American Society for Microbiology

Hyphal growth: a tale of motors, lipids, and the spitzenkorper

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Filamentous fungi are a large and evolutionarily successful group of organisms of enormous ecological importance (27, 114). Fungi also have a considerable impact on our economy because they serve as bio-factories for the industrial production of proteins (90, 130) and because many fungi are human and plant pathogens that pose a threat to public health and agriculture (1, 105, 124).

The basic unit of a filamentous fungus is the hypha, which usually consists of a chain of elongated cells that expand at the apex of the tip cell (10, 41, 115). Hyphal tip growth is characterized by the initial establishment of one growth site, which is followed by its continuous maintenance. This growth mode is different from budding in the yeast Saccharomyces cerevisiae. Here a short period of polarized apical growth is followed by extended isotrophic growth, which allows delivery of cell wall material over the entire bud surface and which leads to the almost spherical daughter cell (28, 68). In contrast, hyphal growth results in an elongated tip cell, which raises new requirements. Among these is the long-distance transport between the subapical part and the apex of the tip cell. It is thought that microtubule (MT)-based motors, including kinesin-1 and kinesin-3, deliver vesicles and growth supplies over long distances to the hyphal tip (see below). However, in agreement with the described differences between hyphal growth and budding, these motors are not even encoded by the genome of S. cerevisiae.

Hyphal growth is accompanied by the secretion of exoenzymes that participate in lysis of the substrate or are involved in the synthesis of the fungal cell wall (3, 42). The cell wall can be considered as an extracellular matrix consisting mainly of a meshwork of polysaccharides and manno-proteins that shelters the cell and resists the internal turgor pressure to maintain the shape of the hypha (112).

It is currently thought that growth of fungal hyphae is mediated by cytoskeleton-based polar exocytosis at the hyphal tip and cytoplasmic expansion forces that push the cytoplasm against the flexible apical wall (summarized in reference 7). This model is in part based on the phenotypic similarities between fungal cells and plant cells that grow at their tips, such as pollen tubes or root hairs (36). However, phylogenetic comparison of rRNA or conserved proteins demonstrates that fungi are more closely related to animals (6, 131), and there is evidence for amoeboid motility of fungal cells (50). In this article, I will summarize recent results from different fields of fungal cell biology that are instrumental for understanding hyphal tip growth. This includes research on the Spitzenkörper, the polarisome, the role of the cytoskeleton in endo- and exocytosis, the cellular function of sterol-rich plasma membrane domains, and the mechanism that generates the force for extension of the hypha. Finally, I will integrate all of these results from different fungal systems in a model for hyphal tip growth, and I will end the review by providing directions for future research.

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