Synchronization of oscillatory growth prepares fungal hyphae for fusion
- Karlsruhe Institute of Technology, Germany
Abstract
Communication is crucial for organismic interactions, from bacteria, to fungi, to humans. Humans may use the visual sense to monitor the environment before starting acoustic interactions. In comparison, fungi, lacking a visual system, rely on a cell-to-cell dialogue based on secreted signaling molecules to coordinate cell fusion and establish hyphal networks. Within this dialogue, hyphae alternate between sending and receiving signals. This pattern can be visualized via the putative signaling protein Soft (SofT), and the mitogen-activated protein kinase MAK-2 (MakB) which are recruited in an alternating oscillatory manner to the respective cytoplasmic membrane or nuclei of interacting hyphae. Here, we show that signal oscillations already occur in single hyphae of Arthrobotrys flagrans in the absence of potential fusion partners (cell monologue). They were in the same phase as growth oscillations. In contrast to the anti-phasic oscillations observed during the cell dialogue, SofT and MakB displayed synchronized oscillations in phase during the monologue. Once two fusion partners came into each other's vicinity, their oscillation frequencies slowed down (entrainment phase) and transit into anti-phasic synchronization of the two cells'; oscillations with frequencies of 104 +/- 28 sec and 117 +/- 19 sec, respectively. Single-cell oscillations, transient entrainment, and anti-phasic oscillations were reproduced by a mathematical model where nearby hyphae can absorb and secrete a limited molecular signaling component into a shared extra-cellular space. We show that intracellular Ca2+ concentrations oscillate in two approaching hyphae, and depletion of Ca2+ from the medium affected vesicle-driven extension of the hyphal tip, abolished the cell monologue and the anti-phasic synchronization of two hyphae. Our results suggest that single hyphae engage in a 'monologue' that may be used for exploration of the environment and can dynamically shift their extra-cellular signaling systems into a 'dialogue' to initiate hyphal fusion.
Data availability
All raw images and data files resulting from the analyses are available at Zenodo (https://zenodo.org/record/6830734#.Ys_KmS2w1TY).The simulation script is also available at [https://github.com/vkumpost/cell-dialog].
Article and author information
Author details
Funding
Deutsche Forschungsgemeinschaft (Fi 459/26-1)
- Reinhard Fischer
Deutsche Bundesstiftung Umwelt (2018/552)
- Valentin Wernet
Helmholtz Association (HIDSS4Health)
- Vojtech Kumpost
- Ralf Mikut
- Lennart Hilbert
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Antonis Rokas, Vanderbilt University, United States
Version history
- Received: September 7, 2022
- Preprint posted: September 26, 2022 (view preprint)
- Accepted: August 19, 2023
- Accepted Manuscript published: August 21, 2023 (version 1)
- Version of Record published: September 26, 2023 (version 2)
Copyright
© 2023, Wernet et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Synchronization of oscillatory growth prepares fungal hyphae for fusion
eLife 12:e83310.
https://doi.org/10.7554/eLife.83310
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