The social network: deciphering fungal language

Key Points

  • Fungi interact with one another and respond to environmental cues using a sophisticated series of extracellular signals and cellular responses. Here, we focus on molecules secreted by the largest phylum of fungi, the Ascomycota, and the quest to understand their biological functions.

  • Germination of asexual spores (conidia) is inhibited by auto-inhibitors, which are produced by a wide range of ascomycetes and have varying specificities and structures.

  • Unknown extracellular signals regulate cell fusion events between germinated conidia, which forms the basis of the interconnected hyphal network; coordination of germination results in faster establishment of colonies and networks. During the communication that precedes these fusion events in Neurospora crassa, cells alternate between signal-sending and signal-perceiving states in order to efficiently coordinate growth towards one another without undergoing terminal developmental differentiation.

  • Communication signals within an individual (or cellular network) are used to regulate growth and development. During starvation in Saccharomyces cerevisiae, connecting fibrils develop between cells, and these fibrils are proposed to have roles in cell–cell communication.

  • Asexual development is regulated by both environmental conditions and developmental age, and has been extensively studied in Aspergillus nidulans. Common regulatory pathways regulate asexual development and mycotoxin production in Aspergillus spp.

  • Many ascomycetes secrete compounds that inhibit the growth of other organisms, including fungi, in their immediate environment. These compounds can cause cell cycle arrest, membrane damage and cell wall stress, or can block asexual reproduction.

  • Mycoparasites, which are fungi that parasitize other fungi, use extracellular sensing to guide them towards their prey. In Trichoderma spp., mutations in a G protein subunit that is involved in signal transduction affect the balance between asexual reproduction and mycoparasitism.

Abstract

It has been estimated that up to one quarter of the world's biomass is of fungal origin, comprising approximately 1.5 million species. In order to interact with one another and respond to environmental cues, fungi communicate with their own chemical languages using a sophisticated series of extracellular signals and cellular responses. A new appreciation for the linkage between these chemical languages and developmental processes in fungi has renewed interest in these signalling molecules, which can now be studied using post-genomic resources. In this Review, we focus on the molecules that are secreted by the largest phylum of fungi, the Ascomycota, and the quest to understand their biological function.

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Figure 1: Extracellular signalling during the life cycle of Neurospora crassa.
Figure 2: Cell–cell communication during germling fusion in Neurospora crassa.
Figure 3: Antagonistic interactions between ascomycetes.
Figure 4: Asexual development in model filamentous ascomycete species.

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Acknowledgements

A.C.L. and J.P.-G. are supported by a research grant from the US National Science Foundation, which was awarded to N.L.G. for studies on germling and hyphal anastomosis. We thank M. North for helpful comments on the manuscript and colleagues for their contributions to the work described.

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Glossary

Hyphae

Multicellular filaments that grow by tip extension.

Mycelium

A fungal colony made up of interconnected hyphae.

Conidiophores

Specialized structures that produce asexual spores (conidia).

Germlings

Aexual spores that have recently germinated.

Chemotropism

Growth of a cell towards a concentration gradient of a chemical stimulus.

Optical tweezers

A microscope equipped with a highly focused laser beam that provides attractive or repulsive forces, which allows for the manipulation of objects such as cells.

Non-autonomous trait

The phenomenon of a genetic mutation in one cell affecting the phenotype of other cells, regardless of their genotype

Orthologue

One of two or more functionally equivalent genes that are derived from a common ancestor.

Basal fungi

Four diverse fungal groups (arbuscular mycorrhizal fungi, microsporidia, chytrids and zygomycetes) that form the base of the fungal phylogenetic tree.

Oomycota

A phylogenetically distinct lineage of fungus-like eukaryotes.

Negative autotropism

A mode of behaviour in which cells actively grow away from one another.

Quorum sensing

Extracellular signalling that coordinates cellular behaviour according to population density.

Pseudohyphae

Chains of elongated cells that arise by budding.

G proteins

Guanine-nucleotide-binding proteins that coordinate extracellular-signal transmission and/or reception responses within a cell.

Metabolome

The complete set of cellular metabolites (including hormones, small-molecule signals and metabolite intermediates).

Antibiosis

Antagonistic interactions between two or more individuals that occur at a distance through the production of extracellular molecules.

Mycoparasitism

A situation in which one fungus parasitizes (that is, benefits at the expense of) a prey fungus.

Deletion collections

Collections of strains containing individuals that are derived from a common parent. Within the collection, each strain contains a single deletion of a predicted gene.

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Leeder, A., Palma-Guerrero, J. & Glass, N. The social network: deciphering fungal language. Nat Rev Microbiol 9, 440–451 (2011). https://doi.org/10.1038/nrmicro2580

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