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.

The vascular wilt fungi Verticillium dahliae and V. albo-atrum infect over 200 plant species, causing billions of dollars in annual crop losses. The characteristic wilt symptoms are a result of colonization and proliferation of the pathogens in the xylem vessels, which undergo fluctuations in osmolarity. To gain insights into the mechanisms that confer the organisms' pathogenicity and enable them to proliferate in the unique ecological niche of the plant vascular system, we sequenced the genomes of V. dahliae and V. albo-atrum and compared them to each other, and to the genome of Fusarium oxysporum, another fungal wilt pathogen. Our analyses identified a set of proteins that are shared among all three wilt pathogens, and present in few other fungal species. One of these is a homolog of a bacterial glucosyltransferase that synthesizes virulence-related osmoregulated periplasmic glucans in bacteria. Pathogenicity tests of the corresponding V. dahliae glucosyltransferase gene deletion mutants indicate that the gene is required for full virulence in the Australian tobacco species Nicotiana benthamiana. Compared to other fungi, the two sequenced Verticillium genomes encode more pectin-degrading enzymes and other carbohydrate-active enzymes, suggesting an extraordinary capacity to degrade plant pectin barricades. The high level of synteny between the two Verticillium assemblies highlighted four flexible genomic islands in V. dahliae that are enriched for transposable elements, and contain duplicated genes and genes that are important in signaling/transcriptional regulation and iron/lipid metabolism. Coupled with an enhanced capacity to degrade plant materials, these genomic islands may contribute to the expanded genetic diversity and virulence of V. dahliae, the primary causal agent of Verticillium wilts. Significantly, our study reveals insights into the genetic mechanisms of niche adaptation of fungal wilt pathogens, advances our understanding of the evolution and development of their pathogenesis, and sheds light on potential avenues for the development of novel disease management strategies to combat destructive wilt diseases. Vascular wilts are chronic and very often severe plant diseases that cause billions of dollars in annual crop losses. The characteristic wilt symptom is a result of water blockage caused by the colonization and proliferation of pathogenic microbes in the plant xylem, a water-conducting system. We sequenced genomes of two Verticillium wilt pathogens and compared them to the genome of another wilt fungus, Fusarium oxysporum. The shared genomic features among these three wilt fungi suggest the acquisition of homologs of a bacterial glucosyltransferase, involved in adaptation to osmotic stress, through horizontal transfer. Analyses of glucosyltransferase gene deletion mutants in Verticillium dahliae revealed decreased virulence in the host plant Nicotiana benthamiana. Compared to other fungi, both Verticillium genomes encode more plant cell wall degrading enzymes, including those that are able to degrade cell walls of live plants. Between the two closely related Verticillium genomes, we discovered flexible genomic islands in the primary causal agent of Verticillium wilts, Verticillium dahliae. Coupled with the impressive arsenal of plant cell wall-degrading enzymes, these flexible genomic islands may have contributed to expanding genetic diversity for this organism to invade more plant hosts. In summary, our study reveals insights into the evolution and niche adaptation of fungal wilt pathogens and sheds light on the development of novel disease management strategies for combating the destructive wilt diseases.

Brown rot decay removes cellulose and hemicellulose from wood—residual lignin contributing up to 30% of forest soil carbon—and is derived from an ancestral white rot saprotrophy in which both lignin and cellulose are decomposed. Comparative and functional genomics of the “dry rot” fungus Serpula lacrymans, derived from forest ancestors, demonstrated that the evolution of both ectomycorrhizal biotrophy and brown rot saprotrophy were accompanied by reductions and losses in specific protein families, suggesting adaptation to an intercellular interaction with plant tissue. Transcriptome and proteome analysis also identified differences in wood decomposition in S. lacrymans relative to the brown rot Postia placenta. Furthermore, fungal nutritional mode diversification suggests that the boreal forest biome originated via genetic coevolution of above- and below-ground biota.

• Parasitism and saprotrophic wood decay are two fungal strategies fundamental for succession and nutrient cycling in forest ecosystems. An opportunity to assess the trade‐off between these strategies is provided by the forest pathogen and wood decayer Heterobasidion annosum sensu lato. • We report the annotated genome sequence and transcript profiling, as well as the quantitative trait loci mapping, of one member of the species complex: H. irregulare. Quantitative trait loci critical for pathogenicity, and rich in transposable elements, orphan and secreted genes, were identified. • A wide range of cellulose‐degrading enzymes are expressed during wood decay. By contrast, pathogenic interaction between H. irregulare and pine engages fewer carbohydrate‐active enzymes, but involves an increase in pectinolytic enzymes, transcription modules for oxidative stress and secondary metabolite production. • Our results show a trade‐off in terms of constrained carbohydrate decomposition and membrane transport capacity during interaction with living hosts. Our findings establish that saprotrophic wood decay and necrotrophic parasitism involve two distinct, yet overlapping, processes.

The appropriate development of conidia and appressoria is critical in the disease cycle of many fungal pathogens, including Magnaporthe oryzae. A total of eight genes (MoHOX1 to MoHOX8) encoding putative homeobox transcription factors (TFs) were identified from the M. oryzae genome. Knockout mutants for each MoHOX gene were obtained via homology-dependent gene replacement. Two mutants, ΔMohox3 and ΔMohox5, exhibited no difference to wild-type in growth, conidiation, conidium size, conidial germination, appressorium formation, and pathogenicity. However, the ΔMohox1 showed a dramatic reduction in hyphal growth and increase in melanin pigmentation, compared to those in wild-type. ΔMohox4 and ΔMohox6 showed significantly reduced conidium size and hyphal growth, respectively. ΔMohox8 formed normal appressoria, but failed in pathogenicity, probably due to defects in the development of penetration peg and invasive growth. It is most notable that asexual reproduction was completely abolished in ΔMohox2, in which no conidia formed. ΔMohox2 was still pathogenic through hypha-driven appressoria in a manner similar to that of the wild-type. However, ΔMohox7 was unable to form appressoria either on conidial germ tubes, or at hyphal tips, being non-pathogenic. These factors indicate that M. oryzae is able to cause foliar disease via hyphal appressorium-mediated penetration, and MoHOX7 is mutually required to drive appressorium formation from hyphae and germ tubes. Transcriptional analyses suggest that the functioning of M. oryzae homeobox TFs is mediated through the regulation of gene expression and is affected by cAMP and Ca²⁺ signaling and/or MAPK pathways. The divergent roles of this gene set may help reveal how the genome and regulatory pathways evolved within the rice blast pathogen and close relatives. Pathogens have evolved diverse strategies to cause disease. Magnaporthe oryzae is the fungal phytopathogen that causes rice blast and is considered an important model for understanding mechanisms in fungal development and pathogenicity. Asexual reproduction and infection-related development play key roles in M. oryzae disease development. The conidium of M. oryzae differentiates a specialized structure, an appressorium. The appressorium generates turgor pressure that allows penetration through the mechanical rupture of host cuticle layers. After colonizing host cells, the fungus produces massive conidia via conidiogenesis, serving as secondary propagules for the polycyclic disease. To elucidate molecular mechanisms in asexual reproduction and appressorium-mediated disease development, we identified eight homeobox transcription factors through a genome-wide in silico analysis. Characterization using deletion mutants revealed that each homeobox TF functions as a stage-specific regulator for conidial shape, hyphal growth, conidiation, appressorium development, and invasive growth during M. oryzae development. Notably, conidiation and appressorium development were entirely abolished in ΔMohox2 and ΔMohox7, respectively. This study also provides evidence that M. oryzae is able to cause rice blast by means of hypha-driven appressoria upon responses to host signaling factors. This study will aid in the understanding of regulatory networks associated with fungal development and pathogenicity.