Evolution of moss leaf-like organs through variations in deeply conserved developmental principles

Leaves and leaf-like organs with laminar structures and determinate growth arose multiple times independently in land plants. The cellular basis of leaf development is well characterized in flowering plants, and molecular studies have shown that the plant hormone auxin plays a central role in this process, orchestrating cellular growth and differentiation. Auxin is also crucial for the formation of phyllids, the leaf-like organs of bryophytes, yet its precise role in morphogenesis remains unclear. More broadly, whether similar developmental principles are shared across distantly related evolutionary lineages is unknown. Here, we combine live-imaging, genetics, pharmacological treatments, and modeling to investigate the cellular and molecular basis of phyllid development in the model moss Physcomitrium patens. By tracking phyllid morphogenesis from a single initial cell to full maturity, we uncover the cellular growth dynamics underlying organ development. We demonstrate that auxin spatially inhibits cell divisions and promotes cellular elongation and differentiation. However, unlike in vascular plants, moss PIN transporters do not participate in polar auxin transport during phyllid development but mainly reduce intracellular auxin concentration. These findings indicate that while auxin's role in organogenesis is conserved, its transport mechanisms have diverged across land plants. Overall, our study reveals shared principles of planar organ morphogenesis, highlighting how the repeated deployment of similar developmental strategies, with lineage-specific variations, drove the convergent evolution of leaves and leaf-like organs.