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The WRKY70 transcription factor of Arabidopsis influences both the plant senescence and defense signaling pathways

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Abstract

Regulatory proteins play critical roles in controlling the kinetics of various cellular processes during the entire life span of an organism. Leaf senescence, an integral part of the plant developmental program, is fine-tuned by a complex transcriptional regulatory network ensuring a successful switch to the terminal life phase. To expand our understanding on how transcriptional control coordinates leaf senescence, we characterized AtWRKY70, a gene encoding a WRKY transcription factor that functions as a negative regulator of developmental senescence. To gain insight into the interplay of senescence and plant defense signaling pathways, we employed a collection of mutants, allowing us to specifically define the role of AtWRKY70 in the salicylic acid-mediated signaling cascades and to further dissect the cross-talk of signal transduction pathways during the onset of senescence in Arabidopsis thaliana. Our results provide strong evidence that AtWRKY70 influences plant senescence and defense signaling pathways. These studies could form the basis for further unraveling of these two complex interlinked regulatory networks.

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Abbreviations

ET:

Ethylene

JA:

Jasmonic acid

SA:

Salicylic acid

References

  • AbuQamar S, Chen X, Dhawan R, Bluhm B, Salmeron J, Lam S, Dietrich RA, Mengiste T (2006) Expression profiling and mutant analysis reveals complex regulatory networks involved in Arabidopsis response to Botrytis infection. Plant J 48:28–44

    Article  PubMed  CAS  Google Scholar 

  • Bartsch M, Gobbato E, Bednarek P, Debey S, Schultze JL, Bautor J, Parker JE (2006) Salicylic acid-independent enhanced disease susceptibility1 signaling in Arabidopsis immunity and cell death is regulated by the monooxygenase FMO1 and the nudix hydrolase NUDT7. Plant Cell 18:1038–1051

    Article  PubMed  CAS  Google Scholar 

  • Benedetti CE, Costa CL, Turcinelli SR, Arruda P (1998) Differential expression of a novel gene in response to coronatine, methyl jasmonate, and wounding in the coi1 mutant of Arabidopsis. Plant Physiol 116:1037–1042

    Article  PubMed  CAS  Google Scholar 

  • Bieleski RL, Reid MS (1992) Physiological changes accompanying senescence in the ephemeral daylily flower. Plant Physiol 98:1042–1049

    Article  PubMed  CAS  Google Scholar 

  • Brodersen P, Petersen M, Pike HM, Olszak B, Skov S, Ødum N, Jørgensen LB, Brown RE, Mundy J (2002) Knockout of Arabidopsis accelerated-cell-death11 encoding a sphingosine transfer protein causes activation of programmed cell death and defense. Genes Dev 16:490–502

    Article  PubMed  CAS  Google Scholar 

  • Buchanan-Wollaston V, Earl S, Harrison E, Mathas E, Navabpour S, Page T, Pink D (2003) The molecular analysis of leaf senescence—a genomics approach. Plant Biotechnol J 1:3–22

    Article  PubMed  CAS  Google Scholar 

  • Buchanan-Wollaston V, Page T, Harrison E, Breeze E, Lim PO, Nam HG, Lin JF, Wu SH, Swidzinski J, Ishizaki K, Leaver CJ (2005) Comparative transcriptome analysis reveals significant differences in gene expression and signalling pathways between developmental and dark/starvation-induced senescence in Arabidopsis. Plant J 42:567–585

    Article  PubMed  CAS  Google Scholar 

  • Century KS, Holub EB, Staskawicz BJ (1995) NDR1, a locus of Arabidopsis thaliana that is required for disease resistance to both a bacterial and a fungal pathogen. Proc Natl Acad Sci USA 92:6597–6601

    Article  PubMed  CAS  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip:a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  PubMed  CAS  Google Scholar 

  • Frye CA, Tang D, Innes RW (2001) Negative regulation of defense responses in plants by a conserved MAPKK kinase. Proc Natl Acad Sci USA 98:373–378

    Article  PubMed  CAS  Google Scholar 

  • Gepstein S (2004) Leaf senescence—not just a ‘wear and tear’ phenomenom. Genome Biol 5:212

    Article  PubMed  Google Scholar 

  • Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227

    Article  PubMed  CAS  Google Scholar 

  • Govrin EM, Levine A (2000) The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Curr Biol 10:751–757

    Article  PubMed  CAS  Google Scholar 

  • van der Graaff E, Schwacke R, Schneider A, Desimone M, Flugge UI, Kunze R (2006) Transcription analysis of Arabidopsis membrane transporters and hormone pathways during developmental and induced leaf senescence. Plant Physiol 141:776–792

    Article  PubMed  CAS  Google Scholar 

  • Grbic V, Bleecker AB (1995) Ethylene regulates the timing of leaf senescence in Arabidopsis. Plant J 8:595–602

    Article  CAS  Google Scholar 

  • Guo Y, Gan S (2005) Leaf senescence: signals, execution, and regulation. Curr Top Dev Biol 71:83–112

    PubMed  CAS  Google Scholar 

  • Guo Y, Gan S (2006) AtNAP, a NAC family transcription factor, has an important role in leaf senescence. Plant J 46:601–612

    Article  PubMed  CAS  Google Scholar 

  • Guo Y, Cai Z, Gan S (2004) Transcriptome of Arabidopsis leaf senescence. Plant Cell Environ 27:521–549

    Article  CAS  Google Scholar 

  • Hanfrey C, Fife M, Buchanan-Wollaston V (1996) Leaf senescence in Brassica napus: expression of genes encoding pathogenesis-related proteins. Plant Mol Biol 30:597–609

    Article  PubMed  CAS  Google Scholar 

  • He Y, Fukushiga H, Hildebrand DF, Gan S (2002) Evidence supporting a role of jasmonic acid in Arabidopsis leaf senescence. Plant Physiol 128:876–884

    Article  PubMed  CAS  Google Scholar 

  • Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: β-glucuronidase a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–3907

    PubMed  CAS  Google Scholar 

  • John CF, Morris K, Jordan BR, Thomas B, A-H-Mackerness S (2001) Ultraviolet-B exposure leads to up-regulation of senescence-associated genes in Arabidopsis thaliana. J Exp Bot 52:1367–1373

    Article  PubMed  CAS  Google Scholar 

  • Kieber JJ, Rothenberg M, Roman G, Feldmann KA, Ecker JR (1993) CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a Raf family of protein kinases. Cell 72:427–441

    Article  PubMed  CAS  Google Scholar 

  • Koncz C, Schell J (1986) The promotor of TL-DNA gene 5 controls the tissue-specific expression of chimaeric genes carried by a novel type of Agrobacterium binary vector. Mol Gen Genet 204:383–396

    Article  CAS  Google Scholar 

  • Kus JV, Zaton K, Sarkar R, Cameron RK (2002) Age-related resistance in Arabidopsis is a developmentally regulated defense response to Pseudomonas syringae. Plant Cell 14:479–490

    Article  PubMed  CAS  Google Scholar 

  • La Camera S, Geoffroy P, Samaha H, Ndiaye A, Rahim G, Legrand M, Heitz T (2005) A pathogen-inducible patatin-like lipid acyl hydrolase facilitates fungal and bacterial host colonization in Arabidopsis. Plant J 44:810–825

    Article  PubMed  CAS  Google Scholar 

  • Li J, Brader G, Palva ET (2004) The WRKY70 transcription factor: a node of convergence for jasmonate-mediated and salicylate-mediated signals in plant defense. Plant Cell 16:319–331

    Article  PubMed  CAS  Google Scholar 

  • Li J, Brader G, Kariola T, Tapio Palva E (2006) WRKY70 modulates the selection of signaling pathways in plant defense. Plant J 46:477–491

    Article  PubMed  CAS  Google Scholar 

  • Lin J-F, Wu S-H (2004) Molecular events in senescing Arabidopsis leaves. Plant J 39:612–628

    Article  PubMed  CAS  Google Scholar 

  • Maleck K, Levine A, Eulgem T, Morgen A, Schmid J, Lawton K, Dangl JL, Dietrich RA (2000) The transcriptome of Arabidopsis thaliana during systemic acquired resistance. Nat Genet 26:403–410

    Article  PubMed  CAS  Google Scholar 

  • Miao Y, Laun T, Zimmermann P, Zentgraf U (2004) Targets of the WRKY53 transcription factor and its role during leaf senescence in Arabidopsis. Plant Mol Biol 55:853–867

    PubMed  CAS  Google Scholar 

  • Morris K, A-H-Mackerness S, Page T, John CF, Murphy AM, Carr JP, Buchanan-Wollaston V (2000) Salicylic acid has a role in regulating gene expression during leaf senescence. Plant J 23:677–685

    Article  PubMed  CAS  Google Scholar 

  • Oh SA, Lee SY, Chung IK, Lee C-H, Nam HG (1996) A senescence-associated gene of Arabidopsis thaliana is distinctively regulated during natural and artificially induced leaf senescence. Plant Mol Biol 30:739–754

    Article  PubMed  CAS  Google Scholar 

  • Oh SA, Park JH, Lee GI, Paek KH, Park SK, Nam HG (1997) Identification of three genetic loci controlling leaf senescence in Arabidopsis thaliana. Plant J 12:527–535

    Article  PubMed  CAS  Google Scholar 

  • Olsen AN, Ernst HA, Leggio LL, Skriver K (2005) NAC transcription factors: structurally distinct, functionally diverse. Trends Plant Sci 10:79–87

    Article  PubMed  CAS  Google Scholar 

  • Park J-H, Halitschke R, Kim HB, Baldwin IT, Feldmann K, Feyereisen R (2002) A knock-out mutation in allene oxide synthase results in male sterility and defective wound signal transduction in Arabidopsis due to a block in jasmonic acid biosynthesis. Plant J 31:1–12

    Article  PubMed  Google Scholar 

  • Quirino BF, Noh Y-S, Himelblau E, Amasino RM (2000) Molecular aspects of leaf senescence. Trends Plant Sci 5:278–282

    Article  PubMed  CAS  Google Scholar 

  • Robatzek S, Somssich IE (2001) A new member of the Arabidopsis WRKY transcription factor family, AtWRKY6, is associated with both senescence- and defense-related processes. Plant J 28:123–133

    Article  PubMed  CAS  Google Scholar 

  • Rosso MG, Li Y, Strizhov N, Reiss B, Dekker K, Weisshaar B (2003) An Arabidopsis thaliana T-DNA mutagenized population (GABI-Kat) for flanking sequence tag-based reverse genetics. Plant Mol Biol 53:247–259

    Article  PubMed  CAS  Google Scholar 

  • Schenk PM, Kazan K, Rusu AG, Manners JM, Maclean DJ (2005) The SEN1 gene of Arabidopsis is regulated by signals that link plant defence responses and senescence. Plant Physiol Biochem 43:997–1005

    Article  PubMed  CAS  Google Scholar 

  • Schmid M, Davison TS, Henz SR, Pape UJ, Demar M, Vingron M, Scholkopf B, Weigel D, Lohmann JU (2005) A gene expression map of Arabidopsis thaliana development. Nat Genet 37:501

    Article  PubMed  CAS  Google Scholar 

  • Swidzinski JA, Sweetlove LJ, Leaver CJ (2002) A custom microarray analysis of gene expression during programmed cell death in Arabidopsis thaliana. Plant J 30:431–446

    Article  PubMed  CAS  Google Scholar 

  • Tang D, Innes RW (2002) Overexpression of a kinase-deficient form of the EDR1 genes enhances powdery mildew resistance and ethylene-induced senescence in Arabidopsis. Plant J 32:975–983

    Article  PubMed  CAS  Google Scholar 

  • Ward ER, Uknes SJ, Williams SC, Dincher SS, Wiederhold DL, Alexander DC, Ahl-Goy P, Métraux J-P, Ryals JA (1991) Coordinate gene activity in response to agents that induce systemic acquired resistance. Plant Cell 3:1085–1094

    Article  PubMed  CAS  Google Scholar 

  • Weaver LM, Amasino RM (2001) Senescence is induced in individually darkened Arabidopsis leaves, but inhibited in whole darkened plants. Plant Physiol 127:876–886

    Article  PubMed  CAS  Google Scholar 

  • Wyatt S, Pan S, Kuc J (1991) Beta-1,3-Glucanase, chitinase and peroxidase activities in tobacco tissues resistant and susceptible to blue mould as related to flowering, age and sucker development. Physiol Mol Plant Pathol 39:433–440

    Article  CAS  Google Scholar 

  • Yoshida S, Ito M, Nishida I, Watanabe A (2001) Isolation and RNA gel blot analysis of genes that could serve as potential molecular markers for leaf senescence in Arabidopsis thaliana. Plant Cell Physiol 42:170–178

    Article  PubMed  CAS  Google Scholar 

  • Yoshida S, Ito M, Callis J, Nishida I, Watanabe A (2002a) A delayed leaf senescence mutant is defective in arginyl-tRNA:protein arginyl transferase, a component of the N-end rule pathway in Arabidopsis. Plant J 32:129–137

    Article  CAS  Google Scholar 

  • Yoshida S, Ito M, Nishida I, Watanabe A (2002b) Identification of a novel gene HYS1/CPR5 that has a repressive role in the induction of leaf senescence and pathogen-defense responses in Arabidopsis thaliana. Plant J 29:427–437

    Article  CAS  Google Scholar 

  • Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W (2004) GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol 136:2621–2632

    Article  PubMed  CAS  Google Scholar 

  • Zimmermann P, Hennig L, Gruissem W (2005) Gene-expression analysis and network discovery using Genevestigator. Trends Plant Sci 10:407–409

    Article  PubMed  CAS  Google Scholar 

  • Ülker B, Somssich IE (2004) WRKY transcription factors: from DNA binding towards biological function. Curr Opin Plant Biol 7:491–498

    Article  PubMed  CAS  Google Scholar 

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Acknowledgment

We thank Dr. Karolina Pajerowska-Mukhtar for critically reading of the manuscript. M.S.M was supported by International Max Planck Research School (Max Planck Society, Munich, Germany). Financial support of B.U. was partly provided by the EU-funded REGIA project.

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Author notes

  1. Bekir Ülker

    Present address: School of Biological and Biomedical Sciences, Durham University, Science Site, South Road, Durham, DH1 3LE, UK

  2. M. Shahid Mukhtar

    Present address: Department of Biology, University of North Carolina at Chapel Hill, CB# 3280, 108 Coker Hall, Chapel Hill, NC, 27599, USA

Authors and Affiliations

  1. Max Planck Institute for Plant Breeding Research, Abteilung Molekulare Phytopathologie, Carl-von-Linné-Weg 10, 50829, Cologne, Germany

    Bekir Ülker, M. Shahid Mukhtar & Imre E. Somssich

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  1. Bekir Ülker
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  2. M. Shahid Mukhtar
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  3. Imre E. Somssich
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Correspondence to Imre E. Somssich.

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Ülker, B., Shahid Mukhtar, M. & Somssich, I.E. The WRKY70 transcription factor of Arabidopsis influences both the plant senescence and defense signaling pathways. Planta 226, 125–137 (2007). https://doi.org/10.1007/s00425-006-0474-y

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  • DOI: https://doi.org/10.1007/s00425-006-0474-y

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