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Isolates of Fusarium graminearum collected 40–320 meters above ground level cause Fusarium head blight in wheat and produce trichothecene mycotoxins

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Abstract

The aerobiology of fungi in the genus Fusarium is poorly understood. Many species of Fusarium are important pathogens of plants and animals and some produce dangerous secondary metabolites known as mycotoxins. In 2006 and 2007, autonomous unmanned aerial vehicles (UAVs) were used to collect Fusarium 40–320 m above the ground at the Kentland Farm in Blacksburg, Virginia. Eleven single-spored isolates of Fusarium graminearum (sexual stage Gibberella zeae) collected with autonomous UAVs during fall, winter, spring, and summer months caused Fusarium head blight on a susceptible cultivar of spring wheat. Trichothecene genotypes were determined for all 11 of the isolates; nine isolates were DON/15ADON, one isolate was DON/3ADON, and one isolate was NIV. All of the isolates produced trichothecene mycotoxins in planta consistent with their trichothecene genotypes. To our knowledge, this is the first report of a NIV isolate of F. graminearum in Virginia, and DON/3ADON genotypes are rare in populations of the fungus recovered from infected wheat plants in the eastern United States. Our data are considered in the context of a new aerobiological framework based on atmospheric transport barriers, which are Lagrangian coherent structures present in the mesoscale atmospheric flow. This framework aims to improve our understanding of population shifts of F. graminearum and develop new paradigms that may link field and atmospheric populations of toxigenic Fusarium spp. in the future.

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References

  • Aylor, D. E. (2003). Spread of plant disease on a continental scale: Role of aerial dispersal of pathogens. Ecology, 84, 1989–1997.

    Article  Google Scholar 

  • Bowman, K. P., Pan, L. L., Campos, T., & Gao, R. (2007). Observations of fine-scale transport structure in the upper troposphere from the High-performance Instrumented Airborne Platform for Environmental research. Journal of Geophysical Research, 112, D18111.

    Article  Google Scholar 

  • Bush, B. J., Carson, M. L., Cubeta, M. A., Hagler, W. M., & Payne, G. A. (2004). Infection and fumonisin production by Fusarium verticillioides in developing maize kernels. Phytopathology, 94, 88–93.

    Article  CAS  Google Scholar 

  • Chaimovitsh, D., Dudai, N., Putievsky, E., & Ashri, A. (2006). Inheritance of resistance to Fusarium wilt in sweet basil. Plant Disease, 90, 58–60.

    Article  Google Scholar 

  • d’Ovidio, F., Fernandez, V., Hernandez-Garca, E., & Lopez, C. (2004). Mixing structures in the Mediterranean Sea from finite-size Lyapunov exponents. Geophysical Research Letters, 31, L17203.

    Article  Google Scholar 

  • Dellnitz, M., Junge, O., Koon, W. S., Lekien, F., Lo, M. W., Marsden, J. E., et al. (2005). Transport in dynamical astronomy and multibody problems. International Journal of Bifurcation and Chaos, 15, 699–727.

    Article  Google Scholar 

  • Dill-Macky, R., & Jones, R. K. (2000). The effect of previous crop residues and tillage on Fusarium head blight of wheat. Plant Disease, 84, 71–76.

    Article  Google Scholar 

  • Dingus, B. R., Schmale, D. G., & Reinholtz, C. (2007). Development of an autonomous unmanned aerial vehicle for aerobiological sampling. Phytopathology, 97, S184.

    Article  Google Scholar 

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

    Google Scholar 

  • Francl, L., Shaner, G., Bergstrom, G., Gilbert, J., Pedersen, W., Dill-Macky, R., et al. (1999). Daily inoculum levels of Gibberella zeae on wheat spikes. Plant Disease, 83, 662–666.

    Article  Google Scholar 

  • Froyland, G., & Padberg, K. (2009). Almost-invariant sets and invariant manifolds—Connecting probabilistic and geometric descriptions of coherent structures in flows. Physica D, 238, 1507–1523.

    Article  CAS  Google Scholar 

  • Froyland, G., Padberg, K., England, M. H., & Treguier, A. M. (2007). Detection of coherent oceanic structures via transfer operators. Physical Review Letters, 98, 224503.

    Article  Google Scholar 

  • Gale, L. R., Ward, T. J., Balmas, V., & Kistler, H. C. (2007). Population subdivision of Fusarium graminearum sensu stricto in the upper midwestern United States. Phytopathology, 97, 1434–1439.

    Article  CAS  Google Scholar 

  • Geiser, D. M., Delmar Jimenez-Gasco, M., Kang, S., Makalowska, I., Veeraraghavan, N., Ward, T. J., et al. (2004). Fusarium-ID v.1.0: A DNA sequence database for identifying Fusarium. European Journal of Plant Pathology, 110, 473–479.

    Article  CAS  Google Scholar 

  • Goswami, R. S., & Kistler, H. C. (2005). Pathogenicity and in planta mycotoxin accumulation among members of the Fusarium graminearum species complex on wheat and rice. Phytopathology, 95, 1397–1404.

    Article  CAS  Google Scholar 

  • Guo, X. W., Fernando, W. G. D., & Seow-Brock, H. Y. (2008). Population structure, chemotype diversity, and potential chemotype shifting of Fusarium graminearum in wheat fields of Manitoba. Plant Disease, 92, 756–762.

    Article  CAS  Google Scholar 

  • Haller, G., & Yuan, G. (2000). Lagrangian coherent structures and mixing in two-dimensional turbulence. Physica D, 147, 352–370.

    Article  Google Scholar 

  • Ichinoe, M., Kurata, H., Sugiura, Y., & Ueno, Y. (1983). Chemotaxonomy of Gibberella zeae with special reference to production of trichothecenes and zearalenone. Applied and Environmental Microbiology, 46, 1364–1369.

    CAS  Google Scholar 

  • Inanc, T., Shadden, S. C., & Marsden, J. E. (2005). Optimal trajectory generation in ocean flows. In Proceedings of 2005 American Control Conference, 674–679.

  • Isard, S. A., & Gage, S. H. (2001). Flow of life in the atmosphere. East Lansing: Michigan State University Press.

    Google Scholar 

  • Katan, T., Shlevin, E., & Katan, J. (1997). Sporulation of Fusarium oxysporum f. sp. lycopersici on stem surfaces of tomato plants and aerial dissemination of inoculum. Phytopathology, 87, 712–719.

    Article  CAS  Google Scholar 

  • Lekien, F., Coulliette, C., Mariano, A. J., Ryan, E. H., Shay, L. K., Haller, G., et al. (2005). Pollution release tied to invariant manifolds: A case study for the coast of Florida. Physica D, 210, 1–20.

    Article  Google Scholar 

  • Lekien, F., & Ross, S. D. (2010). The computation of finite-time Lyapunov exponents on unstructured meshes and for non-Euclidean manifolds. Chaos, 20, 017505.

    Article  Google Scholar 

  • Leslie, J. F., & Summerell, B. A. (2006). The fusarium laboratory manual (p. 388). Ames, Iowa: Blackwell Publishing.

    Book  Google Scholar 

  • Maldonado-Ramirez, S. L., Schmale, 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. Journal of Agricultural and Forest Meteorology, 132, 20–27.

    Article  Google Scholar 

  • McMullen, M. P., Jones, R., & Gallenberg, D. (1997). Scab of wheat and barley: A re-emerging disease of devastating impact. Plant Disease, 81, 1340–1348.

    Article  Google Scholar 

  • Ohe, C., Gauthier, V., Tamburic-Ilincic, L., Brule-Babel, A., Fernando, W. G. D., Clear, R., et al. (2010). A comparison of aggressiveness and deoxynivalenol production between Canadian Fusarium graminearum isolates with 3-acetyl and 15-acetyldeoxynivalenol chemotypes in field-grown spring wheat. European Journal of Plant Pathology, 127, 407–417.

    Article  CAS  Google Scholar 

  • Reaver, D., & Schmale, D. G. (2007). High-throughput homogenization of grain samples for deoxynivalenol testing. Page 10 in Proc. 2007 National Fusarium Head Blight Forum, Kansas City, MO, December 2–4.

  • Schmale, D. G., Arntsen, Q. A., & Bergstrom, G. C. (2005). The forcible discharge distance of ascospores of Gibberella zeae. Canadian Journal of Plant Pathology, 27, 376–382.

    Article  Google Scholar 

  • Schmale, D.G., & Bergstrom, G.C. (2003). Fusarium head blight. The Plant Health Instructor. doi:10.1094/PHI-I-2003-0612-01.

  • Schmale, D. G., Dingus, B. R., & Reinholtz, C. F. (2008). Development and application of an autonomous unmanned aerial vehicle for precise aerobiological sampling above agricultural fields. Journal of Field Robotics, 25, 133–147.

    Article  Google Scholar 

  • Schmale, D. G., Fetters, T., Ross, S., Tallapragada, P., & Dingus, B. (2010). Isolates of Fusarium graminearum collected 40 to 300 meters above ground level cause Fusarium head blight and produce trichothecene mycotoxins. Phytopathology, 100, S208.

    Article  Google Scholar 

  • Schmale, D. G., & Gordon, T. R. (2003). Variation in susceptibility to pitch canker disease, caused by Fusarium circinatum, in native stands of Pinus muricata. Plant Pathology, 52, 720–725.

    Article  Google Scholar 

  • Schmale, D. G., Leslie, J. F., Saleh, A. A., Shields, E. J., & Bergstrom, G. C. (2006). Genetic structure of atmospheric populations of Gibberella zeae. Phytopathology, 96, 1021–1026.

    Article  CAS  Google Scholar 

  • Schmale, D.G., Wood-Jones, A.K., Cowger, C., Bergstrom, G.C., & Arellano, C. (2011). Trichothecene genotypes of Gibberella zeae from winter wheat fields in the eastern United States. Plant Pathology. doi:10.1111/j.1365-3059.2011.02443.x.

  • Senatore, C. & Ross, S. D. (2008). Fuel-efficient navigation in complex flows. In Proceedings of 2008 American Control Conference, 1244–1248.

  • Senatore, C. & Ross, S. D. (2011). Detection and characterization of transport barriers in complex flows via ridge extraction of the finite time Lyapunov exponent field. International Journal for Numerical Methods in Engineering. doi:10.1002/nme.3101.

  • Shadden, S. C., Lekien, F., & Marsden, J. E. (2005). Definition and properties of Lagrangian coherent structures: Mixing and transport in two-dimensional aperiodic flows. Physica D, 212, 271–304.

    Article  Google Scholar 

  • Shadden, S. C., & Taylor, C. A. (2008). Characterization of coherent structures in the cardiovascular system. Annals of Biomedical Engineering, 36, 1152–1162.

    Article  Google Scholar 

  • Stremler, M. A., Ross, S. D., Grover, P., & Kumar, P. (2011). Topological chaos and periodic braiding of almost-cyclic sets. Physical Review Letters, 106, 114101.

    Article  Google Scholar 

  • Tallapragada, P. (2010). Identifying dynamical boundaries and phase space transport using Lagrangian coherent structures. Ph.D. dissertation. Virginia Polytechnic Institute and State University, Blacksburg.

  • Techy, L., Schmale, D. G., & Woolsey, C. A. (2010). Coordinated aerobiological sampling of a plant pathogen in the lower atmosphere using two autonomous unmanned aerial vehicles. Journal of Field Robotics, 27, 335–343.

    Google Scholar 

  • Tew Kai, E., Rossi, V., Sudre, J., Weimerskirch, H., Lopez, C., Hernandez-Garcia, E., et al. (2009). Top marine predators track Lagrangian coherent structures. Proceedings of the National Academy of Sciences, 106, 8245–8825.

    Article  Google Scholar 

  • Wang, B., & Jeffers, S. N. (2000). Fusarium root and crown rot: A disease of container-grown hostas. Plant Disease, 84, 980–988.

    Article  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 gene cluster of phytopathogenic Fusarium. Proceedings of the National Academy of Sciences, 99, 9278–9283.

    Article  CAS  Google Scholar 

  • Ward, T. J., Clear, R. M., Rooney, A. P., O’Donnell, K., Gaba, D., Patrick, S., et al. (2008). An adaptive evolutionary shift in Fusarium head blight pathogen populations is driving the rapid spread of more toxigenic Fusarium graminearum in North America. Fungal Genetics and Biology, 45, 473–484.

    Article  Google Scholar 

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Acknowledgments

We thank N. McMaster for her excellent technical assistance with the GC/MS. This material is based upon work supported by the National Science Foundation under Grant No. 0919088. Any opinions, findings, and conclusions or recommendations expressed in this material are those of the author(s) and do not necessarily reflect the views of the National Science Foundation.

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Correspondence to D. G. Schmale III.

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Schmale, D.G., Ross, S.D., Fetters, T.L. et al. Isolates of Fusarium graminearum collected 40–320 meters above ground level cause Fusarium head blight in wheat and produce trichothecene mycotoxins. Aerobiologia 28, 1–11 (2012). https://doi.org/10.1007/s10453-011-9206-2

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  • DOI: https://doi.org/10.1007/s10453-011-9206-2

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