De novo meristem development in Marchantia polymorpha requires light and an apical auxin signaling minimum

Meristems are generative centers from which the bodies of land plants develop. Marchantia polymorpha spores are single cells formed during meiosis that-upon germination-form an early cell mass on which a flat prothallus develops. A single stem cell niche (meristem) develops de novo at the margin of the prothallus to generate the thallus plant body. Here we show that the prothallus forms at the apical pole of the early cell mass and represses the formation of other prothalli in a light- and auxin-dependent manner. Light is required for prothallus development and the formation of an apical auxin signaling minimum, marked by expression of LOW AUXIN RESPONSIVE (MpLAXR). MpLAXR marks the sporeling apex-the site of organogenesis-and predicts the positioning of the future apical stem cell on the prothallus. Ablation of the dominant prothallus induces the development of a suppressed prothallus in a process comparable to apical dominance. A similar molecular program operates during plant regeneration from a single differentiated thallus cell, which regains stemness (pluripotency) upon surgical isolation from its tissue context, and the isolated cell divides, forming an early cell mass with an MpLAXR-expressing apex where a flat prothallus with a single meristem forms. We conclude that a light-dependent, apical auxin signaling minimum is required for the formation of the prothallus and the de novo development of the first meristem in Marchantia polymorpha.