Abstract
In many interactions between plants and their pathogens, resistance to infection is specified by plant resistance (R) genes and corresponding pathogen avirulence (Avr) genes. In tomato, the Cf-4 and Cf-9 resistance genes map to the same location but confer resistance to Cladosporium fulvum through recognition of different avirulence determinants (AVR4 and AVR9) by a molecular mechanism that has yet to be determined. Here, we describe the cloning and characterization of Cf-4, which also encodes a membrane-anchored extracellular glycoprotein. Cf-4 contains 25 leucine-rich repeats, which is two fewer than Cf-9. The proteins have > 91% identical amino acids. DNA sequence comparison suggests that Cf-4 and Cf-9 are derived from a common progenitor sequence. Amino acid differences distinguishing Cf-4 and Cf-9 are confined to their N termini, delimiting a region that determines the recognitional specificity of ligand binding. The majority of these differences are in residues interstitial to those of the leucine-rich repeat consensus motif. Many of these residues are predicted to form a solvent-exposed surface that can interact with the cognate ligand. Both Cf-4 and Cf-9 are located within a 36-kb region comprising five tandemly duplicated homologous genes. These results provide further insight into the molecular basis of pathogen perception by plants and the organization of complex R gene loci.
Full Text
The Full Text of this article is available as a PDF (3.8 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- 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]
- 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]
- Buchanan S. G., Gay N. J. Structural and functional diversity in the leucine-rich repeat family of proteins. Prog Biophys Mol Biol. 1996;65(1-2):1–44. doi: 10.1016/s0079-6107(96)00003-x. [DOI] [PubMed] [Google Scholar]
- Church G. M., Gilbert W. Genomic sequencing. Proc Natl Acad Sci U S A. 1984 Apr;81(7):1991–1995. doi: 10.1073/pnas.81.7.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Emsley P., Charles I. G., Fairweather N. F., Isaacs N. W. Structure of Bordetella pertussis virulence factor P.69 pertactin. Nature. 1996 May 2;381(6577):90–92. doi: 10.1038/381090a0. [DOI] [PubMed] [Google Scholar]
- Hammond-Kosack K. E., Harrison K., Jones J. D. Developmentally regulated cell death on expression of the fungal avirulence gene Avr9 in tomato seedlings carrying the disease-resistance gene Cf-9. Proc Natl Acad Sci U S A. 1994 Oct 25;91(22):10445–10449. doi: 10.1073/pnas.91.22.10445. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hu G., Richter T. E., Hulbert S. H., Pryor T. Disease Lesion Mimicry Caused by Mutations in the Rust Resistance Gene rp1. Plant Cell. 1996 Aug;8(8):1367–1376. doi: 10.1105/tpc.8.8.1367. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Isaacs N. W. Cystine knots. Curr Opin Struct Biol. 1995 Jun;5(3):391–395. doi: 10.1016/0959-440x(95)80102-2. [DOI] [PubMed] [Google Scholar]
- 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]
- Jones J. D., Shlumukov L., Carland F., English J., Scofield S. R., Bishop G. J., Harrison K. Effective vectors for transformation, expression of heterologous genes, and assaying transposon excision in transgenic plants. Transgenic Res. 1992 Nov;1(6):285–297. doi: 10.1007/BF02525170. [DOI] [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]
- Joosten M. H., Vogelsang R., Cozijnsen T. J., Verberne M. C., De Wit P. J. The biotrophic fungus Cladosporium fulvum circumvents Cf-4-mediated resistance by producing unstable AVR4 elicitors. Plant Cell. 1997 Mar;9(3):367–379. doi: 10.1105/tpc.9.3.367. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kajava A. V., Vassart G., Wodak S. J. Modeling of the three-dimensional structure of proteins with the typical leucine-rich repeats. Structure. 1995 Sep 15;3(9):867–877. doi: 10.1016/S0969-2126(01)00222-2. [DOI] [PubMed] [Google Scholar]
- 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]
- Kooman-Gersmann M., Honee G., Bonnema G., De Wit PJGM. A High-Affinity Binding Site for the AVR9 Peptide Elicitor of Cladosporium fulvum Is Present on Plasma Membranes of Tomato and Other Solanaceous Plants. Plant Cell. 1996 May;8(5):929–938. doi: 10.1105/tpc.8.5.929. [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]
- Lovering R., Sweatman A. K., O'Reilly M. A., Genet S. A., Middleton-Price H., Malcolm S., Levinsky R. J., Kinnon C. Physical mapping identifies DXS265 as a useful genetic marker for carrier detection and prenatal diagnosis of X-linked agammaglobulinemia. Hum Genet. 1993 Mar;91(2):178–180. doi: 10.1007/BF00222721. [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]
- McDonald N. Q., Hendrickson W. A. A structural superfamily of growth factors containing a cystine knot motif. Cell. 1993 May 7;73(3):421–424. doi: 10.1016/0092-8674(93)90127-c. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- Thomas C. M., Jones D. A., English J. J., Carroll B. J., Bennetzen J. L., Harrison K., Burbidge A., Bishop G. J., Jones J. D. Analysis of the chromosomal distribution of transposon-carrying T-DNAs in tomato using the inverse polymerase chain reaction. Mol Gen Genet. 1994 Mar;242(5):573–585. doi: 10.1007/BF00285281. [DOI] [PubMed] [Google Scholar]
- Thomas C. M., Vos P., Zabeau M., Jones D. A., Norcott K. A., Chadwick B. P., Jones J. D. Identification of amplified restriction fragment polymorphism (AFLP) markers tightly linked to the tomato Cf-9 gene for resistance to Cladosporium fulvum. Plant J. 1995 Nov;8(5):785–794. doi: 10.1046/j.1365-313x.1995.08050785.x. [DOI] [PubMed] [Google Scholar]
- Van den Ackerveken G. F., Van Kan J. A., De Wit P. J. Molecular analysis of the avirulence gene avr9 of the fungal tomato pathogen Cladosporium fulvum fully supports the gene-for-gene hypothesis. Plant J. 1992 May;2(3):359–366. doi: 10.1111/j.1365-313x.1992.00359.x. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- Wise R. P., Ellingboe A. H. Fine structure and instability of the Ml-a locus in barley. Genetics. 1985 Sep;111(1):113–130. doi: 10.1093/genetics/111.1.113. [DOI] [PMC free article] [PubMed] [Google Scholar]