Fusarium species are among the most important phytopathogenic and toxigenic fungi. To understand the molecular underpinnings of pathogenicity in the genus Fusarium, we compared the genomes of three phenotypically diverse species: Fusarium graminearum, Fusarium verticillioides and Fusarium oxysporum f. sp. lycopersici. Our analysis revealed lineage-specific (LS) genomic regions in F. oxysporum that include four entire chromosomes and account for more than one-quarter of the genome. LS regions are rich in transposons and genes with distinct evolutionary profiles but related to pathogenicity, indicative of horizontal acquisition. Experimentally, we demonstrate the transfer of two LS chromosomes between strains of F. oxysporum, converting a non-pathogenic strain into a pathogen. Transfer of LS chromosomes between otherwise genetically isolated strains explains the polyphyletic origin of host specificity and the emergence of new pathogenic lineages in F. oxysporum. These findings put the evolution of fungal pathogenicity into a new perspective.
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Acknowledgements The 43 sequence of F. verticillioides was provided by Syngenta Biotechnology Inc. Generation of the other 43 sequence of F. verticillioides and 6.83 sequence of F. oxysporum f. sp. lycopersici was funded by the National Research Initiative of USDA’s National Institute of Food and Agriculture through the Microbial Genome Sequencing Program (2005-35600-16405) and conducted by the Broad Institute Sequencing Platform. Wayne Xu and the Minnesota Supercomputing Institute for Advanced Computational Research are also acknowledged for their support. The authors thank Leslie Gaffney at the Broad Institute for graphic design and editing and Tracy E. Anderson of the University of Minnesota, College of Biological Sciences Imaging Center for spore micrographs.