A unique chromatin profile defines adaptive genomic regions in a fungal plant pathogen

Abstract

Genomes store information at scales beyond the linear nucleotide sequence, which impacts genome function at the level of an individual, while influences on populations and long-term genome function remains unclear. Here, we addressed how physical and chemical DNA characteristics influence genome evolution in the plant pathogenic fungus Verticillium dahliae. We identified incomplete DNA methylation of repetitive elements, associated with specific genomic compartments originally defined as Lineage-Specific (LS) regions that contain genes involved in host adaptation. Further chromatin characterization revealed associations with features such as H3 Lys-27 methylated histones (H3K27me3) and accessible DNA. Machine learning trained on chromatin data identified twice as much LS DNA as previously recognized, which was validated through orthogonal analysis, and we propose to refer to this DNA as adaptive genomic regions. Our results provide evidence that specific chromatin profiles define adaptive genomic regions, and highlight how different epigenetic factors contribute to the organization of these regions.

Chromatin profiling reveals genome stability heterogeneity in clinical isolates of the human pathogen Aspergillus fumigatus

“…Here, we described that half of Af293 LINE-transposons were located at subtelomeric regions and contained H3K9me3 modification only at their boundaries, while the other retrotransposon families (e.g., Gypsy, Afut1 and Copia) were mostly localized at internal chromosomal regions and bound by H3K9me3 along their entire length, implying more activity of LINE-transposons when compared to other families. These results are also consistent with recent findings in the fungal plant pathogen Verticillium dahliae, where individual transposon families have distinct epigenetic and compactation profiles (Cook et al, 2020). In this species, the younger transposons display lower level of nucleotide divergence from the consensus sequence and are more transcriptionally active, as opposed to older transposons, which are more mutated and less active (Faino et al, 2016).…”

Transposable Elements Contribute to Genome Dynamics and Gene Expression Variation in the Fungal Plant PathogenVerticillium dahliae

“…Initially, LS regions were solely defined by presence/absence polymorphisms among sequenced strains ( de Jonge et al 2013 ; Faino et al 2016 ). However, subsequent work on the chromatin landscape in V. dahliae has revealed that these LS regions display a unique chromatin profile ( Cook et al 2020 ). Moreover, it was shown that a substantial number of additional genomic regions share chromatin characteristics with LS regions and, accordingly, that the amount of LS DNA has been underestimated ( Cook et al 2020 ).…”

“…However, subsequent work on the chromatin landscape in V. dahliae has revealed that these LS regions display a unique chromatin profile ( Cook et al 2020 ). Moreover, it was shown that a substantial number of additional genomic regions share chromatin characteristics with LS regions and, accordingly, that the amount of LS DNA has been underestimated ( Cook et al 2020 ). The originally identified LS regions, together with the additional genomic regions that share a similar chromatin profile, are now referred to as adaptive genomic regions ( Cook et al 2020 ).…”

“…Moreover, it was shown that a substantial number of additional genomic regions share chromatin characteristics with LS regions and, accordingly, that the amount of LS DNA has been underestimated ( Cook et al 2020 ). The originally identified LS regions, together with the additional genomic regions that share a similar chromatin profile, are now referred to as adaptive genomic regions ( Cook et al 2020 ). Importantly, these adaptive genomic regions are enriched for in planta-induced effector genes that contribute to host colonization ( Klosterman et al 2011 ; de Jonge et al 2012 , 2013 ; Kombrink et al 2017 ; Gibriel et al 2019 ; Cook et al 2020 ; Chavarro-Carrero et al 2021 ).…”

A 20‐kb lineage‐specific genomic region tames virulence in pathogenic amphidiploid Verticillium longisporum

“…Some of these might be connected to niche adaptation. LS regions of V. dahliae could represent a unique chromatin state with regard to transposable elements, methylation marks, and DNA accessibility when compared to the core genome (Cook et al, 2020).…”