Interspecies hybridization as a route of accessory chromosome origin in fungal pathogens

Fungal plant pathogens have dynamic genomic architectures that can contribute to rapid evolution and adaptation to new niches. <i>Zymoseptoria tritici</i>, an important fungal pathogen of wheat, has a compartmentalized and rapidly evolving genome. In the genome of the reference isolate <i>Z. tritici</i> IPO323, 8 of the 21 chromosomes are accessory. In spite of the profound impact on genome organization, the origin of accessory chromosomes in <i>Z. tritici</i> is still poorly understood. By combining a multi-omics approach, we discovered an additional chromosome in <i>Z. tritici</i> isolates infecting wild grasses from the genus <i>Aegilops</i>, and we use this discovery to study the origin of accessory chromosomes. The newly identified chromosome presents characteristics similar to known accessory chromosomes in <i>Zymoseptoria</i> species, including presence-absence variation and enrichment with heterochromatin-associated histone methylation marks (H3K27me3). Interestingly, we found an orthologous chromosome in <i>Zymoseptoria ardabiliae</i>, a closely related fungal species also infecting wild grasses. This orthologous chromosome also presents accessory chromosome characteristics but lacks the enrichment of heterochromatin-associated methylation marks. Transcriptomic analyses revealed that the orthologous chromosome in <i>Z. ardabiliae</i> harbors active transposable elements (TEs) congruent with lower signatures of host-genome defense mechanisms against TE expansion and spread (quantified as repeat-induced-point mutation signatures). Our findings suggest that the chromosome has been exchanged between <i>Z. tritici</i> and <i>Z. ardabiliae</i> by introgressive hybridization events, underlining the relevance of hybridization in the evolution of new accessory chromosomes. We speculate that the regulation of TEs has not yet occurred on this new accessory chromosome in <i>Z. ardabiliae</i>, contributing to its rapid evolution.IMPORTANCESome species of fungi have accessory chromosomes that show presence-absence variation among individuals in a population. In some species, accessory chromosomes can encode important genes, whereas in others, they have been described as selfish elements. The evolutionary origin of accessory chromosomes is still poorly understood. Here, we characterize a new accessory chromosome in a plant-pathogenic fungus. We demonstrate that this chromosome was recently acquired through interspecific hybridization. Using population genomic data, we also characterize the mechanisms by which accessory chromosomes diverge rapidly. Our study demonstrates how the evolution of accessory chromosomes can be shaped by the interplay between transposable element activity and genome defense mechanisms and illustrates a possible route of chromosome emergence in fungal species.