Genome compartmentalization predates species divergence in the plant pathogen genusZymoseptoria

Background Antagonistic 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 pathogenZymoseptoria triticiwith its highly variable genome, has emerged as a model organism to study genome evolution of plant pathogens. Here, we compared genomes ofZ. triticiisolates and of sister species infecting wild grasses to address the evolution of genome composition and structure. Results Using long-read technology, we sequenced and assembled genomes ofZ. ardabiliae,Z. brevis,Z. pseudotriticiandZ. passerinii, together with two isolates ofZ. tritici. We report a high extent of genome collinearity amongZymoseptoriaspecies 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 amongZymoseptoriaspecies, yet exhibiting a high level of presence-absence polymorphism withinZ. tritici. Usingin plantatranscriptomic data fromZ. tritici, we suggest different roles for the shared orthologs and for the accessory genes during infection of their hosts. Conclusion Despite previous reports of high genomic plasticity inZ. tritici, we describe here a high level of conservation in genomic, epigenomic and transcriptomic composition and structure across the genusZymoseptoria. The compartmentalized genome allows the maintenance of a functional core genome co-occurring with a highly variable accessory genome.