Patterns and mechanisms of fungal genome plasticity

The fungal kingdom is a diverse eukaryotic clade largely composed of microbial organisms. Comprised of indispensable plant symbionts, major environmental decomposers, and important plant and animal pathogens, fungi directly shape the biological world. Advancements in genomics have increased our understanding of fungal genomic variation, the mechanisms that generate it, and the association of genomic plasticity with fungal ecological lifestyles and adaptation. In this review, we discuss the patterns and mechanisms underlying fungal genomic plasticity, juxtaposing them, where known, with patterns and mechanisms observed in plants and animals. We begin by describing the plasticity of fungal genomes, which ranges from large-scale variation in size and ploidy to the physical or temporal compartmentalization of evolutionary rates. We summarize notable patterns of genomic plasticity that have evolved independently across the fungal kingdom, including but not limited to accessory chromosomes, two-speed genomes, and hypermutation; some of these patterns are unique to fungi and largely absent from animals or plants. Strikingly, certain patterns are associated with specific ecological lifestyles, raising the hypothesis that the plasticity of fungal genomes facilitates these lifestyles. We then describe the wide variety of mechanisms that contribute to fungal genome plasticity, including sexual reproduction, transposable-element mobilization, and aneuploidy. Some mechanisms appear to be lineage-specific (for example, Starship transposable elements and repeat-induced point mutations), whereas others are more broadly distributed (parasexual and sexual reproduction). We conclude by discussing how a more balanced sampling of fungal genomes, including population genomic data, will lead to greater insights into fungal genome plasticity and its origins.