Mutagenesis of 18 type III effectors reveals virulence function of XopZPXO99in xanthomonas oryzae pv. oryzae

Molecular Plant-Microbe Interactions

Volumn 23, Issue 7, 2010, Pages 893-902

  Song, Congfeng ^a,b   Yang, B ^a  

^a IOWA STATE UNIVERSITY   (United States)

^b NANJING AGRICULTURAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN;

ARTICLE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR CLONING; MUTAGENESIS; MUTATION; PATHOGENICITY; PHYLOGENY; PHYSIOLOGY; VIRULENCE; XANTHOMONAS;

BACTERIAL PROTEINS; CLONING, MOLECULAR; GENE EXPRESSION REGULATION, BACTERIAL; MUTAGENESIS; MUTATION; PHYLOGENY; VIRULENCE; XANTHOMONAS;

BACTERIA (MICROORGANISMS); NICOTIANA BENTHAMIANA; XANTHOMONAS; XANTHOMONAS ORYZAE PV. ORYZAE;

EID: 77953224223     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-23-7-0893     Document Type: Article

References (65)

1. Almeida, N. F., Yan, S., Lindeberg, M., Studholme, D. J., Schneider, D. J., Condon, B., Liu, H., Viana, C. J., Warren, A., Evans, C., Kernen, E., Maclean, D., Angot, A., Martin, G. B., Jones, J. D., Collmer, A., Setubal, J. C., and Vinatzer, B. A. 2009. A draft genome sequence of Pseudomonas syringae pv. tomato T1 reveals a type III effector repertoire significantly divergent from that of Pseudomonas syringae pv. tomato DC3000. Mol. Plant-Microbe Interact. 22:52-62.
2. Ausubel, F., Brent, R., Kingston, R., Moore, D., Seidman, J., and Struhl, K. 1993. Current Protocols in Molecular Biology, 1st ed. John Wiley and Sons, New York.
3. Bartetzko, V., Sonnewald, S., Vogel, F., Hartner, K., Stadler, R., Hammes, U. Z., and Bornke, F. 2009. The Xanthomonas campestris pv. vesicatoria type III effector protein XopJ inhibits protein secretion: Evidence for interference with cell wall-associated defense responses. Mol. PlantMicrobe Interact. 22:655-664.
4. Block, A., Li, G., Fu, Z. Q., and Alfano, J. R. 2008. Phytopathogen type III effector weaponry and their plant targets. Curr. Opin. Plant Biol. 11:396-403.
5. Boch, J., Scholze, H., Schornack, S., Landgraf, A., Hahn, S., Kay, S., Lahaye, T., Nickstadt, A., and Bonas, U. 2009. Breaking the code of DNA binding specificity of TAL-type III effectors. Science 326:1509-1512.
6. Boiler, T., and Felix, G. 2009. A renaissance of elicitors: Perception of microbe-associated molecular patterns and danger signals by patternrecognition receptors. Annu. Rev. Plant. Biol. 60:379-406.
7. 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.
8. Buttner, D., and Bonas, U. 2006. Who comes first? How plant pathogenic bacteria orchestrate type III secretion. Curr. Opin. Microbiol. 9:193-200.
9. Buttner, D., and He, S. Y. 2009. Type III protein secretion in plant pathogenic bacteria. Plant Physiol. 150:1656-1664.
10. Castaneda, A., Reddy, J. D., El-Yacoubi, B., and Gabriel, D. W. 2005. Mutagenesis of all eight avr genes in Xanthomonas campestris pv. campestris had no detected effect on pathogenicity, but one avr gene affected race specificity. Mol. Plant-Microbe Interact. 18:1306-1317.
11. Chisholm, S. T., Coaker, G., Day, B., and Staskawicz, B. J. 2006. Hostmicrobe interactions: Shaping the evolution of the plant immune response. Cell 124:803-814.
12. Cho, H. J., Park, Y. J., Noh, T. H., Kim, Y. T., Kim, J. G., Song, E. S., Lee, D. H., and Lee, B. M. 2008. Molecular analysis of the hrp gene cluster in Xanthomonas oryzae pathovar oryzae KACC10859. Microb. Pathog. 44:473-483.
13. Cunnac, S., Occhialini, A., Barberis, P., Boucher, C., and Genin, S. 2004, Inventory and functional analysis of the large Hrp regulon in Ralstonia solanacearum: Identification of novel effector proteins translocated to plant host cells through the type III secretion system, Mol. Microbiol. 53:115-128.
14. Cunnac, S., Lindeberg, M., and Collmer, A. 2009. Pseudomonas syringae type III secretion system effectors: Repertoires in search of functions, Curr. Opin. Microbiol. 12:53-60.
15. da Cunha, L., Sreerekha, M. V., and Mackey, D. 2007. Defense suppression by virulence effectors of bacterial phytopathogens. Curr. Opin. Plant Biol. 10:349-357.
16. da Silva, A. C., Ferro, J. A., Reinach, F. C., Farah, C. S., Furlan, L. R., Quaggio, R. B., Monteiro-Vitorello, C. B., Van Sluys, M. A., Almeida, N. F., Alves, L. M., do Amaral, A. M., Bertolini, M. C., Camargo, L. E., Camarotte, G., Cannavan, F., Cardozo, J., Chambergo, F., Ciapina, L. P., Cicarelli, R. M., Coutinho, L. L., Cursino-Santos, J. R., El-Dorry, H., Faria, J. B., Ferreira, A. J., Ferreira, R. C., Ferro, M. I., Formighieri, E. F., Franco, M. C., Greggio, C. C., Gruber, A., Katsuyama, A. M., Kishi, L. T., Leite, R. P., Lemos, E. G., Lemos, M. V., Locali, E. C., Machado, M. A., Madeira, A. M., Martinez-Rossi, N. M., Martins, E. C., Meidanis, J., Menck, C. F., Miyaki, C. Y., Moon, D. H., Moreira, L. M., Novo, M. T., Okura, V. K., Oliveira, M. C., Oliveira, V. R., Pereira, H. A., Rossi, A., Sena, J. A., Silva, C., de Souza, R. F., Spinola, L. A., Takita, M. A., Tamura, R. E., Teixeira, E. C., Tezza, R. I., Trindade dos Santos, M., Truffi, D., Tsai, S. M., White, F. F., Setubal, J. C., and Kitajima, J. P. 2002. Comparison of the genomes of two Xanthomonas pathogens with differing host specificities. Nature 417:459-463.
17. Datsenko, K. A., and Wanner, B. L. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U.S.A. 97:6640-6645.
18. Ding, X., Richter, T., Chen, M., Fujii, H., Seo, Y. S., Xie, M., Zheng, X., Kanrar, S., Stevenson, R. A., Dardick, C., Li, Y., Jiang, H., Zhang, Y., Yu, F., Bartley, L. E., Chern, M., Bart, R., Chen, X., Zhu, L., Farmerie, W. G., Gribskov, M., Zhu, J. K., Fromm, M. E., Ronald, P. C., and Song, W. Y. 2009. A rice kinase-protein interaction map. Plant Physiol. 149:1478-1492.
19. Furutani, A., Takaoka, M., Sanada, H., Noguchi, Y., Oku, T., Tsuno, K., Ochiai, H., and Tsuge, S. 2009. Identification of novel type III secretion effectors in Xanthomonas oryzae pv. oryzae. Mol. Plant-Microbe Interact. 22:96-106.
20. Gabriel, D. W., Allen, C., Schell, M., Denny, T. P., Greenberg, J. T., Duan, Y. P., Flores-Cruz, Z., Huang, Q., Clifford, J. M., Presting, G., Gonzalez, E. T., Reddy, J., Elphinstone, J., Swanson, J., Yao, J., Mulholland, V., Liu, L., Farmerie, W., Patnaikuni, M., Balogh, B., Norman, D., Alvarez, A., Castillo, J. A., Jones, J., Saddler, G., Walunas, T., Zhukov, A., and Mikhailova, N. 2006. Identification of open reading frames unique to a select agent: Ralstonia solanacearum race 3 biovar 2. Mol. Plant-Microbe Interact. 19:69-79.
21. Gassmann, W., Dahlbeck, D., Chesnokova, O., Minsavage, G. V., Jones, J. B., and Staskawicz, B. J. 2000. Molecular evolution of virulence in natural field strains of Xanthomonas campestris pv. vesicatoria. J. Bacteriol. 182:7053-7059.
22. Grant, S. R., Fisher, E. J., Chang, J. H., Mole, B. M., and Dangl, J. L. 2006. Subterfuge and manipulation: Type III effector proteins of phytopathogenic bacteria. Annu. Rev. Microbiol. 60:425-449.
23. 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. F. gene expression induced by a type-III effector triggers disease resistance in rice. Nature 435:1122-1125.
24. Guo, M., Tian, F., Wamboldt, Y., and Alfano, J. R. 2009. The majority of the type III effector inventory of Pseudomonas syringae pv. tomato DC3000 can suppress plant immunity. Mol. Plant-Microbe Interact. 22:1069-1080.
25. Gurlebeck, D., Thieme, F., and Bonas, U. 2006. Type III effector proteins from the plant pathogen Xanthomonas and their role in the interaction with the host plant. J. Plant Physiol. 163:233-255.
26. Guttman, D. S., Vinatzer, B. A., Sarkar, S. E, Ranall, M. V., Kettler, G., and Greenberg, J. T. 2002. A functional screen for the type III (Hrp) secretome of the plant pathogen Pseuaomonas syringae. Science 295:1722-1726.
27. 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.
28. Hotson, A., Chosed, R., Shu, H., Orth, K., and Mudgett, M. B. 2003. Xanthomonas type III effector XopD targets SUMO-conjugated proteins in planta. Mol. Microbiol. 50:377-389.
29. Jiang, B. L., He, Y. Q., Cen, W. J., Wei, H. Y., Jiang, G. F., Jiang, W., Hang, X. H., Feng, J. X., Lu, G. T., Tang, D. J., and Tang, J. L. 2008. The type III secretion effector XopXccN of Xanthomonas campestris pv. campestris is required for full virulence. Res. Microbiol. 159:216-220.
30. Joardar, V., Lindeberg, M., Jackson, R. W., Selengut, J., Dodson, R., Brinkac, L. M., Daugherty, S. C., Deboy, R., Durkin, A. S., Giglio, M. G., Madupu, R., Nelson, W. C., Rosovitz, M. J., Sullivan, S., Crabtree, J., Creasy, T., Davidsen, T., Haft, D. H., Zafar, N., Zhou, L., Halpin, R., Holley, T., Khouri, H., Feldblyum, T., White, O., Fraser, C. M., Chatterjee, A. K., Cartinhour, S., Schneider, D. J., Mansfield, J., Collmer, A., and Buell, C. R. 2005. Whole-genome sequence analysis of Pseuaomonas syringae pv. phaseolicola 1448A reveals divergence among pathovars in genes involved in virulence and transposition. J. Bacteriol. 187:6488-6498.
31. Kauffman, H. E., Reddy, A. P. K., Hsiek, S. P., and Marca, S. D. 1973. An improved technique for evaluating resistance of race varieties to Xanthomonas oryza. Plant Dis. Rep. 57:537-541.
32. Kay, S., Hahn, S., Marois, E., Hause, G., and Bonas, U. 2007. A bacterial effector acts as a plant transcription factor and induces a cell size regulator. Science 318:648-651.
33. Kearney, B., and Staskawicz, B. J. 1990. Widespread distribution and fitness contribution of Xanthomonas campestris avirulence gene avrBs2. Nature 346:385-386.
34. Keshavarzi, M., Soylu, S., Brown, I., Bonas, U., Nicole, M., Rossiter, J., and Mansfield, J. 2004. Basal defenses induced in pepper by lipopolysaccharides are suppressed by Xanthomonas campestris pv. vesicatoria. Mol. Plant-Microbe Interact. 17:805-815.
35. Kim, J. G., Taylor, K. W., Hotson, A., Keegan, M., Schmelz, E. A., and Mudgett, M. B. 2008. XopD SUMO protease affects host transcription, promotes pathogen growth, and delays symptom development in Xanthomonas-iniecled tomato leaves. Plant Cell 20:1915-1929.
36. Kim, J. G., Li, X., Roden, J. A., Taylor, K. W., Aakre, C. D., Su, B., Lalonde, S., Kirik, A., Chen, Y., Baranage, G., McLane, H., Martin, G. B., and Mudgett, M. B. 2009. Xanthomonas T3S effector XopN suppresses PAMP-triggered immunity and interacts with a tomato atypical receptor-like kinase and TFT1. Plant Cell 21:1305-1323.
37. Kumar, S., Tamura, K., and Nei, M. 2004. MEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform. 5:150-163.
38. 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.
39. Lee, B. M., Park, Y. J., Park, D. S., Kang, H. W., Kim, J. G., Song, E. S., Park, I. C., Yoon, U. H., Hahn, J. H., Koo, B. S., Lee, G. B., Kim, H., Park, H. S., Yoon, K. O., Kim, J. H., Jung, C. H., Koh, N. H., Seo, J. S., and Go, S. J. 2005. The genome sequence of Xanthomonas oryzae pathovar oryzae KACC10331, the bacterial blight pathogen of rice. Nucleic Acids Res. 33:577-586.
40. Lee, S. W., Han, S. W., Sririyanum, M., Park, C. J., Seo, Y. S., and Ronald, P. C. 2009. A type I-secreted, sulfated peptide triggers XA21-mediated innate immunity. Science 326:850-853.
41. Mazzola, M., Leach, J. E., Nelson, R., and White, F. F. 1994. Analysis of the interaction between Xanthomonas oryzae pv. oryzae and the rice cultivars IR24 and IRBB21. Phytopathology 84:392-397.
42. Metz, M., Dahlbeck, D., Morales, C. Q., Al Sady, B., 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.
43. Mew, T. W. 1987. Current status and future prospects of research on bacterial blight of rice. Annu. Rev. Phytopathol. 25:359-382.
44. Moscou, M. J., and Bogdanove, A. J. 2009. A simple cipher governs DNA recognition by TAL effectors. Science 326:1501.
45. Mudgett, M. B. 2005. New insights to the function of phytopathogenic bacterial type III effectors in plants. Annu. Rev. Plant. Biol. 56:509-531.
46. Ochiai, H., Inoue, Y., Takeya, M., Sasaki, A., and Kaku, H. 2005.Genome sequence of Xanthomonas oryzae pv. oryzae suggests contribution of large numbers of effector genes and insertion sequences to its race diversity. Jpn. Agric. Res. Q. 39:275-287.
47. Qian, W., Jia, Y., Ren, S. X., He, Y. Q., Feng, J. X., Lu, L. RR., Sun, Q., Ying, G., Tang, D. J., Tang, H., Wu, W., Hao, P., Wang, L., Jiang, B. L., Zeng, S., Gu, W. Y., Lu, G., Rong, L., Tian, Y., Yao, Z., Fu, G., Chen, B., Fang, R., Qiang, B., Chen, Z., Zhao, G. P., Tang, J. L., and He, C. 2005. Comparative and functional genomic analyses of the pathogenicity of phytopathogen Xanthomonas campestris pv. campestris. Genome Res. 15:757-767.
48. Roden, J. A., Belt, B., Ross, J. B., Tachibana, T., Vargas, J., and Mudgett, M. B. 2004. A genetic screen to isolate type III effectors translocated into pepper cells during Xanthomonas infection. Proc. Natl. Acad. Sci. U.S.A. 101:16624-16629.
49. Romer, P., Hahn, S., Jordan, T., Strauss, T., Bonas, U., and Lahaye, T. 2007. Plant pathogen recognition mediated by promoter activation of the pepper Bs3 resistance gene. Science 318:645-648.
50. Saitou, N., and Nei, M. 1987. The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4:406-425.
51. Salanoubat, M., Genin, S., Artiguenave, F., Gouzy, J., Mangenot, S., Arlat, M., Billault, A., Brottier, P., Camus, J. C., Cattolico, L., Chandler, M., Choisne, N., Claudel-Renard, C., Cunnac, S., Demange, N., Gaspin, C., Lavie, M., Moisan, A., Robert, C., Saurin, W., Schiex, T., Siguier, P., Thebault, P., Whalen, M., Wincker, P., Levy, M., Weissenbach, J., and Boucher, C. A. 2002. Genome sequence of the plant pathogen Ralstonia solanacearum. Nature 415:497-502.
52. A. BMC Genomics 9:204.
53. Sugio, A., Yang, B., Zhu, T., and White, F. F. 2007. Two type III effector genes of Xanthomonas oryzae pv. oryzae control the induction of the host genes OsTFIIAγ1 and OsTFX1 during bacterial blight of rice. Proc. Natl. Acad. Sci. U.S.A. 104:10720-10725.
54. Takai, R., Isogai, A., Takayama, S., and Che, F. S. 2008. Analysis of flagellin perception mediated by flg22 receptor OsFLS2 in rice. Mol. PlantMicrobe Interact. 21:1635-1642.
55. Thieme, F., Koebnik, R., Bekel, T., Berger, C., Boch, J., Buttner, D., Caldana, C., Gaigalat, L., Goesmann, A., Kay, S., Kirchner, O., Lanz, C., Linke, B., McHardy, A. C., Meyer, F., Mittenhuber, G., Nies, D. H., Niesbach-Klosgen, U., Patschkowski, T., Ruckert, C., Rupp, O., Schneiker, S., Schuster, S. C., Vorholter, F. J., Weber, E., Puhler, A., Bonas, U., Bartels, D., and Kaiser, O. 2005. Insights into genome plasticity and pathogenicity of the plant pathogenic bacterium Xanthomonas campestris pv. vesicatoria revealed by the complete genome sequence. J. Bacteriol. 187:7254-7266.
56. Tsuge, S., Fukunaka, R., Oku, T., Tsuno, K., Ochiai, H., Inoue, Y., Kaku, H., and Kubo, Y. 2002. Expression of Xanthomonas oryzae pv. oryzae hrp genes in XOM2, a novel synthetic medium. J. Gen. Plant Pathol. 68:363-371.
57. Vorholter, F. J., Schneiker, S., Goesmann, A., Krause, L., Bekel, T., Kaiser, O., Linke, B., Patschkowski, T., Ruckert, C., Schmid, J., Sidhu, V. K., Sieber, V., Tauch, A., Watt, S. A., Weisshaar, B., Becker, A., Niehaus, K., and Puhler, A. 2008. The genome of Xanthomonas campestris pv. campestris B100 and its use for the reconstruction of metabolic pathways involved in xanthan biosynthesis. J. Biotechnol. 134:33-45.
58. Wang, C. L., Xu, A., Gao, Y., Fan, Y. L., Liang, Y. T., Zheng, C. K., Sun, L. Q., Wang, W. Q., and Zhao, K. J. 2008. Generation and characterisation of Tn5-tagged Xanthomonas oryzae pv. oryzae mutants that overcome Xa23 -mediated resistance to bacterial blight of rice. Eur. J. Plant Pathol. 123:343-351.
59. White, F. F., and Yang, B. 2009. Host and pathogen factors controlling the vice-Xanthomonas oryzae interaction. Plant Physiol. 150:1677-1686.
60. White, F. F., Potnis, N., Jones, J. B., and Koebnik, R. 2009. The type III effectors of Xanthomonas. Mol. Plant. Pathol. 10:749-766.
61. Wichmann, G., and Bergelson, J. 2004. Effector genes of Xanthomonas axonopoais pv. vesicatoria promote transmission and enhance other fitness traits in the field. Genetics 166:693-706.
62. Willems, A., Goor, M., Thielemans, S., Gillis, M., Kersters, K., and De Ley, J. 1992. Transfer of several phytopathogenic Pseudomonas species to Acidovorax as Acidovorax avenae subsp. avenae subsp. nov., comb, nov., Acidovorax avenae subsp. citrulli, Acidovorax avenae subsp. cattleyae, and Acidovorax konjaci. Int. J. Syst. Bacteriol. 42:107-119.
63. 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.
64. Yang, B., Sugio, A., and White, F. F. 2006. Os8N3 is a host disease-sus-ceptibility gene for bacterial blight of rice. Proc. Natl. Acad. Sci. U.S.A. 103:10503-10508.
65. 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. The Xanthomonas Resource: www.xanthomonas.org/t3e.html