Divergent evolution of a thermospermine-dependent regulatory pathway in land plants

Abstract

Plants adapted to life on land by developing diverse anatomical features across lineages. The molecular basis of these innovations often involves the emergence of new genes or establishing new connections between conserved elements, though evidence for evolutionary genetic circuit rewiring remains scarce. Here, we show that the thermospermine-dependent pathway regulating vascular cell proliferation in Arabidopsis thaliana operates as two distinct modules with different functions in the bryophyte Marchantia polymorpha. One module controls dichotomous branching at meristems, while the other one modulates gemmae and rhizoid production in the thallus. Heterologous assays and comparative expression analyses reveal that the molecular links between these modules, forming a unified circuit in vascular plants, emerged early in tracheophyte evolution. Our results illustrate how the thermospermine-dependent circuit elements followed two divergent evolutionary trajectories in bryophytes and tracheophytes, eventually influencing distinct developmental processes.