Skip to main content
SpringerLink
Log in

Characterization of the rice pathogen-related protein Rir1a and regulation of the corresponding gene

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

In rice (Oryza sativa L.), local acquired resistance against Pyricularia oryzae (Cav.), the causal agent of rice blast, can be induced by a preinoculation with the non-host pathogen Pseudomonas syringae pv. syringae. We have cloned a cDNA (Rir1a) and a closely related gene (Rir1b) corresponding to transcripts that accumulate in leaf tissue upon inoculation with P. syringae pv. syringae. The cDNA encodes a putative 107 amino acid protein, Rir1a, that exhibits a putative signal peptide cleavage site in its hydrophobic N-terminal part and a C-terminal part that is relatively rich in glycine and proline. The Rir1b gene contains a Tourist and a Wanderer miniature transposable element in its single intron and encodes a nearly identical protein. Rir1a is similar in sequence (ca. 35% identical and ca. 60% conservatively changed amino acids) to the putative Wir1 family of proteins that are encoded by pathogen-induced transcripts in wheat. Using antibodies raised against a Rir1a-fusion protein we show that Rir1a is secreted from rice protoplasts transiently expressing a 35S::Rir1a construct and that the protein accumulates in the cell wall compartment of rice leaves upon inoculation with P. syringae pv. syringae. Possible roles of Rir1a in pathogen defense are discussed.

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

  1. Alexander D, Goodman RM, Gut-Rella M, Glascock D, Weymann K, Friedrich L, Maddox D, Ahl-Goy P, Luntz T, Ward E, Ryals J: Increased tolerance to two oomycete pathogens in transgenic tobacco expressing pathogenesis-related protein 1a. Proc Natl Acad Sci USA 90: 7327–7331 (1993).

    PubMed  Google Scholar 

  2. Ausubel FM, Brent R, Kingston RE, Moore DD, Smith JA, Seidman JG, Struhl K: Current Protocols in Molecular Biology. Wiley, New York (1987).

    Google Scholar 

  3. Bohlmann H, Clausen S, Behuke S, Giese H, Hiller C, Reimann-Philipp U, Schrader G, Barkholt V, Apel K: Leaf-specific thionins of barley: a novel class of cell wall proteins toxic to plant-pathogenic fungi and possibly involved in the defense mechanism of plants. EMBO J 7: 1559–1565 (1988).

    Google Scholar 

  4. Broglie K, Chet I, Holliday M, Cressman R, Biddle P, Knowlton S, Mauvais CJ, Broglie R: Transgenic plants with enhanced resistance to the fungal pathogen Rhizoctonia solani. Science 254: 1194–1197 (1991).

    Google Scholar 

  5. Bull J, Mauch F, Hertig C, Rebmann G, Dudler R: Sequence of a wheat gene encoding a novel protein associated with pathogen-defense. Mol Plant-Microbe Interact 5: 516–519 (1992).

    PubMed  Google Scholar 

  6. Bureau TE, Ronald PC, Wessler SR: A computer-based systematic survey reveals the predominance of small inverted-repeat elements in wild-type rice genes. Proc Natl Acad Sci USA 93: 8524–8529 (1996).

    PubMed  Google Scholar 

  7. Cho BH, Smedegaard-Petersen V: Induction of resistance to Erysiphe graminis f. sp. hordei in near-isogenic barley lines. Phytopathology 76: 301–305 (1986).

    Google Scholar 

  8. Datta SK, Peterhans A, Datta K, Potrykus I: Genetically engineered fertile Indica-rice recovered from protoplasts. Bio/technology 8: 736–740 (1990).

    Article  Google Scholar 

  9. Dudler R, Hertig C: Structure of an mdr-like gene from Arabidopsis thaliana: evolutionary implications. J Biol Chem 267: 5882–5888 (1992).

    PubMed  Google Scholar 

  10. Epple P, Apel K, Bohlmann H: Overexpression of an endogenous thionin enhances resistance of Arabidopsis against Fusarium oxysporum. Plant Cell 9: 509–520 (1997).

    PubMed  Google Scholar 

  11. Franck S, Dudler R: Nucleotide sequence (Gen-Bank/EMBL/DDBJ accession number X87686) of a wheat cDNA encoding a putative pathogen-inducible protein homologous to PWIR1. Plant Physiol 109: 338 (1995).

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  13. Gregersen PL, Thordal-Christensen H, Förster H, Collinge DB: Differential gene transcript accumulation in barley leaf epidermis and mesophyll in response to attack by Blumeria graminis f. sp. hordei (syn. Erysiphe graminis f. sp. hordei). Physiol Mol Plant Path 51: 85–97 (1997).

    Google Scholar 

  14. Horino O: Induction of bacterial leaf blight resistance by incompatible strains of Xanthomonas oryzae in rice. In Tomiyama K, Daly J, Uritani I, Oku H, Ouchi S (eds). Biochemistry and Cytology of Plant Parasite Interactions, pp. 43–55. Kodanska, Tokyo (1976).

    Google Scholar 

  15. Jach G, Görnhardt B, Mundy J, Logemann J, Pinsdorf E, Leah R, Schell J, Maas C: Enhanced quantitative resistance against fungal disease by combinatorial expression of different barley antifungal proteins in transgenic tobacco. Plant J 8: 97–109 (1995).

    PubMed  Google Scholar 

  16. Jose M, Puigdoménech P: Structure and expression of genes coding for structural proteins of the plant cell wall. New Phytol 125: 259–282 (1993).

    Google Scholar 

  17. Kieliszewski MJ, Lamport DTA: Extensin: Repetitive motifs, functional sites, post-translational codes, and phylogeny. Plant J 5: 157–172 (1994).

    Article  PubMed  Google Scholar 

  18. Kuc J: Induced immunity to plant disease. Bioscience 32: 854–860 (1982).

    Google Scholar 

  19. Langcake P, Wickens SGA: Studies on the actions of dichloro-cyclopropanes on the host-parasite relationship in rice blast disease. Physiol Plant Path 7: 113–126 (1975).

    Google Scholar 

  20. Liu D, Raghothama KG, Hasegawa PM, Bressan RA: Osmotin overexpression in potato delays development of disease symptoms. Proc Natl Acad Sci USA 91: 1888–1892 (1994).

    PubMed  Google Scholar 

  21. Logemann J, Melchers LS, Tigelaar H, Sela-Buurlage MB, Ponstein AS, van Roekel JSC, Bres-Vloemans SA, Dekker I, Cornelissen BJC, van den Elzen PJM, Jongedijk E: Synergistic activity of chitinase and β-1,3-glucanase enhances Fusarium resistance in transgenic tomato plants. J Cell Biochem 18A: 88 (1994).

    Google Scholar 

  22. Maniatis T, Fritsch EF, Sambrook J: Molecular Cloning: A Laboratory Manual, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY (1982).

    Google Scholar 

  23. Mauch F, Mauch-Mani B, Boller T: Antifungal hydrolases in pea tissue. Plant Physiol 88: 936–942 (1988).

    Google Scholar 

  24. Métraux JP, Ahl-Goy P, Staub T, Speich J, Steinemann A, Ryals J, Ward E: Induced systemic resistance in cucumber in response to 2,6-dichloro-isonicotinic acid and pathogens. In: Hennecke H, Verma DPS (eds) Advances in Molecular Genetics of Plant-Microbe Interactions, vol. 1, pp. 432–439. Kluwer Academic Publishers, Dordrecht, Netherlands (1991).

    Google Scholar 

  25. Neuhaus JM, Sticher L, Meins F Jr, Boller T: A short C-terminal sequence is necessary and sufficient for the targeting of chitinases to the plant vacuole. Proc Natl Acad Sci USA 88: 10362–10366 (1991).

    PubMed  Google Scholar 

  26. Niderman T, Genetet I, Bruyere T, Gees R, Stintzi A, Legrand M, Fritig B, Mösinger E: Pathogenesis-related PR-1 proteins are antifungal: Isolation and characterization of three 14-kilodalton proteins of tomato and of a basic PR-1 of tobacco with inhibitory activity against Phytophthora infestans. Plant Physiol 108: 17–27 (1995).

    PubMed  Google Scholar 

  27. Ouchi S, Oku H, Hibino C: Localization of induced resistance and susceptibility in barley leaves inoculated with the powdery mildew fungus. Phytopathology 66: 901–905 (1976).

    Google Scholar 

  28. Ouchi S, Oku H, Hibino C, Aldyama I: Induction of accessibility and resistance in leaves of barley by some races of Erysiphe graminis. Phytopath Z 79: 24–34 (1974).

    Google Scholar 

  29. Reimmann C, Hofmann C, Mauch F, Dudler R: Characterization of a rice gene induced by Pseudomonas syringae pv. syringae: Requirement for the bacterial lemA gene function. Physiol Mol Plant Path 46: 71–81 (1995).

    Google Scholar 

  30. Ross AF: Systemic acquired resistance induced by localized virus infections in plants. Virology 14: 340–358 (1961).

    Article  PubMed  Google Scholar 

  31. Ross AF: Systemic effects of local lesion formation. In: Beemster ABR, Dijkstra J (eds) Viruses of Plants, pp. 127–150. North-Holland, Amsterdam (1966).

  32. Ryals JA, Neuenschwander UH, Willits MG, Molina A, Steiner HY, Hunt MD: Systemic acquired resistance. Plant Cell 8: 1809–1819 (1996).

    Article  PubMed  Google Scholar 

  33. Sanger F, Nicklen S, Coulson AR: DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74: 5463–5467 (1977).

    PubMed  Google Scholar 

  34. Schweizer P, Hunziker W, Mosinger E: Complementary DNA cloning in vitro transcription, and partial sequence analysis of messenger RNA from winter wheat Triticum aestivum L. with induced resistance to Erysiphe graminis f. sp. tritici. PlantMol Biol 12: 643–654 (1989).

    Google Scholar 

  35. Showalter AM: Structure and function of cell wall proteins. Plant Cell 5: 9–23 (1993).

    Article  PubMed  Google Scholar 

  36. Smith JA, Métraux JP: Pseudomonas syringae pathovar syringae induces systemic resistance to Pyricularia oryzae in rice. Physiol Mol Plant Path 39: 451–461 (1991).

    Google Scholar 

  37. Stüber D, Matile H, Garotta G: System for high-level production in Escherichia coli and rapid purification of recombinant proteins: applications to epitpope mapping, preparation of antibodies, and structure-function analysis. In: Levkovits I, Pernis B (eds) Immunological Methods, vol. 4, pp. 121–152. Academic Press, New York (1990).

    Google Scholar 

  38. Vigers AJ, Wiedemann S, Roberts WK, Legrand M, Selitren-nikoff CP, Fritig B: Thaumatin-like pathogenesis-related proteins are antifungal. Plant Sci 83: 155–161 (1992).

    Article  Google Scholar 

  39. von Heijne G: A new method for predicting signal sequence cleavage sites. Nucl Acids Res 14: 4683–4690 (1986).

    PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  41. White RF: Acetylsalicylic acid (aspirin) induces resistance to tobacco mosaic virus in tobacco. Virology 99: 410–412 (1979).

    Article  Google Scholar 

  42. Woloshuk CP, Meulenhoff JS, Sela Buurlage M, van den Elzen PJM, Cornelissen BJC: Pathogen-induced proteins with inhibitory activity toward Phytophthora infestans. Plant Cell 3: 619–628 (1991).

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Plant Biology, University of Zurich, Zollikerstrasse 107, 8008, Zurich, Switzerland;

    Ernst Freydl & Robert Dudler

  2. Institute of Plant Biology, University of Fribourg, 1700, Fribourg, Switzerland

    Felix Mauch

  3. Laboratoire de Biologie Microbienne, Université de Lausanne, 1015, Lausanne, Switzerland

    Cornelia Reimmann

  4. Institute of Biology III, RWTH Aachen, 52056, Aachen, Germany

    Ulrich Schaffrath

Authors
  1. Felix Mauch
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cornelia Reimmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ernst Freydl
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ulrich Schaffrath
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Robert Dudler
    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

Mauch, F., Reimmann, C., Freydl, E. et al. Characterization of the rice pathogen-related protein Rir1a and regulation of the corresponding gene. Plant Mol Biol 38, 577–586 (1998). https://doi.org/10.1023/A:1006041404436

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1006041404436

Search

Navigation