Skip to main content
SpringerLink
Log in

Quantification of the relationship between the environment and Fusarium head blight, Fusarium pathogen density, and mycotoxins in winter wheat in Europe

  • Published:
European Journal of Plant Pathology Aims and scope Submit manuscript

Abstract

Measurements of local environmental conditions, intensity of Fusarium head blight (FHB) in wheat spikes, biomass of Fusarium graminearum, F. culmorum, and F. poae (pathogens causing FHB) and concentration of the mycotoxins deoxynivalenol (DON) and nivalenol (NIV) in harvested wheat grain were obtained in a total of 150 location-years, originating in three European countries (Hungary, Ireland, United Kingdom) from 2001 to 2004. Through window-pane methodology, the length and starting time of temporal windows where the environmental variables were significantly associated with the biological variables were identified. Window lengths of 5 to 30 days were evaluated, with starting times from 18 days before anthesis to harvest. Associations were quantified with nonparametric Spearman correlation coefficients. All biological variables were significantly associated with at least one evaluated environmental variable (P ≤ 0.05). Moisture-related variables (e.g., average relative humidity, hours of relative humidity above 80%) had the highest positive correlations with the biological variables, but there also was a significant negative correlation between average temperature and several biological variables. When significant correlations were found, they were generally for all window lengths, but for a limited number of window start times (generally before anthesis for disease index and after anthesis for the toxins and late-season fungal biomasses). Semi-partial Spearman correlation coefficients were used to evaluate the relationship between the environmental variables and the concentration of DON and NIV after the effects of FHB intensity and fungal biomass on the mycotoxins were removed. Significant semi-partial correlations were found between relative humidity variables and DON, and between temperature and relative humidity variables and NIV for time windows that started after anthesis (and not for any earlier time windows). Results confirm that the environment influences disease, fungal biomass, and mycotoxin production, and help refine the time windows where the association is greatest. However, variability in the relationships was high, indicating that no single environmental variable is sufficient for prediction of disease or mycotoxin contamination.

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
Fig. 3

Similar content being viewed by others

References

  • Arseniuk, E., Foremska, E., Góral, T., & Chełkowski, J. (1999). Fusarium head blight reactions and accumulation of deoxynivalenol (DON) and some of its derivatives in kernels of wheat, triticale and rye. Journal of Phytopathology, 147, 577–590.

    Article  CAS  Google Scholar 

  • Bai, G.-H., & Shaner, G. (1996). Variation in Fusarium graminearum and cultivar resistance to wheat scab. Plant Disease, 80, 975–979.

    Article  Google Scholar 

  • Birzele, B., Meier, A., Hindorf, H., Krämer, J., & Dehne, H.-W. (2002). Epidemiology of Fusarium infection and deoxynivalenol content in winter wheat in the Rhineland, Germany. European Journal of Plant Pathology, 108, 667–673.

    Article  CAS  Google Scholar 

  • Bottalico, A., & Perrone, G. (2002). Toxigenic Fusarium species and mycotoxins associated with head blight small-grains in Europe. European Journal of Plant Pathology, 108, 611–624.

    Article  CAS  Google Scholar 

  • Calvero, S. B., Jr., Coakley, S. M., & Teng, P. S. (1996). Development of empirical forecasting models for rice blast based on weather factors. Plant Pathology, 45, 667–678.

    Article  Google Scholar 

  • Coakley, S. M., McDaniel, L. R., & Shaner, G. (1985). Model for predicting severity of Septoria tritici blotch on winter wheat. Phytopathology, 75, 1245–1251.

    Article  Google Scholar 

  • Cowger, C., Patton-Özkurt, J., Brown-Guedira, G., & Perugini, L. (2009). Post-anthesis moisture increased Fusarium head blight and deoxynivalenol levels in North Carolina winter wheat. Phytopathology, 99, 320–327.

    Article  PubMed  CAS  Google Scholar 

  • Culler, M. D., Miller-Garvin, J., & Dill-Macky, R. (2007). Effect of extended irrigation and host resistance on deoxynivalenol accumulation in Fusarium-infected wheat. Plant Disease, 91, 1464–1472.

    Article  CAS  Google Scholar 

  • Demeke, T., Gräfenhan, T., Clear, R. M., Phan, A., Ratnayaka, I., Chapados, J., Patrick, S. K., Gaba, D., Lévesque, C. A., & Seifert, K. A. (2010). Development of a specific TaqMan® real-time PCR assay for quantification of Fusarium graminearum clade 7 and comparison of fungal biomass determined by PCR with deoxynivalenol content in wheat and barley. International Journal of Food Microbiology, 141, 45–50.

    Article  PubMed  CAS  Google Scholar 

  • De Wolf, E. D., Madden, L. V., & Lipps, P. E. (2003). Risk assessment models for wheat Fusarium head blight epidemics based on within-season weather data. Phytopathology, 93, 428–435.

    Article  PubMed  Google Scholar 

  • Doohan, F. M., Parry, D. W., Jenkinson, P., & Nicholson, P. (1998). The use of species-specific PCR-based assays to analyse Fusarium ear blight of wheat. Plant Pathology, 47, 197–205.

    Article  CAS  Google Scholar 

  • Gilbert, J., Woods, S. M., & Kromer, U. (2008). Germination of ascospores of Gibberella zeae after exposure to various levels of relative humidity and temperature. Phytopathology, 98, 504–508.

    Article  PubMed  CAS  Google Scholar 

  • Glynn, N. C., Hare, M. C., Parry, D. W., & Edwards, S. G. (2005). Phylogenetic analysis of EF- 1 alpha gene sequences from isolates of Microdochium nivale leads to elevation of varieties majus and nivale to species status. Mycological Research, 109, 872–880.

    Article  PubMed  CAS  Google Scholar 

  • Hart, L. P., Pestka, J. J., & Liu, M. T. (1984). Effect of kernel development and wet periods on production of deoxynivalenol in wheat infected with Gibberella zeae. Phytopathology, 74, 1415–1418.

    Article  CAS  Google Scholar 

  • Hope, R., Aldred, D., & Magan, N. (2005). Comparison of environmental profiles for growth and deoxynivalenol production by Fusarium culmorum and F. graminearum on wheat grain. Letters in Applied Microbiology, 40, 295–300.

    Article  PubMed  CAS  Google Scholar 

  • Jennings, P., Coates, M. E., Turner, J. A., Chandler, E. A., & Nicholson, P. (2004). Determination of deoxynivalenol and nivalenol chemotypes of Fusarium culmorum isolates from England and Wales by PCR assay. Plant Pathology, 53, 182–190.

    Article  CAS  Google Scholar 

  • Kriss, A. B., Paul, P. A., & Madden, L. V. (2010). Relationship between yearly fluctuations in Fusarium head blight intensity and environmental variables: A window-pane analysis. Phytopathology, 100, 784–797.

    Article  PubMed  CAS  Google Scholar 

  • Lacey, J., Bateman, G. L., & Mirocha, C. J. (1999). Effects of infection time and moisture on development of ear blight and deoxynivalenol production by Fusarium spp. in wheat. Annals of Applied Biology, 134, 277–282.

    Article  CAS  Google Scholar 

  • Lu, W. H., Chen, S. H., & Wang, Y. Z. (2001). Research of Fusarium head Scab in China. Beijing: Science Publisher.

    Google Scholar 

  • Magan, N. (2007). Fungi in extreme environments. In C. P. Kubicek & I. S. Druzhinina (Eds.), The mycota IV, environmental and microbial relationships (2nd ed., pp. 85–103). Berlin: Springer.

    Google Scholar 

  • Nganje, W. E., Bangsund, D. A., Leistritz, F. L., Wilson, W. W., & Tiapo, N. M. (2004). Regional economic impacts of Fusarium head blight in wheat and barley. Review of Agricultural Economics, 26, 332–347.

    Article  Google Scholar 

  • Oerke, E.-C., Meier, A., Dehne, H.-W., Sulyok, M., Krska, R., & Steiner, U. (2010). Spatial variability of Fusarium head blight pathogens and associated mycotoxins in wheat crops. Plant Pathology, 59, 671–682.

    Article  CAS  Google Scholar 

  • Parry, D. W., Jenkinson, P., & McLeod, L. (1995). Fusarium ear blight (scab) in small grain cereals – a review. Plant Pathology, 44, 207–238.

    Article  Google Scholar 

  • Paul, P. A., Lips, P. E., & Madden, L. V. (2005). Relationship between visual estimates of Fusarium head blight intensity and deoxynivalenol accumulation in harvested wheat grain: A meta-analysis. Phytopathology, 95, 1225–1236.

    Article  PubMed  CAS  Google Scholar 

  • Paul, P. A., Lipps, P. E., De Wolf, E., Shaner, G., Buechley, G., Adhikari, T., Ali, S., Stein, J., Osborne, L., & Madden, L. V. (2007). A distributed lag analysis of the relationship between Gibberella zeae inoculum density on wheat spikes and weather variables. Phytopathology, 97, 1608–1624.

    Article  PubMed  CAS  Google Scholar 

  • Pietravalle, S., Shaw, M. W., Parker, S. R., & van den Bosch, F. (2003). Modeling of relationships between weather and Septoria tritici epidemics on winter wheat: A critical approach. Phytopathology, 93, 1329–1339.

    Article  PubMed  CAS  Google Scholar 

  • Pugh, G. W., Johann, H., & Dickson, J. G. (1933). Factors affecting infection of wheat heads by Gibberella saubinetii. Journal of Agricultural Research, 46, 771–797.

    Google Scholar 

  • Rossi, V., Ravanetti, A., Pattori, E., & Giosuè, S. (2001). Influence of temperature and humidity on the infection of wheat spikes by some fungi causing Fusarium head blight. Journal of Plant Pathology, 83, 189–198.

    Google Scholar 

  • Sheskin, D. J. (2007). Spearman’s rank-order correlation coefficient. In Handbook of parametric and nonparametric statistical procedures, 4th edition, (pp. 1353–1370). Florida: Chapman & Hall/CRC

  • Simes, R. J. (1986). An improved Bonferroni procedure for multiple tests of significance. Biometrika, 73, 751–754.

    Article  Google Scholar 

  • Simpson, D. R., Rezanoor, H. N., Parry, D. W., & Nicholson, P. (2000). Evidence for differential host preference in Microdochium nivale var. majus and Microdochium nivale var. nivale. Plant Pathology, 49, 261–268.

    Article  Google Scholar 

  • Spearman, C. (1904). The proof and measurement of association between two things. The American Journal of Psychology, 15, 72–101.

    Article  Google Scholar 

  • Te Beest, D. E., Paveley, N. D., Shaw, M. W., & van den Bosch, F. (2008). Disease–weather relationships for powdery mildew and yellow rust on winter wheat. Phytopathology, 98, 609–617.

    Article  Google Scholar 

  • Trail, F., & Common, R. (2000). Perithecial development by Gibberella zeae: a light microscopy study. Mycologia, 92, 130–138.

    Article  Google Scholar 

  • Turner, J. A., & Jennings, P. (1997). The effect of increasing humidity on Fusarium ear blight and grain quality. Cereal Research Communications, 25, 825–826.

    Google Scholar 

  • van der Fels-Klerv, H. J., Burgers, S. L. G. E., & Booij, C. J. H. (2010). Descriptive modeling to predict deoxynivalenol in winter wheat in the Netherlands. Food Additives and Contaminants, 27, 636–643.

    Article  Google Scholar 

  • Waalwijk, C., Kastelein, P., de Vries, I., Kerényi, Z., van der Lee, T., Hesselink, T., Köhl, J., & Kema, G. (2003). Major changes in Fusarium spp. in wheat in the Netherlands. European Journal of Plant Pathology, 109, 743–754.

    Article  CAS  Google Scholar 

  • Ward, T. J., Bielawski, J. P., Kistler, H. C., Sullivan, E., & O’Donnell, K. (2002). Ancestral polymorphism and adaptive evolution in the trichothecene mycotoxin gene cluster of phytopathogenic Fusarium. Procedures of the National Academy of Sciences, 99, 9278–9283.

    Article  CAS  Google Scholar 

  • Westfall, P. H., Tobias, R. D., Rom, D., Wolfinger, R. D., & Hochberg, Y. (1999). Multiple comparisons and multiple tests: using the SAS System. Cary: SAS Institute Inc.

    Google Scholar 

  • Xu, X. M., Monger, W., Ritieni, A., & Nicholson, P. (2007). Effect of temperature and duration of wetness during initial infection periods on disease development, fungal biomass and mycotoxin concentrations on wheat inoculated with single, or combinations of, Fusarium species. Plant Pathology, 56, 943–956.

    Article  CAS  Google Scholar 

  • Xu, X.-M., Parry, D. W., Edwards, S. G., Cooke, B. M., Doohan, F. M., van Maanen, A., Brennan, J. M., Monaghan, S., Moretti, A., Tocco, G., Mule, G., Hornok, L., Giczey, G., Tatnell, J., Nicholson, P., & Ritieni, A. (2004). Relationship between the incidences of ear and spikelet infection of Fusarium ear blight in wheat. European Journal of Plant Pathology, 110, 959–971.

    Article  Google Scholar 

  • Xu, X.-M., Parry, D. W., Nicholson, P., Thomsett, M. A., Simpson, D., Edwards, S. G., Cooke, B. M., Doohan, F. M., Brennan, J. M., Moretti, A., Tocco, G., Mule, G., Hornok, L., Giczey, G., & Tatnell, J. (2005). Predominance and association of pathogenic fungi causing Fusarium ear blight in wheat in four European countries. European Journal of Plant Pathology, 112, 143–154.

    Article  Google Scholar 

  • Xu, X.-M., Nicholson, P., Thomsett, M. A., Simpson, D., Cooke, B. M., Doohan, F. M., Brennan, J., Monaghan, S., Moretti, A., Mule, G., Hornok, L., Beki, E., Tatnell, J., Ritieni, A., & Edwards, S. G. (2008a). Relationship between the fungal complex causing Fusarium head blight of wheat and environmental conditions. Phytopathology, 98, 69–78.

    Article  Google Scholar 

  • Xu, X.-M., Parry, D. W., Nicholson, P., Thomsett, M. A., Simpson, D., Edwards, S. G., Cooke, B. M., Doohan, F. M., Monaghan, S., Moretti, A., Tocco, G., Mule, G., Hornok, L., Béki, E., Tatnell, J., & Ritieni, A. (2008b). Within-field variability of Fusarium head blight pathogens and their associated mycotoxins. European Journal of Plant Pathology, 120, 21–34.

    Article  CAS  Google Scholar 

  • Zadoks, J. C., Chang, T. T., & Konzak, C. F. (1974). A decimal code for the growth stages of cereals. Weed Research, 14, 415–421.

    Article  Google Scholar 

Download references

Acknowledgements

European FHB data were obtained with the funding from the European Commission, Quality of Life and Management of Living Resources Programme (QOL), Key Action 5 on Sustainable Agriculture, Contract No. QLK5-CT-2000-01517 (RAMFIC). Financial support for L.

Madden was provided funding in part by USDA Special Grant 2010-34493-21087.

Author information

Authors and Affiliations

  1. Department of Plant Pathology, The Ohio State University, Ohio Agricultural Research and Development Center, Wooster, OH, USA

    Alissa B. Kriss, Pierce A. Paul & Laurence V. Madden

  2. East Malling Research, New Road, East Malling, Kent, ME19 6BJ, UK

    Xiangming Xu

  3. Department of Disease and Stress Biology, John Innes Centre, Norwich Research Park, Colney, Norwich, NR4 7UH, UK

    Paul Nicholson

  4. School of Biological and Environmental Science, UCD Agriculture and Food Science Centre, University College Dublin, Belfield, Dublin 4, Ireland

    Fiona M. Doohan

  5. Agricultural Biotechnology Center, Mycology Group of the Hungarian Academy of Sciences, Institute of Plant Protection, Szent István University, Gödöllő, Hungary

    Laszlo Hornok

  6. Dipartimento di Scienza degli Alimenti, Università di Napoli “Federico II”, Parco Gussone, 80055, Portici, (NA), Italy

    Alberto Rietini

  7. Crop and Environment Research Centre, Harper Adams University College, Newport, Shropshire, TF10 8NB, UK

    Simon G. Edwards

Authors
  1. Alissa B. Kriss
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Pierce A. Paul
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xiangming Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Paul Nicholson
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Fiona M. Doohan
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Laszlo Hornok
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Alberto Rietini
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Simon G. Edwards
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Laurence V. Madden
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Laurence V. Madden.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kriss, A.B., Paul, P.A., Xu, X. et al. Quantification of the relationship between the environment and Fusarium head blight, Fusarium pathogen density, and mycotoxins in winter wheat in Europe. Eur J Plant Pathol 133, 975–993 (2012). https://doi.org/10.1007/s10658-012-9968-6

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-012-9968-6

Keywords

Search

Navigation