Lessons from sporeling development: How to form plant organs and meristems de novo?

Abstract

Marchantia polymorpha develops from unicellular spores in isolation from the parental plant, which allows all stages of development to be observed. We discovered that the Marchantia spore undergoes reproducibly oriented cell divisions to form the first meristem from which the photosynthetically active and flat thallus plant body develops. The initial division of the spore is asymmetric: one daughter cell forms a differentiated rhizoid while the other proliferates into an early cell mass. An auxin minimum is established in a light-dependent manner at the apical pole of the early cell mass to induce organogenesis of the first flat body structure – the prothallus. Prothallus development starts with a formative division at the apical pole that generates the prothalloblast. Symmetric division of the prothalloblast followed by two transverse divisions form a four-celled plate. One quadrant of the plate gives rise to a flat flabellum. An apical stem cell is specified by a local auxin minimum at the mid-flabellum margin and forms the centre of the first meristem. The transcription factor Class III HD-Zip (MpC3HDZ) polarises to the dorsal side of the developing prothallus. Mpc3hdz mutants are defective in setting up dorsoventrality and grow radialized thalli. Using proximity labelling, we identified the first potential MpC3HDZ dimerization partners, which will help to discover the molecular networks of dorsoventral thallus development. In summary, we report that light and an apical auxin signalling minimum are required to initiate prothallus development in five consecutive stages, ultimately forming the first flat body structure and meristem de novo.

References

Wallner ES, Edelbacher N, Dolan L; De novo meristem development in Marchantia requires light and an apical auxin signaling minimum. Current Biology (2025), doi: 10.1016/j.cub.2025.11.016

Wallner ES, Dolan L; Reproducibly oriented cell divisions pattern the prothallus to set up dorsoventrality and de novo meristem formation in Marchantia polymorpha. Current Biology (2024), doi: 10.1016/j.cub.2024.07.099

Specer V, Wallner ES, Jandrasits K, Edelbacher N, Mosiolek M, Dolan L; The three-dimensional anatomy and dorsoventral asymmetry of the mature Marchantia polymorpha meristem develops from a symmetrical gemma meristem. Development (2024), doi: 10.1242/dev.204349