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Take-all of Wheat and Natural Disease Suppression: A Review

  • Kwak, Youn-Sig (Department of Applied Biology and Institute of Agriculture & Life Science, Gyeongsang National University) ;
  • Weller, David M. (United States Department of Agriculture, Agricultural Research Service, Root Disease and Biological Control Research Unit)
  • 투고 : 2012.07.23
  • 심사 : 2012.09.25
  • 발행 : 2013.06.01

초록

In agro-ecosystems worldwide, some of the most important and devastating diseases are caused by soil-borne necrotrophic fungal pathogens, against which crop plants generally lack genetic resistance. However, plants have evolved approaches to protect themselves against pathogens by stimulating and supporting specific groups of beneficial microorganisms that have the ability to protect either by direct inhibition of the pathogen or by inducing resistance mechanisms in the plant. One of the best examples of protection of plant roots by antagonistic microbes occurs in soils that are suppressive to take-all disease of wheat. Take-all, caused by Gaeumannomyces graminis var. tritici, is the most economically important root disease of wheat worldwide. Take-all decline (TAD) is the spontaneous decline in incidence and severity of disease after a severe outbreak of take-all during continuous wheat or barley monoculture. TAD occurs worldwide, and in the United States and The Netherlands it results from a build-up of populations of 2,4-diacetylphloroglucinol (2,4-DAPG)-producing fluorescent Pseudomonas spp. during wheat monoculture. The antibiotic 2,4-DAPG has a broad spectrum of activity and is especially active against the take-all pathogen. Based on genotype analysis by repetitive sequence-based-PCR analysis and restriction fragment length polymorphism of phlD, a key 2,4-DAPG biosynthesis gene, at least 22 genotypes of 2,4-DAPG producing fluorescent Pseudomonas spp. have been described worldwide. In this review, we provide an overview of G. graminis var. tritici, the take-all disease, Pseudomonas biocontrol agents, and mechanism of disease suppression.

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참고문헌

  1. Achkar, J., Xian, M., Zhao, H. and Frost, J. W. 2005. Biosynthesis of phloroglucinol. J. Am. Chem. Soc. 127:5332−5333.
  2. Andersen, J. B., Koch, B., Nielsen, T. H., Sorensen, D., Hansen, M., Nybroe, O., Christophersen, C., Sorensen, J., Molin, S. and Givskov, M. 2003. Surface motility in Pseudomonas sp. DSS73 is required for efficient biological containment of the root-pathogenic microfungi Rhizoctonia solani and Pythium ultimum. Microbiology 149:37−46.
  3. Baehler, E., de Werra, P., Wick, L. Y., Pechy-Tarr, M., Mathys, S., Maurhofer, M. and Keel, C. 2006. Two novel MvaT-like global regulators control exoproduct formation and biocontrol activity in root-associated Pseudomonas fluorescens CHA0. Mol. Plant-Microbe Interact. 19:313−329.
  4. Baker, K. F. and Cook, R. J. 1974. Biological Control of Plant Pathogens. W.H. Freeman, San Francisco. 433pp.
  5. Bangera, M. G. and Thomashow, L. S. 1999. Identification and characterization of a gene cluster for synthesis of the polyketide antibiotic 2,4-diacetylphloroglucinol from Pseudomonas fluorescens Q2-87. J. Bacteriol. 181:3155−3163.
  6. Bergasma-Vlami, M., Prins, M. E. and Raaijmakers, J. M. 2005. Influence of plant species on population dynamics, genotypic diversity and antibiotic production in the rhizosphere by indigenous Pseudomonas spp. FEMS Microbiol. Ecol. 52:59−69.
  7. Calvent, V., de Orellano, M. E., Sansone, G., Benuzzi, D. and de Tosetti, M. I. S. 2001. Effect of nitrogen source and pH on siderophore production by Rhodotorula strains and their application to biocontrol of phytopathogenic moulds. J. Ind. Microbiol. Biotechnol. 26:226−229.
  8. Chet, I. and Inbar, J. 1994. Biological control of fungal pathogens. Appl. Biochem. Biotechnol. 48:37−43.
  9. Conrath, U., Pieterse, C. M. J. and Mauch-Mani, B. 2002. Priming in plant-pathogen interaction. Trends Plant Sci. 7:210−216. https://doi.org/10.1016/S1360-1385(02)02244-6
  10. Cook, R. J. and Rovira, A. D. 1976. The role of bacteria in the biological control of Gaeumannomyces graminis by suppressive soils. Soil Biol. Biochem. 8:269−273.
  11. Cook, R. J., Thomashow, L. S., Weller, D. M., Fujimoto, D., Mazzola, M., Bangera, G. and Kim, D. S. 1995. Molecular mechanism of defense by rhizobacteria against root disease. Proc. Natl. Acad. Sci. USA 92:4179−4201.
  12. Cook, R. J. 2003. Take-all of wheat. Physiol. Mol. Plant Pathol. 62:73−86.
  13. Cronin, D., Moenne-Loccoz, T., Fenton, A., Dunne, C., Dowling, D. N. and O'Gara, F. 1997a. Ecological interaction of a biocontrol Pseudomonas fluorescens strain producing 2,4-diacetylphloroglucinol with the soft rot potato pathogen Erwinia carotovora subsp. atroseptica. FEMS Microbiol. Ecol. 23:95−106.
  14. Cronin, D., Moenne-Loccoz, T., Fenton, A., Dunne, C., Dowling, D. N. and O'Gara, F. 1997b. Role of 2,4-diacetylphloroglucinol in the interactions of the biocontrol pseudomonad strain F113 with the potato cyst nematode Globodera rostochiensis. Appl. Environ. Microbiol. 63:1357−1361.
  15. D'aes, J., Hoang Hua, G. K., De Maeyer, K., Pannecoucque, J., Forrez, I., Ongena, M., Dietrich, L. E. P., Thomashow, L. S., Mavrodi, D. V. and Hofte, M. 2011. Biological control of Rhizoctonia root rot on bean by phenazine and cyclic lipopeptide-producing Pseudomonas CMR12a. Phytopathology 101:996−1004.
  16. De La Fuente, L., Landa, B. B. and Weller, D. M. 2006. Host crop affects rhizosphere colonization and competitiveness of 2,4-diacetylphloroglucinol-producing Pseudomonas fluorescens. Phytopathology 96:751−762. https://doi.org/10.1094/PHYTO-96-0751
  17. De Vleesschauwer, D. and Hfte, M. 2009. Rhizobacteria-induced systemic resistance. Adv. Bot. Res. 51:223−281.
  18. de Souza, J. T., Arnould, C., Deulvot, C., Lemanceau, P., Gianinazzi-Pearson, N. and Raajimakers, J. M. 2003a. Effect of 2,4-diacetylphloroglucinol on Pythium: cellular responses and variation in sensitivity among propagules and species. Phytopathology 93:966−975.
  19. de Souza, J. T., Weller, D. M. and Raaijmakers, J. M. 2003b. Frequency, diversity, and activity of 2,4-diacetylphloroglucinolproducing fluorescent Pseudomonas spp. in Dutch take-all decline soils. Phytopathology 93:54−63.
  20. Duffy, B. K. and Defago, G. 1997. Zinc improves biocontrol of Fusarium crown and root rot of tomato by Pseudomonas fluorescens and represses the production of pathogen metabolites inhibitory to bacterial antibiotic biosynthesis. Phytopathology 87:1250−1257.
  21. Duffy, B., Schouten, A. and Raaijmakers, J. M. 2003. Pathogen self-defense: mechanisms to counteract microbial antagonism. Annu. Rev. Phytopathol. 41:501−538.
  22. Fenton, A. M., Stephens, P. M., Crowley, J., Ocallaghan, M. and O'Gara, F. 1992. Exploitation of gene(s) involved in 2,4-diacetylphloroglucinol biosynthesis to confer a new biocontrol capability to a Pseudomonas strain. Appl. Environ. Microbiol. 58:3873−3878.
  23. Fleissner, A., Sopalla, C. and Weltring, K. M. 2002. An ATPbinding cassette multidrug-resistance transporter is necessary for tolerance of Gibberella pulicaris to phytoalexins and virulence on potato tubers. Mol. Plant-Microbe Interact. 15:102-108. https://doi.org/10.1094/MPMI.2002.15.2.102
  24. Fravel, D. R. 1992. Role of antibiosis in the biocontrol of plant diseases. Annu. Rev. Phytopathol. 26:75−91.
  25. Freeman, J. and Ward, E. 2004. Gaeumannomyces graminis, the take-all fungus and its relatives. Mol. Plant Pathol. 5:235−252.
  26. Haas, D. and Defago, G. 2005. Biological control of soil-borne pathogens by fluorescent Pseudomonas. Nature Rev. Microbiol. 3:307−319.
  27. Haas, D., Keel, C. and Reimmann, C. 2002. Signal transduction in plant-beneficial rhizobacteria with biocontrol properties. Antonie Leeuwenhoek 81:385−395.
  28. Haas, D. and Keel, C. 2003. Regulation of antibiotic production in root-colonizing Pseudomonas spp. and relevance for biological control of plant disease. Annu. Rev. Phytopathol. 41:117−153.
  29. Hammer, P., Hill, D. S., Lam, S. T., van Pe, K. H. and Ligon, J. M. 1997. Four genes from Pseudomonas fluorescens that encode the biosynthesis of pyrrolnitrin. Appl. Environ. Microbiol. 63:2147−2154.
  30. Hornby, D. 1998. Take-All of Cereals. A Regional Perspective. CAB International, Wallingford, UK.
  31. Iavicoli, A., Boutet, E., Buchala, A. and Metraux, J. P. 2003 Induced systemic resistance in Arabidopsis thaliana in response to root inoculation with Pseudomonas fluorescens CHA0. Mol. Plant-Microbe Interact. 16:851−858.
  32. Keel, C., Schnider, U., Maurhofer, M., Voisard, C., Laville, J., Burger, U., Wirthner, P., Haas, D. and Defago, G. 1992. Suppression of root diseases by Pseudomonas fluorescens CHA0: Important of the bacterial secondary metabolite 2,4-diacetylphloroglucinol. Mol. Plant-Microbe Interact. 5:4−13.
  33. Keel, C., Weller, D. M., Natsch, A., Defago, G., Cook, R. J. and Thomashow, L. S. 1996. Conservation of the 2,4-diacetylphloroglucinol biosynthesis locus among fluorescent Pseudomonas strains from diverse geographic locations. Appl. Environ. Microbiol. 62:552−563.
  34. Kollmorgen, J. F. and Walsgott, D. N. 1984. Saprophytic survival of Gaeumannomyces graminis var. tritici at various depths in soil. Trans. Brit. Mycol. Soc. 82:346−348.
  35. Kwak, Y.-S., Bakker, P. A. H. M., Glandorf, D. C. M., Rice, J. T., Paulitz, T. C. and Weller D. M. 2009. Diversity, virulence, and 2,4-diacetylphloroglucinol sensitivity of Gaeumannomyces graminis var. tritici isolates from Washington State. Phytopathology 99:472−479.
  36. Kwak, Y.-S., Bonsall, R. F., Okubara, P. A., Paulitz, T. C., Thomashow, L. S. and Weller, D. M. 2012. Factors impacting the activity of 2,4-diacetylphloroglucinol-producing Pseudomonas fluorescens against take-all of wheat. Soil Biol. Biochem. 54:48−56.
  37. Kwak, Y.-S., Han, S., Thomashow, L. S., Rice, J. T., Paulitz, T. C., Kim, D. and Weller, D. M. 2011. Saccharomyces cerevisiae genome-wide mutant screen for sensitivity to 2,4-diacetylphloroglucinol, an antibiotic produced by Pseudomonas fluorescens. Appl. Environ. Microbiol. 77:1770−1776.
  38. Landa, B. B., de Werd, H. A. E., McSpadden-Gardener, B. B. and Weller, D. M. 2002a. Comparison of three methods for monitoring populations of different genotypes of 2,4-diacetylphloroglucinol-producing Pseudomonas fluorescens in the rhizosphere. Phytopathology 92:129−137.
  39. Landa, B. B., Mavrodi, O. V., Raaijmakers, J. M., McSpadden-Gardener, B. B., Thomashow, L. S. and Weller, D. M. 2002b. Differential ability of genotypes of 2,4-diacetylphloroglucinol-producing Pseudomonas fluorescens to colonize the roots of pea. Appl. Environ. Microbiol. 68: 3226-3237. https://doi.org/10.1128/AEM.68.7.3226-3237.2002
  40. Landa, B. B., Mavrodi, D., Thomashow, L. S. and Weller, D. M. 2003. Interactions between strains of 2,4-diacetylphloroglucinol-producing Pseudomonas fluorescens in the rhizosphere of wheat. Phytopathology 93:982−994.
  41. Landa, B. B., Mavrodi, O. V., Schroeder, K. L., Allende-Molar, R. and Weller, D. M. 2006. Enrichment and genotypic diversity of phlD-containing fluorescent Pseudomonas spp. in two soils after a century of wheat and flax monoculture. FEMS Microbiol. Ecol. 55:351−368.
  42. Ligon, J. M., Hill, D. S., Hammer, P. E., Torkewitz, N. R., Horhmann, D., Kempf, H. J. and van Pe, H. H. 2000. Natural products with antifungal activity from Pseudomonas biocontrol bacteria. Pest Manag. Sci. 56:688−695.
  43. Loper, J. E. and Gross, H. 2007. Genomic analysis of antifungal metabolite production by Pseudomonas fluorescens Pf-5. Eur. J. Plant Pathol. 119:265−278.
  44. Loper, J. E., Hassan, K. A., Mavrodi, D. V., Davis II, E. W., Lim, C. K., Shaffer, B. T., Elbourne, L. D. H., 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 III, L. S., Pierson, E. A., Lindow, S. E., Kobayashi, D. Y., Raaijmakers, J. M., Weller, D. M., Thomahsow, 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 Genetics 8:e1002784. https://doi.org/10.1371/journal.pgen.1002784
  45. Lugtenberg, B. J. J. and Kravchenoko, L. V. 1999. Tomato seed and root exudate sugars: composition, utilization by Pseudomonas biocontrol strains and role in rhizosphere colonization. Environ. Microbiol. 1:439−446.
  46. Maurhofer, M., Keel, C., Haas, D. and Dfago, G. 1995. Influence of plant species on disease suppression by Pseudomonas fluorescens strain CHA0 with enhanced antibiotic production. Plant Pathol. 44:40−50.
  47. Mavrodi, D. V., Blankenfeldt, W. and Thomashow, L. S. 2006a. Phenazine compounds in fluorescent Pseudomonas spp. biosynthesis and regulation. Annu. Rev. Phytopathol. 44:417−445.
  48. Mavrodi, O. V., Mavrodi, D., Park, A. A., Weller, D. M. and Thomashow, L. S. 2006b. The role of dsbA in colonization of the wheat rhizosphere by Pseudomonas fluorescens Q8r1-96. Microbiology 152:863−872.
  49. Mavrodi, O. V., Mavrodi, D., Weller, D. M. and Thomashow, L. S. 2006c. Role of ptsP, orfT, and sss recombinase genes in root colonization by Pseudomonas fluorescens Q8r1-96. Appl. Environ. Microbiol. 72:7111−7122.
  50. Mazzola, M., Fujimoto, D. K., Thomashow, L. S. and Cook, R. J. 1995. Variation in sensitivity of Gaeumannomyces graminis to antibiotics produced by fluorescent Pseudomonas spp. and effect on biological control of take-all of wheat. Appl. Environ. Microbiol. 61:2554−2559.
  51. Mazzola, M., Funnell, D. L. and Raaijmakers, J. M. 2004. Wheat cultivar-specific selection of 2,4-diacetylphloroglucinol producing fluorescent Pseudomonas species from resident soil populations. Microbial Ecol. 48:338−348.
  52. McSpadden Gardener, B. B., Schroeder, K. L., Kalloger, S. E., Raaijmakers, J. M., Thomashow, L. S. and Weller, D. M. 2000. Genotypic and phenotypic diversity of phlD-containing Pseudomonas isolated from rhizosphere of wheat. Appl. Environ. Microbiol. 66:1939−1946.
  53. McSpadden Gardener, B. B., Mavrodi, D. V., Thomashow, L. S. and Weller, D. M. 2001. A rapid polymerase chain reactionbased assay characterizing rhizosphere populations of 2,4-diacetylphloroglucinolproducing bacteria. Phytopathology 91:44−54.
  54. McSpadden-Gardener, B. B., Gutierrez, L. J., Joshi, R., Edema, R. and Lutton, E. 2005. Distribution and biocontrol potential of $phlD^{+}$ Pseudomonas in corn and soybean fields. Phytopathology 95:715−724. https://doi.org/10.1094/PHYTO-95-0715
  55. Moore, K. J. and Cook, R. J. 1984. Increased take-all of wheat with direct drilling in the Pacific Northwest. Phytopathology 74:1044−1049.
  56. Morrissey, J. P. and Osbourn, A. E. 1999. Fungal resistance to plant antibiotics as a mechanism of pathogenesis. Microbiol. Mol. Biol. Rev. 63:708-724.
  57. Notz, R., Maurhofer, M., Schnider-Keel, U., Duffy, B. K., Hass, D. and Defago, G. 2001. Biotic factors affecting expression of the 2,4-diacetylphloroglucinol biosynthesis gene phlA in Pseudomonas fluorescens biocontrol strain CHA0 in the rhizosphere. Phytopathology 91:873−883.
  58. Okubara, P. A., Kornoely, J. P. and Landa, B. B. 2004. Rhizosphere colonization of hexaploid wheat by Pseudomonas fluorescens strains Q8r1-96 and Q2-87 is cultivar-variable and associated with changes in gross root morphology. Biol. Cont. 30:391−403.
  59. Okubara, P. A. and Bonsall, R. F. 2008. Accumulation of Pseudomonas-derived 2,4-diacetylphloroglucinol on wheat seedling roots is influenced by host cultivar. Biol. Cont. 46:322−331.
  60. Paulsen, I. T., Press, C., Ravel, J., Kobayashi, D. Y., Myers, G. S. A., 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., Nelson, W. C., Weidman, J., Watkins, K., Tran, K., Khouri, H., Pierson, E. A., Pierson III, L. S. Thomashow, L. S. and Loper, J. E. 2005. Complete genome sequence of the plant commensal Pseudomonas fluorescens Pf-5: insights into the biological control of plant disease. Nature Biotechnol. 23:873−878.
  61. Picard, C., Frascaroli, E. and Bosco, M. 2004. Frequency and biodiversity of 2,4-diacetylphloroglucinol-producing rhizobacteria are differentially affected by the genotype of two maize inbred lines and their hybrid. FEMS Microbiol. Ecol. 49:207−215.
  62. 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.
  63. Potvin, E., Sanschagrin, F. and Levesque, R. C. 2008. Sigma factors in Pseudomonas aeruginosa. FEMS Microbiol. Rev. 32:38−55.
  64. Raaijmakers, J. M., Bonsall, R. F. and Weller, D. M. 1999. Effect of population density of Pseudomonas fluorescens on production of 2,4-diacetylphloroglucinol in the rhizosphere of wheat. Phytopathology 89:470−475.
  65. Raaijmakers, J. M., de Bruijn, I. and de Kock, M. J. D. 2006. Cyclic lipopeptide production by plant-associated Pseudomonas spp.: diversity, activity, biosynthesis, and regulation. Mol. Plant-Microbe Interact. 19:669−710.
  66. Raaijmakers, J. M. and Weller, D. M. 1998. Natural plant protection by 2,4-diacetylphloroglucionl-producing Pseudomonas spp. in take-all decline soils. Mol. Plant-Microbe Interact. 11:144−152.
  67. Raaijmakers, J. M. and Weller, D. M. 2001. Exploiting genotype diversity of 2,4-diasctylphloroglucinol producing Pseudomonas spp.: Characterization of superior root-colonizing P. fluorescens strain Q8r1-96. Appl. Environ. Microbiol. 67:2545−2554.
  68. Ramette, A., Moenne-Loccoz, Y. and Defago, G. 2001. Polymorphism of the polyketide synthase gene phlD in biocontrol fluorescent pseudomonas producing 2,4-diacetylphloroglucinol and comparison of PhlD with plant polyketide synthases. Mol. Plant-Microbe Interact. 14:639−652.
  69. Ran, H., Hassett, D. J. and Lau, G. W. 2003. Human targets of Pseudomonas aeruginosa pyocyanin. Proc. Nat. Acad. Sci. USA 100:14315−14320.
  70. Schnider, U., Keel, C., Blumer, C., Troxler, J., Defago, G. and Haas, D. 1995. Amplification of the housekeeping sigma factor in Pseudomonas fluorescens CHA0 enhances antibiotic production and improves biocontrol abilities. J. Bacteriol. 117:5387−5393.
  71. Shanahan, P., O'Sullivan, D. J., Simpson, P., Glennon, J. D. and O'Gara, F. 1992. Isolation of 2,4-diacetylphloroglucinol from a fluorescent pseudomonad and investigation of physiological parameters influencing its production. Appl. Environ. Microbiol. 58:353−358.
  72. Smiley, R. W. and Cook, R. J. 1973. Relationship between take-all of wheat and rhizosphere pH in soils fertilized with ammonium vs. nitrate-nitrogen. Phytopathology 63:882−890.
  73. Stutz, E. W., Defago, G. and Kern, H. 1986. Naturally occurring fluorescent Pseudomonas involved in suppression of block root rot of tobacco. Phytopathology 76:181−185.
  74. Thomashow, L. S. 1996. Biological control of plant root pathogens. Curr. Opin. Biotechnol. 7:343−347.
  75. Thomashow, L. S. and Weller, D. M. 1988. Role of a phenazine antibiotic from Pseudomonas fluorescens in biological control of Gaeumannomyces graminis var. tritici. J. Bacteriol. 170:3499−3508.
  76. Tjamos, S., Flemetakis, E., Paplomatas, E. and Katinakis, P. 2005. Induction of resistance to Verticillium dahliae in Arabidopsis thaliana by the biocontrol agent K-165 and pathogenesisrelated proteins gene expression. Mol. Plant-Microbe Interact. 18:555−561.
  77. van Etten, H., Temporini, E. and Wasmann, C. 2001. Phytoalexin (and phytoanticipin) tolerance as a virulence trait: why is it not required by all pathogens? Physiol. Mol. Plant Pathol. 59:83-93. https://doi.org/10.1006/pmpp.2001.0350
  78. Verhagen, B. M., Glazebrook, J., Zhu, T., Chang, H. S., van Loon, L. C. and Pieterse, C. M. 2004. The transcriptome of rhizobacteria induced systemic resistance in Arabidopsis. Mol. Plant-Microbe Interact. 17:895−908.
  79. Voisard, C., Keel, C., Haas, D. and Defago, G. 1989. Cyanide production by Pseudomonas fluorescens helps suppress black root rot of tobacco under gnotobiotic conditions. EMBO J. 8:351−358.
  80. Wang, C. X., Ramette, A., Punjasamarnwong, P., Zala, M., Natsch, A., Moenne-Loccoz, Y. and Defago, G. 2001. Cosmopolitan distribution of phlD-containing dicotyledonous cropassociated biocontrol pseudomonads of worldwide origin. FEMS Microbiol. Ecol. 37:105−116.
  81. Weller, D. M. 1988. Biological control of soilborne plant pathogens in the rhizosphere with bacteria. Annu. Rev. Phytopathol. 26:379−417.
  82. Weller, D. M., Landa, B. B., Mavrodi, O. V., Schroeder, K. L., De La Fuente, L., Bankhead, B. S., Allende Molar, R., Bonsall, R. F., Mavrodi, D. and Thomashow, L. S. 2007. Role of 2,4-diacetylphloroglucinol-producing fluorescent Pseudomonas spp. in the defense of plant roots. Plant Biol. 9:4−20. https://doi.org/10.1055/s-2006-924761
  83. Weller, D. M., Raaijmakers, J. M., McSpadden-Gardener, B. B. and Thomashow, L. S. 2002. Microbial populations responsible for specific soil suppressiveness to plant pathogens. Annu. Rev. Phytopathol. 40:309−348.
  84. Weller, D. M., Marrodi, D. V., van Pelt, J. A., Pieterse, C. M., van Loon, L. C. and Bakker, P. A. H. M. 2012. Induced systemic resistance in Arabidopsis thaliana against Pseudomonas syringae pv. tomato by 2,4-diacetylphloroglucinol-producing Pseudomonas fluorescens. Phytopathology 102:403−412.
  85. Wiese, M. V. 1987. Compendium of Wheat Disease. Second Edition. APS Press, St. Paul, Minnesota.

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