A dialogue-like cell communication mechanism is conserved in filamentous ascomycete fungi and mediates interspecies interactions

Abstract

Significance This study reveals that a dialogue-like communication mechanism, which mediates cell–cell fusion in filamentous fungi, is a conserved complex trait. It allows the communication and behavioral coordination of cells of distantly related species and mediates their mutual attraction and subsequent physical contact, although interspecies fusion does not occur. Through the activation of this signaling machinery, one species can reprogram the developmental program of the other fungus. These data promote our understanding of microbial communication, illustrate the mechanism of repurposing of existing building blocks in cellular evolution, revive the hypothesis of vegetative fusion as an avenue of horizontal gene transfer in fungi, and establish the idea of developmental reprogramming as a tool for controlling fungi.

Components of TOR and MAP kinase signaling control chemotropism and pathogenicity in the fungal pathogen Verticillium dahliae

“…Moreover, genomic evidence for horizontal gene transfer from F. oxysporum to V. dahliae has been reported (Chen et al, 2018). We speculate that under particular selective conditions the two species might be able to undergo vegetative fusion or communicate via physical cell contact (Haj Hammadeh et al, 2022), and that their pheromone-sensing systems might mediate such interspecific interactions.…”

Hyphal Fusions Enable Efficient Nutrient Distribution in Colletotrichum graminicola Conidiation and Symptom Development on Maize

“…Based on experiments with a so deletion strain in N. crassa, it was hypothesized that the corresponding protein is crucial for signal secretion [18,20]. As several other studies have indicated, the fusion signal might be conserved amongst fungi and can induce chemotropic interactions in distantly related species such as Botrytis cinerea and N. crassa [25]. The inter-species formation of germling fusion has also been shown to promote genetic variability in several Colletotrichum species [26,27].…”

Synchronization of oscillatory growth prepares fungal hyphae for fusion

“…As the cell-to-cell dialogue appears to be based on a single, chemical communication channel, it is proposed that the two involved cells undergo oscillatory secretion of a signaling compound with a refractory period that prevents self-stimulation and can contribute to overcoming critical threshold concentrations (1). We recently studied the cell-to-cell dialogue during trap formation in the nematode-trapping fungus Arthrobotrys flagrans (Duddingtonia flagrans) (9). A. flagrans is able to switch from a saprotrophic to a predatory lifestyle, and sophisticated signaling regimes between the fungus and its prey, Caenorhabditis elegans, control trap formation, attraction of the prey and attack of the nematode (11)(12)(13)(14).…”

“…In addition, signal oscillations have been described at the hyphal tips during the fusion of hyphal cells (5)(6)(7). These signal oscillations were named cell-to-cell dialogue and are probably based on a conserved diffusible signaling molecule, which remains to be discovered (8)(9)(10). As the cell-to-cell dialogue appears to be based on a single, chemical communication channel, it is proposed that the two involved cells undergo oscillatory secretion of a signaling compound with a refractory period that prevents self-stimulation and can contribute to overcoming critical threshold concentrations (1).…”

“…A. flagrans is able to switch from a saprotrophic to a predatory lifestyle, and sophisticated signaling regimes between the fungus and its prey, Caenorhabditis elegans, control trap formation, attraction of the prey and attack of the nematode (11)(12)(13)(14). One of the hallmark proteins during the cell-to-cell dialogue is the soft protein, SofT, which shows oscillatory recruitment to the plasma membrane of interacting cells (7,9). Although its molecular function remains elusive, SofT is thought to be involved in generating a signal during the cell-to-cell dialogue.…”