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.
Highlights
Genomes are not randomly organized and comprise complex information beyond their linear nucleic acid sequence (Sexton and Cavalli, 2015)
We present a detailed analysis of the epigenome and physical DNA accessibility of the vascular wilt pathogen V. dahliae and link these analyses to previous characterizations of genomic regions contributing to host colonization and adaptation (Klosterman et al, 2011; de Jonge et al, 2013; Faino et al, 2016; Shi-Kunne et al, 2018)
The heterochromatin is characterized by a high density of transposable elements (TEs) with low GC content, high levels of DNA and H3K9 methylation, low DNA accessibility and clear signatures of repeat-induced point mutation (RIP) mutations at repetitive sequences
Summary
Genomes are not randomly organized and comprise complex information beyond their linear nucleic acid sequence (Sexton and Cavalli, 2015). There is a great need to decode the complex information stored in these genomes, to understand genomic responses over various time scales, and to more fully understand how genotypes lead to phenotypes. Present day genome organization reflects evolutionary solutions to the challenges of information processing and adaptation; a genome must faithfully pass vast amounts of information across cell cycles and reproduction, packaged into limited physical space, while achieving correct access to the information in response to developmental, environmental, or chemical signals. Organisms undergoing mainly asexual reproduction face an additional evolutionary constraint as they must generate this genetic variation in the absence of meiotic recombination (Seidl and Thomma, 2014). Fungal pathogens are subject to additional evolutionary pressure from their
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