Abstract

Since the completion of the yeast genome, fungal genomics are leading eukaryotic genomics research advancing our knowledge in comparative genomics to pan-genomics and population genomics of fungi along with the rapid spread of sequencing technologies. The early studies of single fungal genomes told us in particular the gene contents, sex nature and particular protein families in association with fungal life styles. Pan-genome sequencing of fungal strains of the same or different species belonging to the same genus is facilitating the understanding of fungal speciation trajectory, convergence and divergence evolutions. The accumulated evidence of substantial genetic alternations existing between fungal strains promotes the sequencing/resequencing of dozens to hundreds of isolates collected from different environments for a single species. Population genomic/genetic studies of these isolates can well benefit the understanding of species origin, adaptation (including domestication), genetic selection, and phenotype-genotype associations. We are studying ascomycete insect pathogenic fungi. Genome sequencing of the model species of Metarhizium and Beauveria indicated that insect pathogens evolved with the expanded families of proteases and chitinases to target the protein- and chitin-rich insect cuticles. Species of insect pathogens can perform either sexual or asexual reproduction in nature that determines the genome structures. Comparative and phylogenomic analyses of Metarhizium species with different host ranges revealed that the generalist species evolved from the specialists via transitional species with intermediate host ranges and that this shift paralleled insect host speciation and evolution. We found that fungal host specialization was associated with the retention of sexuality and rapid evolution of existing protein sequences whereas generalization was associated with protein-family expansion, loss of genome-defense mechanisms, genome restructuring, horizontal gene transfer, and positive selection that was accelerated after reinforcement of reproductive isolation. Comparative genomic analysis with the plant and mammalian pathogens indicated that, unexpectedly, more common orthologous protein groups are shared between the insect and plant pathogens than between the insect and mammalian pathogens. We also found that the pathogenicity of host-adapted fungi evolved multiple times, and that both divergent and convergent evolution occurred during pathogen-host arms races. In particular, the effector-like proteins identified in plant and animal pathogens are highly linked to fungal host adaptation, suggesting the existence of similar gene-for-gene relationships in fungus-animal interactions that has not been established before. We also performed population genetics analysis of more than 200 field isolates of B. bassiana and revealed the population genetic diversity variations between seasons, frequent host jumping, and genetic recombination and exchanges between strains and populations. It is of importance to find that the industrial strain released for insect pest control could persist in the field and infect non-target hosts but could not displace the local populations. For different fungal species, more population genetics studies are required to help understand the nature and features of fungal adaptation to diverse environments including hosts.

Abstract