, Volume 226, Issue 1, pp 125–137 | Cite as

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

  • Bekir Ülker
  • M. Shahid Mukhtar
  • Imre E. SomssichEmail author
Original Article


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.


Atwrky70 mutants Dark-induced senescence Salicylic acid Signaling crosstalk 





Jasmonic acid


Salicylic acid



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.


  1. 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 48:28–44PubMedCrossRefGoogle Scholar
  2. 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 18:1038–1051PubMedCrossRefGoogle Scholar
  3. 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 116:1037–1042PubMedCrossRefGoogle Scholar
  4. Bieleski RL, Reid MS (1992) Physiological changes accompanying senescence in the ephemeral daylily flower. Plant Physiol 98:1042–1049PubMedCrossRefGoogle Scholar
  5. 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 16:490–502PubMedCrossRefGoogle Scholar
  6. 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 1:3–22PubMedCrossRefGoogle Scholar
  7. 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 42:567–585PubMedCrossRefGoogle Scholar
  8. 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 92:6597–6601PubMedCrossRefGoogle Scholar
  9. Clough SJ, Bent AF (1998) Floral dip:a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743PubMedCrossRefGoogle Scholar
  10. Frye CA, Tang D, Innes RW (2001) Negative regulation of defense responses in plants by a conserved MAPKK kinase. Proc Natl Acad Sci USA 98:373–378PubMedCrossRefGoogle Scholar
  11. Gepstein S (2004) Leaf senescence—not just a ‘wear and tear’ phenomenom. Genome Biol 5:212PubMedCrossRefGoogle Scholar
  12. Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227PubMedCrossRefGoogle Scholar
  13. Govrin EM, Levine A (2000) The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Curr Biol 10:751–757PubMedCrossRefGoogle Scholar
  14. 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 141:776–792PubMedCrossRefGoogle Scholar
  15. Grbic V, Bleecker AB (1995) Ethylene regulates the timing of leaf senescence in Arabidopsis. Plant J 8:595–602CrossRefGoogle Scholar
  16. Guo Y, Gan S (2005) Leaf senescence: signals, execution, and regulation. Curr Top Dev Biol 71:83–112PubMedGoogle Scholar
  17. Guo Y, Gan S (2006) AtNAP, a NAC family transcription factor, has an important role in leaf senescence. Plant J 46:601–612PubMedCrossRefGoogle Scholar
  18. Guo Y, Cai Z, Gan S (2004) Transcriptome of Arabidopsis leaf senescence. Plant Cell Environ 27:521–549CrossRefGoogle Scholar
  19. Hanfrey C, Fife M, Buchanan-Wollaston V (1996) Leaf senescence in Brassica napus: expression of genes encoding pathogenesis-related proteins. Plant Mol Biol 30:597–609PubMedCrossRefGoogle Scholar
  20. He Y, Fukushiga H, Hildebrand DF, Gan S (2002) Evidence supporting a role of jasmonic acid in Arabidopsis leaf senescence. Plant Physiol 128:876–884PubMedCrossRefGoogle Scholar
  21. Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: β-glucuronidase a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–3907PubMedGoogle Scholar
  22. 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 52:1367–1373PubMedCrossRefGoogle Scholar
  23. 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 72:427–441PubMedCrossRefGoogle Scholar
  24. 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 204:383–396CrossRefGoogle Scholar
  25. 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 14:479–490PubMedCrossRefGoogle Scholar
  26. 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 44:810–825PubMedCrossRefGoogle Scholar
  27. 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 16:319–331PubMedCrossRefGoogle Scholar
  28. Li J, Brader G, Kariola T, Tapio Palva E (2006) WRKY70 modulates the selection of signaling pathways in plant defense. Plant J 46:477–491PubMedCrossRefGoogle Scholar
  29. Lin J-F, Wu S-H (2004) Molecular events in senescing Arabidopsis leaves. Plant J 39:612–628PubMedCrossRefGoogle Scholar
  30. 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 26:403–410PubMedCrossRefGoogle Scholar
  31. 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 55:853–867PubMedGoogle Scholar
  32. 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 23:677–685PubMedCrossRefGoogle Scholar
  33. 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 30:739–754PubMedCrossRefGoogle Scholar
  34. 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 12:527–535PubMedCrossRefGoogle Scholar
  35. Olsen AN, Ernst HA, Leggio LL, Skriver K (2005) NAC transcription factors: structurally distinct, functionally diverse. Trends Plant Sci 10:79–87PubMedCrossRefGoogle Scholar
  36. 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 31:1–12PubMedCrossRefGoogle Scholar
  37. Quirino BF, Noh Y-S, Himelblau E, Amasino RM (2000) Molecular aspects of leaf senescence. Trends Plant Sci 5:278–282PubMedCrossRefGoogle Scholar
  38. 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 28:123–133PubMedCrossRefGoogle Scholar
  39. 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 53:247–259PubMedCrossRefGoogle Scholar
  40. 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 43:997–1005PubMedCrossRefGoogle Scholar
  41. 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 37:501PubMedCrossRefGoogle Scholar
  42. Swidzinski JA, Sweetlove LJ, Leaver CJ (2002) A custom microarray analysis of gene expression during programmed cell death in Arabidopsis thaliana. Plant J 30:431–446PubMedCrossRefGoogle Scholar
  43. 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 32:975–983PubMedCrossRefGoogle Scholar
  44. 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 3:1085–1094PubMedCrossRefGoogle Scholar
  45. Weaver LM, Amasino RM (2001) Senescence is induced in individually darkened Arabidopsis leaves, but inhibited in whole darkened plants. Plant Physiol 127:876–886PubMedCrossRefGoogle Scholar
  46. 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 39:433–440CrossRefGoogle Scholar
  47. 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 42:170–178PubMedCrossRefGoogle Scholar
  48. 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 32:129–137CrossRefGoogle Scholar
  49. 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 29:427–437CrossRefGoogle Scholar
  50. Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W (2004) GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol 136:2621–2632PubMedCrossRefGoogle Scholar
  51. Zimmermann P, Hennig L, Gruissem W (2005) Gene-expression analysis and network discovery using Genevestigator. Trends Plant Sci 10:407–409PubMedCrossRefGoogle Scholar
  52. Ülker B, Somssich IE (2004) WRKY transcription factors: from DNA binding towards biological function. Curr Opin Plant Biol 7:491–498PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Bekir Ülker
    • 1
    • 2
  • M. Shahid Mukhtar
    • 1
    • 3
  • Imre E. Somssich
    • 1
    Email author
  1. 1.Max Planck Institute for Plant Breeding Research, Abteilung Molekulare PhytopathologieCologneGermany
  2. 2.School of Biological and Biomedical SciencesDurham UniversityDurhamUK
  3. 3.Department of BiologyUniversity of North Carolina at Chapel HillChapel HillUSA

Personalised recommendations