Control of fusarium wilt of radish by combining Pseudomonas putida strains that have different disease-suppressive mechanisms

Phytopathology

Volumn 93, Issue 5, 2003, Pages 626-632

  De Boer, Marjan ^a   Bom, Peter ^a   Kindt, Frodo ^a   Keurentjes, Joost J B ^a   Van Der Sluis, Ientse ^a   Van Loon, L C ^a   Bakker, Peter A H M ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA (MICROORGANISMS); FUNGI; FUSARIUM; PSEUDOMONAS; PSEUDOMONAS PUTIDA; RAPHANUS SATIVUS;

EID: 0037406650     PISSN: 0031949X     EISSN: None     Source Type: Journal    
DOI: 10.1094/PHYTO.2003.93.5.626     Document Type: Article

References (59)

1. Alabouvette, C., Schippers, B., Lemanceau, P., and Bakker, P. A. H. M. 1998. Biological control of fusarium wilts. Pages 15-36 in: Plant-Microbe Interactions and Biological Control. G. J. Boland and L. D. Kuykendall, eds. Marcel Dekker, New York.
2. Anjaiah, V., Koedam, N., Nowak-Thompson, B., Loper, J. E., Höfte, M., Tambong, J. T., and Cornelis, P. 1998. Involvement of phenazines and anthranilate in the antagonism of Pseudomonas aeruginosa PNA1 and Tn5 derivatives toward Fusarium spp. and Pythium spp. Mol. Plant-Microbe Interact. 11:847-854.
3. Bakker, P. A. H. M., Weisbeek, P. J., and Schippers, B. 1988. Siderophore production by plant growth-promoting Pseudomonas spp. J. Plant Nutr. 11:925-933.
4. Camprubí, A., Calvet, C., and Estaún. V. 1995. Growth enhancement of Citrus reshni after inoculation with Glomus intraradices and Trichoderma aureoviride and associated effects on microbial populations and enzyme activity in potting mixes. Plant Soil 173:233-238.
5. Chin-A-Woeng, T. F. C., Bloemberg, G. V., Van der Bij, A. J., Van der Drift, K. M. G. F., Schripsema, J., Kroon, B., Scheffer, R. J., Keel, C., Bakker, P. A. H. M., Tichy, H. V., De Bruijn, F. J., Thomas-Oates, J. E., and Lugtenberg, B. J. J. 1998. Biocontrol by phenazine-1-carboxamide-producing Pseudomonas chlororaphis PCL1391 of tomato root rot caused by Fusarium oxysporum f. sp. radicis-lycopersici. Mol. Plant-Microbe Interact, 11:1069-1077.
6. Couteaudier, Y., and Alabouvette, C. 1990. Quantitative comparison of Fusarium oxysporum competitiveness in relation to carbon utilization. FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Ecol. 74:261-268.
7. De Boer, M., Van der Sluis, I., Van Loon, L. C., and Bakker, P. A. H. M. 1999. Combining fluorescent Pseudomonas spp. strains to enhance suppression of fusarium wilt of radish. Eur. J. Plant Patrol. 105:201-210.
8. Duffy, B. K., and Weller, D. M. 1995. Use of Gaeumannomyces graminis var. graminis alone and in combination with fluorescent Pseudomonas spp. to suppress take-all of wheat. Plant Dis. 79:907-911.
9. Duijff, B. J., Recorbet, G., Bakker, P. A. H. M., Loper, J. E., and Lemanceau, P. 1999. Microbial antagonism at the root level is involved in the suppression of fusarium wilt by the combination of nonpathogenic Fusarium oxysporum Fo47 and Pseudomonas putida WCS358. Phytopathology 89:1073-1079.
10. Dunne, C., Moenne-Loccoz, Y., McCarthy, J., Higgins, P., Powell, J., Dowling, D. N., and O'Gara, F. 1998. Combining proteolytic and phloroglucinol-producing bacteria for improved biocontrol of Pythium-mediated damping-off of sugar beet. Plant Pathol. 47:299-307.
11. Elad, Y., and Baker, R. 1985. The role of competition for iron and carbon in suppression of chlamydospore germination of Fusarium spp. by Pseudomonas spp. Phytopathology 75:1053-1059.
12. Fuchs, J. G., Moenne-Loccoz, Y., and Défago, G. 1997. Nonpathogenic Fusarium oxysporum strain Fo47 induces resistance to fusarium wilt in tomato. Plant Dis. 81:492-496.
13. Geels, F. P., and Schippers, B. 1983. Selection of antagonistic fluorescent Pseudomonas spp. and their root colonization and persistence following treatment of seed potatoes. Phytopathol. Z. 180:193-206.
14. Glandorf, D. C. M., Brand I., Bakker, P. A. H. M., and Schippers, B. 1992. Stability of rifampicin resistance as a marker for root colonization studies of Pseudomonas putida in the field. Plant Soil 147:135-142.
15. Guetsky, R., Shtienberg, D., Elad, Y., and Dinoor, A. 2001. Combining biocontrol agents to reduce the variability of biological control. Phytopathology 91:621-627.
16. Guetsky, R., Shtienberg, D., Elad, Y., Fischer, E., and Dinoor, A. 2002. Improving biological control by combining biocontrol agents each with several mechanisms of disease suppression. Phytopathology 92:976-985.
17. Handelsman, J., and Stabb, E. V. 1996. Biocontrol of soilborne plant pathogens. Plant Cell 8:1855-1869.
18. Hoagland, D. R., and Amon, D. I. 1938. The water culture method for growing plants without soil. Bull. Calif. Agric. Exp. Stn. 347:36-39.
19. Höfflich, G., Wiehe, W., and Kühn, G. 1994. Plant growth stimulation by inoculation with symbiotic and associative rhizosphere microorganisms. Experientia 50:897-905.
20. Janisiewicz, W. J., and Bors, B. 1995. Development of a microbial community of bacterial and yeast antagonists to control wound-invading postharvest pathogens of fruits. Appl. Environ. Microbiol. 61:3261-3267.
21. Jetiyanon, K., and Kloepper, J. W. 2002. Mixtures of plant growth-promoting rhizobacteria for induction of resistance against multiple plant diseases. Biol. Control 24:285-291.
22. Jorgensen, R. A., Rothstein, S. J., and Reznikoff, W. S. 1979. A restriction enzyme cleavage map of Tn5 and location of a region encoding neomycin resistance. Mol. Gen. Genet. 177:65-72.
23. King, E. O., Ward, M. K., and Raney, D. E. 1954. Two simple media for the demonstration of pyocyanin and fluorescin. J. Lab. Clin. Med. 44:301-307.
24. Kragelund, L., and Nybroe, O. 1996. Competition between Pseudomonas fluorescens Ag1 and Alcaligenes eutrophus JMP134 (pJP4) during colonization of barley roots. FEMS Microbiol. Ecol. 20:41-51.
25. Lamers, J. B., Schippers, B., and Geels, F. P. 1988. Soilborne disease of wheat in the Netherlands and results of seed bacterization with pseudomonads against Gaeumannomyces graminis var. tritici. Pages 134-139 in: Cereal Breeding Related to Integrated Production. M. L. Jorna and L. A. Slootmaker, eds. Pudoc, Wageningen, the Netherlands.
26. Leeman, M., Den Ouden, F. M., van Pelt, J. A., Cornelissen, C., Matamala-Garros, A., Bakker, P. A. H. M., and Schippers, B. 1996. Suppression of fusarium wilt of radish by co-inoculation of fluorescent Pseudomonas spp. and root-colonizing fungi. Eur. J. Plant Pathol. 102:21-31.
27. Leeman, M., Den Ouden, F. M., van Pelt, J. A., Dirkx, F. P. M., Steijl, H., Bakker, P. A. H. M., and Schippers, B. 1996. Iron availability affects induction of systemic resistance to fusarium wilt of radish by Pseudomonas fluorescens. Phytopathology 86:149-155.
28. Leeman, M., Raaijmakers, J. M., Bakker, P. A. H. M, and Schippers, B. 1991. Immunofluorescence colony-staining for monitoring pseudomonads introduced into soil. Pages 374-380 in: Biotic Interactions and Soilborne Diseases. A. B. R. Beemster, G. J. Bollen, M. Gerlagh, M. A. Ruisen, B. Schippers, and A. Tempel, eds. Elsevier, Amsterdam.
29. Leeman, M., Van Pelt, J. A., Den Ouden, F. M., Heinsbroek, M., Bakker, P. A. H. M., and Schippers, B. 1995. Induction of systemic resistance by Pseudomonas fluorescens in radish cultivars differing in susceptibility to fusarium wilt, using a novel bioassay. Eur. J. Plant Pathol. 101:655-664.
30. Leeman, M., Van Pelt, J. A., Hendrickx, M. J., Scheffer, R. J., Bakker, P. A. H. M., and Schippers, B. 1995. Biocontrol of fusarium wilt of radish in commercial greenhouse trials by seed treatment with Pseudomonas fluorescens WCS374. Phytopathology 85:1301-1305.
31. Lemanceau, P., Bakker, P. A. H. M., De Kogel, W. J., Alabouvette, C., and Schippers, B. 1992. Effect of pseudobactin 358 production by Pseudomonas putida WCS358 on suppression of fusarium wilt of carnations by nonpathogenic Fusarium oxysporum Fo47. Appl. Environ. Microbiol. 58:2978-2982.
32. Lemanceau, P., Bakker, P. A. H. M., De Kogel, W. J., Alabouvette, C., and Schippers, B. 1993. Antagonistic effect of nonpathogenic Fusarium oxysporum Fo47 and pseudobactin 358 upon pathogenic Fusarium oxysporum f. sp. dianthi. Appl. Environ. Microbiol. 59:74-82.
33. Lindow, S. E. 1990. Bacterial ice-nucleation activity. Pages 185-198 in: Methods in Phytobacteriology. Z. Klement, K. Rudolf, and D. C. Sands, eds. Akadémiai Kiadó, Budapest, Hungary.
34. Loper, J. E., and Henkels, M. D. 1997. Availability of iron to Pseudomonas fluorescens in rhizosphere and bulk soil evaluated with an ice nucleation reporter gene. Appl. Environ. Microbiol. 63:99-105.
35. Loper, J. E., and Henkels, M. D. 1999. Utilization of heterologous siderophores enhances levels of iron available of Pseudomonas putida in the rhizosphere. Appl. Environ. Microbiol. 65:5357-5363.
36. Loper, J. E., and Lindow, S. E. 1994. A biological sensor for iron available to bacteria in their habitats on plant surfaces. Appl. Environ. Microbiol. 60:1934-1941.
37. Loper, J. E., Suslow, T. V., and Schroth, M. N. 1984. Lognormal distribution of bacterial populations in the rhizosphere. Phytopathology 74:1454-1460.
38. Mao, W., Lewis, J. A., Lumsden, R. D., and Hebbar, K. P. 1998. Biocontrol of selected soilborne diseases of tomato and pepper plants. Crop Prot. 17:535-542.
39. Marugg, J. D., Van Spanje, M., Hoekstra, W. P. M., Schippers, B., and Weisbeek, P. J. 1985. Isolation and analysis of genes involved in siderophore biosynthesis in plant growth-stimulating Pseudomonas putida WCS358. J. Bacteriol. 164:563-570.
40. Mercado-Banco, J., Van der Drift, K. M. G. M., Olsson, P. E., Thomas-Oates, J. E., Van Loon, L. C., and Bakker, P. A. H. M. 2001. Analysis of the pmsCEAB gene cluster involved in biosynthesis of salicylic acid and the siderophore pseudomonine in the biocontrol strain Pseudomonas fluorescens WCS374. J. Bacteriol. 183:1909-1920.
41. Meyer, J. M., and Abdallah, M. A. 1978. The fluorescent pigment of Pseudomonas fluorescens: Biosynthesis, purification and physico-chemical properties. J. Gen. Microbiol. 107:319-328.
42. Miller, J. H. 1972. Experiments in Molecular Genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
43. Pierson, E. A., and Weller, D. M. 1994. Use of mixtures of fluorescent pseudomonads to suppress take-all and improve the growth of wheat. Phytopathology 84:940-947.
44. Pieterse, C. M. J., Van Wees, S. C. M., Van Pelt, J. A., Knoester, M., Laan, R., Gerrits, H., Weisbeek, P. J., and Van Loon, L. C. 1998. A novel signaling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell 10:1571-1580.
45. Raaijmakers, J. M. 1994. Microbial interactions in the rhizosphere: Root colonization by Pseudomonas spp. and suppression of fusarium wilt. Ph.D. diss. Utrecht University, Utrecht, the Netherlands.
46. Raaijmakers, J. M., Leeman, M., Van Oorschot, M. M. P., Van der Sluis, I., Schippers, B., and Bakker, P. A. H. M. 1995. Dose-response relationships in biological control of fusarium wilt of radish by Pseudomonas spp. Phytopathology 85:1075-1081.
47. Raaijmakers, J. M., van der Sluis, I., Koster, M., Bakker, P. A. H. M., Weisbeek, P. J., and Schippers, B. 1995. Utilization of heterologous siderophores and rhizosphere competence of fluorescent Pseudomonas spp. Can. J. Microbiol 41:126-135.
48. Raupach, G. S., and Kloepper, J. W. 1998. Mixtures of plant growth-promoting rhizobacteria enhance biological control of multiple cucumber pathogens. Phytopathology 88:1158-1164.
49. Schippers, B. 1992. Prospects for management of natural suppressiveness to control soilborne pathogens. Pages 21-34 in: Biological Control of Plant Diseases, Progress and Challenges For the Future. E. C. Tjamos, G. C. Papavizas, and R. J. Cook, eds. Plenum Press, New York.
50. Schippers, B., Bakker, A. W., and Bakker, P. A. H. M. 1987. Interactions of deleterious and beneficial rhizosphere microorganisms and the effect of cropping practices. Annu. Rev. Phytopathol. 25:339-358.
51. Schisler, D. A., Slininger, P. J., and Bothast, R. J. 1997. Effects of antagonist cell concentration and two-strain mixtures on biological control of fusarium dry rot of potatoes. Phytopathology 87:177-183.
52. Schwyn, B., and Neilands, J. B. 1987. Universal chemical assay for the detection and determination of siderophores. Anal. Biochem 160:47-56.
53. Singh, P. P., Shin, Y. C., Park, C. S., and Chung, Y. R. 1999. Biological control of fusarium wilt of cucumber by chitinolytic bacteria. Phytopathology 89:92-99.
54. Sung, K. C., and Chung, Y. R. 1997. Enhanced suppression of rice sheath blight using combination of bacteria which produce chitinases or antibiotics. Pages 370-372 in: Plant Growth-Promoting Rhizobacteria: Present Status and Future Prospects. A. Ogoshi, K. Kobayashi, Y. Homma, F. Kodama, N. Kondo, and S. Akino, eds. Faculty of Agriculture, Hokkaido University, Sapporo, Japan.
55. Van Loon, L. C., Bakker, P. A H. M., and Pieterse, C. M. J. 1998. Systemic resistance induced by rhizosphere bacteria. Annu. Rev. Phytopathol. 36:453-483.
56. Van Peer, R., Niemann, G. J., and Schippers, B. 1991. Induced resistance and phytoalexin accumulation in biological control of fusarium wilt of carnation by Pseudomonas sp. WCS417r. Phytopathology 81:728-734.
57. Van Vuurde, J. W. L. 1990. Immunofluorescence colony staining. Pages 299-305 in: Serological Methods for Detection and Identification of Viral and Bacterial Plant Pathogens. R. Hampton, E. Ball, and S. De Boer, eds. The American Phytopathological Society, St. Paul, MN.
58. Van Wees, S. C. M., Pieterse, C. M. J., Trijssenaar, A., Van 't Westende. Y. A. M., Hartog, F., and Van Loon, L. C. 1997. Differential induction of systemic resistance in Arabidopsis by biocontrol bacteria. Mol. Plant-Microbe Interact. 10:716-724.
59. Weller, D. M. 1988. Biological control of soilborne plant pathogens in the rhizosphere with bacteria. Annu. Rev. Phytopathol. 26:379-407.