Skip to main content
The Plant Cell logoLink to The Plant Cell
. 1998 Aug;10(8):1251–1266. doi: 10.1105/tpc.10.8.1251

The tomato Cf-9 disease resistance gene functions in tobacco and potato to confer responsiveness to the fungal avirulence gene product avr 9

KE Hammond-Kosack 1, S Tang 1, K Harrison 1, JD Jones 1
PMCID: PMC144066  PMID: 9707527

Abstract

The Cf-9 gene encodes an extracytoplasmic leucine-rich repeat protein that confers resistance in tomato to races of the fungus Cladosporium fulvum that express the corresponding avirulence gene Avr 9. We investigated whether the genomic Cf-9 gene functions in potato and tobacco. Transgenic tobacco and potato plants carrying Cf-9 exhibit a rapid hypersensitive cell death response (HR) to Avr 9 peptide injection. Cf 9 tobacco plants were reciprocally crossed to Avr 9-producing tobacco. A developmentally regulated seedling lethal phenotype occurred in F1 progeny when Cf9 was used as the male parent and Avr 9 as the female parent. However, when Cf9 was inherited in the maternal tissue and a heterozygous Avr 9 plant was used as the pollen donor, a much earlier reaction was caused, leading to no germination of any F1 seed. Detailed analysis of the Avr 9-induced responses in Cf 9 tobacco leaves revealed that (1) most mesophyll cells died within 3 hr (compared with 12 to 16 hr in tomato); (2) the macroscopic HR was visible at an Avr 9 titer five times lower than that which caused visible symptoms in tomato; (3) the HR invariably extended into noninjected panels of the tobacco leaf; (4) no HR occurred in leaves of young tobacco plants; (5) in older plants, the HR was dramatically enhanced by sequential Avr 9 challenges; and (6) coexpression of a salicylate hydroxylase transgene (nahG) from Pseudomonas putida reduced the severity of the macroscopic leaf HR and also restored germination to Cf 9 x 35S:Avr 9 F1 seedlings. Simultaneous introduction of Cf-9 homologs (Hcr 9-9 genes A and B or D) along with the native Cf-9 gene did not alter the responses that were specifically induced by Avr 9. Various ways to use the Cf-9-Avr 9 gene combination to engineer broad-spectrum disease resistance in several solanaceous species are discussed.

Full Text

The Full Text of this article is available as a PDF (308.7 KB).

Selected References

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

  1. A simple and general method for transferring genes into plants. Science. 1985 Mar 8;227(4691):1229–1231. doi: 10.1126/science.227.4691.1229. [DOI] [PubMed] [Google Scholar]
  2. Baker B., Zambryski P., Staskawicz B., Dinesh-Kumar S. P. Signaling in plant-microbe interactions. Science. 1997 May 2;276(5313):726–733. doi: 10.1126/science.276.5313.726. [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. Century K. S., Shapiro A. D., Repetti P. P., Dahlbeck D., Holub E., Staskawicz B. J. NDR1, a pathogen-induced component required for Arabidopsis disease resistance. Science. 1997 Dec 12;278(5345):1963–1965. doi: 10.1126/science.278.5345.1963. [DOI] [PubMed] [Google Scholar]
  5. De Wit P. J., Hofman A. E., Velthuis G. C., Kuć J. A. Isolation and Characterization of an Elicitor of Necrosis Isolated from Intercellular Fluids of Compatible Interactions of Cladosporium fulvum (Syn. Fulvia fulva) and Tomato. Plant Physiol. 1985 Mar;77(3):642–647. doi: 10.1104/pp.77.3.642. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Delaney T. P., Uknes S., Vernooij B., Friedrich L., Weymann K., Negrotto D., Gaffney T., Gut-Rella M., Kessmann H., Ward E., Ryals J. A central role of salicylic Acid in plant disease resistance. Science. 1994 Nov 18;266(5188):1247–1250. doi: 10.1126/science.266.5188.1247. [DOI] [PubMed] [Google Scholar]
  7. 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]
  8. Gaffney T., Friedrich L., Vernooij B., Negrotto D., Nye G., Uknes S., Ward E., Kessmann H., Ryals J. Requirement of salicylic Acid for the induction of systemic acquired resistance. Science. 1993 Aug 6;261(5122):754–756. doi: 10.1126/science.261.5122.754. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. 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]
  11. 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]
  12. Hammond-Kosack K. E., Silverman P., Raskin I., Jones JDG. Race-Specific Elicitors of Cladosporium fulvum Induce Changes in Cell Morphology and the Synthesis of Ethylene and Salicylic Acid in Tomato Plants Carrying the Corresponding Cf Disease Resistance Gene. Plant Physiol. 1996 Apr;110(4):1381–1394. doi: 10.1104/pp.110.4.1381. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. 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]
  14. Jabs T., Dietrich R. A., Dangl J. L. Initiation of runaway cell death in an Arabidopsis mutant by extracellular superoxide. Science. 1996 Sep 27;273(5283):1853–1856. doi: 10.1126/science.273.5283.1853. [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. 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]
  17. Keen N. T. Gene-for-gene complementarity in plant-pathogen interactions. Annu Rev Genet. 1990;24:447–463. doi: 10.1146/annurev.ge.24.120190.002311. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. Kooman-Gersmann M., Vogelsang R., Hoogendijk E. C., De Wit P. J. Assignment of amino acid residues of the AVR9 peptide of Cladosporium fulvum that determine elicitor activity. Mol Plant Microbe Interact. 1997 Sep;10(7):821–829. doi: 10.1094/MPMI.1997.10.7.821. [DOI] [PubMed] [Google Scholar]
  20. Lamb Chris, Dixon Richard A. THE OXIDATIVE BURST IN PLANT DISEASE RESISTANCE. Annu Rev Plant Physiol Plant Mol Biol. 1997 Jun;48(NaN):251–275. doi: 10.1146/annurev.arplant.48.1.251. [DOI] [PubMed] [Google Scholar]
  21. March R. Muscle up. STEP Perspect. 1998 Fall;98(3):6-7, 12. [PubMed] [Google Scholar]
  22. May M. J., Hammond-Kosack K. E., Jones JDG. Involvement of Reactive Oxygen Species, Glutathione Metabolism, and Lipid Peroxidation in the Cf-Gene-Dependent Defense Response of Tomato Cotyledons Induced by Race-Specific Elicitors of Cladosporium fulvum. Plant Physiol. 1996 Apr;110(4):1367–1379. doi: 10.1104/pp.110.4.1367. [DOI] [PMC free article] [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. 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]
  25. Rommens C. M., Salmeron J. M., Oldroyd G. E., Staskawicz B. J. Intergeneric transfer and functional expression of the tomato disease resistance gene Pto. Plant Cell. 1995 Oct;7(10):1537–1544. doi: 10.1105/tpc.7.10.1537. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Ryals J. A., Neuenschwander U. H., Willits M. G., Molina A., Steiner H. Y., Hunt M. D. Systemic Acquired Resistance. Plant Cell. 1996 Oct;8(10):1809–1819. doi: 10.1105/tpc.8.10.1809. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Salmeron J. M., Oldroyd G. E., Rommens C. M., Scofield S. R., Kim H. S., Lavelle D. T., Dahlbeck D., Staskawicz B. J. 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. 1996 Jul 12;86(1):123–133. doi: 10.1016/s0092-8674(00)80083-5. [DOI] [PubMed] [Google Scholar]
  28. Shirasu K., Nakajima H., Rajasekhar V. K., Dixon R. A., Lamb C. Salicylic acid potentiates an agonist-dependent gain control that amplifies pathogen signals in the activation of defense mechanisms. Plant Cell. 1997 Feb;9(2):261–270. doi: 10.1105/tpc.9.2.261. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Thilmony R. L., Chen Z., Bressan R. A., Martin G. B. Expression of the Tomato Pto Gene in Tobacco Enhances Resistance to Pseudomonas syringae pv tabaci Expressing avrPto. Plant Cell. 1995 Oct;7(10):1529–1536. doi: 10.1105/tpc.7.10.1529. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. 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]
  31. 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]
  32. Whitham S., McCormick S., Baker B. The N gene of tobacco confers resistance to tobacco mosaic virus in transgenic tomato. Proc Natl Acad Sci U S A. 1996 Aug 6;93(16):8776–8781. doi: 10.1073/pnas.93.16.8776. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. 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