Self-organized patterning of cell morphology via mechanosensitive feedback.

Natalie A Dye,Romina Piscitello-Gómez,Marko Popović,Suzanne Eaton,Jana F Fuhrmann,K Venkatesan Iyer,Frank Jülicher

doi:10.7554/elife.57964

Abstract

Tissue organization is often characterized by specific patterns of cell morphology. How such patterns emerge in developing tissues is a fundamental open question. Here, we investigate the emergence of tissue-scale patterns of cell shape and mechanical tissue stress in the Drosophila wing imaginal disc during larval development. Using quantitative analysis of the cellular dynamics, we reveal a pattern of radially oriented cell rearrangements that is coupled to the buildup of tangential cell elongation. Developing a laser ablation method, we map tissue stresses and extract key parameters of tissue mechanics. We present a continuum theory showing that this pattern of cell morphology and tissue stress can arise via self-organization of a mechanical feedback that couples cell polarity to active cell rearrangements. The predictions of this model are supported by knockdown of MyoVI, a component of mechanosensitive feedback. Our work reveals a mechanism for the emergence of cellular patterns in morphogenesis.

Highlights

During morphogenesis, tissues with complex morphologies are formed from the collective interplay of many cells
We have shown that patterns of cell shape and stress in the mid-third instar Drosophila wing disc do not rely on PCP pathways or differential growth
We have presented a continuum model of tissue dynamics for this self-organization based on a mechanosensitive nematic cell polarity that accounts for the observed patterns of cell area, T1 transitions, and cell shape

Summary

Introduction

Tissues with complex morphologies are formed from the collective interplay of many cells. Spatial patterns of cell morphology emerge during growth of the Drosophila larval imaginal discs, which are precursors of adult tissues (Aegerter-Wilmsen et al, 2010; Condic et al., 1991; LeGoff et al, 2013; Mao et al, 2013). These patterns have been proposed to be involved in the eversion process, during which these flattened epithelial sacs turn themselves inside out when the animal transitions from larva to pupa (Condic et al, 1991). While extensive work has studied the emergence of biochemical signaling patterns, how patterns of cellular morphology arise during tissue development is poorly understood

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