Microtubule-Dependent Confinement of a Cell Signaling and Actin Polymerization Control Module Regulates Polarized Cell Growth

Abstract

Cell types with wildly varying shapes use many of the same signaling and cytoskeletal proteins to dynamically pattern their geometry [1-3]. Plant cells are encased in a tough outer cell wall, and growth patterns are indirectly controlled by the cytoskeleton and its ability to locally specify the material properties of the wall [4, 5]. Broad and non-overlapping domains of actin and microtubules are predicted to create sharp cell-wall boundaries with distinct mechanical properties [6] that are often proposed to direct growth patterns and cell shape [1, 6, 7]. However, mechanisms by which the cytoskeleton is patterned at the spatial and temporal scales that dictate cell morphology are not known. Here, we used combinations of live-cell imaging probes and unique morphology mutants in Arabidopsis to discover how the microtubule and actin systems are spatially coordinated to pattern polarized growth in leaf epidermal cells. The DOCK family guanine nucleotide exchange factor (GEF) SPIKE1 [8, 9] clusters and activates conserved heteromeric WAVE/SCAR and ARP2/3 complexes at the cell apex to generate organized actin networks that define general cytoplasmic flow patterns. Cortical microtubules corral punctate SPIKE1 signaling nodules and restrict actin polymerization within a broad microtubule-depletion zone at the cell apex. Our data provide a useful model for cell-shape control, in which a GEF, actin filament nucleation complexes, microtubules, and the cell wall function as interacting systems that dynamically pattern polarized growth.