Implications of the three-dimensional chromatin organization for genome evolution in a fungal plant pathogen

Abstract

The spatial organization of eukaryotic genomes is linked to their biological functions, although it is not clear how this impacts the overall evolution of a genome. Here, we uncover the three-dimensional (3D) genome organization of the phytopathogen Verticillium dahliae, known to possess distinct genomic regions, designated adaptive genomic regions (AGRs), enriched in transposable elements and genes that mediate host infection. Short-range DNA interactions form clear topologically associating domains (TADs) with gene-rich boundaries that show reduced levels of gene expression and reduced genomic variation. Intriguingly, TADs are less clearly structured in in AGRs than in the core genome. At a global scale, the genome contains bipartite long-range interactions, particularly enriched for AGRs and more generally containing segmental duplications. Notably, the patterns observed for V. dahliae are also present in other Verticillium species. Thus, our analysis links 3D genome organization to evolutionary features conserved throughout the Verticillium genus.

Nuclear genome organization in fungi: from gene folding to Rabl chromosomes

“…5 , Box 1 ). Additional Hi-C data from a plethora of filamentous fungi show that the centromeres contact independent of—and distinct from—telomere clustering and thus confirmed the existence of Rabl chromosomes, including in ascomycetes [ Penicillium oxalicum (Li et al 2022 ), E. festucae (Winter et al 2018 ), V. dahliae (Seidl et al 2020 , Torres et al 2023 ), Candida albicans (Burrack et al 2016 ), Fusarium verticillioides (Yao et al 2023 ), and Cladosporium fulvum (Zaccaron et al 2022 )] and basidiomycetes [ Puccinia polysora (Liang et al 2022 ), Puccinia graminis (Sperschneider et al 2021 , Henningsen et al 2022 ), Austropuccinia psidii (Edwards et al 2022 ), and Agaricus bisporus (Hoencamp et al 2021 )] ( Table S1 , Supporting Information ). Interestingly, R. irregularis does not show clear centromere bundling for organizing its chromosomes, but it does seem to exhibit telomere bundling (Yildirir et al 2022 ).…”

“…Another example of TAD-like structures is found in V. dahliae and related Verticillium species where Hi-C datasets display TAD-like structures with increased internal chromatin contact probabilities and few intrachromosomal contacts beyond the TAD-like structure boundaries (Fig. 3C ) (Torres et al 2023 ). In contrast to the situation in N. crassa , (differentially) expressed genes occur at, or in proximity to, TAD-like boundaries in V. dahliae and E. festucae , suggesting that TAD-like structures in these fungi are necessary for proper gene expression.…”

“…Even though the hierarchical organization of nuclear genome organization is largely conserved between the fungal species examined to date, we also highlighted intriguing differences between species, including the species-specific characteristics defining TAD-like structures. Recent work comparing the position of TAD-like structures and conservation of TAD boundaries between fungal strains and species of the same genus suggests that there is limited TAD variation (Torres et al 2023 ), which is reminiscent of observations in other eukaryotes (Rao et al 2014 , Harmston et al 2017 , Rowley et al 2017 , Krefting et al 2018 , Fudenberg and Pollard 2019 , Liao et al 2021 , McArthur and Capra 2021 ). These data favor a hypothesis where TAD-like structures are generally conserved in related fungi but may be less conserved when greater fungal diversity is considered.…”

“…(A) A generalized schematic of the folding of chromatin from the “beads-on-a-string” model of the 10-nm fiber in which DNA is bound to histone proteins to form nucleosome, to the formation of loops/globules with the action of cohesin, to the folding of those globules into TAD-like/regional globule clusters in the fungal genome. The folding of TAD-like structures inferred from Hi-C contact data in (B) N. crassa (Rodriguez et al 2022 ) and (C) V. dahliae (Torres et al 2023 ). (D) The compartmentalization of heterochromatic (stronger interactions) and euchromatic regions can be observed in the genome of Rhizophagus irregularis (Yildirir et al 2022 ).…”

A minimal Fanconi Anemia complex in early diverging fungi

“…A hypergeometric distribution test performed on 56 genome datasets showed that the observed co-occurrences of FA genes are not expected at random (with the highest p value = 0.009) (10.5281/zenodo.10911400, Supplementary Table S1 ). Co-occurrence of proteins in distances greater than 250 kb were classified into long-range colocalization patterns 49 . FA genes were not localized on the same contig with any other FA gene in a minority of taxa (7/36 Dikarya and 30/116 EDF) (10.5281/zenodo.10911400, Supplementary Table S1 ).…”