. Herrmann S.C. Weller P.B. Goldsbrough (1991) ArticleTitleCloning and nucleotide sequence of a complementary DNA encoding 3-deoxy-D-arabino- heptulosonate 7-phosphate synthase from tobacco Plant Physiol. 97 847–848
S.V. Wesley C.A. Halliwell N.A. Smith M. Wang D.T. Rouse Q. Liu P.S. Gooding S.P. Singh D. Abbott P.A. Stoutjesdijk S.P. Robinson A.P. Gleave A.G. Green P.M. Waterhouse (2001) ArticleTitleConstruct design for efficient, effective and highthroughput gene silencing in plants Plant J. 27 581–590
E.A. Weststeijn (1981) ArticleTitleLesion 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 °C Physiol. Plant Pathol. 18 357–368
Y. Yamaguchi H. Yoda K. Akiyama H. Sano (2003) ArticleTitleInduction of transcripts encoding a novel seven-transmembrane protein during the hypersensitive response to tobacco mosaic virus infection in tobacco plants Planta 218 249–253
Y.-K. Yap K. Kakamu Y. Yamaguchi N. Koizumi H. Sano (2002) ArticleTitlePromoter analysis of WIPK, a gene encoding a tobacco MAP kinase, with reference to wounding and tobacco mosaic virus infection J. Plant Physiol. 159 77–83
H. Yoda M. Ogawa Y. Yamaguchi N. Koizumi T. Kusano H. Sano (2002) ArticleTitleIdentification of early-responsive genes associated with the hypersensitive response to tobacco mosaic virus and characterization of a WRKY-type transcription factor in tobacco plants Mol. Genet. Genom. 267 154–161
H. Yoda Y. Yamaguchi H. Sano (2003) ArticleTitleInduction of hypersensitive cell death by hydrogen peroxide produced through polyamine degradation in tobacco plants Plant Physiol. 132 1973–1981
K.T. Yoshida S. Naito G. Takeda (1994) ArticleTitlecDNA cloning of regeneration specific genes in rice by differential screening of randomly amplified cDNAs using PAPD primers Plant Cell. Physiol. 35 1003–1009
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Sugimoto, M., Yamaguchi, Y., Nakamura, K. et al. A hypersensitive response-induced ATPase associated with various cellular activities (AAA) protein from tobacco plants. Plant Mol Biol 56, 973–985 (2004). https://doi.org/10.1007/s11103-004-6459-y
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DOI: https://doi.org/10.1007/s11103-004-6459-y