Polarisome Meets Spitzenkörper: Microscopy, Genetics, and Genomics Converge

Abstract

7The impact of filamentous fungi on human welfare has never been greater. Fungi are acknowledged as the most economically devastating plant pathogens (1) and are attaining increasing notoriety for their ability to cause life-threatening infections in humans (57,71), and fungal products sustain a billiondollar manufacturing industry (70). The tools available to study filamentous fungi are more sophisticated than ever and include the complete annotated genome sequences of multiple filamentous fungi (12), resources being made available through various functional genomics projects, and advanced bioimaging methods, including high-resolution live-cell imaging (20, 32) and electron tomography (19,50). The increasing impact of filamentous fungi, along with the rediscovery of pseudohyphal growth in yeast (22), has focused attention on the molecular mechanisms underlying hyphal morphogenesis.Attempts to understand hyphal morphogenesis have historically followed two different lines of investigation. Microscopists have defined, with increasing detail, the subcellular organization of the hyphal tip. This led to the description of the Spitzenkörper, an apical cluster of vesicles, cytoskeletal elements, and other proteins, which plays a crucial role in hyphal extension (4). Geneticists have identified gene products required for hyphal morphogenesis by characterizing morphological mutants (51,52). Initial studies in the laboratories of Beadle, Tatum, and colleagues attempted to link morphogenesis to specific biochemical pathways. More recent screens have identified a multitude of signaling and cytoskeletal functions required for hyphal extension (62, 72).In the past few years, comparative genomics efforts have allowed fungal biologists interested in hyphal morphogenesis to exploit the wealth of knowledge about polarized growth in the yeast Saccharomyces cerevisiae. Many informative homologies between filamentous fungi and yeast have been uncovered. Notably, this includes several components of a multiprotein complex termed the polarisome (28), which regulates microfilament formation at polarized growth sites in yeast (61).Perhaps more importantly, several gene products involved in hyphal morphogenesis have been shown to have no homologue outside of the filamentous fungi. This emphasizes the potential novelty of the mechanisms underlying hyphal morphogenesis. In this review, we summarize past efforts to understand hyphal morphogenesis and pose a series of questions designed to focus future efforts in this area. HYPHAL MORPHOGENESIS: A BRIEF OVERVIEWFungal hyphae originate from either a germinating spore or another hypha (i.e., during branch formation). Initially, an axis of polarity is established from a symmetrically expanding spore or hyphal compartment. Subsequently, cell surface expansion is restricted to the specified axis, thereby leading to the formation of a polarized hypha that displays a gradient of expansion that peaks at the tip (2,15,25,30,52). Maintenance of the polarity axis allows hyphae to achieve a linear extens...

The Actomyosin Ring Recruits Early Secretory Compartments to the Division Site in Fission Yeast

“…Similarly, Bevis et al, 2002 have suggested that the Golgi elements in Pichia pastoris might preferentially localize toward the budding site. During hyphal growth in Candida albicans, cells assemble the vesicle-rich Spitzenkö rper structure at the tips of growing hyphae (Harris et al, 2005). The intimate association between Spitzenkör-per behavior and hyphal morphogenesis suggests that the Spitzenkö rper might function as a "Vesicle Supply Center," producing the secretory vesicles (Bartnicki-Garcia et al, 1989).…”

The Tip Growth Apparatus ofAspergillus nidulans

“…(Note that there are also some larger SYNA-containing structures that could correspond to larger endosomal compartments; see below.) The Spitzenkö rper ("apical body" or "tip body" in English) is an incompletely defined structure observed at the tips of growing hyphae in many fungi that is thought to be critically important for tip growth (recently reviewed by Harris et al, 2005), and vesicles are a major component of the Spitzenkö rper. Thus, one would expect GFP-SYNA to reveal the Spitzenkö rper, and, indeed, in rapidly growing hyphal tips a vesicle cluster or Spitzenkö rper was visible ( Figure 2B).…”

“…A great deal of progress has been made in understanding fungal tip growth (summarized by Harris et al, 2005;Steinberg, 2007a,b;Riquelme et al, 2007), but key questions remain unanswered. There is general agreement that fungal tip growth involves the synthesis of cell wall components in the cell body, the incorporation of these components into vesicles, the transport of these vesicles to the cell tip, the fusion of these vesicles with the plasma membrane in the area of the cell tip (exocytosis) to release their contents, and the cross-linking of the components after release.…”

“…It is particularly important in filamentous fungi where nearly all growth occurs by hyphal tip extension (reviewed by Momany, 2002). Given that some filamentous fungi are important fermentation organisms, the growth of which is of considerable economic importance, whereas others are serious plant, animal, and human pathogens, there is considerable interest in the mechanisms of tip growth in these organisms.A great deal of progress has been made in understanding fungal tip growth (summarized by Harris et al, 2005; Steinberg, 2007a,b;Riquelme et al, 2007), but key questions remain unanswered. There is general agreement that fungal tip growth involves the synthesis of cell wall components in the cell body, the incorporation of these components into vesicles, the transport of these vesicles to the cell tip, the fusion of these vesicles with the plasma membrane in the area of the cell tip (exocytosis) to release their contents, and the cross-linking of the components after release.…”

From Function to Shape: A Novel Role of a Formin in Morphogenesis of the FungusAshbya gossypii

“…An extreme case of polar growth has evolved in filamentous fungi, which are able to extend the tips of their tubelike cells, called hyphae, for unlimited time, provided nutrients are available (Gow, 1995;Momany, 2002;Harris et al, 2005). Hyphae not only very efficiently elongate but regularly establish new axes of polarity along their cortex, thus forming lateral branches, which themselves again generate lateral branches.…”