Research Topic C - Endocytosis and early endosome motility
Research articles
Wedlich-Söldner, R., Bölker, M., Kahmann, R. & Steinberg, G. (2000) A putative endosomal t-SNARE links exo- and endocytosis in the phytopathogenic fungus Ustilago maydis. EMBO J. 19, 1974-1986.
Summary - We undertook a genetic screen in order to find proteins required for shaping the cell. We found a SNAP25-like tSNARE, named Yup1, that localizes on the surface of motile early endosomes, where it controls entry into the organelle. Consequently, defects in Yup1 result in a block in later steps of endocytosis, but also morphogenesis, suggesting that endocytic recycling supports hyphal growth. This paper provides first evidence that endocytosis is required for hyphal growth of fungi.
Wedlich-Söldner, R., Straube, A., Friedrich, M.W. & Steinberg, G. (2002) A balance of KIF1A-like kinesin and dynein organizes early endosomes in the fungus Ustilago maydis. EMBO J, 21, 2946-2957.
Summary - Early endosomes move rapidly along microtubules. Motility is driven by a kinesin-3 motor that counteracts cytoplasmic dynein. Bidirectional movements ensure that early endosomes become rearranged during the cell cycle of yeast-like cells, which is a perquisite for an alternating budding pattern at both poles of the elongating cell. This paper demonstrates that kinesin-3 and dynein establish a balance of force in endosome motility.
Lenz, J.H., Straube, A. & Steinberg, G. (2006) A dynein loading zone for retrograde endosome motility at microtubule plus-ends. EMBO J, 25, 2275-2286.
Summary - In hyphae early endosomes reach the growing tip by the transport activity of kinesin-3. Dynein is concentrated at microtubule plus-ends, where it becomes activated when organelles arrive. Early endosomes are loaded onto dynein and are taken back towards subapical parts of the hypha. Kinesin-3 is travelling backwards as passive cargo of dynein, whereas dynein requires kinesin-1 for targeting to plus-ends. These findings led to the concept of an apical dynein loading zone that is established in the hyphal tip in order to ensure that organelles reach the hyphal tip before they reverse direction (Figure 2).
Fuchs, U., Hause, G., Schuchardt I. and Steinberg, G. (2006) Endocytosis is essential for pathogenic development in the corn smut fungus Ustilago maydis. Plant Cell, 18, 2066-2081.
Summary - Making use of a temperature-sensitive Yup1 mutant we demonstrate that endocytosis is essential for several steps during pathogenic development of U. maydis, including cell-cell recognition and spore formation. The defect in early cell-cell recognition is due to a lack of recycling of the pheromone receptor (Figure 1), which results in depletion from the surface and makes the cell 'blind' for the mating pheromone of the partner. This is the first demonstration that endocytosis is essential for fungal pathogenicity; identification of the first molecular cargo for recycling in filamentous fungi.
Overview articles
Steinberg, G. (2007) On the move: Endosomes in fungal growth and pathogenicity. Nat. Rev. Microbiol., 5, 309-316.
Fuchs, U. & Steinberg, G. (2005) Endocytosis in the plant pathogenic fungus Ustilago maydis. Protoplasma, 226, 75-80.
Steinberg, G. & Fuchs, U. (2004) Microtubules in cellular organisation and endocytosis in the plant pathogen Ustilago maydis. J. Microscopy, 214, 114-123.
Figure 1: Pheromone induced a-hyphae that express the pheromone sensing receptor (Pra1) and histone 4 (H4) that labels the nucleus. The receptor is concentrated at the growing tip, but also becomes endocytosed and is sorted to the vacuole. Image provided by U. Fuchs.
Figure 2: Model of the role of kinesin-1, kinesin-3 and dynein in bi-directional transport of early endosomes in U. maydis hyphae. (1) Kinesin-1 is thought to take dynein/dynactin (and maybe Lis1) to the plus-ends in the hyphal tip, where (2) dynein and its activators accumulate until (3) an organelle reaches the tip by the activity of kinesin-3. This is thought to activate dynein (maybe via an unknown Lis1 activator), resulting in retrograde endosome motility. Image modified from Lenz et al. 2006, EMBO J. 25:2275.