Skip to main content
The Plant Cell logoLink to The Plant Cell
. 1998 Nov;10(11):1915–1925. doi: 10.1105/tpc.10.11.1915

The tomato Cf-5 disease resistance gene and six homologs show pronounced allelic variation in leucine-rich repeat copy number.

M S Dixon 1, K Hatzixanthis 1, D A Jones 1, K Harrison 1, J D Jones 1
PMCID: PMC143956  PMID: 9811798

Abstract

The tomato Cf-2 and Cf-5 genes confer resistance to Cladosporium fulvum and map to a complex locus on chromosome 6. The Cf-5 gene has been isolated and is predicted to encode a largely extracytoplasmic protein containing 32 leucine-rich repeats (LRRs), resembling the previously isolated Cf-2 gene, which has 38 LRRs. Three haplotypes of this locus from Lycopersicon esculentum, L. pimpinellifolium, and L. esculentum var cerasiforme were compared, and five additional homologs of Cf-5 were sequenced. All share extensive sequence identity, particularly within the C-terminal portions of the predicted proteins. In striking contrast to the Cf-9 gene family, six of seven homologs in the Cf-2/Cf-5 gene family vary in LRR copy number, ranging from 25 to 38 LRRs. Cf-5 and one adjacent homolog differ by only two LRRs. Recombination events that vary the LRR copy number in this region could provide a mechanism for the generation of new specificities for recognition of different ligands. A recombination breakpoint between the Cf-2 and Cf-5 loci was fully characterized and shown to be intragenic.

Full Text

The Full Text of this article is available as a PDF (418.4 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Anderson P. A., Lawrence G. J., Morrish B. C., Ayliffe M. A., Finnegan E. J., Ellis J. G. Inactivation of the flax rust resistance gene M associated with loss of a repeated unit within the leucine-rich repeat coding region. Plant Cell. 1997 Apr;9(4):641–651. doi: 10.1105/tpc.9.4.641. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. 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]
  3. Bent A. F. Plant Disease Resistance Genes: Function Meets Structure. Plant Cell. 1996 Oct;8(10):1757–1771. doi: 10.1105/tpc.8.10.1757. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bisgrove S. R., Simonich M. T., Smith N. M., Sattler A., Innes R. W. A disease resistance gene in Arabidopsis with specificity for two different pathogen avirulence genes. Plant Cell. 1994 Jul;6(7):927–933. doi: 10.1105/tpc.6.7.927. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Botella M. A., Coleman M. J., Hughes D. E., Nishimura M. T., Jones J. D., Somerville S. C. Map positions of 47 Arabidopsis sequences with sequence similarity to disease resistance genes. Plant J. 1997 Nov;12(5):1197–1211. doi: 10.1046/j.1365-313x.1997.12051197.x. [DOI] [PubMed] [Google Scholar]
  6. Carroll B. J., Klimyuk V. I., Thomas C. M., Bishop G. J., Harrison K., Scofield S. R., Jones J. D. Germinal transpositions of the maize element Dissociation from T-DNA loci in tomato. Genetics. 1995 Jan;139(1):407–420. doi: 10.1093/genetics/139.1.407. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Dickinson M. J., Jones D. A., Jones J. D. Close linkage between the Cf-2/Cf-5 and Mi resistance loci in tomato. Mol Plant Microbe Interact. 1993 May-Jun;6(3):341–347. doi: 10.1094/mpmi-6-341. [DOI] [PubMed] [Google Scholar]
  8. Dixon M. S., Jones D. A., Hatzixanthis K., Ganal M. W., Tanksley S. D., Jones J. D. High-resolution mapping of the physical location of the tomato Cf-2 gene. Mol Plant Microbe Interact. 1995 Mar-Apr;8(2):200–206. doi: 10.1094/mpmi-8-0200. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. Dooner H. K., Martínez-Férez I. M. Recombination occurs uniformly within the bronze gene, a meiotic recombination hotspot in the maize genome. Plant Cell. 1997 Sep;9(9):1633–1646. doi: 10.1105/tpc.9.9.1633. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Ellis J., Lawrence G., Ayliffe M., Anderson P., Collins N., Finnegan J., Frost D., Luck J., Pryor T. Advances in the molecular genetic analysis of the flax-flax rust interaction. Annu Rev Phytopathol. 1997;35:271–291. doi: 10.1146/annurev.phyto.35.1.271. [DOI] [PubMed] [Google Scholar]
  12. 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]
  13. 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]
  14. Hammond-Kosack Kim E., Jones Jonathan D. G. PLANT DISEASE RESISTANCE GENES. Annu Rev Plant Physiol Plant Mol Biol. 1997 Jun;48(NaN):575–607. doi: 10.1146/annurev.arplant.48.1.575. [DOI] [PubMed] [Google Scholar]
  15. Higgins D. G., Sharp P. M. CLUSTAL: a package for performing multiple sequence alignment on a microcomputer. Gene. 1988 Dec 15;73(1):237–244. doi: 10.1016/0378-1119(88)90330-7. [DOI] [PubMed] [Google Scholar]
  16. Hulbert S. H. Structure and evolution of the rp1 complex conferring rust resistance in maize. Annu Rev Phytopathol. 1997;35:293–310. doi: 10.1146/annurev.phyto.35.1.293. [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. 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]
  19. Kajava A. V. Structural diversity of leucine-rich repeat proteins. J Mol Biol. 1998 Apr 3;277(3):519–527. doi: 10.1006/jmbi.1998.1643. [DOI] [PubMed] [Google Scholar]
  20. 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]
  21. Leister D., Ballvora A., Salamini F., Gebhardt C. A PCR-based approach for isolating pathogen resistance genes from potato with potential for wide application in plants. Nat Genet. 1996 Dec;14(4):421–429. doi: 10.1038/ng1296-421. [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. 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]
  24. Osbourn A. E. Preformed Antimicrobial Compounds and Plant Defense against Fungal Attack. Plant Cell. 1996 Oct;8(10):1821–1831. doi: 10.1105/tpc.8.10.1821. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Parker J. E., Coleman M. J., Szabò V., Frost L. N., Schmidt R., van der Biezen E. A., Moores T., Dean C., Daniels M. J., Jones J. D. The Arabidopsis downy mildew resistance gene RPP5 shares similarity to the toll and interleukin-1 receptors with N and L6. Plant Cell. 1997 Jun;9(6):879–894. doi: 10.1105/tpc.9.6.879. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Parniske M., Hammond-Kosack K. E., Golstein C., Thomas C. M., Jones D. A., Harrison K., Wulff B. B., Jones J. D. Novel disease resistance specificities result from sequence exchange between tandemly repeated genes at the Cf-4/9 locus of tomato. Cell. 1997 Dec 12;91(6):821–832. doi: 10.1016/s0092-8674(00)80470-5. [DOI] [PubMed] [Google Scholar]
  27. 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]
  28. Song W. Y., Pi L. Y., Wang G. L., Gardner J., Holsten T., Ronald P. C. Evolution of the rice Xa21 disease resistance gene family. Plant Cell. 1997 Aug;9(8):1279–1287. doi: 10.1105/tpc.9.8.1279. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. 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]
  30. 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]
  31. 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]
  32. Thomas C. M., Jones D. A., Parniske M., Harrison K., Balint-Kurti P. J., Hatzixanthis K., Jones J. D. Characterization of the tomato Cf-4 gene for resistance to Cladosporium fulvum identifies sequences that determine recognitional specificity in Cf-4 and Cf-9. Plant Cell. 1997 Dec;9(12):2209–2224. doi: 10.1105/tpc.9.12.2209. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Vervoort J., van den Hooven H. W., Berg A., Vossen P., Vogelsang R., Joosten M. H., de Wit P. J. The race-specific elicitor AVR9 of the tomato pathogen Cladosporium fulvum: a cystine knot protein. Sequence-specific 1H NMR assignments, secondary structure and global fold of the protein. FEBS Lett. 1997 Mar 10;404(2-3):153–158. doi: 10.1016/s0014-5793(97)00117-8. [DOI] [PubMed] [Google Scholar]
  34. van Kan J. A., van den Ackerveken G. F., de Wit P. J. Cloning and characterization of cDNA of avirulence gene avr9 of the fungal pathogen Cladosporium fulvum, causal agent of tomato leaf mold. Mol Plant Microbe Interact. 1991 Jan-Feb;4(1):52–59. doi: 10.1094/mpmi-4-052. [DOI] [PubMed] [Google Scholar]

Articles from The Plant Cell are provided here courtesy of Oxford University Press

RESOURCES