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.
This is a preview of subscription content, access via your institution.
Buy single article
Instant access to the full article PDF.
Tax calculation will be finalised during checkout.
Subscribe to journal
Immediate online access to all issues from 2019. Subscription will auto renew annually.
Tax calculation will be finalised during checkout.
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.
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.
Amann RI, Ludwig W & Schleifer (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol. Rev. 59: 143–169.
Broadbent P & Baker KF (1974) Behavior of Phytophthora cinnamomi in soils suppressive and conducive to root rot. Aust. J. Agric. Res. 25: 121–137.
Bruehl GW (1987) Soilborne Plant Pathogens. Macmillan Publishing Co., New York.
Chet I & Baker R (1980) Induction of suppressiveness to Rhizoctonia solani in soil. Phytopathology 70: 994–998.
Cook RJ & Baker KF (1983) The Nature and Practice of Biological Control of Plant Pathogens. APS Press, St. Paul, MN.
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.
Couteaudier Y & Alabouvette C (1990) Quantitative comparison of Fusarium oxysporum competitiveness in realtion to carbon utilization. FEMS Microbiol. Ecol. 74: 261–268.
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.
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.
Glynne MD (1935) Incidence of take-all on wheat and barley on experimental plots at Woburn. Ann. Appl. Biol. 22: 225–235.
Gu Y-H & Mazzola M (2001a) Influence of wheat cultivation on genetic composition of fluorescent pseudomonad populations from apple replant soils. Phytopathology 91: S33.
Gu Y-H & Mazzola M (2001b) Evaluation of wheat cultivars for ability to induce microbe-mediated control of apple replant disease. Phytopathology 91: S33.
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.
Hancock JG (1977) Factors affecting soil populations of Pythium ultimum in the San Joaquin Valley of California. Hilgardia 45: 107–122.
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.
Henis Y, Ghaffar A & Baker R (1979) Factors affecting suppressiveness to Rhizoctonia solani in soil. Phytopathology 69: 1164–1169.
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.
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.
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.
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.
Kerry BR (1988) Fungal parasites of cyst nematodes. Agric. Ecosyst. Environ. 24: 293–305.
Kloepper JW, Leong J, Teintze M & Schroth MN (1980) Enhanced plant growth by siderophores produced by plant growth-promoting rhizobacteria. Nature 286: 885–886.
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.
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.
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.
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.
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.
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.
Liu S & Baker R (1980) Mechanism of biological control in soil suppressive to Rhizoctonia solani. Phytopathology 70: 404–412.
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.
Mazzola M (1997) Identification and pathogenicity of Rhizoctonia spp. isolated from apple roots and orchard soils. Phytopathology 87: 582–587.
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.
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.
Mazzola M (1999) Transformation of soil microbial community structure and Rhizoctonia-suppressive potential in response to apple roots. Phytopathology 89: 920–927.
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.
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.
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.
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.
Menzies JD (1959) Occurrence and transfer of a biological factor in soil that suppresses potato scab. Phytopathology 49: 648–652.
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.
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.
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.
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.
Raaijmakers JM, Weller DM & Thomashow LS (1997) Frequency of antibiotic-producing Pseudomonas spp. in natural environments. Appl. Environ. Microbiol. 63: 881–887.
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.
Rodriguez-Kabana R & Canullo GH (1992) Cropping systems for the management of phytonematodes. Phytoparasitica 20: 211–224.
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.
Scher FM & Baker R (1980) Mechanism of biological control in a Fusarium-suppressive soil. Phytopathology 70: 412–417.
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.
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.
Smiley RW (1978) Colonization of wheat roots by Gaeumannomyces graminis inhibited by specific soils, microorganisms and ammonium nitrogen. Soil Biol. Biochem. 10: 175–179.
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.
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.
Van Bruggen AHC (1995) Plant disease severity in high-input compared to reduced-input and organic farming systems. Plant Dis. 79: 976–983.
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.
Walker JC & Snyder WC (1934) Pea wilt much less severe on certain soils. Univ. Wis. Agr. Exp. Sta. Bull. 428 (pp 95–96).
Westphal A & Becker JO (1999) Biological suppression and natural population decline of Heterodera schachtii in a California field. Phytopathology 89: 434–440.
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.
About this article
Cite this article
Mazzola, M. Mechanisms of natural soil suppressiveness to soilborne diseases. Antonie Van Leeuwenhoek 81, 557–564 (2002). https://doi.org/10.1023/A:1020557523557
- apple replant disease
- Fusarium wilt
- suppressive soils
- take-all decline