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2007 Plant Management Network.
Accepted for publication 14 February 2007. Published 26 July 2007.


The Aerobiology and Population Genetic Structure of Gibberella zeae


David G. Schmale III, Department of Plant Pathology, Physiology, and Weed Science, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061 (formerly, Department of Plant Pathology, Cornell University, Ithaca, NY 14853); and Gary C. Bergstrom, Department of Plant Pathology, Cornell University, Ithaca, NY 14853


Corresponding author: David G. Schmale III. dschmale@vt.edu


Schmale, D. G. III, and Bergstrom, G. C. 2007. The aerobiology and population genetic structure of Gibberella zeae. Online. Plant Health Progress doi:10.1094/PHP-2007-0726-04-RV.


Abstract

Gibberella zeae causes Fusarium head blight (FHB) of wheat and barley and Gibberella ear rot (GER) of corn. Ascospores of G. zeae rely on atmospheric motion systems for transport to susceptible host plants. A long term objective of our research is to determine where inoculum for FHB and GER comes from and how far it travels. We measured the distance that ascospores of G. zeae were forcibly discharged in still air, and determined that long-range transport is favored by day-time ascospore release. We used remote-piloted aircraft to collect viable spores of G. zeae in the lower atmosphere. Viable spores of G. zeae were abundant in the lower atmosphere during all times of the day and night under a broad range of environmental conditions. Viable spores of G. zeae were deposited over wheat and corn fields mainly at random and predominantly at night. We used amplified fragment length polymorphisms (AFLPs) to characterize the genetic structure of atmospheric populations of G. zeae over multiple years. Genotypic diversity was high in the atmospheric populations of G. zeae, and nearly all of the isolates in each of the populations represented unique AFLP haplotypes. Diverse atmospheric populations of G. zeae are indicative of well-mixed sources of aerial inoculum, potentially originating from local and more distant sources. Introduced strains of G. zeae with altered virulence or mycotoxin profiles, moving over long distances, have the potential to spread rapidly into previously unexposed wheat and corn production regions.


The Aerobiology of Gibberella zeae

Many plant pathogens utilize the atmosphere to flow from one habitat to another. The movement of these pathogens in the atmosphere is characterized by processes of liberation (takeoff and ascent), horizontal transport (drift), and deposition (descent and landing) (3) (Fig. 1). Knowledge of the liberation, horizontal transport, and deposition of spores of Gibberella zeae, causal agent of Fusarium head blight (FHB) of wheat and barley and Gibberella ear rot (GER) of corn, is limited.


 

Fig. 1. Aerobiological processes demonstrating the movement of airborne plant pathogens in the atmosphere. Pathogens that rely on atmospheric motion systems for transport must proceed through these stages in order from left to right. Figure adapted from Isard and Gage, 2001 (3).

 

Liberation of Ascospores

Liberation is influenced by various ecological and environmental factors that dictate the timing and mechanism of spore release. G. zeae overwinters in residues of corn and small grains (16), and in the following spring and summer, perithecia emerge from these residues and forcibly discharge ascospores into the air (8). We measured the distance that ascospores of G. zeae were forcibly discharged, and related this distance to the conditions necessary for transport into the atmosphere (10). Ascospores were discharged distances less than 10 mm away from culture surfaces inside small glass chambers. Ascospores of G. zeae released during daylight hours have the potential to be transported over long distances in the atmosphere (10).


Horizontal Transport

Fig. 2. A remote-piloted aircraft for sampling viable spores of Gibberella zeae in the planetary boundary layer of the atmosphere.

 

Horizontal transport is associated with the passive, directed movement away from the ground surface in turbulent air currents. The bulk of the literature suggests that most spores of G. zeae are dispersed only a short distance from a source (1,2,7,17). We demonstrated that viable spores of G. zeae may be transported long distances in the atmosphere (4). We used remote-piloted aircraft (Fig. 2) to measure the relative abundance of viable spores of G. zeae in the planetary boundary layer, 60 m above the surface of the earth (4). We collected a total of nearly 13,000 viable spores of G. zeae over 158 sampling flights in four consecutive years (1999-2002). Viable spores of G. zeae were abundant in the planetary boundary layer during every hour of the day and night. More viable spores were collected during cloudy conditions, than during clear or rainy conditions. Spores may survive longer in the atmosphere on cloudy days than on clear, sunny days (6). Since viable spores of G. zeae were abundant in the planetary boundary layer under a broad range of meteorological conditions that are conducive for the infection of local wheat and corn, the role of long-distance transport of inoculum of G. zeae in regional epidemics of FHB and GER should be considered.


Deposition of Viable Spores

Deposition involves descent and landing at a new destination. Little is known about the spatial and temporal dynamics of viable spore deposition of G. zeae within and above crop canopies. Viable, airborne spores of G. zeae were collected in rotational (lacking any apparent within-field inoculum sources of G. zeae) wheat and corn fields in New York in May through August over three years (2002-2004) (9,11,12,13). Petri plates containing a Fusarium selective medium were placed in wheat and corn canopies and exposed to the atmosphere during day or night sample periods (Fig. 3). These studies demonstrated that viable spore deposition in wheat and corn canopies occurred predominantly at night (9,13) and almost entirely at random (11,12).


 

Fig. 3. Petri plates containing a Fusarium selective medium were used to trap viable spores of Gibberella zeae in wheat and corn canopies during day and night sample periods.

 

Genetic Structure of Atmospheric Populations

An increased understanding of the genetic structure of plant pathogen populations is a prerequisite to developing informed approaches to managing plant diseases (5). Little is known about the genetic structure of atmospheric populations of G. zeae. We used a series of amplified fragment length polymorphism (AFLP) markers (18) to analyze the genetic structure of New York atmospheric populations of G. zeae over multiple years (14,15). Results from these studies demonstrated that genotypic diversity was high in each of the atmospheric populations of G. zeae, and nearly all of the isolates in each of the populations represented unique AFLP haplotypes. Sub-populations within the larger New York atmospheric populations maintained high levels of genotypic diversity over different temporal scales (isolates collected over consecutive calendar dates, during day and night sample periods, during two-hour sampling intervals throughout the night, and collected at different field locations in a similar year) (15). The maintenance of high genetic diversity over time may be the result of the continued mixing of atmospheric inoculum sources of G. zeae, potentially from multiple origins over great geographic distances (14).


Significance

Spores of G. zeae released during the day have the greatest chance of becoming airborne in turbulent air currents and transported great distances away from their source (10). Viable spores of G. zeae may be transported over long distances in the planetary boundary layer of the atmosphere (4). Spore deposition of G. zeae in rotational wheat and corn fields occurred predominantly at night (9,13) and mostly at random (11,12), indicative of well-mixed atmospheric populations. Our finding that spore release and spore deposition may be uncoupled in time, suggests that inoculum deposited in wheat and corn fields may have originated from distant sources. The high genetic diversity of atmospheric populations of G. zeae also suggests that inoculum in wheat and corn fields may have originated from multiple locations, and mixed over great geographic distances. The long-distance transport of G. zeae would suggest that the management of inoculum sources on a local scale, unless performed over extensive production areas, would be insufficient for the management of FHB and GER. Our findings suggest that introduced strains of G. zeae with altered virulence or mycotoxin profiles have the potential to spread rapidly into previously unexposed wheat and corn production regions.


Acknowledgments

This research was supported in part by grants to G. C. Bergstrom from the US Wheat and Barley Scab Initiative (USWBSI) of the US Department of Agriculture (USDA) and from Cornell University Hatch Project NYC153433. Any opinions, findings, conclusions, or recommendations expressed in this publication are those of the authors and do not necessarily reflect the view of the USDA. We thank Elson J. Shields, John F. Leslie, and Denis A. Shah for their outstanding contributions to this work.


Literature Cited

1. De Luna, L., Bujold, I., Carisse, O., and Paulitz, T. C. 2002. Ascospore gradients of Gibberella zeae from overwintered inoculum in wheat fields. Can. J. Plant Pathol. 24:457-464.

2. Fernando, W. G. D., Paulitz, T. C., Seaman, W. L., Dutilleul, P., and Miller, J. D. 1997. Head blight gradients caused by Gibberella zeae from area sources of inoculum in wheat field plots. Phytopathology 87:414-421.

3. Isard, S. A., and Gage, S. H. 2001. Flow of Life in the Atmosphere. Michigan State Univ. Press, East Lansing, MI.

4. Maldonado-Ramirez, S. L., Schmale, D. G., Shields, E. J., and 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. Agric. For. Meteorol. 132:20-27.

5. Milgroom, M. G., and Fry, W. E. 1997. Contributions of population genetics to plant disease epidemiology and management. Adv. Botan. Res. 24:1-30.

6. Mizubuti, E. S. G., Aylor, D. E., and Fry, W. 2001. Survival of Phytophthora infestans sporangia exposed to solar radiation. Phytopathology 90:78-84.

7. Paulitz, T. C. 1996. Diurnal release of ascospores by Gibberella zeae in inoculated wheat plots. Plant Dis. 80:674-678.

8. Schmale, D. G., and Bergstrom, G. C. 2003. Fusarium head blight. Online. The Plant Health Instructor. DOI:10.1094/PHI-I-2003-0612-01.

9. Schmale, D. G., and Bergstrom, G. C. 2004. Spore deposition of the ear rot pathogen, Gibberella zeae, inside corn canopies. Can. J. Plant Pathol. 26:591-595.

10. Schmale, D. G., Arntsen, Q. A., and Bergstrom, G. C. 2005. The forcible discharge distance of ascospores of Gibberella zeae. Can. J. Plant Pathol. 27:376-382.

11. Schmale, D. G., Shah, D. A., and Bergstrom, G. C. 2005. Spatial patterns of viable spore deposition of Gibberella zeae in wheat fields. Phytopathology 95:472-479.

12. Schmale, D. G., Shah, D. A., and Bergstrom, G. C. 2005. Spatial patterns of viable spore deposition of the corn ear rot pathogen, Gibberella zeae, in first-year corn fields. Can. J. Plant Pathol. 27: 225-233.

13. Schmale, D. G., Shields, E. J., and Bergstrom, G. C. 2006. Night-time spore deposition of the Fusarium head blight pathogen, Gibberella zeae, in rotational wheat fields. Can. J. Plant Pathol. 28:100-108.

14. Schmale, D. G., Leslie, J. F., Bowden, R. L., Zeller, K. A., Saleh, A. A., Shields, E. J., and Bergstrom, G. C. 2006. Genetic structure of atmospheric populations of Gibberella zeae. Phytopathology. 96:1021-1026.

15. Schmale, D. G., Leslie, J. F., Saleh, A. A., Shields, E. J., and Bergstrom, G. C. 2005. Temporal scales of genetic diversity within New York atmospheric populations of Gibberella zeae. Page 149 in: Proc. 2005 Natl. Fusarium Head Blight Forum, Michigan State Univ., East Lansing, MI.

16. Shaner, G. E. 2003. Epidemiology of Fusarium head blight of small grain cereals in North America. Pages 84-119 in: Fusarium Head Blight of Wheat and Barley. K. J. Leonard and W. Bushnell, eds. American Phytopathological Society, St. Paul, MN.

17. Stack, R. W. 1997. Gradients of Fusarium head blight in wheat along transects away from a concentrated source of Gibberella zeae ascospore inoculum. Page 60 in: Current Research on Fusarium Head Blight of Small Grains. R. Stack, ed. North Dakota State University, Fargo, ND.

18. Vos, P., Hogers, R., Bleeker, M., Reijans, M., van de Lee, T., Hornes, M., Frijters, A., Pot, J., Peleman, J., Kuiper, M., and Zabeau, M. 1995. AFLP: A new technique for DNA fingerprinting. Nucleic Acids Res. 23:4407-4414.