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Transactivation of wound-responsive genes containing the core sequence of the auxin-responsive element by a wound-induced protein kinase-activated transcription factor in tobacco plants

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Abstract

Mitogen-activated protein kinases (MAPKs) constitute one of the most critical signaling components in plants. A typical example is wound-induced protein kinase (WIPK), which functions during pathogen responses in tobacco plants (Nicotiana tabacum). Searching for direct down-stream components, we previously isolated a novel transcription factor, which was activated upon phosphorylation by WIPK and designated as N. tabacum WIPK-interacting factor (NtWIF). Overexpression of NtWIF in tobacco plants enhanced the hypersensitive response (HR) upon tobacco mosaic virus infection and cryptogein treatment, while its silencing by RNAi suppressed such HR. NtWIF contains a specific motif similar to the B3 DNA binding domain, which recognizes the core TGTCTC motif called the auxin-responsive element (ARE). Using synthetic ARE sequences, NtWIF was also shown to recognize the ARE motifs and to transactivate the Luciferase (Luc)-reporter gene driven by such AREs in tobacco BY2 cultured cells. Subsequent microarray screening of NtWIF overexpressing tobacco identified 49 stress-responsive genes, and in silico analyses of available promoter regions of these genes revealed β-1,3-glucanase, ACS2, P-450, and WIPK itself to contain the ARE core motif consisted of either TGTCTC or TGTCCT. Gel shift assay showed NtWIF to efficiently bind to both sequences. Assays with 1.5-kb PR-Q and 1.2 kb WIPK promoter regions, each fused to the Luc-reporter gene, indicated NtWIF to exhibit a clear transactivation activity, which was increased up to 3-fold upon phosphorylation by WIPK. These results revealed that NtWIF directly regulates multiple stress-responsive genes containing the ARE motif in their promoters, thereby partly filling up the last step of the MAPK cascade.

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Abbreviations

ACS:

Aminocyclopropane carboxylic acid synthase

ARE:

Auxin responsive element

HR:

Hypersensitive response

MAPK:

Mitogen-activated protein kinase

MEK:

MAPK/extra cellular signal-regulated kinase (ERK) kinase

MEKK:

MEK kinase

SA:

Salicylic acid

TMV:

Tobacco mosaic virus

References

  • Cheong YH, Moon BC, Kim JK, Kim CY, Kim MC, Kim IH, Park CY, Kim JC, Park BO, Koo SC, Yoon HW, Chung WS, Lim CO, Lee SY, Cho MJ (2003) BWMK1, a rice mitogen-activated protein kinase, locates in the nucleus and mediates pathogenesis-related gene expression by activation of a transcription factor. Plant Physiol 132:1961–1972

    Article  PubMed  CAS  Google Scholar 

  • Giraudat J, Hauge BM, Valcon C, Smalle J, Parcy F, Goodman HM (1992) Isolation of the Arabidopsis ABI3 gene by positional cloning. Plant Cell 4:1251–1261

    Article  PubMed  CAS  Google Scholar 

  • Guilfoyle TJ, Hagen G, Li Y, Ulmasov T, Liu Z, Strabala T, Gee MA (1993) Auxin-regulated transcription. Aust J Plant Physiol 20:489–502

    Article  CAS  Google Scholar 

  • Guilfoyle TJ, Ulmasov T, Hagen G (1998) The ARF family of transcription factors and their role in plant hormone responsive transcription. Cell Mol Life Sci 54:619–627

    Article  PubMed  CAS  Google Scholar 

  • Hahn MG, Bucheli D, Cervone F, Coares SH, O’Neill RA, Darvill A, Albersheim P (1989) The roles of cell wall constituents in plant–pathogen interaction. In: Nester E, Kosuge T (eds) Plant microbe interactions, vol 3. McGraw-Hill Publishing Co., New York, pp 131–181

    Google Scholar 

  • Ito M, Koike A, Koizumi N, Sano H (2003) Methylated DNA-binding proteins from Arabidopsis. Plant Physiol 133:1747–1754

    Article  PubMed  CAS  Google Scholar 

  • Katoh A, Yamaguchi Y, Sano H, Hashimoto T (2003) Analysis of expression sequence tags from Nicotiana sylvestris. Proc Jpn Acad 79(Series B):151–154

    Article  CAS  Google Scholar 

  • Lei L, Chuanyou L, Gyu IL, Gregg AH (2002) Distinct roles for jasmonate synthesis and action in the systemic wound response of tomato. Proc Natl Acad Sci USA 30:6416–6421

    Article  CAS  Google Scholar 

  • Ligterink W (2000) MAP kinases in plant signal transduction: how many, and what for? Result Probl Cell Differ 27:11–27

    CAS  Google Scholar 

  • Ligterink W, Hirt H (2001) Mitogen-activated protein (MAP) kinase pathways in plants: versatile signaling tools. Int Rev Cytol 201:209–275

    Article  PubMed  CAS  Google Scholar 

  • Liu Y, Zhang S (2004) Phosphorylation of 1-aminocyclopropane-1-carboxylic acid synthase by MPK6, a stress-responsive mitogen-activated protein kinase, induces ethylene biosynthesis in Arabidopsis. Plant Cell 16:3386–3399

    Article  PubMed  CAS  Google Scholar 

  • Mauch F, Mauch-Mani B, Boller T (1988) Antifungal hydrolases in pea tissue: II inhibition of fungal growth by combinations of chitinase and beta-1,3-glucanase. Plant Physiol 88:936–942

    Article  PubMed  CAS  Google Scholar 

  • McCarty DR, Hattori T, Carson CB, Vasil V, Lazar M, Vasil IK (1991) The viviparous-1 developmental gene of maize encodes a novel transcriptional activator. Cell 66:895–905

    Article  PubMed  CAS  Google Scholar 

  • Menke FLH, Kang H, Chen Z, Park HM, Kumar D, Klessig DF (2005) Tobacco transcription factor WRKY1 phophorylated by the MAP Kinase SIPK and mediates HR-like cell death in tobacco. Mol Plant Microbe Interact 18:1027–1034

    Article  PubMed  CAS  Google Scholar 

  • Nakagami H, Pitzschke A, Hirt H (2005) Emerging MAPKinase pathways in plant stress signaling. Trend Plant Sci 10:339–346

    Article  CAS  Google Scholar 

  • Niki T, Mitsuhara I, Seo S, Ohtsubo N, Ohashi Y (1998) Antagonistic effect of salicylic acid and jasmonic acid on the expression of pathogenesis-related (PR) protein genes in wounded mature tobacco leavese. Plant Cell Physiol 39:500–507

    CAS  Google Scholar 

  • Payne G, Ahl P, Moyer M, Harper A, Beck J, Meins FJ, Ryals J (1990) Isolation of complementary DNA clones encoding pathogenesis-related proteins P and Q, two acidic chitinase from tobacco. Proc Natl Acad Sci USA 87:98–102

    Article  PubMed  CAS  Google Scholar 

  • Seo S, Okamoto M, Seto H, Ishizuka K, Sano H, Ohashi Y (1995) Tobacco MAP kinase: a possible mediator in wound signal transduction pathways. Science 270:1988–1992

    Article  PubMed  CAS  Google Scholar 

  • Sharrocks AD, Yang SH, Galanis A (2000) Docking domains and substrate specificity determination for MAP kinases. Trends Biochem Sci 25:448–453

    Article  PubMed  CAS  Google Scholar 

  • Suzuki M, Kao CY, Cocciolone S, McCarty DR (2001) Maize VP1 complements Arabidopsis abi3 and confers a novel ABA/auxin interaction in roots. Plant J 28:409–418

    Article  PubMed  CAS  Google Scholar 

  • Thordal-Christensen H, Zhang Z, Wei Y, Collinge DB (1997) Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J 11:1187–1194

    Article  CAS  Google Scholar 

  • Ueda H, Yamaguchi Y, Sano H (2006) Direct interaction between the tobacco mosaic virus helicase domain and the ATP-bound resistance protein, N factor during the hypersensitive response in tobacco plants. Plant Mol Biol 61:31–45

    Article  PubMed  CAS  Google Scholar 

  • Ulmasov T, Liu ZB, Hagen G, Guilfoyle TJ (1995) Composite structure of auxin response elements. Plant Cell 7:1611–1623

    Article  PubMed  CAS  Google Scholar 

  • Ulmasov T, Hagen G, Guilfoyle TJ (1997) ARF1, a transcription factor that binds to auxin response elements. Science 276:1865–1868

    Article  PubMed  CAS  Google Scholar 

  • Ulmasov T, Hagen G, Guilfoyle TJ (1999) Activation and repression of transcription by auxin-response factors. Proc Natl Acad Sci USA 96:5844–5849

    Article  PubMed  CAS  Google Scholar 

  • Viard MP, Martin F, Pugin A, Ricci P, Blein JP (1994) Protein phosphorylation is induced in tobacco cells by the elicitor cryptogein. Plant Physiol 104:1245–1249

    PubMed  CAS  Google Scholar 

  • Wada Y, Ohya H, Yamaguchi Y, Koizumi N, Sano H (2003) Preferential de novo methylation of cytosine residues in non-CpG sequences by a domains rearranged DNA methyltransferase from tobacco plants. J Biol Chem 278:42386–42393

    Article  PubMed  CAS  Google Scholar 

  • Waller F, Müller A, Chung KM, Yap YK, Nakamura K, Weiler E, Sano H (2006) Expression of a WIPK-activated transcription factor results in increase of endogenous salicylic acid and pathogen resistance in tobacco plants. Plant Cell Physiol 47:1169–1174

    Article  PubMed  CAS  Google Scholar 

  • Wang LC, Li H, Ecker JR (2002) Ethylene biosynthesis and signaling networks. Plant Cell 14:S131–S151

    PubMed  CAS  Google Scholar 

  • Yamamoto YY, Deng XY (1989) A new vector set for GAL4-dependent transactivation assay in plants. Plant Biotechnol 15:217–220

    Google Scholar 

  • Yang SH, Sharrocks AD, Whitmarsh AJ (2003) Transcriptional regulation by the MAPKinase signaling cascades. Gene 320:3–21

    Article  PubMed  CAS  Google Scholar 

  • Yap YK, Kakamu K, Yamaguchi Y, Koizumi N, Sano H (2002) Promoter analysis of WIPK, a gene coding a tobacco MAPKinase, with reference to wounding and tobacco mosaic virus infection. J Plant Physiol 159:77–83

    Article  CAS  Google Scholar 

  • Yap YK, Kodama Y, Waller F, Chung KM, Ueda H, Nakamura K, Oldsen M, Yoda H, Yamaguchi Y, Sano H (2005) Activation of a novel transcription factor through phosphorylation by WIPK, a wound-induced mitogen-activated protein kinase in tobacco plants. Plant Physiol 139:127–137

    Article  PubMed  CAS  Google Scholar 

  • Yoda H, Yamaguchi Y, Sano H (2003) Induction of hypersensitive cell death by hydrogen peroxide produced through polyamine degradation in tobacco plants. Plant Physiol 132:1973–1981

    Article  PubMed  CAS  Google Scholar 

  • Yoda H, Hiroi Y, Sano H (2006) Polyamine oxidase is one of the key elements for oxidative burst to induce programmed cell death in tobacco cultured cells. Plant Physiol 142:193–206

    Article  PubMed  CAS  Google Scholar 

  • Zhang S, Klessig DF (1998) Resistance gene N-mediated de novo synthesis and activation of a tobacco mitogen-activated protein kinase by tobacco mosaic virus infection. Proc Natl Acad Sci USA 95:7433–7438

    Article  PubMed  CAS  Google Scholar 

  • Zhang S, Klessig DF (2001) MAPK cascades in plant defense signaling. Trends Plant Sci 6:520–527

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

The authors thank Drs Akira Katoh and Hiroshi Yoda (Nara Institute of Science and Technology) for instructions regarding microarray experiments and a generous gift of cryptogein, respectively, and Dr Malcolm Moore (Intermal, Nagoya) for critical reading of the manuscript. This work was partly supported by a grant from the Japan Society for the Promotion of Science and by a Grant-in-Aid for the 21st Century COE Research from the Ministry of Education, Culture, Sports, Science and Technology.

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Correspondence to Hiroshi Sano.

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Chung, KM., Sano, H. Transactivation of wound-responsive genes containing the core sequence of the auxin-responsive element by a wound-induced protein kinase-activated transcription factor in tobacco plants. Plant Mol Biol 65, 763–773 (2007). https://doi.org/10.1007/s11103-007-9240-1

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