Mechanisms of natural soil suppressiveness to soilborne diseases

Abstract

Suppressive soils are characterized by a very low level of disease development even though a virulent pathogen and susceptible host are present. Biotic and abiotic elements of the soil environment contribute to suppressiveness, however most defined systems have identified biological elements as primary factors in disease suppression. Many soils possess similarities with regard to microorganisms involved in disease suppression, while other attributes are unique to specific pathogen-suppressive soil systems. The organisms operative in pathogen suppression do so via diverse mechanisms including competition for nutrients, antibiosis and induction of host resistance. Non-pathogenic Fusarium spp. and fluorescent Pseudomonas spp. play a critical role in naturally occurring soils that are suppressive to Fusarium wilt. Suppression of take-all of wheat, caused by Gaeumannomyces graminis var. tritici, is induced in soil after continuous wheat monoculture and is attributed, in part, to selection of fluorescent pseudomonads with capacity to produce the antibiotic 2,4-diacetylphloroglucinol. Cultivation of orchard soils with specific wheat varieties induces suppressiveness to Rhizoctonia root rot of apple caused by Rhizoctonia solani AG 5. Wheat cultivars that stimulate disease suppression enhance populations of specific fluorescent pseudomonad genotypes with antagonistic activity toward this pathogen. Methods that transform resident microbial communities in a manner which induces natural soil suppressiveness have potential as components of environmentally sustainable systems for management of soilborne plant pathogens.

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References

  1. Alavouvette C, Lemanceau P & Steinberg C (1996) Biological control of fusarium wilts: opportunities for developing a commercial product. In: Hall R (Ed), Principles and Practice of Managing Soilborne Plant Pathogens (pp 192–212). APS Press, St. Paul, MN.

    Google Scholar 

  2. Amir H & Alabouvette C (1993) Involvement of soil abiotic factors in the mechanisms of soil suppressiveness to fusarium wilt. Soil Biol. Biochem. 25: 157–164.

    Article  Google Scholar 

  3. Amann RI, Ludwig W & Schleifer (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol. Rev. 59: 143–169.

    PubMed  CAS  Google Scholar 

  4. Broadbent P & Baker KF (1974) Behavior of Phytophthora cinnamomi in soils suppressive and conducive to root rot. Aust. J. Agric. Res. 25: 121–137.

    Article  Google Scholar 

  5. Bruehl GW (1987) Soilborne Plant Pathogens. Macmillan Publishing Co., New York.

    Google Scholar 

  6. Chet I & Baker R (1980) Induction of suppressiveness to Rhizoctonia solani in soil. Phytopathology 70: 994–998.

    Google Scholar 

  7. Cook RJ & Baker KF (1983) The Nature and Practice of Biological Control of Plant Pathogens. APS Press, St. Paul, MN.

    Google Scholar 

  8. Cook RJ & Rovira AD (1976) The role of bacteria in the biological control of Gaeumannomyces graminis by suppressive soils. Soil Biol. Biochem. 8: 267–273.

    Article  Google Scholar 

  9. Couteaudier Y & Alabouvette C (1990) Quantitative comparison of Fusarium oxysporum competitiveness in realtion to carbon utilization. FEMS Microbiol. Ecol. 74: 261–268.

    CAS  Article  Google Scholar 

  10. Duijff BJ, Pouhair D, Olivain C, Alabouvette C & Lemanceau P (1998) Implication of systemic induced resistanc in the suppression of Fusaium vilt of tomato by Pseudomonas fluorescens WCS417r and nonpathogenic Fusarium oxysporum Fo47. Eur. J. Plant Pathol. 104: 903–910.

    Article  Google Scholar 

  11. Duijff BJ, Recorbet G, Bakker PAHM, Loper JE & Lemanceau P (1999) Microbial antagonism at the root level is involve in the suppression of Fusarium wilt by the combination of nonpathogenic Fusarium oxysporum Fo47 and Pseudomonas putida WCS358. Phytopathology 89: 1073–1979.

    PubMed  CAS  Google Scholar 

  12. Glynne MD (1935) Incidence of take-all on wheat and barley on experimental plots at Woburn. Ann. Appl. Biol. 22: 225–235.

    CAS  Article  Google Scholar 

  13. Gu Y-H & Mazzola M (2001a) Influence of wheat cultivation on genetic composition of fluorescent pseudomonad populations from apple replant soils. Phytopathology 91: S33.

    Google Scholar 

  14. Gu Y-H & Mazzola M (2001b) Evaluation of wheat cultivars for ability to induce microbe-mediated control of apple replant disease. Phytopathology 91: S33.

    Google Scholar 

  15. Gu Y-H & Mazzola M (2001c) Impact of carbon starvation on stress resistance, survival in soil habitats and biocontrol ability of Pseudomonas putida strain 2C8. Soil Biol. Biochem. 33: 1155–1162.

    CAS  Article  Google Scholar 

  16. Hancock JG (1977) Factors affecting soil populations of Pythium ultimum in the San Joaquin Valley of California. Hilgardia 45: 107–122.

    Google Scholar 

  17. Henis Y, Ghaffar A & Baker R (1978) Integrated control of Rhizoctonia solani damping-off of radish: effect of successive plantings, PCNB and Trichoderma harzianum on pathogen and disease. Phytopathology 68: 900–907.

    CAS  Google Scholar 

  18. Henis Y, Ghaffar A & Baker R (1979) Factors affecting suppressiveness to Rhizoctonia solani in soil. Phytopathology 69: 1164–1169.

    CAS  Google Scholar 

  19. Höper H, Steinberg C & Alabouvette C (1995) Involvement of clay type and pH in the mechanism of soil suppressiveness to Fusarium wilt of flax. Soil Biol. Biochem. 27: 955–967.

    Article  Google Scholar 

  20. Huber DM & Schneider RW (1982) The description and occurrence of suppressive soils. In: Schneider RW (Ed), Suppressive Soils and Plant Diseases (pp 1–7). APS Press. St. Paul, MN.

    Google Scholar 

  21. Huber DM (1989) The role of nutrition in the take-all disease of wheat and other small grains. In: Englehard AW (Ed), Soilborne Plant Pathogens: Management of Diseases with Macroand Microelements (pp 46–74). APS Press, St. Paul, MN.

    Google Scholar 

  22. Keel C, Schnider U, Maurhofer M, Voisard C, Laville J, Burger P, Wirthner P, Haas D & Défago G (1992) Suppression of root diseases by Pseudomonas fluorescens CHAO: importance of the secondary metabolite 2,4-diacetylphloroglucinol. Mol. Plant-Microbe Interact. 5: 4–13.

    CAS  Google Scholar 

  23. Kerry BR (1988) Fungal parasites of cyst nematodes. Agric. Ecosyst. Environ. 24: 293–305.

    Article  Google Scholar 

  24. Kloepper JW, Leong J, Teintze M & Schroth MN (1980) Enhanced plant growth by siderophores produced by plant growth-promoting rhizobacteria. Nature 286: 885–886.

    CAS  Article  Google Scholar 

  25. Kraus J & Loper JE (1995) Characterization of a genomic region required for production of the antibiotic pyoluteorin by the biological control agent Pseudomonas fluorescens Pf-5. Appl. Environ. Microbiol. 61: 849–854.

    PubMed  CAS  Google Scholar 

  26. Larkin RP, Hopkins DL & Martin FN (1993a) Effect of successive watermelon plantings on Fusarium oxysporum and other microorganisms suppressive and conducive to Fusarium wilt of watermelon. Phytopathology 83: 1097–1105.

    Google Scholar 

  27. Larkin RP, Hopkins DL & Martin FN (1993b) Ecology of Fusarium oxysporum f. sp. niveum in soils suppressive and conducive to Fusarium wilt of watermelon. Phytopathology 83: 1105–1116.

    Google Scholar 

  28. Larkin RP, Hopkins DL & Martin FN (1996) Suppression of Fusarium wilt of watermelon by nonpathogenic Fusarium oxysporum and other microorganisms recovered from a disease-suppressive soil. Phytopathology 96: 812–819.

    Google Scholar 

  29. Lemanceau P, Bakker PAHM, De Kogel WJ, Alabouvette C & 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.

    PubMed  CAS  Google Scholar 

  30. Lemanceau P, Bakker PAHM, De Kogel WJ, Alabouvette C & Schippers B (1993) Antagonistic effect of nonpathogenic Fusarium oxysporum strain Fo47 and pseudobactin 358 upon pathogenic Fusarium oxysporum f. sp. dianthi. Appl. Environ. Microbiol. 59: 74–82.

    PubMed  CAS  Google Scholar 

  31. Liu S & Baker R (1980) Mechanism of biological control in soil suppressive to Rhizoctonia solani. Phytopathology 70: 404–412.

    Google Scholar 

  32. Liu W-T, Marsh TL, Cheng H & Forney LJ (1997) Characterization of microbial diversity by determining terminal restriction fragment length polymophisms of genes encoding 16S rRNA. Appl. Environ. Microbiol. 63: 4516–4522.

    PubMed  CAS  Google Scholar 

  33. Mazzola M (1997) Identification and pathogenicity of Rhizoctonia spp. isolated from apple roots and orchard soils. Phytopathology 87: 582–587.

    PubMed  CAS  Google Scholar 

  34. Mazzola M (1998a) Towards the development of sustainable alternatives for the control of apple replant disease in Washington. In: Proceedings, Annual International Research Conference on Methyl Bromide Alternatives and Emissions Reductions (pp 8.1–8.3). MBAO, Fresno, CA.

    Google Scholar 

  35. Mazzola M (1998b) Elucidation of the microbial complex having a causal role in the development of apple replant disease in Washington. Phytopathology 88: 930–938.

    PubMed  CAS  Google Scholar 

  36. Mazzola M (1999) Transformation of soil microbial community structure and Rhizoctonia-suppressive potential in response to apple roots. Phytopathology 89: 920–927.

    PubMed  CAS  Google Scholar 

  37. Mazzola M & Gu Y-H (2000a) Impact of wheat cultivation on microbial communities from replant soils and apple growth in greenhouse trials. Phytopathology 90: 114–119.

    PubMed  CAS  Google Scholar 

  38. Mazzola M & Gu Y-H (2000b) Phyto-management of microbial community structure to enhance growth of apple in replant soils. ACTA Horticulturae 532: 73–78.

    Google Scholar 

  39. Mazzola M, Fujimoto DK, Thomashow LS & Cook RJ (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.

    PubMed  CAS  Google Scholar 

  40. McSpadden Gardener BB, Schroeder KL, Kalloger SE, Raaijmakers JM, Thomashow LS & Weller DM (2000) Genotypic and phnenotypic diversity of phlD-containing Pseudomonas strains isolated from the rhizosphere of wheat. Appl. Environ. Microbiol. 66: 1939–1946.

    PubMed  CAS  Article  Google Scholar 

  41. Menzies JD (1959) Occurrence and transfer of a biological factor in soil that suppresses potato scab. Phytopathology 49: 648–652.

    Google Scholar 

  42. Murakami H, Tsushima S & Shishido Y (2000) Soil suppressiveness to clubroot disease of Chinese cabbage caused by Plasmodiophora brassicae. Soil Biol. Biochem. 32: 1637–1642.

    CAS  Article  Google Scholar 

  43. Pierson LS & Thomashow LS (1992) Cloning and heterologous expression of the phenazine biosynthetic locus from Pseudomonas aureofaciens 30-84. Mol. Plant Microbe Interact. 5: 330–339.

    PubMed  CAS  Google Scholar 

  44. Raaijmakers JM, Bonsall RF & Weller DM (1999) Effect of population density of Pseudomonas fluorescens on production of 2,4-diacetylphloroglucinol in the rhizosphere of wheat. Phytopathology 89: 470–475.

    CAS  PubMed  Google Scholar 

  45. Raaijmakers JM, van der Sluis I, Koster M, Bakker PAHM, Weisbeek PJ & Schippers B (1995) Utilization of heterologous siderophores and rhizosphere competence of fluorescent Pseudomonas spp. Can. J. Microbiol. 41: 126–135.

    CAS  Article  Google Scholar 

  46. Raaijmakers JM, Weller DM & Thomashow LS (1997) Frequency of antibiotic-producing Pseudomonas spp. in natural environments. Appl. Environ. Microbiol. 63: 881–887.

    PubMed  CAS  Google Scholar 

  47. Raaijmakers JM & Weller DM (1998) Natural protection by 2,4-diacetylphloroglucinol-producing Pseudomonas spp. in take-all decline soils. Mol. Plant-Microbe Interact. 11: 144–152.

    CAS  Google Scholar 

  48. Rodriguez-Kabana R & Canullo GH (1992) Cropping systems for the management of phytonematodes. Phytoparasitica 20: 211–224.

    Google Scholar 

  49. Rouxel F, Alabouvette C & Louvet J (1979) Recherches sur la résistance des sols aux maladies. IV. Mise en évidence du rôle des Fusarium autochtones dans la résistance d'un sol à la fusriose vasculaire du melon. Ann. Phytopathol. 11: 199–207.

    Google Scholar 

  50. Scher FM & Baker R (1980) Mechanism of biological control in a Fusarium-suppressive soil. Phytopathology 70: 412–417.

    Article  Google Scholar 

  51. Shipton PJ (1975) Take-all decline during cereal monoculture. In: Bruehl GW (Ed) Biology and Control of Soilborne Pathogens (pp 137–144). American Phytopathological Society. St. Paul, MN.

    Google Scholar 

  52. Simon A & Sivasithamparam K (1989) Pathogen-suppression: A case study in biological suppression of Gaeumannomyces graminis var. tritici in soil. Soil. Biol. Biochem. 21: 331–337.

    Article  Google Scholar 

  53. Smiley RW (1978) Colonization of wheat roots by Gaeumannomyces graminis inhibited by specific soils, microorganisms and ammonium nitrogen. Soil Biol. Biochem. 10: 175–179.

    CAS  Article  Google Scholar 

  54. Stotzky G & Martin RT (1963) Soil mineralogy in relation to the spread of Fusarium wilt of banana in Central America. Plant Soil 18: 317–337.

    CAS  Article  Google Scholar 

  55. Thomashow LS & Weller DM (1988) Role of phenazine antibiotic from Pseudmonas fluorescens in biological control of Gaeumannomyces graminis var. tritici. J. Bacteriol. 170: 3499–3508.

    PubMed  CAS  Google Scholar 

  56. Van Bruggen AHC (1995) Plant disease severity in high-input compared to reduced-input and organic farming systems. Plant Dis. 79: 976–983.

    Article  Google Scholar 

  57. Vargas-Ayala R, Rodríguez-Kábana R, Morgan-Jones G, McInroy JA & Kloepper JW (2000) Shifts in soil microflora induced by velvetbean (Mucuna deeringiana) in cropping systems to control root knot nematodes. Biol. Control 17: 11–22.

    Article  Google Scholar 

  58. Walker JC & Snyder WC (1934) Pea wilt much less severe on certain soils. Univ. Wis. Agr. Exp. Sta. Bull. 428 (pp 95–96).

    Google Scholar 

  59. Westphal A & Becker JO (1999) Biological suppression and natural population decline of Heterodera schachtii in a California field. Phytopathology 89: 434–440.

    PubMed  CAS  Google Scholar 

  60. Workneh F, van Bruggen AHC, Drinkwater LE & Shennan C (1993) Variables associated with Corky Root and Phytophthora Root Rot of tomatoes in organic and conventional farms. Phytopathology 83: 581–589.

    Google Scholar 

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Mazzola, M. Mechanisms of natural soil suppressiveness to soilborne diseases. Antonie Van Leeuwenhoek 81, 557–564 (2002). https://doi.org/10.1023/A:1020557523557

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  • apple replant disease
  • Fusarium wilt
  • Rhizoctonia
  • suppressive soils
  • take-all decline