Abstract
We previously proposed that a spermine (Spm)-mediated signal transduction pathway is involved in the hypersensitive response induced by Tobacco mosaic virus (TMV) in tobacco plants. To identify regulatory component(s) of this pathway, we surveyed a tobacco cDNA library and found that the ZFT1 gene, which encodes a Cys2/His2 type zinc-finger protein, is Spm-responsive. ZFT1 was not induced by two other polyamines, putrescine and spermidine, or by salicylic acid (SA), jasmonic acid or ethylene. Furthermore, ZFT1 was upregulated in TMV- inoculated tobacco plants in an N gene-dependent manner. Notably, induction of ZFT1 by Spm and by TMV infection was unimpaired in NahG-transgenic tobacco plants, indicating that cross-talk with an SA signaling pathway is not involved in this response. Within the Spm-signaling pathway, we found that ZFT1 functioned downstream of both mitochondrial dysfunction and mitogen-activated protein kinase activation. The ZFT1 protein has two zinc finger motifs and shows a high degree of similarity to ZPT2-3 in petunia and SCOF1 in soybean. However, unlike the latter two proteins, ZFT1 binds to the EP1S sequence and functions as a transcription repressor. Moreover, interestingly, ZFT1 overexpression rendered tobacco plants more tolerant to TMV. Based on the results presented here, we propose that ZFT1 functions as a transcription repressor in a Spm signaling pathway, thereby accelerating necrotic local region formation in tobacco leaves.
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References
T. Berberich H. Sano T. Kusano (1999) ArticleTitleInvolvement of a MAP kinase, ZmMPK5, in senescence and recovery from low-temperature stress in maize Mol. Gen. Genet. 262 534–542 Occurrence Handle10.1007/s004380051115 Occurrence Handle10589842
A. Bouchereau A. Aziz F. Larher J. Martin-Tanguy (1999) ArticleTitlePolyamines and environmental challenges: recent development Plant Sci. 140 103–125 Occurrence Handle10.1016/S0168-9452(98)00218-0
Z. Chen J. Malamy J. Henning U. Conrath P. Sanchez-Casa H. Silva J. Ricigliano D.F. Klessig (1995) ArticleTitleInduction, modification, and transduction of the salicylic acid signal in plant defense responses Proc. Natl. Acad. Sci. USA 92 4134–4137 Occurrence Handle11607539
A.R. Krol Particlevan der R.M. Poecke Particlevan O.F. Vorst C. Voogt W. Leeuwen Particlevan T.W. Borst-Vrensen H. Takatsuji L.H. Plas Particlevan der (1999) ArticleTitleDevelopment and wound-, cold-, desiccation-, ultraviolet-B-stress-induced modulations in the expression of the petunia zinc finger transcription factor gene, ZPT2-2 Plant Physiol. 121 1153–1162 Occurrence Handle10.1104/pp.121.4.1153 Occurrence Handle10594102
X. Dong (1998) ArticleTitleSA, JA, ethylene, and disease resistance in plants Curr. Opin. Plant Biol. 1 316–323 Occurrence Handle10.1016/1369-5266(88)80053-0 Occurrence Handle10066607
F. Frugier S. Poirier B. Satiat-Jeunemaitre A. Kondorosi M. Crespi (2000) ArticleTitleA Krüppel-like zinc finger protein is involved in nitrogen-fixing root nodule organogenesis Genes Dev. 14 475–482 Occurrence Handle10691739
D.R. Gallie D.E. Sleat J.W. Watts P.C. Turner T.M.A. Wilson (1987) ArticleTitleThe 5-leader sequence of tobacco mosaic virus RNA enhances the expression of foreign gene transcripts in vitro and in vivo Nucleic Acid. Res. 15 3257–3273 Occurrence Handle3575095
S. Hiraga H. Ito K. Sasaki H. Yamakawa I. Mitsuhara H. Toshima H. Matsui M. Honma Y. Ohashi (2000a) ArticleTitleWound-induced expression of a tobacco peroxidase is not enhanced by ethephon and suppressed by methyl jasmonate and coronatine Plant Cell Physiol. 41 165–170
S. Hiraga H. Ito H. Yamakawa N. Ohtsubo S. Seo I. Mitsuhara H. Matsui M. Honma Y. Ohashi (2000b) ArticleTitleAn HR-induced tobacco peroxidase gene is responsive to spermine, but not to salicylate, methyl jasmonate, and ethephon Mol. Plant-Microbe Interact. 13 210–216
K. Hiratsu M. Ohta K. Matsui M. Ohme-Takagi (2002) ArticleTitleThe SUPERMAN protein is an active repressor whose carboxy-terminal repression domain is required for the development of normal flowers FEBS Lett. 514 351–354 Occurrence Handle10.1016/S0014-5793(02)02435-3 Occurrence Handle11943180
A. Iida T. Kazuoka S. Torikai. H. Kikuchi K. Oeda (2000) ArticleTitleA zinc finger protein RHL41 mediates the light acclimation response in Arabidopsis Plant J. 24 191–203 Occurrence Handle10.1046/j.1365-313x.2000.00864.x Occurrence Handle11069694
C. Isernia E. Bucci M. Leone L. Zaccaro P. Lello ParticleDi G. Digilio S. Esposito M. Saviano B. Blasio ParticleDi C. Pedone P.V. Pedone R. Fattorusso (2003) ArticleTitleNMR structure of the single QALGGH zinc finger domain from the Arabidopsis thaliana SUPERMAN protein Chembiochem 4 171–180 Occurrence Handle10.1002/cbic.200390028 Occurrence Handle12616630
J.C. Kim S.H. Lee Y.H. Cheong C.-M. Yoo S.I. Lee H.J. Chun D.-J. Yun J.C. Hong S.Y. Lee C.O. Lim M.J. Cho (2001) ArticleTitleA novel cold-inducible zinc finger protein from soybean, SCOF-1, enhances cold tolerance in transgenic plants Plant J. 25 247–259 Occurrence Handle10.1046/j.1365-313x.2001.00947.x Occurrence Handle11208017
S.H. Kim J.K. Hong S.C. Lee K.H. Sohn H.W. Jung B.K. Hwang (2004) ArticleTitleCAZFP1, Cys2/His2-type zinc-finger transcription factor gene functions as a pathogen-induced early-defense gene in Capsium annuum Plant Mol. Biol. 55 883–904 Occurrence Handle15604723
D.F. Klessig J. Malamy (1994) ArticleTitleThe salicylic acid signal in plants Plant Mol. Biol. 26 1439–1458 Occurrence Handle10.1007/BF00016484 Occurrence Handle7858199
K. Kubo A. Sakamoto A. Kobayashi Z. Rybka Y. Kanno H. Nakagawa H. Takatsuji (1998) ArticleTitleCys2/His2 zinc-finger protein family of petunia: evolution and general mechanism of target-sequence recognition Nucleic Acid. Res. 26 608–615 Occurrence Handle10.1093/nar/26.2.608 Occurrence Handle9421523
A. Kumar T. Altabella M. Taylor A.F. Tiburcio (1997) ArticleTitleRecent advances in polyamine research Trends Plant Sci. 2 124–130 Occurrence Handle10.1016/S1360-1385(97)01013-3
V. Lippuner M.S. Cyert C.S. Gasser (1996) ArticleTitleTwo classes of plant cDNA clones differentially complement yeast calcineurin mutants and increase salt tolerance of wild-type yeast J. Biol. Chem. 271 12859–12866 Occurrence Handle10.1074/jbc.271.22.12859 Occurrence Handle8662738
R.L. Malmberg M.B. Watson G.L. Galloway W. Yu (1998) ArticleTitleMolecular genetic analysis of plant polyamines Crit. Rev. Plant Sci. 17 199–224 Occurrence Handle10.1016/S0735-2689(98)00358-X
R. Marathe Z. Guan R. Anandalakshmi H. Zhao S.P. Dinesh-Kumar (2004) ArticleTitleStudy of Arabidopsis thaliana resistome in response to cucumber mosaic virus infection using whole genome microarray Plant Mol. Biol. 55 501–520 Occurrence Handle10.1007/s11103-004-0439-0 Occurrence Handle15604696
H. Matsumura S. Reich A. Ito H. Saitoh S. Kamoun P. Winter G. Kahl M. Reuter D.H. Krüger R. Terauchi (2003) ArticleTitleGene expression analysis of plant host-pathogen interactions by SuperSAGE Proc. Natl. Acad. Sci. USA 100 15718–15723 Occurrence Handle10.1073/pnas.2536670100 Occurrence Handle14676315
R. Meissner A.J. Michael (1997) ArticleTitleIsolation and characterization of a diverse family of Arabidopsis two and three-fingered C2H2 zinc finger protein genes and cDNAs Plant Mol. Biol. 33 615–624 Occurrence Handle10.1023/A:1005746803089 Occurrence Handle9132053
F. Nagy S.A. Kay N.-H. Chua (1988) Analysis of gene expression in transgenic plants S.B. Gelvin R.A. Schilperoort (Eds) Plant Molecular Biology Manual Kluwer Academic Publishers Dordrecht 1–29
M. Ohta K. Matsui K. Hiratsu H. Shinshi M. Ohta-Takagi (2001) ArticleTitleRepression domains of class II ERF transcriptional repressors share an essential motif for active repression Plant Cell 13 1959–1968 Occurrence Handle10.1105/tpc.13.8.1959 Occurrence Handle11487705
D. Pontier L. Godiard Y. Marco D. Roby (1994) ArticleTitlehsr203J, a tobacco gene whose activation is rapid, highly localized and specific for incompatible plant/pathogen interactions Plant J. 5 507–521 Occurrence Handle8012404
A. Sakamoto M. Minami G.H. Huh M. Iwabuchi (1993) ArticleTitleThe putative zinc-finger protein WZF1 interacts with a cis-acting element of wheat histone genes Eur. J. Biochem. 217 1049–1056 Occurrence Handle10.1111/j.1432-1033.1993.tb18336.x Occurrence Handle8223628
H. Sakamoto K. Maruyama Y. Sakuma T. Meshi M. Iwabuchi K. Shinozaki K. Yamaguchi-Shinozaki (2004) ArticleTitleArabidopsis Cys2/His2-type zinc-finger proteins function as transcription repressors under drought, cold, and high-salinity stress conditions Plant Physiol. 136 2734–2746 Occurrence Handle10.1104/pp.104.046599 Occurrence Handle15333755
S. Seo M. Okamoto H. Seto K. Ishizuka H. Sano Y. Ohashi (1995) ArticleTitleTobacco MAP kinase: a possible mediator in wound signal transduction pathways Science 270 1988–1992 Occurrence Handle8533090
P.C. Sharma A. Ito T. Shimizu R. Terauchi S. Kamoun H. Saitoh (2003) ArticleTitleVirus-induced silencing of WIPK and SIPK genes reduces resistance to a bacterial pathogen, but has no effect on the INF1-induced hypersensitive response (HR) in Nicotiana benthamiana Mol. Gen. Genomics 269 583–591 Occurrence Handle10.1007/s00438-003-0872-9
S. Sugano H. Kaminaka Z. Rybka R. Catala J. Salinas K. Matsui M. Ohme-Takagi H. Takatsuji (2003) ArticleTitleStress-responsive zinc finger gene ZPT2-3 plays a role in drought tolerance in petunia Plant J. 36 830–841 Occurrence Handle10.1046/j.1365-313X.2003.01924.x Occurrence Handle14675448
Y. Takahashi T. Berberich A. Miyazaki S. Seo Y. Ohashi T. Kusano (2003) ArticleTitleSpermine signalling in tobacco: activation of mitogen-activated protein kinases by spermine is mediated through mitochondrial dysfunction Plant J. 36 820–829 Occurrence Handle10.1046/j.1365-313X.2003.01923.x Occurrence Handle14675447
Y. Takahashi T. Berberich K. Yamashita Y. Uehara A. Miyazaki T. Kusano (2004a) ArticleTitleIdentification of tobacco HIN1 and two closely related genes as spermine-responsive genes and their differential expression during the Tobacco mosaic virus-induced hypersensitive response and during leaf- and flower- senescence Plant Mol. Biol. 54 613–622 Occurrence Handle10.1023/B:PLAN.0000038276.95539.39
Y. Takahashi Y. Uehara T. Berberich A. Ito H. Saitoh A. Miyazaki R. Terauchi T. Kusano (2004b) ArticleTitleA subset of the hypersensitive response marker genes including HSR203J is downstream target of a spermine-signal transduction pathway in tobacco Plant J. 40 586–595 Occurrence Handle10.1111/j.1365-313X.2004.02234.x
H. Takatsuji (1999) ArticleTitleZinc-finger proteins: the classical zinc finger emerges in contemporary plant science Plant Mol. Biol. 39 1073–1078 Occurrence Handle10.1023/A:1006184519697 Occurrence Handle10380795
H. Takatsuji T. Matsumoto (1996) ArticleTitleTarget-sequence recognition by separate-type Cys2/His2 Zinc finger proteins in plants J. Biol. Chem. 271 23368–23373 Occurrence Handle10.1074/jbc.271.38.23368 Occurrence Handle8798540
H. Takatsuji M. Mori P.N. Benfey L. Ren N.-H. Chua (1992) ArticleTitleCharacterization of a zinc-finger DNA binding protein expressed specifically in Petunia petals and seedlings EMBO J. 11 241–249 Occurrence Handle1740109
H. Takatsuji N. Nakamura Y. Katsumoto (1994) ArticleTitleA new family of zinc finger proteins in petunia: structure, DNA sequence recognition, and floral organ-specific expression Plant Cell 6 947–958 Occurrence Handle10.1105/tpc.6.7.947 Occurrence Handle8069106
D.R. Walters (2003a) ArticleTitlePolyamines and plant disease Phytochemistry 64 97–107 Occurrence Handle10.1016/S0031-9422(03)00329-7
D.R. Walters (2003b) ArticleTitleResistance to plant pathogens: possible roles for free polyamines and polyamine catabolism New Phytol. 159 109–115 Occurrence Handle10.1046/j.1469-8137.2003.00802.x
H. Yamakawa H. Kamada M. Satoh Y. Ohashi (1998) ArticleTitleSpermine is a salicylate-independent endogenous inducer for both tobacco acidic pathogenesis-related proteins and resistance against tobacco mosaic virus infection Plant Physiol. 118 1213–1222 Occurrence Handle10.1104/pp.118.4.1213 Occurrence Handle9847095
S.H. Yang T. Berberich A. Miyazaki H. Sano T. Kusano (2003) ArticleTitleNtdin, a tobacco senescence-associated gene, is involved in molybdenum cofactor biosynthesis Plant Cell Physiol. 44 1037–1044 Occurrence Handle10.1093/pcp/pcg122 Occurrence Handle14581628
K.-Y. Yang Y. Liu S. Zhang (2001) ArticleTitleActivation of a mitogen-activated protein kinase pathway is involved in disease resistance in tobacco Proc. Natl Acad . Sci. USA 98 741–746 Occurrence Handle10.1073/pnas.98.2.741 Occurrence Handle11209069
S.Y. Yi J.-H. Kim Y.-H. Joung S. Lee W.-T. Kim S.H. Yu D. Choi (2004) ArticleTitleThe pepper transcription factor CaPF1 confers pathogen and freezing tolerance in Arabidopsis Plant Physiol. 136 2862–2874 Occurrence Handle10.1104/pp.104.042903 Occurrence Handle15347795
K. Yoshioka S. Fukushima T. Yamazaki M. Yoshida H. Takatsuji (2001) ArticleTitleThe plant zinc finger protein ZPT2-2 has a unique mode of DNA interaction J. Biol. Chem. 276 35802–35807 Occurrence Handle10.1074/jbc.M104079200 Occurrence Handle11454859
S. Zhang D.F. Klessig (1997) ArticleTitleSalicylic acid activates a 48-kDa MAP kinase in tobacco Plant Cell 9 809–824 Occurrence Handle10.1105/tpc.9.5.809 Occurrence Handle9165755
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Uehara, Y., Takahashi, Y., Berberich, T. et al. Tobacco ZFT1, a Transcriptional Repressor with a Cys2/His2 Type Zinc Finger Motif that Functions in Spermine-Signaling Pathway. Plant Mol Biol 59, 435–448 (2005). https://doi.org/10.1007/s11103-005-0272-0
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DOI: https://doi.org/10.1007/s11103-005-0272-0