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.