ReviewOscillatory fungal cell growth
Introduction
Filamentous fungi grow as highly polarized tubular cells called hyphae, that extend the cell body at one end in a process called “tip growth”. Cell extension sites are maintained at hyphal tips, where simultaneous actin assembly, exocytosis and tip extension occur (Fischer et al., 2008, Riquelme et al., 2011, Takeshita et al., 2014). Several filamentous fungi that extend cells in this manner are excellent systems for analyzing this process (Lopez-Franco et al., 1994). Some filamentous fungi are pathogenic to animals and plants and invade host cells via hyphal growth (Perez-Nadales et al., 2014). Others have uses in biotechnology and food production such as enzyme production and fermentation, respectively, as they secrete large amounts of enzymes (Kobayashi et al., 2007, Punt et al., 2002). Both the pathogenicity and enzyme secretory ability of fungi are closely associated with hyphal growth. Thus, understanding polarized growth in filamentous fungi can provide insights that are important to medicine, agriculture and biotechnology.
The extension of hyphal tips requires constant enlargement of the cell membrane. Vesicle trafficking supplies the required proteins and lipids via actin, as well as microtubule cytoskeletons and their corresponding motor proteins (Egan et al., 2012, Penalva et al., 2017, Steinberg, 2011, Taheri-Talesh et al., 2008). Microtubules serve as tracks of secretory vesicles for long-distance transport to hyphal tips and are important for rapid hyphal growth (Horio and Oakley, 2005, Seiler et al., 1997). Actin cables formed from the hyphal tip in the retrograde direction are involved in exocytosis and secretory vesicle accumulation before exocytosis (Berepiki et al., 2011, Bergs et al., 2016). Secretory vesicles accumulate and then secretion results in the formation of a fungal-specific structure, called the Spitzenkörper (Harris et al., 2005, Riquelme and Sanchez-Leon, 2014).
Besides their role as tracks for vesicle traffic, microtubules are necessary to maintain the direction of hyphal growth (Riquelme et al., 1998). Polar organization of the actin cytoskeleton is mediated mainly by microtubule-dependent positioning of polarity marker proteins. One polarity marker in Aspergillus nidulans (TeaA) is specifically delivered to the apex by growing microtubules, and it is anchored to the apical membrane by direct interaction with another polarity marker (TeaR) at the plasma membrane (Fischer et al., 2008, Takeshita et al., 2008). Their interdependent interaction at the apical membrane initiates the recruitment of additional components including the formin which polymerizes actin cables for targeted cargo delivery. Defective polarity markers result in hyphae that are curved or zigzagged instead of straight.
Although the stepwise cell extension at hyphal tips of several filamentous fungi was discovered 20 years ago (Lopez-Franco et al., 1994), most of the molecular details of the mechanism have remained obscure.
Section snippets
Oscillation of fungal tip growth
A recent study using advanced super-resolution microscopy revealed that TeaR transiently assembles at the hyphal tip membrane of A. nidulans (Fig. 1A)(Ishitsuka et al., 2015). A microtubule grows towards the hyphal tip, pauses in close contact with the apical membrane, and then undergoes a catastrophic event resulting in retraction. TeaR accumulates at the hyphal tip membrane, then decreases immediately after a microtubule plus-end touches the tip membrane and starts to shrink. Super-resolution
Transient Ca2+ influx
Several Ca2+ channels, pumps and transporters, such as the plasma membrane, ER, Golgi, mitochondria and vacuoles function in fungal organelles (Zelter et al., 2004). The Ca2+ channels at the plasma membrane of Saccharomyces cerevisiae, Mid1 and Cch1p, share a single pathway that responds to environmental stressors and ensures cellular Ca2+ homeostasis (Iida et al., 1994, Locke et al., 2000, Paidhungat and Garrett, 1997). Deletion of the orthologues midA and cchA from A. nidulans causes
Growth oscillation in other organisms
Oscillations in cell growth are conserved among various organisms. Small clusters of the Rho-type GTPase Cdc42 emerge in budding yeast cells immediately before a bud emerges, then they disperse and re-form in an oscillatory manner (Howell et al., 2012). In fission yeast cells undergoing bipolar growth after NETO, GTP-bound Cdc42 accumulates at one tip, then disperses from it while simultaneously accumulating at another in an oscillatory manner (Fig. 2A)(Das et al., 2012). Active GTPases
Biological meaning of oscillations
Relationships between cellular responses and receptor stimuli are encoded by the spatial and temporal dynamics of downstream signaling networks (Kholodenko, 2006). Positive feedback, alone or in combination with negative feedback, can trigger oscillations, for example the Ca2+ oscillations that arise from Ca2+-induced Ca2+ release (Goldbeter, 2002). The shape of oscillations is characterized by their amplitude and phase. The frequency modulation of Ca2+ oscillations provides an efficient means
Perspectives
The dynamic responses to external and internal signals are fundamental to the increased understanding of chemotropism, cell-cell fusion, microbial interaction and the fungal penetration of plant and animal cells. Live cell imaging will continue to be a powerful tool. In addition, a combination with microfluidic devices would be a new tool to monitor cellular behavior at the single cell level. Tip growth in filamentous fungi has an advantage in these analyses. These new insights will be
Acknowledgements
The work was supported by the Japan Society for the Promotion of Science (JSPS) KAKENHI Grant Number 15K18663 and JST ERATO Grant Number JPMJER1502, Japan.
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