The STRIPAK component SipC is involved in morphology and cell-fate determination in the nematode-trapping fungus <i>Duddingtonia flagrans</i>

Wernet, Valentin; Wäckerle, Jan; Fischer, Reinhard

doi:10.1093/genetics/iyab153

Cited by 17 publications

(13 citation statements)

References 55 publications

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“…Recent studies have shown that the highly conserved Slt2 MAPK of the cell wall integrity pathway ( Zhen et al 2018 ) and the Fus3 MAPK of the pheromone response pathway ( Chen et al 2021 ) both play vital roles in A. oligospora trap differentiation, with Fus3 signaling being essential to induce trap morphogenesis. Moreover, lack of the SipC component of the STRIPAK (striatin-interacting phosphatases and kinases) complex in another species of NTF ( Duddingtonia flagrans ) that forms 3-dimensional traps results in incomplete loop formation and column-like trap structures ( Wernet et al 2022 ). A recent report linked intracellular cAMP signaling to prey sensing in A. oligospora , which demonstrated that deletion mutants of 2 cAMP phosphodiesterases, PdeH and Pdel, resulted in increased cAMP levels during vegetative growth and trap morphogenesis.…”

Section: Discussionmentioning

confidence: 99%

The cAMP-PKA pathway regulates prey sensing and trap morphogenesis in the nematode-trapping fungus Arthrobotrys oligospora

Chen

Lin

Hsueh

2022

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Sensing environmental factors and responding swiftly to them is essential for all living organisms. For instance, predators must act rapidly once prey is sensed. Nematode-trapping fungi (NTF) are predators that use “traps” differentiated from vegetative hyphae to capture, kill, and consume nematodes. These traps undergo drastic and rapid morphological changes upon nematode induction. Multiple signaling hubs have been shown to regulate this remarkable process. Here, we demonstrate that the conserved cAMP-PKA signaling pathway exerts a crucial role in trap morphogenesis of the NTF Arthrobotrys oligospora. A gene deletion mutant of the PKA catalytic subunit TPK2 proved insensitive towards nematode presence. Moreover, we show that the G protein alpha subunit GPA2 acts upstream of adenylate cyclase, with GPA2 deletion resulting in substantially reduced trap formation, whereas exogenous provision of cAMP rescued the prey-sensing and trap morphogenesis defects of a gpa2 mutant. Thus, we show that cAMP production triggered by G protein signaling and downstream PKA activity are vital for prey-sensing and trap development in A. oligospora, demonstrating that this highly conserved signaling pathway is critical for NTF and nematode predator-prey interactions.

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Section: Discussionmentioning

confidence: 99%

The cAMP-PKA pathway regulates prey sensing and trap morphogenesis in the nematode-trapping fungus Arthrobotrys oligospora

Chen

Lin

Hsueh

2022

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“…Of particular interest to nematode-trapping (NT) fungi are the special trapping devices (traps) involved in capturing and killing nematodes ( 13 – 16 ). The traps are specifically formed by the vegetative hyphae of NT fungi, divided into adhesive knobs and columns, adhesive networks, and constricting and nonconstricting rings according to their different predatory methods ( 17 – 19 ). Arthrobotrys oligospora is one of the best-known species of NT fungi, which can develop adhesive networks for nematode predation, and its whole genome has previously been sequenced ( 20 ).…”

Section: Introductionmentioning

confidence: 99%

AMPK Is Involved in Regulating the Utilization of Carbon Sources, Conidiation, Pathogenicity, and Stress Response of the Nematode-Trapping Fungus Arthrobotrys oligospora

et al. 2022

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NT fungi are widely distributed in various ecosystems and are important factors in the control of nematode populations in nature; their trophic mycelia can form unique infectious devices (traps) for capturing nematodes. Arthrobotrys oligospora is a representative NT fungi which can develop complex three-dimensional networks (adhesive networks) for nematode predation. Here, we demonstrated that AMPK plays an important role in the glycerol utilization, conidiation, trap formation, and nematode predation of A. oligospora , which was further confirmed by transcriptomic analysis of the wild-type and mutant strains.

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“…One kb flanks homologous to the 5’ and 3’ regions of the gene of interest were amplified by PCR with 25 bp overhangs homologous to either the hygromycin-B ( hph ) or geneticin sulfate (G418, neo ) resistance cassette as well as to the pJET1.2 plasmid backbone. Verification of homologous recombination was performed as described in Wernet et al, 2022 .…”

Section: Methodsmentioning

confidence: 99%

Synchronization of oscillatory growth prepares fungal hyphae for fusion

Wernet,

Kriegler,

Kumpost

et al. 2023

eLife

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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.

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The STRIPAK component SipC is involved in morphology and cell-fate determination in the nematode-trapping fungus Duddingtonia flagrans

Cited by 17 publications

References 55 publications

The cAMP-PKA pathway regulates prey sensing and trap morphogenesis in the nematode-trapping fungus Arthrobotrys oligospora

The cAMP-PKA pathway regulates prey sensing and trap morphogenesis in the nematode-trapping fungus Arthrobotrys oligospora

AMPK Is Involved in Regulating the Utilization of Carbon Sources, Conidiation, Pathogenicity, and Stress Response of the Nematode-Trapping Fungus Arthrobotrys oligospora

Synchronization of oscillatory growth prepares fungal hyphae for fusion

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