CD2-1, the C-terminal region of flagellin, modulates the induction of immune responses in rice

Molecular Plant-Microbe Interactions

Volumn 28, Issue 6, 2015, Pages 648-658

  Katsuragi, Yuya ^a   Takai, Ryota ^a   Furukawa, Takehito ^a   Hirai, Hiroyuki ^a   Morimoto, Takumi ^a   Katayama, Takara ^a   Murakami, Takahiko ^a   Che, Fang Sik ^a  

^a NAGAHAMA INSTITUTE OF BIO SCIENCE AND TECHNOLOGY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ACIDOVORAX AVENAE; ARABIDOPSIS;

ARABIDOPSIS PROTEIN; BACTERIAL PROTEIN; CALLOSE; EPITOPE; FLAGELLIN; FLS2 PROTEIN, ARABIDOPSIS; GLUCAN; HYDROGEN PEROXIDE; PROTEIN KINASE; RECOMBINANT PROTEIN; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; ARABIDOPSIS; CELL CULTURE; COMAMONADACEAE; DNA MICROARRAY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; PLANT DISEASE; PLANT IMMUNITY; RICE; TRANSGENIC PLANT;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BACTERIAL PROTEINS; CELLS, CULTURED; COMAMONADACEAE; EPITOPES; FLAGELLIN; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GLUCANS; HOST-PATHOGEN INTERACTIONS; HYDROGEN PEROXIDE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; ORYZA SATIVA; PLANT DISEASES; PLANT IMMUNITY; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; PROTEIN KINASES; RECOMBINANT PROTEINS;

EID: 84926504707     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-11-14-0372-R     Document Type: Article

References (47)

1. Asai, T., Tena, G., Plotnikova, J., Willmann, M. R., Chiu, W. L., Gomez-Gomez, L., Boller, T., Ausubel, F. M., and Sheen, J. 2002. MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415:977-983.
2. Baba, A., Hasezawa, S., and Syono, K. 1986. Cultivation of rice protoplasts and their transformation mediated by Agrobacterium spheroplasts. Plant Cell Physiol. 27:463-472.
3. Boller, T., and Felix, G. 2009. A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu. Rev. Plant Biol. 60:379-406.
4. Cai, R., Lewis, J., Yan, S., Liu, H., Clarke, C. R., Campanile, F., Almeida, N. F., Studholme, D. J., Lindeberg, M., Schneider, D., Zaccardelli, M., Setubal, J. C., Morales-Lizcano, N. P., Bernal, A., Coaker, G., Baker, C., Bender, C. L., Leman, S., and Vinatzer, B. A. 2011. The plant pathogen Pseudomonas syringae pv. tomato is genetically monomorphic and under strong selection to evade tomato immunity. PLoS Pathog. 7: e1002130.
5. Che, F. S., Iwano, M., Tanaka, N., Takayama, S., Minami, E., Shibuya, N., Kadota, I., and Isogai, A. 1999. Biochemical and morphological features of rice cell death induced by Pseudomonas avenae. Plant Cell Physiol. 40:1036-1045.
6. Che, F. S., Nakajima, Y., Tanaka, N., Iwano, M., Yoshida, T., Takayama, S., Kadota, I., and Isogai, A. 2000. Flagellin from an incompatible strain of Pseudomonas avenae induces a resistance response in cultured rice cells. J. Biol. Chem. 275:32347-32356.
7. Clarke, C. R., Chinchilla, D., Hind, S. R., Taguchi, F., Miki, R., Ichinose, Y., Martin, G. B., Leman, S., Felix, G., and Vinatzer, B. A. 2013. Allelic variation in two distinct Pseudomonas syringae flagellin epitopes modulates the strength of plant immune responses but not bacterial motility. New Phytol. 200:847-860.
8. Felix, G., Duran, J. D., Volko, S., and Boller, T. 1999. Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J. 18:265-276.
9. Fliegmann, J., Mithofer, A., Wanner, G., and Ebel, J. 2004. An ancient enzyme domain hidden in the putative beta-glucan elicitor receptor of soybean may play an active part in the perception of pathogen-associated molecular patterns during broad host resistance. J. Biol. Chem. 279: 1132-1140.
10. Fujiwara, S., Tanaka, N., Kaneda, T., Takayama, S., Isogai, A., and Che, F. S. 2004. Rice cDNA microarray-based gene expression profiling of the response to flagellin perception in cultured rice cells. Mol. Plant Microbe Interact. 17:986-998.
11. Furukawa, T., Inagaki, H., Takai, R., Hirai, H., and Che, F. S. 2014. Two distinct EF-Tu epitopes induce immune responses in rice and Arabidopsis. Mol. Plant Microbe Interact. 27:113-124.
12. Gómez-Gómez, L., and Boller, T. 2000. FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol. Cell 5:1003-1011.
13. Hayashi, F., Smith, K. D., Ozinsky, A., Hawn, T. R., Yi, E. C., Goodlett, D. R., Eng, J. K., Akira, S., Underhill, D. M., and Aderem, A. 2001. The innate immune response to bacterial flagellin is mediated by toll-like receptor 5. Nature 410:1099-1103.
14. Hirai, H., Takai, R., Iwano, M., Nakai, M., Kondo, M., Takayama, S., Isogai, A., and Che, F. S. 2011. Glycosylation regulates specific induction of rice immune responses by Acidovorax avenae flagellin. J. Biol. Chem. 286:25519-25530.
15. Ichimura, K., Casais, C., Peck, S. C., Shinozaki, K., and Shirasu, K. 2006. MEKK1 is required for MPK4 activation and regulates tissue-specific and temperature-dependent cell death in Arabidopsis. J. Biol. Chem. 281:36969-36976.
16. 2 accumulation preceding hypersensitive cell death induced by an incompatible strain of Pseudomonas avenae in cultured rice cells. Mol. Plant Pathol. 3:1-8.
17. Jones, J. D., and Dangl, J. L. 2006. The plant immune system. Nature 444: 323-329.
18. Kadota, I., Mizuno, A., and Nishiyama, K. 1996. Detection of a protein specific to the strain of Pseudomonas avenae Manns 1909 pathogenic to rice. Jpn. J. Phytopathol. 62:425-428.
19. 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. USA 103:11086-11091.
20. Kaneda, T., Taga, Y., Takai, R., Iwano, M., Matsui, H., Takayama, S., Isogai, A., and Che, F. S. 2009. The transcription factor OsNAC4 is a key positive regulator of plant hypersensitive cell death. EMBO J. 28:926-936.
21. Klarzynski, O., Plesse, B., Joubert, J. M., Yvin, J. C., Kopp, M., Kloareg, B., and Fritig, B. 2000. Linear beta-1,3 glucans are elicitors of defense responses in tobacco. Plant Physiol. 124:1027-1038.
22. Komoriya, K., Shibano, N., Higano, T., Azuma, N., Yamaguchi, S., and Aizawa, S. I. 1999. Flagellar proteins and type III-exported virulence factors are the predominant proteins secreted into the culture media of Salmonella typhimurium. Mol. Microbiol. 34:767-779.
23. Kunze, G., Zipfel, C., Robatzek, S., Niehaus, K., Boller, T., and Felix, G. 2004. The N terminus of bacterial elongation factor Tu elicits innate immunity in Arabidopsis plants. Plant Cell 16:3496-3507.
24. Laquitaine, L., Gomès, E., François, J., Marchive, C., Pascal, S., Hamdi, S., Atanassova, R., Delrot, S., and Coutos-Thévenot, P. 2006. Molecular basis of ergosterol-induced protection of grape against Botrytis cinerea: induction of type I LTP promoter activity, WRKY, and stilbene synthase gene expression. Mol. Plant Microbe Interact. 19:1103-1112.
25. Luna, E., Pastor, V., Robert, J., Flors, V., Mauch-Mani, B., and Ton, J. 2011. Callose deposition: a multifaceted plant defense response. Mol. Plant Microbe Interact. 24:183-193.
26. Malapaka, R. R., Adebayo, L. O., and Tripp, B. C. 2007. A deletion variant study of the functional role of the Salmonella flagellin hypervariable domain region in motility. J. Mol. Biol. 365:1102-1116.
27. Nakashita, H., Yoshioka, K., Takayama, M., Kuga, R., Midoh, N., Usami, R., Horikoshi, K., Yoneyama, K., and Yamaguchi, I. 2001. Characterization of PBZ1, a probenazole-inducible gene, in suspension-cultured rice cells. Biosci. Biotechnol. Biochem. 65:205-208.
28. Qiu, J. L., Zhou, L., Yun, B. W., Nielsen, H. B., Fiil, B. K., Petersen, K., Mackinlay, J., Loake, G. J., Mundy, J., and Morris, P. C. 2008. Arabidopsis mitogen-activated protein kinase kinases MKK1 and MKK2 have overlapping functions in defense signaling mediated by MEKK1, MPK4, and MKS1. Plant Physiol. 148:212-222.
29. Romeis, T., Piedras, P., Zhang, S., Klessig, D. F., Hirt, H., and Jones, J. D. 1999. Rapid Avr9- and Cf-9 -dependent activation of MAP kinases in tobacco cell cultures and leaves: convergence of resistance gene, elicitor, wound, and salicylate responses. Plant Cell 11:273-287.
30. Samakovlis, C., Asling, B., Boman, H. G., Gateff, E., and Hultmark, D. 1992. In vitro induction of cecropin genes - An immune response in a Drosophila blood cell line. Biochem. Biophys. Res. Commun. 188: 1169-1175.
31. Samatey, F. A., Imada, K., Nagashima, S., Vonderviszt, F., Kumasaka, T., Yamamoto, M., and Namba, K. 2001. Structure of the bacterial flagellar protofilament and implications for a switch for supercoiling. Nature 410: 331-337.
32. Schuster, S. C., and Khan, S. 1994. The bacterial flagellar motor. Annu. Rev. Biophys. Biomol. Struct. 23:509-539.
33. 2+) and protein-kinase activity. Planta 187:136-141.
34. Shiu, S. H., Karlowski, W. M., Pan, R., Tzeng, Y. H., Mayer, K. F., and Li, W. H. 2004. Comparative analysis of the receptor-like kinase family in Arabidopsis and rice. Plant Cell 16:1220-1234.
35. Silipo, A., Molinaro, A., Sturiale, L., Dow, J. M., Erbs, G., Lanzetta, R., Newman, M. A., and Parrilli, M. 2005. The elicitation of plant innate immunity by lipooligosaccharide of Xanthomonas campestris. J. Biol. Chem. 280:33660-33668.
36. Singh, P., Kuo, Y. C., Mishra, S., Tsai, C. H., Chien, C. C., Chen, C. W., Desclos-Theveniau, M., Chu, P. W., Schulze, B., Chinchilla, D., Boller, T., and Zimmerli, L. 2012. The lectin receptor kinase-VI.2 is required for priming and positively regulates Arabidopsis pattern-triggered immunity. Plant Cell 24:1256-1270.
37. Song, W. Y., Wang, G. L., Chen, L. L., Kim, H. S., PiL. Y.Holsten. T., Gardner. J., Wang. B., Zhai. W. X., Zhu. L. H., Fauquet. C., Ronald. P. 1995. A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science 270:1804-1806.
38. Takai, R., Kaneda, T., Isogai, A., Takayama, S., and Che, F. S. 2007. A new method of defense response analysis using a transient expression system in rice protoplasts. Biosci. Biotechnol. Biochem. 71:590-593.
39. Takai, R., Isogai, A., Takayama, S., and Che, F. S. 2008. Analysis of flagellin perception mediated by flg22 receptor OsFLS2 in rice. Mol. Plant Microbe Interact. 21:1635-1642.
40. Tanaka, N., Nakajima, Y., Kaneda, T., Takayama, S., Che, F. S., and Isogai, A. 2001. DNA laddering during hypersensitive cell death in cultured rice cell induced by an incompatible strains of Pseudomonas avenae. Plant Biotechnol. 18:295-299.
41. 2 generation accompanying hypersensitive cell death and expression of PAL, Cht-1, and PBZ1, but not of Lox in rice. Mol. Plant Microbe Interact. 16:422-428.
42. Toki, S. 1997. Rapid and efficient Agrobacterium-mediated transformation in rice. Plant Mol. Biol. Rep. 15:16-21.
43. Wilson, D. R., and Beveridge, T. J. 1993. Bacterial flagellar filaments and their component flagellins. Can. J. Microbiol. 39:451-472.
44. Wyant, T. L., Tanner, M. K., and Sztein, M. B. 1999. Potent immunoregulatory effects of Salmonella typhi flagella on antigenic stimulation of human peripheral blood mononuclear cells. Infect. Immun. 67:1338-1346.
45. Yamaguchi, T., Yamada, A., Hong, N., Ogawa, T., Ishii, T., and Shibuya, N. 2000. Differences in the recognition of glucan elicitor signals between rice and soybean: beta-glucan fragments from the rice blast disease fungus Pyricularia oryzae that elicit phytoalexin biosynthesis in suspension-cultured rice cells. Plant Cell 12:817-826.
46. Yonekura, K., Maki-Yonekura, S., and Namba, K. 2003. Complete atomic model of the bacterial flagellar filament by electron cryomicroscopy. Nature 424:643-650.
47. Zhu, Q., Dabi, T., Beeche, A., Yamamoto, R., Lawton, M. A., and Lamb, C. 1995. Cloning and properties of a rice gene encoding phenylalanine ammonia-lyase. Plant Mol. Biol. 29:535-550.