Coordinated rearrangements of cytoskeletal structures are the principal source of forces that govern cell and tissue morphogenesis. However, unlike for actin-based mechanical forces, our knowledge about the contribution of forces originating from other cytoskeletal components remains scarce. Here, we establish microtubules as central components of cell mechanics during tissue morphogenesis. We find that individual cells are mechanically autonomous during early Drosophila wing epithelium development. Each cell contains a polarized apical non-centrosomal microtubule cytoskeleton that bears compressive forces, whereby acute elimination of microtubule-based forces leads to cell shortening. We further establish that the Fat planar cell polarity (Ft-PCP) signalling pathway couples microtubules at adherens junctions (AJs) and patterns microtubule-based forces across a tissue via polarized transcellular stability, thus revealing a molecular mechanism bridging single cell and tissue mechanics. Together, these results provide a physical basis to explain how global patterning of microtubules controls cell mechanics to coordinate collective cell behaviour during tissue remodelling. These results also offer alternative paradigms towards the interplay of contractile and protrusive cytoskeletal forces at the single cell and tissue levels.

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Creating ordered structures from chaotic environments is at the core of biological processes at the subcellular, cellular and organismic level. In this perspective, we explore the physical as well as biological features of two prominent concepts driving self-organization, namely phase transition and reaction-diffusion, before closing with a discussion on open questions and future challenges associated with studying self-organizing systems.This article is part of the theme issue 'Self-organization in cell biology'.

Significance Cellular signaling pathways respond to a wide range of stimuli. How signaling circuits are activated without an instructive stimulus and what this is good for are less clear. Combining theoretical and experimental approaches, we show that curvature-sensing proteins stabilize stochastic membrane deformations to nucleate a self-organizing actin-regulatory signaling circuit. In neurons, these signaling hubs control the initiation of exploratory filopodia that sample the cell vicinity for appropriate synaptic partners. The extent and diversity of proteins capable of forming self-organizing circuits at stochastically deformed membranes indicates a general signaling mechanism.

A novel approach based on the convex-hull algorithm is used for parallel analysis of growth dynamics and relative spatiotemporal protein concentration along flexible filopodial protrusions. Testing of filopodia formation in silico, in vitro, and in vivo validates the robustness and sensitivity of the proposed approach.