Flagella mediate endophytic competence rather than act as MAMPs in rice-Azoarcus sp. strain BH72 interactions

Molecular Plant-Microbe Interactions

Volumn 25, Issue 2, 2012, Pages 191-199

  Buschart, Anna ^a,b   Sachs, Sabrina ^a   Chen, Xi ^a   Herglotz, Julia ^a,c   Krause, Andrea ^a   Reinhold Hurek, Barbara ^a  

^a UNIVERSITY OF BREMEN   (Germany)

^b HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

^c INSTITUTE FOR TUMOR BIOLOGY AND EXPERIMENTAL THERAPY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; FLAGELLIN;

AMINO ACID SEQUENCE; ARTICLE; AZOARCUS; BACTERIAL GENOME; ENDOPHYTE; FLAGELLUM; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETICS; GENOMICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; MUTATION; PHYSIOLOGY; PLANT IMMUNITY; PLANT ROOT; RICE; SEEDLING; SYMBIOSIS; ULTRASTRUCTURE;

AMINO ACID SEQUENCE; AZOARCUS; BACTERIAL PROTEINS; ENDOPHYTES; FLAGELLA; FLAGELLIN; GENE EXPRESSION; GENE EXPRESSION REGULATION, BACTERIAL; GENOME, BACTERIAL; GENOMICS; MOLECULAR SEQUENCE DATA; MUTATION; ORYZA SATIVA; PLANT IMMUNITY; PLANT ROOTS; SEEDLING; SYMBIOSIS;

AZOARCUS; AZOARCUS SP.; BACTERIA (MICROORGANISMS); BETAPROTEOBACTERIA;

EID: 84862965440     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-05-11-0138     Document Type: Article

References (49)

1. Atsumi, T., Maekawa, Y., Yamada, T., Kawagishi, I., Imae, Y., and Homma, M. 1996. Effect of viscosity on swimming by the lateral and polar flagella of Vibrio alginolyticus. J. Bacteriol. 178:5024-5026. (Pubitemid 26321308)
2. Ausubel, F. M., Brent, R., Kingston, R. E., Moore, D. D., Seidman, J. G., Smith, J. A., and Struhl, K. 1987. Current protocols in molecular biology. John Wiley & Sons, New York.
3. Böhm, M., Hurek, T., and Reinhold-Hurek, B. 2007. Twitching motility is essential for endophytic rice colonization by the N2-fixing endophyte Azoarcus sp. strain BH72. Mol. Plant-Microbe Interact. 20:526-533. (Pubitemid 46641430)
4. Capdevila, S., Martinez-Granero, F. M., Sanchez-Contreras, M., Rivilla, R., and Martin, M. 2004. Analysis of Pseudomonas fluorescens F113 genes implicated in flagellar filament synthesis and their role in competitive root colonization. Microbiol. 150:3889-3897. (Pubitemid 39545333)
5. 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.
6. Cooley, M. B., Miller, W. G., and Mandrell, R. E. 2003. Colonization of Arabidopsis thaliana with Salmonella enterica and enterohemorrhagic Escherichia coli O157:H7 and competition by Enterobacter asburiae. Appl. Environ. Microbiol. 69:4915-4926. (Pubitemid 36992957)
7. Darzins, A. 1993. The pilG gene product, required for Pseudomonas aeruginosa pilus production and twitching motility, is homologous to the enteric, single-domain response regulator CheY. J. Bacteriol. 175:5934-5944. (Pubitemid 23277442)
8. Dörr, J., Hurek, T., and Reinhold-Hurek, B. 1998. Type IV pili are involved in plant-microbe and fungus-microbe interactions. Mol. Microbiol. 30:7-17. (Pubitemid 28446616)
9. Egener, T., Hurek, T., and Reinhold-Hurek, B. 1998. Use of green fluorescent protein to detect expression of nif genes of Azoarcus sp. BH72, a grass-associated diazotroph, on rice roots. Mol. Plant-Microbe Interact. 11:71-75. (Pubitemid 28158968)
10. Egener, T., Hurek, T., and Reinhold-Hurek, B. 1999. Endophytic expression of nif genes of Azoarcus sp. strain BH72 in rice roots. Mol. Plant-Microbe Interact. 12:813-819. (Pubitemid 29402958)
11. Felix, G., and Boller, T. 2003. Molecular sensing of bacteria in plants. The highly conserved RNA-binding motif RNP-1 of bacterial cold shock proteins is recognized as an elicitor signal in tobacco. J. Biol. Chem. 278:6201-6208. (Pubitemid 36800875)
12. 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. The Plant Journal 18:265-276.
13. Figurski, D. H., and Helinski, D. R. 1979. Replication of an origincontaining derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc. Natl. Acad. Sci. U.S.A. 76:1648-1652. (Pubitemid 9175374)
14. 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. (Pubitemid 39098887)
15. Gomez-Gomez, 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.
16. Harshey, R. M. 1994. Bees aren't the only ones: Swarming in gramnegative bacteria. Mol. Microbiol. 13:389-394. (Pubitemid 24260068)
17. Hossain, M. M., Shibata, S., Aizawa, S.-I., and Tsuyumu, S. 2005. Motility is an important determination for pathogenesis of Erwinia carotovora subsp. carotovora. Physiol. Mol. Plant Pathol. 66:134-143. (Pubitemid 41406046)
18. Hurek, T., and Reinhold-Hurek, B. 2003. Azoarcus sp. strain BH72 as a model for nitrogen-fixing grass endophytes. J. Biotechnol. 106:169-178. (Pubitemid 37494855)
19. Hurek, T., Reinhold-Hurek, B., Van Montagu, M., and Kellenberger, E. 1994. Root colonization and systemic spreading of Azoarcus sp. Strain BH72 in grasses. J. Bacteriol. 176:1913-1923. (Pubitemid 24103539)
20. Hurek, T., Van Montagu, M., Kellenberger, E., and Reinhold-Hurek, B. 1995. Induction of complex intracytoplasmic membranes related to nitrogen fixation in Azoarcus sp. BH72. Mol. Microbiol. 18:225-236.
21. Hurek, T., Egener, T., and Reinhold-Hurek, B. 1997. Divergence in nitrogenases of Azoarcus spp., Proteobacteria of the β-subclass. J. Bacteriol. 179:4172-4178. (Pubitemid 27291045)
22. Hurek, T., Handley, L., Reinhold-Hurek, B., and Piché, Y. 2002. Azoarcus grass endophytes contribute fixed nitrogen to the plant in an unculturable state. Mol. Plant-Microbe Interact. 15:233-242. (Pubitemid 34262133)
23. Iniguez, A. L., Dong, Y., Carter, H. D., Ahmer, B. M. M., Stone, J. M., and Triplett, E. W. 2005. Regulation of enteric endophytic bacterial colonization by plant defenses. Mol. Plant-Microbe Interact. 18:169-178.
24. Jones, J. D., and Dangl, J. L. 2006. The plant immune system. Nature 444:323-329. (Pubitemid 44764102)
25. Kawagishi, I., Müller, V., Williams, A. W., Irikuray, V. M., and Macnab, R. M. 1992. Subdivision of flagellar region I11 of the Escherichia coli and Salmonella typhimurium chromosomes and identification of two additional flagellar genes. J. Gen. Microbiol. 138:1051-1065.
26. Krause, A., Ramakumar, A., Bartels, D., Battistoni, F., Bekel, T., Boch, J., Böhm, M., Friedrich, F., Hurek, T., Krause, L., Linke, B., McHardy, A., Sarkar, A., Schneiker, S., Syed, A. A., Thauer, R., Vorhölter, F., Weidner, S., Pühler, A., Reinhold-Hurek, B., Kaiser, A., and Goesmann, A. 2006. Genomic insights into the lifestyle of the mutualistic, N2- fixing grass endophyte Azoarcus sp. strain BH72. Nat. Biotechnol. 24:1385-1391. (Pubitemid 44722102)
27. Krause, A., Leyser, B., Miché, L., Battistoni, F., and Reinhold-Hurek, B. 2011. Exploring the function of alcohol dehydrogeanses during the endophytic life of Azoarcus sp. strain BH72. Mol. Plant-Microbe Interact. 24:1325-1332.
28. 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. (Pubitemid 41096021)
29. Mattick, J. S. 2002. Type IV pili and twitching motility. Annu. Rev. Microbiol. 56:289-314. (Pubitemid 35217457)
30. Medzhitov, R., and Janeway, C. A., Jr. 2002. Decoding the patterns of self and nonself by the innate immune system. Science 296:298-300. (Pubitemid 34303673)
31. Pfund, C., Tans-Kersten, J., Dunning, F. M., Alonso, J. M., Ecker, J. R., Allen, C., and Bent, A. F. 2004. Flagellin is not a major defense elicitor in Ralstonia solanacearum cells or extracts applied to Arabidopsis thaliana. Mol. Plant-Microbe Interact. 17:696-706. (Pubitemid 38642213)
32. Reinhold, B., Hurek, T., and Fendrik, I. 1985. Strain-specific chemotaxis of Azospirillum spp. J. Bacteriol. 162:190-195.
33. Reinhold, B., Hurek, T., Niemann, E.-G., and Fendrik, I. 1986. Close association of Azospirillum and diazotrophic rods with different root zones of Kallar grass. Appl. Environ. Microbiol. 52:520-526.
34. Reinhold-Hurek, B., and Hurek, T. 1998. Life in grasses: Diazotrophic endophytes. Trends Microbiol. 6:139-144. (Pubitemid 28197802)
35. Reinhold-Hurek, B., and Hurek, T. 2011. Living inside plants: Bacterial endophytes. Curr. Opin. Plant Biol. 14:435-443.
36. Reinhold-Hurek, B., Hurek, T., Gillis, M., Hoste, B., Vancanneyt, M., Kersters, K., and De Ley, J. 1993. Azoarcus gen. nov., nitrogen-fixing proteobacteria associated with roots of Kallar grass (Leptochloa fusca (L.) Kunth) and description of two species Azoarcus indigens sp. nov. and Azoarcus communis sp. nov. Int. J. Syst. Bacteriol. 43:574-584. (Pubitemid 23210440)
37. Reinhold-Hurek, B., Maes, T., Gemmer, S., Van Montagu, M., and Hurek, T. 2006. An endoglucanase is involved in infection of rice roots by the not cellulose-metabolizing endophyte Azoarcus sp. BH72. Mol. Plant- Microbe Interact. 19:181-188. (Pubitemid 43172832)
38. Rodriguez-Navarro, D. N., Dardanelli, M. S., and Ruiz-Sainz, J. E. 2007. Attachment of bacteria to the roots of higher plants. FEMS Microbiol. Lett. 272:127-136. (Pubitemid 47074607)
39. Schäfer, A., Tauch, A., Jager, W., Kalinowski, J., Thierbach, G., and Puhler, A. 1994. Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: Selection of defined deletions in the chromosome of Corynebacterium glutamicum. Gene 145:69-73. (Pubitemid 24224965)
40. Scharf, B., Schuster-Wolff-Buhring, H., Rachel, R., and Schmitt, R. 2001. Mutational analysis of the Rhizobium lupini H13-3 and Sinorhizobium meliloti flagellin genes: Importance of flagellin A for flagellar filament structure and transcriptional regulation. J. Bacteriol. 183:5334-5342. (Pubitemid 32802605)
41. Shinoda, S., and Okamoto, K. 1977. Formation and function of Vibrio parahaemolyticus lateral flagella. J. Bacteriol. 129:1266-1271. (Pubitemid 8109664)
42. 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. Biotech. Biochem. 71:590-593.
43. 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.
44. Takakura, Y., Che, F. S., Ishida, Y., Tsutsumi, F., Kurotani, K., Usami, S., Isogai, A., and Imaseki, H. 2008. Expression of a bacterial flagellin gene triggers plant immune responses and confers disease resistance in transgenic rice plants. Mol. Plant Pathol. 9:525-529. (Pubitemid 351832403)
45. Tans-Kersten, J., Huang, H., and Allen, C. 2001. Ralstonia solanacearum needs motility for invasive virulence on tomato. J. Bacteriol. 183:3597-3605. (Pubitemid 32510427)
46. Thuerig, B., Felix, G., Binder, A., Boller, T., and Tamm, L. 2006. An extract of Penicillium chrysogenum elicits early defense-related responses and induces resistance in Arabidopsis thaliana independently of known signalling pathways. Physiol. Mol. Plant Pathol. 67:180-193. (Pubitemid 43810178)
47. Yokoseki, T., Kutsukake, K., Ohnishi, K., and lino, T. 1995. Functional analysis of the flagellar genes in the fliD operon of Salmonella typhimurium. Microbiol. 141:1715-1722.
48. Zipfel, C. 2009. Early molecular events in PAMP-triggered immunity. Curr. Opin. Plant Biol. 12:414-420.
49. The Sanger Institute's Pfam database: pfam.sanger.ac.uk