Regional Growth Rate Differences Specified by Apical Notch Activities Regulate Liverwort Thallus Shape

Plants have undergone 470 million years of evolution on land and different groups have distinct body shapes. Liverworts are the most ancient land plant lineage and have a flattened, creeping body (the thallus), which grows from apical cells in an invaginated “notch.” The genetic mechanisms regulating liverwort shape are almost totally unknown, yet they provide a blueprint for the radiation of land plant forms. We have used a combination of live imaging, growth analyses, and computational modeling to determine what regulates liverwort thallus shape in Marchantia polymorpha. We find that the thallus undergoes a stereotypical sequence of shape transitions during the first 2 weeks of growth and that key aspects of global shape depend on regional growth rate differences generated by the coordinated activities of the apical notches. A “notch-drives-growth” model, in which a diffusible morphogen produced at each notch promotes specified isotropic growth, can reproduce the growth rate distributions that generate thallus shape given growth suppression at the apex. However, in surgical experiments, tissue growth persists following notch excision, showing that this model is insufficient to explain thallus growth. In an alternative “notch-pre-patterns-growth” model, a persistently acting growth regulator whose distribution is pre-patterned by the notches can account for the discrepancies between growth dynamics in the notch-drives-growth model and real plants following excision. Our work shows that growth rate heterogeneity is the primary shape determinant in Marchantia polymorpha and suggests that the thallus is likely to have zones with specialized functions.