Abstract
We demonstrate that the interaction of the avirulence gene avrRpt2 and the cognate resistance gene RPS2 interferes with the interaction of avrRpm1-RPM1 in Arabidopsis. Interference is mediated outside of the bacterial pathogen Pseudomonas syringae, presumably at the level of recognition of avr-dependent signals, yet does not require the wild-type RPS2 product. A numerical excess of P. syringae expressing avrRpm1 can overcome this interference in mixed inoculations. The interference of avrRpt2-RPS2 engagement with RPM1-dependent functions is mirrored by transcriptional activation of genes preferentially expressed during RPM1- or RPS2-mediated disease resistance reactions. This demonstration of interference between two plant disease resistance genes suggests that their products compete for a common element(s) in a signal transduction pathway leading to disease resistance.
Full Text
The Full Text of this article is available as a PDF (1.2 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Bent A. F., Kunkel B. N., Dahlbeck D., Brown K. L., Schmidt R., Giraudat J., Leung J., Staskawicz B. J. RPS2 of Arabidopsis thaliana: a leucine-rich repeat class of plant disease resistance genes. Science. 1994 Sep 23;265(5180):1856–1860. doi: 10.1126/science.8091210. [DOI] [PubMed] [Google Scholar]
- Dangl J. L. Pièce de Résistance: novel classes of plant disease resistance genes. Cell. 1995 Feb 10;80(3):363–366. doi: 10.1016/0092-8674(95)90485-9. [DOI] [PubMed] [Google Scholar]
- Dangl J. L., Ritter C., Gibbon M. J., Mur L. A., Wood J. R., Goss S., Mansfield J., Taylor J. D., Vivian A. Functional homologs of the Arabidopsis RPM1 disease resistance gene in bean and pea. Plant Cell. 1992 Nov;4(11):1359–1369. doi: 10.1105/tpc.4.11.1359. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dangl J. L. The enigmatic avirulence genes of phytopathogenic bacteria. Curr Top Microbiol Immunol. 1994;192:99–118. doi: 10.1007/978-3-642-78624-2_5. [DOI] [PubMed] [Google Scholar]
- Dénarié J., Cullimore J. Lipo-oligosaccharide nodulation factors: a minireview new class of signaling molecules mediating recognition and morphogenesis. Cell. 1993 Sep 24;74(6):951–954. doi: 10.1016/0092-8674(93)90717-5. [DOI] [PubMed] [Google Scholar]
- Freialdenhoven A., Scherag B., Hollricher K., Collinge D. B., Thordal-Christensen H., Schulze-Lefert P. Nar-1 and Nar-2, Two Loci Required for Mla12-Specified Race-Specific Resistance to Powdery Mildew in Barley. Plant Cell. 1994 Jul;6(7):983–994. doi: 10.1105/tpc.6.7.983. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Grant M. R., Godiard L., Straube E., Ashfield T., Lewald J., Sattler A., Innes R. W., Dangl J. L. Structure of the Arabidopsis RPM1 gene enabling dual specificity disease resistance. Science. 1995 Aug 11;269(5225):843–846. doi: 10.1126/science.7638602. [DOI] [PubMed] [Google Scholar]
- Hammond-Kosack K. E., Jones D. A., Jones JDG. Identification of Two Genes Required in Tomato for Full Cf-9-Dependent Resistance to Cladosporium fulvum. Plant Cell. 1994 Mar;6(3):361–374. doi: 10.1105/tpc.6.3.361. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Innes R. W., Bent A. F., Kunkel B. N., Bisgrove S. R., Staskawicz B. J. Molecular analysis of avirulence gene avrRpt2 and identification of a putative regulatory sequence common to all known Pseudomonas syringae avirulence genes. J Bacteriol. 1993 Aug;175(15):4859–4869. doi: 10.1128/jb.175.15.4859-4869.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Joosten M. H., Cozijnsen T. J., De Wit P. J. Host resistance to a fungal tomato pathogen lost by a single base-pair change in an avirulence gene. Nature. 1994 Jan 27;367(6461):384–386. doi: 10.1038/367384a0. [DOI] [PubMed] [Google Scholar]
- Kunkel B. N., Bent A. F., Dahlbeck D., Innes R. W., Staskawicz B. J. RPS2, an Arabidopsis disease resistance locus specifying recognition of Pseudomonas syringae strains expressing the avirulence gene avrRpt2. Plant Cell. 1993 Aug;5(8):865–875. doi: 10.1105/tpc.5.8.865. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lawrence G. J., Finnegan E. J., Ayliffe M. A., Ellis J. G. 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. 1995 Aug;7(8):1195–1206. doi: 10.1105/tpc.7.8.1195. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Long S. R., Staskawicz B. J. Prokaryotic plant parasites. Cell. 1993 Jun 4;73(5):921–935. doi: 10.1016/0092-8674(93)90271-q. [DOI] [PubMed] [Google Scholar]
- Martin G. B., Brommonschenkel S. H., Chunwongse J., Frary A., Ganal M. W., Spivey R., Wu T., Earle E. D., Tanksley S. D. Map-based cloning of a protein kinase gene conferring disease resistance in tomato. Science. 1993 Nov 26;262(5138):1432–1436. doi: 10.1126/science.7902614. [DOI] [PubMed] [Google Scholar]
- Mindrinos M., Katagiri F., Yu G. L., Ausubel F. M. The A. thaliana disease resistance gene RPS2 encodes a protein containing a nucleotide-binding site and leucine-rich repeats. Cell. 1994 Sep 23;78(6):1089–1099. doi: 10.1016/0092-8674(94)90282-8. [DOI] [PubMed] [Google Scholar]
- Preston G., Huang H. C., He S. Y., Collmer A. The HrpZ proteins of Pseudomonas syringae pvs. syringae, glycinea, and tomato are encoded by an operon containing Yersinia ysc homologs and elicit the hypersensitive response in tomato but not soybean. Mol Plant Microbe Interact. 1995 Sep-Oct;8(5):717–732. doi: 10.1094/mpmi-8-0717. [DOI] [PubMed] [Google Scholar]
- Reuber T. L., Ausubel F. M. Isolation of Arabidopsis genes that differentiate between resistance responses mediated by the RPS2 and RPM1 disease resistance genes. Plant Cell. 1996 Feb;8(2):241–249. doi: 10.1105/tpc.8.2.241. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ritter C., Dangl J. L. The avrRpm1 gene of Pseudomonas syringae pv. maculicola is required for virulence on Arabidopsis. Mol Plant Microbe Interact. 1995 May-Jun;8(3):444–453. doi: 10.1094/mpmi-8-0444. [DOI] [PubMed] [Google Scholar]
- Salmeron J. M., Barker S. J., Carland F. M., Mehta A. Y., Staskawicz B. J. Tomato mutants altered in bacterial disease resistance provide evidence for a new locus controlling pathogen recognition. Plant Cell. 1994 Apr;6(4):511–520. doi: 10.1105/tpc.6.4.511. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Staskawicz B. J., Dahlbeck D., Keen N. T. Cloned avirulence gene of Pseudomonas syringae pv. glycinea determines race-specific incompatibility on Glycine max (L.) Merr. Proc Natl Acad Sci U S A. 1984 Oct;81(19):6024–6028. doi: 10.1073/pnas.81.19.6024. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tamaki S. J., Kobayashi D. Y., Keen N. T. Sequence domains required for the activity of avirulence genes avrB and avrC from Pseudomonas syringae pv. glycinea. J Bacteriol. 1991 Jan;173(1):301–307. doi: 10.1128/jb.173.1.301-307.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Whalen M. C., Innes R. W., Bent A. F., Staskawicz B. J. Identification of Pseudomonas syringae pathogens of Arabidopsis and a bacterial locus determining avirulence on both Arabidopsis and soybean. Plant Cell. 1991 Jan;3(1):49–59. doi: 10.1105/tpc.3.1.49. [DOI] [PMC free article] [PubMed] [Google Scholar]