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Title: An adaptive evolutionary shift in Fusarium head blight pathogen populations is driving the rapid spread of more toxigenic Fusarium graminerarum in North America

Author
item Ward, Todd
item CLEAR, RANDALL - CANADIAN GRAIN COMMISSION
item Rooney, Alejandro - Alex
item O Donnell, Kerry
item GABA, DON - CANADIAN GRAIN COMMISSION
item PATRICK, SUSAN - CANADIAN GRAIN COMMISSION
item STARKEY, DAVID - UNIV CNTRL AR, CONWAY AR
item GILBERT, JEANNIE - AG & AGRI-FOOD CANADA
item GEISER, DAVID - PENN STATE UNIV
item NOWICKI, TOM - CANADIAN GRAIN COMMISSION

Submitted to: Fungal Genetics and Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/10/2007
Publication Date: 2/15/2008
Citation: Ward, T.J., Clear, R.M., Rooney, A.P., O Donnell, K., Gaba, D., Patrick, S., Starkey, D.E., Gilbert, J., Geiser, D.M., Nowicki, T.W. 2008. An adaptive evolutionary shift in Fusarium head blight pathogen populations is driving the rapid spread of more toxigenic Fusarium graminerarum in North America. Fungal Genetics and Biology. 45(4):473-484.

Interpretive Summary: Fungal pathogens within the Fusarium graminearum species complex cause diseases of cereal crops worldwide, including Fusarium head blight (FHB) of wheat and barley. These diseases result in billion dollar losses to agriculture each year. In addition, these fungi contaminate grain with trichothecene mycotoxins that pose a serious threat to animal health and food safety. Recently, unexpected species and toxin variation has been identified among these pathogens. Through the development and use of a unique molecular test for rapid identification of FHB species and their toxins we determined that the previously dominant FHB pathogen population is rapidly being replaced by a highly toxigenic pathogen population in North America. In addition to producing more toxin, strains of this novel pathogen population have significant advantages in terms of growth and reproduction. As such, the rapid spread of this novel pathogen population represents a significant threat to food safety and the economics of cereal production in North America. In addition to calling attention to this situation, the unique molecular tools we developed provide a means to conduct pathogen monitoring needed to counter the threat posed by these highly toxigenic pathogens. This work will inform plant breeding and disease control efforts that will benefit cereal producers and consumers.

Technical Abstract: Toxigenic fungi responsible for Fusarium head blight (FHB) place significant constraints on the production of cereals worldwide and contaminate grain with trichothecene mycotoxins that pose a serious threat to food safety. A fraction of the global FHB species and trichothecene chemotype diversity is present in North America, where 15ADON-producing Fusarium graminearum is the dominant FHB pathogen. However, our active surveillance with a unique multilocus genotyping assay revealed for the first time that 3ADON-producing isolates of F. graminearum are prevalent in North America. In addition, we identified a dramatic longitudinal chemotype cline in Canada and documented a recent and unprecedented shift in FHB pathogen composition by demonstrating that the 3ADON chemotype frequency in western Canada increased more than 14-fold between 1998 and 2004. We also identified significant population structure associated with trichothecene chemotype differences (GST = 0.243 - 0.311, P < 0.001) and a potential bias in the direction of gene flow favoring the 3ADON genome (P < 0.05). On average, isolates from both 3ADON populations we identified produced significantly (P < 0.05) higher levels of trichothecene and had significantly (P < 0.005) higher fecundity and growth rates than the 15ADON population. Our results strongly indicate that selection is driving the replacement of the dominant FHB pathogen in North America by a recently introduced or emergent F. graminearum population. In addition, the demonstration that a vigorous and more toxigenic FHB pathogen population is rapidly replacing less toxigenic pathogens has significant implications for food safety and cereal production in North America.