The role of vegetative cell fusions in the development and asexual reproduction of the wheat fungal pathogenZymoseptoria tritici

Background The ability of fungal cells to undergo cell-to-cell communication and anastomosis, the process of vegetative hyphal fusion, allows them to maximize their overall fitness. Previous studies in a number of fungal species have identified the requirement of several signaling pathways for anastomosis, including the so far best characterizedsoft(So) gene, and the MAPK pathway components MAK-1 and MAK-2 ofNeurospora crassa. Despite the observations of hyphal fusions' involvement in pathogenicity and host adhesion, the connection between cell fusion and fungal lifestyles is still unclear. Here, we address the role of anastomosis in fungal development and asexual reproduction inZymoseptoria tritici, the most important fungal pathogen of wheat in Europe. Results We show thatZ. triticiundergoes self-fusion between distinct cellular structures, and its mechanism is dependent on the initial cell density. Contrary to other fungi, cell fusion inZ. triticionly resulted in cytoplasmic mixing but not in multinucleated cell formation. The deletion of theSoorthologousZtSof1disrupted cell-to-cell communication affecting both hyphal and germling fusion. We show thatZ. triticimutants for MAPK-encodingZtSlt2(orthologous toMAK-1) andZtFus3(orthologous toMAK-2) genes also failed to undergo anastomosis, demonstrating the functional conservation of this signaling mechanism across species. Additionally, the Delta ZtSof1mutant was severely impaired in melanization, suggesting that theSogene function is related to melanization. Finally, we demonstrated that anastomosis is dispensable for pathogenicity, but essential for the pycnidium development, and its absence abolishes the asexual reproduction ofZ. tritici. Conclusions We demonstrate the role forZtSof1,ZtSlt2, andZtFus3in cell fusions ofZ. tritici. Cell fusions are essential for different aspects of theZ. triticibiology, and theZtSof1gene is a potential target to control septoria tritici blotch (STB) disease.