European Journal of Plant Pathology

, Volume 140, Issue 2, pp 341–352 | Cite as

Biofumigation potential of Brassicaceae cultivars to Verticillium dahliae

  • Christian NeubauerEmail author
  • Benedikt Heitmann
  • Caroline Müller
Original Research


The biofumigation potential of brassicaceous green manures to Verticillium dahliae was systematically assessed. In a toxicological study, five different isothiocyanates (ITCs) were tested using a bioassay with sterile quartz sand artificially infested with microsclerotia. For 2-propenyl ITC, a LD90 value of 88.7 nmol g−1 was determined. Furthermore, 2-propenyl ITC with a dose of 150 nmol g−1 soil was tested in 22 naturally infested soils. The efficiency varied from 9 % to 92 % and was negatively correlated with the organic carbon content of the soils, indicating that in many soils much higher concentrations will be necessary to achieve sufficient control. To evaluate the biofumigation potential of different Brassicaceae, 19 cultivars of Brassica juncea, Rhaphanus sativus and Sinapis alba were grown in the field. Biomass production was measured and glucosinolate concentrations were analyzed. Simulating the field situation, the biofumigation effect of cultivars was assessed in a standardized laboratory bioassay with microsclerotia-infested sterile quartz sand amended with freeze-dried ground plant tissues. Amendments of B. juncea shoot tissue reduced the number of viable microsclerotia significantly with efficiencies from 69.3 to 81.3 %. Total potentially released amounts of 2-propenyl ITC ranged between 50.6–78.1 nmol g−1sand and indicate a clear ITC-related suppression. However these are considered too low for effective control in practice as low release efficiencies mean that effective levels fall well short of the estimated 150 nmol g−1 of soil required. In comparison with B. juncea, the R. sativus and S. alba were less effective due to lower concentrations and/or toxicity of the ITC released. In summary, the biofumigation potential of the cultivars tested appears insufficient alone for effective control, especially on soils with higher (>1.0 %) organic carbon content.


Verticillium dahliae Biofumigation Brassica juncea Glucosinolates Isothiocyanates 



This research was funded by the program FhprofUnd - Research at Universities of Applied Sciences and Companies - of the German Federal Ministry of Education and Research.


  1. Abdalsamee, M. A., & Müller, C. (2012). Effects of indole glucosinolates on performance and sequestration by the sawfly Athalia rosae and consequences of feeding on the plant defense system. Journal of Chemical Ecology, 38, 1366–1375.PubMedCrossRefGoogle Scholar
  2. Agerbirk, N., & Olsen, C. E. (2012). Glucosinolate structure and evolution. Phytochemistry, 77, 16–45.PubMedCrossRefGoogle Scholar
  3. Angus, J. F., Gardner, P. A., Kirkegaard, J. A., & Desmarchelier, J. M. (1994). Biofumigation - Isothiocyanates released from Brassica roots inhibit growth of the take-all fungus. Plant & Soil, 162, 107–112.CrossRefGoogle Scholar
  4. Bailey, K. L., & Lazarovits, G. (2003). Suppressing soil-borne diseases with residue management and organic amendments. Soil and Tillage Research, 72, 169–180.CrossRefGoogle Scholar
  5. Bellostas, N., Sorensen, J. C., & Sorensen, H. (2004). Qualitative and quantitative evaluation of glucosinolates in cruciferous plants during their life cycle. Proc. Ith IS: Biofumigation - a possible alternative to methylbromide ? Agroindustria, 3, 267–272.Google Scholar
  6. Bending, D. D., & Lincoln, S. D. (1999). Characterization of volatile sulphur-containing compounds produced during decomposition of Brassica juncea tissues in soil. Soil Biology and Biochemistry, 31, 695–703.CrossRefGoogle Scholar
  7. Borek, V., Morra, M. J., Brown, P. D., & McCaffrey, J. P. (1995). Transformation of the glucosinolate-derived allelochemicals allyl isothiocyanate and allyl nitrile in soil. Journal of Agricultural and Food Chemistry, 43, 1935–1940.CrossRefGoogle Scholar
  8. Brown, P. D., Morra, M. J., Mccaffrey, J. P., Auld, D. L., & Williams, L. (1991). Allelochemicals produced during glucosinolate degradation in soil. Journal of Chemical Ecology, 17, 2021–2034.PubMedCrossRefGoogle Scholar
  9. Brown, P. D., & Morra, M. J. (1997). Control of soil-borne plant pests using glucosinolate-containing plants. Advances in Agronomy, 61, 167–231.CrossRefGoogle Scholar
  10. Brown, P. D., Tokuhisa, J. G., Reichelt, M., & Gershenzon, J. (2003). Variation of glucosinolate accumulation among different organs and developmental stages of Arabidopsis thaliana. Phytochemistry, 62, 471–481.PubMedCrossRefGoogle Scholar
  11. Brown, J., & Morra, M. J. (2005). Glucosinolate-containing seed meal as a soil amendment to control plant pests (Subcontract Report NREL/SR-510-35254). Golden: National Renewable Energy Laboratory.CrossRefGoogle Scholar
  12. Cohen, M. F., Yamasaki, H., & Mazola, M. (2005). Brassica napus seed meal soil amendment modifies microbial community structure, nitric oxide production and incidence of Rhizoctonia root rot. Soil Biology and Biochemistry, 37, 1215–1227.CrossRefGoogle Scholar
  13. Collins, H. P., Alva, A., Boydston, R. A., Cochran, R. L., Hamm, P. B., Mcguire, A., & Riga, E. (2006). Soil microbial, fungal, and nematode responses to soil fumigation and cover crops under potato production. Biology and Fertility of Soils, 42, 247–257.CrossRefGoogle Scholar
  14. Daugovish, O., Downer, J., Becker, O., Browne, G., & Dunniway, J. (2004). Mustard-derived Biofumigation for vegetable crops and strawberries. Proc. Ith IS: Biofumigation - a possible alternative to methylbromide? Agroindustria, 3, 335–338.Google Scholar
  15. Debode, J., Clewes, E., De Backer, G., & Höfte, M. (2005). Lignin is involved in the reduction of Verticillium dahliae var. longisporum inoculum in soil by crop residue incorporation. Soil Biology Biochemistry, 37, 301–309.CrossRefGoogle Scholar
  16. Finney, D. J. (1971). Probit analysis (3rd ed.). Cambridge: Cambridge University Press.Google Scholar
  17. Gimsing, A. L., & Kirkegaard, J. A. (2006). Glucosinolate and isothiocyanate concentration in soil following incorporation of Brassica biofumigants. Soil Biology and Biochemistry, 38, 2255–2264.CrossRefGoogle Scholar
  18. Gimsing, A. L., & Kirkegaard, J. A. (2009). Glucosinolates and biofumigation: fate of glucosinolates and their hydrolysis products in soil. Phytochemistry Reviews, 8, 299–310.CrossRefGoogle Scholar
  19. Gimsing, A. L., Strobel, B. W., & Hansen, H. C. B. (2009). Degradation and sorption of 2-propenyl and benzylisothiocyanate. Environmental Toxicology and Chemistry, 28, 1178–1184.PubMedCrossRefGoogle Scholar
  20. Harris, D. C., Yang, Y. R., & Ridout, M. S. (1993). The detection and estimation of Verticillium dahliae in naturally infested soil. Plant Pathology, 42, 238–250.CrossRefGoogle Scholar
  21. Huisman, O. C. (1988). Seasonal colonization of roots of field-grown cotton by Verticillium dahliae and V. tricorpus. Phytopathology, 78, 708–717.CrossRefGoogle Scholar
  22. Kirkegaard, J. A., & Sarwar, M. (1998). Biofumigation potential of brassicas. I Variation in glucosinolate profiles of diverse field-grown brassicas. Plant and Soil, 201, 71–89.CrossRefGoogle Scholar
  23. Kirkegaard, J. A., & Matthiessen, J. (2004). Developing and refining the biofumigation concept. Proc. Ith IS: Biofumigation - a possible alternative to methylbromide ? Agroindustria, 3, 233–239.Google Scholar
  24. Manici, L. M., Lazzeri, L., & Palmieri, S. (1997). In vitro fungitoxic activity of some glucosinolates and their enzyme-derived products toward plant pathogenic fungi. Journal of Agricultural and Food Chemistry, 45, 2768–2773.CrossRefGoogle Scholar
  25. Matthiessen, J. N., & Kirkegaard, J. A. (2006). Biofumigation and Enhanced Biodegradation: Opportunity and Challenge in Soilborne Pest and Disease Management. Critical Reviews in Plant Sciences, 25, 235–265.CrossRefGoogle Scholar
  26. Martin, F. N. (2003). Development of alternative strategies for management of soilborne pathogens currently controlled with methyl bromide. Annual Review of Phytopathology, 41, 325–350.PubMedCrossRefGoogle Scholar
  27. Mol, L., van Halteren, J. M., Scholte, K., & Struik, P. C. (1996). Effects of crop species, crop cultivars and isolates of Verticillium dahliae on the population of microsclerotia in the soil, and consequences for crop yield. Plant Pathology, 45, 205–214.CrossRefGoogle Scholar
  28. Morra, M. J., & Kirkegaard, J. A. (2002). Isothiocyanate release from soil-incorporated Brassica tissues. Soil Biology and Biochemistry, 34, 1683–1690.CrossRefGoogle Scholar
  29. Müller, C., Agerbirk, N., Olsen, C. E., Boevé, J.-L., Schaffner, U., & Brakefield, P. M. (2001). Sequestration of host plant glucosinolates in the defensive hemolymph of the sawfly Athalia rosae. Journal of Chemical Ecology, 27, 2505–2516.PubMedCrossRefGoogle Scholar
  30. Neubauer, C., & Heitmann, B. (2011). Quantitative detection of Verticillium dahliae in soil as a basis for selection of planting sites in horticulture. Journal für Kulturpflanzen, 63, 1–8.Google Scholar
  31. Pegg, G. F., & Brady, B. L. (2002). Verticillium Wilts. Wallingford: CAB International.CrossRefGoogle Scholar
  32. Rosa, E. A. S., Heaney, R. K., Fenwick, G. R., & Portas, C. A. M. (1997). Glucosinolates in crop plants. Horticultural Reviews, 19, 19–215.Google Scholar
  33. Sarwar, M., & Kirkegaard, J. A. (1998). Biofumigation potential of brassicas. II Effect of environment and ontogeny on glucosinolate production and implications for screening. Plant and Soil, 201, 91–101.CrossRefGoogle Scholar
  34. Sarwar, M., Kirkegaard, J. A., Wong, P. T. W., & Desmarchelier, J. M. (1998). Biofumigation potential of brassicas. III In vitro toxicity of isothiocyanates to soil-borne fungal pathogens. Plant and Soil, 201, 103–112.CrossRefGoogle Scholar
  35. Smith, B. J., & Kirkegaard, J. A. (2002). In vitro inhibition of soil microorganisms by 2-phenylethyl isothiocyanate. Plant Pathology, 51, 585–593.CrossRefGoogle Scholar
  36. Smolinska, U., Morra, M. J., Knudsen, G. R., & James, R. L. (2003). Isothiocyanates produced by Brassicaceae species as inhibitors of Fusarium oxysporum. Plant Disease, 87, 407–412.CrossRefGoogle Scholar
  37. Travers-Martin, N., & Müller, C. (2008). Matching plant defence syndromes with performance and preference of a specialist herbivore. Functional Ecology, 22, 1033–1043.CrossRefGoogle Scholar
  38. Triky-Dotan, S., Austerweil, M., Steiner, B., Peretz-Alon, Y., Katan, J., & Gamliel, A. (2007). Generation and Dissipation of Methyl Isothiocyanate in Soils Following Metam Sodium Fumigation: Impact on Verticillium Cantrol and Potato Yield. Plant Disease, 91, 497–503.CrossRefGoogle Scholar
  39. Tsror, L., Shlevin, E., & Peeeeretz-Alon, I. (2005). Efficacy of metam sodium for controlling Verticillium dahliae prior to potato production in sandy soils. American Journal of Potato Research, 82, 419–423.CrossRefGoogle Scholar
  40. Warton, B., Matthiessen, J. N., & Shackleton, M. A. (2001). Glucosinolate Content and Isothiocyanate Evolution - Two Measures of the Biofumigation Potential of Plants. Journal of Agricultural and Food Chemistry, 49, 5244–5250.PubMedCrossRefGoogle Scholar
  41. Warton, B., Matthiessen, J. N., & Shackleton, M. A. (2003). Cross-enhancement: enhanced biodegradation of isothiocyanates in soils previously treated with metham sodium. Soil Biology and Biochemistry, 35, 1123–1127.CrossRefGoogle Scholar
  42. Wathelet, J. P., Iori, R., Leoni, O., Rollin, P., Quinsac, A., & Palmieri, S. (2004). Guidelines for glucosinolate analysis in green tissues used for biofumigation. Proc. Ith IS: Biofumigation - a possible alternative to methylbromide ? Agroindustria, 3, 257–266.Google Scholar

Copyright information

© Koninklijke Nederlandse Planteziektenkundige Vereniging 2014

Authors and Affiliations

  • Christian Neubauer
    • 1
    Email author
  • Benedikt Heitmann
    • 1
  • Caroline Müller
    • 2
  1. 1.Department of Plant Pathology, Faculty of Agricultural SciencesUniversity of Applied Sciences OsnabrückOsnabrückGermany
  2. 2.Department of Chemical Ecology, Faculty of BiologyBielefeld UniversityBielefeldGermany

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