Planar polarized force propagation integrates cell behavior with tissue shaping during convergent extension

Abstract

Convergent extension (CE) is an evolutionarily conserved developmental process that elongates tissues and organs via collective cell movements known as cell intercalation. Here, we sought to understand the mechanisms connecting cell behaviors and tissue shaping. We focus on an often-overlooked aspect of cell intercalation, the resolution of 4-cell rosettes. Our data reveal that polarized cellular forces are involved in a timely rosette resolution, which in turn, enables propagation of such cellular forces, facilitating the propagation of tissue-scale CE. Conversely, delayed rosette resolution leads to a subtle but significant change of tissue-wide cell packing and exerts a profound impact by blocking force propagation, resulting in CE propagation defects. Our findings propose a collaborative nature of local cell intercalations in propagating tissue-wide CE. It unveils a multiscale biomechanical synergy underpinning the cellular mechanisms that orchestrate tissue morphogenesis during CE. HighlightsO_LI4-cell rosette is resolved by a two-step process: t-junction extension, then rotation. C_LIO_LIDelayed t-junction rotation significantly impacts the tissue-wide cell packing configuration. C_LIO_LITimely resolved 4-cell rosettes enable polarized force coupling and propagation both in silico and in vivo. C_LIO_LIPolarized force propagation is involved in the propagation of tissue shaping. C_LI