Abstract
BackgroundThe 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.ResultsWe 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.ConclusionsWe 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.
Highlights
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
Cell fusions in Z. tritici allow the bidirectional transfer of cytoplasmic content but do not enable multinucleated cell formation We co-inoculated either blastospores or pycnidiospores of both 1E4 strains expressing cytoplasmic green fluorescent protein (GFP) (1E4GFP) and 1E4mCh fluorescent strains onto water agar (WA—1% agar in water), a hyphal-inducing medium, to investigate the ability of Z. tritici to undergo self-fusions
Conidial anastomosis tube (CAT) formed between blastospores or pycnidiospores germlings happened at high cell density (107 blastospores/mL), starting after 4 h of incubation, but they were frequently observed after 17 h of incubation, resulting in cells co-expressing both fluorescent proteins (Fig. 1b)
Summary
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. The ability to communicate effectively may affect mating, predation, competition, dominance hierarchy, signal modalities, and survival [1,2,3]. This complex mechanism starts when a given organism (the sender) secretes in the environment a self-produced molecular signal (the message) that alters the behavior of another organism (the receiver) [1, 3].
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