Hyphal Growth

Steven D Harris, University of Nebraska, Lincoln, Nebraska, USA

Published online: September 2012

DOI: 10.1002/9780470015902.a0000367.pub2

Hyphae are tubular structures that constitute the basic unit of a fungal mycelium. It is the efficient growth of hyphae that plays a crucial role in fungal colonisation of a substrate. Hyphal growth is driven by localised cell surface expansion and cell wall deposition at the hyphal tip. Spatial and temporal regulatory mechanisms enforce this growth pattern by controlling the recruitment of the morphogenetic machinery, which consists of the cytoskeletal and vesicle trafficking elements that mobilise the precursors needed for growth. In addition to the establishment and maintenance of hyphal polarity, the ability to regulate the termination of polarised growth is likely to be important because it facilitates transitions from hyphal growth to development or pathogenesis. Hyphal growth presumably evolved as an adaptation that enabled filamentous fungi to efficiently colonise terrestrial habitats.

Key Concepts:

  • Hyphal growth is the defining feature of filamentous fungi.
  • The morphogenetic machinery consists of those elements of the cytoskeleton and vesicle trafficking components that are needed to drive extension of the hyphal tip.
  • The Spitzenkörper is a vesicle supply and transit centre located at the hyphal tip that is required for optimal rates of tip extension.
  • The spatial separation of exocytosis and endocytosis within the hyphal tip complex enables rapid tip extension.
  • The direction of hyphal extension is regulated by a microtubule-based marking system that conveys positional information to the morphogenetic machinery.
  • Reactive oxygen species and calcium appear to serve as signals that regulate tip growth and the emergence of branches.
  • Duplication cycle describes the events that encompass the doubling of cell mass and nuclear numbers during hyphal growth.
  • The termination of polarised hyphal growth is often a key prerequisite for development and pathogenesis.
  • The hyphal mode of growth appears to have independently evolved on multiple occasions during evolution.

Keywords: colony growth; hyphal extension; hyphal tip cell; morphogenetic machinery; mycelium; polarised growth; septum formation

Figure 1. Morphogenetic events during the early stages of hyphal growth. (a) Dormant spore. (b) Swollen spore that has undergone isotropic expansion. (c) Establishment of a polarity axis. (d) Germ tube emergence. (e) Germ tube extension. (f) Septum formation. Maximal extension rates are typically achieved following septation. (g) Emergence of a lateral branch.
Figure 2. Organisation of the cytoskeleton in fungal hyphae. Mature Aspergillus nidulans hyphae were imaged to detect microtubules (a) and actin (b). Microtubules were detected in living hyphae using a GFP-tubA fusion protein. Actin was detected in fixed hyphae using a monoclonal anti-actin antibody. Note that microtubules extend the length of the hypha, whereas actin localises to the septation site (arrow) and the hyphal tip (arrowhead). Bar, 3 m.
Figure 3. Organisation of hyphal tip cells and sub-apical cells. Schematic depiction of an extending hypha. Note the asymmetric organisation of the hyphal tip cell. Nuclei (blue) exhibit a gradient of mitosis, with condensed mitotic nuclei located proximal to the tip. In addition, vacuoles (open red circles) and endomembranes (green) are more fragmented near the tip. Finally, the tip also houses the Spitzenkörper (stippled black circle) and the polarisome (yellow). The enlarged depiction of the hyphal tip shows the exocyst (orange), microtubules (green lines), actin filaments (red lines) and actin patches (filled red circles). Adapted from Harris SD (2010).
Figure 4. A microtubule-based marking system that recruits the morphogenetic machinery to hyphal tips. Kinesin-dependent transport utilises microtubules (green) to deliver TeaA to the hyphal tip. TeaR is tethered to the membrane at the hyphal tip, and serves as a ‘receptor’ for TeaA. Upon interaction with TeaR, TeaA recruits the formin SepA, which in turn nucleates the formation of actin filaments (purple).
close
 References
    Araujo-Palomares CL, Castro-Longoria E and Riquelme M (2007) Ontogeny of the Spitzenkorper in germlings of Neurospora crassa. Fungal Genetics and Biology 44: 492–503.
    Bartnicki-Garcia S, Hergert F and Gierz G (1989) Computer simulation of fungal morphogenesis and the mathematical basis for hyphal tip growth. Protoplasma 153: 46–57.
    Bidlingmaier S and Snyder M (2004) Regulation of polarized growth initiation and termination cycles by the polarisome and Cdc42 regulators. Journal of Cell Biology 164: 207–218.
    Borkovich KA, Alex LA, Yarden O et al. (2004) Lessons from the genome sequence of Neurospora crassa: tracing the path from genomic blueprint to multicellular organism. Microbiology and Molecular Biology Reviews 68: 1–108.
    Bruno KS, Morrell JL, Hamer JE and Staiger CJ (2001) SEPH, a Cdc7p orthologue from Aspergillus nidulans, functions upstream of actin ring formation during cytokinesis. Molecular Microbiology 42: 3–12.
    Caudron F and Barral Y (2009) Septins and the lateral compartmentalization of eukaryotic membranes. Developmental Cell 16: 493–506.
    Chang F and Peter M (2003) Yeasts make their mark. Nature Cell Biology 5: 294–299.
    book Crous PW, Verkley GJM, Groenewald JZ and Samson RA (2009) CBS Laboratory Manual Series: Fungal Biodiversity. Utrecht: CBS-KNAW Fungal Biodiversity Centre.
    Fiddy C and Trinci APJ (1976) Mitosis, septation and the duplication cycle in Aspergillus nidulans. Journal of General Microbiology 97: 169–184.
    Fischer R, Zekert N and Takeshita N (2008) Polarized growth in fungi – interplay between the cytkeleton, positional markers and membrane domains. Molecular Microbiology 68: 813–826.
    Girbardt M (1957) Der Spitzenkörper von Polystictus versicolor. Planta 50: 47–59.
    Hamer JE, Valent B and Chumley FG (1989) Mutations at the smo genetic locus affect the shape of diverse cell types in the rice blast fungus. Genetics 122: 351–361.
    Harris SD (2008) Branching of fungal hyphae: regulation, mechanisms, and comparison with other branching systems. Mycologia 100: 823–832.
    book Harris SD (2010) "Hyphal growth and polarity". In: Borkovich KA and Ebbole DJ (eds) Cellular and Molecular Biology of Filamentous Fungi, pp. 238–259. Washington: ASM Press.
    Harris SD (2011) Hyphal morphogenesis: an evolutionary perspective. Fungal Biology 115: 475–484.
    Harris SD and Kraus PR (1998) Regulation of septum formation in Aspergillus nidulans by a DNA damage checkpoint pathway. Genetics 148: 1055–1067.
    Harris SD, Turner G, Meyer V et al. (2009) Morphology and development in Aspergillus nidulans: a complex puzzle. Fungal Genetics and Biology 46: S82–S92.
    Köhli M, Galati V, Boudier K, Roberson RW and Philippsen P (2008) Growth-speed-correlated localization of exocyst and polarisome components in growth zones of Ashbya gossypii hyphal tips. Journal of Cell Science 121: 3878–3889.
    Lindsey R, Cowden S, Hernández-Rodríguez Y and Momany M (2010) Septins AspA and AspC are important for normal development and limit the emergence of new growth foci in the multicellular fungus Aspergillus nidulans. Eukaryotic Cell 9: 155–163.
    book Read ND, Fleiner A, Roca MG and Glass NL (2010) "Hyphal fusion". In: Borkovich KA and Ebbole DJ (eds) Cellular and Molecular Biology of Filamentous Fungi, pp. 260–273. Washington: ASM Press.
    Riquelme M, Yarden O, Bartnicki-Garcia S et al. (2011) Architecture and development of the Neurospora crassa hypha—a model cell for polarized growth. Fungal Biology 115: 446–474.
    Shaw BD, Chung DW, Wang CL, Quintanilla LA and Upadhyay S (2011) A role for endocytic recycling in hyphal growth. Fungal Biology 115: 541–546.
    Stajich JE, Berbee ML, Blackwell M et al. (2009) The fungi. Current Biology 19: R840–R845.
    Sudbery P (2011) Fluorescent proteins illuminate the structure and function of the hyphal tip apparatus. Fungal Genetics and Biology 48: 849–857.
    Sudbery P, Gow N and Berman J (2004) The distinct morphogenic states of Candida albicans. Trends in Microbiology 12: 317–324.
    Taheri-Talesh N, Horio T, Araujo-Bazán L et al. (2005) The tip growth apparatus of Aspergillus nidulans. Molecular Biology of the Cell 19: 1439–1449.
    book Trinci APJ, Wiebe NG and Robson GD (1994) "The fungal mycelium as an integrated entity". In: Wessels JGH and Meinhardt F (eds) The Mycota, Growth and Differentiation and Sexuality, vol. 1, pp. 175–193. Heidelberg: Springer-Verlag.
 Further Reading
    Berepiki A, Lichius A and Read ND (2011) Actin organization and dynamics in filamentous fungi. Nature Reviews Microbiology 9: 876–887.
    Lichius A, Berepiki A and Read ND (2011) Form follows function – the versatile fungal cytoskeleton. Fungal Biology 115: 518–540.
    book Moore D, Robson GD and Trinci APJ (2011) 21st Century Guidebook to Fungi. Cambridge: Cambridge University Press.
    Seiler S and Justa-Schuch D (2010) Conserved components, but distinct mechanisms for the placement and assembly of the cell division machinery in unicellular and filamentous ascomycetes. Molecular Microbiology 78: 1058–1076.

Related Sub-Topics:

Composition and Structure of Microbial Cells | Fungi
Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

Article Title: Hyphal Growth
 
How to Cite close
Harris, Steven D(Sep 2012) Hyphal Growth. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0000367.pub2]