Abstract
In the yeast two-hybrid system, the Pto kinase interacts with three putative transcription factors Pti4, Pti5 and Pti6. The Pti4/5/6 proteins contain a DNA binding domain that recognizes and binds a DNA sequence (5′-AGCCGCC-3′ the 'PR box') present in the promoter region of a large number of genes encoding 'pathogenesis-related' (PR) proteins. We have now investigated the pathogen-induced expression of PR box-containing genes in tomato. We isolated a tomato osmotin gene that contains two PR boxes in its promoter region and demonstrated that the abundance of the osmotin transcript rapidly increases during an incompatible interaction involving Pto-containing tomato plants and the bacterial pathogen Pseudomonas syringae pv. tomato expressing the avrPto gene. In addition, we found that transcripts of two other tomato PR genes (encoding endochitinase and β-1,3-glucanase B) and at least one ACC oxidase gene, all of which contain PR boxes in their promoter regions, rapidly accumulate in the incompatible interaction. These data support the hypothesis that the tomato Pto kinase regulates the expression of certain defense genes in tomato by interaction with transcription factors that bind the PR box.
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Ashfield, M., Hammond-Kosack, K.E., Harrison, K. and Jones, J.D.G. 1994. Cf gene-dependent induction of a β-1,3-glucanase promoter in tomato plants infected with Cladosporium fulvum. Mol. Plant-Microbe Interact. 7: 645—657.
Ausubel, F.M., Brent, R., Kingston, R.E., Moore, D.D., Smith, J.A., Seidman, J.G. and Struhl, K. (Eds.). 1987. Protocols in Molecular Biology, John Wiley, New York.
Barry, C.S., Blume, B., Bouzayen, M., Cooper, W., Hamilton, A.J. and Grierson, D. 1996. Differential expression of the 1-aminocyclopropane-1-carboxylate oxidase gene family of tomato. Plant J. 9: 524–535.
Bent, A.F., Innes, R.W., Ecker, J.R. and Staskawicz, B.J. 1992. Disease development in ethylene-insensitive Arabidopsis thaliana infected with virulent and avirulent Pseudomonas and Xanthomonas pathogens. Mol. Plant-Microbe Interact. 5: 372–378.
Bowling, S.A., Guo, A., Cao, H., Gordon, A.S., Klessig, D.F. and Dong, X. 1994. A mutation in Arabidopsis that leads to constitutive expression of systemic acquired resistance. Plant Cell 6: 1845–1857.
Brady, C.J. and Speirs, J. 1991. Ethylene in fruit ontogeny and abscission. In: A.K. Mattoo and J.C. Suttle (Eds), The Plant Hormone Ethylene, CRC Press, Boca Raton, FL, pp. 235–258.
Cameron, R.K., Dixon, R.A., Lamb, C.J. 1994. Biological induced systemic acquired resistance in Arabidopsis thaliana. Plant J. 5: 715–725.
Cao, H., Bowling, S.A., Gordon, A.S. and rDong, X. 1994. Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell 6: 1583–1592.
Danhash, N., Wagemakers, C.A.M., van Kan, J.A.L. and de Wit, P.J.G.M. 1993. Molecular characterization of four chitinase cDNAs obtained from Cladosporium fulvum-infected tomato. Plant Mol. Biol. 22: 1017–1029.
Davidson, A.D., Manners, J.M., Simpson, R.S. and Scott, K.J. 1987. cDNA cloning of mRNAs induced in resistant barley infection by Erysiphe graminis f. sp. hordei. Plant Mol. Biol. 8: 77–85.
Dong, X., Mindrinos, M., Davis, K.R. and Ausubel, F.M. 1991. Induction of Arabidopsis defense genes by virulent and avirulent Pseudomonas syringae strains and by a cloned avirulence gene. Plant Cell 8: 155–168.
Ecker, J. 1996. The ethylene signal transduction pathway in plants. Science 268: 667–675.
Feinberg, A.P. and Vogelstein, B. 1983. A technique for radiolabeling DNA fragments to high specific activity. Anal. Biochem. 132: 6–13.
Goldsbrough, P.B. and Cullis, C.A. 1981. Characterization of the genes for ribosomal RNA in flax. Nucl. Acids Res. 9: 1301–1309.
Gurley, W.B. and Key, J.L. 1991. Transcriptional regulation of the heat-shock response: a plant perspective. Biochemistry 30: 1–12.
Hart, C.M., Nagy, F. and Meins Jr. F. 1993. A 61 bp enhancer element of the tobacco β-1,3-glucanase B gene interacts with one or more regulated nuclear proteins. Plant Mol. Biol. 21: 121–131.
Jakobek, J.L. and Lindgren, P.B. 1993. Generalized induction of defense responses in bean is not correlated with the induction of the hypersensitive reaction. Plant Cell 5: 49–56.
Jia, Y., Loh, Y.-T., Zhou, J. and Martin, G.B. 1997. Alleles of Pto and Fen occur in bacterial speck-susceptible and fenthioninsensitive tomato cultivars and encode active protein kinases. Plant Cell 9: 61–73.
Kiedrowski, S., Kawalleck, P., Hahlbrock, K., Somssich, I.E. and Dangl, J. 1992. Rapid activation of a novel plant defense gene is strictly dependent on the Arabidopsis RPM1 disease resistance. EMBO J. 11: 4677–4684.
King, G.J., Victoria, A., Hussey Jr., C.E., Wurtele, E.S. and Lee, M. 1988. Isolation and characterization of a tomato cDNA clone which codes for a salt-induced protein. Plant Mol. Biol. 10: 401–412.
Lawton, K.A., Potter, S.L., Uknes, S. and Ryals, J. 1994. Acquired resistance signal transduction in Arabidopsis is ethylene independent. Plant Cell 6: 581–588.
Linthorst, H.J.M. 1991. Pathogenesis-related proteins of plants. Crit. Rev. Plant Sci. 10: 123–150.
Liu, D., Raghothama, K.G., Hasegawa, P.M. and Bressan, R.A. 1994. Osmotin overexpression in potato delays development of disease symptoms. Proc. Natl. Acad Sci. USA 91: 1888–1892.
Liu, D., Narasimhan, M.L., Xu, Y., Raghothama, K.G., Hasegawa, P.M., Bressan, R.A. 1995. Fine structure and function of the osmotin gene promoter. Plant Mol. Biol. 29: 1015–1026.
Martin, G.B., Brommonschenkel, S., Chunwongse, J., Frary, A., Ganal, M.W., Spivey, R., Wu, T., Earle, E.D. and Tanksley, S.D. 1993. Map-based cloning of a protein kinase gene conferring disease resistance in tomato. Science 262: 1432–1436.
Mason, H.S., DeWald, D.B. and Mullet, J.E. 1993. Identification of a methyl jasmonate-responsive domain in the soybean vspB promoter. Plant Cell 5: 241–251.
Matton, D.P., Prescott, G., Bertrand, C., Camirand, A. and Brisson, N. 1993. Identification of cis-acting elements involved in the regulation of the pathogenesis related gene STH-2 in potato. Plant Mol. Biol. 22: 279–291.
Melchers, L.S., Sela-Buurlage, M.B., Vloemans, S.A., Woloshuk, C.P., van Roekel, J.S., Pen, J., van den Elzen, P.J. and Cornelissen, B.J. 1993. Extracellular targeting of the vacuolar tobacco proteins AP24, chitinase and β-1,3-glucanase in transgenic plants. Plant Mol. Biol. 21: 583–593.
Nagao, R.T., Goekjian, V.H., Hong, J.C. and Key, J.L. 1993. Identi-fication of protein binding DNA sequences in an auxin-regulated gene of soybean. Plant Mol. Biol. 21: 1147–1162.
Nelson, D.E., Raghothama, K.G., Singh, N.K., Hasegawa, P.M. and Bressan, R.A. 1992. Analysis of structure and transcriptional activation of an osmotin gene. Plant Mol. Biol. 19: 577–588.
Nemestothy, G.S. and Guest, D.I. 1990. Phytoalexin accumulation, phenylalanine ammonia lyase activity and ethylene biosynthesis in fosetyl-Al treated resistant susceptible tobacco cultivars infected with Phytophthora nicotianae var. nicotianae. Physiol. Mol. Plant Path. 37: 207–219.
Ohl, S., Hedrick, S.A., Chory, J. and Lamb, C.J. 1990. Functional properties of phenylalanine ammonia-lyase promoter from Arabidopsis. Plant Cell 2: 837–848.
Ohme-Takagi, M. and Shinshi, H. 1995. Ethylene-inducible DNAbinding proteins that interact with an ethylene-responsive element. Plant Cell 7: 173–182.
Palm, C.J., Costa, M.A., An, G. and Ryan, C.A. 1990. Woundinducible nuclear protein binds DNA fragments that regulate a proteinase inhibitor II gene from potato. Proc. Natl. Acad. Sci. USA 87: 603–607.
Paradies, I., Konze, J.R., Elstner, E.F. and rPaxton, J. 1980. Ethylene: indicator but not inducer of phytoalexin synthesis in soybean. Plant Physiol. 66: 1106–1109.
Pastuglia, M., Roby, D., Dumas, C. and Cock, J.M. 1997. Rapid induction by wounding and bacterial infection of an S gene family receptor-like kinase gene in Brassica oleracea. Plant Cell 9: 49–60.
Perry, L.K. and Francki, R.I.B. 1992. Insect-mediated transmission of mixed and reasserted cucumovirus genomic RNAs. J. Gen. Virol. 73: 2105–2114.
Reuber, T.L. and Ausubel, F.M. 1996.Isolation of Arabidopsis genes that differentiate between resistance responses mediated by the RPS2 and RPM1 disease resistance genes. Plant Cell 8: 241–249.
Ronald, P.C., Salmeron, J.M., Carland, F.M. and Staskawicz, B.J. 1992. The cloned avirulence gene avrPto induces disease resistance in tomato cultivars containing the Pto resistance gene. J Bact. 174: 1604–1611.
Salmeron, J.M., Baker, S.J., Carland, F.M., Mehta, A.Y. and Staskawicz, B.J. 1996. Tomato Prf is a member of the leucinerich repeat class of plant disease resistance genes and lies embedded within the Pto kinase gene cluster. Cell 86: 123–133.
Sato, F., Kitajimz, S., Koyama, T. and Yamada, Y. 1996. Ethylene induced gene expression of osmotin-like protein, a neutral isoform of tobacco PR-5, is mediated by the GCCGCC cissequence. Plant Cell Physiol. 37: 249–255.
Scofield, S.R., Tobias, C.M., Rathjen, J.P., Chang, J.H., Lavelle, D.T., Michelmore, R.W. and Staskawicz, B.J. 1996. Molecular basis of gene-for-gene specificity in bacterial speck disease of tomato. Science 274: 2063–2065.
Sessa, G., Meller, Y. and Fluhr, R. 1995. A GCC element and a Gbox motif participate in ethylene-induced expression of the PRB-1b gene. Plant Mol. Biol. 28: 857–863.
Sutliff, T.D., Lanahan, M.B. and Ho, T.-H.D. 1993. Gibberellin treatment stimulates nuclear factor binding to the gibberellin response complex in a barley α-amylase promoter. Plant Cell 5: 1681–1692.
Tang, X., Frederick, R.D., Zhou, J., Halterman, D.A., Jia, Y. and Martin, G.B. 1996. Initiation of plant disease resistance by physical interaction of avrPto and Pto kinase. Science 274: 2060–2063.
van Kan, J.A.L., Joosten, M.H.A.J., Wagemakers, C.A.M., van den Berg-Velthuis, G.C.M. and de Wit, P.J.G.M. 1992. Differential accumulation of mRNAs encoding extracellular and intracellular PR proteins in tomato induced by virulent and avirulent races of Cladosporium fulvum. Plant Mol. Biol. 20: 513–527.
van Loon, L.C. and van Kammen, A. 1970. Polyacrylamide disc electrophoresis of the soluble leaf proteins from Nicotiana tabacum cvs. ‘Xanthi-nc’ and 'samsun NN'. II. Changes in protein constitutions after infection with tobacco mosaic virus. Virology 40: 199–211.
van Loon, L.C., Pierpoint, W.S., Boller, T. and Conejero, V. 1994. Recommendations for naming plant pathogenesis-related proteins. Plant Mol. Biol. Rep. 12: 245–264.
Voisey, C.R. and Slusarenko, A.J. 1989. Chitinase mRNA and enzyme activity in Phaseolus vulgaris (L.) increase more rapidly in response to avirulent than to virulent cells of Pseudomonas syringae pv. phaseolicola. Physiol. Mol. Plant Path. 35: 403–412.
Wubben, J.P., Lawrence, C.B. and de Wit, P.J.G.M. 1996. Differential induction of chitinase and 1,3-β-glucanase gene expression in tomato by Cladosporium fulvum and its race-specific elicitors. Physiol. Mol. Plant Path. 48: 105–116.
Yang, S.F. and Hoffman, N.E. 1984. Ethylene biosynthesis and its regulation in higher plants. Annu. Rev. Plant Physiol. 35: 155–189.
Zhou, J., Loh, Y.T., Bressan, R.A. and Martin, G.B. 1995. The tomato gene Pti1 encodes a serine/threonine kinase that is phosphorylated by Pto and is involved in the hypersensitive response. Cell 83: 925–935.
Zhou, J., Tang, X. and Martin, G.B. 1997. The Pto kinase conferring resistance to tomato bacterial speck disease interacts with proteins that binds a cis-element of pathogen-related genes. EMBO J. 16: 3207–3218.
Zhu, B., Chen, T.H. and Li, P.H. 1995. Activation of two osmotinlike protein genes by abiotic stimuli and fungal pathogen in transgenic potato plants. Plant Physiol. 108: 929–937.
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Jia, Y., Martin, G.B. Rapid transcript accumulation of pathogenesis-related genes during an incompatible interaction in bacterial speck disease-resistant tomato plants. Plant Mol Biol 40, 455–465 (1999). https://doi.org/10.1023/A:1006213324555
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DOI: https://doi.org/10.1023/A:1006213324555