Skip to main content
SpringerLink
Log in

Chemical induction of disease resistance in rice is correlated with the expression of a gene encoding a nucleotide binding site and leucine-rich repeats

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Probenazole (3-allyloxy-1,2-benzisothiazole-1,1-dioxide) is an agricultural chemical primarily used to prevent rice blast disease. Probenazole-treated rice acquires resistance to blast fungus irrespective of the rice variety. The chemical is applied prophylactically, and is thought to induce or bolster endogenous plant defenses. However, the mechanisms underlying this effect have not been established. To understand the mode of the chemical's action, we screened for novel probenazole-responsive genes in rice by means of differential display and identified a candidate gene, RPR1. RPR1 contains a nucleotide binding site and leucine-rich repeats, thus sharing structural similarity with known disease resistance genes. The expression of RPR1 in rice can be up-regulated by treatment with chemical inducers of systemic acquired resistance (SAR) and by inoculation with pathogens. RPR1-related sequences in rice varieties seem to be varied in sequence and/or expression, indicating that RPR1 itself is not a crucial factor for induced resistance in rice. However, Southern blot analysis revealed the existence of homologous sequences in all varieties examined. While the role of RPR1 has yet to be clarified, this is the first report of the identification of a member of this gene class and its induction during the systemic expression of induced disease resistance.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Bradley, D.J., Kjellbom, P. and Lamb, C.J. 1992. Elicitor-and wound-induced oxidative cross-linking of a proline-rich plant cell wall protein: a novel, rapid defense response. Cell 70: 21-30.

    Google Scholar 

  • Cai, D., Kleine, M., Kifle, S., Harloff, H.-J., Sandal, N.N., Marcker, K.A., Klein-Lankhorst, R.M., Salentijn, E.M.J., Lange, W., Stiekema, W.J., Wyss, U., Grundler, F.M.W. and Jung, C. 1997. Positional cloning of a gene for nematode resistance in sugar beet. Science 275: 832-834.

    Google Scholar 

  • Cao, H., Glazebrook, J., Clarke, J.D., Volko, S. and Dong, X 1997. The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell 88: 57-63.

    Google Scholar 

  • Causse, M.A., Fulton, T.M., Cho, Y.G., Ahn, S.N., Chunwongse, J., Wu, K., Xiao, J., Yu, Z., Ronald, P.C., Harrington, S.E., Second, G., McCouch, S.R. and Tanksley, S.D. 1994. Saturated molecular map of the rice genome based on an interspecific backcross population. Genetics 138: 1251-1274.

    Google Scholar 

  • Flor, H. 1971. Current status of the gene-for-gene concept. Annu. Rev. Phytopath. 9: 275-296.

    Google Scholar 

  • Friedrich, L., Lawton, K., Dincher, S., Winter, A., Staub, T., Uknes, S., Kessmann, H. and Ryals, J. 1996. Benzothiadiazole induces systemic acquired resistance in tobacco. Plant J. 10: 61-70.

    Google Scholar 

  • Gaffney, T., Friedrich, L., Vernooij, B., Negrotto, D., Nye, G., Uknes, S., Ward, E., Kessmann, H. and Ryals, J. 1993. Requirement of salicylic acid for the induction of systemic acquired resistance. Science 261: 754-756.

    Google Scholar 

  • Grant, M.R., Godiard, L., Straube, E., Ashfield, T., Lewald, J., Sattler, A., Innes, R.W. and Dangl, J.L. 1995. Structure of the Arabidopsis RPM1 gene enabling dual specificity disease resistance. Science 269: 843-846.

    Google Scholar 

  • Görlach, J., Volrath, S., Knauf-Beiter, G., Hengy, G., Beckhove, U., Kogel, K.-H., Oostendorp, M., Staub, T., Ward, E., Kessmann, H. and Ryals, J 1996. Benzothiadiazole, a novel class of inducers of systemic acquired resistance, activates gene expression and disease resistance in wheat. Plant Cell 8: 629-643.

    Google Scholar 

  • Hammerschmid, R., Nuckles, E.M. and Kuc, J. 1982. Association of enhanced peroxidase activity with induced systemic resistance of cucumber to Colletotrichum. Physiol. Plant Path. 20: 73-82.

    Google Scholar 

  • Hanks, S.K., Quinn, A.M. and Hunter, T. 1988. The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science 241: 42-52.

    Google Scholar 

  • Kobe, B., Deisenhofer, J. 1994. The leucine-rich repeat: a versatile binding motif. Trends Biochem. Sci. 19: 415-421.

    Google Scholar 

  • Lamb, C.J., Lawton, M.A., Dron, M. and Dixon, R.A. 1989. Signals and transduction mechanisms for activation of plant defenses against microbial attack. Cell 56: 215-224.

    Google Scholar 

  • Lander, E.S., Green, P., Abrahamson, J., Barlow, A., Daly, M.J., Lincoln, S.E. and Newburg, L. 1987. MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and populations. Genomics 1: 174-181.

    Google Scholar 

  • Lawrence, G.J., Finnegan, E.J., Ayliffe, M.A. and Ellis, J.G. 1995. The L6 gene for flax rust resistance is related to the Arabidopsis bacterial resistance gene RPS2 and the tobacco viral resistance gene N. Plant Cell 7: 1195-1206.

    Google Scholar 

  • Lawton, K., Friedrich, L., Hunt, M., Weymann, K., Staub, T., Kessmann, H. and Ryals, J. 1996. Benzothiadiazole induces disease resistance in Arabidopsis by activation of the systemic acquired resistance signal transduction pathway. Plant J. 10: 71-82.

    Google Scholar 

  • Leister, D., Kurth, J., Laurie, D.A., Yano, M., Sasaki, T., Devos, K., Graner, A. and Schulze-Lefert, P. 1998. Rapid reorganization of resistance gene homologues in cereal genomes. Proc. Natl. Acad. Sci. USA 95: 370-375.

    Google Scholar 

  • Levine, A., Tenhaken, R., Dixon, R. and Lamb, C. 1994. H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79: 583-593.

    Google Scholar 

  • Liang, P. and Pardee, A.B. 1992. Differential display of eukaryotic messenger RNA by means of the polymerase chain reaction. Science 257: 967-971.

    Google Scholar 

  • Midoh, N. and Iwata, M. 1996. Cloning and characterization of a probenazole-inducible gene for an intracellular pathogenesisrelated protein in rice. Plant Cell Physiol. 37: 9-18.

    Google Scholar 

  • Midoh, N. and Iwata, M. 1997. Expression of defense-related genes by probenazole or 1,2-benzisothiazole-3(2H)-one 1,1-dioxide. J. Pesticide Sci. 22: 45-47.

    Google Scholar 

  • Milligan, S.B., Bodeau, J., Yaghoobi, J., Kaloshian, I., Zabel, P. and Williamson, V.M. 1998. The root knot nematode resistance gene Mi from tomato is a member of the leucine zipper, nucleotide binding, leucine-rich repeat family of plant genes. Plant Cell 10: 1307-1319.

    Google Scholar 

  • Minami, E., Ozeki, Y., Matsuoka, M., Koizuka, N. and Tanaka Y. 1989. Structure and some characterization of the gene for phenylalanine ammonia-lyase from rice plants. Eur. J. Biochem. 185: 19-25.

    Google Scholar 

  • Mindrinos, M., Katagiri, F., Yu, G.-L. and Ausubel, F.M. 1994. The A. thaliana disease resistance gene RPS2 encodes a protein containing a nucleotide-binding site and leucine-rich repeats. Cell 78: 1089-1099.

    Google Scholar 

  • Nishizawa, Y. and Hibi, T. 1991. Rice chitinase gene: cDNA cloning and stress-induced expression. Plant Sci. 76: 211-218.

    Google Scholar 

  • Ori, N., Eshed, Y., Paran, I., Presting, G., Aviv, D., Tanksley, S., Zamir, D. and Fluhr, R. 1997. The I2C family from the wilt disease resistance locus I2 belongs to the nucleotide binding, leucineriche repeat superfamily of plant resistance genes. Plant Cell 9: 521-532.

    Google Scholar 

  • Parker, J.E., Coleman, M.J., Szabo, V., Frost, L.N., Schmidt, R., van der Biezen, E.A., Moores, T., Dean, C., Daniels, M.J. and Jones, J.D.G 1997. The Arabidopsis downy mildew resistance gene RPP5 shares similarity to the toll and interleukin-1 receptors with N and L6. Plant Cell 9: 879-894.

    Google Scholar 

  • Parniske, M., Hammond-Kosack, K.E., Golstein, C., Thomas, C.M., Jones, D.A., Harrison, K., Wulff, B.B.H. and Jones, J.D.G. 1997. Novel disease resistance specificities result from sequence exchange between tandemly repeated genes at the Cf-4/9 locus of tomato. Cell 91: 821-832.

    Google Scholar 

  • Reimmann, C., Ringli, C. and Dudler, R. 1992. Complementary DNA cloning and sequence analysis of a pathogen-induced putative peroxidase from rice. Plant Physiol. 100: 1611-1612.

    Google Scholar 

  • Rogers, S.O. and Bendich, A.J. 1985. Extraction of DNA from milligram amounts of fresh, herbarium and mummified plant tissues. Plant Mol Biol 5: 69-76.

    Google Scholar 

  • Ryals, J.A., Neuenschwander, U.H., Willits, M.G., Molina, A., Steiner, H.-Y. and Hunt, M.D. 1996. Systemic acquired resistance. Plant Cell 8: 1809-1819.

    Google Scholar 

  • Ryals, J.A., Weymann, K., Lawton, K., Freidrich, L., Ellis, D., Steiner, H.-Y., Johnson, J., Delaney, T.P., Jesse, T., Vos, P. and Uknes, S. 1997. The Arabidopsis NIM1 protein shows homology to the mammalian transcription factor inhibitor IkB. Plant Cell 9: 425-439.

    Google Scholar 

  • Salmeron, J.M., Oldroyd, G.E.D., Rommens, C.M.T., Scofield, S.R., Kim, H.-S., Lavelle, D.T., Dahlbeck, D. and Staskawicz, B.J. 1996. Tomato Prf is a member of the leucine-rich repeat class of plant disease resistance genes and lies embedded within the Pto kinase gene cluster. Cell 86: 123-133.

    Google Scholar 

  • Saraste, M., Sibbald, P.R. and Wittinghofer, A. 1990. The P-loop: a common motif in ATP-and GTP-binding proteins. Trends Biochem. Sci. 15: 430-434.

    Google Scholar 

  • Shimura, M., Iwata, M., Tashiro, N., Sekizawa, Y., Suzuki, Y., Mase, S. and Watanabe, T. 1981. Anti-conidial germination factors induced in the presence of probenazole and properties of four active substances. Agric. Biol. Chem. 45: 1431-1435.

    Google Scholar 

  • Silverman, P., Seskar, M., Kanter, D., Schweizer, P., Métraux, J.-P. and Raskin, I. 1995. Salicylic acid in rice. Plant Physiol 108: 633-639.

    Google Scholar 

  • Smith, J.A. and Métraux, J.P. 1991. Pseudomonas syringae pv. syringae induces systemic resistance to Pyricularia oryzae in rice. Physiol. Mol. Plant Path. 39: 451-461.

    Google Scholar 

  • Song, W.-Y., Pi, L.-Y., Wang, G.-L., Gardner, J., Holsten, T. and Ronald, P. 1997. Evolution of the rice Xa21 disease resistance gene family. Plant Cell 9: 1279-1287.

    Google Scholar 

  • Traut, T.W. 1994. The functions and consensus motifs of nine types of peptide segments that form different types of nucleotidebinding sites. Eur. J. Biochem. 222: 9-19.

    Google Scholar 

  • Tsunematsu, H., Yoshimura, A., Harushima, Y., Nagamura, Y., Kurata, N., Yano, M., Sasaki, T. and Iwata, N. 1996. RFLP framework map using recombinant inbred lines in rice. Breed. Sci. 46: 279-284.

    Google Scholar 

  • Valent, B., Farrall, L. and Chumley, F.G. 1991. Magnaporthe grisea genes for pathogenicity and virulence identified through a series of backcrosses. Genetics 127: 87-101.

    Google Scholar 

  • Verwoerd, T.C., Dekker, B.M.M. and Hoekema, A. 1989. A smallscale procedure for the rapid isolation of plant RNAs. Nucl. Acids Res. 17: 2362.

    Google Scholar 

  • Ward, E.R., Uknes, S.J., Williams, S.C., Dincher, S.S., Wiederhold, D.L., Alexander, D.C., Ahl-Goy, P., Métraux, J.-P. and Ryals, J.A. 1991. Coordinate gene activity in response to agents that induce systemic acquired resistance. Plant Cell 3: 1085-1094.

    Google Scholar 

  • Warren, R.F., Henk, A., Mowery, P., Holub, E. and Innes, R.W. 1998. A mutation within the leucine-rich repeat domain of the Arabidopsis disease resistance gene RPS5 partially suppresses multiple bacterial and downy mildew resistance genes. Plant Cell 10: 1439-1452.

    Google Scholar 

  • Watanabe, T., Sekizawa, Y., Shimura, M., Suzuki, Y., Matsumoto, K., Iwata, M. and Mase, S. 1979. Effects of probenazole (Oryzemate) on rice plants with reference to controlling rice blast. J. Pesticide Sci. 4: 53-59.

    Google Scholar 

  • White, R.F. 1979. Acetylsalicylic acid (aspirin) induces resistance to tobacco mosaic virus in tobacco. Virology 99: 410-412.

    Google Scholar 

  • Whitham, S., Dinesh-Kumar, S.P., Choi, D., Hehl, R., Corr, C. and Baker, B. 1994. The product of the tobacco mosaic virus resistance gene N: similarity to Toll and the interleukin-1 receptor. Cell 78: 1101-1115.

    Google Scholar 

  • Yoshimura, S., Yamanouchi, U., Katayose, Y., Toki, S., Wang, ZW., Kono, I., Kurata, N., Yano, M., Iwata, N. and Sasaki, T. 1998. Expression of Xa1, a bacterial blight-resistance gene in rice, is induced by bacterial inoculation. Proc. Natl. Acad. Sci. USA 95: 1663-1668.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Mitsui Plant Biotechnology Research Institute, TCI D-21, Sengen 2-1-6, Tsukuba, 305-0047, Japan

    Koji Sakamoto, Yuichi Tada, Hiromori Akagi & Norio Ichikawa

  2. Life Science Laboratory, Mitsui Chemicals, Inc., Togo 1144, Mobara, 297-0017, Japan

    Yumi Yokozeki & Tatsuhito Fujimura

  3. Aichi-ken Agriculture Research Center Institute, Mountainous Region Agricultural Reset Institute, Susogaeto 11, Inahashi, Inabu, Kita-shitara 441-25, Aichi, Japan

    Nagao Hayashi

Authors
  1. Koji Sakamoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yuichi Tada
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yumi Yokozeki
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hiromori Akagi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Nagao Hayashi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Tatsuhito Fujimura
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Norio Ichikawa
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sakamoto, K., Tada, Y., Yokozeki, Y. et al. Chemical induction of disease resistance in rice is correlated with the expression of a gene encoding a nucleotide binding site and leucine-rich repeats. Plant Mol Biol 40, 847–855 (1999). https://doi.org/10.1023/A:1006244323934

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1006244323934

Search

Navigation