Skip to main content
SpringerLink
Log in

Aerobiological aspects of quarantine risks in grain warehouses: a study on bunt (Tilletia spp.) dispersal

  • Original Paper
  • Published:
Aerobiologia Aims and scope Submit manuscript

Abstract

Several countries refuse the import of wheat if it is contaminated with Tilletia spp. Local quarantine regulations are in effect regarding Tilletia indica and Tilletia controversa as part of a strategy to first hinder the disease from establishing in the country or eradicate the disease and, more recently, to prohibit the spread of it. Because of the economic importance of these fungal pathogens in the warehouses, the aerobiology of Tilletia spp. should be known better. Air (with a portable Hirst-type volumetric impaction sampler) and wheat seeds were collected in two central grain warehouses in Budapest (Bp) and Jászapáti (Ja) and in 14 farm warehouses. Quarantine organisms (T. controversa and T. indica) were not detected in any of the samples. Tilletia caries dominated in the air and seed samples, while Tilletia laevis were present only in a low concentration in the samples collected in Bp, but this fungus was absent in both Ja and the farm warehouses. Teliospore levels of the two different sites of wheat storage rooms in Bp were compared, but no significant difference was found between them (p = 0.16). Similarly, the volume of stored wheat did not significantly affect the Tilletia spp. concentrations (p = 0.46) in the air. Teliospore levels in seed samples correlated with those in the air samples which were collected from above the wheat heaps (r = 0.596, p < 0.05). In Bp, teliospore dispersal takes place rapidly between storage rooms and floors via open-top walls and spouts, respectively. Consequently, there is a higher risk of contamination because of the high teliospore concentration in the air and the high probability of teliospore dispersal. It is proposed that warehouses could be tested for quarantine or economically important Tilletia spp. not only by seed sampling but by aerobiological methods as well. Our results claim attention on the quarantine risk of airborne contamination with Tilletia spp. teliospores of grain warehouses, and some modification in control strategy against warehouse contamination is suggested.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Bechtel, D. B., Wilson, J. D., Eutace, W. D., Behnke, K. C., Whitaker, T. B., Peterson, G. L., et al. (1999). Fate of dwarf bunt fungus teliospores during milling of wheat to flour. Cereal Chemistry, 76, 270–275.

    Article  CAS  Google Scholar 

  • Bonde, M. R., Peterson, G. L., Schaad, N. W., & Smilanick, J. L. (1997). Karnal bunt of wheat. Plant Disease, 81, 1370–1377.

    Article  Google Scholar 

  • Calderon, C., Ward, E., Freeman, J., & McCartney, A. (2002). Detection of airborne fungal spores sampled by rotating-arm and Hirst-type spore traps using polymerase chain reaction assays. Journal of Aerosol Science, 33, 283–296.

    Article  CAS  Google Scholar 

  • Cattlin, N. D., Murray, T. D., & Parry, D. W. (1998). Bunts/smuts. In A. Colour (Ed.), Handbook of diseases of small grain cereal crops (pp. 9–11). London: Manson Publishing.

    Google Scholar 

  • Chen, K., Yao, W., Zhang, Z., Xiao, Y., Yan, J., Xu, Y., et al. (2002). Establishment of risk analysis and divisions of TCK in China. Acta Phytopathologica Sinica, 32(4), 312–318.

    CAS  Google Scholar 

  • Cheung, S.-S. C., & Gerrard, J. W. (1980). Airborne fungal spores in grain elevators of Saskatchewan. In J. A. Dosman & D. J. Cotton (Eds.), Occupational pulmonary diseases, focus on grain dust and health (pp. 463–468). New York, NY: Academic Press.

    Google Scholar 

  • Cook, R. J., & Veseth, R. J. (1991). Wheat health management. St. Paul, MN: APS Press.

    Google Scholar 

  • Crotzer, V., & Levetin, E. (1996). The aerobiological significance of smut spores in Tulsa, Oklahoma. Aerobiologia, 12, 177–184.

    Article  Google Scholar 

  • DA, U. S. (1998). Risk assessment for the importation of U.S. milling wheat containing teliospores of Tilletia controversa (TCK) into the People’s Republic of China (pp. 1–45). Washington, D.C.: United States Department of Agriculture.

    Google Scholar 

  • EFSA Panel on Plant Health (PLH). (2010). Scientific opinion on a quantitative pathway analysis of the likelihood of Tilletia indica M. Introduction into EU with importation of US wheat. EFSA Journal, 8(6), 1621–1709.

    Google Scholar 

  • FAO/IPGRI. (1995). Technical guidelines for the safe movement of germplasm (pp. 24–27).

  • Forster, R. L., & Goates, B. J. (1997). Karnal bunt. University of Idaho. CIS 1067. http://www.cals.uidaho.edu/edComm/pdf/CIS/CIS1067.pdf. Accessed May 10, 2010.

  • Fuentes-Davila, G. (1996). 3. Karnal bunt of wheat. In R. D. Wilcoxson & E. E. Saari (Eds.), Bunt and smut diseases of wheat: Concepts and methods of disease management (pp. 26–32). Mexico: CIMMYT.

    Google Scholar 

  • Goates, B. J. (2008). Quantification of Tilletia indica teliospores in sori of commercially harvested wheat grains. Phytopathology, 98(6), S60.

    Google Scholar 

  • Hamilton, E. D. (1959). Studies in the air spora. Acta Allergologica, 13(2), 143–173.

    Article  CAS  Google Scholar 

  • Hanna, W. F., Vickery, H. B., & Pucher, G. W. (1932). The isolation of trimethylamine from spores of Tilletia laevis. The stinking smut of wheat. The Journal of Biological Chemistry, 97(2), 351–358.

    CAS  Google Scholar 

  • Herrman, T. J., Jardine, D. J., Miller, T., & Sim, T. (2003). Karnal bunt. Questions and answers. Manhattan, KS: Kansas State University.

    Google Scholar 

  • Hirst, J. M. (1952). An automatic volumetric spore trap. Annals of Applied Biology, 39, 257–265.

    Article  Google Scholar 

  • Jia, W. M., Zhou, Y. L., Duan, X. Y., Luo, Y., Ding, S. L., Cao, X. R., et al. (2013). Assessment of risk of establishment of wheat dwarf bunt (Tilletia controversa) in China. Journal of Integrative Agriculture, 12(1), 87–94.

    Article  Google Scholar 

  • Jones, D. R. (2009). Towards a more reasoned assessment of the threat to wheat crops from Tilletia indica, the cause of Karnal bunt disease. European Journal of Plant Pathology, 123, 247–259.

    Article  Google Scholar 

  • Lacey, J. (1980). The microflora of grain dusts. In J. A. Dosman & D. J. Cotton (Eds.), Occupational pulmonary diseases, focus on grain dust and health (pp. 417–440). New York, NY: Academic Press.

    Google Scholar 

  • Lacey, J. (1981). The aerobiology of conidial fungi. In C. T. Cole & B. Kendrick (Eds.), The biology of conidial fungi (Vol. I, pp. 370–416). New York, NY: Academic Press.

    Google Scholar 

  • Lee, S. B., & Taylor, J. W. (1990). Isolation of DNA from fungal mycelia and single spores. In M. A. Innis, D. H. Gelfand, J. J. Sninsky, & T. J. White (Eds.), PCR protocols: A guide to methods and applications (pp. 282–287). San Diego, CA: Academic Press.

    Google Scholar 

  • Majumder, D., Rajesh, T., Suting, E. G., & Debbarma, A. (2013). Detection of seed borne pathogens in wheat: Recent trends. Australian Journal of Crop Science, 7(4), 500–507.

    CAS  Google Scholar 

  • Mathre, D. E. (1996). Dwarf bunt: Politics, identification, and biology. Annual review of Phytopathology, 34, 67–85.

    Article  CAS  Google Scholar 

  • Matur, S. B., & Kongsdal, O. (2003). Common laboratory seed health testing methods for detecting fungi (p. 74). Bassersdorf, Switzerland: International Seed Health Testing Association.

  • OEPP/EPPO. (1982). Data sheets on quarantine organisms no. 83, Tilletia controversa Kühn. OEPP/EPPO Bulletin, 12, 137–142.

    Google Scholar 

  • OEPP/EPPO. (1991). Quarantine procedure no. 37, Tilletia indica. Bulletin OEPP/EPPO Bulletin, 21, 265–266.

    Article  Google Scholar 

  • OEPP/EPPO. (2007). Tilletia indica. Diagnostics PM 7/29 (2). Bulletin OEPP/EPPO Bulletin, 37, 503–520.

    Article  Google Scholar 

  • Peterson, G. L., Whitaker, T. B., Stefanski, R. J., Podleckis, E. V., Phillips, J. G., Wu, J. S., et al. (2009). A risk assessment model for importation of United States milling wheat containing Tilletia controversa. Plant Disease, 93, 560–573.

    Article  Google Scholar 

  • Pimentel G., Carris L. M., Levy L., & Meyer R. J. (1998). Genetic variability among isolates of Tilletia barclayana, T. indica and allied species. Mycologia, 90, 1017–1027.

  • Rattan, G. S., & Aujla, S. S. (1990). Spore load in Karnal bunt infected wheat grains. Annals of Biology, 7(2), 225–228.

    Google Scholar 

  • Russel, B. W., & Mills, D. (1994). Morphological, physiological, and genetic evidence in support of a conspecific status for Tilletia caries, T. controversa and T. foetida. Phytopathology, 84, 576–582.

    Article  Google Scholar 

  • Savino, E., & Caretta, G. (1992). Airborne fungi in an Italian rice mill. Aerobiologia, 8, 267–275.

    Article  Google Scholar 

  • Sinha, R. N. (1992). The fungal community in the stored grain ecosystem. In G. C. Carroll & D. T. Wicklow (Eds.), The fungal community (pp. 797–815). New York, NY: Marcel Dekker.

    Google Scholar 

  • Suffert, F., Latxague, É., & Sache, I. (2009). Plant pathogens as agroterrorist weapons: assessment of the threat for European agriculture and forestry. Food Security, 2, 221–232.

    Article  Google Scholar 

  • Tan, M.-K., Brennan, J. P., Wright, D., & Murray, G. M. (2013). A review of the methodology to detect and identify Karnal bunt—a serious biosecurity threat. Australasian Plant Pathology, 42, 95–102.

    Article  Google Scholar 

  • Trione, E. J. (1982). Dwarf bunt of wheat and its importance in international wheat-trade. Plant Disease, 66(11), 1083–1088.

    Article  Google Scholar 

  • Tse, K. S. N., Craven, N., & Cherniak, R. M. (1980). Allergy to saprophytic fungi in grain workers. In J. A. Dosman & D. J. Cotton (Eds.), Occupational pulmonary diseases, focus on grain dust and health (pp. 335–346). New York, NY: Academic press.

    Google Scholar 

  • USDA, Agricultural Marketing Grain Division Service. (1974). Examination of the spores of T. controversa (dwarf bunt).

  • Vánky, K. (2012). Smut fungi of the world. St. Paul, MN: APS Press.

    Google Scholar 

  • Wei, S. Q., Zhang, Z., & Zheng, Y. S. (1995). Evaluation on the establishment potential of wheat dwarf bunt with bioclimatic analogical distance model. Acta Agriculturae Universitatis Pekinensis, 21, 127–131.

    Google Scholar 

  • West, J. S., Atkins, S. D., Emberlin, J., & Fitt, B. D. L. (2008). PCR to predict risk of airborne disease. Trends in Microbiology, 16(8), 380–387.

    Article  CAS  Google Scholar 

  • Whitby, S. M. (2002). Biological warfare against crops. New York, NY: Palgrave.

    Google Scholar 

  • White, T. J., Bruns, T., Lee, S., & Taylor, J. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In M. A. Innis, D. H. Gelfand, J. J. Sninsky, & T. J. White (Eds.), PCR protocols: A guide to methods and applications (pp. 315–322). San Diego, CA: Academic Press.

    Google Scholar 

  • Wiese, M. V. (1998). Compendium of wheat diseases (2nd ed., pp. 18–21). Minnesota, MN: APS Press.

  • Wilcoxson, R. D., & Saari, E. E. (Eds.). (1996). Bunt and smut diseases of wheat: Concepts and methods of disease management (p. 26). Mexico: CIMMYT.

    Google Scholar 

  • Williams, R. H., Ward, E., & McCartney, H. A. (2001). Methods for integrated air sampling and DNA analysis for the detection of airborne fungal spores. Applied and Environmental Microbiology, 67, 2453–2459.

    Article  CAS  Google Scholar 

  • Zhou, Y., Duan, X., & Jia, W. (2006). Risk assessment of Tilletia controversa establishment in China. Czech Journal of Genetics and Plant Breeding, 42, 84.

    Google Scholar 

Download references

Acknowledgments

This research was supported by Hungarian State Research Grants (OTKA F67908, 77612) and the National Food Chain Safety Office. The authors would like to thank Ede Böszörményi for revising the English version of the manuscript.

Author information

Authors and Affiliations

  1. Plant Health and Molecular Biology Laboratory, Directorate of Plant Protection, Soil Conservation and Agri-Environment, National Food Chain Safety Office, Budaörsi út 141-145, 1118, Budapest, Hungary

    Ágnes Halász

  2. Department of Aerobiological Monitoring, National Institute of Environmental Health, Albert Flórián út 2-6, 1097, Budapest, Hungary

    Donát Magyar & János Bobvos

Authors
  1. Ágnes Halász
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Donát Magyar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. János Bobvos
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Donát Magyar.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Halász, Á., Magyar, D. & Bobvos, J. Aerobiological aspects of quarantine risks in grain warehouses: a study on bunt (Tilletia spp.) dispersal. Aerobiologia 30, 161–171 (2014). https://doi.org/10.1007/s10453-013-9314-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10453-013-9314-2

Keywords

Search

Navigation