Contractile actomyosin cables and pulling forces from adjacent tissue cooperate to drive Drosophila germ-band extension.

Abstract

Germ-band extension in Drosophila is a major embryogenesis event, when convergent-extension dramatically reshapes the germ-band. Fluid-like cell motions narrow the germ-band in one direction (dorsal-ventral axis, DV), elongating in the other (anterior-posterior axis, AP). What forces drive germ-band extension? This is controversial. (1) One force is from planar polarized myosin at cell-cell junctions parallel to DV. Blocking myosin activation with optogenetic RhoGAP (optoGAP) activation reduced germ-band elongation ∼1/3 and suppressed cell intercalation (Herrera-Perez et al., 2021). (2) Pulling forces from the invaginating posterior midgut, adjacent to the germ-band posterior end, also contribute. Blocking invagination with the torso mutation reduced germ-band elongation ∼1/3 (Collinet et al., 2015). Further, DV cell elongation is reduced with the torso-like mutation blocking pulling forces (Lye et al., 2015), but little-affected by optoGAP-mediated myosin blocking. Thus, experiment implicates both myosin cables and pulling forces from adjacent tissue, but their contributions and the mechanisms are poorly understood. Here, we developed a biophysical model of Drosophila germ-band extension, with junctional actomyosin contractility, elastic restoring forces, internal viscous forces, extracellular drag, forces from adjacent tissues and cell intercalation (T1 transitions or rosette formation). Our results quantitatively reveal that planar polarized myosin and posterior midgut pulling are driving forces for convergent extension in the DV and AP directions, respectively. Actomyosin cables shrink junctions and intercalate cells, but cannot elongate tissue at wild-type rates, consistent with the phenotype of torso mutants (Collinet et al., 2015). Normal tissue elongation required both myosin cables and posterior midgut pulling, and in simulations with both, the profile of cell lengths reproduced the experimental monotonic increase in the AP direction (Lye et al., 2015). These results suggest convergent extension is cooperatively driven by myosin contractility and active pulling from adjacent tissue.