Gene shuffling-generated and natural variants of the tomato resistance gene Cf-9 exhibit different auto-necrosis-inducing activities in Nicotiana species

Plant Journal

Volumn 40, Issue 6, 2004, Pages 942-956

  Wulff, Brande B H ^a,d   Kruijt, Marco ^b   Collins, Peter L ^a   Thomas, Colwyn M ^c   Ludwig, Andrea A ^a,e   De Wit, Pierre J G M ^b   Jones, Jonathan D G ^a  

^a SAINSBURY LABORATORY   (United Kingdom)

^b WAGENINGEN UNIVERSITY   (Netherlands)

^c UNIVERSITY OF EAST ANGLIA   (United Kingdom)

^d Universitat Politècnica de València   (Spain)

^e UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Auto activator; Cf 9; Cladosporium fulvum; Resistance gene; Shuffling; Tomato

Indexed keywords

FUNGI; GENES; PROTEINS;

HYPERSENSITIVE RESPONSE (HR); TOMATO SPECIES;

PLANTS (BOTANY);

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

ALLELE; AMINO ACID SEQUENCE; ARTICLE; CLADOSPORIUM; GENE; GENE LIBRARY; GENE VECTOR; GENETIC VARIABILITY; GENETICS; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; MULTIGENE FAMILY; NECROSIS; NUCLEOTIDE SEQUENCE; PATHOGENICITY; PLANT DISEASE; RHIZOBIUM; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; SPECIES DIFFERENCE; TOBACCO; TOMATO;

ALLELES; AMINO ACID SEQUENCE; CLADOSPORIUM; GENE LIBRARY; GENES, PLANT; GENETIC VECTORS; LYCOPERSICON ESCULENTUM; MEMBRANE GLYCOPROTEINS; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; NECROSIS; PLANT DISEASES; PLANT PROTEINS; RECOMBINANT FUSION PROTEINS; RHIZOBIUM; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; SPECIES SPECIFICITY; TOBACCO; VARIATION (GENETICS);

FUNGI; GENES; PLANTS; TOMATOES;

CLADOSPORIUM; CLADOSPORIUM FULVUM; LYCOPERSICON; LYCOPERSICON ESCULENTUM; LYCOPERSICON PERUVIANUM; NICOTIANA; NICOTIANA BENTHAMIANA;

EID: 11144223858     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2004.02268.x     Document Type: Article

References (70)

1. Austin, M.J., Muskett, P., Kahn, K., Feys, B.J., Jones, J.D.G. and Parker, J.E. (2002) Regulatory role of SGT1 in early R gene-mediated plant defenses. Science, 295, 2077-2080.
2. Azevedo, C., Sadanandom, A., Kitagawa, K., Freialdenhoven, A., Shirasu, K. and Schulze-Lefert, P. (2002) The RAR1 interactor SGT1, an essential component of R gene-triggered disease resistance. Science, 295, 2073-2076.
3. Bendahmane, A., Farnham, G., Moffett, P. and Baulcombe, D.C. (2002) Constitutive gain-of-function mutants in a nucleotide binding site-leucine rich repeat protein encoded at the Rx locus of potato. Plant J. 32, 195-204.
4. + channels of Cf-9 transgenic tobacco guard cells as targets for Cladosporium fulvum Avr9 elicitor-dependent signal transduction. Plant J, 19, 453-462.
5. Brading, P.A., Hammond-Kosack, K.E., Parr, A. and Jones, J.D.G. (2000) Salicylic acid is not required for Cf-2 and Cf-9 dependent resistance of tomato to Cladosporium fulvum. Plant J. 23, 305-318.
6. Chang, J.F., Tai, Y.-S., Bernai, A.J., Lavelle, D.T., Staskawicz, B.J. and Michelmore, R.W. (2002) Functional analyses of the Pto resistance gene family in tomato and the identification of a minor resistance determinant in a susceptible haplotype. Mol. Plant Microbe Interact. 15, 281-291.
7. Dangl, J.L. and Jones, J.D.G. (2001) Plant pathogens and integrated defence responses to infection. Nature, 411, 826-833.
8. De Jong, C.F., Honée, G., Joosten, M.H.A.J. and De Wit, P.J.G.M. (2000) Early defence responses induced by AVR9 and mutant analogues in tobacco cell suspensions expressing the Cf-9 resistance gene. Physiol. Mol. Plant Pathol. 56, 169-177.
9. De Jong, C.F, Takken, F.L.W., Cai, X., De Wit, P.J.G.M. and Joosten, M.H.A.J. (2002) Attenuation of Cf-mediated defence responses at elevated temperatures correlates with a decrease in elicitor-binding sites. Mol. Plant Microbe Interact. 15, 1040-1049.
10. De Wit, P.J.G.M. and Spikman, G. (1982) Evidence for the occurrence of race- and cultivar-specific elicitors of necrosis in intercellular fluids of compatible interactions between Cladosporium fulvum and tomato. Physiol. Plant Pathol. 21, 1-11.
11. Dixon, M.S., Jones, D.A., Keddie, J.S., Thomas, C.M., Harrison, K. and Jones, J.D.G. (1996) The tomato CT-2 disease resistance locus comprises two functional genes encoding leucine-rich repeat proteins. Cell, 84, 451-459.
12. 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.
13. Dixon, 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. USA, 97, 8807-8814.
14. Flor, H.H. (1946) Genetics of pathogenicity in Melampsora lini. J. Agric. Res. 73, 335-357.
15. Frost, D., Way, H., Howles, P., Luck, J., Manners, J., Hardham, A., Finnegan, J. and Ellis, J. (2004) Tobacco transgenic for the flax rust resistance gene L expresses allele-specific activation of defense responses. Mol. Plant Microbe Interact. 17, 224-232.
16. Hammond-Kosack, K.E. and Jones, J.D.G. (1996) Resistance gene-dependent plant defence responses. Plant Cell, 8, 1773-1791.
17. 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.
18. Honée, G., Buitink, J., Jabs, T., De Kloe, J., Sijbolts, F., Apotheker, M., Weide, R., Sijen, T., Stuiver, M. and De Wit, P.J.G.M. (1998) Induction of defense-related responses in Cf9 tomato cells by the AVR9 elicitor peptide of Cladosporium fulvum is developmentally regulated. Plant Physiol. 177, 809-820.
19. Horsch, R.B., Fry, J.E., Hoffmann, N.L., Eichholtz, D. and Fraley, R.T. (1985) A simple and general method for transferring genes into plants. Science, 273, 1229-1231.
20. Hu, G.S., Richter, T.E., Hulbert, S.H. and Pryor, T. (1996) Disease lesion mimicry caused by mutations in the rust resistance gene rp1. Plant Cell, 8, 1367-1376.
21. Hwang, C.F. and Williamson, V.M. (2003) Leucine-rich repeat-mediated intramolecular interactions in nematode recognition and cell death signalling by the tomato resistance protein Mi. Plant J. 34, 585-593.
22. Hwang, C.F., Bhakta, A.V., Truesdell, G.M., Pudlo, W.M. and Williamson, V.M. (2000) Evidence for a role of the N terminus and leucine-rich repeat region of the Mi gene product in regulation of localized cell death. Plant Cell, 12, 1319-1329.
23. Jones, D.A. and Jones, J.D.G. (1997) The role of leucine-rich repeat proteins in plant defences. Adv. Bot. Res. 24, 91-167.
24. Jones, J.D.G., Shlumukov, L., Carland, F., English, J., Scofield, S.R., Bishop, G.J. and Harrison, K. (1992) Effective vectors for transformation, expression of heterologous genes, and assaying transposon excision in transgenic plants. Transgenic Res. 1, 285-297.
25. 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.
26. Joosten, M.H.A.J. and De Wit, P.G.J.M. (1999) The tomato-Cladosporium fulvum interaction: a versatile experimental system to study plant-pathogen interactions. Annu. Rev. Phytopathol. 37, 335-367.
27. Kooman-Gersmann, M., Honée, G., Bonnema, G. and De Wit, P.J.G.M. (1996) A high-affinity binding site for Avr9 peptide elicitor of Cladosporium fulvum is present on plasma membranes of tomato and other solanaceous plants. Plant Cell, 8, 929-938.
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 required for Cf-2-dependent disease resistance and suppression of autonecrosis. Science, 296, 744-747.
29. Kruijt, M., Brandwagt, B.F. and De Wit, P.J.G.M. (2004a) Rearrangements in the Cf-9 disease resistance gene cluster of wild tomato have resulted in three genes that mediate Avr9 responsiveness. Genetics (in press).
30. Kruijt, M., Kip, D.J., Joosten, M.H.A.J., Brandwagt, B.F. and De Wit, P.J.G.M. (2004b) The Cf-4 and Cf-9 resistance genes against Cladosporium fulvum are conserved throughout the tomato genus. PhD Thesis. Wageningen University, pp. 53-72.
31. Laugé, R., Dmitriev, A.P., Joosten, M.H.A.J. and De Wit, P.J.G.M. (1998) Additional resistance genes against Cladosporium fulvum present on the Cf-9 introgression segment are associated with strong PR protein accumulation. Mol. Plant Microbe Interact. 11, 301-308.
32. 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.
33. Luderer, R., Rivas, S., Nürnberger, T. et al. (2000) 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.
34. Martin, G.B., Bogdanove, A.J. and Sessa, G. (2003) Understanding the functions of plant disease resistance proteins. Annu. Rev. Plant Biol. 54, 23-61.
35. Moffet, P., Farnham, G., Peart, J. and Baulcombre, D.C. (2002) Interaction between domains of a plant NBS-LRR protein in disease resistance-related cell death. EMBO J. 21, 4511-4519.
36. Murashige, T. and Skoog, F. (1962) A revised medium for rapid growth and bioassay with tobacco tissue cultures. Physiol. Plant. 15, 473-497.
37. Nimchuk, Z., Eulgem, T., Holt, B.F., III and Dangl, J.L. (2003) Recognition and response in the plant immune system. Annu. Rev. Genet. 37, 579-609.
38. Oldroyd, G.E.D. and Staskawicz, B.J. (1998) Genetically engineered broad-spectrum disease resistance in tomato. Proc. Natl Acad. Sci. USA, 95, 10300-10305.
39. 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.
40. 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. USA, 96, 5850-5855.
41. 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 Cf4/9 locus of tomato. Cell, 91, 821-832.
42. Peart, J.R., Lu, R., Sadanandom, A. et al. (2002) Ubiquitin ligase-associated protein SGT1 is required for host and nonhost disease resistance in plants. Proc. Natl Acad. Sci. USA, 99, 10865-10869.
43. Piedras, P., Hammond-Kosack, K.E., Harrison, K. and Jones, J.D.G. (1998) Rapid Cf-9 and Avr9-dependent production of active oxygen species in tobacco cell suspension cultures. Mol. Plant Microbe Interact. 11, 1155-1166.
44. Rathjen, J.P., Chang, J.H., Staskawicz, B.J. and Michelmore, R.W. (1999) Constitutively active Pro induces a Prf-dependent hyper-sensitive response in the absence of avrPto. EMBO J. 18, 3232-3240.
45. Rick, C.M. (1979) Biosystematic studies in Lycopersicon and closely related species of Solanum. In The Biology and Taxonomy of the Solanaceae. New York: Academic Press, Linn. Soc. Symp. Series, 7, 667-677.
46. Rivas, S. and Thomas, C.M. (2002) Recent advances in the study of tomato resistance genes. Mol. Plant Pathol. 3, 277-282.
47. Rivas, R., Rougon-Cardoso, A., Smoker, M., Schauser, L., Yoshioka, H. and Jones, J.D.G. (2004) CITRX thioredoxin is a negative regulator of cell death and defence responses that interacts with the tomato Cf-9 resistance protein. EMBO J. 23, 2156-2165.
48. Romeis, T., Piedras, P., Zhang, S., Klessig, D., Hirt, H. and Jones, J.D.G. (1999) Rapid Avr9- and Cf-9-dependent activation of MAP kinases in tobacco cell cultures and leaves: convergence of resistance gene, elicitor, wound, and salicylate responses. Plant Cell, 11, 273-287.
49. Romeis, T., Piedras, P. and Jones, J.D.G. (2000) Resistance gene-dependent activation of a calcium-dependent protein kinase in the plant defence response. Plant Cell, 12, 803-815.
50. Romeis, T., Ludwig, A.A., Martin, R. and Jones, J.D.G. (2001) Calcium-dependant protein kinases play an essential role in a plant defence response. EMBO J. 20, 5556-5567.
51. Stemmer, W.P.C. (1994) Rapid evolution of a protein in vitro by DNA shuffling. Proc. Natl Acad. Sci. USA. 91, 10747-10751.
52. Sun, Q., Collins, N.C., Ayliffe, M., Smith, S.M., Drake, J., Pryor, T. and Hulbert, S.H. (2001) Recombination between paralogues at the rp1 rust resistance locus in maize. Genetics, 158, 423-438.
53. Takken, F.L.W., Thomas, C.W., Joosten, M.H.A.J., Golstein, C., Westerink, N., Hille, J., Nijkamp, H.J.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.
54. Tang, X.Y., Xie, M.T., Kim, Y.J., Zhou, J.M., Klessig, D.F. and Martin, G.B. (1999) Overexpression of Pto activates defence responses and confers broad resistance. Plant Cell, 11, 15-29.
55. Tao, Y., Yuan, F.H., Leister, R.T., Ausubel, F.M. and Katagiri, F. (2000) Mutational analysis of the Arabidopsis nucleotide binding site-leucine-rich repeat resistance gene RPS2. Plant Cell, 12, 2541-2554.
56. 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.
57. 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.
58. Tian, D., Traw, M.B., Chen, J.Q., Kreitman, M. and Bergelson, J. (2003) Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature, 423, 74-77.
59. 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) Isolation and characterization of two putative pathogenicity genes of Cladosporium fulvum. Mol. Plant Microbe Interact. 6, 210-215.
60. 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.
61. 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 analysis of Avr9/Cf-9 and Avr4/Cf-4 induced necrosis. Mol. Plant Microbe Interact. 13, 439-446.
62. 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. (2001a) Intragenic recombination generated two distinct Cf genes that mediate AVR9 recognition in the natural population of Lycopersicon pimpinellifolium. Proc. Natl Acad. Sci. USA, 98, 10493-10498.
63. Van der Hoorn, R.A.L., Roth, R. and De Wit, P.J.G.M. (2001b) 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.
64. Van der Hoorn, R.A.L., Joosten, M.H.A.J. and De Wit, P.J.G.M. (2002) Balancing selection favors guarding resistance proteins. Trends Plant Sci. 7, 67-71.
65. Van der Hoorn, R.A.L, Rivas, S., Wulff, B.B.H., Jones, J.D.G. and Joosten, M.H.AJ. (2003) Rapid migration in gel filtration of the Cf-4 and Cf-9 resistance proteins is an intrinsic property of Cf proteins and not because of their association with high-molecular-weight proteins. Plant J. 35, 305-315.
66. Warnock, S.J. (1988) A review of taxonomy and phylogeny of the genus Lycopersicon. Hortic. Sci. 23, 669-673.
67. Westerink, N., Roth, R., Van den Burg, H.A., De Wit, P.J.G.M. and Joosten, M.H.A.J. (2002) The AVR4 elicitor protein of Cladosporium fulvum binds to fungal components with high affinity. Mol. Plant Microbe Interact. 15, 1219-1227.
68. 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, 546-560.
69. Wulff, 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.
70. Wulff, B.B.H., Thomas, C.M., Parniske, M. and Jones, J.D.G. (2004) Genetic variation at the tomato Cf-4/Cf-9 locus induced by EMS mutagenesis and intralocus recombination. Genetics, 167, 459-470.