Rhizoxin analogs contribute to the biocontrol activity of a newly isolated Pseudomonas strain

Molecular Plant-Microbe Interactions

Volumn 28, Issue 3, 2015, Pages 333-342

  Takeuchi, Kasumi ^a   Noda, Naomi ^a   Katayose, Yuichi ^a   Mukai, Yoshiyuki ^a   Numa, Hisataka ^a   Yamada, Kosumi ^b   Someya, Nobutaka ^c  

^a NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

^b UNIVERSITY OF TSUKUBA   (Japan)

^c FOOD RESEARCH INSTITUTE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

PSEUDOMONAS; PSEUDOMONAS SP.; SOLANUM TUBEROSUM;

2,4-DIACETYLPHLOROGLUCINOL; ANTIINFECTIVE AGENT; BACTERIAL PROTEIN; BIOLOGICAL CONTROL AGENT; HYBRID PROTEIN; MACROLIDE; PHLOROGLUCINOL; POLYKETIDE SYNTHASE; RHIZOXIN;

ANALOGS AND DERIVATIVES; ANTIBIOSIS; BACILLUS; BACTERIAL GENOME; BIOLOGICAL CONTROL AGENT; CHEMISTRY; CUCUMBER; DNA SEQUENCE; DRUG EFFECTS; FUSARIUM; GENETICS; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; MULTIGENE FAMILY; NUCLEOTIDE SEQUENCE; PLANT DISEASE; PLANT ROOT; PREVENTION AND CONTROL; PSEUDOMONAS; PYTHIUM; REPORTER GENE; RHIZOSPHERE; SPECIES DIFFERENCE;

ANTI-BACTERIAL AGENTS; ANTIBIOSIS; BACILLUS; BACTERIAL PROTEINS; BASE SEQUENCE; BIOLOGICAL CONTROL AGENTS; CUCUMIS SATIVUS; FUSARIUM; GENES, REPORTER; GENOME, BACTERIAL; MACROLIDES; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; PHLOROGLUCINOL; PLANT DISEASES; PLANT ROOTS; POLYKETIDE SYNTHASES; PSEUDOMONAS; PYTHIUM; RECOMBINANT FUSION PROTEINS; RHIZOSPHERE; SEQUENCE ANALYSIS, DNA; SPECIES SPECIFICITY;

EID: 84923205399     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-09-14-0294-FI     Document Type: Article

References (47)

1. Altschul, S. F., Gish, W., Miller, W., Myers, E. W., and Lipman, D. J. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
2. Bertels, F., Silander, O. K., Pachkov, M., Rainey, P. B., and Nimwegen, E. 2014. Automated reconstruction of whole-genome phylogenies from short sequence reads. Mol. Biol. Evol. 31:1077-1088.
3. Blin, K., Medema M. H, Kazempour, D., Fischbach, M. A., Breitling, R., Takano, E., and Weber, T. 2013. antiSMASH 2. 0-a versatile platform for genome mining of secondary metabolite producers. Nucleic Acids Res. 41:W204-W212.
4. 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.
5. Duffy, B. K., and Défago, G. 1999. Environmental factors modulating antibiotic and siderophore biosynthesis by Pseudomonas fluorescens biocontrol strains. Appl. Environ. Microbiol. 65:2429-2438.
6. 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.
7. Gross, H., and Loper, J. E. 2009. Genomics of secondary metabolite production by Pseudomonas spp. Nat. Prod. Rep. 26:1408-1466.
8. Gross, H., Stockwell, V. O., Henkels, M. D., Nowak-Thompson, B., Loper, J. E., and Gerwick, W. H. 2007. The genomisotopic approach: A systematic method to isolate products of orphan biosynthetic gene clusters. Chem. Biol. 14:53-63.
9. Haas, D., and Défago, G. 2005. Biological control of soil-borne pathogens by fluorescent pseudomonads. Nat. Rev. Microbiol. 3:307-319.
10. Haas, D., and Keel, C. 2003. Regulation of antibiotic production in rootcolonizing Pseudomonas spp. and relevance for biological control of plant disease. Annu. Rev. Phytopathol. 41:117-153.
11. Hassan, K. A., Johnson, A., Shaffer, B. T., Ren, Q., Kidarsa, T. A., Elbourne, L. D. H., Hartney, S., Duboy, R., Goebel, N. C., Zabriskie, T. M., Paulsen, I. T., and Loper, J. E. 2010. Inactivation of the GacA response regulator in Pseudomonas fluorescens Pf-5 has far-reaching transcriptomic consequences. Environ. Microbiol. 12:899-915.
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.
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.
14. 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.
15. Iwasaki, S., Kobayashi, H., Furukawa, J., Namikoshi, M., Okuda, S., Sato, Z., Matsuda, I., and Noda, T. 1984. Studies on macrocyclic lactone antibiotics. VII. Structure of a phytotoxin "rhizoxin" produced by Rhizopus chinensis. J. Antibiot. 37:354-362.
16. Johansson, P. M., and Wright, S. A. 2003. Low-temperature isolation of disease-suppressive bacteria and characterization of a distinctive group of pseudomonads. Appl. Environ. Microbiol. 69:6464-6474.
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.
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.
19. Keel, C., Schnider, U., Maurhofer, M., Voisard, C., Laville, J., Burger, U., Wirthner, P., Haas, D., and Défago, G. 1992. Suppression of root diseases by Pseudomonas fluorescens CHA0: Importance of the bacterial secondary metabolite 2,4-diacetylphloroglucinol. Mol. Plant-Microbe Interact. 5:4-13.
20. 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 fluorescens Pf-5. Mol. Microbiol. 81:395-414.
21. Kim, Y. C., Leveau, J., McSpadden Gardener, B. B., Pierson, E. A., Pierson, L. S., III, and Ryu, C. M. 2011. The multifactorial basis for plant health promotion by plant-associated bacteria. Appl. Environ. Microbiol. 77:1548-1555.
22. Lackner, G., Moebius, N., Partida-Martinez, L., and Hertweck, C. 2011. Complete genome sequence of Burkholderia rhizoxinica, an endosymbiont of Rhizopus microsporus. J. Bacteriol. 193:783-784.
23. Langille, M. G., Hsiao, W. W., and Brinkman, F. S. 2010. Detecting genomic islands using bioinformatics approaches. Nat. Rev. Microbiol. 8:373-382.
24. Lapouge, K., Schubert, M., Allain, F. H.-T., and Haas, D. 2008. Gac/Rsm signal transduction pathway of-proteobacteria: From RNA recognition to regulation of social behaviour. Mol. Microbiol. 67:241-253.
25. Loper, J. E., Henkels, M. D., Shaffer, B. T., Valeriote, F. A., and Gross, H. 2008. Isolation and identification of rhizoxin analogs from Pseudomonas fluorescens Pf-5 by using a genomic mining strategy. Appl. Environ. Microbiol. 74:3085-3093.
26. Loper, J. E., Hassan, K. A., Mavrodi, D. V., Davis, E. W., II, Lim, C. K., Shaffer, B. T., Elbourne, L. D., Stockwell, V. O., Hartney, S. L., Breakwell, K., Henkels, M. D., Tetu, S. G., Rangel, L. I., Kidarsa, T. A., Wilson, N. L., van de Mortel, J. E., Song, C., Blumhagen, R., Radune, D., Hostetler, J. B., Brinkac, L. M., Durkin, A. S., Kluepfel, D. A., Wechter, W. P., Anderson, A. J., Kim, Y. C., Pierson, L. S., III., Pierson, E. A., Lindow, S. E., Kobayashi, D. Y., Raaijmakers, J. M., Weller, D. M., Thomashow, L. S., Allen, A. E., and Paulsen, I. T. 2012. Comparative genomics of plant-associated Pseudomonas spp.: Insights into diversity and inheritance of traits involved in multitrophic interactions. PLoS Genet. 8:e1002784. Published online.
27. Mao, Y., Varoglu, M., and Sherman, D. H. 1999. Molecular characterization and analysis of the biosynthetic gene cluster for the antitumor antibiotic mitomycin C from Streptomyces lavendulae NRRL 2564. Chem. Biol. 6:251-263.
28. 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.
29. Miller, J. H. 1972. Experiments in Molecular Genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, U. S. A.
30. Partida-Martinez, L. P., and Hertweck, C. 2005. Pathogenic fungus harbours endosymbiotic bacteria for toxin production. Nature 437:884-888.
31. Partida-Martinez, L. P., and Hertweck, C. 2007. A gene cluster encoding rhizoxin biosynthesis in "Burkholderia rhizoxina", the bacterial endosymbiont of the fungus Rhizopus microspores. Chem. Biochem. 8:41-45.
32. Paulsen, I. T., Press, C. M., Ravel, J., Kobayashi, D. Y., Myers, G. S., Mavrodi, D. V., DeBoy, R. T., Seshadri, R., Ren, Q., Madupu, R., Dodson, R. J., Durkin, A. S., Brinkac, L. M., Daugherty, S. C., Sullivan, S. A., Rosovitz, M. J., Gwinn, M. L., Zhou, L., Schneider, D. J., Cartinhour, S. W., Nelson, W. C., Weidman, J., Watkins, K., Tran, K., Khouri, H., Pierson, E. A., Pierson, L. S., III,, Thomashow, L. S., and Loper, J. E. 2005. Complete genome sequence of the plant commensal Pseudomonas fluorescens Pf-5. Nat. Biotechnol. 23:873-878.
33. Péchy-Tarr, M., Bruck, D. J., Maurhofer, M., Fischer, E., Vogne, C., Henkels, M. D., Donahue, K. M., Grunder, J., Loper, J. E., and Keel, C. 2008. Molecular analysis of a novel gene cluster encoding an insect toxin in plant-associated strains of Pseudomonas fluorescens. Environ. Microbiol. 10:2368-2386.
34. 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.
35. Richter, M., and Rosselló-Móra, R. 2009. Shifting the genomic gold standard for the prokaryotic species definition. Proc. Natl. Acad. Sci. U. S. A. 106:19126-19131.
36. Sambrook, J., Russell, D. W., and Irwin, N. 2001. Molecular Cloning: A Laboratory Manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, U. S. A. .
37. 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.
38. Schubert, M., Lapouge, K., Duss, O., Oberstrass, F. C., Jelesarov, I., Haas, D., and Allain, F. H. 2007. Molecular basis of messenger RNA recognition by the specific bacterial repressing clamp RsmA/CsrA. Nat. Struct. Mol. Biol. 14:807-813.
39. Someya, N., Morohoshi, T., Ikeda, T., Tsuchiya, K., and Ikeda, S. 2012. Genetic diversity and ecological evaluation of fluorescent pseudomonads isolated from the leaves and roots of potato plants. Microbes Environ. 27:122-126.
40. 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.
41. Takeuchi, K., Yamada, K., and Haas, D. 2012. ppGpp controlled by the Gac/Rsm regulatory pathway sustains biocontrol activity in Pseudomonas fluorescens CHA0. Mol. Plant-Microbe Interact. 25:1440-1449.
42. Takeuchi, K., Noda, N., and Someya, N. 2014. Complete genome sequence of the biocontrol strain Pseudomonas protegens Cab57 discovered in Japan reveals strain-specific diversity of this species. PLoS One 9:e93683. Published online.
43. 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.
44. 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.
45. 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.
46. Winsor, G. L., Lam, D. K., Fleming, L., Lo, R., Whiteside, M. D., Yu, N. Y., Hancock, R. E., and Brinkman, F. S., 2011. Pseudomonas Genome Database: Improved comparative analysis and population genomics capability for Pseudomonas genomes. Nucleic Acids Res. 39:D596-D600.
47. Youard, Z. A., Mislin, G. L., Majcherczyk, P. A., Schalk, I. J., and Reimmann, C. 2007. Pseudomonas fluorescens CHA0 produces enantiopyochelin, the optical antipode of the Pseudomonas aeruginosa siderophore pyochelin. J. Biol. Chem. 282:35546-35553.