Resistance of tomato and pepper to T3 strains of Xanthomonas campestris pv. vesicatoria is specified by a plant-inducible avirulence gene

Molecular Plant-Microbe Interactions

Volumn 13, Issue 9, 2000, Pages 911-921

  Astua Monge, Gustavo ^a   Minsavage, Gerald V ^a   Stall, Robert E ^a   Davis, Michael J ^b   Bonas, Ulla ^c   Jones, Jeffrey B ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

^c MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AVIRULENCE GENE; AVRXV3 GENE; CLONE; COSMID; DISEASE RESISTANCE; GENE FUSION; GENE LOCATION; GENETIC LINE; GENOME LIBRARY; OPEN READING FRAME; PEPPER; RACE; TRANSCRIPTION INITIATION;

AGROBACTERIUM TUMEFACIENS; EMBRYOPHYTA; LYCOPERSICON ESCULENTUM; XANTHOMONAS; XANTHOMONAS CAMPESTRIS; XANTHOMONAS CAMPESTRIS PV. VESICATORIA;

EID: 0033841684     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI.2000.13.9.911     Document Type: Article

References (58)

1. Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D. J. 1997. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
2. Ausubel, F. M., Brent, R., Kingston, R. E., Moore, D. D., Seidman, J. G., Smith, J. A., and Struhl, K., eds. 1992. Current Protocols in Molecular Biology. John Wiley & Sons, New York.
3. Bent, A. 1996. Function meets structure in the study of plant disease resistance genes. Plant Cell 8:1757-1771.
4. Bonas, U. 1994. hrp genes of phytopathogenic bacteria. Curr. Top. Microbiol. Immunol. 192:79-98.
5. Bonas, U., Schulte, R., Fenselau, S., Minsavage, G. V., Staskawicz, B. J., and Stall, R. E. 1991. Isolation of a gene cluster from Xanthomonas campestris pv. vesicatoria that determines pathogenicity and the hypersensitive response on pepper and tomato. Mol. Plant-Microbe Interact. 4:81-88.
6. Bonas, U., Stall, R. E., and Staskawicz, B. J. 1989. Genetic and structural characterization of the avirulence gene avrBs3 from Xanthomonas campestris pv. vesicatoria. Mol. Gen. Genet. 218:127-136.
7. Bonas, U., and Van den Ackerveken, G. 1997. Recognition of bacterial avirulence proteins occurs inside the plant cell: A general phenomenon in resistance to bacterial diseases? Plant J. 12: 1-7.
8. Boyer, H. W., and Roulland-Dussoix, D. 1969. A complementation analysis of the restriction and modification of DNA in Escherichia coli. J. Mol. Biol. 41:459-472.
9. Ciesiolka, L. D., Hwin, T., Gearlds, J. D., Minsavage, G. V., Saenz, R., Bravo, M., Handley, V., Conover, S. M., Zhang, H., Caporgno, J., Phengrasamy, N. B., Toms, A. O., Stall, R. E., and Whalen, M. C. 1999. Regulation of expression of avirulence gene avrRxv and identification of a family of host interaction factors by sequence analysis of avrBsT. Mol. Plant-Microbe Interact. 12:35-44.
10. Crowe, J. S., Cooper, H. J., Smith, M. A., Sims, M.. J., Parker, D., and Gewert, D. 1991. Improved cloning efficiency of polymerase chain reaction (PCR) products after proteinase K digestion. Nucleic Acids Res. 19:184.
11. Daniels, M. J., Barber, C. E., Turner, P. C., Sawczyc, M. K., Byrde, R. J. W., and Fielding, A. H. 1984. Cloning of genes involved in pathogenicity of Xanthomonas campestris pv. campestris using the broad host range cosmid pLAFR1. EMBO J. 3:3323-3328.
12. de Feyter, R., and Gabriel, D. W. 1991. Use of cloned DNA methylase genes to increase the frequency of transfer of foreign genes into Xanthomonas campestris pv. malvacearum. S. Bacteriol. 173:6421-6427.
13. de Feyter, R., McFadden, H., and Dennis, L. 1998. Five avirulence genes from Xanthomonas campestris pv. malvacearum cause genotype-specific cell death when expressed transiently in cotton. Mol. Plant-Microbe Interact. 11:698-701.
14. Deblaere, R., Bytebier, B., De Greve, H., Deboeck, F., Schell, J., Van Montagu, M., and Leemans, J. 1985. Efficient octopine Ti plasmid-derived vectors for Agrobacterium-mediated gene transfer to plants. Nucleic Acids Res. 13:4777-4788.
15. Ditta, G., Stanfield, S., Corbin, D., and Helinski, D. 1980. Broad host range DNA cloning system for gram-negative bacteria: Construction of a gene bank of Rhitobium meliloti. Proc. Natl. Acad. Sci. USA 77: 7347-7351.
16. Duan, Y. P., Castañeda, A., Erdos, G., and Gabriel, D. W. 1999. Expression of a single, host-specific, bacterial pathogenicity gene in plant cells elicits division, enlargement, and cell death. Mol. Plant-Microbe Interact. 12: 556-560.
17. Fenselau, S., and Bonas, U. 1995. Sequence and expression analysis of the hrpB pathogenicity operon of Xanthomonas campestris pv. vesicatoria which encodes eight proteins with similarity to components of the Hrp, Ysc, Spa, and Fli secretion systems. Mol. Plant-Microbe Interact. 8:845-854.
18. Figurski, D., and Helinski, D. R. 1979. Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc. Natl. Acad. Sci. USA 76:1648-1652.
19. Flor, H. H. 1971. Current status of the gene-for-gene concept. Annu. Rev. Phytopathol. 9:275-296.
20. Golemis, E. A., and Brent, R. 1997. Searching for interacting proteins with the two-hybrid system III. Pages 43-72 in: The Yeast Two-Hybrid System. P. L. Bartel and S. Fields, eds. Oxford University Press, New York.
21. Goodrich, J. A., Cutler, G., and Tijian, R. 1996. Contacts in context: Promoter specificity and macromolecular interactions in transcription. Cell 84:825-830.
22. Gopalan, S., Bauer, D. W., Alfano, J. A., Loniello, A. O., He, S. Y., and Collmer, A. 1996. Expression of the Pseudomonas syringae avirulence protein AvrB in plant cells alleviates its dependence on the hypersensitive response and pathogenicity (Hrp) secretion system in eliciting genotype-specific hypersensitive cell death. Plant Cell 8: 1095-1105.
23. Hibberd, A. M., Stall, R. E., and Bassett, M. J. 1987. Different pheno-types associated with incompatible races and resistance genes in bacterial spot disease of pepper. Plant Dis. 71:1075-1078.
24. Hueck, C. J. 1998. Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol. Mol. Biol. Rev. 62:379-433.
25. Hyun-Han, J., Bauer, D. W., Fouts, D. E., and Collmer, A. 1998. A cloned Erwinia chrysanthemi Hrp (type III protein secretion system) functions in Escherichia coli to deliver Pseudomonas syringae Avr signals to plant cell and to secrete Avr proteins in culture. Proc. Natl. Acad. Sci. USA 95:10206-10211.
26. Jefferson, R. A. 1987. Assaying chimeric genes in plants: The GUS gene fusion system. Plant Mol. Biol. Rep. 5:387-405.
27. Jefferson, R. A., Kavanagh, T. A., and Bevan, M. W. 1987. GUS fusions: β-Glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6:3901-3907.
28. Jones, J. B., Stall, R. E., and Bouzar, H. 1998. Diversity among Xanthomonas pathogenic on pepper and tomato. Annu. Rev. Phytopathol. 36: 41-58.
29. Jones, J. B., Stall, R. E., Scott, J. W., Somodi, G. C., Bouzar, H., and Hodge, N. C. 1995. A third tomato race of Xanthomonas campestris pv. vesicatoria. Plant Dis. 79:395-398.
30. Kapila, J., De Rycke, R., Van Montagu, M., and Angenon, G. 1997. An Agrobacterium-medizled transient gene expression system for intact leaves. Plant Sci. 122:101-108.
31. Kearney, B., and Staskawicz, B. J. 1990. Widespread distribution and fitness contribution of Xanthomonas campestris avirulence gene avrBs2. Nature 346:541-543.
32. Leach, J. E., and White, F. F. 1996. Bacterial avirulence genes. Annu. Rev. Phytopathol. 34: 153-179.
33. Leister, R. T., Ausubel, F. M., and Katagiri, F. 1996. Molecular recognition of pathogen attack occurs inside the plant cells in plant disease resistance specified by the Arabidopsis gene RPS2 and RPM1. Proc. Natl. Acad. Sci. USA 93:15497-15502.
34. Maniatis, T. A., Fritsch, E. F., and Sambrook, J. 1982. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
35. Minsavage, G. V., Dahlbeck, D., Whalen, M. C., Kearney, B., Bonas, U., Staskawicz, B. J., and Stall, R. E. 1990. Gene-for-gene relationships specifying disease resistance in Xanthomonas campestris pv. vesicatoria - pepper interactions. Mol. Plant-Microbe Interact. 3:41-47.
36. Minsavage, G. V., Jones, J. B., and Stall, R. E. 1996. Cloning and sequencing of an avirulence gene (avrRxv3) isolated from Xanthomonas campestris pv. vesicatoria tomato race 3. Phytopathology 86:S15 (Abstr.)
37. Parker, J. E., and Coleman, J. M. 1997. Molecular intimacy between proteins specifying plant-pathogen recognition. TIBS 22:291-296.
38. Polson, A., Coetzer, T., Krager, J., von Maltzahn, E., and van der Merwe, K. J. 1985. Improvements in the isolation of IgY from the yolks of eggs laid by immunized hens. Immun. Invest. 14:323-327.
39. Ptashne, M., and Gann, A. 1997. Transcriptional activation by recruitment. Nature 386:569-577.
40. Rossier, O., Wengelnik, K., Hahn, K., and Bonas, U. 1999. The Xanthomonas Hrp type III system secretes proteins from plant and mammalian bacterial pathogens. Proc. Natl. Acad. Sci. USA 96:9368-9373.
41. Schulte, R., and Bonas, U. 1992. Expression of the Xanthomonas campestris pv. vesicatoria hrp gene cluster, which determines pathogenicity and hypersensitivity on pepper and tomato, is plant inducible. J. Bacteriol. 174:815-823.
42. Scofield, S. R., Tobias, C. M., Rathjen, J. P., Chang, J. H., Lavelle, D. T., Michelmore, R. W., and Staskawicz, B. J. 1996. Molecular basis of gene-for-gene specificity in bacterial speck disease of tomato. Science 274:2063-2065.
43. Scott, J. W., Jones, J. B., and Somodi, G. C. 1995. Screening tomato accessions for resistance to Xanthomonas campestris pv. vesicatoria, race T3. HortScience 30:579-581.
44. Shaw, G. 1995. Protein sequence interpretation using a spreadsheet program. BioTechniques 19:978-983.
45. Smith, D. E., and Fisher, P. A. 1984. Identification, developmental regulation, and response to heat shock of two antigenically related forms of a major nuclear envelope protein in Drosophila embryos: Application of an improved method for affinity purification of antibodies using polypeptides immobilized on nitrocellulose blots. J. Cell Biol. 99:20-28.
46. Stachel, S. E., An, G., Flores, C., and Nester, E. W. 1985. A Tn3 lacZ transposon for the random generation of β-galactosidase gene fusions: Application to the analysis of gene expression in Agrobacterium. EMBO J. 4:891-898.
47. Stall, R. E. 1995. Xanthomonas campestris pv. vesicatoria. Pages 167-181 in: Pathogenesis and Host Specificity in Plant Diseases: Histopathological, Biochemical, Genetic and Molecular Bases. U. S. Singh, R. P. Singh, and K. Kohmoto, eds. Elsevier Science, New York.
48. Staskawicz, B. J., Dahlbeck, D., Keen, N., and Napoli, C. 1987. Molecular characterization of cloned avirulence genes from race 0 and race 1 of Pseudomonas syringae pv. glycinea. J. Bacteriol. 169:5789-5794.
49. Swords, K. M. M., Dahlbeck, D., Kearney, B., Roy, M., and Staskawicz, B. J. 1996. Spontaneous and induced mutations in a single open reading frame alter both virulence and avirulence in Xanthomonas campestris pv. vesicatoria avrBs2. J. Bacteriol. 178: 4661-4669.
50. Tang, X., Frederick, R. D., Zhou, J., Halterman, D. A., Jia, Y., and Martin, G. B. 1996. Initiation of plant disease resistance by physical interaction of AvrPto and Pto kinase. Science 274:2060-2063.
51. Van den Ackerveken, G., Morois, E., and Bonas, U. 1996. Recognition of the bacterial avirulence protein AvrBs3 occurs inside the host plant cell. Cell 87:1307-1316.
52. Wengelnik, K., and Bonas, U. 1996. HrpXv, an AraC-type regulator, activates expression of five out of six loci in the hrp cluster of Xanthomonas campestris pv. vesicatoria. J. Bacteriol. 178:3462-3469.
53. Wengelnik, K., Marie, C., Russel, M., and Bonas, U. 1996a. Expression and localization of HrpA1, a protein of Xanthomonas campestris pv. vesicatoria essential for pathogenicity and induction of the hypersensitive reaction. J. Bacteriol. 178:1061-1069.
54. Wengelnik, K., Rossier, O., and Bonas, U. 1999. Mutations in the regulatory gene hrpG of Xanthomonas campestris pv. vesicatoria result in constitutive expression of all hrp genes. J. Bacteriol. 181:6828-6831.
55. Wengelnik, K., Van den Ackerveken, G., and Bonas, U. 1996b. HrpG, a key hrp regulatory protein of Xanthomonas campestris pv. vesicatoria is homologous to two-component response regulators. Mol. Plant-Microbe Interact. 9:704-712.
56. Whalen, M. C., Wang, J. F., Garland, F. M., Heiskell, M. E., Dahlbeck, D., Minsavage, G. V., Jones, J. B., Scott, J. W., Stall, R. E., and Staskawicz, B. J. 1993. Avirulence gene avrRxv from Xanthomonas campestris pv. vesicatoria specifies resistance on tomato line Hawaii 7998. Mol. Plant-Microbe Interact. 6:616-627.
57. Young, S. A., White, F. F., Hopkins, C. M., and Leach J. E. 1994. AVRXa10 protein is in the cytoplasm of Xanthomonas oryzae pv. oryzae. Mol. Plant-Microbe Interact. 7: 799-804.
58. Zhu, W., Yang, B., Chittoor, J. M., Johnson, L. B., and White, F. F. 1998. AvrXa10 contains an acidic transcriptional activation domain in the functionally conserved C terminus. Mol. Plant-Microbe Interact. 11: 824-832.