Rapid Divergence of Genome Architectures Following the Origin of an Ectomycorrhizal Symbiosis in the Genus Amanita

Abstract

Fungi are evolutionary shape shifters and adapt quickly to new environments. Ectomycorrhizal (EM) symbioses are mutualistic associations between fungi and plants and have evolved repeatedly and independently across the fungal tree of life, suggesting lineages frequently reconfigure genome content to take advantage of open ecological niches. To date analyses of genomic mechanisms facilitating EM symbioses have involved comparisons of distantly related species, but here, we use the genomes of three EM and two asymbiotic (AS) fungi from the genus Amanita as well as an AS outgroup to study genome evolution following a single origin of symbiosis. Our aim was to identify the defining features of EM genomes, but our analyses suggest no clear differentiation of genome size, gene repertoire size, or transposable element content between EM and AS species. Phylogenetic inference of gene gains and losses suggests the transition to symbiosis was dominated by the loss of plant cell wall decomposition genes, a confirmation of previous findings. However, the same dynamic defines the AS species A. inopinata, suggesting loss is not strictly associated with origin of symbiosis. Gene expansions in the common ancestor of EM Amanita were modest, but lineage specific and large gene family expansions are found in two of the three EM extant species. Even closely related EM genomes appear to share few common features. The genetic toolkit required for symbiosis appears already encoded in the genomes of saprotrophic species, and this dynamic may explain the pervasive, recurrent evolution of ectomycorrhizal associations.

Large-scale genome sequencing of mycorrhizal fungi provides insights into the early evolution of symbiotic traits

“…Prior comparisons of genomes from ectomycorrhizal, orchid and ericoid mycorrhizal fungi, wood decayers and soil decomposers have elucidated the mechanisms of several transitions from saprotrophy to mutualism in Dikarya [9][10][11][12][13][14][15][16] . These analyses have shown that multiple lineages of ectomycorrhizal fungi have lost most genes encoding lignocellulose-degrading enzymes present in their saprotrophic ancestors, explaining the reduced capacity of ectomycorrhizal fungi to acquire C complexed in soil organic matter (SOM) and plant cell walls 17 and, as a consequence, their increasing dependence on the host plant sugars.…”

Laccaria bicolor MiSSP8 is a small‐secreted protein decisive for the establishment of the ectomycorrhizal symbiosis

“…A comparative phylogenomics analysis of 49 fungal genomes revealed that ECM fungi have evolved several times from saprotrophic ancestors, these being either white rot, brown rot or soil decayers, by developing a set of symbiotic genes with rapid turnover, and in particular gain of genes such as MiSSPs (Kohler et al ., ). Moreover, a recent comparative analysis of five Amanita genomes, two ECM symbionts and three asymbiotic species concluded that several genetic components of the toolkit used by ECM symbionts are already encoded in the genome of their saprotrophic relatives, explaining the recurrent emergence of the ECM symbiosis over time (Hess et al ., ). Consistent with this finding, MiSSP8 shares similarities with other saprotrophic proteins through its fungal‐specific repetitive motif.…”

Seeking the Roles for Fungal Small-Secreted Proteins in Affecting Saprophytic Lifestyles

“…In fact, 34 out of 201 species of wood-decay basidiomycetes were shown to be able to colonize the roots of at least one tree species, supporting the feasibility for facultative biotrophic relationships in some free-living saprotrophs (Smith et al, 2017). Research on the genus Amanita showed that the origin of the genetic toolkit required for symbiosis is found in a saprotrophic species (Hess et al, 2018). Could some of these features be attributed to the unknown and partially conserved effectors in the genome of saprophytes?…”