Inhibition of resistance gene-mediated defense in rice by Xanthomonas oryzae pv. oryzicola

Molecular Plant-Microbe Interactions

Volumn 19, Issue 3, 2006, Pages 240-249

  Makino, Seiko ^a   Sugio, Akiko ^b   White, Frank ^b   Bogdanove, Adam J ^a  

^a IOWA STATE UNIVERSITY   (United States)

^b KANSAS STATE UNIVERSITY   (United States)

Author keywords

Phytopathogenic bacteria

Indexed keywords

BACTERIAL PROTEIN; RECOMBINANT PROTEIN;

ARTICLE; GENE EXPRESSION REGULATION; GENETICS; HISTOLOGY; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PEPPER; PLANT DISEASE; PLANT LEAF; RICE; VIRULENCE; XANTHOMONAS;

BACTERIAL PROTEINS; CAPSICUM; GENE EXPRESSION REGULATION, BACTERIAL; GENE EXPRESSION REGULATION, PLANT; ORYZA SATIVA; PLANT DISEASES; PLANT LEAVES; RECOMBINANT PROTEINS; VIRULENCE; XANTHOMONAS;

BACTERIA (MICROORGANISMS); XANTHOMONAS; XANTHOMONAS ORYZAE PV. ORYZAE; XANTHOMONAS ORYZAE PV. ORYZICOLA;

EID: 33144474076     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-19-0240     Document Type: Article

References (62)

1. Abramovitch, R. B., and Martin, G. B. 2004. Strategies used by bacterial pathogens to suppress plant defenses. Curr. Opin. Plant Biol. 7:356-364.
2. Abramovitch, R. B., and Martin, G. B. 2005. AvrPtoB: A bacterial type III effector that both elicits and suppresses programmed cell death associated with plant immunity. FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Lett. 245:1-8.
3. Alfano, J. R., and Collmer, A. 2004. Type III secretion system effector proteins: Double agents in bacterial disease and plant defense. Annu. Rev. Phytopathol. 42:385-414.
4. Bai, J., Choi, S.-H., Ponciano, G., Leung, H., and Leach, J. E. 2000. Xanthomonas oryzae pv. oryzae avirulence genes contribute differently and specifically to pathogen aggressiveness. Mol. Plant-Microbe Interact. 13:1322-1329.
5. Ballvora, A., Pierre, M., van den Ackerveken, G., Schornack, S., Rossier, O., Ganal, M., Lahaye, T., and Bonas, U. 2001. Genetic mapping and functional analysis of the tomato Bs4 locus governing recognition of the Xanthomonas campestris pv. vesicatoria AvrBs4 protein. Mol. Plant-Microbe Interact. 14:629-638.
6. Bogdanove, A. J., Beer, S. V., Bonas, U., Boucher, C., Collmer, A., Coplin, D. L., Cornelis, G. R., Huang, H.-C., Hutchenson, S. W., Panopoulos, N. J., and Van Gijsegem, F. 1996. Unified nomenclature for broadly conserved hrp genes of phytopathogenic bacteria. Mol. Microbiol. 20:681-683.
7. Bonas, U., Stall, R. E., and Staskawicz, B. 1989. Genetic and structural characterization of the avirulence gene avrBs3 from Xanthomonas campestris pv. vesicatoria. Mol. Gen. Genet. 218:127-136.
8. Bowen, B., Steinberg, J., Laemmli, U. K., and Weintraub, H. 1980. The detection of DNA-binding proteins by protein blotting. Nucleic Acids Res. 8:1-20.
9. Brizzard, B. L., Chubet, R. G., and Vizard, D. L. 1994. Immunoaffinity purification of FLAG epitope-tagged bacterial alkaline phosphatase using a novel monoclonal antibody and peptide elution. BioTechniques 16:730-735.
10. Brunings, A. M., and Gabriel, D. W. 2003. Xanthomonas citri: Breaking the surface. Mol. Plant Pathol. 4:141-157.
11. Buttner, D., and Bonas, U. 2002. Getting across - Bacterial type III effector proteins on their way to the plant cell. EMBO (Eur. Mol. Biol. Organ.) J. 21:5313-5322.
12. Buttner, D., Gurlebeck, D., Noel, L. D., and Bonas, U. 2004. HpaB from Xanthomonas campestris pv. vesicatoria acts as an exit control protein in type III-dependent protein secretion. Mol. Microbiol. 54:755-768.
13. Casper-Lindley, C., Dahlbeck, D., Clark, E. T., and Staskawicz, B. J. 2002. Direct biochemical evidence for type III secretion-dependent translocation of the AvrBs2 effector protein into plant cells. Proc. Natl. Acad. Sci. U.S.A. 99:8336-8341.
14. Chang, J. H., Goel, A. K., Grant, S. R., and Dangl, J. L. 2004. Wake of the flood: Ascribing functions to the wave of type III effector proteins of phytopathogenic bacteria. Curr. Opin. Microbiol. 7:11-18.
15. Choi, S. H., and Leach, J. E. 1994. Genetic manipulation of Xanthomonas oryzae pv. oryzae. Int. Rice Res. Notes 19:31-32.
16. Cornelis, G. R., and Van Gijsegem, F. 2000. Assembly and function of type III secretory systems. Annu. Rev. Microbiol. 54:735-774.
17. Das, S. R. 1977. Assessment of rice varieties for resistance to bacterial leaf streak disease caused by Xanthomonas translucens f. sp. oryzicola. Sci. Cult. 43:93.
18. DebRoy, S., Thilmony, R., Kwack, Y.-B., Nomura, K., and He, S.-Y. 2004. A family of conserved bacterial effectors inhibits salicylic acid-mediated basal immunity and promotes disease necrosis in plants. Proc. Natl. Acad. Sci. U.S.A. 101:9927-9932.
19. Flor, H. H. 1971. Current status of the gene-for-gene concept. Annu. Rev. Phytopathol. 9:275-296.
20. Greenberg, J. T., and Yao, N. 2004. The role and regulation of programmed cell death in plant-pathogen interactions. Cell. Microbiol. 6:201-211.
21. Gu, K., Yang, B., Tian, D., Wu, L., Wang, D., Sreekala, C., Yang, F., Chu, Z., Wang, G.-L., White, F. F., and Yin, Z. 2005. R gene expression induced by a type-III effector triggers disease resistance in rice. Nature 435:1122-1125.
22. Hammond-Kosack, K. E., and Jones, J. D. G. 1996. Resistance gene-dependent plant defense responses. Plant Cell 8:1773-1791.
23. Herbers, K., Conrads-Strauch, J., and Bonas, U. 1992. Race-specificity of plant resistance to bacterial spot disease determined by repetitive motifs in a bacterial avirulence protein. Nature 356:172-174.
24. Hopkins, C. M., White, F. F., Choi, S. H., Guo, A., and Leach, J. E. 1992. Identification of a family of avirulence genes from Xanthomonas oryzae pv. oryzae. Mol. Plant-Microbe Interact. 5:451-459.
25. Hueck, C. J. 1998. Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol. Mol. Biol. Rev. 62:379-433.
26. Innes, R. W., Hirose, M. A., and Kuempel, P. L. 1988. Induction of nitrogen-fixing nodules on clover requires only 32 kilobase pairs of DNA from the Rhizobium trifolii symbiosis plasmid. J. Bacteriol. 170:3793-3802.
27. Keen, N. T. 1990. Gene-for-gene complementarity in plant-pathogen interactions. Annu. Rev. Genet. 24:447-463.
28. Kim, H.-S., Desveaux, D., Singer, A. U., Patel, P., Sondek, J., and Dangl, J. L. 2005. The Pseudomonas syringae effector AvrRpt2 cleaves its C-terminally acylated target, RIN4, from Arabidopsis membranes to block RPM1 activation. Proc. Natl. Acad. Sci. U.S.A. 102:6496-6501.
29. Klement, Z. 1982. Hypersensitivity. Pages 149-177 in: Phytopathogenic Prokaryotes. M. S. Mount and G. S. Lacy, eds. Academic Press, New York.
30. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
31. Lee, K. S., Rasabandith, S., Angeles, E. R., and Khush, G. S. 2003. Inheritance of resistance to bacterial blight in 21 cultivars of rice. Phytopathology 93:147-152.
32. 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.
33. Metz, M., Dahlbeck, D., Morales, C. Q., Sady, B. A., Clark, E.T., and Staskawicz, B. J. 2005. The conserved Xanthomonas campestris pv. vesicatoria effector protein XopX is a virulence factor and suppresses host defense in Nicotiana benthamiana. Plant J. 41:801-814.
34. Mew, T. W. 1993. Xanthomonas oryzae pathovars on rice: Cause of bacterial blight and bacterial leaf streak. Pages 30-40 in: Xanthomonas. J. G. Swings and E. L. Civerolo, eds. Chapman and Hall, New York.
35. Mew, T. W., Alvarez, A. M., Leach, J. E., and Swings, J. 1993. Focus on bacterial blight of rice. Plant Dis. 77:5-12.
36. Miao, E. A., Scherer, C. A., Tsolis, R. M., Kingsley, R. A., Adams, L. G., Baumler, A. J., and Miller, S. I. 1999. Salmonella typhimurium leucine-rich repeat proteins are targeted to the SPI1 and SPI2 type III secretion systems. Mol. Microbiol. 34:850-864.
37. Mudgett, M. B., Chesnokova, O., Dahlbeck, D., Clark, E. T., Rossier, O., Bonas, U., and Staskawicz, B. J. 2000. Molecular signals required for type III secretion and translocation of the Xanthomonas campestris AvrBs2 protein to pepper plants. Proc. Natl. Acad. Sci. U.S.A. 97:13324-13329.
38. Noda, T., Yamamoto, T., Kaku, H., and Horino, O. 1996. Geographical distribution of pathogenic races of Xanthomonas oryzae pv. oryzae in Japan in 1991 and 1993. Ann. Phytopathol. Soc. Japan 62:549-553.
39. Ou, S. H. 1985. Rice Diseases. Commonwealth Agricultural Bureau, Kew, Surrey.
40. Rao, Y. P., Shekhawat, G. S., Mohan, S. K., and Reddy, P. R. 1972. Evaluation of rice varieties for resistance to bacterial leaf-streak (Xanthomonas translucens). Ind. J. Agr. Sci. 42:502-505.
41. Sambrook, J., Fritsch, E. F., and Maniatis, T. E. 1989. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. U.S.A.
42. Schaad, N. W., Wang, Z. K., Di, M., McBeath, J., Peterson, G. L., and Bonde, M. R. 1996. An improved infiltration technique to test the pathogenicity of Xanthomonas oryzae pv. oryzae in rice seedlings. Seed Sci. Technol. 24:449-456.
43. Soby, S. D., and Daniels, M. J. 1996. Catabolite-repressor-like protein regulates the expression of a gene under the control of the Escherichia coli lac promoter in the plant pathogen Xanthomonas campestris pv. campestris. Appl. Microbiol. Biotechnol. 46:559-561.
44. Sory, M. P., and Cornelis, G. R. 1994. Translocation of a hybrid YopE-adenylate cyclase from Yersinia enterocolitica into HeLa cells. Mol. Microbiol. 14:583-594.
45. Swarup, S., De Feyter, R., Brlansky, R. H., and Gabriel, D. N. 1991. A pathogenicity locus from Xanthomonas citri enables strains from several pathovars of Xanthomonas campestris to elicit canker-like lesions on citrus. Phytopathology 81:802-808.
46. Swings, J., Van Den Mooter, M., Vauterin, L., Hoste, B., Gillis, M., Mew, T. W., and Kersters, K. 1990. Reclassification of the causal agents of bacterial blight (Xanthomonas campestris pathovar oryzae) and bacterial leaf streak (Xanthomonas campestris pathovar oryzicola) of rice as pathovars of Xanthomonas oryzae new species (ex Ishiyama 1922) sp. nov., nom. rev. Int. J. Syst. Bacteriol. 40:309-311.
47. Szurek, B., Marois, E., Bonas, U., and van den Ackerveken, G. 2001. Eukaryotic features of the Xanthomonas type III effector AvrBs3: Protein domains involved in transcriptional activation and the interaction with nuclear import receptors from pepper. Plant J. 26:523-534.
48. Szurek, B., Rossier, O., Hause, G., and Bonas, U. 2002. Type III-dependent translocation of the Xanthomonas AvrBs3 protein into the plant cell. Mol. Microbiol. 46:13-23.
49. Tang, D., Wu, W., Li, W., Lu, H., and Worland, A. J. 2000. Mapping of QTLs conferring resistance to bacterial leaf streak in rice. Theor. Appl. Genet. 101:286-291.
50. Tsuge, S., Furutani, A., Fukunaka, R., Kubo, Y., and Horino, O. 2001. Growth complementation of hrpXo mutants of Xanthomonas oryzae pv. oryzae by virulent strains in rice cultivars resistant and susceptible to the parental strain. J. Gen. Plant Pathol. 67:51-57.
51. Van Der Bij, A. J., De Weger, L. A., Tucker, W. T., and Lugtenberg, B. J. J. 1996. Plasmid stability in Pseudomonas fluorescens in the rhizosphere. Appl. Environ. Microbiol. 62:1076-1080.
52. Vidaver, A. K. 1967. Synthetic and complex media for the rapid detection of fluorescence of phytopathogenic pseudomonads: Effect of the carbon source. Appl. Microbiol. 15:1523-1524.
53. Wright, C. A., and Beattie, G. A. 2004. Pseudomonas syringae pv. tomato cells encounter inhibitory levels of water stress during the hypersensitive response of Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 101:3269-3274.
54. Yang, B., and White, F. F. 2004. Diverse members of the AvrBs3/PthA family of type III effectors are major virulence determinants in bacterial blight disease of rice. Mol. Plant-Microbe Interact. 17:1192-1200.
55. Yang, B., Zhu, W., Johnson, L. B., and White, F. F. 2000. The virulence factor AvrXa7 of Xanthomonas oryzae pv. oryzae is a type III secretion pathway-dependent nuclear-localized double-stranded DNA-binding protein. Proc. Natl. Acad. Sci. U.S.A. 97:9807-9812.
56. Yang, B., Sugio, A., and White, F. F. 2005. Avoidance of host recognition by alterations in the repetitive and C-terminal regions of AvrXa7, a type III effector of Xanthomonas oryzae pv. oryzae. Mol. Plant-Microbe Interact. 18:142-149.
57. Yang, Z., Sun, X., Wang, S., and Zhang, Q. 2003. Genetic and physical mapping of a new gene for bacterial blight resistance in rice. Theor. Appl. Genet. 106:1467-1472.
58. Zhao, B., Ardales, E. Y., Raymundo, A., Bai, J., Trick, H. N., Leach, J. E., and Hulbert, S. H. 2004. The avrRxo1 gene from the rice pathogen Xanthamonas oryzae pv. oryzicola confers a nonhost defense reaction on maize with resistance gene Rxo1. Mol. Plant-Microbe Interact. 17:771-779.
59. Zhao, B., Lin, X., Poland, J., Trick, H., Leach, J., and Hulbert, S. 2005. A maize resistance gene functions against bacterial streak disease in rice. Proc. Natl. Acad. Sci. U.S.A. 102:15383-15388.
60. 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.
61. Zhu, W., Yang, B., Wills, N., Johnson, L. B., White, F. F., Zhu, W. G., and Yang, B. 1999. The C-terminus of AvrXa10 can be replaced by the transcriptional activation domain of VP16 from the herpes simplex virus. Plant Cell 11:1665-1674.
62. Zhu, W., MaGbanua, M. M., and White, F. F. 2000. Identification of two novel Arp-associated genes in the hrp gene cluster of Xanthomonas oryzae pv. oryzae. J. Bacteriol. 182:1844-1853.