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Population Dynamics of Biocontrol Agents and Pathogens in Soils and Rhizospheres

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Abstract

Understanding the dynamics between a pathogen and a biocontrol agent (BCA) in soil or in an infection court such as the rhizosphere is crucial for predicting the success of biological control. This is especially true for biological control using the strategy of reduction of initial inoculum prior to infection. By studying the population density fluxes over time, one can observe how the BCA and pathogen influence each other's population and life cycles, and how the biological and physical environment influence this relationship. Methods for quantifying fungi and bacteria in soil, including classical (dilution plating, baiting, bioassays), immunological (ELISA, IFC, immunomagnetic) and molecular (DNA hybridization, PCR, marker and reporter genes) methods, are discussed and critiqued. Finally, the value of mathematical modeling of population dynamics as a means of providing important information about the tripartite relationship between the pathogen, BCA, and host plant is reviewed.

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References

  • Adams PB (1990) The potential of mycoparasites for biological control of plant pathogens. Annu Rev Phytopathology 28: 59–72

    Google Scholar 

  • Ali-Shtayeh MS, Macdonald JD and Kabashima J (1991) A method for using commercial ELISA tests to detect zoospores of Phytophthora and Pythium species in irrigation water. Plant Disease 75: 305–311

    Google Scholar 

  • Assmus B, Hutzler P, Kirchhof G, Amann R, Lawrence JR and Hartmann A (1995) In situ localization of Azospirillumbrasilense in the rhizosphere of wheat with fluorescently labeled rRNA-targeted oligonucleotide probes and scanning confocal laser microscopy. Appl Environ Microbiol 61: 1013–1019

    Google Scholar 

  • Bailey DJ and Gilligan CA (1997) Biological control of pathozone behaviour and disease dynamics of Rhizoctonia solani by Trichoderma viride. New Phytologist 136: 359–367

    Google Scholar 

  • Bailey DJ and Gilligan CA (1999) Dynamics of primary and secondary infection in take-all epidemics. Phytopathology 89: 84–91

    Google Scholar 

  • Baker KF and Snyder WC (eds.) (1965) Ecology of Soil-Borne Plant Pathogens: Prelude to Biological Control. University of California Press, Berkeley, CA, 571 pp

    Google Scholar 

  • Baker RR (1978) Inoculum potential. In: Horsfall JG and Cowling EB (eds) Plant Disease, an Advanced Treatise. Vol II. How Disease Develops in Populations (pp 137–157) Academic Press, Inc., New York

    Google Scholar 

  • Bao JR (1999) Use of GUS for detection of Fusarium oxysporum in tomato roots. PhD Thesis, The University of Western Ontario, London

    Google Scholar 

  • Benson DM (1994) Inoculum. In: Campbell CL and Benson DM (eds) Epidemiology and Management of Root Diseases (pp 1–33) Springer-Verlag, Berlin

    Google Scholar 

  • Berger RD (1981) Comparison of the gompertz and logistic equations to describe plant disease progress. Phytopathology 71: 716–719

    Google Scholar 

  • Bounou S, Jabaji-Hare SH, Hogue R and Charest PM (1999) Polymerase chain reaction-based assay for specific detection of Rhizoctonia solani. Mycol Res 103: 1–8

    Google Scholar 

  • Bull CT, Weller DM and Thomashow LS (1991) Relationship between root colonization and suppression of Gaeumannomyces graminis var tritici by Pseudomonas fluorescens strain 2–79. Phytopathology 81: 954–959

    Google Scholar 

  • Campbell CL and Madden LV (1990) Introduction to Plant Disease Epidemiology. John Wiley and Sons, NY, 532 pp

    Google Scholar 

  • Campbell CL and Neher DA (1994) Estimating disease severity and incidence. In: Campbell CL and Benson DM (eds) Epidemiology and Management of Root Diseases (pp 115–147) Springer-Verlag, Berlin, 344 pp

    Google Scholar 

  • Campbell CL and Noe JP (1985) The spatial analysis of soilborne pathogens and root diseases. Annu Rev Phytopathol 23: 127–148

    Google Scholar 

  • Campbell CL and van der Gaag DJ (1993) Temporal and spatial dynamics of microsclerotia of Macrophomina phaseolina in three fields in North Carolina over four to five years. Phytopathology 83: 1434–1440

    Google Scholar 

  • Dane F and Shaw JJ (1993) Growth of bioluminescent Xanthomonas campestris pv. campestris in and on susceptible and resistant host plants. Mol Plant-Microb Interactions 6: 786–789

    Google Scholar 

  • de Weger LA, Dunbar P, Mahaffee WF, Lugtenberg BJJ and Sayler GS (1991) Use of bioluminescence markers to detect Pseudomonas spp. in the rhizosphere. Appl Environ Microbiol 57: 3641–3644

    Google Scholar 

  • Dewey FM, Thornton CR and Gilligan CA (1997) Use of monoclonal antibodies to detect, quantify and visualize fungi in soils. Advances in Botanical Research 24: 275–308

    Google Scholar 

  • Dhingra OD and Sinclair JB (1995) Basic Plant Pathology Methods, 2nd edn. CRC Lewis Publishers, Boca Raton, FL, 434 pp

    Google Scholar 

  • Eparvier A and Alabouvette C (1994) Use of ELISA and GUS-transformed strains to study competition between pathogenic and non-pathogenic Fusarium oxysporum for root colonization. Biocontrol Science and Technology 4: 35–47

    Google Scholar 

  • Gamard P, Sauriol F, Benhamou N, Bélanger RR and Paulitz TC (1997) Novel butyrolactones with antifungal activity produced by Pseudomonas aureofaciens strain 63–28. J Antibiotics 50: 742–749

    Google Scholar 

  • Gilligan CA (1990) Antagonistic interactions involving plant pathogens: fitting and analysis of models to non-monotonic curves for population and disease dynamics. New Phytologist 115: 649–665

    Google Scholar 

  • Gilligan CA (1994) Temporal aspects of the development of root disease epidemics. In: Campbell CL and Benson DM (eds) Epidemiology and Management of Root Diseases (pp 148–194) Springer-Verlag, Berlin, 344 pp

    Google Scholar 

  • Gilligan CA (1995) Modelling soil-borne plant pathogens: reaction-diffusion models. Can J Plant Path 17: 96–108

    Google Scholar 

  • Gilligan CA and Bailey DJ (1997) Components of pathozone behaviour. New Phytologist 136: 343–358

    Google Scholar 

  • Goodwin PH, Kirkpatrick BC and Duniway JM (1989) Cloned DNA probes for identification of Phytophthora parasitica. Phytopathology 79: 2482–2486

    Google Scholar 

  • Goodwin PH, Kirkpatrick BC and Duniway JM (1990) Identification of Phytophthora citrophthora with cloned DNA probes. Appl Environ Microbiol 56: 669–674

    Google Scholar 

  • Gottwald TR, Reynolds KM, Campbell C and Timmer LW(1992) Spatial and spatiotemporal autocorrelation analysis of citrus canker epidemics in citrus nurseries and groves in Argentina. Phytopathology 82: 843–851

    Google Scholar 

  • Green H and Jensen DF (1995) A tool for monitoring Trichoderma harzianum. II. The use of a GUS transformant for ecological studies in the rhizosphere. Phytopathology 85: 1436–1440

    Google Scholar 

  • Hahn D, Amann RI and Zeyer J (1994) Oligonucleotide probes for the detection and identification of bacteria. In: Ryder MH, Stephens PM and Bowen GD (eds) Improving Plant Productivity with Rhizosphere Bacteria (pp 163–171) CSIRO Division of Soils, Adelaide, Australia, 288 pp

    Google Scholar 

  • Hall R (ed) (1996) Principles and Practice of Managing Soilborne Plant Pathogens. American Phytopathological Society Press, St. Paul, MN, 330 pp

    Google Scholar 

  • Henson JM and French R (1993) The polymerase chain reaction and plant disease diagnosis. Annu Rev Phytopathology 31: 81–109

    Google Scholar 

  • Herdina, Jabaji-Hare S, Neate SM, Ophel-Keller K and Roget DK (1999) Persistence of DNA of Gaeumannomyces graminis var tritici in soil as measured by a DNA-based assay. In: Proceedings of the Annual Meeting of the Australian Plant Pathology Society, 27–30 September, Canberra

  • Higuchi R, Fockler C, Dolllinger G and Watson R (1993) Kinetic PCR: real time monitoring of DNA amplification reactions. Bio/Technology 11: 1026–1030

    Google Scholar 

  • Hornby D (ed) (1990) Biological Control of Soil-borne Plant Pathogens. CAB International, Wallingford, UK

    Google Scholar 

  • Hu X, Nazar RN and Robb J (1993) Quantification of Verticillium biomass in wilt disease development. Physiol Mol Plant Pathol 42: 23–36

    Google Scholar 

  • Hu X, Lai F-M, Reddy ASN and Ishimaru CA (1995) Quantitative detection of Clavibacter michiganensis subsp. sepedonicus by competitive polymerase chain reaction. Phytopathology 85: 1468–1473

    Google Scholar 

  • Johnson KB (1994) Dose-response relationships and inundative biological control. Phytopathology 84: 780–784

    Google Scholar 

  • Johnson KB and DiLeone JA (1999) Effect of antibiosis on antagonist dose-plant disease response relationships for the biological control of crown gall of tomato and cherry. Phytopathology 89: 974–980

    Google Scholar 

  • Jones JB and van Vuurde JWL (1996) Immunomagnetic isolation of Xanthomonas campestris pv. pelargonii. J Appl Bacteriol 81: 78–82

    Google Scholar 

  • Kluepfel DA, Kline EL, Skipper HD, Hughes TA, Gooden DT, Drahos DJ, Barry GF, Hemming BC and Brandt EJ (1991) The release and tracking of genetically engineered bacteria in the environment. Phytopathology 81: 348–352

    Google Scholar 

  • Kraus J and 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

    Google Scholar 

  • Kurian KM, Watson CJ and Wyllie AH (1999) DNA chip technology. J Pathol 187: 267–271

    Google Scholar 

  • Leblanc K, Charest PM and Hogue R (1999) A PCR ELISA for detection of Rhizoctonia solani, anastomosis group 3 (AG-3). Phytopathology 89: S44

    Google Scholar 

  • Lee SB, White TJ and Taylor JW (1993) Detection of Phytophthora species by oligonucleotide hybridization to amplified ribosomal DNA spacers. Phytopathology 83: 177–181

    Google Scholar 

  • Lemieux B, Aharoni A and Schena M (1998) Overview of DNA chip technology. Molecular Breeding 4: 277–289

    Google Scholar 

  • Lévesque CA, Harlton CE and de Cock AWAM (1998) Identification of some oomycetes by reverse dot blot hybridization. Phytopathology 88: 213–222

    Google Scholar 

  • Lipshutz RJ, Fodor SPA, Gingeras TR and Lockhart DJ (1999) High density synthetic oligonucleotide arrays. Nature Genetics Supplement 21: 20–24

    Google Scholar 

  • Lo C-T, Nelson EB, Hayes CK and Harman GE (1998) Ecological studies of transformed Trichoderma harzianum strain 1295–22 in the rhizosphere and on the phylloplane of creeping bentgrass. Phytopathology 88: 129–136

    Google Scholar 

  • Loper JE and Lindow SE (1997) Reporter gene systems useful in evaluating in situ gene expression by soil-and plant-associated bacteria. In: Hurst CJ, Knudsen GR, McInerney MJ, Stetzenbach LD and Walter MV (eds) Manual of Environmental Microbiology (pp 482–493) American Society for Microbiology, Washington, DC

    Google Scholar 

  • Lovic BR, Martyn RD and Miller ME (1995) Sequence analysis of the ITS region of rDNA in Monosporascus spp. to evaluate its potential for PCR-mediated detection. Phytopathology 85: 655–661

    Google Scholar 

  • MacGuidwin AE and Rouse DI (1990) Effect of Meloidogyne hapla, alone and in combination with subthreshold populations of Verticillium dahliae, on disease symptomology and yield of potato. Phytopathology 80: 482–486

    Google Scholar 

  • Mahaffee WF, Bauske EM, van Vuurde JWL, van der Wolf JM, van den Brink M and Kloepper JW (1997) Comparative analysis of antibiotic resistance, immunofluorescent colony staining, and a transgenic marker (bioluminescence) for monitoring the environmental fate of a rhizobacterium. Appl Environ Microbiol 63: 1617–1622

    Google Scholar 

  • Mahuku GS, Goodwin PH and Hall R (1995) A competitive polymerase chain reaction to quantify DNA of Leptosphaeria maculans during blackleg development in oilseed rape. Mol Plant-Microb Interactions 8: 761–767

    Google Scholar 

  • Mandeel Q and Baker R (1991) Mechanisms involved in biological control of Fusarium wilt of cucumber with strains of nonpathogenic Fusarium oxysporum. Phytopathology 81: 462–469

    Google Scholar 

  • Maor R, Puyesky M, Horwitz BA and Sharon A (1998) Use of green fluorescent protein (GFP) for studying development and fungal-plant interaction in Cochlioibolus heterostrophus. Mycol Res 102: 491–296

    Google Scholar 

  • Meikle A, Killham K, Prosser JI and Glover LA (1992) Luminometric measurement of population activity of genetically modified Pseudomonas fluorescens in the soil. FEMS Microbiology Letters 99: 217–220

    Google Scholar 

  • Mihail J (1989) Macrophomina phaseolina: spatio-temporal dynamics of inoculum and of disease in a highly susceptible crop. Phytopathology 79: 848–855

    Google Scholar 

  • Miller SA (1996) Detecting propagules of plant pathogenic fungi. Advances in Botanical Research 23: 73–102

    Google Scholar 

  • Miller SA, Madden LV and Schmitthenner AF (1997) Distribution of Phytophthora spp. in field soils determined by immunoassay. Phytopathology 87: 101–107

    Google Scholar 

  • Mills D and Russell BW (1999) Multiplex PCR ELISA detection of Clavibacter michiganensis subsp. sepedonicus in potato core fluid. Phytopathology 89: S53

    Google Scholar 

  • Montesinos E and Bonaterra A (1996) Dose-response models in biological control of plant pathogens: an empirical verification. Phytopathology 86: 464–472

    Google Scholar 

  • Nicot P and Rouse DI (1987) Relationship between soil inoculum density of Verticillium dahliae and systemic colonization of potato stems in commercial fields over time. Phytopathology 77: 1346–1355

    Google Scholar 

  • Oyarzun PJ, Dijst G, Zoon FC and Maas PWTh (1997) Comparison of soil receptivity to Thielaviopsis basicola, Aphanomyces euteiches, and Fusarium solani f. sp. pisi causing root rot in pea. Phytopathology 87: 534–541

    Google Scholar 

  • Parker CA, Rovira AD, Moore KJ and Wong PTW (eds) (1985) Ecology and Management of Soilborne Plant Pathogens. American Phytopathological Society Press, St. Paul, MN, 358 pp

    Google Scholar 

  • Poggi Pollini G, Giunchedi L and Bassani R (1997) Immunoenzymatic detection of PCR products for the identification of phytoplasmas in plants. J Phytopathology 145: 371–374

    Google Scholar 

  • Raaijmakers JM, Leeman M, van Oorschot MMP, van der Sluis I, Schippers B and Bakker PAHM (1995) Dose-response relationships in biological control of Fusarium wilt of radish by Pseudomonas spp. Phytopathology 85: 1075–1081

    Google Scholar 

  • Raaijmakers JM and Weller DM (1998) Natural plant protection by 2,4–diacetylphloroglucinol-producing Pseudomonas spp. in take-all decline soils. Mol Plant-Microb Interactions 11: 144–152

    Google Scholar 

  • Rankin L (1992) Evaulation of native rhizosphere bacteria for use as biological control agents against Pythium aphanidermatum root rot of European greenhouse cucumbers. MSc Thesis, McGill University, Montreal, Quebec

    Google Scholar 

  • Rankin L and Paulitz TM (1994) Evaluation of rhizosphere bacteria for biological control of Pythium root rot of greenhouse cucumbers in hydroponic culture. Plant Disease 78: 447–451

    Google Scholar 

  • Reynolds KM, Madden LV and Ellis MA (1988) Spatio-temporal analysis of epidemic development of leather rot of strawberry. Phytopathology 78: 240–246

    Google Scholar 

  • Sanford GB (1926) Some factors affecting the pathogenicity of Actinomyces scabies. Phytopathology 16: 525–546

    Google Scholar 

  • Schaad NW, Berthier-Schaad Y, Sechler A and Knorr D (1999) Detection of Clavibacter michiganensis subsdp. sepedonicus in potato tubers by BIO-PCR and an automated real-time fluorescence detection system. Plant Disease 83: 1095–1100

    Google Scholar 

  • Schilling AG, Möller EM and Geiger HH (1996) Polymerase chain reaction-based assays for species-specific detection of Fusarium culmorum, F. graminearum and F. avenaceum. Phytopathology 86: 515–522

    Google Scholar 

  • Schneider RW (1984) Effects of nonpathogenic strains of Fusarium oxysporum on celery root infection by F. oxysporum f. sp. apii and a novel use of the Lineweaver-Burk double reciprocal plot technique. Phytopathology 74: 646–653

    Google Scholar 

  • Schober BM and van Vuurde JWL (1997) Detection and enumeration of Erwinia carotovora subsp. atroseptica using spiral plating and immunofluorescence colony staining. Can J Microbiol 43: 847–853

    Google Scholar 

  • Schoen CD, Knorr D and Leone G (1996) Detection of potato leaf-roll virus in dormant potato tubers by immunocapture and a fluorogenic 50 nuclease RT-PCR assay. Phytopathology 86: 993–999

    Google Scholar 

  • Seresinhe N, Reyes AA and Brown GL (1997) Suppression of rhizoctonia stem rot on poinsettias with Pseudomonas aureofaciens strain 63–28. Can J Plant Pathol 19: 116

    Google Scholar 

  • Shaw JJ, Dane F, Geiger D and Kloepper JW (1992) Use of bioluminescence for detection of genetically engineered microorganisms released into the environment. Appl Environ Microbiol 58: 267–273

    Google Scholar 

  • Silcock DJ, Waterhouse RN, Glover LA, Prosser JI and Killham K (1992) Detection of a single genetically modified bacterial cell in soil by using charge coupled device-enhanced microscopy. Appl Environ Microbiol 58: 2444–2448

    Google Scholar 

  • Singleton LL, Mihail JD and Rush CM (eds) (1992) Methods for Research on Soilborne Phytopathogenic Fungi. American Phytopathological Society Press, St. Paul, MN

    Google Scholar 

  • Smith KP, Handelsman J and Goodman RM (1997) Modeling dose-response relationships in biological control: partitioning host responses to the pathogen and biocontrol agent. Phytopathology 87: 720–729

    Google Scholar 

  • Thornton CR (1996) Detection and quantification of Rhizoctonia solani in soil by monoclonal antibody-based immuno-magnetic bead assay. Soil Biol Biochem 28: 527–532

    Google Scholar 

  • Thornton CR, O'Neill TM, Hilton G and Gilligan CA (1999) Detection and recovery of Rhizoctonia solani in naturally infested glasshouse soils using a combined baiting, double monoclonal antibody ELISA. Plant Pathology 48: 627–634

    Google Scholar 

  • Timmer LW, Menge JA, Zitko SE, Pond E, Miller SA and Johnson ELV (1993) Comparison of ELISA techniques and standard isolation methods for Phytophthora detection in citrus orchards in Florida and California. Plant Disease 77: 791–796

    Google Scholar 

  • Weindling R (1932) Trichoderma lignorum as a parasite of other soil fungi. Phytopathology 22: 837–845

    Google Scholar 

  • van der Wolf JM, Hyman LJ, Jones DAC, Grevesse C, van Beckhoven JRCM, van Vuurde JWL and Pérombelon MCM (1996) Immunomagnetic separation of Erwinia carotovora subsp. atroseptica from potato peel extracts to improve detection sensitivity on a crystal violet pectate medium or by PCR. J Appl Bacteriol 80: 487–495

    Google Scholar 

  • van Vuurde JWL (1990) Immunofluorescence colony staining. In: Hampton R, Ball E and De Boer S (eds) Serological Methods for Detection and Identification of Viral and Bacterial Plant Pathogens. A Laboratory Manual (pp 299–305) APS Press, St. Paul, MN

    Google Scholar 

  • van Wymelenberg AJ, Cullen D, Spear RN, Schoenike B and Andrews JH (1997) Expression of green fluorescent protein in Aureobasidium pullans and quantification of the fungus on leaf surfaces. Biotechniques 26: 44–46

    Google Scholar 

  • Volossiouk T, Robb EJ and Nazar RN (1995) Direct DNA extraction for PCR-mediated assays of soil organisms. Appl Environ Microbiol 61: 3972–3976

    Google Scholar 

  • Xiao CL, Hao JJ and Subbarao KV (1997) Spatial patterns of microsclerotia of Verticillium dahliae in soil and Verticillium wilt of cauliflower. Phytopathology 87: 325–331

    Google Scholar 

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Paulitz, T. Population Dynamics of Biocontrol Agents and Pathogens in Soils and Rhizospheres. European Journal of Plant Pathology 106, 401–413 (2000). https://doi.org/10.1023/A:1008733927515

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