Population genomics of Fusarium graminearum reveals signatures of divergent evolution within a major cereal pathogen

Authors: Kelly, Amy; Ward, Todd

Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/6/2018
Publication Date: 3/27/2018
Citation: Kelly, A.C., Ward, T.J. 2018. Population genomics of Fusarium graminearum reveals signatures of divergent evolution within a major cereal pathogen. PLoS One. 13(3):e0194616.

Interpretive Summary: Fusarium graminearum is the major cause of Fusarium head blight (FHB), a significant disease of wheat, barley, and other cereal crops world-wide. In addition, the fungus contaminates grain with mycotoxins that pose a significant threat to food safety and animal health. The recent appearance of novel pathogen populations and toxin types in North America is of concern because this diversity may include novel adaptations that enable the fungus to rapidly adapt in response to FHB control measures. Therefore, we sequenced the genomes of 60 isolates of F. graminearum sampled across North America to identify genes that play a key role in helping this important pathogen adapt to agricultural environments. We demonstrated that there are at least three distinct pathogen populations in North America and identified 121 genes that distinguish these populations. In addition, we identified 14 regions of the genome that have responded differently to selection pressure in these populations, indicating that these regions of the genome harbor population-specific adaptations. Based on the functions encoded by genes that distinguish these populations, our findings suggest that FHB pathogen populations utilize unique sets of tools to invade and obtain nutrients from their hosts, compete with other microbes, and adapt to different climatic conditions. The genes identified in this study will be of use to scientists, disease control specialists, and producers working to develop and deploy more effective disease and mycotoxin control measures that counter adaptations within all of the major FHB pathogen populations.

Technical Abstract: The cereal pathogen Fusarium graminearum is the primary cause of Fusarium head blight (FHB) and a significant threat to food safety and crop production. To elucidate population structure and identify genomic targets of selection within major FHB pathogen populations in North America we sequenced the genomes of 60 diverse F. graminearum isolates. We also assembled the first pan-genome for F. graminearum to clarify population-level differences in gene content potentially contributing to adaptive diversity. Bayesian and phylogenomic analyses revealed genetic structure associated with the novel NX-2 mycotoxin, suggesting an endemic population that has remained genetically distinct from native and introduced cereal-infecting populations. Genome scans uncovered distinct signatures of selection within populations, focused in high diversity, frequently recombining regions. These patterns suggested significant adaptive divergence at the trichothecene toxin gene cluster and thirteen additional regions containing genes potentially involved in pathogen specialization. Gene content differences further distinguished populations, in that 121 genes showed population-specific patterns of conservation indicative of divergent selection. Genes that differentiated populations had predicted functions related to pathogenesis, secondary metabolism and antagonistic interactions, though a subset had unique roles in temperature and light sensitivity. Our results indicated that F. graminearum populations are distinguished by dozens of genes with signatures of selection, and an array of modular, accessory genes, suggesting that each of these FHB pathogen populations are equipped with different adaptations to exploit the agroecosystem. These findings provide insights into the genomic bases for population divergence in plant pathogens and highlight specific genes that may be responsible for population-level adaptation across evolutionarily and ecologically diverse fungi.