The landscape and predicted roles of structural variants in Fusarium graminearum genomes

Authors: DHAKAL, UPASANA - Kansas State University; Kim, Hye-Seon; TOOMAJIAN, CHRISTOPHER - Kansas State University

Submitted to: Genes, Genomes, and Genomics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/22/2024
Publication Date: 3/28/2024
Citation: Dhakal, U., Kim, H.-S., Toomajian, C. 2024. The landscape and predicted roles of structural variants in Fusarium graminearum genomes. Genes, Genomes, and Genomics. https://doi.org/10.1093/g3journal/jkae065.
DOI: https://doi.org/10.1093/g3journal/jkae065

Interpretive Summary: The fungus Fusarium graminearum causes head blight disease of wheat and barley and contaminates grain with toxins that pose health hazards to humans and animals. Together, head blight and toxin contamination can cause losses of hundreds of millions of dollars to U.S. agriculture each year. It is not clear how naturally occurring changes to chromosomes of F. graminearum contribute to the ability of the fungus to continue to cause head blight epidemics and toxin contamination with changing agricultural practices and environmental conditions. To address this knowledge gap, scientists at ARS in Peoria, Illinois, and Kansas State University compared high-quality genome sequences from eight strains of F. graminearum that represent a wide range of genetic diversity of the fungus that exists in North America. They discovered marked differences in chromosomes among North American strains of F. graminearum. These differences indicate acquisition, loss, and rearrangements of many genes, including genes that can affect the ability of the fungus to infect and colonize plants and to produce toxins. Knowledge of changes that occur to F. graminearum chromosomes as the fungus adapts to changing conditions will aid efforts to control head blight epidemics and toxin contamination through plant breeding, fungicides and other methods.

Technical Abstract: Structural rearrangements, such as inversions, translocations, duplications, and large insertions and deletions, are large-scale genomic variants that can play an important role in shaping phenotypic variation and in genome adaptation and evolution. We used chromosomal-level assemblies from eight Fusarium graminearum isolates to study structural variants and their role in fungal evolution. We generated the assemblies of four of these genomes after Oxford Nanopore sequencing. A total of 87 inversions, 159 translocations, 245 duplications, 58,489 insertions and 34,102 deletions were detected. Regions of high recombination rate are associated with structural rearrangements, and a significant proportion of inversions, translocations, and duplications overlap with the repeat content of the genome, suggesting recombination and repeat elements are major factors in the origin of structural rearrangements in F. graminearum. Large insertions and deletions introduce presence-absence polymorphisms for many genes, including secondary metabolite biosynthesis cluster genes and predicted effectors genes. Translocation events were found to be shuffling predicted effector-rich regions of the genomes and are likely contributing to the gain and loss of effectors facilitated by recombination. Breakpoints of some structural rearrangements fall within coding sequences and are likely altering the protein products. Structural rearrangements in F. graminearum thus have an important role to play in shaping pathogen-host interactions and broader evolution through genome reorganization, the introduction of presence-absence polymorphisms, and changing protein products and gene regulation.