European Journal of Plant Pathology

, Volume 113, Issue 4, pp 417–435 | Cite as

Effect of Organic Management of Soils on Suppressiveness to Gaeumannomyces graminis var. tritici and its Antagonist, Pseudomonas fluorescens

  • Gerbert A. Hiddink
  • Ariena H. C. van Bruggen
  • Aad J. Termorshuizen
  • Jos M. Raaijmakers
  • Alexander V. Semenov
Article

Abstract

Organic management of soils is generally considered to reduce the incidence and severity of plant diseases caused by soil-borne pathogens. In this study, take-all severity on roots of barley and wheat, caused by Gaeumannomyces graminis var. tritici, was significantly lower in organically-managed than in conventionally-managed soils. This effect was more pronounced on roots of barley and wheat plants grown in a sandy soil compared to a loamy organically-managed soil. Fluorescent Pseudomonas spp. and in particular phlD+ pseudomonads, key factors in the take-all decline phenomenon, were represented at lower population densities in organically-managed soils compared to conventionally-managed soils. Furthermore, organic management adversely affected the initial establishment of introduced phlD+ P. fluorescens strain Pf32-gfp, but not its survival. In spite of its equal survival rate in organically- and conventionally-managed soils, the efficacy of biocontrol of take-all disease by introduced strain Pf32-gfp was significantly stronger in conventionally-managed soils than in organically-managed soils. Collectively, these results suggest that phlD+ Pseudomonas spp. do not play a critical role in the take-all suppressiveness of the soils included in this study. Consequently, the role of more general mechanisms involved in take-all suppressiveness in the organically-managed soils was investigated. The higher microbial activity found in the organically-managed sandy soil combined with the significantly lower take-all severity suggest that microbial activity plays, at least in part, a role in the take-all suppressiveness in the organically-managed sandy soil. The significantly different bacterial composition, determined by DGGE analysis, in organically-managed sandy soils compared to the conventionally-managed sandy soils, point to a possible additional role of specific bacterial genera that limit the growth or activity of the take-all pathogen.

Keywords

bacterial diversity disease suppression organic agriculture take-all suppressiveness Pseudomonas 

Abbreviations

2,4-DAPG

2,4-diacetylphloroglucinol

CFU

colony forming units

Ggt

Gaeumannomyces graminis var. tritici

Pf32-gfp

Pseudomonas fluorescens strain (Pf32) gfp tagged

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Ball DF (1964) Loss on ignition as an estimate of organic matter and organic carbon in non-calcareous soils. Journal of Soil Science. 15:84–92. In: Houba VJG, van der Lee JJ, Novozamsky I and Walinga I (1989) Soil and plant analysis. A serie of syllabi, part 5. Soil analysis procedures, Pages 4/1–4/2. Department of soil science and plant nutrition, Wageningen UniversityGoogle Scholar
  2. Bruggen van, AHC 1995Plant-disease severity in high-input compared to reduced-input and organic farming systemsPlant Disease79976984Google Scholar
  3. Bruggen van, AHC, Termorshuizen, AJ 2003Integrated approaches to root disease management in organic farming systemsAustralasian Plant Pathology32141156Google Scholar
  4. Carpenter-Boggs, L, Kennedy, AC, Reganold, JP 2000Organic and biodynamic management: effects on soil biologySoil Scientific Society of America Journal6416511659Google Scholar
  5. Cook, RJ 2003Take-all of wheatPhysiological and Molecular Plant Pathology627386Google Scholar
  6. Freitas, JR, Germida, JJ 1992aGrowth promotion of winter wheat by fluorescent pseudomonads under growth chamber conditionsSoil Biology and Biochemistry2411271135Google Scholar
  7. Freitas, JR, Germida, JJ 1992bGrowth promotion of winter wheat by fluorescent pseudomonads under field conditionsSoil Biology and Biochemistry2411371146Google Scholar
  8. Drinkwater, LE, Letourneau, K, Workneh, F, Bruggen van, AHC, Shennan, C 1995Fundamental differences between conventional and organic tomato agroecosystems in CaliforniaEcological Applications510981112Google Scholar
  9. Duffy, BK, Weller, DM 1994A semiselective and diagnostic medium for Gaeumanomyces graminis var. triticiPhytopathology8414071415Google Scholar
  10. Duffy, BK, Défago, G 1999Environmental factors modulating antibiotic and siderophore biosynthesis by Pseudomonas fluorescens biocontrol strainsApplied and Environmental Microbiology6524292438PubMedGoogle Scholar
  11. Eichner, CA, Erb, RW, Timmis, KN, Wagner-Döbler, I 1999Thermal gradient gel electrophoresis analysis of bioprotection from pollutant shocks in the activated sludge microbial communityApplied and Environmental Microbiology65102109PubMedGoogle Scholar
  12. Fravel, D 1999Hurdles and bottlenecks on the road to biocontrol of plant pathogensAustralasian Plant Pathology285356CrossRefGoogle Scholar
  13. Gerlagh, M 1968Introduction of Ophiobolus graminis Into New Polders and its Decline. Agricultural Reseach reports 713Centre for Agricultural Publishing and DocumentationWageningen97Google Scholar
  14. Germida, JJ, Siciliano, SD 2001Taxonomic diversity of bacteria associated with the roots of modern, recent and ancient wheat cultivarsBiology and Fertility of Soils33410415Google Scholar
  15. Glick, BR 1995The enhancement of plant growth by free-living bacteriaCanadian Journal of Microbiology41109117Google Scholar
  16. Gunapala, N, Scow, KM 1998Dynamics of soil microbial biomass and activity in conventional and organic farming systemsSoil Biology and Biochemistry30805816Google Scholar
  17. Hannukukulla, AO, Tapio, E 1990Conventional and organic cropping systems at Suitita. V. Cereal diseasesJournal of Agricultural Science Finland62339347Google Scholar
  18. Heinemeyer, O, Insam, H, Kaiser, EA, Walenzik, G 1989Soil microbial biomass and respiration measurements: an automated technique based on infra-red gas analysisPlant and Soil116191195CrossRefGoogle Scholar
  19. Heuer, H, Smalla, K 1997

    Application of denaturing gradient gel electrophoresis and temperature gradient gel electrophoresis for studying soil microbial communities

    Van Elsas, JDTrevors, JTWellington, EMH eds. Modern Soil MicrobiologyMarcel Dekker IncNew York353373
    Google Scholar
  20. Hollins, TW, Scott, PR, Gregory, RS 1986The relative resistance of wheat, rye and triticale to take-all caused by Gaeumannomyces graminisPlant Pathology3593100Google Scholar
  21. Houba VJG and Novozamsky I (1998) Influence of storage time and temperature of dry soils on pH and extractable nutrients using 0.01 M CaCl2. Fresenius’ Journal of Analytical Chemistry 360: 362–365. In: Houba VJG, van der Lee JJ, Novozamsky I and Walinga I (1989) Soil and plant analysis. A serie of syllabi, part 5. Soil analysis procedures, Pages 15/5–15/21. Department of soil science and plant nutrition, Wageningen UniversityGoogle Scholar
  22. Kloepper, JW, Lifshitz, R, Zablotowicz,  1989Free-living bacterial inocula for enhancing crop productivityTrends in Biotechnology73944CrossRefGoogle Scholar
  23. Knudsen, IMB, Debosz, K, Hockenhull, J, Jensen, DF, Elmholt, S 1999Suppressiveness of organically managed soils towards brown foot rot of barleyApplied Soil Ecology126172CrossRefGoogle Scholar
  24. Koch, B, Worm, J, Jensen, LE, Hojberg, O, Nybroe, O 2001Carbon limitation induces ss-dependent gene expression in Pseudomonas fluorescens in soilApplied and Environmental Microbiology6733633370CrossRefPubMedGoogle Scholar
  25. Koch, G 1991Fungal pathogens on winter wheat in comparison of 2 conventional farms and one biodynamic farm in Hess (FRG) 1986/87Zeitschrift für Pflanzenkrankheiten Pflanzenschütz98125136Google Scholar
  26. Landa, BB, Navas-Cortés, JA, Jiménez-Díaz, RM 2004Influence of temperature on plant-rhizobacteria interactions related to biocontrol potential for suppression of Fusarium wilt of chickpeaPlant Pathology53341352CrossRefGoogle Scholar
  27. Larkin, RP, Fravel, DR 2002Effects of varying environmental conditions on biological control of Fusarium wilt of tomato by nonpathogenic Fusarium sppPhytopathology9211601166Google Scholar
  28. Lotter, DW, Granett, J, Omer, AD 1999Differences in grape phylloxera related grapevine root damage in organically and conventionally-managed vineyards in CaliforniaHortScience3411081111Google Scholar
  29. Lucas, P, Jeuffroy, MH, Schoeny, A, Sarniquet, A 1997Basis for nitrogen fertilisation management of winter wheat crops infected with take-allAspects of Applied Biology50255262Google Scholar
  30. Mäder, P, Fliessbach, A, Dubois, D, Gunst, L, Fried, P, Niggli, U 2002Soil fertility and biodiversity in organic farmingScience29616941697PubMedGoogle Scholar
  31. Mazzola, M, Funnell, DL, Raaijmakers, JM 2004Wheat cultivar-specific selection of 2,4-diacetylphloroglucinol-producing fluorescent Pseudomonas species from resident soil populationsMicrobial Ecology48338348CrossRefPubMedGoogle Scholar
  32. Miller, WGL, Lindow, SE 1997An improved GFP cloning cassette designed for prokaryotic transcriptional fusionsGene191149153CrossRefPubMedGoogle Scholar
  33. Nei, M, Li, WH 1979Mathematical model for studying genetic variation in terms of restriction endonucleasesProceedings of the National Academy of Sciences of the United States of America7652695273PubMedGoogle Scholar
  34. Nieuwenhuizen J, Maas YEM and Middelburg JJ (1994) Rapid analysis of organic carbon and nitrogen in particulate materials. Marine Chemistry 45: 217–224. In: Houba VJG, van der Lee JJ, Novozamsky I and Walinga I (1989) Soil and plant analysis. A serie of syllabi, part 5. Soil analysis procedures, Pages 15/5–15/21. Department of soil science and plant nutrition, Wageningen UniversityGoogle Scholar
  35. Ownley, BH, Duffy, BK, Weller, DM 2003Identification and manipulation of soil properties to improve the biological control performance of phenazine-producing Pseudomonas fluorescensApplied and Environmental Microbiology6933333343CrossRefPubMedGoogle Scholar
  36. Patten, CL, Glick, BR 2002Role of Pseudomonas putida indoleacetic acid in development of the host plant root systemApplied and Environmental Microbiology6837953801CrossRefPubMedGoogle Scholar
  37. Peer van de, Y, Wachter, R 1994TREECON for Windows: a software package for the construction and drawing of evolutionary trees for the Microsoft Windows environmentComputer Applications in the Biosciences10569570Google Scholar
  38. Pierson, EA, Weller, DM 1994Use of mixtures of fluorescent pseudomonads to suppress take-all and improve growth of wheatPhytopathology84940947Google Scholar
  39. Raaijmakers, JM, Weller, DM, Thomashow, LS 1997Frequency of antibiotic-producing Pseudomonas spp. in natural environmentsApplied and Environmental Microbiology63881887Google Scholar
  40. Raaijmakers, JM, Weller, DM 1998Natural plant protection by 2,4-diacetylphloroglucinol producing Pseudomonas spp. in take-all decline soilsMolecular Plant-Microbe Interactions11144152Google Scholar
  41. Reganold, JP, Palmer, AS, Lockhart, JC, Macgregor, AN 1993Soil quality and financial performance of biodynamic and conventional farms in New ZealandScience260344349Google Scholar
  42. Rosado, AS, Duarte, GR, Seldin, L, Elsas, JD 1998Genetic diversity of nifH gene sequences in Paenibacillus azotofixans strains and soil samples analyzed by denaturing gradient gel electrophoresis of PCR-amplified gene fragmentsApplied and Environmental Microbiology6427702779PubMedGoogle Scholar
  43. Ryu, C, Farag, MA, Hu, C, Reddy, MS, Wei, H, Pare, PW, Kloepper, JW 2003Bacterial volatiles promote growth in ArabidopsisProceedings of the National Academy of Sciences of the USA10049274932PubMedGoogle Scholar
  44. Schabenberger, O, Pierce, FJ 2002Contemporary Statisical Models for the Plant And Soil SciencesCRC Press LLCBoca Raton, USA405520Google Scholar
  45. Schjønning, P, Elmholt, S, Munkholm, LJ, Debosz, K 2002Soil quality aspects of humid sandy loams as influenced by organic and conventional long-term managementAgriculture, Ecosystems and Environment88195214Google Scholar
  46. Shah, DA, Madden, LV 2004Nonparametric analysis of ordinal data in designed factorial experimentsPhytopathology943343Google Scholar
  47. Simon, A, Ridge, EH 1974The use of ampicillin in a simplified selective medium for the isolation of fluorescent pseudomonadsJournal of Applied Bacteriology37459460PubMedGoogle Scholar
  48. Smiley, RW, Cook, RJ 1973Relationship between take-all of wheat and rhizosphere pH in soils fertilized with ammonium- vs. nitrate-nitrogenPhytopathology63882890Google Scholar
  49. Smiley, RW 1978aColonization of wheat roots by Gaeumannomyces graminis inhibited by specific soils, microorganisms and ammonium-nitrogenSoil Biology and Biochemistry10175179Google Scholar
  50. Smiley, RW 1978bAntagonists of Gaeumannomyces graminis from the rhizoplane of wheat in soils fertilized with ammonium- or nitrate-nitrogenSoil Biology and Biochemistry10169174Google Scholar
  51. Smith, KP, Handelsman, J, Goodman, RM 1999Genetic basis in plants for interactions with disease suppressive bacteriaProceedings of the Nactional Academy of Sciences of the USA9647864790Google Scholar
  52. Souza, JT de, Raaijmakers, JM 2003Polymorphisms within the prnD and pltC genes from pyrrolnitrin and pyoluteorin-producing Pseudomonas and Burkholderia sppFEMS Microbiology Ecology432134CrossRefGoogle Scholar
  53. Thomashow, LS, Weller, DM 1988Role of a phenazine antibiotic from Pseudomonas fluorescens in biological control of Gaeumannomyces graminis var. triticiJournal of Bacteriology17034993508PubMedGoogle Scholar
  54. Weller, DM 1988Biological control of soil-borne pathogens in the rhizosphere with bacteriaAnnual Review of Phytopathology26379407CrossRefGoogle Scholar
  55. Weller, DM, Raaijmakers, JM, McSpadden Gardener, BB, Thomashow, LS 2002Microbial populations responsible for specific soil suppressiveness to plant pathogensAnnual Review of Phytopathology40309348CrossRefPubMedGoogle Scholar
  56. Whipps, JM 1997Developments in the biological control of␣soil-borne plant pathogensAdvances in Botanical Research261134Google Scholar
  57. Workneh, F, Bruggen, AHC 1994Microbial density, composition, and diversity in organically and conventionally-managed rhizosphere soil in relation to suppression of corky root of tomatoesApplied Soil Ecology.1219230CrossRefGoogle Scholar

Copyright information

© Springer 2005

Authors and Affiliations

  • Gerbert A. Hiddink
    • 1
  • Ariena H. C. van Bruggen
    • 1
  • Aad J. Termorshuizen
    • 1
  • Jos M. Raaijmakers
    • 2
  • Alexander V. Semenov
    • 1
  1. 1.Biological Farming Systems GroupWageningen UniversityWageningenThe Netherlands
  2. 2.Laboratory of PhytopathologyWageningen UniversityWageningenThe Netherlands

Personalised recommendations