Abstract
BackgroundAntagonistic co-evolution can drive rapid adaptation in pathogens and shape genome architecture. Comparative genome analyses of several fungal pathogens revealed highly variable genomes, for many species characterized by specific repeat-rich genome compartments with exceptionally high sequence variability. Dynamic genome structure may enable fast adaptation to host genetics. The wheat pathogen Zymoseptoria tritici with its highly variable genome, has emerged as a model organism to study genome evolution of plant pathogens. Here, we compared genomes of Z. tritici isolates and of sister species infecting wild grasses to address the evolution of genome composition and structure.ResultsUsing long-read technology, we sequenced and assembled genomes of Z. ardabiliae, Z. brevis, Z. pseudotritici and Z. passerinii, together with two isolates of Z. tritici. We report a high extent of genome collinearity among Zymoseptoria species and high conservation of genomic, transcriptomic and epigenomic signatures of compartmentalization. We identify high gene content variability both within and between species. In addition, such variability is mainly limited to the accessory chromosomes and accessory compartments. Despite strong host specificity and non-overlapping host-range between species, predicted effectors are mainly shared among Zymoseptoria species, yet exhibiting a high level of presence-absence polymorphism within Z. tritici. Using in planta transcriptomic data from Z. tritici, we suggest different roles for the shared orthologs and for the accessory genes during infection of their hosts.ConclusionDespite previous reports of high genomic plasticity in Z. tritici, we describe here a high level of conservation in genomic, epigenomic and transcriptomic composition and structure across the genus Zymoseptoria. The compartmentalized genome allows the maintenance of a functional core genome co-occurring with a highly variable accessory genome.
Highlights
Antagonistic co-evolution can drive rapid adaptation in pathogens and shape genome architecture
We sequenced and assembled the genome of the reference isolates of Z. ardabiliae, Z. brevis, Z. pseudotritici and Z. passerinii and the genomes of two Z. tritici isolates sampled in Denmark and Iran [30]
The resulting assembly lengths ranged from 38.1 Mb for Z. ardabiliae to 41.6 Mb for Z. brevis, which is comparable to the reference assembly length of Z. tritici (39.7 Mb) but larger than previous short-read based assemblies
Summary
Antagonistic co-evolution can drive rapid adaptation in pathogens and shape genome architecture. Rapid evolution may be fueled by highly dynamic genome architecture involving repeat-rich compartments such as gene-sparse islands of repetitive DNA and accessory chromosomes [2, 3]. These compartments can show a high plasticity revealed by a high extent of gene and/or chromosome presence-absence variation and structural variants, such as inversions, insertions and deletions [4, 5]. Virulence determinants may be exchanged between clonal lineages as accessory chromosomes in this species were shown to encode host specific virulence determinants and transcription factors regulating their expression [12]
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