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. 1997 Jun;9(6):879–894. doi: 10.1105/tpc.9.6.879

The Arabidopsis downy mildew resistance gene RPP5 shares similarity to the toll and interleukin-1 receptors with N and L6.

J E Parker 1, M J Coleman 1, V Szabò 1, L N Frost 1, R Schmidt 1, E A van der Biezen 1, T Moores 1, C Dean 1, M J Daniels 1, J D Jones 1
PMCID: PMC156965  PMID: 9212464

Abstract

Plant disease resistance genes operate at the earliest steps of pathogen perception. The Arabidopsis RPP5 gene specifying resistance to the downy mildew pathogen Peronospora parasitica was positionally cloned. It encodes a protein that possesses a putative nucleotide binding site and leucine-rich repeats, and its product exhibits striking structural similarity to the plant resistance gene products N and L6. Like N and L6, the RPP5 N-terminal domain resembles the cytoplasmic domains of the Drosophila Toll and mammalian interleukin-1 transmembrane receptors. In contrast to N and L6, which produce predicted truncated products by alternative splicing, RPP5 appears to express only a single transcript corresponding to the full-length protein. However, a truncated form structurally similar to those of N and L6 is encoded by one or more other members of the RPP5 gene family that are tightly clustered on chromosome 4. The organization of repeated units within the leucine-rich repeats encoded by the wild-type RPP5 gene and an RPP5 mutant allele provides molecular evidence for the heightened capacity of this domain to evolve novel configurations and potentially new disease resistance specificities.

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Selected References

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  1. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
  2. Bell C. J., Ecker J. R. Assignment of 30 microsatellite loci to the linkage map of Arabidopsis. Genomics. 1994 Jan 1;19(1):137–144. doi: 10.1006/geno.1994.1023. [DOI] [PubMed] [Google Scholar]
  3. 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]
  4. Dinesh-Kumar S. P., Whitham S., Choi D., Hehl R., Corr C., Baker B. Transposon tagging of tobacco mosaic virus resistance gene N: its possible role in the TMV-N-mediated signal transduction pathway. Proc Natl Acad Sci U S A. 1995 May 9;92(10):4175–4180. doi: 10.1073/pnas.92.10.4175. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Dixon M. S., Jones D. A., Keddie J. S., Thomas C. M., Harrison K., Jones J. D. The tomato Cf-2 disease resistance locus comprises two functional genes encoding leucine-rich repeat proteins. Cell. 1996 Feb 9;84(3):451–459. doi: 10.1016/s0092-8674(00)81290-8. [DOI] [PubMed] [Google Scholar]
  6. Ellis J. G., Lawrence G. J., Finnegan E. J., Anderson P. A. Contrasting complexity of two rust resistance loci in flax. Proc Natl Acad Sci U S A. 1995 May 9;92(10):4185–4188. doi: 10.1073/pnas.92.10.4185. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Fryxell K. J. The coevolution of gene family trees. Trends Genet. 1996 Sep;12(9):364–369. doi: 10.1016/s0168-9525(96)80020-5. [DOI] [PubMed] [Google Scholar]
  8. Gopalan S., Bauer D. W., Alfano J. R., Loniello A. O., He S. Y., Collmer A. 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. 1996 Jul;8(7):1095–1105. doi: 10.1105/tpc.8.7.1095. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Grill E., Somerville C. Construction and characterization of a yeast artificial chromosome library of Arabidopsis which is suitable for chromosome walking. Mol Gen Genet. 1991 May;226(3):484–490. doi: 10.1007/BF00260662. [DOI] [PubMed] [Google Scholar]
  10. Hammond-Kosack K. E., Jones J. D. Resistance gene-dependent plant defense responses. Plant Cell. 1996 Oct;8(10):1773–1791. doi: 10.1105/tpc.8.10.1773. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hashimoto C., Hudson K. L., Anderson K. V. The Toll gene of Drosophila, required for dorsal-ventral embryonic polarity, appears to encode a transmembrane protein. Cell. 1988 Jan 29;52(2):269–279. doi: 10.1016/0092-8674(88)90516-8. [DOI] [PubMed] [Google Scholar]
  12. Hulbert S. H., Bennetzen J. L. Recombination at the Rp1 locus of maize. Mol Gen Genet. 1991 May;226(3):377–382. doi: 10.1007/BF00260649. [DOI] [PubMed] [Google Scholar]
  13. Hultmark D. Insect immunology. Ancient relationships. Nature. 1994 Jan 13;367(6459):116–117. doi: 10.1038/367116a0. [DOI] [PubMed] [Google Scholar]
  14. Ip Y. T., Reach M., Engstrom Y., Kadalayil L., Cai H., González-Crespo S., Tatei K., Levine M. Dif, a dorsal-related gene that mediates an immune response in Drosophila. Cell. 1993 Nov 19;75(4):753–763. doi: 10.1016/0092-8674(93)90495-c. [DOI] [PubMed] [Google Scholar]
  15. Jones D. A., Thomas C. M., Hammond-Kosack K. E., Balint-Kurti P. J., Jones J. D. Isolation of the tomato Cf-9 gene for resistance to Cladosporium fulvum by transposon tagging. Science. 1994 Nov 4;266(5186):789–793. doi: 10.1126/science.7973631. [DOI] [PubMed] [Google Scholar]
  16. Klimyuk V. I., Carroll B. J., Thomas C. M., Jones J. D. Alkali treatment for rapid preparation of plant material for reliable PCR analysis. Plant J. 1993 Mar;3(3):493–494. doi: 10.1111/j.1365-313x.1993.tb00169.x. [DOI] [PubMed] [Google Scholar]
  17. Kobe B., Deisenhofer J. The leucine-rich repeat: a versatile binding motif. Trends Biochem Sci. 1994 Oct;19(10):415–421. doi: 10.1016/0968-0004(94)90090-6. [DOI] [PubMed] [Google Scholar]
  18. Konieczny A., Ausubel F. M. A procedure for mapping Arabidopsis mutations using co-dominant ecotype-specific PCR-based markers. Plant J. 1993 Aug;4(2):403–410. doi: 10.1046/j.1365-313x.1993.04020403.x. [DOI] [PubMed] [Google Scholar]
  19. Kyte J., Doolittle R. F. A simple method for displaying the hydropathic character of a protein. J Mol Biol. 1982 May 5;157(1):105–132. doi: 10.1016/0022-2836(82)90515-0. [DOI] [PubMed] [Google Scholar]
  20. Lemaitre B., Meister M., Govind S., Georgel P., Steward R., Reichhart J. M., Hoffmann J. A. Functional analysis and regulation of nuclear import of dorsal during the immune response in Drosophila. EMBO J. 1995 Feb 1;14(3):536–545. doi: 10.1002/j.1460-2075.1995.tb07029.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lemaitre B., Nicolas E., Michaut L., Reichhart J. M., Hoffmann J. A. The dorsoventral regulatory gene cassette spätzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell. 1996 Sep 20;86(6):973–983. doi: 10.1016/s0092-8674(00)80172-5. [DOI] [PubMed] [Google Scholar]
  22. 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]
  23. Parker J. E., Holub E. B., Frost L. N., Falk A., Gunn N. D., Daniels M. J. Characterization of eds1, a mutation in Arabidopsis suppressing resistance to Peronospora parasitica specified by several different RPP genes. Plant Cell. 1996 Nov;8(11):2033–2046. doi: 10.1105/tpc.8.11.2033. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Plant J., Wood E. C. E.D. involvement grows in audit activities, rape treatment. Hospitals. 1977 Apr 1;51(7):107-8, 110,112. [PubMed] [Google Scholar]
  25. Reignault P., Frost L. N., Richardson H., Daniels M. J., Jones J. D., Parker J. E. Four Arabidopsis RPP loci controlling resistance to the Noco2 isolate of Peronospora parasitica map to regions known to contain other RPP recognition specificities. Mol Plant Microbe Interact. 1996 Aug;9(6):464–473. doi: 10.1094/mpmi-9-0464. [DOI] [PubMed] [Google Scholar]
  26. Richter T. E., Pryor T. J., Bennetzen J. L., Hulbert S. H. New rust resistance specificities associated with recombination in the Rp1 complex in maize. Genetics. 1995 Sep;141(1):373–381. doi: 10.1093/genetics/141.1.373. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Rosetto M., Engström Y., Baldari C. T., Telford J. L., Hultmark D. Signals from the IL-1 receptor homolog, Toll, can activate an immune response in a Drosophila hemocyte cell line. Biochem Biophys Res Commun. 1995 Apr 6;209(1):111–116. doi: 10.1006/bbrc.1995.1477. [DOI] [PubMed] [Google Scholar]
  28. Ryals J., Uknes S., Ward E. Systemic Acquired Resistance. Plant Physiol. 1994 Apr;104(4):1109–1112. doi: 10.1104/pp.104.4.1109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Scofield SR, Tobias CM, Rathjen JP, Chang JH, Lavelle DT, Michelmore RW, Staskawicz BJ. Molecular Basis of Gene-for-Gene Specificity in Bacterial Speck Disease of Tomato. Science. 1996 Dec 20;274(5295):2063–2065. doi: 10.1126/science.274.5295.2063. [DOI] [PubMed] [Google Scholar]
  30. Sims J. E., Acres R. B., Grubin C. E., McMahan C. J., Wignall J. M., March C. J., Dower S. K. Cloning the interleukin 1 receptor from human T cells. Proc Natl Acad Sci U S A. 1989 Nov;86(22):8946–8950. doi: 10.1073/pnas.86.22.8946. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Song W. Y., Wang G. L., Chen L. L., Kim H. S., Pi L. Y., Holsten T., Gardner J., Wang B., Zhai W. X., Zhu L. H. A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science. 1995 Dec 15;270(5243):1804–1806. doi: 10.1126/science.270.5243.1804. [DOI] [PubMed] [Google Scholar]
  32. Staskawicz B. J., Ausubel F. M., Baker B. J., Ellis J. G., Jones J. D. Molecular genetics of plant disease resistance. Science. 1995 May 5;268(5211):661–667. doi: 10.1126/science.7732374. [DOI] [PubMed] [Google Scholar]
  33. Sudupak M. A., Bennetzen J. L., Hulbert S. H. Unequal exchange and meiotic instability of disease-resistance genes in the Rp1 region of maize. Genetics. 1993 Jan;133(1):119–125. doi: 10.1093/genetics/133.1.119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Tang X, Frederick RD, Zhou J, Halterman DA, Jia Y, Martin GB. Initiation of Plant Disease Resistance by Physical Interaction of AvrPto and Pto Kinase. Science. 1996 Dec 20;274(5295):2060–2063. doi: 10.1126/science.274.5295.2060. [DOI] [PubMed] [Google Scholar]
  35. Torii K. U., Mitsukawa N., Oosumi T., Matsuura Y., Yokoyama R., Whittier R. F., Komeda Y. The Arabidopsis ERECTA gene encodes a putative receptor protein kinase with extracellular leucine-rich repeats. Plant Cell. 1996 Apr;8(4):735–746. doi: 10.1105/tpc.8.4.735. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Tornero P., Mayda E., Gómez M. D., Cañas L., Conejero V., Vera P. Characterization of LRP, a leucine-rich repeat (LRR) protein from tomato plants that is processed during pathogenesis. Plant J. 1996 Aug;10(2):315–330. doi: 10.1046/j.1365-313x.1996.10020315.x. [DOI] [PubMed] [Google Scholar]
  37. Traut T. W. The functions and consensus motifs of nine types of peptide segments that form different types of nucleotide-binding sites. Eur J Biochem. 1994 May 15;222(1):9–19. doi: 10.1111/j.1432-1033.1994.tb18835.x. [DOI] [PubMed] [Google Scholar]
  38. Valvekens D., Van Montagu M., Van Lijsebettens M. Agrobacterium tumefaciens-mediated transformation of Arabidopsis thaliana root explants by using kanamycin selection. Proc Natl Acad Sci U S A. 1988 Aug;85(15):5536–5540. doi: 10.1073/pnas.85.15.5536. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Whitham S., Dinesh-Kumar S. P., Choi D., Hehl R., Corr C., Baker B. The product of the tobacco mosaic virus resistance gene N: similarity to toll and the interleukin-1 receptor. Cell. 1994 Sep 23;78(6):1101–1115. doi: 10.1016/0092-8674(94)90283-6. [DOI] [PubMed] [Google Scholar]
  40. Yang Y., Gabriel D. W. Intragenic recombination of a single plant pathogen gene provides a mechanism for the evolution of new host specificities. J Bacteriol. 1995 Sep;177(17):4963–4968. doi: 10.1128/jb.177.17.4963-4968.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Zhou J., Loh Y. T., Bressan R. A., Martin G. B. The tomato gene Pti1 encodes a serine/threonine kinase that is phosphorylated by Pto and is involved in the hypersensitive response. Cell. 1995 Dec 15;83(6):925–935. doi: 10.1016/0092-8674(95)90208-2. [DOI] [PubMed] [Google Scholar]

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