Shaping fission yeast with microtubules

Abstract

For cell morphogenesis, the cell must establish distinct spatial domains at specified locations at the cell surface. Here, we review the molecular mechanisms of cell polarity in the fission yeast Schizosaccharomyces pombe. These are simple rod-shaped cells that form cortical domains at cell tips for cell growth and at the cell middle for cytokinesis. In both cases, microtubule-based systems help to shape the cell by breaking symmetry, providing endogenous spatial cues to position these sites. The plus ends of dynamic microtubules deliver polarity factors to the cell tips, leading to local activation of the GTPase cdc42p and the actin assembly machinery. Microtubule bundles contribute to positioning the division plane through the nucleus and the cytokinesis factor mid1p. Recent advances illustrate how the spatial and temporal regulation of cell polarization integrates many elements, including historical landmarks, positive and negative controls, and competition between pathways.

Figure 1.

Cytoskeleton organization during the cell cycle. The cell growth cycle of fission yeast is represented, with sites of active growth labeled by the red lines and arrows. The microtubules (green), actin cytoskeleton (dark red), and sterol-rich membrane domains (light blue) are depicted at representative cell cycle stages. Individual images of these structures are shown at the bottom, where the actin cytoskeleton is stained with phalloidin, microtubules are shown with GFP-atb2, and sterol-rich domains are labeled with filipin.

Figure 2.

Shape mutants. Calcofluor staining showing the normal rod shape of wild-type cells and the aberrant elongated, round, T, curved, and dumpy shapes of cdc2-33, orb6-25, tea1Δ, tip1Δ, and for3Δ cells, respectively. Bar, 5 µm.

Figure 3.

The cdc42p module. Schematic depiction of cdc42p signaling in fission yeast. Active, GTP-bound cdc42p localizes to sites of active growth and to the division site.

Figure 4.

Microtubule-dependent polarization. (A) Model for how the tea1/4p complex is deposited at cell ends by microtubules and recruits the formin for3p for actin cable assembly. These in turn provide tracks for the delivery of myosin V-driven cargoes to cell tips. (B) Microtubule-induced tea1/4p-independent polarization at ectopic cortical sites.

Figure 5.

Positive and negative signals for septum positioning and cell cycle regulation. The medially positioned nucleus provides positive signal for the localization of midsome component mid1p, whereas polarity regulators, including the kinase pom1p, inhibit mid1p localization and septum formation at the tips. Pom1p also negatively regulates the midsome component cdr2p to delay M phase entry until sufficient cell length has been reached.