Comparative analyses reveal rapid turnover and emergence of transitory 3D genome architectures in the fungal kingdom

The three-dimensional architecture of genomes plays major roles in biological processes such as gene expression and DNA replication. The architecture of genomes has evolved substantially with distinct 3D genome shapes being identified in different lineages. The factors driving the evolution of genome architectures have primarily been assessed in animals and plants, yet large parts of the tree of life remain poorly explored. Fungi offer excellent models to assess the evolution of 3D genome architecture in a phylogenetic context given rapid genome size changes and chromosomal sequence turnover. Here, we analyzed chromosome conformation data (Hi-C) of 55 fungal species with completely assembled genomes. We identified ten species with Rabl, one species with chromosome territories and ten with a novel, intermediate chromosomal architecture, where centromeres and telomeres are at opposites in the nucleus (Rabl-like) but with a distinct 3D organization. This "bean" shape likely evolved several times independently. The discovery of a genome with a chromosome territories conformation was unexpected, as this was thought to be associated with condensin II subunits in the animal kingdom. We investigated whether 3D conformations correlated with genome size and repeat content using phylogenetic independent contrasts, however we found no genomic feature to be significantly associated with changes in genome architecture. Overall, we report the first large-scale comparison of 3D genome architecture in the fungal kingdom and identify a novel "bean" configuration. SignificanceThree-dimensional genome architecture strongly influences gene regulation, yet little is known about 3D genome architecture in an organismal group that has adapted to nearly all ecosystems on our planet, Fungi. We reconstructed 3D genome architectures from 55 fungal species covering three different phyla and demonstrate that most species do not conform to the existing definitions of 3D architectures. We identified the first case of Chromosome Territories in the Fungal Kingdom and a previously undescribed organization that we label "bean-shaped", and show that some fungal species do not conform to the canonical 3D-architecture categories of the animal and plant kingdoms. The diversity of genome architectures observed in the study could reflect the diverse gene regulatory mechanisms known from Fungi and marks the beginning of mapping out 3D genome organizations in this diverse clade. Further research in this area will uncover the diverse strategies employed by Fungi in light of their rapid adaptation.