Spontaneous and induced mutations in a single open reading frame alter both virulence and avirulence in Xanthomonas campestris pv. vesicatoria avrBs2

Journal of Bacteriology

Volumn 178, Issue 15, 1996, Pages 4661-4669

  Swords, Kathy M M ^a,b   Dahlbeck, Douglas ^a   Kearney, Brian ^a   Roy, Margaret ^a   Staskawicz, Brian J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b MONSANTO COMPANY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACTERIAL GENE; BACTERIAL MUTATION; BACTERIAL VIRULENCE; CONTROLLED STUDY; ESCHERICHIA COLI; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; RHIZOBIUM RADIOBACTER; XANTHOMONAS;

AGROBACTERIUM TUMEFACIENS; BACTERIA (MICROORGANISMS); BRASSICA; ESCHERICHIA COLI; XANTHOMONAS; XANTHOMONAS CAMPESTRIS PV. CAMPESTRIS; XANTHOMONAS CAMPESTRIS PV. VESICATORIA;

EID: 0029743977     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/jb.178.15.4661-4669.1996     Document Type: Article

References (64)

1. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
2. Amemura, A., and J. Cabrera-Crespo. 1986. Extracellular oligosaccharides and low-Mr polysaccharides containing (1→2)-β-D-glucosidic linkages from strains of Xanthomonas, Escherichia coli and Klebsiella pneumoniae. J. Gen. Microbiol. 132:2443-2452.
3. Batley, M., J. W. Redmond, S. P. Djordjevic, and B. G. Rolfe. 1987. Characterization of glycerophophorylated cyclic β-(1,2)-glucans from a fast-growing Rhizobium species. Biochim. Biophys. Acta 901:119-125.
4. Bonas, U. 1994. hrp gene of phytopathogenic bacteria, p. 79-98. In J. L. Dangl (ed.), Bacterial pathogenesis of plants and animals: molecular and cellular mechanisms, vol. 192. Springer-Verlag, Heidelberg.
5. Bonas, U., R. E. Stall, and B. Staskawicz. 1989. Genetic and structural characterization of the avirulence gene avrBs3 from Xanthomonas campestris pv. vesicatoria. Mol. Gen. Genet. 218:127-136.
6. Breedveld, M. W., and K. J. Miller. 1994. Cyclic β-glucans of members of the family Rhizobiaceae. Microbiol. Rev. 58:145-161.
7. Brzoska, P., and W. Boos. 1989. The ugp-encoded glyerophosphoryldiester phosphodiesterase, a transport-related enzyme of Escherichia coli. FEMS Microbiol. Rev. 63:115-124.
8. Cangelosi, G. A., G. Martinetti, and E. W. Nester. 1990. Osmosensitivity phenotypes of Agrobacterium tumefaciens mutants that lack periplasmic β-1,2-glucans. J. Bacteriol. 172:2172-2174.
9. Cook, A. A., and R. E. Stall. 1963. Differentiation of pathotypes among isolates of Xanthomonas vesicatoria. Plant Dis. Rep. 53:617-619.
10. Dahlbeck, D., and R. E. Stall. 1979. Mutations for change of race in cultures of Xanthomonas vesicatoria. Phytopathogy 69:634-636.
11. 10a. Dahlbeck, D., and B.-J. Staskawicz. Unpublished observations.
12. Dangl, J. L. 1994. The enigmatic avirulence genes of phytopathogenic bacteria, p. 99-118. In J. L. Dangl (ed.), Bacterial pathogenesis of plants and animals: molecular and cellular mechanisms, vol. 192. Springer-Verlag, Heidelberg.
13. Daniels, M. J., C. E. Barber, P. C. Turner, W. G. Cleary, and M. K. Sawczyc. 1984. Isolation of mutants of Xanthomonas campestris pv. campestris showing altered pathogenicity. J. Gen. Microbiol. 130:2447-2455.
14. Ditta, G., S. Stanfield, D. Corbin, and D. R. Helinski. 1980. Broad host range DNA cloning system for Gram-negative bacteria: construction of a gene bank of Rhizobium meliloti. Proc. Natl. Acad. Sci. USA 77:7347-7351.
15. Dylan, T., D. R. Helinski, and G. S. Ditta. 1990. Hypoosmotic adaptation in Rhizobium meliloti requires β-(1→2)-glucan. J. Bacteriol. 172:1400-1408.
16. Fenselau, S., I. Balbo, and U. Bonas. 1992. Determinants of pathogcnicity in Xanthomonas campestris pv. vesicatoria are related to proteins involved in secretion in bacterial pathogens of animals. Mol. Plant-Microbe Interact. 5:390-396.
17. Fenselau, S., and U. Bonas. 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 D. R. Helinski. 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. Foster, P. L., and J. M. Trimarchi. 1994. Adaptive reversion of a frameshift mutation in Escherichia coli by simple base deletions in homopolymeric runs. Science 265:407-409.
20. Geiger, O., A. C. Weissborn, and E. P. Kennedy. 1991. Biosynthesis and excretion of cyclic glucans by Rhizobium meliloti 1021. J. Bacteriol. 173:3021-3024.
21. Gough, C. L., S. Genin, C. Zisihek, and C. Boucher. 1992. hrp genes of Pseudomonas solanacearum are homologous to pathogenicity determinants of animal pathogenic bacteria and are conserved among plant pathogenic bacteria. Mol. Plant-Microbe Interact. 5:384-389.
22. Hibberd, A. M., M. J. Bassett, and R. E. Stall. 1987. Allelism tests of three dominant genes for hypersensitive resistance to bacterial spot of pepper. Phytopathology 77:1304-1307.
23. 21a. Hibberd, A. M., and R. E. Stall. Personal cummunication.
24. Huynh, T. V., D. Dahlbeck, and B. J. Staskawicz. 1989. Bacterial blight of soybean: regulation of a pathogen gene determining host cultivar specificity. Science 245:1374-1377.
25. Innes, R. I., A. F. Bent, B. N. Kunkel, S. R. Bisgrove, and B. J. Staskawicz. 1993. Molecular analysis of avirulence gene avrRpt2 and identification of a putative regulatory sequence common to all known Pseudomonas syringae avirulence genes. J. Bacteriol. 175:4859-4869.
26. Innes, R. I., M. A. Hirose, and P. L. Kuempel. 1988. Induction of nitrogenfixing nodules on clover requires only 32 kilobase pairs of DNA from the Rhizobium trifolii symbiosis plasmid. J. Bacteriol. 170:3793-3802.
27. Kearney, B. 1989. Ph.D. thesis. University of California, Berkeley.
28. Kearney, B., P. C. Ronald, D. Dahlbeck, and B. J. Staskawicz. 1988. Molecular basis for evasion of plant host defense in bacterial spot of pepper. Nature (London) 332:541-543.
29. Kearney, B., and B. J. Staskawicz. 1990. Widespread distribution and fitness contribution of Xanthomonas campestris avirulence gene avrBs2. Nature (London) 346:385-386.
30. Kearney, B., and B. J. Staskawicz. 1990. Characterization of 1S476 and its role in bacterial spot disease of tomato and pepper. J. Bacteriol. 172:143-148.
31. Keen, N. T. 1990. Gene-for-gene complementarity in plant-pathogen interactions. Annu. Rev. Genet. 24:447-463.
32. Kousik, C. S., and D. F. Ritchie. 1995. Isolation of pepper races 4 and 5 of Xanthomonas campestris pv. vesicatoria from diseased peppers in southeastern U.S. fields. Plant Dis. 79:540.
33. Kyte, J., and R. F. Doolittle. 1982. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157:105-132.
34. Levinson, G., and G. A. Gutman. 1987. High frequencies of short framcshifts in poly-CA/TG tandem repeats borne by hacteriophage M13 in Escherichia coli K-12. Nucleic Acids Res. 15:5323-5338.
35. Lorang, J. M., H. Shen, D. Kobayashi, D. Cooksey, and N. T. Keen. 1994. avrA and avrE in Pseudomonas syringae pv. tomato PT23 play a role in virulence on tomato plants. Mol. Plant-Microbe Interact. 7:508-515.
36. Loubers, I., L. Debarbieux, A. Bnin, J.-M. Lacroix, and J.-P. Bohin. 1993. Homology between a genetic locus (mdoA) involved in the osmoregulated biosynthesis of neriplasmic glucans in Escherichia coli and a genetic locus (hrpM) controlling pathogenicity of Pseudomonas syringae. Mol. Microbiol. 10:329-340.
37. Midland, S. L., N. T. Keen, J. J. Sims, M. M. Midland, M. M. Stayton, V. Burton, K. J. Graham, and J. Clardy. 1993. The structures of syringolides 1 and 2, novel C-glycosidic elicitors from Pseudomonas syringae pv. tomato. J. Org. Chem. 58:2940-2945.
38. Miller, K. J., R. S. Gore, and A. J. Benesi. 1988. Phosphoglycerol substituents present on the cyclic β-1,2-glucans of Rhizobium meliloti 1021 are derived from phosphatidylglycerol. J. Bacterol. 170:4569-4575.
39. Miller, K. J., J. A. Hadley, and D. L. Gustine. 1994. Cyclic (J-1,6-1,3-glucans of Bradyrhizobium japonicum USDA 110 elicit isoflavonoid production in the soybean (Glycine max) host. Plant Physiol. 104:917-923.
40. Miller, K. J., E. P. Kennedy, and V. N. Reinhold. 1986. Osmotic adaptation by gram-negative bacteria: possible role for periplasmic oligosaccharides. Science 231:48-51.
41. Minsavage, G. V., D. Dahlbeck, M. C. Whalen, B. Kearney, U. Bonas, B. J. Staskawicz, and R. E. Stall. 1990. Gene-for-gene relationships specifying disease resistance in Xanthomonas campestris pv. vesicatoria-peppet interactions. Mol. Plant-Microbe Interact. 3:41-47.
42. Murillo, J., H. Shen, D. Gerhold, A. Sharma, D. A. Cooksey, and N. T. Keen. 1994. Characterization of pPT23B, the plasmid involved in syringolide production by Pseudomonas syringae pv. tomato PT23. Plasmid 31:275-287.
43. Paulus, F., and L. Otten. 1993. Functional and mutated agrocinopine syn- thase genes on octopine T-DNAs. Mol. Plant-Microbe Interact. 6:393-402.
44. Ritter, C., and J. L. Dangl. 1995. The avrRpm1 gene of Pseudomonas syringae pv. maculicola is required for virulence on Arabidopsis. Mol. Plant-Microbe Interact. 8:444-453.
45. Ryder, M. H., M. E. Tate, and G. P. Jones. 1984. Agrocinopine A, a tumor-inducing plasmid-coded enzyme product, is a phosphodiester of sucrose and L-arabinose. J. Biol. Chem. 259:9704-9710.
46. Sahin, F., and S. A. Miller. 1995. First report of pepper race 6 of Xanthomonas campestris pv. vesicatoria, causal agent of bacterial spot of pepper. Plant Dis. 79:1188.
47. Salmeron, J. M., and B. J. Staskawicz. 1993. Molecular characterization and hrp dependence of the avirulence gene avrPto from Pseudamonas syringae pv. tomato. Mol. Gen. Genet. 239:6-16.
48. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual. 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
49. Shen, H., and N. T. Keen. 1993. Characterization of the promoter of avirulence gene D from Pseudamonas syringae pv. tomato, J. Bacteriol. 175:5916-5924.
50. Shine, J., and L. Dalgarno. 1974. The 3′-terminal sequence of Escherichia coli 16S ribosomal RNA: complementary to nonsense triplets and ribosome binding sites. Proc. Natl. Acad. Sci. USA 71:1342-1346.
51. Smith, M. J., E. P. Mazzola, J. J. Sims, S. L. Midland, N. T. Keen, V. Burton, and M. M. Stayton. 1993. The syringolides: bacterial C-glycosyl lipids that trigger plant disease resistance. Tetrahedron Lett. 34:223-226.
52. Smith, T. F., and M. S. Waterman. 1981. Comparison of bio-sequences. Adv. Appl. Math. 2:482-489.
53. 50a. Stall, R. E. Personal communication.
54. Slaskawicz, B., D. Dahlbeck, N. Keen, and C. Napoli. 1987. Molecular characterization of cloned avirulence genes from race 0 and race 1 of Pseudomonas syringae pv. glycinea. J. Bacteriol. 169:5789-5794.
55. Staskawicz, B. J., F. M. Ausubel, B. J. Baker, J. G. Ellis, and J. D. G. Jones. 1995. Molecular genetics of plant disease resistance. Science 268:661-667.
56. Strand, M., T. A. Prolla, R. M. Liskay, and T. D. Petes. 1993. Destabilization of tracts of simple repetitive DNA in yeast by mutations affecting DNA mismatch repair. Nature (London) 365:274-276.
57. Swanson, J., B. Kearney, D. Dahlbeck, and B. Staskawicz. 1988. Cloned avirulence gene of Xanthomonas campestris pv. vesicatoria complements spontaneous race change mutants. Mol. Plant-Microbe Interact. 1:5-9.
58. 54a. Swords, K. M. M., and B. J. Staskawicz. Unpublished observations.
59. Taylor, J. W., J. Ott, and F. Eckstein. 1985. The rapid generation of oligonucleotide-directed mutations at high frequency using phosphorothiodatemodified DNA. Nucleic Acids Res. 13:8764-8785.
60. Tommassen, J., K. Eiglmeier, S. T. Cole, P. Overduin, T. J. Larson, and W. Boos. 1991. Characterization of two genes, glpQ and ngpQ, encoding glyccrophosphoryl diester phosphodiesterases of Escherichia coli. Mol. Gen. Genet. 226:321-327.
61. Vieira, J., and J. Messing. 1987. Production of single-stranded plasmids. Methods Enzymol. 153:3-11.
62. Whalen, M. C., J. F. Wang, F. M. Garland, M. E. Heiskell, D. Dahlbeck, G. V. Minsavage, J. B. Jones, J. W. Scotl, and B. J. Staskawicz. 1993. Avirulence gene avrRxv from Xanthomonas campestris pv. resicatoria specifies resistance on tomato line Hawaii 7998. Mol. Plant-Microbe Interact. 6:616-627.
63. Xiao, Y. X., Y. Lu, S. G. Heu, and S. W. Hutcheson. 1992. Organization and environmental regulation of the Pseudomonas syringae pv. syringae 61 hrp cluster. J. Bacteriol. 174:1734-1741.
64. Yang, Y., R. De Feyter, and D. W. Gabriel. 1994. Host-specific symptoms and increased release of Xanthomonas citri and X. campestris pv. malvacearum from leaves arc determined by the 102-bp tandem repeats of pthA and avrb6, respectively. Mol. Plant-Microbe Interact. 7:345-355.