Advertisement

Use of transient expression in plants for the study of the “gene-for-gene” interaction

  • Fumiaki Katagiri
  • R. Todd Leister
Conference paper
Part of the NATO ASI Series book series (volume 104)

Abstract

One of the common responses in disease resistance defined by the “gene-for-gene” interaction is the hypersensitive response (HR), which is a rapid and localized cell death of plants at the site of infection. This specific cell death was used to develop a biolistic transient expression assay for the resistance response. If the transiently expressed gene causes the HR, the expression level of a cointroduced reporter gene decreases due to the rapid death of the cell. Using this assay, it was shown that expression of the Pseudomonas syringae avirulence genes, avrRpt2 or avrB, in Arabidopsis thaliana can elicit the HR when the plants carry the corresponding resistance gene, RPS2 or RPM1, respectively. This indicates that the avirulence genes are the only bacterial factors that are required to elicit the specific resistance response as long as the avirulence gene products are localized properly. This observation and others strongly suggest that the molecular recognition of pathogen attack occurs inside of plant cells for these combinations of avirulence gene and resistance gene. RPS2 and RPM1 are members of NBS-LRR class of resistance genes. NBS-LRR proteins could be cytoplasmic receptors for specific signal molecules from avirulent pathogens. We propose a speculative model to view different classes of resistance gene products from a unified perspective.

Keywords

Resistance Gene Hypersensitive Response Transient Expression Assay Avirulence Gene Biolistic Transformation 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Ackerveken, G. v. d., E. Marois, and U. Bonas. 1996. Recognition of the bacterial avirulence protein AvrBs3 occurs inside the host plant cell. Cell 87: 1307–1316.CrossRefPubMedGoogle Scholar
  2. 2.
    Anderson, P. A., G. J. Lawrence, B. C. Morrish, M. A. Ayliffe, E. J. Finnegan, and J. G. Ellis. 1997. Inactivation of the flax rust resistance gene M associated with loss of a repeated unit within the leucine-rich repeat coding region. Plant Cell 9: 641–651.CrossRefPubMedGoogle Scholar
  3. 3.
    Bent, A. F. 1996. Plant disease resistance genes: Function meets Structure. Plant Cell 8: 1757–1771.CrossRefPubMedGoogle Scholar
  4. 4.
    Bent, A. F., B. N. Kunkel, D. Dahlbeck, K. L. Brown, R. Schmidt, J. Giraudat, J. Leung, and B. J. Staskawicz. 1994. RPS2 of Arabidopsis thaliana: A leucine-rich repeat class of plant disease resistance genes. Science 265: 1856–1860.CrossRefPubMedGoogle Scholar
  5. 5.
    Bisgrove, S. R., M. T. Simonich, N. M. Smith, A. Sattler, and R. W. Innes. 1994. A disease resistance gene in Arabidopsis with specificity for two different pathogen avirulence genes. Plant Cell 6: 927–933.CrossRefPubMedGoogle Scholar
  6. 6.
    Cai, D., M. Kleine, S. Kifle, H.-J. Harloff, N. N. Sandal, K. A. Marcker, R. M. Klein-Lankhorst, E. M. J. Salentijn, W. Lange, W. J. Stiekema, U. Wyss, F. M. W. Grundler, and C. Jung. 1997. Positional cloning bf a gene for nematode resistance in sugar beet. Science 275: 832–834.CrossRefPubMedGoogle Scholar
  7. 7.
    Chittenden, T., C. Flemington, A. B. Houghton, R. G. Ebb, G. J. Gallo, B. Elangovan, G. Chinnadurai, and R. J. Lutz. 1995. A conserved domain in Bak, distinct from BH1 and BH2, mediates cell death and protein binding functions. EMBO J. 14: 5589–5596.PubMedGoogle Scholar
  8. 8.
    Dixon, M. S., D. A. Jones, J. S. Keddie, C. M. Thomas, K. Harrison, and J. D. G. Jones. 1996. The tomato Cf-2 disease resistance locus comprises two functional genes encoding leucine-rich repeat proteins. Cell 84: 451–459.CrossRefPubMedGoogle Scholar
  9. 9.
    Ellingboe, A. H. 1981. Changing concepts in host-pathogen genetics. Ann. Rev. Phytopathol. 19: 125–143.CrossRefGoogle Scholar
  10. 10.
    Flor, H. H. 1971. Current status of gene-for-gene concept. Ann. Rev. Phytopathol. 9: 275–296.CrossRefGoogle Scholar
  11. 11.
    Gabriel, D. W., and B. G. Rolfe. 1990. Working models of specific recognition in plant-microbe interactions. Ann. Rev. Phytopathol. 28:365– 391.CrossRefGoogle Scholar
  12. 12.
    Gopalan, S., D. W. Bauer, J. R. Alfano, A. O. Loniello, S. Y. He, and A. Collmer. 1996. Expression of the Pseudomonas syringae avirulence protein AvrB in plant cells alleviates its dependence on the hypersensitive response and pathogenicity ( Hrp) secretion system in eliciting genotype-specific hypersensitive cell death. Plant Cell 8: 1095–1105.CrossRefPubMedGoogle Scholar
  13. 13.
    Grant, M. R., L. Godiard, E. Straube, T. Ashfield, J. Lewald, A. Sattler, R. W. Innes, and J. L. Dangl. 1995. Structure of the Arabidopsis RPM1 gene which enables dual-specificity disease resistance. Science 269: 843–846.CrossRefPubMedGoogle Scholar
  14. 14.
    Hammond-Kosack, K. E., and J. D. G. Jones. 1996. Resistance gene-dependent plant defense responses. Plant Cell 8: 1773–1791.CrossRefPubMedGoogle Scholar
  15. 15.
    Huang, H. C., R. H. Lin, C. J. Chang, A. Collmer, and W. L. Deng. 1995. The complete hrp gene cluster of Pseudomonas syringae pv. syringae 61 includes two blocks of genes required for harpinpSS secretion that are arranged colinearly with Yersinia ysc homologs. Mol. Plant-Microbe Interact. 8:733– 746.CrossRefPubMedGoogle Scholar
  16. 16.
    Innes, R. W., A. F. Bent, B. N. Kunkel, S. R. Bisgrove, and B. J. Staskawicz. 1993. Molecular analysis of avirulence gene avrRpt2 and identification of a putative regulatory sequence common to all known Pseudomonas syringae avirulence genes. J. Bacteriol. 175: 4859–4869.PubMedGoogle Scholar
  17. 17.
    Jefferson, R. A., T. A. Kavanagh, and M. W. Bevan. 1987. GUS fusions: 6- glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 13: 3901–3907.Google Scholar
  18. 18.
    Jones, D. A., C. M. Thomas, K. E. Hammond-Kosack, P. J. Balint-Kurti, and J. D. G. Jones. 1994. Isolation of the Tomato Cf-9 Gene for Resistance to Cladosporium fulvum by Transposon Tagging. Science 266: 789–793.CrossRefPubMedGoogle Scholar
  19. 19.
    Keen, N. T. 1992. The molecular biology of disease resistance. Plant Molecular Biology 19: 109–122.CrossRefPubMedGoogle Scholar
  20. 20.
    Klement, Z. 1982. Hypersensitivity, p. 149–177. In M. S. Mount, and G. H. Lacy (ed.), Phytopathogenic Procaryotes, Vol. 2, vol. 2. Academic Press, New York.Google Scholar
  21. 21.
    Kunkel, B. N., A. F. Bent, D. Dahlbeck, R. W. Innes, and B. J. Staskawicz. 1993. RPS2, an Arabidopsis disease resistance locus specifying recognition of Pseudomonas syringae strains expressing the avirulence gene avrRpt2. Plant Cell 5: 865–875.CrossRefPubMedGoogle Scholar
  22. 22.
    Lamb, C. J., M. A. Lawton, M. Dron, and R. A. Dixon. 1989. Signals and transduction mechanisms for activation of plant defenses against microbial attack. Cell 56: 215–224.CrossRefPubMedGoogle Scholar
  23. 23.
    Lawrence, G. J., E. J. Finnegan, M. A. Ayliffe, and J. G. Ellis. 1995. The L6 gene for flax rust resistance is related to the Arabidopsis bacterial resistance gene RPS2 and the tobacco viral resistance gene N. The Plant Cell 7:1195– 1206.CrossRefPubMedGoogle Scholar
  24. 24.
    Leister, R. T., F. M. Ausubel, and F. Katagiri. 1996. Molecular recognition of pathogen attack occurs inside of plant cells in plant disease resistance specified by the Arabidopsis genesRPS2 and RPM1. Proc. Natl. Acad. Sci. USA 93: 15497–15502.CrossRefPubMedGoogle Scholar
  25. 25.
    Lindgren, P. B., R. C. Peet, and N. J. Panopoulos. 1986. Gene cluster of Pseudomonas syringae pv. phaseolicola controls pathogenicity on bean and hypersensitivity on non-host plants. J. Bacteriol. 168: 512–522.PubMedGoogle Scholar
  26. 26.
    Martin, G. B., S. H. Brommonschenkel, J. Chunwongse, A. Frary, M. W. Ganal, R. Spivey, T. Wu, E. D. Earle, and S. D. Tanksley. 1993. Map-based cloning of a protein kinase gene conferring disease resistance in tomato. Science 262: 1432–1436.CrossRefPubMedGoogle Scholar
  27. 27.
    Martin, G. B., A. Frary, T. Wu, S. Brommonschenkel, J. Chunwongse, E. D. Earle, and S. D. Tanksley. 1994. A member of the tomato Pto gene family confers sensitivity to fenthion resulting in rapid cell death. Plant Cell 6:1543– 1552.CrossRefPubMedGoogle Scholar
  28. 28.
    Mindrinos, M., F. Katagiri, G.-L. Yu, and F. M. Ausubel. 1994. The A. thaliana disease resistance gene RPS2 encodes a protein containing a nucleotide-binding site and leucine-rich repeats. Cell 78: 1089–1099.CrossRefPubMedGoogle Scholar
  29. 29.
    Ori, N., Y. Eshed, I. Paran, G. Presting, D. Aviv, S. Tanksley, D. Zamir, and R. Fluhr. 1997. The I2C family from the wilt disease resistance locus 12 belongs to the nucleotide binding, leucine-rich repeat superfamily of plant resistance gene. Plant Cell 9: 521–531.CrossRefPubMedGoogle Scholar
  30. 30.
    Pirhonen, M. U., M. C. Lidell, D. L. Rowley, S. W. Lee, S. Jin, Y. Liang, S. Silverstone, N. T. Keen, and S. W. Hutcheson. 1996. Phenotypic expression of Pseudomonas syringae avr genes in E. coli linked to the activities of the hrp-encoded secretion system. Mol Plant-Microbe Interact 9: 252–260.Google Scholar
  31. 31.
    Rommens, C. M., J. M. Salmeron, G. E. Oldroyd, and B. J. Staskawicz. 1995. Intergeneric transfer and functional expression of the tomato disease resistance gene Pto. Plant Cell 7: 1537–1544.CrossRefPubMedGoogle Scholar
  32. 32.
    Rommens, C. M. T., J. M. Salmeron, D. C. Baulcombe, and B. J. Staskawicz. 1995. Use of a gene expression system based on potato virus X to rapidly identify and characterize a tomato Pto homolog that controls fenthion sensitivity. Plant Cell 7: 249–257.CrossRefPubMedGoogle Scholar
  33. 33.
    Rosqvist, R., S. Hakansson, A. Forsberg, and H. Wolf-Watz. 1995. Functional conservation of the secretion and translocation machinery for virulence proteins of yersiniae, salmonellae and shigellae. EMBO J 14:4187–4195.PubMedGoogle Scholar
  34. 34.
    Ryals, J. A., U. H. Newenschwander, M. G. Willits, A. Molina, H.-Y. Steiner, and M. D. Hunt. 1996. Systemic acquired resistance. Plant Cell 8: 1809–1819.CrossRefPubMedGoogle Scholar
  35. 35.
    Salmeron, J. M., G. E. D. Oldroyd, C. M. T. Rommens, S. R. Scofield, H.- S. Kim, D. T. Lavelle, D. Dahlbeck, and B. J. Stackawicz. 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.CrossRefPubMedGoogle Scholar
  36. 36.
    Scofield, S. R., C. M. Tobias, J. P. Rathjen, J. H. Chang, D. T. Lavelle, R. W. Michelmore, and B. J. Staskawicz. 1996. Molecular basis of gene-for-gene specificity in bacterial speck disease of tomato. Science 274: 2063–2065.CrossRefPubMedGoogle Scholar
  37. 37.
    37.Smith, M., E. Mazzola, J. Sims, S. Midland, and N. Keen. 1993. The syringolides: Bacterial C-glycosyl lipids that trigger plant disease resistance. Tetrahedron Lett. 34:223–226.CrossRefGoogle Scholar
  38. 38.
    Song, W.-Y., G.-L. Wang, L.-L. Chen, H.-S. Kim, L.-Y. Pi, T. Holsten, J. Gardner, B. Wang, W.-X. Zhai, L.-H. Zhu, C. Fauquet, and P. Ronald. 1995. A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science 270: 1804–1806CrossRefPubMedGoogle Scholar
  39. 39.
    Tamaki, S., D. Dahlbeck, B. Staskawicz, and N. T. Keen. 1988. Characterization and expression of two avirulence genes cloned from Pseudomonas syringae pv. glycinea. J. Bacteriol 170: 4846–4854.PubMedGoogle Scholar
  40. 40.
    Tang, X., R. D. Frederick, J. Zhou, D. A. Halterman, Y. Jia, and G. B. Martin. 1996. Initiation of plant disease resistance by physical interaction of AvrPto and Pto kinase. Science 274: 2060–2063.CrossRefPubMedGoogle Scholar
  41. 41.
    Wet, J. R. d., K. V. Wood, D. R. Helinski, and M. DeLuca. 1985. Cloning of firefly luciferase cDNA and the expression of active luciferase in Escherichia coli. Proc. Natl. Acad. Sci. USA 82: 7870–7873.CrossRefPubMedGoogle Scholar
  42. 42.
    Whitham, S., S. P. Dinesh-Kumar, D. Choi, R. Hehl, C. Corr, and B. Baker. 1994. The product of the tobacco mosaic resistance gene N: Similarity to toll and the interleukin-1 receptor. Cell 78: 1101–1105.CrossRefPubMedGoogle Scholar
  43. 43.
    Whitham, S., S. McCormick, and B. Baker. 1996. The N gene of tobacco confers resistance to tobacco mosaic virus in transgenic tomato. Proc. Natl. Acad. Sci. USA 93: 8776–8781.CrossRefPubMedGoogle Scholar
  44. 44.
    Yu, G.-L., F. Katagiri, and F. M. Ausubel. 1993. Arabidopsis mutations at the RPS2 locus result in loss of resistance to Pseudomonas syringae strains expressing the avirulence gene avrRpt2. Mol. Plant-Microbe Interact. 6:434– 443.CrossRefPubMedGoogle Scholar
  45. 45.
    Zhou, J., Y.-T. Loh, R. A. Bressan, and G. B. Martin. 1995. The tomato gene Ptil encodes a serine/threonine kinase that is phosphorylated by Pto and is involved in the hypersensitive response. Cell 83: 925–935.CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1998

Authors and Affiliations

  • Fumiaki Katagiri
    • 1
  • R. Todd Leister
    • 1
  1. 1.Department of Biological SciencesUniversity of Maryland Baltimore CountyBaltimoreUSA

Personalised recommendations