Rapid mitochondrial genome structure evolution in Zymoseptoria tritici and beyond
Mitochondria play crucial roles in eukaryotic cells, serving as hubs for ATP production and encoding their own genomes. Fungal mitogenomes exhibit high diversity in both size and composition, yet this diversity has primarily been characterized at the genus or higher levels. In our study, we focused on analyzing mitogenome variation generated over short evolutionary time within species, by examining thousands of strains of the major wheat pathogen Zymoseptoria tritici. We uncovered incongruences between mitochondrial and nuclear population structures, as mitogenome genetic clusters did not correspond to nuclear genetic clusters. To reveal structural variation underpinning mitogenome diversity, we assembled ~2000 mitochondrial genomes based on long-reading and short-read sequencing. We found four primary haplotypes distinguished mainly by two large (up to ~10% of the entire mitogenome) insertion/deletions. Notably, a small subset of genomes shared an additional sequence encoding a selfish genetic element identified as a GIY-YIG homing endonuclease (HE). Comparative analyses of mitogenomes from closely related Zymoseptoria species revealed substantial variability at the genus level and revealed the closest orthologs of the HE gene. This suggests that a deletion affecting the GIY-YIG HE occurred early in the evolution of Z. tritici. Our findings shed light on the extensive variability of mitochondrial genomes over short evolutionary time spans.