Cargando…

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 anas...

Descripción completa

Detalles Bibliográficos
Autores principales: Francisco, Carolina Sardinha, Zwyssig, Maria Manuela, Palma-Guerrero, Javier
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7477884/
https://www.ncbi.nlm.nih.gov/pubmed/32782023
http://dx.doi.org/10.1186/s12915-020-00838-9
_version_ 1783579972899700736
author Francisco, Carolina Sardinha
Zwyssig, Maria Manuela
Palma-Guerrero, Javier
author_facet Francisco, Carolina Sardinha
Zwyssig, Maria Manuela
Palma-Guerrero, Javier
author_sort Francisco, Carolina Sardinha
collection PubMed
description 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.
format Online
Article
Text
id pubmed-7477884
institution National Center for Biotechnology Information
language English
publishDate 2020
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-74778842020-09-09 The role of vegetative cell fusions in the development and asexual reproduction of the wheat fungal pathogen Zymoseptoria tritici Francisco, Carolina Sardinha Zwyssig, Maria Manuela Palma-Guerrero, Javier BMC Biol Research Article 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. BioMed Central 2020-08-11 /pmc/articles/PMC7477884/ /pubmed/32782023 http://dx.doi.org/10.1186/s12915-020-00838-9 Text en © The Author(s). 2020 Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Francisco, Carolina Sardinha
Zwyssig, Maria Manuela
Palma-Guerrero, Javier
The role of vegetative cell fusions in the development and asexual reproduction of the wheat fungal pathogen Zymoseptoria tritici
title The role of vegetative cell fusions in the development and asexual reproduction of the wheat fungal pathogen Zymoseptoria tritici
title_full The role of vegetative cell fusions in the development and asexual reproduction of the wheat fungal pathogen Zymoseptoria tritici
title_fullStr The role of vegetative cell fusions in the development and asexual reproduction of the wheat fungal pathogen Zymoseptoria tritici
title_full_unstemmed The role of vegetative cell fusions in the development and asexual reproduction of the wheat fungal pathogen Zymoseptoria tritici
title_short The role of vegetative cell fusions in the development and asexual reproduction of the wheat fungal pathogen Zymoseptoria tritici
title_sort role of vegetative cell fusions in the development and asexual reproduction of the wheat fungal pathogen zymoseptoria tritici
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7477884/
https://www.ncbi.nlm.nih.gov/pubmed/32782023
http://dx.doi.org/10.1186/s12915-020-00838-9
work_keys_str_mv AT franciscocarolinasardinha theroleofvegetativecellfusionsinthedevelopmentandasexualreproductionofthewheatfungalpathogenzymoseptoriatritici
AT zwyssigmariamanuela theroleofvegetativecellfusionsinthedevelopmentandasexualreproductionofthewheatfungalpathogenzymoseptoriatritici
AT palmaguerrerojavier theroleofvegetativecellfusionsinthedevelopmentandasexualreproductionofthewheatfungalpathogenzymoseptoriatritici
AT franciscocarolinasardinha roleofvegetativecellfusionsinthedevelopmentandasexualreproductionofthewheatfungalpathogenzymoseptoriatritici
AT zwyssigmariamanuela roleofvegetativecellfusionsinthedevelopmentandasexualreproductionofthewheatfungalpathogenzymoseptoriatritici
AT palmaguerrerojavier roleofvegetativecellfusionsinthedevelopmentandasexualreproductionofthewheatfungalpathogenzymoseptoriatritici