Endocytosis and Membrane Turnover in the Germ Tube ofUromyces fabae

Hoffmann, Jochen; Mendgen, Kurt

doi:10.1006/fgbi.1998.1059

Cited by 66 publications

(52 citation statements)

References 30 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

mentioning

confidence: 72%

“…In filamentous fungi, the endocytotic pathway may be required for polarized growth because of the need for membrane recycling. This has been strongly implied from studies in Ustilago maydis (Wedlich-Söldner et al, 2000) and Uromyces fabae (Hoffmann and Mendgen, 1998).Membrane recycling may be particularly important during the very rapid transition in growth that accompanies penetration peg formation and the release of appressorial turgor. If PDE1 is required for the efficient movement and docking of endosomal vesicles, then this too might account for its requirement in penetration peg formation.…”

mentioning

confidence: 92%

See 1 more Smart Citation

PDE1 Encodes a P-Type ATPase Involved in Appressorium-Mediated Plant Infection by the Rice Blast Fungus Magnaporthe grisea

Balhadère

Talbot

2001

Plant Cell

View full text Add to dashboard Cite

Plant infection by the rice blast fungus Magnaporthe grisea is brought about by the action of specialized infection cells called appressoria. These infection cells generate enormous turgor pressure, which is translated into an invasive force that allows a narrow penetration hypha to breach the plant cuticle. The Magnaporthe pde1 mutant was identified previously by restriction enzyme-mediated DNA integration mutagenesis and is impaired in its ability to elaborate penetration hyphae. Here we report that the pde1 mutation is the result of an insertion into the promoter of a P-type ATPase-encoding gene. Targeted gene disruption confirmed the role of PDE1 in penetration hypha development and pathogenicity but highlighted potential differences in PDE1 regulation in different Magnaporthe strains. The predicted PDE1 gene product was most similar to members of the aminophospholipid translocase group of P-type ATPases and was shown to be a functional homolog of the yeast ATPase gene ATC8 . Spatial expression studies showed that PDE1 is expressed in germinating conidia and developing appressoria. These findings implicate the action of aminophospholipid translocases in the development of penetration hyphae and the proliferation of the fungus beyond colonization of the first epidermal cell. INTRODUCTIONOne of the principal reasons why pathogenic fungi are so successful at causing plant disease is their ability to penetrate the plant cuticle directly, often using specialized infection cells called appressoria (Mendgen et al., 1996). A wide variety of fungal pathogens form appressoria, and the development of these cells involves a complex morphogenetic program that results in rapid differentiation of a highly specialized structure (Dean, 1997). The rice blast fungus Magnaporthe grisea is an important pathogen of cultivated rice and has emerged as an experimental model for the study of plant infection processes (for reviews, see Howard and Valent, 1996;Hamer and Talbot, 1998). Magnaporthe develops dome-shaped appressoria, which form at the ends of germ tubes soon after spore germination on the leaf surface. Appressoria attach strongly to the leaf and then generate enormous turgor pressure (up to 8 MPa), which is used to rupture the plant cuticle (Howard et al., 1991). The turgor inside appressoria is generated by a rapid increase in intracellular glycerol levels, which is maintained by a specialized cell wall layer containing melanin (Howard and Ferrari, 1989;de Jong et al., 1997). If melanin biosynthesis is blocked, either by chemical intervention or mutation, then Magnaporthe is unable to penetrate the plant surface and cannot cause disease (Chida and Sisler, 1987;Chumley and Valent, 1990).How such enormous cellular turgor is translated into the substantial invasive force necessary to breach the plant cell wall is not clear, but it appears to involve polarization of the cytoskeleton to the point of infection and localized cell wall modification Howard, 1990, 1992;Bechinger et al., 1999). A narrow penetration hypha forms at t...

show abstract

mentioning

confidence: 72%

mentioning

confidence: 92%

PDE1 Encodes a P-Type ATPase Involved in Appressorium-Mediated Plant Infection by the Rice Blast Fungus Magnaporthe grisea

Balhadère

Talbot

2001

Plant Cell

View full text Add to dashboard Cite

show abstract

“…Pioneering studies of the endocytic pathway in the yeast Saccharomyces cerevisiae have shown that the amphiphilic styryl dye FM4-64 is internalized by endocytosis and is delivered to the fungal vacuole via the endocytic pathway (127). Surprisingly, similar studies in filamentous fungi have demonstrated that FM4-64 transiently stains the Spitzenkörper (20,31,48,53), which indicates that endocytic vesicles cluster in the hyphal tip. Indeed, endocytic recycling via early endosomes is essential for proper hyphal morphology and pathogenicity in the corn smut Ustilago maydis (33,134 [also see below]).…”

Section: Endocytosis and Hyphal Growthmentioning

confidence: 99%

Hyphal Growth: a Tale of Motors, Lipids, and the Spitzenkörper

2007

View full text Add to dashboard Cite

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 Spitzenkör-per, 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 ...

show abstract

“…An important breakthrough was the observation that the endocytosis marker dye FM4-64 rapidly stains vesicles within the Spitzenkörper (Fig. 1b to d) (18,32,35), not only providing evidence for the interconnection of endocytic and secretory pathways but demonstrating the dye's utility for visualizing and analyzing Spitzenkörper behavior in wild-type and mutant strains (31,32).…”

Section: Microscopymentioning

confidence: 99%

Polarisome Meets Spitzenkörper: Microscopy, Genetics, and Genomics Converge

et al. 2005

View full text Add to dashboard Cite

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...

show abstract

Endocytosis and Membrane Turnover in the Germ Tube ofUromyces fabae

Cited by 66 publications

References 30 publications

PDE1 Encodes a P-Type ATPase Involved in Appressorium-Mediated Plant Infection by the Rice Blast Fungus Magnaporthe grisea

PDE1 Encodes a P-Type ATPase Involved in Appressorium-Mediated Plant Infection by the Rice Blast Fungus Magnaporthe grisea

Hyphal Growth: a Tale of Motors, Lipids, and the Spitzenkörper

Polarisome Meets Spitzenkörper: Microscopy, Genetics, and Genomics Converge

Contact Info

Product

Resources

About