Research Topic A - Microtubule organisation and interphase function

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Research articles

Steinberg, G., Wedlich-Söldner, R., Brill, M., & Schulz, I. (2001) Microtubules in the fungal pathogen Ustilago maydis are highly dynamic and determine cell polarity. J. Cell Sci., 114, 609-622.

Microtubules in the fungal pathogen <em>Ustilago maydis</em> are highly dynamic and determine cell polarity (740Kb PDF)   View movie

Summary - Microtubules in yeast-like cells of U. maydis form a prominent array that becomes reorganized during the cell cycle. The spindle pole bodies form the mitotic spindle in the daughter cell but are silent in interphase, when long bundles of microtubules extend to the cell poles. In budding cells tubulin structures appear at the boundary between mother and daughter cell that seem to organize the microtubules in U. maydis. Conditional alpha-tubulin mutants undergo lateral budding, indicating that microtubules support cell polarization. Surprisingly, interphase microtubules are very dynamic and undergo numerous types of motility, including bending and translocation. Taken together, this is the first report on motility of microtubules in a fungus.

Wedlich-Söldner, R., Schulz, I., Straube, A. & Steinberg, G. (2002) Dynein supports motility of the endoplasmic reticulum in the fungus Ustilago maydis. Mol. Biol. Cell, 13, 965-977.

Dynein Supports Motility of Endoplasmic Reticulum in the Fungus <em>Ustilago maydis </em>(792Kb PDF)

Summary - This paper is the first report on a role for interphase microtubules and dynein in motility of fungal endoplasmic reticulum. In U. maydis the endoplasmic reticulum forms a peripheral network, within which individual tubules are rapidly moving. This motility is driven by cytoplasmic dynein and is required for re-establishing the network after osmotic disruption.

Straube, A., Brill, M, Oakley, B.R. , Horio, T. & Steinberg G. (2003) Microtubule organization requires cell cycle dependent nucleation at dispersed cytoplasmic sites, polar and perinuclear MTOCs in the plant pathogen Ustilago maydis, Mol. Biol. Cell, 14, 642-657.

Microtubule Organization Requires Cell Cycledependent Nucleation at Dispersed Cytoplasmic Sites: Polar and Perinuclear Microtubule Organizing Centers in the Plant Pathogen <em>Ustilago maydis</em> (1Mb PDF)   View movie

Summary - This work describes that microtubule organization in U. maydis depends on cell cycle-specific nucleation at numerous MTOCs, including cytoplasmic sites and the SPB. Making use of a plus-end marker Peb1 (an EB1-homolouge) we provide a detailed quantitative study on microtubule organization and orientation in yeast-like cells. In G1/S-phase cytoplasmic microtubule-organizing centres form an antipolar array. The array becomes reorganized in G2, when gamma-tubulin containing MTOCs appear at the boundary between mother and daughter cell. From here microtubules grow towards both cell poles.

Adamíková, L., Schulz, I., Straube, A., & Steinberg G. (2004) A SERCA-type Ca2+ATPase required for dynein-dependent microtubule organization in the pathogenic fungus Ustilago maydis. Mol. Biol. Cell, 15, 1969-1980.

Calcium Signaling Is Involved in Dynein-dependent Microtubule Organization (664Kb PDF)

Summary - This is the first report on a connection between calcium signalling, dynein, and microtubule organization in fungal morphogenesis. In a genetic screen for factors that organize the interphase microtubule array we identified a sarcoplasmic/endoplasmic calcium ATPase. Defects in this calcium pump resulted in Ca(2+)/calmodulin-dependent kinases-dependent alteration of microtubule dynamics. In many respects these alterations reflect the phenotype of dynein mutants indicating that calcium-signalling regulates dynein activity, thereby controlling microtubule organization.

Fuchs, U., Manns, I. & Steinberg, G. (2005) Microtubules are dispensable for the initial pathogenic development but required for long-distance hyphal growth in the corn smut fungus Ustilago maydis. Mol. Biol. Cell, 16, 2746-2758.

Microtubules Are Dispensable for the Initial Pathogenic Development but Required for Long-Distance Hyphal Growth in the Corn Smut Fungus <em>Ustilago maydis</em> (760Kb PDF)

Summary - This fundamental study addresses the role of the cytoskeleton in U. maydis, and is the first systematic analysis of the role of the cytoskeleton in fungal pathogenicity. We found an essential role of F-actin (=microfilaments) in polarized growth in yeast-like cells, pheromone-induced hyphae and dikaryotic infectious hyphae. In addition, F-actin is required for essential steps during early pathogenic development, including cell-cell fusion and pheromone secretion. In contrast, microtubules are not needed for cell-cell fusion and are less important for polarized growth. However, microtubule-based processes become essential when hyphae exceed a length of approximately 50 µm, which might be related to nuclear migration defects.

Fink, G. & Steinberg, G. (2006) Dynein-dependent microtubule motility supports polarization of the tubulin cytoskeleton in the fungus Ustilago maydis. Mol. Biol. Cell, 17, 3242-53.

Dyneindependent Motility of Microtubules and Nucleation Sites Supports Polarization of the Tubulin Array in the Fungus <em>Ustilago maydis</em>   View movie

Summary - This study addresses the molecular basis and the cellular reason for the motility of free microtubules in yeast-like cells in U. maydis. We show that dynein accumulates at the plus-ends of moving microtubules from where it becomes 'off-loaded' and thereby slides the tubulin polymers along the cortex. In growing cells this activity appears to focus bipolar cytoplasmic microtubule-organising centres at the boundary between the daughter and mother cell, which is an essential step in polarizing the microtubule array. This is the first and only report on a role of dynein in microtubule motility and polarization of the microtubule array in a system other than the mammalian neuron, suggesting that this process is evolutionary conserved.

Straube, A., Hause, G. & Steinberg, G. (2006) Conventional kinesin mediates microtubule-microtubule interactions in vivo. Mol. Biol. Cell.,17, 907-16.

Conventional Kinesin Mediates Microtubule-Microtubule Interactions In Vivo

Summary - Kinesin-1 is a well-established organelle transporter. In this study, we provide in vivo evidence for a role of this conventional kinesin in mediating microtubule-microtubule interactions in the model fungus U. maydis. We further demonstrate that microtubule cross-linking is mediated by a conserved stretch in the tail of the kinesin-1 heavy chain. This study suggests a so far not appreciated new function for conventional kinesin. In doing so it challenges the dogma that motors are either membrane transporter or microtubule organizer.

Review articles

Steinberg, G. (2007) Tracks for traffic: Microtubules in the plant pathogen Ustilago maydis. New Phytol., 174, 721-733.

Tracks for traffic: microtubules in the plant pathogen <em>Ustilago maydis</em> (350Kb)

Steinberg, G. (2007) Preparing the way: Fungal motors in microtubule organization, Trends Microbiol., 15, 14-21.

Preparing the way: Fungal motors in microtubule organization (283Kb)

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Microtubules in an unbudded yeast-like cell of Ustilago maydis

Figure 1: Microtubules (stained with GFP-alpha-tubulin, Tub1) in an unbudded yeast-like cell of U. maydis. Note that the microtubule array requires cytoplasmic nucleation of microtubules and that the nuclear spindle pole body is silent at this stage (nuclear DNA is stained by histone 4, H4).

Microtubules in an unbudded yeast-like cell of Ustilago maydis

Figure 2: Microtubules (stained with GFP-alpha-tubulin, Tub1) in a distal part of a hypha. The growing plus ends are labelled by an EB1-homologue (EB1). More than 90% of all plus-ends are directed to the hyphal tip, indicating that kinesin motors are supporting apical growth and cell expansion. The image was taken from Schuchardt et al. 2005, Mol Biol Cell. 16, 5191.