Phylogenetic diversity and mycotoxin potential of emergent phytopathogens within the Fusarium tricinctum species complex

Authors: LARABA, IMANE - Orise Fellow; Busman, Mark; GEISER, DAVID - Pennsylvania State University; O Donnell, Kerry

Submitted to: Phytopathology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/4/2022
Publication Date: 5/5/2022
Citation: Laraba, I., Busman, M., Geiser, D.M., O'Donnell, K. 2022. Phylogenetic diversity and mycotoxin potential of emergent phytopathogens within the Fusarium tricinctum species complex. Phytopathology. 112(6):1284-1298. https://doi.org/10.1094/PHYTO-09-21-0394-R.
DOI: https://doi.org/10.1094/PHYTO-09-21-0394-R

Interpretive Summary: Fusarium head blight (FHB) is increasingly becoming a constraint to cereal production globally. The Fusarium pathogens responsible for this economically destructive disease also pose a significant threat to food safety and human health because they frequently contaminate food and feed with several toxins. Recent pathogen surveys within the United States and elsewhere throughout the world have reported members of the F. tricinctum species complex (FTSC) are becoming important contributors to FHB. To date, no global survey has been conducted to assess pathogen diversity within the FTSC and their toxin potential. Thus, a 151-strain collection originating from diverse hosts and substrates from different agroclimatic regions throughout the world was selected from 460 strains to represent the breadth of FTSC diversity. Analyses of DNA data resolved the 151 strains as 24 genetically distinct species, including nine that are new to science. In addition, our reanalysis of nine published DNA-based studies on the FTSC identified 11 additional novel taxa, suggesting this complex comprises at least 36 species. Toxin analyses of FTSC strains grown on cracked corn cultures revealed they produce structurally diverse toxins, among which enniatins and moniliformin are the most frequent and of greatest concern to food safety. Results on FTSC pathogen diversity and toxin potential will be of interest to plant disease specialists, quarantine officials and plant breeders who are focused on controlling Fusarium pathogens, minimizing toxin contamination of food and feed and developing cereal cultivars with broad based resistance to FHB.

Technical Abstract: Recent studies on multiple continents indicate members of the Fusarium tricinctum species complex (FTSC) are emerging as predominant pathogens of small-grain cereals, pulses, and other economically important crops. These understudied fusaria produce structurally diverse mycotoxins, among which enniatins (ENNs) and moniliformin (MON) are the most frequent and of greatest concern to food and feed safety. Herein a large survey of fusaria in the Fusarium Research Center and Agricultural Research Service culture collections was undertaken to assess species diversity and mycotoxin potential within the FTSC. A 151-strain collection originating from diverse hosts and substrates from different agroclimatic regions throughout the world was selected from 460 FTSC strains to represent the breadth of FTSC phylogenetic diversity. Evolutionary relationships inferred from a 5-locus dataset, using maximum likelihood and parsimony, resolved the 151 strains as 24 phylogenetically distinct species, including nine that are new to science. Of the five genes analyzed, nearly full-length phosphate permease sequences contained the most phylogenetically informative characters, establishing its suitability for species-level phylogenetics within the FTSC. Fifteen of the species produced ENNs, MON, the sphingosine analog 2-amino-14,16- dimethyloctadecan-3-ol (AOD), and the toxic pigment aurofusarin (AUR) on a cracked corn kernel substrate. Interestingly, the five most basal species in the FTSC phylogeny (i.e., F. iranicum, F. flocciferum, F. torulosum, Fusarium spp. FTSC 8 and 24) failed to produce AOD and MON, but synthesized ENNs and/or AUR. Moreover, our reassessment of nine published phylogenetic studies on the FTSC identified 11 additional novel taxa, suggesting this complex comprises at least 36 species.