Mechanical competition alters the cellular interpretation of an endogenous genetic program

Abstract

The intrinsic genetic program of a cell is not sufficient to explain all of the cell’s activities. External mechanical stimuli are increasingly recognized as determinants of cell behavior. In the epithelial folding event that constitutes the beginning of gastrulation in Drosophila, the genetic program of the future mesoderm leads to the establishment of a contractile actomyosin network that triggers apical constriction of cells and thereby tissue folding. However, some cells do not constrict but instead stretch, even though they share the same genetic program as their constricting neighbors. We show here that tissue-wide interactions force these cells to expand even when an otherwise sufficient amount of apical, active actomyosin is present. Models based on contractile forces and linear stress–strain responses do not reproduce experimental observations, but simulations in which cells behave as ductile materials with nonlinear mechanical properties do. Our models show that this behavior is a general emergent property of actomyosin networks in a supracellular context, in accordance with our experimental observations of actin reorganization within stretching cells.

Embryo-scale epithelial buckling forms a propagating furrow that initiates gastrulation

“…1 g). This corroborates previous experimental evidence and quantitative analysis showing that cells further away from the midline increase their surface area during furrow formation 4 , 10 , 33 , 58 , 61 , 62 . This spatial strain pattern is reproduced by our computational model (Fig.…”

Generation and timing of graded responses to morphogen gradients

“…When most of the transcription sites in the ventral region are triggered over time, the differences in mRNA production diminish. Indeed, monitoring apical Myosin II recruitment showed that lateral mesodermal cells eventually recruit similar levels to the ventral-most cells ( Bhide et al, 2021 ). For optimal function, the probability of transcription activation should be high enough to prime a significant number of TSs and yet not plateau within the critical time window.…”

High-resolution line-scan Brillouin microscopy for live-imaging of mechanical properties during embryo development

“…2a-b,e-f ). During early VFF, cells with mesodermal fate (marked by the expression of the transcription factor Snail) located on the ventral side of the embryo undergo complex changes in cell geometry that will enable the complete invagination of these cells in ~15min 28 ( Fig. 2a,b ).…”