Fusarium poae: Secondary Metabolism and Accessory Chromosomes

Abstract

Fusarium poae is of concern to plant pathologists as it is a globally distributed contributor to Fusarium head blight in wheat, barley and oats, and threatens consumers by the production of harmful mycotoxins. Recent characterization of F. poae strain genomic architecture revealed the species harbors small chromosomes with structural features and genetic content consistent with rapidly evolving 'accessory' genomes in plant pathogenic fungi. Termed 'supernumerary' or 'accessory' chromosomes, these dynamic chromosomes can encode transcriptionally active secondary metabolite biosynthetic gene clusters (BGCs), high numbers of transposable elements, and undergo frequent sequence duplications, disruptions, inversions and translocations compared to core chromosomes. The presence of accessory chromosomes with active BGCs is promising for the discovery of novel chemistry within a population via untargeted metabolomic screening, and has implications for the evolution of endophytic and pathogenic fungi. In this thesis research, an untargeted metabolomics profiling method was developed and applied alongside population-level, whole-genome sequencing to analyze the chemistry of Canadian F. poae populations. F. poae metabolomes included a mixture of diverse trichothecene mycotoxins and other secondary metabolites of interest to plant pathogen research. Furthermore, genomic analyses indicated F. poae strains are incapable of producing T-2/HT-2 toxins, strictly regulated trichothecenes which were historically predicted to be produced by F. poae. Telomereto-telomere genome assemblies revealed the presence of highly polymorphic accessory chromosomes with lineage-specific BGCs affecting secondary metabolite profiles detected in vitro and in planta. Ten percent of the profiled F. poae strains were predicted to have an accessory chromosome expressing the BGC for the acutely toxic cyclic peptide apicidin, not previously known to be produced by F. poae. Furthermore, a rare BGC on an accessory chromosome was characterized to produce fusadapamides, novel small peptide secondary metabolites distinguished by their incorporation of L-2,3-diaminopropionic acid (Dap). Dap is a rare, non-proteinogenic amino acid which was not known to be produced by fungi prior to this research. The multi-omics analysis presented in this thesis contributes to the understanding of fungal accessory chromosomes as dynamic genomic reservoirs for unique secondary metabolite diversity within species. The genomic and metabolomic data produced in this research are foundational for further research to understand the biology of F. poae colonization of cereal crop hosts.