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Identification of meteorological predictors of Fusarium graminearum ascospore release using correlation and causality analyses

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Abstract

Fusarium head blight (FHB), caused by the plant pathogen Fusarium graminearum, is a significant threat to small grains production worldwide. Additional knowledge is required to clarify the influence of meteorological conditions on the release of ascospores of F. graminearum. Here, a new application of causality analysis is used to determine how meteorological conditions cause ascospore release. Two types of causality analyses, convergent cross mapping and multivariate state space forecasting, were applied to field measurements of airborne ascospores of F. graminearum over two years. Convergent cross mapping identified relative humidity, solar radiation, wind speed, and air temperature as predictors of ascospore release. Multivariate state space forecasting identified solar radiation and relative humidity as effective predictors of ascospore release. Increased concentration of ascospores in the atmosphere primarily occurred during periods of high relative humidity, low solar radiation, and low wind speed. Results from this study may assist producers in managing FHB in small grains by narrowing the timing and application of fungicides around major ascospore release intervals predicted by meteorological conditions.

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References

  • Abarbanel, H. (1996). Analysis of observed chaotic data. Berlin: Springer-Verlag.

    Book  Google Scholar 

  • Ayers, J., Pennypacker, S., Nelson, P., & Pennypacker, B. (1975). Environmental factors associated with airborne ascospores of Gibberella zeae in corn and wheat fields. Phytopathology, 65:835.

  • Bolton, D. (1980). The computation of equivalent potential temperature. Monthly Weather Review, 108(7), 1046–1053.

    Article  Google Scholar 

  • BozorgMagham, A. E., Motesharrei, S., Penny, S. G., & Kalnay, E. (2015). Causality analysis: Identifying the leading element in a coupled dynamical system. PLoS One, 10(6), e0131226. doi:10.1371/journal.pone.0131226.

  • Burt, P., Rutter, J., & Gonzales, H. (1997). Short-distance wind dispersal of the fungal pathogens causing Sigatoka diseases in banana and plantain. Plant Pathology, 46(4), 451–458.

    Article  Google Scholar 

  • Burt, P., Rosenberg, L., Rutter, J., Ramirez, F., & Gonzales, O. H. (1999). Forecasting the airborne spread of Mycosphaerella fijiensis, a cause of black Sigatoka disease on banana: estimations of numbers of perithecia and ascospores. Annals of Applied Biology, 135(1), 369–377.

    Article  Google Scholar 

  • Buttner, M. P., & Stetzenbach, L. D. (1993). Monitoring airborne fungal spores in an experimental indoor environment to evaluate sampling methods and the effects of human activity on air sampling. Applied and Environmental Microbiology, 59(1), 219–226.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen, X., & Yuan, C. (1984). Application of microcomputer in studying wheat scab epidemiology and forecasting. Zhejiang Agricultural Science, 2, 55–60.

    Google Scholar 

  • Clark, A. T., Ye, H., Isbell, F., Deyle, E. R., Cowles, J. M., Tilman, D., et al. (2015). Spatial 'convergent cross mapping' to detect causal relationships from short time-series. Ecology, 96(5), 1174–1181.

    Article  PubMed  Google Scholar 

  • Clarkson, J. P., Staveley, J., Phelps, K., Young, C. S., & Whipps, J. M. (2003). Ascospore release and survival in Sclerotinia sclerotiorum. Mycological Research, 107(02), 213–222.

    Article  PubMed  Google Scholar 

  • Del Ponte, E. M., Fernandes, J. M. C., Pavan, W., & Baethgen, W. E. (2009). A model-based assessment of the impacts of climate variability on fusarium head blight seasonal risk in southern Brazil. Journal of Phytopathology, 157(11–12), 675–681.

  • Deyle, E. R., Fogarty, M., Hsieh, C.-H., Kaufman, L., MacCall, A. D., Munch, S. B., et al. (2013). Predicting climate effects on Pacific sardine. Proceedings of the National Academy of Sciences, 110(16), 6430–6435.

    Article  CAS  Google Scholar 

  • Farmer, J. D., & Sidorowich, J. J. (1987). Predicting chaotic time series. Physical Review Letters, 59(8), 845.

    Article  PubMed  Google Scholar 

  • Fernando, W. G., Miller, J., Seaman, W., Seifert, K., & Paulitz, T. (2000). Daily and seasonal dynamics of airborne spores of Fusarium graminearum and other Fusarium species sampled over wheat plots. Canadian Journal of Botany, 78(4), 497–505.

    Article  Google Scholar 

  • Gadoury, D. M., Stensvand, A., & Seem, R. C. (1998). Influence of light, relative humidity, and maturity of populations on discharge of ascospores of Venturia inaequalis. Phytopathology, 88(9), 902–909.

    Article  CAS  PubMed  Google Scholar 

  • Gilbert, J., & Fernando, W. (2004). Epidemiology and biological control of Gibberella zeae/Fusarium graminearum. Canadian Journal of Plant Pathology, 26(4), 464–472.

    Article  Google Scholar 

  • Gilbert, J., & Tekauz, A. (2000). Review: Recent developments in research on fusarium head blight of wheat in Canada. Canadian Journal of Plant Pathology-Revue Canadienne De Phytopathologie, 22(1), 1–8.

  • Gilbert, J., Woods, S., & Kromer, U. (2008). Germination of ascospores of Gibberella zeae after exposure to various levels of relative humidity and temperature. Phytopathology, 98(5), 504–508.

    Article  CAS  PubMed  Google Scholar 

  • Granger, C. W. (1969). Investigating causal relations by econometric models and cross-spectral methods. Econometrica: Journal of the Econometric Society, 424–438.

  • Hart, M., Wentworth, J., & Bailey, J. (1994). The effects of trap height and weather variables on recorded pollen concentration at Leicester. Grana, 33(2), 100–103.

    Article  Google Scholar 

  • Holling, C. S. (2001). Understanding the complexity of economic, ecological, and social systems. Ecosystems, 4(5), 390–405.

    Article  Google Scholar 

  • Inch, S., Fernando, W., & Gilbert, J. (2005). Seasonal and daily variation in the airborne concentration of Gibberella zeae (Schw.) Petch spores in Manitoba. Canadian Journal of Plant Pathology, 27(3), 357–363.

    Article  Google Scholar 

  • Jennings, P., & Turner, J. (1996) Towards the prediction of Fusarium ear blight epidemics in the UK-the role of humidity in disease development. In Brighton Crop Protection Conference: Pests & Diseases-1996. Volume 1. Proceedings of an International Conference, Brighton, UK, 18–21 November, 1996 (pp. 233–238): British Crop Protection Council.

  • Maldonado-Ramirez, S. L., Schmale III, D. G., Shields, E. J., & Bergstrom, G. C. (2005). The relative abundance of viable spores of Gibberella zeae in the planetary boundary layer suggests the role of long-distance transport in regional epidemics of fusarium head blight. Agricultural and Forest Meteorology, 132(1–2), 20–27.

  • McMullen, M. P., & Stack, R. W. (1983). Head blight (scab) of small grains. North Dakota Cooperative Extension Service Circular(NPP-8), 1–2.

  • Meredith, D., Lawrence, J., & Firman, I. (1973). Ascospore release and dispersal in black leaf streak disease of bananas (Mycosphaerella fijiensis). Transactions of the British Mycological Society, 60(3), 547–554.

    Article  Google Scholar 

  • Oke, T. R. (1987). Boundary layer climates, 2nd edn. London: Methuen.

    Google Scholar 

  • Parnell, M., Burt, P. J. A., & Wilson, K. (1998). The influence of exposure to ultraviolet radiation in simulated sunlight on ascospores causing Black Sigatoka disease of banana and plantain. International Journal of Biometeorology, 42(1), 22–27.

    Article  Google Scholar 

  • Paulitz, T. (1996). Diurnal release of ascospores by Gibberella zeae in inoculated wheat plots. Plant Disease, 80(6), 674–678.

    Article  Google Scholar 

  • Paulitz, T. (1999). Fusarium head blight: a re-emerging disease. Phytoprotection, 80(2), 127–133.

    Article  Google Scholar 

  • Prussin II, A. J., Li, Q., Malla, R., Ross, S. D., & Schmale III, D. G. (2014a). Monitoring the long distance transport of Fusarium graminearum from field-scale sources of inoculum. Plant Disease, 98(4), 504–511.

  • Prussin II, A. J., Szanyi, N. A., Welling, P. I., Ross, S. D., & Schmale III, D. G. (2014b). Estimating the production and release of ascospores from a field-scale source of Fusarium graminearum inoculum. Plant Disease, 98(4), 497–503.

  • Prussin II, A. J., Marr, L. C., Schmale III, D. G., Stoll, R., & Ross, S. D. (2015). Experimental validation of a long-distance transport model for plant pathogens: Application to Fusarium graminearum. Agricultural and Forest Meteorology, 203(0), 118–130.

  • Reis, E. (1990). Effects of rain and relative humidity on the release of ascospores and on the infection of wheat heads by Gibberella zeae. Fitopatologia Brasileira, 15, 339–343.

    Google Scholar 

  • Rotem, J., & Aust, H. (1991). The effect of ultraviolet and solar radiation and temperature on survival of fungal propagules. Journal of Phytopathology, 133(1), 76–84.

    Article  Google Scholar 

  • Rutter, J., Burt, P. J., & Ramirez, F. (1998). Movement of Mycosphaerella fijiensis spores and sigatoka disease development on plantain close to an inoculum source. Aerobiologia, 14(2–3), 201–208.

  • Sauer, T., Yorke, J. A., & Casdagli, M. (1991). Embedology. Journal of Statistical Physics, 65(3–4), 579–616.

  • Schmale III, D. G., & Bergstrom, G. C. (2004). Spore deposition of the ear rot pathogen, Gibberella zeae, inside corn canopies. Canadian Journal of Plant Pathology-Revue Canadienne De Phytopathologie, 26(4), 591–595.

  • Schmale III, D. G., & Ross, S. D. (2015). Highways in the sky: Scales of atmospheric transport of plant pathogens. Annual Review of Phytopathology, 53(1), 591–611.

  • Schmale III, D. G., Arntsen, Q. A., & Bergstrom, G. C. (2005a). The forcible discharge distance of ascospores of Gibberelia zeae. Canadian Journal of Plant Pathology-Revue Canadienne De Phytopathologie, 27(3), 376–382.

    Article  Google Scholar 

  • Schmale III, D. G., Shah, D. A., & Bergstrom, G. C. (2005b). Spatial patterns of viable spore deposition of Gibberella zeae in wheat fields. Phytopathology, 95(5), 472–479. doi:10.1094/phyto-95-0472.

    Article  PubMed  Google Scholar 

  • Schmale III, D. G., Shields, E. J., & Bergstrom, G. C. (2006). Night-time spore deposition of the fusarium head blight pathogen, Gibberella zeae, in rotational wheat fields. Canadian Journal of Plant Pathology-Revue Canadienne De Phytopathologie, 28(1), 100–108.

    Article  Google Scholar 

  • Schmale III, D. G., Ross, S. D., Fetters, T. L., Tallapragada, P., Wood-Jones, A. K., & Dingus, B. (2012). Isolates of Fusarium graminearum collected 40–320 meters above ground level cause fusarium head blight in wheat and produce trichothecene mycotoxins. Aerobiologia, 28(1), 1–11.

  • Schollenberger, M., Jara, H. T., Suchy, S., Drochner, W., & Müller, H.-M. (2002). Fusarium toxins in wheat flour collected in an area in southwest Germany. International Journal of Food Microbiology, 72(1), 85–89.

    Article  CAS  PubMed  Google Scholar 

  • Spotts, R., & Cervantes, L. (1994). Factors affecting maturation and release of ascospores of Venturia pirina in Oregon. Phytopathology, 84(3), 260–263.

    Article  Google Scholar 

  • Stern, D. I., & Enflo, K. (2013). Causality between energy and output in the long-run. Energy Economics, 39(0), 135–146, doi:10.1016/j.eneco.2013.05.007.

  • Su, H., Van Bruggen, A., & Subbarao, K. (2000). Spore release of Bremia lactucae on lettuce is affected by timing of light initiation and decrease in relative humidity. Phytopathology, 90(1), 67–71.

  • Sugihara, G., May, R., Ye, H., Hsieh, C.-h., Deyle, E., Fogarty, M., et al. (2012). Detecting causality in complex ecosystems. Science, 338(6106), 496–500.

  • Sung, J.-M., & Cook, R. (1981). Effect of water potential on reproduction and spore germination by Fusarium roseum 'Graminearum,' 'Culmorum,' and 'Avenaceum'. Phytopathology, 71(5), 499–504.

  • Sutton, J. (1982). Epidemiology of wheat head blight and maize ear rot caused by Fusarium graminearum. Canadian Journal of Plant Pathology, 4(2), 195–209.

    Article  Google Scholar 

  • Takens, F. (1981). Detecting strange attractors in turbulence. Berlin Heidelberg: Springer.

    Book  Google Scholar 

  • Trail, F. (2007). Fungal cannons: explosive spore discharge in the Ascomycota. FEMS Microbiology Letters, 276(1), 12–18.

    Article  CAS  PubMed  Google Scholar 

  • Trail, F., Xu, H., Loranger, R., & Gadoury, D. (2002). Physiological and environmental aspects of ascospore discharge in Gibberella zeae (anamorph Fusarium graminearum). Mycologia, 94(2), 181–189.

    Article  PubMed  Google Scholar 

  • Trail, F., Gaffoor, I., & Vogel, S. (2005). Ejection mechanics and trajectory of the ascospores of Gibberella zeae (anamorph Fusarium graminearum). Fungal Genetics and Biology, 42(6), 528–533.

    Article  PubMed  Google Scholar 

  • Tschanz, A. T., Horst, R. K., & Nelson, P. E. (1975). Ecological aspects of ascospore discharge in Gibberella zeae. Phytopathology, 65, 597.

    Article  Google Scholar 

  • Windels, C. E. (2000). Economic and social impacts of fusarium head blight: changing farms and rural communities in the Northern Great Plains. Phytopathology, 90(1), 17–21.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This research was supported by the National Science Foundation (NSF) under Grant Numbers DGE-0966125 (IGERT: MultiScale Transport in Environmental and Physiological System (MultiSTEPS)) and CMMI-1150456 (Integrating Geometric, Probabilistic, and Topological Methods for Phase Space Transport in Dynamical Systems). A portion of this work was also supported by a grant through the Virginia Small Grains Board (449281, Improving the Management of FHB through an Increased Understanding of how the Pathogen Releases its Spores). The authors thank Dr. Aaron J. Prussin, II for his input on this project. The authors thank the Virginia Tech Laboratory for Interdisciplinary Statistical Analysis for assistance with statistical methods and interpretation.

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Correspondence to Linsey C. Marr.

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David, R.F., BozorgMagham, A.E., Schmale, D.G. et al. Identification of meteorological predictors of Fusarium graminearum ascospore release using correlation and causality analyses. Eur J Plant Pathol 145, 483–492 (2016). https://doi.org/10.1007/s10658-015-0832-3

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