Research Topic B - Molecular motors in hyphal growth and pathogenicity of U. maydis

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Research articles

Weber, I., Gruber, C, & Steinberg, G. (2003) A class V myosin required for mating, hyphal growth and pathogenicity in the dimorphic plant pathogen Ustilago maydis. Plant Cell, 15, 2826-2842.

A Class-V Myosin Required for Mating, Hyphal Growth, and Pathogenicity in the Dimorphic Plant Pathogen Ustilago maydis (4.1Mb PDF)   View movie

Summary - We show here that a class V myosin, Myo5, participates in polarized growth and pathogenicity of U. maydis. Myo5 was indispensable for conjugation tube formation and myo5 mutants were impaired in the perception of pheromones, indicating that this motor is essential for fungal virulence. This is the first report on the role of a molecular motor in a plant pathogen.

Schuchhardt, I., Aßmann, D., Thines, E, Schuberth, C. & Steinberg, G. (2005) Myosin-V, Kinesin-1 and Kinesin-3 cooperate in long-distance transport in hyphal growth of the fungus Ustilago maydis. Mol. Biol. Cell, 16, 5191-5201.

Myosin-V, Kinesin-1, and Kinesin-3 Cooperate in Hyphal Growth of the Fungus Ustilago maydis (720Kb PDF)   View movie

Summary - In this paper we demonstrate that actin- and microtubule-based transport support hyphal growth. Although microtubule plus-ends are directed to the hyphal tip, only kinesin-1 and kinesin-3 are involved in polarized growth, whereas deletion of all other kinesins was without influence on filamentous growth. This is the first systematic study on the role of molecular motor in hyphal growth of fungi.

Weber, I., Aßmann, D., Thines, E., & Steinberg, G. (2006) Polar localizing class V myosin chitin synthases are essential during early plant infection in the plant pathogenic fungus Ustilago maydis. Plant Cell,18, 225-42.

Polar Localizing Class VMyosin Chitin Synthases Are Essential during Early Plant Infection in the Plant Pathogenic Fungus Ustilago maydis (788Kb PDF)

Summary - Here we show that a myosin-chitin synthase, Mcs1, is essential for early plant infection but not in growth ex planta. In contrast, two class IV chitin synthases are required for shaping yeast cells and hyphae outside of the cell. Although the existence of a myosin motor in Mcs1 suggests motor function, motor activity has not yet been demonstrated. This is the first systematic study that analyses all chitin synthases in different developmental stages. It suggests that chitin synthases have development-specific roles, which challenges the dogma that high numbers of chitin synthases indicate redundancy.

Treitschke, S., Doehlemann, G., Schuster, M. & Steinberg, G. (2010) The myosin-motor domain of fungal chitin synthase V is dispensable for vesicle motility but required for virulence of the maize pathogen Ustilago maydis. Plant Cell, 22, 2476-2494.

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Summary - Filamentous fungi contain a unique chitin synthase (class V) that is fused to a myosin motor head (class XVII myosin) and that is essential for fungal pathogenicity (see above Weber et al. 2006, Plant Cell, 18:225). It was thought that the myosin motor head moves the chitin synthase (and attached chitosomes) towards the growth region. We show in this paper that (a) the myosin motor domain is not involved in chitosome motility and (b) that the chitin synthase domain performs essential roles in masking the invading fungus to avoid the plant defence system (Figure 1).

Schuster, M, Treitschke, S., Molloy, J., Kilaru, S., Harmer, N.J. & Steinberg, G. (2011) Myosin-5, kinesin-1 and myosin-17 cooperate in secretion of fungal chitin synthase. EMBO J., 31, 214-327.

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Summary - This paper builds on the paper by Treitschke et al. (2010, Plant Cell, 22:2476, see above). It addresses (a) the molecular mechanism of chitosomes delivery to the growth region and (b) the precise molecular role of the class XVII myosin motor domain of the class V chitin synthases. We show here that (a) myosin V takes chitosomes along peripheral actin cables towards the growth region, (b) that a second microtubule transport system, involving kinesin-1 and dynein, participates in chitosome delivery, (c) that most secretory chitosomes are moving in a bi-directional fashion and (d) that the class XVII myosin motor domain is needed to tether the vesicles to the apical actin-meshwork, which increases pausing and enhances secretion. This is the first report on the complex motor network involved in membrane trafficking and the first report of the precise function of the pathogenicity-relevant class XVII myosin/class V chitin synthase in filamentous fungi.

Overview article

Steinberg, G. (2011) Motors in fungal morphogenesis: cooperation versus competition. Curr Opin Microbiol, 14, 660-667.

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Histology of plant infection by wildtype U. maydis and mcs1 deletion mutants

Figure 1: Histology of plant infection by wildtype U. maydis and mcs1 deletion mutants. Fungal material is labelled by WGA/AF488 (green), and the plant cell wall is marked with propidium iodide (red). The deletion of the myosin-chitin synthase gene (mcs1) abolishes plant infection and results in swollen hyphae that are attacked by the plant defence system. Figure was modified from Treitschke et al. 2010, Plant Cell, 22:2476.

Delivery mechanism of chitosomes

Figure 2: Delivery mechanism of chitosomes. Microtubules and F-actin cooperate in secretion of chitin synthase-containing secretory vesicles (chitosomes). Myosin-V and kinesin-1 deliver chitosomes, whereas the myosin motor domain of class V chitin synthase (myosin XVII) tethers the arriving vesicle at the site of exocytosis, which primes the vesicle for fusion with the plasma membrane. Note that the majority of the vesicles are not secreted but rather return towards the cell centre, which involves the activity of dynein. Figure modified from Steinberg 2011, Curr. Opin. Microbiol, 14:660.