Diversity of Fusarium head blight populations and trichothecene toxin types reveals regional differences in pathogen composition and temporal dynamics

Authors: Kelly, Amy; CLEAR, RANDALL - Collaborator; O Donnell, Kerry; McCormick, Susan; TURKINGTON, KELLY - Agriculture And Agri-Food Canada; TEKAUZ, ANDY - Agriculture And Agri-Food Canada; GILBERT, JEANNIE - Agriculture And Agri-Food Canada; Kistler, Harold; Busman, Mark; Ward, Todd

Submitted to: Fungal Genetics and Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/21/2015
Publication Date: 6/27/2015
Publication URL: http://handle.nal.usda.gov/10113/62272
Citation: Kelly, A.C., Clear, R.M., O'Donnell, K., McCormick, S., Turkington, T.K., Tekauz, A., Gilbert, J., Kistler, H.C., Busman, M., Ward, T.J. 2015. Diversity of Fusarium head blight populations and trichothecene toxin types reveals regional differences in pathogen composition and temporal dynamics. Fungal Genetics and Biology. 82:22-31.

Interpretive Summary: Fusarium graminearum is a fungus that causes Fusarium head blight (FHB) in wheat and barley, and contaminates grain with trichothecene mycotoxins such as deoxynivalenol (DON) that pose a significant threat to food safety and animal health. Recent studies of genetic variation demonstrated that a recently introduced population of FHB pathogens was spreading rapidly in western Canada and the Midwestern U.S. In addition, fungal strains with a novel trichothecene toxin type (NX-2) were recently discovered in Midwestern wheat. In the current research, we demonstrated that there are significant regional differences in the composition and toxin production capacity of FHB pathogen populations in North America. In addition, we identified F. graminearum strains that produce NX-2 toxin for the first time in Canada, representing a significant expansion of the known range of NX-2 producing strains in North America. We also demonstrated regional differences in the rate and nature of genetic exchange between the introduced and native pathogen populations. The results indicate that FHB pathogen diversity is shaped by local adaptation and these findings highlight the need to consider population-level variation in disease management and toxin control programs. The results also emphasize the need for a regional approach to FHB management. In that context, further studies aimed at elucidating the basis for regional differences in the adaptive landscape could contribute to the development of novel control strategies. Finally, the detection of strains producing the novel NX-2 trichothecene mycotoxin in Canada reinforces the need for continued monitoring of FHB pathogen communities in North America to further characterize trends in pathogen diversity and promote early detection of invasive populations or novel threats to food safety.

Technical Abstract: Analyses of genetic diversity, trichothecene genotype composition, and population structure were conducted using 4,086 Fusarium graminearum isolates collected from wheat in eight Canadian provinces over a three year period between 2005 and 2007. The results revealed substantial regional differences in Fusarium head blight pathogen composition and temporal population dynamics. The 3ADON trichothecene type consistently predominated in Maritime provinces (91%) over the sampled years, and increased significantly (P < 0.05) between 2005 and 2007 in western Canada, accounting for 66% of the isolates in Manitoba by the end of the sampling period. In contrast, 3ADON frequency was lower (22%, P < 0.001) in the eastern Canadian provinces of Ontario and Québec and did not change significantly between 2005 and 2007, resulting in two distinct longitudinal clines in 3ADON frequency across Canada. Overall, genetic structure was correlated with toxin type, as the endemic population (NA1) was dominated by 15ADON isolates (86%), whereas a second population (NA2) consisted largely of 3ADON isolates (88%). However, the percentage of isolates with trichothecene genotypes that were not predictive of their genetic population assignment (recombinant genotypes) increased from 10% in 2005 to 17% in 2007, indicating that trichothecene type became less predictive of population identity over time. In addition, there were substantial regional differences in the composition of recombinant genotypes. In western and maritime provinces, NA2 isolates with 15ADON genotypes were significantly more common than NA1 isolates with 3ADON genotypes (P < 0.001), and the reverse was true in the eastern provinces of Québec and Ontario. Temporal trends in recombinant genotype composition also varied regionally, as the percentage of 15ADON isolates with NA2 genetic backgrounds increased approximately three fold in western and Maritime provinces, while the opposite trends were observed in Québec and Ontario. The results indicate that F. graminearum population dynamics in Canada have been influenced by a complex adaptive landscape comprised of different regional selective pressures, and do not reflect a simple model of dispersal and integration following the introduction of a novel pathogen population. In addition, we identified F. graminearum strains that produce the recently discovered A-trichothecene mycotoxin (NX-2) for the first time in Canada, representing a significant expansion of the known range of NX-2 producing strains in North America.