Species diversity and mycotoxin production by members of the Fusarium tricinctum species complex associated with Fusarium head blight of wheat and barley in Italy

Authors: SENATORE, M - University Of Bologna, Italy; Ward, Todd; CAPPELLETTI, E - University Of Bologna, Italy; BECCARI, G - University Of Perugia; McCormick, Susan; Busman, Mark; LARABA, I - Orise Fellow; O Donnell, Kerry; PRODI, A - University Of Bologna, Italy

Submitted to: International Journal of Food Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/5/2021
Publication Date: 6/15/2021
Citation: Senatore, M.T., Ward, T.J., Cappelletti, E., Beccari, G., McCormick, S.P., Busman, M., Laraba, I., O'Donnell, K., Prodi, A. 2021. Species diversity and mycotoxin production by members of the Fusarium tricinctum species complex associated with Fusarium head blight of wheat and barley in Italy. International Journal of Food Microbiology. https://doi.org/10.1016/j.ijfoodmicro.2021.109298.
DOI: https://doi.org/10.1016/j.ijfoodmicro.2021.109298

Interpretive Summary: Fusarium head blight (FHB) is a disease of cereals crops worldwide and a major food safety concern because FHB pathogens can contaminate grain with fungal toxins (mycotoxins). FHB is caused by a diverse set of fungi that make different sets of mycotoxins. However, the available information on species diversity, mycotoxin potential and the geographic distribution of FHB pathogens is fragmentary and frequently inaccurate. In an international collaborative study, we determined the species diversity and toxin potential among isolates from the Fusarium tricinctum species complex (FTSC), an increasingly important contributor to FHB. Genetic analyses revealed that F. avenaceum and a novel species previously unknown to science were the most common contributors to FHB among FTSC isolates from durum wheat and barley in Italy. Three additional novel species of FHB pathogens were also detected and characterized for the first time in this study. In addition, we demonstrated that the ability to produce bioactive secondary metabolites such as chlamydosporol, acuminatopyrone, longiborneol, fungerin, and butanolide is widespread among the novel species and the FTSC as a whole. These results provide information on FHB pathogen and mycotoxin prevalence needed to develop regionally targeted disease and mycotoxin control programs that improve crop production and food safety.

Technical Abstract: Fusarium head blight (FHB) is a global cereal disease caused by a complex of Fusarium species. In Europe, the main species responsible for FHB are F. graminearum, F. culmorum and F. poae. However, members of the F. tricinctum species complex (FTSC) have become increasingly important. FTSC fusaria can synthesize mycotoxins such as moniliformin (MON), enniatins (ENNs) and several other biologically active secondary metabolites that could compromise food quality. In this study, FTSC isolates primarily from Italian durum wheat and barley, together with individual strains from four non-graminaceous hosts, were collected to assess their genetic diversity and determine their potential to produce mycotoxins in vitro on rice cultures. A multilocus DNA sequence dataset (TEF1, RPB1 and RPB2) was constructed for 117 isolates from Italy and 6 from Iran to evaluate FTSC species diversity and their evolutionary relationships. Phylogenetic analyses revealed wide genetic diversity among Italian FTSC isolates. Among previously described FTSC species, F. avenaceum (FTSC 4) was the most common species in Italy (56/117 = 47.9%) while F. tricinctum (FTSC 3), and F. acuminatum (FTSC 2) accounted 11.1% (13/117) and the 8.5% (10/117), respectively. The second most detected species was a new and unnamed Fusarium sp. (FTSC 12; 32/117 = 19%) resolved as the sister group of F. tricinctum. Collectively, these four phylospecies accounted for 111/117 = 94.9% of the Italian FTSC collection. However, we identified five other FTSC species at low frequencies, including F. iranicum (FTSC 6) and three newly discovered species (Fusarium spp. FTSC 13, 14, 15). Of the 59 FTSC isolates tested for mycotoxin production on rice cultures, 54 and 55 strains, respectively, were able to produce detectable levels of ENNs and MON. In addition, we confirmed that the ability to produce bioactive secondary metabolites such as chlamydosporol, acuminatopyrone, longiborneol, fungerin and butanolide is widespread across the FTSC.