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

摘要

Background: The ability of fungal cells to undergo cell-to-cell communication and anastomosis, the process ofvegetative hyphal fusion, allows them to maximize their overall fitness. Previous studies in a number of fungalspecies have identified the requirement of several signaling pathways for anastomosis, including the so far bestcharacterized soft (So) gene, and the MAPK pathway components MAK-1 and MAK-2 of Neurospora crassa. Despitethe observations of hyphal fusions’ involvement in pathogenicity and host adhesion, the connection between cellfusion and fungal lifestyles is still unclear. Here, we address the role of anastomosis in fungal development andasexual reproduction in Zymoseptoria tritici, the most important fungal pathogen of wheat in Europe.Results: We show that Z. tritici undergoes self-fusion between distinct cellular structures, and its mechanism isdependent on the initial cell density. Contrary to other fungi, cell fusion in Z. tritici only resulted in cytoplasmicmixing but not in multinucleated cell formation. The deletion of the So orthologous ZtSof1 disrupted cell-to-cellcommunication affecting both hyphal and germling fusion. We show that Z. tritici mutants for MAPK-encodingZtSlt2 (orthologous to MAK-1) and ZtFus3 (orthologous to MAK-2) genes also failed to undergo anastomosis,demonstrating the functional conservation of this signaling mechanism across species. Additionally, the ΔZtSof1mutant was severely impaired in melanization, suggesting that the So gene function is related to melanization.Finally, we demonstrated that anastomosis is dispensable for pathogenicity, but essential for the pycnidiumdevelopment, and its absence abolishes the asexual reproduction of Z. tritici.Conclusions: We demonstrate the role for ZtSof1, ZtSlt2, and ZtFus3 in cell fusions of Z. tritici. Cell fusions areessential for different aspects of the Z. tritici biology, and the ZtSof1 gene is a potential target to control septoriatritici blotch (STB) disease.