Abstract
Understanding the influence of meteorological conditions on the release of pathogen spores is necessary for crop management decisions and development of spore transport models. This study investigated the release of ascospores of Fusarium graminearum in a controlled chamber at two temperatures (15 °C and 25 °C) and at three relative humidities (60 %, 75 %, and 95 %). Filter paper pieces containing perithecia from a single isolate of F. graminearum were placed inside custom 3D-printed spore discharge devices, and the number of ascospores released and distance the ascospores were discharged were measured. The number of ascospores released was higher at 15 °C, and increased with increasing levels of relative humidity. Ascospores were discharged 0.5 mm to over 12 mm from perithecia and traveled farther from the perithecia at 25 °C and at the highest levels of relative humidity. Even small differences in discharge distances may be important for the escape of ascospores from the laminar boundary layer and into the turbulent layer. Spore transport models need to consider the impact of environmental conditions on spore release and transport.
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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(7), 835.
Aylor, D. E. (1986). A framework for examining inter-regional aerial transport of fungal spores. Agricultural and Forest Meteorology, 38(4), 263–288.
Aylor, D. E. (1990). The role of intermittent wind in the dispersal of fungal pathogens. Annual Review of Phytopathology, 28(1), 73–92.
Aylor, D. E. (1998). The aerobiology of apple scab. Plant Disease, 82(8), 838–849.
Aylor, D. E. (1999). Biophysical scaling and the passive dispersal of fungus spores: relationship to integrated pest management strategies. Agricultural and Forest Meteorology, 97(4), 275–292.
Aylor, D. E., & Anagnostakis, S. L. (1991). Active discharge distance of ascospores of. Venturia inaequalis. Phytopathology, 81(5), 548–551.
Aylor, D. E., Fry, W. E., Mayton, H., & Andrade-Piedra, J. L. (2001). Quantifying the rate of release and escape of Phytophthora infestans sporangia from a potato canopy. Phytopathology, 91(12), 1189–1196.
Beyer, M., & Verreet, J.-A. (2005). Germination of Gibberella zeae ascospores as affected by age of spores after discharge and environmental factors. European Journal of Plant Pathology, 111(4), 381–389.
Beyer, M., Verreet, J.-A., & Ragab, W. S. (2005). Effect of relative humidity on germination of ascospores and macroconidia of Gibberella zeae and deoxynivalenol production. International Journal of Food Microbiology, 98(3), 233–240.
Brennan, J., Egan, D., Cooke, B., & Doohan, F. (2005). Effect of temperature on head blight of wheat caused by Fusarium culmorum and F. graminearum. Plant Pathology, 54(2), 156–160.
Brown, J. K., & Hovmøller, M. S. (2002). Aerial dispersal of pathogens on the global and continental scales and its impact on plant disease. Science, 297(5581), 537–541.
David, R. F., Bozorgmagham, A. E., Schmale III, D. G., Ross, S. D., & Marr, L. C. (2016). Identification of meteorological predictors of Fusarium graminearum ascospore release using correlation and causality analyses. European Journal of Plant Pathology. doi:10.1007/s10658-015-0832-3.
Del Ponte, E. M., Fernandes, J. M. C., & Pierobom, C. R. (2005). Factors affecting density of airborne Gibberella zeae inoculum. Fitopatologia Brasileira, 30(1), 55–60.
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. doi:10.1111/j.1439-0434.2009.01559.x.
Elbert, W., Taylor, P., Andreae, M., & Pöschl, U. (2007). Contribution of fungi to primary biogenic aerosols in the atmosphere: wet and dry discharged spores, carbohydrates, and inorganic ions. Atmospheric Chemistry and Physics, 7(17), 4569–4588.
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.
Fry, W., Goodwin, S., Dyer, A., Matuszak, M., Drenth, A., & Tooley, P. (1993). Historical and recent migrations of Phytophthora infestans: chronology, pathways, and implications. Plant Disease, 77, 653–661.
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.
Goswami, R. S., & Kistler, H. C. (2004). Heading for disaster: Fusarium graminearum on cereal crops. Molecular Plant Pathology, 5(6), 515–525.
Griffin, D. W., Garrison, V. H., Herman, J. R., & Shinn, E. A. (2001). African desert dust in the Caribbean atmosphere: microbiology and public health. Aerobiologia, 17(3), 203–213.
Hinds, W. C. (1999). Aerosol technology: properties, behavior, and measurement of airborne particles. New York: Wiley Interscience.
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.
Isard, S. A., Gage, S. H., Comtois, P., & Russo, J. M. (2005). Principles of the atmospheric pathway for invasive species applied to soybean rust. Bioscience, 55(10), 851–861. doi:10.1641/0006-3568(2005)055[0851:potapf]2.0.co;2.
Kellogg, C. A., & Griffin, D. W. (2006). Aerobiology and the global transport of desert dust. Trends in Ecology & Evolution, 21(11), 638–644. doi:10.1016/j.tree.2006.07.004.
Klittich, C., & Leslie, J. (1988). Nitrate reduction mutants of. Fusarium moniliforme (Gibberella fujikuroi). Genetics, 118(3), 417–423.
Manstretta, V., & Rossi, V. (2015). Effects of weather variables on ascospore discharge from Fusarium graminearum perithecia. PloS one, 10(9), e0138860.
McMullen, M. P., & Stack, R. W. (1983). Head blight (scab) of small grains. North Dakota Cooperative Extension Service Circular, NPP-8, 1–2.
McMullen, M., Jones, R., & Gallenberg, D. (1997). Scab of wheat and barley: a re-emerging disease of devastating impact. Plant Disease, 81(12), 1340–1348. doi:10.1094/pdis.1997.81.12.1340.
Morvay, Z., & Gvozdenac, D. (2008). Applied Industrial Energy And Environmental Management (Vol. 2). Chichester, UK: John Wiley & Sons.
Nganje, W. E., Bangsund, D. A., Leistritz, F. L., Wilson, W. W., & Tiapo, N. M. (2002). Estimating the economic impact of a crop disease: the case of fusarium head blight in US wheat and barley. 2002 National Fusarium Head Blight Forum Proceedings, 275-281.
Oke, T. R. (1987). Boundary layer climates (2nd ed.). London: Methuen.
Okubara, P., Blechl, A., McCormick, S., Alexander, N., Dill-Macky, R., & Hohn, T. (2002). Engineering deoxynivalenol metabolism in wheat through the expression of a fungal trichothecene acetyltransferase gene. Theoretical and Applied Genetics, 106(1), 74–83.
Paul, P., Lipps, P., De Wolf, E., Shaner, G., Buechley, G., Adhikari, T., et al. (2007). A distributed lag analysis of the relationship between Gibberella zeae inoculum density on wheat spikes and weather variables. Phytopathology, 97(12), 1608–1624.
Paulitz, T. (1996). Diurnal release of ascospores by Gibberella zeae in inoculated wheat plots. Plant Disease, 80(6), 674–678.
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. doi:10.1016/j.agrformet.2014.12.009.
Purdy, L., Krupa, S., & Dean, J. (1985). Introduction of sugarcane rust into the Americas and its spread to Florida. Plant Disease, 69(8), 689–693.
Schmale III, D. G., & Bergstrom, G. C. (2005). The aerobiology and population genetic structure of. Gibberella zeae. Phytopathology, 95(6), S127–S127.
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. doi:10.1146/annurev-phyto-080614-115942.
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.
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.
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.
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. doi:10.1007/s10453-011-9206-2.
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.
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.
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.
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.
Tschanz, A. T., Horst, R. K., & Nelson, P. E. (1975). Ecological aspects of ascospore discharge in Gibberella zeae. Phytopathology, 65, 597.
Tschanz, A. T., Horst, R., & Nelson, P. E. (1976). The effect of environment on sexual reproduction of Gibberella zeae. Mycologia, 68, 327–340.
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.
Acknowledgments
This material is based upon work supported by the National Science Foundation (NSF) under Grant Numbers DGE-0966125 (IGERT: MultiScale Transport in Environmental and Physiological System (MultiSTEPS)) and 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, insight, and guidance on this project. The authors thank Craig Powers for his assistance in designing and printing the 3D-printed spore discharge devices. The authors also thank the Laboratory for Interdisciplinary Statistical Analysis (LISA) at Virginia Tech for their help with statistical analyses.
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David, R.F., Marr, L.C. & Schmale, D.G. Ascospore release and discharge distances of Fusarium graminearum under controlled temperature and relative humidity. Eur J Plant Pathol 146, 59–69 (2016). https://doi.org/10.1007/s10658-016-0891-0
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DOI: https://doi.org/10.1007/s10658-016-0891-0