The role of vegetative cell fusions in the development and asexual reproduction of the wheat fungal pathogen Zymoseptoria 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 characterized soft (So) gene, and the MAPK pathway components MAK-1 and MAK-2 of Neurospora 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 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 is dependent on the initial cell density. Contrary to other fungi, cell fusion in Z. tritici only resulted in cytoplasmic mixing but not in multinucleated cell formation. The deletion of the So orthologous ZtSof1 disrupted cell-to-cell communication affecting both hyphal and germling fusion. We show that Z. tritici mutants for MAPK-encoding ZtSlt2 (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 ΔZtSof1 mutant 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 pycnidium development, 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 are essential for different aspects of the Z. tritici biology, and the ZtSof1 gene is a potential target to control septoria tritici blotch (STB) disease.

Morphological changes in response to environmental stresses in the fungal plant pathogen Zymoseptoria tritici.

During their life cycles, pathogens have to adapt to many biotic and abiotic environmental stresses to maximize their overall fitness. Morphological transitions are one of the least understood of the many strategies employed by fungal plant pathogens to adapt to constantly changing environments, even though different morphotypes may play important biological roles. Here, we first show that blastospores (the "yeast-like" form of the pathogen typically known only under laboratory conditions) can form from germinated pycnidiospores (asexual spores) on the surface of wheat leaves, suggesting that this morphotype can play an important role in the natural history of Z. tritici. Next, we characterized the morphological responses of this fungus to a series of environmental stresses to understand the effects of changing environments on fungal morphology and adaptation. All tested stresses induced morphological changes, but different responses were found among four strains. We discovered that Z. tritici forms chlamydospores and demonstrated that these structures are better able to survive extreme cold, heat and drought than other cell types. Finally, a transcriptomic analysis showed that morphogenesis and the expression of virulence factors are co-regulated in this pathogen. Our findings illustrate how changing environmental conditions can affect cellular morphology and lead to the formation of new morphotypes, with each morphotype having a potential impact on both pathogen survival and disease epidemiology.