XopR, a type III effector secreted by xanthomonas oryzae pv. oryzae, suppresses microbe-associated molecular pattern-triggered immunity in arabidopsis thaliana

Molecular Plant-Microbe Interactions

Volumn 25, Issue 4, 2012, Pages 505-514

  Akimoto Tomiyama, Chiharu ^a   Furutani, Ayako ^a,d   Tsuge, Seiji ^b   Washington, Erica J ^c   Nishizawa, Yoko ^a   Minami, Eiichi ^a   Ochiai, Hirokazu ^a  

^a NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

^b KYOTO PREFECTURAL UNIVERSITY   (Japan)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^d IBARAKI UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; DEXAMETHASONE;

ARABIDOPSIS; ARTICLE; CELL CULTURE; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; PLANT DISEASE; PROMOTER REGION; TOBACCO; TRANSGENIC PLANT; XANTHOMONAS;

ARABIDOPSIS; BACTERIAL PROTEINS; CELLS, CULTURED; DEXAMETHASONE; GENE EXPRESSION REGULATION, BACTERIAL; GENE EXPRESSION REGULATION, PLANT; PLANT DISEASES; PLANTS, GENETICALLY MODIFIED; PROMOTER REGIONS, GENETIC; TOBACCO; XANTHOMONAS;

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

EID: 84858994479     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-06-11-0167     Document Type: Article

References (60)

1. Abramovitch, R. B., Anderson, J. C, and Martin, G. M. 2006. Bacterial elicitation and evasion of plant innate immunity. Nat. Rev. Mol. Cell Biol. 7:601-611. (Pubitemid 44325351)
2. Alfano, J. R., and Collmer, A. 1997. The type III (Hrp) secretion pathway of plant pathogenic bacteria: Trafficking harpins, Avr proteins, and death. J. Bacteriol. 179:5655-5662. (Pubitemid 27398261)
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. (Pubitemid 39308518)
4. Aoyama, T, and Chua, N. H. 1997. A glucocorticoid-mediated transcriptional induction system in transgenic plants. Plant J. 11:605-612. (Pubitemid 27158965)
5. Bartetzko, V., Sonnewald, S., Vogel, F., Hartner, K., Stadler, R., Hammes, U. Z., and Frederik, B. 2009. The Xanthomonas campestris pv. vesica-toria type III effector protein XopJ inhibits protein secretion: Evidence for interference with cell wall-associated defense responses. Mol. Plant-Microbe Interact. 22:655-664.
6. 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.
7. Boller, T, and He, S.Y. 2009. Innate immunity in plants: An arms race between pattern recognition receptors in plants and effectors in microbial pathogens. Science 324:742-744.
8. Brown, I. R., Mansfield, J. W., and Bonas, U. 1995. Hrp genes in Xanthomonas campestris pv. vesicatoria determine ability to suppress papilla deposition in pepper mesophyll cells. Mol. Plant-Microbe Interact. 8:825-836. (Pubitemid 3023304)
9. Büttner, D., and Bonas, U. 2006. Who comes first? How plant pathogenic bacteria orchestrate type III secretion. Curr. Opin. Microbiol. 9:193-200.
10. Büttner, D., and He, S. Y. 2009. Type III protein secretion in plant pathogenic bacteria. Plant Physiol. 150:1656-1664.
11. Clay, N. K., Adio, A. M., Denoux, C, Jander, G., and Ausubel, F. M. 2009. Glucosinolate metabolites required for an Arabidopsis innate immune response. Science 323:95-101.
12. Clough, S. J., and Bent, A. F. 1998. Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16:735-743.
13. Curtis, M. D., and Grossniklaus, U. 2003. A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol. 133:462-469. (Pubitemid 37325657)
14. 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, S. 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. (Pubitemid 34563540)
15. Dowen, R. H., Engel, J. L., Shao, F., Ecker, J. R., and Dixon, J. E. 2009. A family of bacterial cysteine protease type III effectors utilizes acylation-dependent and -independent strategies to localize to plasma membranes. J. Biol. Chem. 284:15867-15879.
16. 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.
17. Goel, A. K., Lundberg, D., Torres, M. A., Matthews, R., Akimoto-Tomiyama, C, Farmer, L., Dangl, J. L., and Grant, S. R. 2008. The Pseudomonas syringae type III effector Hop AM1 enhances virulence on water-stressed plants. Mol. Plant-Microbe. Interact. 21:361-370. (Pubitemid 351398670)
18. Göhre, V, Spallek, T, Häweker, H., Mersmann, S., Mentzel, T., Boller, T., de Torres, M., Mansfield, J. W, and Robatzek, S. 2008. Plant pattern-recognition receptor FLS2 is directed for degradation by the bacterial ubiquitin ligase AvrPtoB. Curr. Biol. 18:1824-1832.
19. Gomez-Gomez, L., and Boller, T. 2002. Flagellin perception: A paradigm for innate immunity. Trends Plant Sci. 7:251-256. (Pubitemid 36726527)
20. 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 phyto-pathogenic bacteria. Annu. Rev. Microbiol. 60:425-449. (Pubitemid 44627956)
21. Griesbeck, O., Baird, G. S, Campbell, R. E., Zacharias, D. A., and Tsien, R.Y 2001. Reducing the environmental sensitivity of yellow fluorescent protein. Mechanism and applications. J. Biol. Chem. 276:29188-29194.
22. 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. (Pubitemid 40910521)
23. He, P., Shan, L., Lin, N. C, Martin, G. B., Kemmerling, B., Nurnberger, T., and Sheen, J. 2006. Specific bacterial suppressors of MAMP signaling upstream of MAPKKK in Arabidopsis innate immunity. Cell 125:563-575.
24. He, P., Shan, L., and Sheen, J. 2007. Elicitation and suppression of microbe-associated molecular pattern-triggered immunity in plant-microbe interactions. Cell Microbiol. 9:1385-1396. (Pubitemid 46774012)
25. Holt, B. F, III, Belkhadir, Y, and Dangl, J. L. 2005. Antagonistic control of disease resistance protein stability in the plant immune system. Science 309:929-932. (Pubitemid 41099928)
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 Rhizobium trifolii symbiosis plasmid. J. Bacteriol. 170:3793-3802.
27. Jelenska, J., Yao, N., Vinatzer, B. A., Wright, C. M., Brodsky, J. L., and Greenberg, J. T. 2007. A J domain virulence effector of Pseudomonas syringae remodels host chloroplasts and suppresses defenses. Curr. Biol. 17:499-508. (Pubitemid 46401385)
28. Kaku, H., Nishizawa, Y, Ishii-Minami, N., Akimoto-Tomiyama, C, Dohmae, N., Takio, K., Minami, E., and Shibuya, N. 2006. Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. Proc. Natl. Acad. Sci. U.S.A. 103:11086-11091. (Pubitemid 44148422)
29. Kauffman, H. E., Reddy, A. P. K., Hsieh, S. P. Y, and Merca, S. D. 1973. An improved technique for evaluating resistance to rice varieties of Xanthomonas oryzae. Plant Dis. Rep. 57:537-541.
30. Kay, S., and Bonas, U. 2009. How Xanthomonas type III effectors manipulate the host plant. Curr. Opin. Microbiol. 12:37-43.
31. 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 Xan-thomonas-infected tomato leaves. Plant Cell. 20:1915-1929. (Pubitemid 352844541)
32. 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.
33. Knodler, L. A., Ibarra, J. A., Pérez-Rueda, E., Yip, C. K., and Steele-Mortimer, O. 2011. Coiled-coil domains enhance the membrane association of Salmonella type III effectors. Cell Microbiol. 13:1497-1517.
34. Kubota, K., Tsuda, S., Tamai, A., and Meshi, T. 2003. Tomato mosaic virus replication protein suppresses virus-targeted posttranscriptional gene silencing. J. Virol. 77:11016-11026. (Pubitemid 37204293)
35. 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, 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. (Pubitemid 40360987)
36. Lindeberg, M., Stavrinides, J., Chang, J. H., Alfano, J. R., Collmer, A., Dangl, J. L, Greenberg, J T. Mansfield, J. W. and Guttman, D. S. 2005. Proposed guidelines for a unified nomenclature and phylogenetic analysis of type III Hop effector proteins in the plant pathogen Pseudomonas syringae. Mol. Plant-Microbe. Interact. 18:275-282. (Pubitemid 40383895)
37. Logemann, E., Birkenbihl, R. P., Uler, B., and Somssich, I. E. 2006. An improved method for preparing Agrobacterium cells that simplifies the Arabidopsis transformation protocol. Plant Methods 2:16.
38. Meyer, D., Lauber, E., Roby, D., Arlat, M., and Kroj, T. 2005. Optimization of pathogenicity assays to study the Arabidopsis thaliana-Xanthomonas campestris pv. campestris pathosystem. Mol. Plant Pathol. 6:327-333. (Pubitemid 40793943)
39. Miller, J. C, Tan, S., Qiao, G, Barlow, K. A., Wang, J., Xia, D. F., Meng, X., Paschon, D. E., Leung, E., and Hinkley, S. J. 2011. A TALE nuclease architecture for highly efficient genome editing. Nat. Biotechnol. 29:143-148.
40. Miller, J. H. 1972. Experiments in Molecular Genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, U.S.A.
41. Miya, A., Albert, P., Shinya, T, Desaki, Y, Ichimura, K., Shirasu, K., Narusaka, Y, Kawakami, N., Kaku, H., and Shibuya, N. 2007. CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 104:19613-19618.
42. Nimchuk, Z., Marois, E., Kjemtrup, S., Leister, R. T, Katagiri, F., and Dangl, J. L. 2000. Eukaryotic fatty acylation drives plasma membrane targeting and enhances function of several type III effector proteins from Pseudomonas syringae. Cell 101:353-363.
43. 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. (Pubitemid 44577089)
44. Robert-Seilaniantz, A., Shan, L., Zhou, J.-M., and Tang, X. 2006. The Pseudomonas syringae pv. tomato DC3000 type III effector HopF2 has a putative myristoylation site required for its avirulence and virulence functions. Mol. Plant-Microbe. Interact. 19:130-138. (Pubitemid 43172827)
45. Salzberg, S. L, Sommer, D. D., Schatz, M. C, Phillippy, A. M., Rabinowicz, P. D., Tsuge, S., Furutani, A., Ochiai, H., Delcher, A. L., Kelley, D., Madupu, R., Puiu, D., Radune, D., Shumway, M., Trapnell, C, Aparna, G, Jha, G., Pandey, A., Patil, P. B., Ishihara, H., Meyer, D. F., Szurek, B., Verdier, V., Koebnik, R., Dow, J. M., Ryan, R. P., Hirata, H., Tsuyumu, S., Won Lee, S., Seo, Y S., Sriariyanum, M., Ronald, P. C, Sonti, R. V., Van Sluys, M. A., Leach, J. E., White, F. F., and Bogdanove, A. J. 2008. Genome sequence and rapid evolution of the rice pathogen Xanthomonas oryzae pv. oryzae PXO99A. BMC Genomics 9:204.
46. Scholze, H., and Boch, J. 2011. TAL effectors are remote controls for gene activation. Curr. Opin. Microbiol. 14:47-53.
47. Shan, L., Thara, V K., Martin, G. B., Zhou, J. M., and Tang, X. 2000. The Pseudomonas AvrPto protein is differentially recognized by tomato and tobacco and is localized to the plant plasma membrane. Plant Cell 12:2323-2338.
48. Shimizu, T, Nakano, T., Takamizawa, D., Desaki, Y, Ishii-Minami, N, Nishizawa, Y, Minami, E., Okada, K., Yamane, H, Kaku, H., and Shibuya, N. 2010. Two LysM receptor molecules, CEBiP and OsCERK1, cooperatively regulate chitin elicitor signaling in rice. Plant J. 64:204-214.
49. Song, C, and Yang, B. 2010. Mutagenesis of 18 type III effectors reveals virulence function of XopZ#inf#PX#/inf#O99 in Xanthomonas oryzae pv. oryzae. Mol. Plant-Microbe. Interact. 23:893-902.
50. Takai, R., Isogai, A., Takayama, S., and Che, F. S. 2008. Analysis of fla-gellin perception mediated by flg22 receptor OsFLS2 in rice. Mol. Plant-Microbe. Interact. 21:1635-1642.
51. Thieme, F, Szczesny, R., Urban, A., Kirchner, O., Hause, G., and Bonas, U. 2007. New type III effectors from Xanthomonas campestris pv. vesi-catoria trigger plant reactions dependent on a conserved N-myristoyla-tion motif. Mol. Plant-Microbe. Interact. 20:1250-1261. (Pubitemid 47417395)
52. 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.
53. Tsuge, S., Furutani, A., 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 a novel synthetic medium, XOM2. J. Gen. Plant Pathol. 68:363-371.
54. 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.
55. Vieira, J., and Messing, J. 1987. Production of single-stranded plasmid DNA. Methods Enzymol. 153:3-11.
56. White, F. F., Potnis, N., Jones, J. B., and Koebnik, R. 2009. The type III effectors of Xanthomonas. Mol. Plant Pathol. 10:749-766.
57. Xiang, T, Zong, N., Zou, Y, Wu, Y, Zhang, J., Xing, W, Li, Y, Tang, X., Zhu, L., Chai, J., and Zhou, J. M. 2008. Pseudomonas syringae effector AvrPto blocks innate immunity by targeting receptor kinases. Curr. Biol. 18:74-80.
58. 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.
59. Zhang, J., Shao, F, Li, Y, Cui, H., Chen, L., Li, H., Zou, Y, Long, C, Lan, L., Chai, J., Chen, S., Tang, X., and Zhou, J. M. 2007. A Pseudomonas syringae effector inactivates MAPKs to suppress PAMP-induced immunity in plants. Cell Host Microbe 17:175-185. (Pubitemid 46706361)
60. Zipfel, C, Robatzek, S., Navarro, L., Oakeley, E. J., and Jones, J. D. 2004. Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428:764-767. (Pubitemid 38508287)