Repeated introduction of genetically modified Pseudomonas putida WCS358r without intensified effects on the indigenous microflora of field-grown wheat

Applied and Environmental Microbiology

Volumn 69, Issue 6, 2003, Pages 3110-3118

  Viebahn, M ^a   Glandorf, D C M ^b   Ouwens, T W M ^a   Smit, E ^b   Leeflang, P ^b   Wernars, K ^b   Thomashow, L S ^c   Van Loon, L C ^a   Bakker, P A H M ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

^b NATIONAL INSTITUTE FOR PUBLIC HEALTH AND THE ENVIRONMENT   (Netherlands)

^c WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; CARBOXYLIC ACIDS; DNA; SEED;

TRANSGENIC DERIVATIVES;

GENETIC ENGINEERING;

ECOLOGICAL IMPACT; GENETICALLY MODIFIED ORGANISM; MICROBIAL COMMUNITY; RHIZOSPHERE; WHEAT;

AMPLIFIED RIBOSOMAL DNA RESTRICTION ANALYSIS; ARTICLE; BACTERIAL COLONIZATION; COLONY FORMING UNIT; GENETICALLY MODIFIED CROP; MICROFLORA; NONHUMAN; POPULATION DYNAMICS; PSEUDOMONAS PUTIDA; RNA GENE; SOIL POLLUTION; STRAIN DIFFERENCE; WHEAT;

BACTERIA (MICROORGANISMS); NEGIBACTERIA; PSEUDOMONAS; PSEUDOMONAS PUTIDA; RHIZOBIALES; SOLANUM TUBEROSUM; TRITICUM AESTIVUM;

EID: 0037980072     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.69.6.3110-3118.2003     Document Type: Article

References (55)

1. Amann, R., B. J. Binder, R. J. Olson, S. W. Chisholm, R. Devereux, and D. A. Stahl. 1990. Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl. Environ. Microbiol. 56:1919-1925.
2. Atlas, R. M., and R. Bartha. 1998. Microbial ecology: fundamentals and applications, 4th ed. Benjamin/Cunnings Science Publishing, Menlo Park, Calif.
3. Bakker, P. A. H. M., J. G. Lamers, A. W. Bakker, J. D. Marugg, P. J. Weisbeek, and B. Schippers. 1986. The role of siderophores in potato tuber yield increase by Pseudomonas putida in short rotation to potato. Neth. J. Plant Pathol. 92:249-256.
4. Bangera, G. M., and L. S. Thomashow. 1996. Characterization of a genomic locus required for synthesis of the antibiotic 2,4-diacetylphloroglucinol by biocontrol control agent Pseudomonas fluorescens Q2-87. Mol. Plant-Microbe Interact. 9:83-90.
5. Bodelier, P. 1997. Nitrification and denitrification in the root zone of Glyceria maxima. Ph.D. thesis. University of Nijmegen, Nijmegen, The Netherlands.
6. Bollen, G. J. 1972. A comparison of the in vitro antifungal spectra of thiophanates and benomyl. Neth. J. Plant Pathol.78:55-64.
7. Bonsall, R. F., D. M. Weller, and L. S. Thomashow. 1997. Quantification of 2,4-diacetylphloroglucinol produced by fluorescent Pseudomonas spp. in vitro and in the rhizosphere of wheat. Appl. Environ. Microbiol. 63:951-955.
8. Cook, R. J. 1992. Wheat root health management and environmental concern. Can. J. Plant Pathol. 14:76-85.
9. Cook, R. J. 1993. Making greater use of introduced microorganisms for biological control of plant pathogens. Annu. Rev. Phytopathol, 31:53-80.
10. De Leij, F. A. A. M., E. J. Sutton, J. M. Whipps, J. S. Fenlon, and J. M. Lynch. 1995. Impact of field release of a genetically modified Pseudomonas fluorescens on indigenous microbial populations of wheat. Appl. Environ. Microbiol. 61:3443-3453.
11. Duijff, B. J., P. A. H. M. Bakker, and B. Schippers. 1994. Suppression of fusarium wilt of carnation by Pseudomonas putida WCS358 at different levels of disease incidence and iron availability. Biocontrol Sci. Technol. 4:279-288.
12. Elad, Y., I. Chet, and Y. Henis. 1981. A selective medium for improving quantitative isolation of Trichoderma spp. from soil. Phytoparasitica 9:59-67.
13. Embley, T. M., J. Smida, and E. Stackebrandt. 1988. Reverse-transcriptase sequencing of 16S ribosomal RNA from Faenia rectivirgula. Pseudonocardia hermophila and Saccharopolyspora hirsuta, 3 wall type IV actinomycetes which lack mycolic acids. J. Gen. Microbiol. 134:961-966.
14. Fujimoto, D. K., D. M. Weller, and L. S. Thomashow. 1995. Role of secondary metabolites in root disease suppression. ACS (Am. Chem. Soc.) Symp. Ser. 582:330-347.
15. Geels, F. P., and B. Schippers. 1983. Reduction of yield depression in high frequency potato cropping soil after seed tuber treatments with antagonistic fluorescent Pseudomonas spp. Phytopathol. Z. 108:207-214.
16. Glandorf, D. C. M., I. Brand, P. A. H. M. Bakker, and B. Schippers. 1992. Stability of rifampin resistance as a marker for root colonization studies of Pseudomonas putida in the field. Plant Soil 147:135-142.
17. Glandorf, D. C. M., L. G. L. Peters, I. Van der Sluis, P. A. H. M. Bakker, and B. Schippers. 1993. Crop specificity of rhizosphere pseudomonads and the involvement of root agglutinins. Soil Biol. Biochem. 25:981-989.
18. Glandorf, D. C. M., P. Verheggen, T. Jansen, J.-W. Jorritsma, E. Smit, P. Leeflang, K. Wernars, L. S. Thomashow, E. Laureijs, J. E. Thomas-Oates, P. A. H. M. Bakker, and L. C. van Loon. 2001. Effect of genetically modified Pseudomonas putida WCS358r on the fungal rhizosphere microflora of field-grown wheat. Appl. Environ. Microbiol. 67:3371-3378.
19. Haas, D., C. Blumer, and C. Keel. 2000. Biocontrol ability of fluorescent pseudomonads genetically dissected: importance of positive feedback regulation. Curr. Opin. Biotechnol. 11:290-297.
20. Handelsmann, J., and C. Stabb. 1996. Biocontrol of soilborne pathogens. Plant Cell 8:1855-1869.
21. Hase, C., F. Macher, Y. Moënne-Loccoz, and G. Défago. 1999. Nutrient deprivation and the subsequent survival of biocontrol Pseudomonas fluorescens CHAO in soil. Soil Biol. Biochem. 31:1181-1188.
22. Herrero, M., V. de Lorenzo, and K. N. Timmis. 1990. Transposon vectors containing non-antibiotic resistance selection markers for cloning and stable chromosomal insertion of foreign genes in gram-negative bacteria. J. Bacteriol. 172:6557-6567.
23. Hill, G. T., N. A. Mitkowski, L. Aldrich-Wolfe, L. R. Emele, D. D. Jurkonie, A. Ficke, S. Maldonado-Ramirez, S. T. Lynch, and E. B. Nelson. 2000. Methods for assessing the composition and diversity of soil microbial communities. Appl. Soil Ecol. 15:25-36.
24. Hugenholtz, P., and N. R. Pace. 1996. Identifying microbial diversity in the natural environment: a molecular phylogenetic approach. Trends Biotechnol. 14:190-197.
25. Keel, C., U. Schnider, M. Maurhofer, C. Voisard, J. Laville, U. Burger, P. Wirthner, D. Haas, and G. Défago. 1992. Suppression of root diseases by Pseudomonas fluorescens CHAO: importance of the bacterial secondary metabolite 2,4-diacetylphloroglucinol. Mol. Plant-Microbe Interact. 5:4-13.
26. King, E. O., M. K. Ward, and D. E. Raney. 1954. Two simple media for demonstration of pycocyanin and fluorescin. J. Lab. Clin. Med. 44:301-307.
27. Komada, H. 1975. Development of a selective medium for quantitative isolation of Fusarium oxysporum from natural soils. Rev. Plant Prot. Res. 8:114-125.
28. Kremer, R. J., M. F. T. Begonia, L. Stanley, and E. T. Lanham. 1990. Characterization of rhizobacteria associated with weed seedlings. Appl. Environ. Microbiol. 56:1649-1655.
29. Lemanceau, P., T. Corberand, L. Gardan, X. Latour, G. Laguerre, J. Boeufgras, and C. Alabouvette. 1995. Effect of two plant species, flax (Linum usitatissinum L.) and tomato (Lycopersicon esculentum Mill.), on the diversity of soilborne populations of fluorescent pseudomonads. Appl. Environ. Microbiol. 61:1004-1012.
30. Maurhofer, M., C. Keel, C. Voisard, D. Haas, and G. Défago. 1992. Influence of enhanced antibiotic production in Pseudomonas fluorescens strain CHAO on its disease suppressive capacity. Phytopathology 82:190-195.
31. Mazzola, M., J. R. Cook, L. S. Thomashow, D. M. Weller, and L. S. Pierson III 1992. Contribution of phenazine antibiotic biosynthesis to the ecological competence of fluorescent pseudomonads in soil habitats. Appl. Environ. Microbiol. 58:2616-2624.
32. Miethling, R., G. Wieland, H. Backhaus, and C. C. Tebbe. 2000. Variation of microbial rhizosphere communities in response to crop species, soil origin, and inoculation with Sinorhizobium meliloti L33. Microb. Ecol. 41:43-56.
33. Olsson, S., and S. Alström. 2000. Characterization of bacteria in soils under barley monoculture and crop rotation. Soil Biol. Biochem. 32:1443-1451.
34. Pierson, L. S., III, and L. S. Thomashow. 1992. Cloning and heterologous expression of the phenazine biosynthetic locus from Pseudomonas aureofaciens 30-84. Mol. Plant-Microbe Interact. 5:330-339.
35. Raaijmakers, J. M., M. Leemann, M. M. P. van Oorschot, I. van der Sluis, B. Schippers, and P. A. H. M. Bakker. 1995. Dose-response relationships in biological control of Fusarium wilt of radish by Pseudomonas spp. Phytopathology 85:1075-1081.
36. Raaijmakers, J. M., D. M. Weller, and L. S. Thomashow. 1997. Frequency of antibiotic-producing Pseudomonas spp. in natural environments. Appl. Environ. Microbiol. 63:881-887.
37. Sambrook, J., E. F. Fritsch, and T. Manniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
38. Schippers, B., A. W. Bakker, and P. A. H. M. Bakker. 1987. Interactions of deleterious and beneficial rhizosphere microorganisms and the effect of cropping practices. Annu. Rev. Phytopathol. 25:339-358.
39. Schmidt, T. M. 1994. Fingerprinting bacterial genomes using ribosomal RNA genes and operons. Methods Mol. Cell. Biol. 5:3-12.
40. Schwieger, F., and C. C. Tebbe. 2000. Effect of field inoculation with Sinorhizobium meliloti L33 on the composition of bacterial communities in rhizospheres of a target plant (Medicago sativa) and a non-target plant (Chenopodium album)-linking of 16S mRNA gene-based single-strand conformation polymorphism community profiles to the diversity of cultivated bacteria. Appl. Environ. Microbiol. 66:3556-3565.
41. Sengeløv, G., K. J. Kreitensen, A. H. Sørensen, N. Kroer, and S. Sørensen. 2001. Effect of genomic location on horizontal transfer of a recombinant gene cassette between Pseudomonas strains in the rhizosphere and spermosphere of barley seedlings. Curr. Microbiol. 42:160-167.
42. Sharifi-Tehrani, A., M. Zala, A. Natsch, Y. Moënne-Loccoz, and G. Défago. 1998. Biocontrol of soil-borne fungal plant diseases by 2,4-diacetylphloroglucinol-producing fluorescent pseudomonads with different restriction profiles of amplified16S rDNA. Eur. J. Plant Pathol. 104:631-643.
43. Smalla, K., N. Cresswell, L. C. Mendonca-Hagler, A. Wolters, and J. D. Van Elsas. 1993. Rapid DNA extraction protocol from soil for polymerase chain reaction-mediated amplification. J. Appl. Bacteriol. 74:78-85.
44. Smit, E., P. Leeflang, B. Glandorf, J. D. van Elsas, and K. Wernars. 1999. Analysis of fungal diversity in the wheat rhizosphere by sequencing of cloned PCR-amplified genes encoding 18S rRNA and temperature gradient gel electrophoresis. Appl. Environ. Microbiol. 65:2614-2621.
45. Stienstra, A. W., P. Klein Gunnewiek, and H. J. Laanbroek. 1994. Repression of nitrification in soils under a climax grassland vegetation. FEMS Microbiol. Ecol. 14:45-52.
46. Thirup, L., F. Ekelund, K. Johnsen, and C. S. Jacobsen. 2000. Population dynamics of the fast-growing sub-populations of Pseudomonas and total bacteria, and their protozoan grazers, revealed by fenpropimorph treatment. Soil Biol. Biochem. 32:1615-1623.
47. Thomashow, L. S., R. F. Bonsall, and D. M. Weller. 1997. Antibiotic production by soil and rhizosphere microbes in situ, p. 493-499. In C. J. Hurst, G. R. Knudsen, M. J. McInery, L. D. Stetzenbach, and M. V. Walter (ed.), Manual of environmental microbiology. ASM Press, Washington, D.C.
48. Timms-Wilson, T. M., R. J. Ellis, A. Renwick, D. J. Rhodes, D. V. Mavrodi, D. M. Weller, L. S. Thomashow, and M. J. Bailey. 2000. Chromosomal insertion of phenazine-l-carboxylic acid biosynthetic pathway enhances efficacy of damping-off disease control by Pseudomonas fluorescens. Mol. Plant-Microbe Interact. 13:1293-1300.
49. Van Overbeek, L. S., J. A. Van Veen, and J. D. Van Elsas. 1997. Induced reporter gene activity, enhanced stress resistance, and competitive ability of a genetically modified Pseudomonas fluorescens strain released into the field. Appl. Environ. Microbiol. 63:1965-1973.
50. Van Wees, S. C. M., C. M. J. Pieterse, A. Trijssenaar, Y. A. M. Van't Westende, F. Hartog, and L. C. Van Loon. 1997. Differential induction of systemic resistance in Arabidopsis by biocontrol bacteria. Mol. Plant-Microbe Interact. 10:716-724.
51. Völksch, B., and R. May. 2000. Biological control of Pseudomonas syringae pv. glycinea by epiphytic bacteria under field conditions. Microb. Ecol. 41:132-139.
52. Walsh, U. F., J. P. Morrissey, and F. O'Gara. 2001. Pseudomonas for biocontrol of phytopathogens: from functional genomics to commercial exploitation. Curr. Opin. Biotechnol. 12:289-295.
53. Weller, D. M. 1988. Biological control of soilborne plant pathogens in the rhizosphere with bacteria. Annu. Rev. Phytopathol. 26:379-407.
54. Weller, D. M., and R. J. Cook. 1983. Suppression of take-all of wheat by seed treatments with fluorescent pseudomonads. Phytopathology 73:463-469.
55. Weller, D. M., J. M. Raaijmakers, B. B. McSpadden, and L. S. Thomashow. 2002. Microbial populations responsible for specific soil suppressiveness to plant pathogens. Annu. Rev. Phytopathol. 40:309-348.