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Sensing the environment: lessons from fungi

Key Points

  • G-protein-coupled receptors (GPCRs) function as both pheromone and glucose sensors in fungi, whereas transceptors such as Snf3 and Rgt2 are involved in glucose sensing. Fungi have evolved sophisticated amino-acid-sensing systems including Ssy1–Ptr3–Ssy5 (SPS), Gap1 and GPCRs. The transceptors Pho84 and Pho87 have key roles in phosphate sensing.

  • In eukaryotic organisms, the cyclic AMP–protein kinase A (cAMP–PKA) and TOR pathways transmit nutrient-derived signals to regulate a myriad of common targets that control complex translational and transcriptional programmes to coordinate nutrient availability with cell growth and differentiation.

  • Fungi sense gases, such as CO2 and ammonia, to control various cellular responses. Carbonic anhydrase maintains CO2/HCO3 homeostasis and thereby regulates the cAMP–PKA pathway, which in turn controls growth, differentiation and virulence factors of pathogenic fungi. Ammonia gas is an intercolony signalling mediator that has an important role in the growth and survival of multicellular yeast colonies.

  • Opsins, phytochromes and white collar-1 proteins function in light sensing in fungi, with a conserved role for white collar proteins in blue-light sensing in diverse species. The downstream signalling events after light exposure are yet to be fully illuminated.

  • Fungi use evolutionarily conserved signalling pathways, including the p38/Hog1 mitogen-activated protein kinase (MAPK) pathway and the nutrient sensing Tor and cAMP–PKA pathway, to confer cellular responses against various environmental stresses. However, the development of fungal-specific upstream and downstream systems is also evident, as exemplified by the multi-component phosphorelay system.

  • For successful virulence, pathogenic fungi must counteract a plethora of host-specific factors, such as serum and immune cells in animals, and plant hormones, fatty acids and hard mechanical surface in plants. Signalling pathways that are responsible for the fungus–host interaction include the cAMP–PKA pathway and calcineurin pathway, however many aspects of fungal–host interactions remain to be elucidated.

Abstract

All living organisms use numerous signal-transduction systems to sense and respond to their environments and thereby survive and proliferate in a range of biological niches. Molecular dissection of these signalling networks has increased our understanding of these communication processes and provides a platform for therapeutic intervention when these pathways malfunction in disease states, including infection. Owing to the expanding availability of sequenced genomes, a wealth of genetic and molecular tools and the conservation of signalling networks, members of the fungal kingdom serve as excellent model systems for more complex, multicellular organisms. Here, we review recent progress in our understanding of how fungal-signalling circuits operate at the molecular level to sense and respond to a plethora of environmental cues.

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Figure 1: The involvement of G protein-coupled receptors in sensing extracellular signals in fungi.
Figure 2: Ammonia and CO2 sensing and metabolic pathways.
Figure 3: Blue-UV light sensing through the white collar-1 protein family.
Figure 4: Fungal stress-response mechanisms.

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Acknowledgements

The authors thank F. A. Mühlschlegel for providing pictures of C. albicans filamentation. This work was supported by the Soongsil University Research Fund to Y-S.B. and R01 grants from the NIAID/NIH to J.H. and NCI/NIH to M.E.C.

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DATABASES

Entrez Genome Project

Aspergillus nidulans

Candida albicans

Coprinus cinereus

Cryptococcus neoformans

Hypocrea jecorina

Kluveromyces lactis

Neurospora crassa

Saccharomyces cerevisiae

Schizosaccharomyces pombe

Ustilago maydis

Saccharomyces Genome database 

Gcn2

Gpa1

Gpa2

Gpr1

Hog1

Mep2

Pbs2

Pho84

Pho87

Ptr3

Rgt2

Sit4

Sko1

Sln1

Snf3

Ssk1

Ssk2

Ssk22

Ssy1

Ssy5

Ste2

Ste3

Stp1

Stp2

Tor1

Tor2

Ypd1

Glossary

Mating type

A strain or clone or other isolate made up of organisms (such as certain fungi or protozoans) that are usually incapable of sexual reproduction with one another but capable of such reproduction with members of other strains of the same organism.

Clamp cell

A bridge-like hyphal connection involved in maintaining the dikaryotic state that forms when cells in dikaryotic hyphae divide.

Protein kinase A

(PKA). A secondary messenger-dependent enzyme that has been implicated in a wide range of cellular processes, including transcription, metabolism, cell-cycle progression and apoptosis.

Rhesus proteins

Mammalian homologues of the Amt/Mep family of proteins that are expressed in many tissues and form part of the rhesus (Rh) blood-group complex.

Autophagy

A degradative pathway elicited by nutrient starvation by which indiscriminate portions of the cytoplasm, including organelles, are engulfed into autophagosomal vesicles for fusion with the vacuole and degradation.

Restenosis

The process whereby intimal hyperplasia occurs to re-occlude a coronary artery and limit cardiac blood flow following cardiac stenting. A common complication that is markedly reduced by using stents impregnated with rapamycin.

EGO complex

A vacuolar membrane-associated multiprotein complex that consists of Ego1, Ego3, Gtr1 and Gtr2. Proposed to function in concert with TORC1 to promote microautophagy in response to amino-acid signals.

Microautophagy

The uptake of cytoplasm at the lysosomal or vacuolar surface. It is thought that this process functions to recycle the vacuolar membrane.

Photosensory protein

A protein with absorbance properties that overlap the wavelength spectrum to which the organism responds. Mutation of its encoding gene should disable this sensing ability.

Chromophore

The light-absorbing chemical associated with a photoreceptor protein.

LOV

A domain found in proteins that sense light, oxygen or voltage that physically interacts with a flavin molecule.

Two-component phosphorelay system

First identified in various bacterial systems and subsequently found in lower eukaryotes including fungi. The signalling is achieved by phosphotransfer from a histidine residue in the sensor histidine kinase to an aspartate residue in the response regulator.

Serum

The liquid component of blood that consists of proteins, lipids and many low molecular-weight molecules.

Appressorium

An enlarged fungal filament that is used for penetration through the surface of the host plant.

Stress regulated element

(STRE). A region in the promoter of genes (consensus sequence CCCCT) to which transcription factors bind to mediate stress-induced transcription.

Calcineurin

A serine/threonine-specific protein phosphatase that is activated by calcium–calmodulin.

Indole-3-acetic acid

(IAA). An auxin plant hormone.

Auxin

A class of plant growth substance (often called phytohormones or plant hormones).

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Bahn, YS., Xue, C., Idnurm, A. et al. Sensing the environment: lessons from fungi. Nat Rev Microbiol 5, 57–69 (2007). https://doi.org/10.1038/nrmicro1578

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