PpGpp controlled by the Gac/Rsm regulatory pathway sustains biocontrol activity in Pseudomonas fluorescens CHA0

Molecular Plant-Microbe Interactions

Volumn 25, Issue 11, 2012, Pages 1440-1449

  Takeuchi, Kasumi ^a   Yamada, Kosumi ^b   Haas, Dieter ^c  

^a NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

^b UNIVERSITY OF TSUKUBA   (Japan)

^c UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

GUANOSINE 3' DIPHOSPHATE 5' DIPHOSPHATE;

ARTICLE; CAPILLARY ELECTROPHORESIS; CUCUMBER; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PSEUDOMONAS FLUORESCENS;

CUCUMIS SATIVUS; ELECTROPHORESIS, CAPILLARY; GENE EXPRESSION REGULATION, BACTERIAL; GUANOSINE TETRAPHOSPHATE; PSEUDOMONAS FLUORESCENS;

EID: 84867370507     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-02-12-0034-R     Document Type: Article

References (45)

1. Babitzke, P., and Romeo, T. 2007. CsrB sRNA family: sequestration of RNA-binding regulatory proteins. Curr. Opin. Microbiol. 10:156-163. (Pubitemid 46590047)
2. Blumer, C., Heeb, S., Pessi, G., and Haas, D. 1999. Global GacA-steered control of cyanide and exoprotease production in Pseudomonas fluorescens involves specific ribosome binding sites. Proc. Natl. Acad. Sci. U. S. A. 96:14073-14078.
3. Boes, N., Schreiber, K., and Schobert, M. 2008. SpoT-triggered stringent response controls usp gene expression in Pseudomonas aeruginosa. J. Bacteriol. 190:7189-7199.
4. Braeken, K., Moris, M., Daniels, R., Vanderleyden, J., and Michiels, J. 2006. New horizons for (p) ppGpp in bacterial and plant physiology. Trends Microbiol. 14:45-54. (Pubitemid 43063191)
5. Chevrot, R., Rosen, R., Haudecoeur, E., Cirou, A., Shelp, B. J., Ron, E., and Faure, D. 2006. GABA controls the level of quorum-sensing signal in Agrobacterium tumefaciens. Proc. Natl. Acad. Sci. U. S. A. 103:7460-7464. (Pubitemid 43727855)
6. Dalebroux, Z. D., Svensson, S. L., Gaynor, E. C., and Swanson, M. S. 2010. ppGpp conjures bacterial virulence. Microbiol. Mol. Biol. Rev. 74:171-199.
7. Edwards, A. N., Patterson-Fortin, L. M., Vakulskas, C. A., Mercante, J. W., Potrykus, K., Vinella, D., Camacho, M. I., Fields, J. A., Thompson, S. A., Georgellis, D., Cashel, M., Babitzke, P., and Romeo, T. 2011. Circuitry linking the Csr and stringent response global regulatory systems. Mol. Microbiol. 80:1561-1580.
8. Gamper, M., Ganter, B., Polito, M. R., and Haas, D. 1992. RNA processing modulates the expression of the arcDABC operon in Pseudomonas aeruginosa. J. Mol. Biol. 226:943-957.
9. Goodman, A. L., Merighi, M., Hyodo, M., Ventre, I., Filloux, A., and Lory, S. 2009. Direct interaction between sensor kinase proteins mediates acute and chronic disease phenotypes in a bacterial pathogen. Genes Dev. 23:249-259.
10. Haas, D., and Défago, G. 2005. Biological control of soil-borne pathogens by fluorescent pseudomonads. Nat. Rev. Microbiol. 3:307-319. (Pubitemid 40443724)
11. Haas, D., Galimand, M., Gamper, M., and Zimmermann, A. 1990. Arginine network of Pseudomonas aeruginosa: Specific and global controls. Pages 303-316 in: Pseudomonas: Biotransformations, Pathogenesis and Evolving Biotechnology. S. Silver, A. M. Chakrabarty, B. Iglewski, and S. Kaplan, eds. ASM Press, Washington DC.
12. Heeb, S., Itoh, Y., Nishijyo, T., Schnider, U., Keel, C., Wade, J., Walsh, U., O'Gara, F., and Haas, D. 2000. Small, stable shuttle vectors based on the minimal pVS1 replicon for use in gram-negative, plant-associated bacteria. Mol. Plant-Microbe Interact. 13:232-237. (Pubitemid 30061607)
13. Heeb, S., Blumer, C., and Haas, D. 2002. Regulatory RNA as mediator in GacA/RsmA-dependent global control of exoproduct formation in Pseudomonas fluorescens CHA0. J. Bacteriol. 184:1046-1056. (Pubitemid 34113373)
14. Heeb, S., Valverde, C., Gigot-Bonnefoy, C., and Haas, D. 2005. Role of the stress sigma factor RpoS in GacA/RsmA-controlled secondary metabolism and resistance to oxidative stress in Pseudomonas fluorescens CHA0. FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Lett. 243:251-258. (Pubitemid 40164414)
15. Heurlier K., Dénervaud V., Haenni, M., Guy, L., Krishnapillai, V., and Haas, D. 2005. Quorum sensing-negative (lasR) mutants of Pseudomonas aeruginosa avoid cell lysis and death. J. Bacteriol. 187:4875-4883. (Pubitemid 40962204)
16. Humair, B., González, N., Mossialos, D., Reimmann, C., and Haas, D. 2009. Temperature-responsive sensing regulates biocontrol factor expression in Pseudomonas fluorescens CHA0. ISME J. 3:955-965.
17. Kay, E., Dubuis, C., and Haas, D. 2005. Three small RNAs jointly ensure secondary metabolism and biocontrol in Pseudomonas fluorescens CHA0. Proc. Natl. Acad. Sci. U. S. A. 102:17136-17141. (Pubitemid 41692696)
18. Kay, E., Humair, B., Dénervaud, V., Riedel, K., Spahr, S., Eberl, L., Valverde, C., and Haas, D. 2006. Two GacA-dependent small RNAs modulate the quorum-sensing response in Pseudomonas aeruginosa. J. Bacteriol. 188:6026-6033. (Pubitemid 44384112)
19. Kidarsa, T. A., Goebel, N. C., Zabriskie, T. M., and Loper, J. E. 2011. Phloroglucinol mediates cross-talk between the pyoluteorin and 2, 4-diacetylphloroglucinol biosynthetic pathways in Pseudomonas fluoresens Pf-5. Mol. Microbiol. 81:395-414.
20. Kim, Y. C., Leveau, J., McSpadden Gardener, B. B., Pierson, E. A., Pierson, L. S., III, and Ryu, C. M. 2011. The multifacterorial basis for plant health promotion by plant-associated bacteria. Appl. Environ. Microbiol. 77:1548-1555.
21. Lapouge, K., Schubert, M., Allain, F. H.-T., and Haas, D. 2008. Gac/Rsm signal transduction pathway of γ-proteobacteria: from RNA recognition to regulation of social behaviour. Mol. Microbiol. 67:241-253. (Pubitemid 350295835)
22. Laville, J., Voisard, C., Keel, C., Maurhofer, M., Défago, G., and Haas, D. 1992. Global control in Pseudomonas fluorescens mediating antibiotic synthesis and suppression of black root rot of tobacco. Proc. Natl. Acad. Sci. U. S. A. 89:1562-1566.
23. Manuel, J., Berry, C., Selin, C., Fernando, W. G., and de Kievit, T. R. 2011. Repression of the antifungal activity of Pseudomonas sp. strain DF41 by the stringent response. Appl. Environ. Microbiol. 77:5635-5642.
24. Matilla, M. A., Travieso, M. I., Ramos, J. L., and Ramos-González, M. I. 2011. Cyclic diguanylate turnover mediated by the sole GGDEF/EAL response regulator in Pseudomonas putida: its role in the rhizosphere and an analysis of its target processes. Environ. Microbiol. 13:1745-1766.
25. Maurhofer, M., Reimmann, C., Schmidli-Sacherer, P., Heeb, S., Haas, D., and Défago, G. 1998. Salicylic acid biosynthetic genes expressed in Pseudomonas fluorescens strain P3 improve the induction of systemic resistance in tobacco against tobacco necrosis virus. Phytopathology 88:678-684. (Pubitemid 28456094)
26. Miller, J. H. 1972. Experiments in Molecular Genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, U. S. A.
27. Molofsky, A. B., and Swanson, M. S. 2004. Differentiate to thrive: lessons from the Legionella pneumophila life cycle. Mol. Microbiol. 53:29-40. (Pubitemid 38901377)
28. Murphy, H., and Cashel, M. 2003. Isolation of RNA polymerase suppressors of a (p) ppGpp deficiency. Methods Enzymol. 371:596-601. (Pubitemid 37542760)
29. Potrykus, K., and Cashel, M. 2008. (p) ppGpp: still magical? Annu. Rev. Microbiol. 62:35-51.
30. Reimmann, C., Valverde, C., Kay, E., and Haas, D. 2005. Posttranscriptional repression of GacS/GacA-controlled genes by the RNA-binding protein RsmE acting together with RsmA in the biocontrol strain Pseudomonas fluorescens CHA0. J. Bacteriol. 187:276-285. (Pubitemid 40024204)
31. Sambrook, J., and Russell, D. W. 2001. Molecular Cloning: A Laboratory Manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, U. S. A.
32. Schnider-Keel, U., Seematter, A., Maurhofer, M., Blumer, C., Duffy, B., Gigot-Bonnefoy, C., Reimmann, C., Notz, R., Défago, G., Haas, D., and Keel, C. 2000. Autoinduction of 2, 4-diacetylphloroglucinol biosynthesis in the biocontrol agent Pseudomonas fluorescens CHA0 and repression by the bacterial metabolites salicylate and pyoluteorin. J. Bacteriol. 182:1215-1225. (Pubitemid 30104396)
33. Soga, T., and Heiger, D. N. 2000. Amino acid analysis by capillary electrophoresis electrospray ionization mass spectrometry. Anal. Chem. 72:1236-1241. (Pubitemid 30163781)
34. Soga, T., Ueno, Y., Naraoka, H., Ohashi, Y., Tomita, M., and Nishioka, T. 2002. Simultaneous determination of anionic intermediates for Bacillus subtilis metabolic pathways by capillary electrophoresis electrospray ionization mass spectrometry. Anal. Chem. 74:2233-2239. (Pubitemid 34526027)
35. Soga, T., Ohashi, Y., Ueno, Y., Naraoka, H., Tomita, M., and Nishioka, T. 2003. Quantitative metabolome analysis using capillary electrophoresis mass spectrometry. J. Proteome Res. 2:488-494. (Pubitemid 37376843)
36. Stutz, E. W., Défago, G., and Kern, H. 1986. Naturally occurring fluorescent Pseudomonads involved in suppression of black root rot of tobacco. Phytopathology 76:181-185.
37. Sugimoto, M., Wong, D. T., Hirayama, A., Soga, T., and Tomita, M. 2010. Capillary electrophoresis mass spectrometry-based saliva metabolomics identified oral, breast and pancreatic cancer-specific profiles. Metabolomics 6:78-95.
38. Takeuchi, K., Kiefer, P., Reimmann, C., Keel, C., Dubuis, C., Rolli, J., Vorholt, J. A., and Haas, D. 2009. Small RNA-dependent expression of secondary metabolism is controlled by Krebs cycle function in Pseudomonas fluorescens. J. Biol. Chem. 284:34976-34985.
39. Valverde, C., Heeb, S., Keel, C., and Haas, D. 2003. RsmY, a small regulatory RNA, is required in concert with RsmZ for GacA-dependent expression of biocontrol traits in Pseudomonas fluorescens CHA0. Mol. Microbiol. 50:1361-1379. (Pubitemid 37475866)
40. Vogt, S. L., Green, C., Stevens, K. M., Day, B., Erickson, D. L., Woods, D. E., and Storey, D. G. 2011. The stringent response is essential for Pseudomonas aeruginosa virulence in the rat lung agar bead and Drosophila melanogaster feeding models of infection. Infect. Immun. 79:4094-4104.
41. Voisard, C., Rella, M., and Haas, D. 1988. Conjugative transfer of plasmid RP1 to soil isolates of Pseudomonas fluorescens is facilitated by certain large RP1 deletions. FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Lett. 55:9-13.
42. Voisard, C., Bull, C. T., Keel, C., Laville, J., Maurhofer, M., Schnider, U., Défago, G., and Haas, D. 1994. Biocontrol of root diseases by Pseudomonas fluorescens CHA0: current concepts and experimental approaches. Pages 67-89 in: Molecular Ecology of Rhizosphere Microorganisms. F. O'Gara, D. N. Dowling, and B. Boesten, eds. VCH, Weinheim, Germany.
43. Workentine, M. L., Chang, L., Ceri, H., and Turner, R. J. 2009. The GacS-GacA two-component regulatory system of Pseudomonas fluorescens: A bacterial two-hybrid analysis. FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Lett. 292:50-56.
44. Zuber, S., Carruthers, F., Keel, C., Mattart, A., Blumer, C., Pessi, G., Gigot-Bonnefoy, C., Schnider-Keel, U., Heeb, S., Reimmann, C., and Haas, D. 2003. GacS sensor domains pertinent to the regulation of exoproduct formation and to the biocontrol potential of Pseudomonas fluorescens CHA0. Mol. Plant-Microbe Interact. 16:634-644. (Pubitemid 36755625)
45. Zusman, T., Gal-Mor, O., and Segal, G. 2002. Characterization of a Legionella pneumophila relA insertion mutant and roles of RelA and RpoS in virulence gene expression. J. Bacteriol. 184:67-75. (Pubitemid 34003285)