Mitotic shape changes drive spatiotemporally segregated cell-contact rearrangements in a proliferating epithelium

In animals, epithelial tissue morphology is determined by the shape, position, and number of its component cells. Nevertheless, it remains incompletely understood how the shape transformations that accompany epithelial mitosis influence tissue packing. Combining an in silico vertex model with live imaging of murine intestinal organoids, we show that mitotic shape changes drive a spatiotemporally segregated sequence of cell-contact rearrangements: basal diminution of mitotic cells, transient multicellular rosette assembly, and reinsertion of the daughter cells. Strikingly, the reinsertion is accompanied by neighbor exchanges oriented perpendicular to the daughter-daughter contact in silico and in organoids, which indicates that reinsertion geometry is sufficient to set the direction of rearrangement. Pharmacological arrest of mitotic progression reveals that basal diminution and daughter reinsertion independently drive distinct contact rearrangements. Together, our results establish that two distinct geometric asymmetries of mitosis, the apico-basal diminution of the dividing cell and the in-plane anisotropy of daughter reinsertion, drive a program of cell rearrangement that reorganizes basal cell-contact topology, thus providing an intrinsic route by which proliferating epithelia accommodate new cells.