Chapter 11 : Cell Biology of Hyphal Growth

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Filamentous fungi are a large and ancient clade of microorganisms that occupy a broad range of ecological niches ( ). Fungi are recyclers, being major decomposers of plant debris ( ); they form mycorrhizal symbiosis with 93% of all flowering plant families ( ), and they serve in the industrial production of proteins ( ). However, fungi pose a threat to public health, the ecosystem, and our food security ( ). The success of filamentous fungi is largely due to their elongate hypha, a chain of cells separated from each other by septa ( ). Hyphae grow rapidly by polarized exocytosis at the apex ( ), which allows the fungus to extend over long distances and invade many substrates, including soils and host tissues. Hyphal tip growth is initiated by establishment of a growth site and the subsequent maintenance of the growth axis, with transport of growth supplies, including membranes and proteins, delivered by motors along the cytoskeleton to the hyphal apex ( ). Among the enzymes delivered are cell wall synthases that are exocytosed for local synthesis of the extracellular cell wall ( ). Exocytosis is opposed by endocytic uptake of soluble and membrane-bound material into the cell ( ). The first intracellular compartment in the endocytic pathway is the early endosomes (EEs), which emerge to perform essential additional functions as spatial organizers of the hyphal cell ( ). Individual compartments within septated hyphae can communicate with each other via septal pores, which allow passage of cytoplasm or organelles ( ) to help differentiation within the mycelium ( ). This article introduces the reader to more detailed aspects of hyphal growth in fungi.

Citation: Steinberg G, Peñalva M, Riquelme M, Wösten H, Harris S. 2017. Cell Biology of Hyphal Growth, p 231-265. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0034-2016
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Image of Figure 1
Figure 1

Growth patterns in fungal hyphae. Growth occurs in an isotropic fashion during spore germination. Specification of a polarity axis ultimately results in the formation of a hypha that continues to grow at the tip. While tip growth is maintained, the specification of additional polarity axes enables the formation of septa and lateral branches. Whereas septum formation is transient, branching results in the formation of a secondary hypha that also continues to grow at the tip. Red arrows designate polarity axes.

Citation: Steinberg G, Peñalva M, Riquelme M, Wösten H, Harris S. 2017. Cell Biology of Hyphal Growth, p 231-265. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0034-2016
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Figure 2

Highly schematic representation of the cisternal maturation process in the nonstacked fungal Golgi, with indication of the different functional stages. COPII-coated vesicles (green) bud off specialized domains of the ER denoted ER exit sites (ERES) or transitional ER (left). COPII vesicles coalesce to form an early Golgi cisterna, represented here as a green fenestrated structure that depicts actual Golgi structures often visible in EM micrographs. Retrograde COPI traffic (violet vesicles) retrieves back to the ER proteins such as cargo receptors that need to be recycled. Early cisternae are equipped with cargo glycosylation enzymes (t0). As time passes (double arrowheads) an early Golgi cisterna becomes progressively enriched in cargo and late Golgi components (represented in red) by delivering early Golgi ones (e.g., glycosylating enzymes) to cisternae in earlier stages of maturation, in a process which is likely mediated by COPI retrograde traffic (t1 and t2). Eventually, late Golgi components become predominate (TGN, t3) and the cargo-enriched cisterna becomes competent to tear off into carriers destined for the plasma membrane (PM) and the endosomes (t4). TGN cisternae also receive traffic from the endosomal system (blue arrows). In the route (dark blue) connecting the cisternae with the PM, the transition between late Golgi and post-Golgi identity is dictated by the recruitment of RabE to the membranes, which is critically regulated by TRAPPII (see text). Proteins that have been shown by microscopy to localize to specific stages are indicated, with green lettering indicating early Golgi and red lettering indicating TGN. The image summarizes work performed with .

Citation: Steinberg G, Peñalva M, Riquelme M, Wösten H, Harris S. 2017. Cell Biology of Hyphal Growth, p 231-265. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0034-2016
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Figure 3

Illustration of a hyphal tip with the main organelles and subcellular components involved in apical cell wall growth. The diagram is based on work with . (Art: Leonora Martínez-Núñez).

Citation: Steinberg G, Peñalva M, Riquelme M, Wösten H, Harris S. 2017. Cell Biology of Hyphal Growth, p 231-265. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0034-2016
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Figure 4

Diagram showing the cooperation of molecular motors in bidirectional EE motility. The illustration is based on results obtained from studies of . See text for detailed description.

Citation: Steinberg G, Peñalva M, Riquelme M, Wösten H, Harris S. 2017. Cell Biology of Hyphal Growth, p 231-265. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0034-2016
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Figure 5

EEs as multifunctional platforms. Proteins that associate with the organelles are shown as colored symbols and described in black; functions are indicated in dark red. The diagram is based on work with , , and . See text for detailed description.

Citation: Steinberg G, Peñalva M, Riquelme M, Wösten H, Harris S. 2017. Cell Biology of Hyphal Growth, p 231-265. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0034-2016
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Figure 6

Time course of the contraction of the CAR during septum formation in the wheat pathogen . The side view of the three-dimensional image stack shows that the CAR is closing with time. Time in minutes is shown in the upper-left corners. The CAR was labeled using an F-actin-specific GFP-LifeAct probe.

Citation: Steinberg G, Peñalva M, Riquelme M, Wösten H, Harris S. 2017. Cell Biology of Hyphal Growth, p 231-265. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0034-2016
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Figure 7

Model for septum formation. A signal emanating from mitotic nuclei is relayed to the septation site via the septation initiation network (SIN). Components needed for assembly of the contractile actin ring (CAR) (actin filaments, Bud4) are already associated with the septation site and operate in conjunction with the SIN to define the division plane. Activation of the GTPase Rho4 at the septation site initiates organization of actin filaments into a CAR. Constriction of the CAR is coincident with appearance of a septin ring. Deposition of the septum is guided by the CAR. The septin ring disassembles once the final size of the septal pore is reached. Several proteins, including calcineurin and Rho4, remain associated with the mature septal pore. The diagram was modified from Beck et al. ( ).

Citation: Steinberg G, Peñalva M, Riquelme M, Wösten H, Harris S. 2017. Cell Biology of Hyphal Growth, p 231-265. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0034-2016
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Figure 8

Model for tip-ward translocation in . Newly formed hyphal compartments are in cytoplasmic contact with neighboring cells. The Woronin body is not plugging the septal pore, and cytoplasmic streaming, as well as diffusion through the septal pore, is possible (green arrow). Older septa are plugged by Woronin bodies, which prevents exchange of cytoplasm. However, selective transport of molecules such as glucose toward the growth region is still possible (red arrows). This may involve septum-associated transporters.

Citation: Steinberg G, Peñalva M, Riquelme M, Wösten H, Harris S. 2017. Cell Biology of Hyphal Growth, p 231-265. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0034-2016
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Figure 9

Schematic drawing of a dolipore in the basidiomycete . The image was redrawn from a reconstruction of electron micrographs, first published in reference .

Citation: Steinberg G, Peñalva M, Riquelme M, Wösten H, Harris S. 2017. Cell Biology of Hyphal Growth, p 231-265. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0034-2016
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