Computer simulation of fungal morphogenesis and the mathematical basis for hyphal (tip) growth

Bartnicki-García, S.; Hergert, F.; Gierz, Gerhard

doi:10.1007/bf01322464

Cited by 277 publications

(220 citation statements)

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“…This is critical for the mechanics of hyphal growth, and it is postulated to be critical for the establishment of the hyphal shape (Bartnicki-Garcia et al, 1989;Bartnicki-Garcia, 1990;Gierz and Bartnicki-Garcia, 2001). Exocytosis presumably creates an excess of membrane at the tip that must be internalized by endocytosis (Read and Kalkman, 2003).…”

Section: Localization Of a Vesicular Snare A Target Snare And The Amentioning

confidence: 99%

“…The sites of exocytosis are also postulated to determine the shape of the growing hypha (Bartnicki-Garcia et al, 1989;Bartnicki-Garcia, 1990;Gierz and Bartnicki-Garcia, 2001); thus, it was of particular interest to follow membrane trafficking by using fusion proteins of the synaptobrevin homologue SYNA, an exocytic SNARE (Gerst, 1997). Given that SYNA is a member of a family of prototypic markers for exocytic vesicles (Protopopov et al, 1993;Gerst, 1997;David et al, 1998), it is strongly predicted to be a component of exocytic vesicles that becomes a transient component of the plasma membrane when exocytosis occurs, and then is recycled by endocytosis.…”

Section: Exocytosis Endocytosis and Hyphal Morphogenesismentioning

confidence: 99%

“…Hyphal shape is thus determined to a very significant extent by where the wall precursors are released from the cytoplasm, i.e., by the positioning of the site(s) of exocytosis. Indeed, in the most current mathematical model of hyphal morphogenesis, the positions of the sites of exocytosis are postulated to be the main determinant of hyphal morphology (Bartnicki-Garcia et al, 1989;Bartnicki-Garcia, 1990;Gierz and Bartnicki-Garcia, 2001). The positions of these sites are, in turn, postulated to be governed by the radial movement of vesicles from a vesicle supply center near the tip.…”

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confidence: 99%

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The Tip Growth Apparatus ofAspergillus nidulans

Taheri-Talesh

Horio

Araújo‐Bazán

et al. 2008

MBoC

271

414

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Hyphal tip growth in fungi is important because of the economic and medical importance of fungi, and because it may be a useful model for polarized growth in other organisms. We have investigated the central questions of the roles of cytoskeletal elements and of the precise sites of exocytosis and endocytosis at the growing hyphal tip by using the model fungus Aspergillus nidulans. Time-lapse imaging of fluorescent fusion proteins reveals a remarkably dynamic, but highly structured, tip growth apparatus. Live imaging of SYNA, a synaptobrevin homologue, and SECC, an exocyst component, reveals that vesicles accumulate in the Spitzenkö rper (apical body) and fuse with the plasma membrane at the extreme apex of the hypha. SYNA is recycled from the plasma membrane by endocytosis at a collar of endocytic patches, 1-2 m behind the apex of the hypha, that moves forward as the tip grows. Exocytosis and endocytosis are thus spatially coupled. Inhibitor studies, in combination with observations of fluorescent fusion proteins, reveal that actin functions in exocytosis and endocytosis at the tip and in holding the tip growth apparatus together. Microtubules are important for delivering vesicles to the tip area and for holding the tip growth apparatus in position. INTRODUCTIONPolarized cell growth occurs in most eukaryotic phyla, and it includes a plethora of important phenomena, such as neuronal growth cone extension in animals and pollen tube extension in vascular plants. 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. It is clear that both microtubules and actin microfilaments play important roles in fungal tip growth, but their exact functions are not yet defined. The exact sites of exocytosis and endocytosis also remain to be determined. The positions of the site(s) of exocytosis are particularly important because fungal walls are relatively stiff structures, and once they have formed the shape of the hypha is established. Hyphal shape is thus determined to a very significant extent by where the wall precursors are released from the cytoplasm, i.e., by the positioning of the site(s) of exocyto...

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Section: Localization Of a Vesicular Snare A Target Snare And The Amentioning

confidence: 99%

Section: Exocytosis Endocytosis and Hyphal Morphogenesismentioning

confidence: 99%

mentioning

confidence: 99%

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The Tip Growth Apparatus ofAspergillus nidulans

Taheri-Talesh

Horio

Araújo‐Bazán

et al. 2008

MBoC

271

414

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“…Therefore, it is difficult to discriminate the dark cloud from the Spitzenkö rper observed by Girbardt (1957) with the light microscope. It may be coincident with the vesicle supply center from where vesicles are assumed to migrate to the apical plasma membrane (Bartnicki-Garcia et al, 1989).…”

Section: Figs 8 Andmentioning

confidence: 99%

Endocytosis and Membrane Turnover in the Germ Tube ofUromyces fabae

Hoffmann

Mendgen

1998

Fungal Genetics and Biology

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Hoffmann, J. and Mendgen, K. 1998. Endocytosis and membrane turnover in the germ tube of Uromyces fabae. Fungal Genetics and Biology 24, 77-85. We have used the fluorescent dye FM4-64 as a tracer to demonstrate bulk membrane internalization (endocytosis) and redistribution of the dye within the cytoplasm of the germ tube of the rust fungus Uromyces fabae. Staining of the hyphal membrane was detected 4 s after application of FM4-64 and reached a maximum after 1 min. The highest fluorescence intensity occurred in the apex. Subsequently, staining of the plasma membrane decreased and a subapical region of the fungal protoplast (5-20 m from the tip) displayed increasing fluorescence with a maximum after 5 min. Fluorescence in the subapical region was redistributed to an area in the hyphal tip, which corresponds to the accumulation of apical vesicles, after 10-15 min and subsequently to a cytoplasmic region in front of the two nuclei (35-45 m from the tip). We conclude from our measurements of membrane fluorescence that the turnover time from endocytosis to secretion of the dye amounts to 15 min. The uptake of the dye into the cytoplasm, but not membrane loading, could be inhibited completely with 5 mM NaN 3 or by a temperature shift to 4°C. This is the first evidence for endocytosis in a fungal germ tube. Academic PressIndex Descriptors: tip growth; hyphal apex; Spitzenkö rper; apical vesicle cluster.

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“…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). In fact, it was recently shown that most of the Golgi apparatus is indeed localized near the growing hyphal tips (Rida et al, 2006).…”

Section: Introductionmentioning

confidence: 99%

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

Vještica

Tang

Oliferenko

2008

MBoC

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The ultimate goal of cytokinesis is to establish a membrane barrier between daughter cells. The fission yeast Schizosaccharomyces pombe utilizes an actomyosin-based division ring that is thought to provide physical force for the plasma membrane invagination. Ring constriction occurs concomitantly with the assembly of a division septum that is eventually cleaved. Membrane trafficking events such as targeting of secretory vesicles to the division site require a functional actomyosin ring suggesting that it serves as a spatial landmark. However, the extent of polarization of the secretion apparatus to the division site is presently unknown. We performed a survey of dynamics of several fluorophore-tagged proteins that served as markers for various compartments of the secretory pathway. These included markers for the endoplasmic reticulum, the COPII sites, and the early and late Golgi. The secretion machinery exhibited a marked polarization to the division site. Specifically, we observed an enrichment of the transitional endoplasmic reticulum (tER) accompanied by Golgi cisternae biogenesis. These processes required actomyosin ring assembly and the function of the EFC-domain protein Cdc15p. Cdc15p overexpression was sufficient to induce tER polarization in interphase. Thus, fission yeast polarizes its entire secretory machinery to the cell division site by utilizing molecular cues provided by the actomyosin ring. INTRODUCTIONCell division is the final event in the cell cycle that results in physical separation of two daughter cells. Despite being studied for more than a hundred years, the underlying molecular mechanisms and the cytological details of the process are still emerging. Various organisms and cell types have established multiple pathways to conduct cell division that are regulated at both signaling and structural levels (for review see Balasubramanian et al., 2004). In recent years, the fission yeast Schizosaccharomyces pombe has emerged as an attractive model for the study of cytokinesis because of its fully sequenced genome (Wood et al., 2002), a cell size convenient for cytological studies and the availability of a large set of conditional mutants compromised in various aspects of cell division (Chang et al., 1996;Balasubramanian et al., 1998).On entry into mitosis, S. pombe assembles an actomyosin ring that is thought to drive a binary cell fission through constriction, similar to many other eukaryotes, including nematodes, insects, and vertebrates (for review see Hales et al., 1999). During early mitosis, actin is assembled into a ring structure through the action of several actin nucleating and bundling proteins and molecular motors. These include the formin Cdc12p (Chang et al., 1997), profilin Cdc3p (Balasubramanian et al., 1992), the extended Fer/CIP4 (EFC) domain protein Cdc15p (Fankhauser et al., 1995), and the myosin heavy chain Myo2p (Kitayama et al., 1997) together with its light chains Cdc4p (McCollum et al., 1995;Naqvi et al., 1999) and Rlc1p (Le Goff et al., 2000). It has been proposed tha...

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Computer simulation of fungal morphogenesis and the mathematical basis for hyphal (tip) growth

Cited by 277 publications

References 36 publications

The Tip Growth Apparatus ofAspergillus nidulans

The Tip Growth Apparatus ofAspergillus nidulans

Endocytosis and Membrane Turnover in the Germ Tube ofUromyces fabae

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

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