Adaptive Genome Architecture and Evolution in Verticillium
Fungal plant pathogens adapt rapidly to changing hosts and environments. In Verticillium dahliae, this adaptability is encoded in a genome with a highly compartmentalized architecture, consisting of a conserved core genome and dynamic adaptive regions enriched for genes involved in host interaction.
Early work from our group revealed that these adaptive regions are structurally plastic, show extensive presence–absence variation, and are enriched in transposable elements and pathogenicity-related genes. This organization provides a framework for rapid genome evolution and strain-specific adaptation.
Left: Chromosomal karyotypes of a set of Verticillium dahliae strains as determined by pulsed-field gel electrophoresis, revealing significant chromosome length and structure polymorphisms between strains.
Right: Circos diagram illustrating collinear blocks in alignments between the eight chromosomes of Verticillium dahliae strains VdLs17 (gray) and JR2 (white). Lineage-specific sequences are indicated as red segments on the chromosomes (figure adapted from de Jonge et al. 2013 & Faino et al., 2016).
Recent research has uncovered the regulatory and structural principles underlying this plasticity. Adaptive regions display a distinct chromatin environment characterized by facultative heterochromatin marks (notably H3K27me3) and altered chromatin accessibility. These features are associated with local, rather than global, changes in gene regulation, highlighting the importance of epigenetic control in shaping genome function.
Left: Collective epigenome and physical DNA characteristics define core and LS regions in V. dahliae. Left: Grouped heatmaps for ten variables collected for transposable elements in the V. dahliae genome, arranged by LS (top) or core (below) localization. The boxes highlight core TEs with euchromatin profiles.
Right: Principal component analysis for seven (epi)genomic variables in 10 kb windows either belonging to core or LS genomic regions (figure adapted from Cook et al. 2020).
Transposable elements are major drivers of this genome dynamics. Active and lineage-specific elements contribute to structural variation and influence the expression of nearby genes, thereby generating functional diversity within pathogen populations. More recently, we showed that genome evolution is also shaped by three-dimensional genome organization. Adaptive regions form characteristic long-range interactions and occupy distinct nuclear domains, linking spatial genome architecture to evolutionary potential.
Adaptive genomic regions physically colocalize in Verticillium dahliae. The circular plot displays the eight chromosomes of V. dahliae with centromeres highlighted in yellow, adaptive genomic regions (AGRs) in blue, and core regions in white. Long-range interactions Edges for centromeric interactions are shown in yellow, AGR interactions in blue, and core interactions in gray.
Our latest work identifies giant mobile elements, termed Starships, as key agents of genome innovation. These elements mobilize large genomic cargo, including virulence-associated genes, and play a central role in shaping adaptive genomic regions and driving virulence evolution. ([40707455])
Together, these findings support a model in which genome evolution in V. dahliae emerges from the interplay between transposable elements, chromatin state, and 3D genome architecture, enabling rapid adaptation and the emergence of new pathogenic traits.
Diverse Starships populate the Verticillium genus. The tree shows the phylogeny of 56 strains based on whole-genome sequence alignments with repertoires of Starship haplotypes (hap.) per strain.
Most relevant literature
Sato et al. (2025). Starship giant transposons dominate plastic genomic regions in a fungal plant pathogen and drive virulence evolution. Nat Commun. 16: 6806.
Torres et al. (2024). Implications of the three-dimensional chromatin organization for genome evolution in a fungal plant pathogen. Nat Commun. 15: 1701.
Kramer et al. (2023). Epigenetic regulation of nuclear processes in fungal plant pathogens. PLoS Pathog. 19: e1011525.
Kramer et al. (2021). Local Rather than Global H3K27me3 Dynamics Are Associated with Differential Gene Expression in Verticillium dahliae. mBio 13: e0356621.
Depotter et al. (2021). The interspecific fungal hybrid Verticillium longisporum displays subgenome-specific gene expression. mBio 12: e0149621.
Torres et al. (2021). Transposable elements contribute to genome dynamics and gene expression variation in the fungal plant pathogen Verticillium dahliae. Genome Biol Evol. 13: evab135.
Kramer et al. (2021). Three putative DNA methyltransferases of Verticillium dahliae differentially contribute to DNA methylation that is dispensable for growth, development and virulence. Epigenetics Chromatin 14: 21.
Cook et al., (2020). A unique chromatin profile defines adaptive genomic regions in a fungal plant pathogen. eLife 9: e62208.
Seidl et al., (2020). Repetitive elements contribute to the diversity and evolution of centromeres in the fungal genus Verticillium. mBio 11: e01714-20.
Depotter et al. (2019). Dynamic virulence-related regions of the plant pathogenic fungus Verticillium dahliae display enhanced sequence conservation. Molecular Ecology 28: 3482-3495.
Shi-Kunne et al. (2018). Evolution within the fungal genus Verticillium is characterized by chromosomal rearrangement and gene loss. Environmental Microbiology 20: 1362-1373.
Seidl MF, Cook DE, Thomma BPHJ (2016). Chromatin biology impacts adaptive evolution of filamentous plant pathogens. PLoS Pathogens 12: e1005920.
Faino et al. (2016). Transposons passively and actively contribute to evolution of the two-speed genome of a fungal pathogen. Genome Research 26: 1091-1100.
Faino et al. (2015). Single-Molecule Real-Time sequencing combined with optical mapping yields completely finished fungal genome. mBio 6: e00936-15.
Cook DE, Mesarich CH, Thomma BPHJ (2015). Understanding plant immunity as a surveillance system to detect invasion. Annual Review of Phytopathology 53: 541-563.
Seidl & Thomma (2014). Sex or no sex: evolutionary adaptation occurs regardless. Bioessays 36: 335-345.
de Jonge et al. (2013). Extensive chromosomal reshuffling drives evolution of virulence in an asexual pathogen. Genome Research 23: 1271-1282.
de Jonge et al. (2012). Tomato immune receptor Ve1 recognizes effector of multiple fungal pathogens uncovered by genome and RNA sequencing. Proceedings of the National Academy of Sciences of the USA 109: 5110-5115.