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Plant Molecular Biology

, Volume 59, Issue 3, pp 435–448 | Cite as

Tobacco ZFT1, a Transcriptional Repressor with a Cys2/His2 Type Zinc Finger Motif that Functions in Spermine-Signaling Pathway

  • Yukiko Uehara
  • Yoshihiro Takahashi
  • Thomas Berberich
  • Atsushi Miyazaki
  • Hideki Takahashi
  • Kyoko Matsui
  • Masaru Ohme-Takagi
  • Hiromasa Saitoh
  • Ryohei Terauchi
  • Tomonobu Kusano
Article

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.

Key words

signal transduction spermine tobacco Tobacco mosaic virus transcription factor zinc finger protein 

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References

  1. Berberich, T., Sano, H., Kusano, T. 1999Involvement of a MAP kinase, ZmMPK5, in senescence and recovery from low-temperature stress in maizeMol. Gen. Genet.262534542CrossRefPubMedGoogle Scholar
  2. Bouchereau, A., Aziz, A., Larher, F., Martin-Tanguy, J. 1999Polyamines and environmental challenges: recent developmentPlant Sci.140103125CrossRefGoogle Scholar
  3. Chen, Z., Malamy, J., Henning, J., Conrath, U., Sanchez-Casa, P., Silva, H., Ricigliano, J., Klessig, D.F. 1995Induction, modification, and transduction of the salicylic acid signal in plant defense responsesProc. Natl. Acad. Sci. USA9241344137PubMedGoogle Scholar
  4. Krol, A.R., Poecke, R.M., Vorst, O.F., Voogt, C., Leeuwen, W., Borst-Vrensen, T.W., Takatsuji, H., Plas, L.H. 1999Development and wound-, cold-, desiccation-, ultraviolet-B-stress-induced modulations in the expression of the petunia zinc finger transcription factor gene, ZPT2-2Plant Physiol.12111531162CrossRefPubMedGoogle Scholar
  5. Dong, X. 1998SA, JA, ethylene, and disease resistance in plantsCurr. Opin. Plant Biol.1316323CrossRefPubMedGoogle Scholar
  6. Frugier, F., Poirier, S., Satiat-Jeunemaitre, B., Kondorosi, A., Crespi, M. 2000A Krüppel-like zinc finger protein is involved in nitrogen-fixing root nodule organogenesisGenes Dev.14475482PubMedGoogle Scholar
  7. Gallie, D.R., Sleat, D.E., Watts, J.W., Turner, P.C., Wilson, T.M.A. 1987The 5-leader sequence of tobacco mosaic virus RNA enhances the expression of foreign gene transcripts in vitro and in vivoNucleic Acid. Res.1532573273PubMedGoogle Scholar
  8. Hiraga, S., Ito, H., Sasaki, K., Yamakawa, H., Mitsuhara, I., Toshima, H., Matsui, H., Honma, M., Ohashi, Y. 2000aWound-induced expression of a tobacco peroxidase is not enhanced by ethephon and suppressed by methyl jasmonate and coronatinePlant Cell Physiol.41165170Google Scholar
  9. Hiraga, S., Ito, H., Yamakawa, H., Ohtsubo, N., Seo, S., Mitsuhara, I., Matsui, H., Honma, M., Ohashi, Y. 2000bAn HR-induced tobacco peroxidase gene is responsive to spermine, but not to salicylate, methyl jasmonate, and ethephonMol. Plant-Microbe Interact.13210216Google Scholar
  10. Hiratsu, K., Ohta, M., Matsui, K., Ohme-Takagi, M. 2002The SUPERMAN protein is an active repressor whose carboxy-terminal repression domain is required for the development of normal flowersFEBS Lett.514351354CrossRefPubMedGoogle Scholar
  11. Iida, A., Kazuoka, T., Torikai., S., Kikuchi, H., Oeda, K. 2000A zinc finger protein RHL41 mediates the light acclimation response in ArabidopsisPlant J.24191203CrossRefPubMedGoogle Scholar
  12. Isernia, C., Bucci, E., Leone, M., Zaccaro, L., Lello, P., Digilio, G., Esposito, S., Saviano, M., Blasio, B., Pedone, C., Pedone, P.V., Fattorusso, R. 2003NMR structure of the single QALGGH zinc finger domain from the Arabidopsis thaliana SUPERMAN proteinChembiochem4171180CrossRefPubMedGoogle Scholar
  13. Kim, J.C., Lee, S.H., Cheong, Y.H., Yoo, C.-M., Lee, S.I., Chun, H.J., Yun, D.-J., Hong, J.C., Lee, S.Y., Lim, C.O., Cho, M.J. 2001A novel cold-inducible zinc finger protein from soybean, SCOF-1, enhances cold tolerance in transgenic plantsPlant J.25247259CrossRefPubMedGoogle Scholar
  14. Kim, S.H., Hong, J.K., Lee, S.C., Sohn, K.H., Jung, H.W., Hwang, B.K. 2004CAZFP1, Cys2/His2-type zinc-finger transcription factor gene functions as a pathogen-induced early-defense gene in Capsium annuumPlant Mol. Biol.55883904PubMedGoogle Scholar
  15. Klessig, D.F., Malamy, J. 1994The salicylic acid signal in plantsPlant Mol. Biol.2614391458CrossRefPubMedGoogle Scholar
  16. Kubo, K., Sakamoto, A., Kobayashi, A., Rybka, Z., Kanno, Y., Nakagawa, H., Takatsuji, H. 1998Cys2/His2 zinc-finger protein family of petunia: evolution and general mechanism of target-sequence recognitionNucleic Acid. Res.26608615CrossRefPubMedGoogle Scholar
  17. Kumar, A., Altabella, T., Taylor, M., Tiburcio, A.F. 1997Recent advances in polyamine researchTrends Plant Sci.2124130CrossRefGoogle Scholar
  18. Lippuner, V., Cyert, M.S., Gasser, C.S. 1996Two classes of plant cDNA clones differentially complement yeast calcineurin mutants and increase salt tolerance of wild-type yeastJ. Biol. Chem.2711285912866CrossRefPubMedGoogle Scholar
  19. Malmberg, R.L., Watson, M.B., Galloway, G.L., Yu, W. 1998Molecular genetic analysis of plant polyaminesCrit. Rev. Plant Sci.17199224CrossRefGoogle Scholar
  20. Marathe, R., Guan, Z., Anandalakshmi, R., Zhao, H., Dinesh-Kumar, S.P. 2004Study of Arabidopsis thaliana resistome in response to cucumber mosaic virus infection using whole genome microarrayPlant Mol. Biol.55501520CrossRefPubMedGoogle Scholar
  21. Matsumura, H., Reich, S., Ito, A., Saitoh, H., Kamoun, S., Winter, P., Kahl, G., Reuter, M., Krüger, D.H., Terauchi, R. 2003Gene expression analysis of plant host-pathogen interactions by SuperSAGEProc. Natl. Acad. Sci. USA1001571815723CrossRefPubMedGoogle Scholar
  22. Meissner, R., Michael, A.J. 1997Isolation and characterization of a diverse family of Arabidopsis two and three-fingered C2H2 zinc finger protein genes and cDNAsPlant Mol. Biol.33615624CrossRefPubMedGoogle Scholar
  23. Nagy, F., Kay, S.A., Chua, N.-H. 1988Analysis of gene expression in transgenic plantsGelvin, S.B.Schilperoort, R.A. eds. Plant Molecular Biology ManualKluwer Academic PublishersDordrecht129Google Scholar
  24. Ohta, M., Matsui, K., Hiratsu, K., Shinshi, H., Ohta-Takagi, M. 2001Repression domains of class II ERF transcriptional repressors share an essential motif for active repressionPlant Cell1319591968CrossRefPubMedGoogle Scholar
  25. Pontier, D., Godiard, L., Marco, Y., Roby, D. 1994hsr203J, a tobacco gene whose activation is rapid, highly localized and specific for incompatible plant/pathogen interactionsPlant J.5507521PubMedGoogle Scholar
  26. Sakamoto, A., Minami, M., Huh, G.H., Iwabuchi, M. 1993The putative zinc-finger protein WZF1 interacts with a cis-acting element of wheat histone genesEur. J. Biochem.21710491056CrossRefPubMedGoogle Scholar
  27. Sakamoto, H., Maruyama, K., Sakuma, Y., Meshi, T., Iwabuchi, M., Shinozaki, K., Yamaguchi-Shinozaki, K. 2004Arabidopsis Cys2/His2-type zinc-finger proteins function as transcription repressors under drought, cold, and high-salinity stress conditionsPlant Physiol.13627342746CrossRefPubMedGoogle Scholar
  28. Seo, S., Okamoto, M., Seto, H., Ishizuka, K., Sano, H., Ohashi, Y. 1995Tobacco MAP kinase: a possible mediator in wound signal transduction pathwaysScience27019881992PubMedGoogle Scholar
  29. Sharma, P.C., Ito, A., Shimizu, T., Terauchi, R., Kamoun, S., Saitoh, H. 2003Virus-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 benthamianaMol. Gen. Genomics269583591CrossRefGoogle Scholar
  30. Sugano, S., Kaminaka, H., Rybka, Z., Catala, R., Salinas, J., Matsui, K., Ohme-Takagi, M., Takatsuji, H. 2003Stress-responsive zinc finger gene ZPT2-3 plays a role in drought tolerance in petuniaPlant J.36830841CrossRefPubMedGoogle Scholar
  31. Takahashi, Y., Berberich, T., Miyazaki, A., Seo, S., Ohashi, Y., Kusano, T. 2003Spermine signalling in tobacco: activation of mitogen-activated protein kinases by spermine is mediated through mitochondrial dysfunctionPlant J.36820829CrossRefPubMedGoogle Scholar
  32. Takahashi, Y., Berberich, T., Yamashita, K., Uehara, Y., Miyazaki, A., Kusano, T. 2004aIdentification 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- senescencePlant Mol. Biol.54613622CrossRefGoogle Scholar
  33. Takahashi, Y., Uehara, Y., Berberich, T., Ito, A., Saitoh, H., Miyazaki, A., Terauchi, R., Kusano, T. 2004bA subset of the hypersensitive response marker genes including HSR203J is downstream target of a spermine-signal transduction pathway in tobaccoPlant J.40586595CrossRefGoogle Scholar
  34. Takatsuji, H. 1999Zinc-finger proteins: the classical zinc finger emerges in contemporary plant sciencePlant Mol. Biol.3910731078CrossRefPubMedGoogle Scholar
  35. Takatsuji, H., Matsumoto, T. 1996Target-sequence recognition by separate-type Cys2/His2 Zinc finger proteins in plantsJ. Biol. Chem.2712336823373CrossRefPubMedGoogle Scholar
  36. Takatsuji, H., Mori, M., Benfey, P.N., Ren, L., Chua, N.-H. 1992Characterization of a zinc-finger DNA binding protein expressed specifically in Petunia petals and seedlingsEMBO J.11241249PubMedGoogle Scholar
  37. Takatsuji, H., Nakamura, N., Katsumoto, Y. 1994A new family of zinc finger proteins in petunia: structure, DNA sequence recognition, and floral organ-specific expressionPlant Cell6947958CrossRefPubMedGoogle Scholar
  38. Walters, D.R. 2003aPolyamines and plant diseasePhytochemistry6497107CrossRefGoogle Scholar
  39. Walters, D.R. 2003bResistance to plant pathogens: possible roles for free polyamines and polyamine catabolismNew Phytol.159109115CrossRefGoogle Scholar
  40. Yamakawa, H., Kamada, H., Satoh, M., Ohashi, Y. 1998Spermine is a salicylate-independent endogenous inducer for both tobacco acidic pathogenesis-related proteins and resistance against tobacco mosaic virus infectionPlant Physiol.11812131222CrossRefPubMedGoogle Scholar
  41. Yang, S.H., Berberich, T., Miyazaki, A., Sano, H., Kusano, T. 2003Ntdin, a tobacco senescence-associated gene, is involved in molybdenum cofactor biosynthesisPlant Cell Physiol.4410371044CrossRefPubMedGoogle Scholar
  42. Yang, K.-Y., Liu, Y., Zhang, S. 2001Activation of a mitogen-activated protein kinase pathway is involved in disease resistance in tobaccoProc. Natl Acad . Sci. USA98741746CrossRefPubMedGoogle Scholar
  43. Yi, S.Y., Kim, J.-H., Joung, Y.-H., Lee, S., Kim, W.-T., Yu, S.H., Choi, D. 2004The pepper transcription factor CaPF1 confers pathogen and freezing tolerance in ArabidopsisPlant Physiol.13628622874CrossRefPubMedGoogle Scholar
  44. Yoshioka, K., Fukushima, S., Yamazaki, T., Yoshida, M., Takatsuji, H. 2001The plant zinc finger protein ZPT2-2 has a unique mode of DNA interactionJ. Biol. Chem.2763580235807CrossRefPubMedGoogle Scholar
  45. Zhang, S., Klessig, D.F. 1997Salicylic acid activates a 48-kDa MAP kinase in tobaccoPlant Cell9809824CrossRefPubMedGoogle Scholar

Copyright information

© Springer 2005

Authors and Affiliations

  • Yukiko Uehara
    • 1
    • 7
  • Yoshihiro Takahashi
    • 1
    • 8
  • Thomas Berberich
    • 1
    • 2
    • 8
  • Atsushi Miyazaki
    • 1
  • Hideki Takahashi
    • 3
  • Kyoko Matsui
    • 4
    • 5
  • Masaru Ohme-Takagi
    • 4
    • 5
  • Hiromasa Saitoh
    • 6
  • Ryohei Terauchi
    • 6
  • Tomonobu Kusano
    • 1
  1. 1.Graduate School of Life SciencesTohoku UniversityMiyagiJapan
  2. 2.Botanisches InstitutGoethe-UniversitätFrankfurt am MainGermany
  3. 3.Graduate School of Agricultural SciencesTohoku UniversityMiyagiJapan
  4. 4.Gene Function Research CenterNational Institute of Advanced Industrial Technology and Science (AIST)TsukubaJapan
  5. 5.CREST, Japan Science and Technology AgencyJapan
  6. 6.Iwate Biotechnology Research CenterIwateJapan
  7. 7.RIKEN Plant Science CenterKanagawaJapan
  8. 8.Iwate Biotechnology Research CenterIwateJapan

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