RHO GTPase of Plants contributes to robust establishment of cellular asymmetry during development from a single cell

A fundamental question in developmental biology is how highly complex, yet reproducible multicellular body plans form from a single cell. The multicellular haploid body of the land plant Marchantia polymorpha develops from a single isolated cell – the spore – that divides asymmetrically. This produces a small terminally differentiating basal cell, and a large proliferative apical cell that gives rise to the multicellular sporeling body. The genetic basis for the establishment of asymmetry, first within the spore, and later within the sporeling body has remained virtually unknown. Here, we show that the plant specific RHO-type GTPase – RHO OF PLANTS (ROP) – polarises to the spore basal pole to ensure spore division is highly and reproducibly asymmetric. We demonstrate this highly asymmetric division is necessary to specify the terminal differentiation of the basal cell. Furthermore, we show that ROP-mediated polarised outgrowth is required to establish asymmetry within the sporeling body derived from the apical cell. Our discovery highlights how ROP function confers developmental robustness and contributes to the establishment of asymmetry during plant development from a single isolated cell.