Recognitional specificity and evolution in the tomato-Cladosporium fulvum pathosystem

Molecular Plant-Microbe Interactions

Volumn 22, Issue 10, 2009, Pages 1191-1202

  Wulff, B B H ^a   Chakrabarti, A ^b,c   Jones, D A ^b  

^a INST DE BIOL MOLEC DES PLANTES   (France)

^b AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^c CSIRO   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CF PROTEIN, LYCOPERSICON ESCULENTUM; FUNGAL PROTEIN; MEMBRANE PROTEIN; VEGETABLE PROTEIN;

CLADOSPORIUM; ECOSYSTEM; EVOLUTION; FUNGAL GENE; GENETIC VARIABILITY; GENETICS; HOST PATHOGEN INTERACTION; MICROBIOLOGY; PATHOGENICITY; PHYSIOLOGY; PLANT DISEASE; PLANT GENE; REVIEW; TOMATO;

CLADOSPORIUM; ECOSYSTEM; EVOLUTION; FUNGAL PROTEINS; GENES, FUNGAL; GENES, PLANT; GENETIC VARIATION; HOST-PATHOGEN INTERACTIONS; LYCOPERSICON ESCULENTUM; MEMBRANE GLYCOPROTEINS; PLANT DISEASES; PLANT PROTEINS;

CLADOSPORIUM; CLADOSPORIUM FULVUM; FUNGI; LYCOPERSICON ESCULENTUM; PASSALORA FULVA; SOLANUM;

EID: 70249116038     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-22-10-1191     Document Type: Review

References (82)

1. Bolton, M. D., van Esse, H. P., Vossen, J. H., de Jonge, R., Stergiopoulos, I., Stulemeijer, I. J. E., van den Berg, G. C. M., Borrás-Hidalgo, O., Dekker, H. L., de Koster, C. G., de Wit, P. J. G. M., Joosten, M. H. A. J., and Thomma, B. P. H. J. 2008. The novel Cladosporium fulvum lysin motif effector Ecp6 is a virulence factor with orthologues in other fungal species. Mol. Microbiol. 69:119-136.
2. Bomblies, K., and Weigel, D. 2007. Hybrid necrosis: Autoimmunity as a potential gene-flow barrier in plant species. Nat. Rev. Genet. 8:382-393.
3. Bomblies, K., Lempe, J., Epple, P., Warthmann, N., Lanz, C., Dangl, J. L., and Weigel, D. 2007. Autoimmune response as a mechanism for a Dobzhansky-Muller-type incompatibility syndrome in plants. PLoS Biol. 5:e236. (Pubitemid 47416594)
4. Caicedo, A. L., and Schaal, B. A. 2004. Heterogeneous evolutionary processes affect R gene diversity in natural populations of Solanum pimpinellifolium. Proc. Natl. Acad. Sci. U.S.A. 101:17444-17449.
5. Chakrabarti, A., Panter, S. N., Harrison, K., Jones, J. D. G., and Jones, D. A. 2009. Regions of the Cf-9B disease resistance protein able to cause spontaneous necrosis in Nicotiana benthamiana lie within the region controlling pathogen recognition in tomato. Mol. Plant-Microbe lnteract. 22:1214-1226
6. Crameri, A., Raillard, S., Bermudez, E., and Stemmer, W. P. C. 1998. DNA shuffling of a family of genes from, diverse species accelerates directed evolution. Nature 391:288-291. (Pubitemid 28099016)
7. Dangl, J. L., and Jones, J. D. G. 200.1. Plant pathogens and integrated defence responses to infection. Nature 411:826-833.
8. de Kock, M. J. D., Iskandar, H. M., Brandwagt, B. F., Laugé, R., de Wit, P. J. G. M., and Lindhout, P. 2004. Recognition of Cladosporium fulvum Ecp2 elicitor by non-host Nicotiana spp. is mediated by a single dominant gene that is not homologous to known Cf-genes. Mol. Plant Pathol. 5:397-408.
9. Kock, M. J. D., Brandwagt, B. F., Bonnema, G., de Wit, P. J. G. M., and Lindhout, P. 2005. The tomato Orion locus comprises a unique class of Hcr9 genes. Mol. Breeding. 15:409-422. (Pubitemid 40876697)
10. de Wit, P. J. G. M., Joosten, M. H. A. J., Thomma, B. P. H. J., and Stergiopoulos, I. 2009. Gene for gene models and beyond: The Cladosporium fulvum-tomato pathosystem. Pages 135-156 in: The Mycota V: Plant Relationships. 2nd ed. H. B. Deising, ed. Springer, Berlin.
11. Dickinson, M., Jones, D. A., and Jones, J. D. G. 1993. Close linkage between the Cf-2/Cf-5 and Mi resistance loci in tomato. Mol. PlantMicrobe Interact. 6:341-347.
12. Dixon, M. S., Jones, D. A., Keddie, J. S., Thomas, C. M., Harrison, K., and Jones J. D. G. 1996. The tomato Cf-2 disease resistance locus comprises two functional genes encoding leucine-rich repeat proteins. Cell 84:451-459.
13. Dixon, M. S., Hatzixanthis, K., Jones, D. A., Harrison, K., and Jones, J. D. G. 1998. The tomato Cf-5 disease resistance gene and six homologs show pronounced allelic variation in leucine-rich repeat copy number. Plant Cell 10:1915-1925.
14. ixon, M. S., Golstein, C., Thomas, C. M., van der Biezen. E. A., and Jones, J. D. G. 2000. Genetic complexity of pathogen perception by plants: The example of Rcr3, a tomato gene required specifically by Cf-2. Proc. Natl. Acad. Sci. U.S.A. 97:8807-8814.
15. Fradin, E. F., Zhang, Z., Juarez Ayala, J. C., Castroverde, C. D. M., Nazar, R. N., Robb, J., Liu, C-M., and Thomma, B. P. H. J. 2009. Genetic dissection of Vertidllium wilt resistance mediated by tomato Vel. Plant Physiol. 150:320-332.
16. Haanstra, J. P. W., Laugé, R., Meijer-Dekens, F., Bonnema, G., de Wit, P. J. G. M., and Lindhout, P. 1999. The Cf-ECP2 gene is linked to, but not part of, the Cf-4/Cf-9 cluster on the short arm of chromosome 1 in tomato. Mol. Gen. Genet. 262:839-845.
17. Haanstra, J. P. W, Meijer-Dekens, F., Laugé, R., Seetanah, D. C., Joosten, M. H. A. J., de Wit, P. J. G. M., and Lindhout, P. 2000. Mapping strategy for resistance genes against Cladopsorium fulvum on the short arm of chromosome 1 of tomato: Cf-ECPS near the Hcr9 Milky Way cluster. Theor. Appl. Genet. 101:661-668. (Pubitemid 30729782)
18. Hammond-Kosack, K. E., Tang, S., Harrison, K., and Jones, J. D. G. 1998. The tomato Cf-9 disease resistance gene functions in tobacco and potato to confer responsiveness to the fungal avirulence gene product Avr9. Plant Cell 10:1251-1266.
19. Hougenhout, S. A., van der Hoorn, R. A. L., Terauchi, R., and Kamoun, S. 2009. Emerging concepts in effector biology of plant associated organisms. Mol. Plant-Microbe Interact. 22:115-122.
20. Jones, D. A., Thomas, C. M., Hammond-Kosack, K. E., Balint-Kurti, P. J., and Jones, J. D. G. 1994. Isolation of the tomato Cf-9 gene for resistance to Cladosporium fulvum by transposon tagging. Science 266:789-793.
21. Joosten, M. H. A. J., Cozijnsen, T. J., and de Wit, P. J. G. M. 1994. Host resistance to a fungal tomato pathogen lost by a single base-pair change in an avirulence gene. Nature 367:384-386.
22. Joosten, M. H. A. J., Vogelsang, R., Cozijnsen, T J., Verberne, M. C., and de Wit, P. J. G. M. 1997. The biotrophic fungus Cladosporium fulvum circumvents cy-4-mediated resistance by producing unstable AVR4 elicitors. Plant Cell 9:367-379.
23. Kobe, B., and Deisenhofer, J. 1995. A structral basis of the interactions between leucine-rich repeats and their protein ligands. Nature 374:183-186.
24. Kooman-Gersmann, M. 1998. The AVR9 elicitor peptide of the tomato pathogen Cladopsorium fulvum: Molecular aspects of recognition. PhD Thesis, Wageningen University.
25. Kooman-Gersmann, M., Honée, G., Bonnema, G., and de Wit P. J. G. M. 1996. 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 8:929-938.
26. Kooman-Gersmann, M., Vogelsang, R., Hoogendijk, E. C. M., and de Wit, P. J. G. M. 1997. Assignment of amino acid residues of the AVR9 peptide of Cladosporium fulvum that determine elicitor activity. Mol. PlantMicrobe Interact. 10:821-829.
27. Kooman-Gersmann, M., Vogelsang, R., Vossen, P., van den Hooven, H. W., Mahé, E., Honée, G., and de Wit, P. J. G. M. 1998. Correlation between binding affinity and necrosis-inducing activity of mutant AVR9 peptide elicitors. Plant Physiol. 117:609-618. (Pubitemid 128652834)
28. Krüger, J., Thomas, C. M., Golstein, C., Dixon, M. S., Smoker, M., Tang, S., Mulder, L., and Jones, J. D. G. 2002. A tomato cysteine protease re- quired for C/-2-dependent disease resistance and suppression of autonecrosis. Science 296:744-747. (Pubitemid 34442004)
29. Kruijt, M., Brandwagt, B. F., and de Wit, and P. J. G. M. 2004. Rearrangements in the Cf-9 disease resistance gene cluster of wild tomato have resulted in three genes that mediate Avr9 responsiveness. Genetics 168:1655-1663.
30. Kruijt, M., Kip, D. J., Joosten, M. H. A. J., Brandwagt, B. F., and de Wit, P. J. G. M. 2005a. The Cf-4 and Cf-9 resistance genes against Cladosporium fulvum are conserved in wild tomato species. Mol. PlantMicrobe Interact. 18:1011-1021.
31. Kruijt, M., de Kock, M. J. D., and de Wit, P. J. G. M. 2005b. Receptor-like proteins involved in plant disease resistance. Mol. Plant Path. 6:85-97.
32. Kvitko, B. H., Park, D. H., Velasquez, A. C., Wei, C.-F., Russell, A. B., Martin, G. B., Schneider, D. J., and Collmer, A. 2009. Deletions in the repertoire of Pseudomonas syringae pv. tomato DC3000 Type III secretion effector genes reveal functional overlap among effectors. PLoS Pathog. 5:e1000388.
33. Laugé, R, Joosten, M. H. A. J., van den Ackerveken, G. F. J. M., van den Broek, H. W. J., and de Wit, P. J. G. M. 1997. The in pfania-produced extracellular proteins ECP1 and ECP2 of Cladosporium fulvum are virulence factors. Mol. Plant-Microbe Interact. 10:725-734.
34. Laugé, R., Dmitriev, A. P., Joosten, M. H. A. J., and de Wit, P. J. G. M. 1998a. Additional resistance gene(s) against Cladosporium fulvum present on the Cf-9 introgression segment are associated with strong PR protein accumulation. Mol. Plant-Microbe Interact. 11:301-308.
35. Laugé, R., Joosten, M. H. A. J., Haanstra, J. P. W., Goodwin, P. H., Lindhout, P., and de Wit, P. J. G. M. 1998b. Successful search for a resistance gene in tomato targeted against a virulence factor of a fungal pathogen. Proc. Natl. Acad. Sci. U.S.A. 95:9014-9018.
36. Laugé, R., Goodwin, P. H., de Wit, P. J. G. M., and Joosten, M. H. A. J. 2000. Specific HR-associated recognition, of secreted proteins from Cladosporium fulvum occurs in both host and non-host plants. Plant J. 23:735-745.
37. Lindhout, P., Korta, W., Cislik, M., Vos, I., and Gerlagh, T. 1989. Further identification of races of Cladosporium fulvum (Fulvia fulva) on tomato originating from the Netherlands, France and Poland. Neth. J. Plant Path. 95:143-148.
38. Luderer, R., Rivas, S., Nürnberger, T., Mattei, B., van den Hooven, H. W., van der Hoorn, R. A. L., Romeis, T., Wehrfritz, J. M., Blume, B., Nennstiel, D., Zuidema, D., Vervoort, J., De Lorenzo, G., Jones, J. D. G., de Wit, P. J. G. M., and Joosten, M. H. A. J. 2001. No evidence for binding between resistance gene product Cf-9 of tomato and avirulence gene product AVR9 of Cladosporium fulvum. Mol. Plant-Microbe Interact. 14:867-876.
39. Luderer, R., Takken, F. L. W., de Wit, P. J. G., M., and Joosten, M. H. A. J. 2002. Cladosporium fulvum overcomes Cf-2-mediated resistance by producing truncated AVR2 elicitor proteins. Mol. Microbiol. 45:875-884.
40. Padmanabhan, M., Cournoyer, P., and Dinesh-Kumar, S. P. 2009. The leucine-rich repeat domain in plant innate immunity: A wealth of possibilities. Cellular Microbiol. 11:191-198.
41. Panter, S. N., Hammond-Kosack, K. E., Harrison, K., Jones, J. D. G., and Jones, D. A. 2002. Developmental control of promoter activity is not responsible for mature onset of Cf-9B-mediated resistance to leaf mold in tomato. Mol. Plant-Microbe Interact. 15:1099-1107.
42. Parniske, M., and Jones, J. D. G. 1999. Recombination between diverged clusters of the tomato Cf-9 plant disease resistance gene family. Proc. Natl. Acad. Sci. U.S.A. 96:5850-5855.
43. Parniske, M., Hammond-Kosack, K. E., Golstein, C., Thomas, C. M., Jones, D. A., Harrison, K., Wulff, B. B. H., and Jones, J. D. G. 1997. Novel disease resistance specificities result from sequence exchange between tandemly repeated genes at the Cf-4/9 locus of tomato. Cell 91:821-832. (Pubitemid 28007738)
44. Parniske, M., Wulff, B. B. H., Bonnema, G., Thomas, C. M., Jones, D. A., and Jones, J. D. G. 1999. Homologues of the Cf-9 disease resistance gene (Hcr9s) are present at multiple loci on the short arm of tomato chromosome 1. Mol. Plant-Microbe Interact. 12:93-102.
45. Rivas, S., and Thomas, C. M. 2005. Molecular interactions between tomato and the leaf mold pathogen Cladosporium fulvum. Ann. Rev. Phytopathol. 43:395-436.
46. Rooney, H. C. E., van't Klooster, J. W., van der Hoorn, R. A. L., Joosten, M. H. A. J., Jones, J. D. G., and de Wit, P. J. G. M. 2005. Cladosporium Avr2 inhibits tomato Rcr3 protease required for Cf-2-dependent disease resistance. Science 308:1783-1786 (Erratum: Science 310:54).
47. Seear, P. J., and Dixon, M. S. 2003. Variable leucine-rich repeats of tomato disease resistance genes Cf-2 and Cf-5 determine specificity. Mol. Plant Pathol. 4:199-202.
48. Shabab, M., Shindo, T., Gu, C., Kaschani. F., Pansuriya. T., Chintha, R., Harzen, A., Colby, T., Kamoun, S., and van der Hoorn, R. A. L. 2008. Fungal effector protein AVR2 targets diversifying defense-related cys proteases of tomato. Plant Cell 20:1169-1183. (Pubitemid 352843986)
49. Song, J., Win, J., Tian, M., Schomack, S., Kaschani, F., Ilyas, M., van der Hoorn, R. A. L., and Kamoun, S. 2009. Apoplastic effectors secreted by two unrelated eukaryotic plant pathogens target the tomato defense protease Rcr3. Proc. Natl. Acad. Sci. U.S.A. 106:1654-1659.
50. Soumpourou, E., lakovidis, M., Chartrain, L., Lyall, V., and Thomas, C. M. 2007. The Solanum pimpinellifolium Cf-ECP1 and Cf-ECP4 genes for resistance to Cladosporium fulvum are located at the Milky Way locus on the short arm of chromosome 1. Theor. Appl. Genet. 115:1127-1136.
51. Stemmer, W. P. C. 1994. Rapid evolution of a protein in vitro by DNA shuffling. Nature 370:389-391.
52. Stergiopoulos, I., and de Wit, P. J. G. M. 2009. Fungal effector proteins. Ann. Rev. Phytopathol. 47:233-263.
53. Stergiopoulos, I., Groenewald, M., Staats, M., Lindhout, P., Crous, P. W., and de Wit, P. J. G. M. 2007a. Mating-type genes and the genetic structure of a world-wide collection of the tomato pathogen Cladosporium fulvum. Fungal Genet. Biol. 44:415-429. (Pubitemid 46483141)
54. Stergiopoulos, I., de Kock, M. J. D., Lindhout, P., and de Wit, P. J. G. M. 2007b. Allelic variation in the effector genes of the tomato pathogen Cladosporium fulvum reveals different modes of adaptive evolution. Mol. Plant-Microbe Interact. 20:1271-1283.
55. Stevens, M. A., and Rick, C. M. 1988. Genetics and breeding. Pages 35-109 in: The Tomato Crop, J. G. Atherton and J. Rudich, eds. Chapman and Hall, London.
56. Takken, F. L., Thomas, C. M., Joosten, M. H. A. J., Golstein, C., Westerink, N., Hille, J., Nijkamp, H. J., de Wit, P. J. G. M., and Jones, J. D. G. 1999. A second gene at the tomato Cf-4 locus confers resistance to Cladosporium fulvum through recognition of a novel avirulence determinant. Plant J. 20:279-288.
57. Thomas, C. M., Jones, D. A., Parniske, M., Harrison, K., Balint-Kurti, P. J., Hatzixanthis, K., and Jones, J. D. G. 1997. 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 9, 2209-2224.
58. Thomas, C. M., Tang, S., Hammond-Kosack, K., and Jones, J. D. G. 2000. Comparison of the hypersensitive response induced by the tomato Cf-4 and Cf-9 genes in Nicotiana spp. Mol. Plant-Microbe Interact. 13:465-469. (Pubitemid 30174530)
59. Tian, M., Win, J., Song, J., van der Hoorn, R., van der Knaap, E., and Kamoun, S. 2007. A Phytophthora infestons cystatin-like protein targets a novel tomato papain-like apoplastic protease. Plant Physiol. 143:364-377.
60. van den Ackerveken, G. F. J. M., van Kan, J. A. L., and de Wit, P. J. G. M. 1992. Molecular analysis of the avirulence gene avr9 of the fungal tomato pathogen Cladosporium fulvum fully supports the gene-for-gene hypothesis. Plant J. 2:359-366.
61. van den Ackerveken, G. F. J. M, van Kan, J. A. L., Joosten, M. H. A. J., Muisers, J. M., Verbakel, H. M., and de Wit, P. J. G. M. 1993. Characterization of two putative pathogenicity genes of the fungal tomato pathogen Cladosporium fulvum. Mol. Plant-Microbe Interact. 6:210-215.
62. 15N double labeling of the avirulence protein AVR4 in a methanolutilizing strain (Mut*) of Pichia pastoris. J. Biomol. NMR 20:251-261.
63. Van den Burg, H. A., Westerink, N., Francoijs, K.J., Roth, R., Woestenenk, E., Boeren, S., de Wit, P. J. G. M., Joosten, M. H. A. J., and Vervoort, J. 2003. Natural disulfide bond-disrupted mutants of AVR4 of the tomato pathogen Cladosporium fulvum are sensitive to proteolysis, circumvent Cf-4-mediated resistance, but retain their chitin binding ability. J. Biol. Chem. 278:27340-27346.
64. van den Burg, H. A., Spronk, C. A. E. M., Boeren, S., Kennedy, M. A., Vissers, J. P. C., Vuister, G. W., de Wit, P. J. G. M., and Vervoort, J. 2004. Binding of the AVR4 elicitor of Cladosporium fulvum to chitotriose units is facilitated by positive allosteric protein-protein interactions: The chitin-binding site of AVR4 represents a novel binding site on the folding scaffold shared between the invertebrate and the plant chitin-binding domain. J. Biol. Chem. 279:16786-16796.
65. Van den Burg, H. A., Harrison, S. J., Joosten, M. H. A. J., Vervoort J, and de Wit, P. J. G. M. 2006. Cladosporium fulvum Avr4 protects fungal cell walls against hydrolysis by plant chitinases accumulating during infection. Mol. Plant-Microbe Interact. 19:1420-1430.
66. van der Biezen, E. A., and Jones, J. D. G. 1998. Plant disease resistance proteins and the "gene-for-gene" concept. Trends Biochem. Sci. 23:454-456.
67. van der Hoorn, R. A. L. 2001. The Cf-4 and Cf-9 proteins of tomato: Molecular aspects of specificity and elicitor perception. Ph.D. thesis, Wageningen University.
68. van der Hoorn, R. A. L., and Kamoun, S. 2008. From Guard to Decoy: A new model for perception of plant pathogen effectors. Plant Cell 20:2009-2017. (Pubitemid 352844506)
69. van der Hoorn, R. A. L., Laurent, F., Roth, R., and de Wit, P. J. G. M. 2000. Agroinfiltration is a versatile tool that facilitates comparative analyses of Avr9/Cf-9-induced and Avr4/Cf-4-induced necrosis. Mol. Plant-Microbe Interact. 13:439-446.
70. van der Hoom, R. A. L., Roth, R., and de Wit, P. J. G. M. 2001a. Identification of distinct specificity determinants in resistance protein Cf-4 allows construction of a Cf-9 mutant that confers recognition of avirulence protein Avr4. Plant Cell 13:273-285. (Pubitemid 32207683)
71. van der Hoorn, R. A. L., Kruijt, M., Roth, R., Brandwagt, B. F., Joosten, M. H. A. J., and de Wit, P. J. G. M. 2001b. Intragenic recombination generated two distinct Cf genes that mediate AV.R9 recognition in the natural population of Lycopersicon pimpinellifolium. Proc. Natl. Acad. Sci. U.S.A. 98:10493-10498. (Pubitemid 32803047)
72. van der Hoorn, R. A. L., Wulff, B. B. H., Rivas, S., Durrant, M. C., van der Ploeg, A., de Wit, P. J. G. M., and Jones, J. D. G. 2005. Structure-function analysis of Cf-9, a receptor-like protein with extracytoplasmic leucine-rich repeats. Plant Cell 17:1000-1015. (Pubitemid 43138236)
73. van Esse, H. P., Bolton, M. D., Stergiopoulos, I., de Wit, P. J. G. M., and Thomma, B. P. H. J. 2007. The chitin-binding Cladosporium fulvum effector protein Avr4 is a virulence factor. Mol. Plant-Microbe Interact. 20:1092-1101.
74. van Esse, H. P., van't Klooster, J. W., Bolton, M. D., Yadeta, K. A., van Baarlen, P., Boeren, S., Vervoort, J., de Wit, P. J. G. M., and Thomma B. P. H. J. 2008. The Cladosporium fulvum virulence protein Avr2 inhibits host proteases required for basal defense. Plant Cell 20:1948-1963.
75. Vervoort, J., van den Hooven, H. W., Berg, A., Vossen, P., Vogelsang, R., Joosten, M. H. A. J., and de Wit, P. J. G. M. 1997. The race-specific elicitor AVR9 of the tomato pauthogen Cladosporium fulvum: A cystine knot protein. Sequence-specific H NMR assignments, secondary structure and global fold of the protein. FEBS (Fed. Eur. Biochem. Soc.) Lett. 404:153-158.
76. Westerink, N. 2003. The role of AVR4 and AVR4E proteins in virulence and avirulence of the tomato pathogen Cladosporium fulvum: Molecular aspects of disease susceptibility and resistance. Ph.D. Thesis, Wageningen University.
77. Westerink, N., Brandwagt, B. F., de Wit, P. J. G. M., and Joosten, M. H. A. J. 2004. Cladosporium fulvum circumvents the second functional resistance gene homologue at the Cf-4 locus (Hcr9-4E) by secretion of a stable avr4E isoform. Mol. Microbiol. 54:533-545.
78. Wubben, J. P., Joosten, M. H. A. J., and de Wit, P. J. G. M. 1994. Expression and localization of two in planta induced extracellular proteins of the fungal tomato pathogen Cladosporium fulvum. Mol. Plant-Microbe Interact. 7:516-524.
79. B. B. H., Thomas, C. M., Smoker, M., Grant, M., and Jones, J. D. G. 2001. Domain swapping and gene shuffling identify sequences required for induction of an Avr-dependent hypersensitive response by the tomato Cf-4 and Cf-9 proteins. Plant Cell 13:255-272. (Pubitemid 32207682)
80. B. B. H., Kruijt, M., Collins, P. L., Thomas, C. M., Ludwig, A. A., de Wit, P. J. G. M., and Jones, J. D. G. 2004a. Gene shuffling-generated and natural variants of the tomato resistance gene Cf-9 exhibit different auto-necrosis-inducing activities in Nicotiana species. Plant J. 40:942-956. (Pubitemid 40047633)
81. Wulff, B. B. H., Thomas, C. M., Parniske, M., and Jones, J. D. G. 2004b. Genetic variation at the tomato Cf-4/Cf-9 locus induced by EMS mutagenesis and intralocus recombination. Genetics 167:459-470.
82. Wulff, B. B. H., Heese, A., Tomlinson-Buhot, L., Jones, D. A., de la Peña, M., and Jones, J. D. G. 2009. The major specificity-determining amino acids of the tomato Cf-9 disease resistance protein are at hypervariable solvent-exposed positions in. the central leucine-rich repeats. Mol. Plant-Microbe Interact. 22:1203-1213.