A nuclear jamming transition in vertebrate organogenesis

Abstract

Jamming of cell collectives and associated rigidity transitions have been shown to play a key role in tissue dynamics, structure and morphogenesis. In cellular jamming, the physical state of the tissue is controlled by cellular density and the mechanics of cell-cell contacts. A potential contribution of subcellular organelles to the emergent tissue mechanics and architecture, as well as in the control of rigidity transitions, has not been explored. Here we show the existence of a nuclear jamming transition in which jamming of nuclei constrains cell movements beyond cellular jamming, with physical interactions between nuclei controlling the emergent physical properties and architecture of the tissue. We develop a computational framework and show that nuclear volume fraction and nuclear anisotropy are key parameters to understand the emergent tissue physical state. Analysis of tissue architecture during eye and brain development in zebrafish shows that these tissues undergo a nuclear jamming transition as they form, with increasing nuclear packing leading to more ordered cellular arrangements, reminiscent of the crystalline cellular packings in the functional adult eye. Our results reveal a novel rigidity transition associated with nuclear jamming, and highlight an important role for the nucleus in the control of emergent tissue mechanics and architecture.