Minimal vertex model explains how the amnioserosa avoids fluidization during Drosophila dorsal closure

Abstract

Dorsal closure is a process that occurs during embryogenesis of Drosophila melanogaster. During dorsal closure, the amnioserosa (AS), a one-cell thick epithelial tissue that fills the dorsal opening, shrinks as the lateral epidermis sheets converge and eventually merge. During this process, both shape index and aspect ratio of amnioserosa cells increase markedly. The standard 2-dimensional vertex model, which successfully describes tissue sheet mechanics in multiple contexts, would in this case predict that the tissue should fluidize via cell neighbor changes. Surprisingly, however, the amnioserosa remains an elastic solid with no such events. We here present a minimal extension to the vertex model that explains how the amnioserosa can achieve this unexpected behavior. We show that continuous shrinkage of the preferred cell perimeter and cell perimeter polydispersity lead to the retention of the solid state of the amnioserosa. Our model accurately captures measured cell shape and orientation changes and predicts non-monotonic junction tension that we confirm with laser ablation experiments. Significance StatementDuring embryogenesis, cells in tissues can undergo significant shape changes. Many epithelial tissues fluidize, i.e. cells exchange neighbors, when the average cell shape index increases above a threshold value, consistent with the standard vertex model. During dorsal closure in Drosophila melanogaster, however, the amnioserosa tissue remains solid even as the average cell shape index increases well above threshold. We introduce perimeter polydispersity and allow the preferred cell perimeters, usually held fixed in vertex models, to decrease linearly with time as seen experimentally. With these extensions to the standard vertex model, we capture experimental observations quantitatively. Our results demonstrate that vertex models can describe the behavior of the amnioserosa in dorsal closure by allowing normally fixed parameters to vary with time.