Lateral inhibition governs ancestral cellular patterning in fossil and extant liverworts.

The incompleteness of the fossil record and the absence of genetic information limit our ability to understand ancient developmental processes and reconstruct their evolution. Gene expression patterns, physiological pathways, or cellular differentiation processes are rarely preserved, leaving major gaps in our understanding of developmental evolution. Here, we combine comparative and mathematical analyses to uncover an ancestral patterning mechanism underlying the specification of liverwort oil body cells, a synapomorphy of the lineage involved in anti-herbivory defense. We demonstrate that oil body cell homologs in fossils of the oldest known liverwort (Metzgeriothallus sharonae) exhibit spatial organization characteristic of lateral inhibition, including regular spacing and an over-representation of idioblasts. We show that a mechanism involving local activation and lateral inhibition reproduces the diversity of patterns observed in the fossils. Finally, we find that the same mechanism can explain oil body cell patterns in the distantly related liverworts Treubia lacunosa, Apotreubia nana, and Marchantia polymorpha, suggesting a deeply conserved mode of cell specification. Our findings illuminate the origin and diversification of oil body cells, underscoring their evolutionary significance for liverwort development and survival.