Transcriptomics reveals the regulation of the immune system of the mushroom-forming fungus Schizophyllum commune during interaction with four competitors

Erik P.W. Beijen; Marieke H. van Maanen; Ioana M. Marian; Janieke X. Klusener; Emmeline van Roosmalen; Koen C. Herman; Margot C. Koster; Robin A. Ohm

doi:10.1016/j.micres.2024.127929

Transcriptomics reveals the regulation of the immune system of the mushroom-forming fungus Schizophyllum commune during interaction with four competitors

Erik P.W. Beijen, Marieke H. van Maanen, Ioana M. Marian, Janieke X. Klusener, Emmeline van Roosmalen, Koen C. Herman, Margot C. Koster, Robin A. Ohm^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › Academic › peer-review

Abstract

Mushroom-forming fungi frequently encounter competitors during their lifecycle, but their defense mechanisms remain largely unexplored. We studied the response of the mushroom-forming fungus Schizophyllum commune during interaction with the fungal competitors Trichoderma harzianum, Trichoderma aggressivum and Purpureocillium lilacinum and the bacterial competitor Serratia quinivorans. Transcriptomics revealed 632 up-regulated genes in the direct interaction zone, which were enriched in small secreted proteins and transporters. A set of 26 genes were up-regulated during all interactions, indicating a core transcriptomic defense response. In the non-interacting edge of the mycelium of S. commune, there were 154 up-regulated genes, suggesting that there is a systemic response due to a signal that reaches unaffected areas. The GATA zinc finger transcription factor gene gat1 was up-regulated during interaction and a Δgat1 strain displayed increased colonization by T. harzianum. Previously linked to mushroom development, this transcription factor apparently has a dual role. Moreover, 138 genes were up-regulated during both interaction and mushroom development, indicating priming of the defense response during development to prepare the fruiting body for future interactions. Overall, we unveiled a defensive response of S. commune during interaction with fungal and bacterial competitors and identified a regulator of this response.

Original language	English
Article number	127929
Number of pages	13
Journal	Microbiological Research
Volume	289
DOIs	https://doi.org/10.1016/j.micres.2024.127929
Publication status	Published - Dec 2024

Bibliographical note

Publisher Copyright:
© 2024 The Authors

Funding

This publication is part of project number VI.Vidi.192.065 of the VIDI research programme which is (partly) financed by the Dutch Research Council (NWO). This project has received funding from the European Research Council (ERC) under the European Union's Horizon 2020 research and innovation programme (grant agreement number 716132). We acknowledge the Utrecht Sequencing Facility (USEQ) for providing sequencing service and data. USEQ is subsidized by the University Medical Center Utrecht and The Netherlands X-omics Initiative (NWO project 184.034.019).

Funders	Funder number
Nederlandse Organisatie voor Wetenschappelijk Onderzoek
European Research Council
Horizon 2020	716132
Horizon 2020
University Medical Center Utrecht	184.034.019

Keywords

Fungal defense
Microbial interactions
Transcriptional regulators
Transcriptomics

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1-s2.0-S0944501324003306-mainFinal published version, 9 MBLicence: CC BY

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Beijen, E. P. W., van Maanen, M. H., Marian, I. M., Klusener, J. X., van Roosmalen, E., Herman, K. C., Koster, M. C., & Ohm, R. A. (2024). Transcriptomics reveals the regulation of the immune system of the mushroom-forming fungus Schizophyllum commune during interaction with four competitors. Microbiological Research, 289, Article 127929. https://doi.org/10.1016/j.micres.2024.127929

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abstract = "Mushroom-forming fungi frequently encounter competitors during their lifecycle, but their defense mechanisms remain largely unexplored. We studied the response of the mushroom-forming fungus Schizophyllum commune during interaction with the fungal competitors Trichoderma harzianum, Trichoderma aggressivum and Purpureocillium lilacinum and the bacterial competitor Serratia quinivorans. Transcriptomics revealed 632 up-regulated genes in the direct interaction zone, which were enriched in small secreted proteins and transporters. A set of 26 genes were up-regulated during all interactions, indicating a core transcriptomic defense response. In the non-interacting edge of the mycelium of S. commune, there were 154 up-regulated genes, suggesting that there is a systemic response due to a signal that reaches unaffected areas. The GATA zinc finger transcription factor gene gat1 was up-regulated during interaction and a Δgat1 strain displayed increased colonization by T. harzianum. Previously linked to mushroom development, this transcription factor apparently has a dual role. Moreover, 138 genes were up-regulated during both interaction and mushroom development, indicating priming of the defense response during development to prepare the fruiting body for future interactions. Overall, we unveiled a defensive response of S. commune during interaction with fungal and bacterial competitors and identified a regulator of this response.",

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doi = "10.1016/j.micres.2024.127929",

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AU - Beijen, Erik P.W.

AU - van Maanen, Marieke H.

AU - Marian, Ioana M.

AU - Klusener, Janieke X.

AU - van Roosmalen, Emmeline

AU - Herman, Koen C.

AU - Koster, Margot C.

AU - Ohm, Robin A.

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Transcriptomics reveals the regulation of the immune system of the mushroom-forming fungus Schizophyllum commune during interaction with four competitors

Abstract

Bibliographical note

Funding

Keywords

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