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Actin organization and dynamics in filamentous fungi

Nature Reviews Microbiology volume 9, pages 876–887 (2011)Cite this article

Subjects

Key Points

  • The dynamic reorganization and polarization of the actin cytoskeleton underpins the growth and morphogenesis of filamentous fungi.

  • Actin has crucial roles in exocytosis, endocytosis, organelle movement and cytokinesis in fungi. These processes are coupled to the production of distinct higher-order structures (actin patches, cables and rings) that generate forces or serve as tracks for intracellular transport.

  • New approaches for imaging filamentous actin (F-actin) in living cells using the reporter Lifeact (an actin-binding peptide fused to GFP) have recently been developed for filamentous fungi. Live-cell imaging of F-actin, together with mutational studies, has yielded key insights into cell polarity, tip growth and long-distance transport.

  • F-actin organization and dynamics in filamentous fungi possess some features that have not been observed in Saccharomyces cerevisiae. For example, some actin patches exhibit bidirectional movement, actin cables can be long (5–20 μm), the polarized organization of actin in hyphal tips undergoes a radical change in organization during the transition from a germ tube to a mature vegetative hypha, and complex actin arrays show retrograde movement in germ tubes.

  • The concentration of F-actin in the core of the vesicle supply centre (the Spitzenkörper) within the tips of growing vegetative hyphae may represent a fourth type of higher-order structure, found in filamentous fungi but absent from S. cerevisiae. The precise roles of the Spitzenkörper remain to be elucidated.

Abstract

Growth and morphogenesis of filamentous fungi is underpinned by dynamic reorganization and polarization of the actin cytoskeleton. Actin has crucial roles in exocytosis, endocytosis, organelle movement and cytokinesis in fungi, and these processes are coupled to the production of distinct higher-order structures (actin patches, cables and rings) that generate forces or serve as tracks for intracellular transport. New approaches for imaging actin in living cells are revealing important similarities and differences in actin architecture and organization within the fungal kingdom, and have yielded key insights into cell polarity, tip growth and long-distance intracellular transport. In this Review, we discuss the contribution that recent live-cell imaging and mutational studies have made to our understanding of the dynamics and regulation of actin in filamentous fungi.

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Figure 1: Properties of actin and higher-order actin structures in filamentous fungi.
Figure 2: Model of actin-related protein 2/3 complex-mediated actin nucleation and actin patch transport in filamentous fungi.
Figure 3: Actin cable assembly and dynamics.
Figure 4: Rearrangement of the tip growth apparatus.
Figure 5: Model of contractile actomyosin ring assembly in Neurospora crassa.

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Acknowledgements

This work was supported by funding from the UK Biotechnological and Biological Sciences Research Council (BBSRC) (grant BB/E010741/1) to N.D.R., a Ph.D. Studentship from The University of Edinburgh to A.L. and a BBSRC Studentship to A.B. The authors also thank the Mexican National Council for Science and Technology (CONACyT) for a postdoctoral fellowship to A.L.

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  1. Fungal Cell Biology Group, Institute of Cell Biology, Rutherford Building, University of Edinburgh, Edinburgh, EH9 3JH, UK

    Adokiye Berepiki, Alexander Lichius & Nick D. Read

  2. Department of Microbiology, Center for Scientific Research and Higher Education of Ensenada (CICESE), Ensenada, 22860, Baja California, Mexico

    Alexander Lichius

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  1. Adokiye Berepiki
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Glossary

Microtubules

Tubular cytoskeletal polymers composed of tubulin dimers. They provide tracks for intracellular transport based on motor proteins (kinesin or dynein) and form the spindle apparatus that allows chromosome segregation during nuclear division.

Filasomes

Vesicles coated in filamentous actin.

Phalloidin

A toxin that binds specifically to the interface between filamentous actin (F-actin) subunits. Phalloidin conjugated to fluorescent dyes has been widely used for imaging F-actin in eukaryotic cells such as Saccharomyces cerevisiae but has not proved useful for staining F-actin in many filamentous fungi.

Clathrin

A structural protein that forms a cage-like, polyhedral molecular arrangement (a triskelion) composed of three heavy chains and three light chains. Clathrin shapes and coats vesicles during their formation.

Wiscott–Aldrich syndrome protein

(WASP). Founding member of a family of activators of the actin-related protein 2/3 (Arp2/3) complex that participate in signal transduction to the actin cytoskeleton.

Myosin

A superfamily of motor proteins that bind to microfilaments and couple ATP hydrolysis to force generation. Class I myosins are monomeric and are involved in endocytosis. Class II myosins are dimeric and can form filaments, which is important for their conserved role in cytokinesis. Class V myosins are dimeric processive motors that translocate cargoes along actin cables.

Fimbrin

A conserved actin-crosslinking protein that contains a conserved 100 amino acid calponin homology domain found in many actin-binding proteins.

FM4-64

A vital, membrane-selective, amphiphilic styryl dye commonly used to study endocytosis, vesicle trafficking, and organelle organization and movement in living fungal cells.

Lucifer yellow

A vital fluorescent dye used as a marker for fluid-phase endocytosis.

Formins

Large protein dimers that nucleate the formation of filamentous actin by the processive addition of globular actin to the barbed ends of actin microfilaments.

Tropomyosin

An actin-binding protein that binds to and stabilises filamentous actin, promoting actin cable formation.

Golgi equivalents

Single Golgi cisternae that are produced by most filamentous fungi instead of the stacks of cisternae found in animal and plant cells. These organelles process and package macromolecules that are destined for secretion.

Conidial anastomosis tubes

Specialized cell protrusions or short hyphae that emerge from asexual fungal spores (conidia) and mediate cell fusion during colony initiation.

Paxillin

An adaptor protein that participates in signal transduction and actin reorganization in mammalian cells.

Epistatic

Pertaining to a gene: masking the phenotypic effect of another gene.

Exocyst

A multiprotein complex involved in determining where vesicles dock and fuse with the plasma membrane.

Anillin

A Drosophila melanogaster scaffold protein that interacts with and organizes structural components of the contractile actin ring. Other eukaryotes encode anillin-related proteins with similar functions.

Actinin

An actin-binding protein that crosslinks filamentous actin and associates with the plasma membrane.

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Berepiki, A., Lichius, A. & Read, N. Actin organization and dynamics in filamentous fungi. Nat Rev Microbiol 9, 876–887 (2011). https://doi.org/10.1038/nrmicro2666

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