WRKY72-type transcription factors contribute to basal immunity in tomato and Arabidopsis as well as gene-for-gene resistance mediated by the tomato R gene Mi-1.
WRKY transcription factors play a central role in transcriptional reprogramming associated with plant immune responses. However, due to functional redundancy, typically the contribution of individual members of this family to immunity is only subtle. Using microarray analysis, we found that the paralogous tomato WRKY genes SlWRKY72a and b are transcriptionally up-regulated during disease resistance mediated by the R gene Mi-1. Virus-induced gene silencing of these two genes in tomato resulted in a clear reduction of Mi-1-mediated resistance as well as basal defense against root-knot nematodes (RKN) and potato aphids. Using Arabidopsis T-DNA insertion mutants, we found that their Arabidopsis ortholog, AtWRKY72, is also required for full basal defense against RKN as well as to the oomycete Hyaloperonospora arabidopsidis. Despite their similar roles in basal defense against RKN in both tested plant species, WRKY72-type transcription factors in tomato, but not in Arabidopsis, clearly contributed to basal defense against the bacterial pathogen Pseudomonas syringae. Of the five R genes that we tested in tomato and Arabidopsis, only Mi-1 appeared to be dependent on WRKY72-type transcription factors. Interestingly, AtWRKY72 target genes, identified by microarray analysis of H. arabidopsidis-triggered transcriptional changes, appear to be largely non-responsive to analogs of the defense hormone salicylic acid (SA). Thus, similarly to Mi-1, which in part acts independently of SA, AtWRKY72 appears to utilize SA-independent defense mechanisms. We propose that WRKY72-type transcription factors play a partially conserved role in basal defense in tomato and Arabidopsis, a function that has been recruited to serve Mi-1-dependent immunity.
Bhattarai
Kishor K
KK
Graduate Program in Plant Pathology, University of California at Riverside, CA 92521, USA.|Department of Nematology, University of California at Riverside, CA 92521, USA.
Atamian
Hagop S
HS
Department of Nematology, University of California at Riverside, CA 92521, USA.|Graduate Program in Genetics, Genomics & Bioinformatics, University of California at Riverside, CA 92521, USA.
Kaloshian
Isgouhi
I
Department of Nematology, University of California at Riverside, CA 92521, USA.|Graduate Program in Genetics, Genomics & Bioinformatics, University of California at Riverside, CA 92521, USA.|Institute for Integrative Genome Biology, University of California at Riverside, CA 92521, USA.|Center for Plant Cell Biology, University of California at Riverside, CA 92521, USA.
Eulgem
Thomas
T
Graduate Program in Genetics, Genomics & Bioinformatics, University of California at Riverside, CA 92521, USA.|Institute for Integrative Genome Biology, University of California at Riverside, CA 92521, USA.|Center for Plant Cell Biology, University of California at Riverside, CA 92521, USA.|Department of Botany and Plant Sciences, University of California at Riverside, CA 92521, USA.
D000595:Amino Acid Sequence; D000818:Animals; D001042:Aphids; D017360:Arabidopsis / Q000235:genetics / Q000276:immunology* / Q000378:metabolism; D004269:DNA, Bacterial / Q000235:genetics; D018506:Gene Expression Regulation, Plant; D020868:Gene Silencing; D007113:Immunity, Innate; D018551:Solanum lycopersicum / Q000235:genetics / Q000276:immunology* / Q000378:metabolism; D008969:Molecular Sequence Data; D016254:Mutagenesis, Insertional; D009348:Nematoda / Q000472:pathogenicity; D020411:Oligonucleotide Array Sequence Analysis; D010802:Phylogeny; D010935:Plant Diseases / Q000235:genetics*; D010940:Plant Proteins / Q000235:genetics / Q000378:metabolism*; D044224:Pseudomonas syringae / Q000472:pathogenicity; D018749:RNA, Plant / Q000235:genetics; D020156:Salicylic Acid / Q000494:pharmacology; D014157:Transcription Factors / Q000235:genetics / Q000378:metabolism*
D004269:DNA, Bacterial; D010940:Plant Proteins; D018749:RNA, Plant; C036483:T-DNA; D014157:Transcription Factors; D020156:Salicylic Acid
Abramovitch, R.B., Anderson, J.C. and Martin, G.B. (2006) Bacterial elicitation and evasion of plant innate immunity. Nat. Rev. Mol. Cell Biol. 7, 601-611.
Abuqamar, S., Chen, X., Dhawan, R., Bluhm, B., Salmeron, J., Lam, S., Dietrich, R.A. and Mengiste, T. (2006) Expression profiling and mutant analysis reveals complex regulatory networks involved in Arabidopsis response to Botrytis infection. Plant J. 48, 28-44.
Alonso, J.M., Stepanova, A.N., Leisse, T.J. et al. (2003) Genome-wide insertional of Arabidopsis thaliana. Science, 301, 653-657.
Asai, T., Tena, G., Plotnikova, J., Willmann, M.R., Chiu, W.-L., Gomez-Gomez, L., Boller, T., Ausubel, F.M. and Sheen, J. (2002) MAP kinase signalling cascade in Arabidopsis innate immunity. Nature, 415, 977-980.
Benjamini, Y., Drai, D., Elmer, G., Kafkafi, N. and Golani, I. (2001) Controlling the false discovery rate in behavior genetics research. Behav. Brain Res. 125, 279-284.
Bhattarai, K.K., Li, Q., Liu, Y., Dinesh-Kumar, S.P. and Kaloshian, I. (2007a) The MI-1-mediated pest resistance requires Hsp90 and Sgt1. Plant Physiol. 144, 312-323.
Bhattarai, K.K., Xie, Q.G., Pourshalimi, D., Younglove, T. and Kaloshian, I. (2007b) Coil-dependent signaling pathway is not required for Mi-1-mediated potato aphid resistance. Mol. Plant-Microbe Interact. 20, 276-282.
Bhattarai, K.K., Xie, Q.G., Mantelin, S., Bishnoi, U., Girke, T., Navarre, D.A. and Kaloshian, I. (2008) Tomato susceptibility to root-knot nematodes requires an intact jasmonic acid signaling pathway. Mol. Plant-Microbe Interact. 21, 1205-1214.
Bisgrove, S.R., Simonich, M.T., Smith, N.M., Sattler, N.M. and Innes, R.W. (1994) A disease resistance gene in Arabidopsis with specificity for two different pathogen avirulence genes. Plant Cell, 6, 927-933.
Cheng, Y.T., Germain, H., Wiermer, M. et al. (2009) Nuclear pore complex component MOS7/Nup88 is required for innate immunity and nuclear accumulation of defense regulators in Arabidopsis. Plant Cell, 21, 2503-2516.
Chisholm, S.T., Coaker, G., Day, B. and Staskawicz, B.J. (2006) Host-microbe interactions: shaping the evolution of the plant immune response. Cell, 124, 803-814.
Czechowski, T., Bari, R.P., Stitt, M., Scheible, W.R. and Udvardi, M.K. (2004) Real-time RT-PCR profiling of over 1400 Arabidopsis transcription factors: unprecedented sensitivity reveals novel root- and shoot-specific genes. Plant J. 38, 366-379.
Deslandes, L., Olivier, J., Theulieres, F., Hirsch, J., Feng, D.X., Bittner-Eddy, P., Beynon, J. and Marco, Y. (2002) Resistance to Ralstonia solanacearum in Arabidopsis thaliana is conferred by the recessive RRS1-R gene, a member of a novel family of resistance genes. Proc. Natl Acad. Sci. USA, 99, 2404-2409.
Deslandes, L., Olivier, J., Peeters, N., Feng, D.X., Khounlotham, M., Boucher, C., Somssich, I., Genin, S. and Marco, Y. (2003) Physical interaction between RRS1-R, a protein conferring resistance to bacterial wilt, and PopP2, a type III effector targeted to the plant nucleus. Proc. Natl Acad. Sci. USA, 100, 8024-8029.
Dong, J., Chen, C. and Chen, Z. (2003) Expression profiles of the Arabidopsis WRKY gene superfamily during plant defense response. Plant Mol. Biol. 51, 21-37.
Eulgem, T. and Somssich, I.E. (2007) Networks of WRKY transcription factors in defense signaling. Curr. Opin. Plant Biol. 10, 366-371.
Eulgem, T., Rushton, P.J., Robatzek, S. and Somssich, I.E. (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci. 5, 199-206.
Eulgem, T., Weigman, V.J., Chang, H.-S., McDowell, J.M., Holub, E.B., Glazebrook, J., Zhu, T.A. and Dangl, J.L. (2004) Gene expression signatures from three genetically separable resistance gene signaling pathways for downy mildew resistance. Plant Physiol. 135, 1129-1144.
Ginzinger, D.G. (2002) Gene quantification using real-time quantitative PCR: an emerging technology hits the mainstream. Exp. Hematol. 30, 503-512.
Glazebrook, J., Zook, M., Mert, F., Kagan, I., Rogers, E.E., Crute, I.R., Holub, E.B. and Ausubel, F.M. (1997) Phytoalexin-deficient mutants of Arabidopsis reveal that PAD4 encodes a regulatory factor and that four PAD genes contribute to downy mildew resistance. Genetics, 146, 381-392.
Horak, C.E. and Snyder, M. (2002) Global analysis of gene expression in yeast. Funct. Integr. Genomics, 2, 171-180.
Jones, J.D. and Dangl, J.L. (2006) The plant immune system. Nature, 444, 323-329.
Journot-Catalino, N., Somssich, I.E., Roby, D. and Kroj, T. (2006) The transcription factors WRKY11 and WRKY17 act as negative regulators of basal resistance in Arabidopsis thaliana. Plant Cell, 18, 3289-3302.
Kalde, M., Barth, M., Somssich, I.E. and Lippok, B. (2003) Members of the Arabidopsis WRKY group III transcription factors are part of different plant defense signaling pathways. Mol. Plant-Microbe Interact. 16, 295-305.
Knoth, C., Ringler, J., Dangl, J.L. and Eulgem, T. (2007) Arabidopsis WRKY70 is required for full RPP4-mediated disease resistance and basal defense against Hyaloperonospora parasitica. Mol. Plant-Microbe Interact. 20, 120-128.
Knoth, C., Salus, M.S., Girke, T. and Eulgem, T. (2009) The synthetic elicitor 3,5-dichloroanthranilic acid induces NPR1-dependent and NPR1-independent mechanisms of disease resistance in Arabidopsis. Plant Physiol. 150, 333-347.
Kunkel, B.N., Bent, A.F., Dahlbeck, D., Innes, R.W. and Staskawicz, B.J. (1993) RPS2, an Arabidopsis disease resistance locus specifying recognition of Pseudomonas syringae strains expressing the avirulence gene avrRpt2. Plant Cell, 5, 865-875.
Lambert, K., Ferrie, B., Nombela, G., Brenner, E. and Williamson, V. (1999) Identification of genes whose transcripts accumulate rapidly in tomato after root-knot nematode infection. Physiol. Mol. Plant Pathol. 55, 341-348.
Li, J., Brader, G., Kariola, T. and Palva, E.T. (2006a) WRKY70 modulates the selection of signaling pathways in plant defense. Plant J. 46, 477-491.
Li, Q., Xie, Q.G., Smith-Becker, J., Navarre, D.A. and Kaloshian, I. (2006b) Mi-1-mediated aphid resistance involves salicylic acid and mitogen-activated protein kinase signaling cascades. Mol. Plant-Microbe Interact. 19, 655-664.
Lippok, B., Birkenbihl, R.P., Rivory, G., Brummer, J., Schmelzer, E., Logemann, E. and Somssich, I.E. (2007) Expression of AtWRKY33 encoding a pathogen- or PAMP-responsive WRKY transcription factor is regulated by a composite DNA motif containing W box elements. Mol. Plant-Microbe Interact. 20, 420-429.
Liu, Y., Schiff, M. and Dinesh-Kumar, S.P. (2004) Involvement of MEK1 MAPKK, NTF6 MAPK, WRKY/MYB transcription factors, COI1 and CTR1 in N-mediated resistance to tobacco mosaic virus. Plant J. 38, 800-809.
Mantelin, S., Bhattarai, K.K. and Kaloshian, I. (2009) Ethylene contributes to potato aphid susceptibility in a compatible tomato host. New Phytol. 183, 444-456.
Martinez de Ilarduya, O., Nombela, G., Hwang, C.F., Williamson, V.M., Muniz, M. and Kaloshian, I. (2004) Rme1 is necessary for Mi-1-mediated resistance and acts early in the resistance pathway. Mol. Plant-Microbe Interact. 17, 55-61.
McDowell, J.M., Cuzick, A., Can, C., Beynon, J., Dangl, J.L. and Holub, E.B. (2000) Downy mildew (Peronospora parasitica) resistance genes in Arabidopsis vary in functional requirements for NDR1, EDS1, NPR1, and salicylic acid accumulation. Plant J. 22, 523-530.
Moran, N.A., Plague, G.R., Sandstrom, J.P. and Wilcox, J.L. (2003) A genomic perspective on nutrient provisioning by bacterial symbionts of insects. Proc. Natl Acad. Sci. USA, 100(Suppl. 2), 14543-14548.
Nimchuk, Z., Eulgem, T., Holt, I.B. and Dangl, J.L. (2003) Recognition and response in the plant immune system. Annu. Rev. Genet. 37, 579-609.
Noutoshi, Y., Ito, T., Seki, M., Nakashita, H., Yoshida, S., Marco, Y., Shirasu, K. and Shinozaki, K. (2005) A single amino acid insertion in the WRKY domain of the Arabidopsis TIR-NBS-LRR-WRKY-type disease resistance protein SLH1 (sensitive to low humidity 1) causes activation of defense responses and hypersensitive cell death. Plant J. 43, 873-888.
Pedley, K.F. and Martin, G.B. (2003) Molecular basis of Pto-mediated resistance to bacterial speck disease in tomato. Annu. Rev. Phytopathol. 41, 215-243.
Riechmann, J.L., Heard, J., Martin, G. et al. (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science, 290, 2105-2110.
Rushton, P.J., Tovar Torres, J., Parniske, M., Wernert, P., Hahlbrock, K. and Somssich, I.E. (1996) Interaction of elicitor-induced DNA-binding proteins with elicitor response elements in the promoters of parsley PR1 genes. EMBO J. 15, 5690-5700.
Schwessinger, B. and Zipfel, C. (2008) News from the frontline: recent insights into PAMP-triggered immunity in plants. Curr. Opin. Plant Biol. 11, 389-395.
Shen, Q.H., Saijo, Y., Mauch, S., Biskup, C., Bieri, S., Keller, B., Seki, H., Ulker, B., Somssich, I.E. and Schulze-Lefert, P. (2007) Nuclear activity of MLA immune receptors links isolate-specific and basal disease-resistance responses. Science, 315, 1098-1103.
Smyth, G. (2004) Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3, 3-7.
Stockinger, E.J. and Walling, L.L. (1994) A chlorophyll a/b-binding protein gene from soybean (Glycine max [L.] Merr.). Plant Physiol. 104, 1475-1476.
Swofford, D.L. (2002) PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sunderland, MA: Sinauer Associates.
Tao, Y., Xie, Z., Chen, W., Glazebrook, J., Chang, H.S., Han, B., Zhu, T., Zou, G. and Katagiri, F. (2003) Quantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae. Plant Cell, 15, 317-330.
Tornero, P. and Dangl, J.L. (2001) A high throughput method for quantifying growth of phytopathogenic bacteria in Arabidopsis thaliana. Plant J. 28, 475-481.
Ulker, B. and Somssich, I.E. (2004) WRKY transcription factors: from DNA binding towards biological function. Curr. Opin. Plant Biol. 7, 491-498.
van der Biezen, E.A., Freddie, C.T., Kahn, K., Parker, J.E. and Jones, J.D.G. (2002) Arabidopsis RPP4 is a member of the RPP5 multigene family of TIR-NB-LRR genes and confers downy mildew resistance through multiple signalling components. Plant J. 29, 439-451.
Wang, D., Amornsiripanitch, N. and Dong, X. (2006) A genomic approach to identify regulatory nodes in the transcriptional network of systemic acquired resistance in plants. PLoS Pathog. 2, e123.
Wirthmueller, L., Zhang, Y., Jones, J.D. and Parker, J.E. (2007) Nuclear accumulation of the Arabidopsis immune receptor RPS4 is necessary for triggering EDS1-dependent defense. Curr. Biol. 17, 2023-2029.
Wu, K.L., Guo, Z.J., Wang, H.H. and Li, J. (2005) The WRKY family of transcription factors in rice and Arabidopsis and their origins. DNA Res. 12, 9-26.
Xu, X., Chen, C., Fan, B. and Chen, Z. (2006) Physical and functional interactions between pathogen-induced Arabidopsis WRKY18, WRKY40, and WRKY60 transcription factors. Plant Cell, 18, 1310-1326.