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

A - Papers appearing in refereed journals

Francisco, C.S., Zwyssig, M.M. and Palma-Guerrero, J. 2020. The role of vegetative cell fusions in the development and asexual reproduction of the wheat fungal pathogen Zymoseptoria tritici. BMC Biology. 18 (article 99). https://doi.org/10.1186/s12915-020-00838-9

AuthorsFrancisco, C.S., Zwyssig, M.M. and Palma-Guerrero, J.
Abstract

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.

KeywordsCell-to-cell communication; Anastomosis; Vegetative growth; Melanization; Asexual reproduction
Year of Publication2020
JournalBMC Biology
Journal citation18 (article 99)
Digital Object Identifier (DOI)https://doi.org/10.1186/s12915-020-00838-9
Web address (URL)https://bmcbiol.biomedcentral.com/articles/10.1186/s12915-020-00838-9#citeas
Open accessPublished as ‘gold’ (paid) open access
FunderCoordination of Superior Level Staff Improvement (CAPES)
Publisher's version
Output statusPublished
Publication dates
Online11 Aug 2020
Publication process dates
Accepted27 Jul 2020
PublisherBiomed Central Ltd
ISSN1741-7007

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