Divergence of trafficking and polarity mechanisms for PIN auxin transporters during land plant evolution

The phytohormone auxin and its directional transport through tissues play a fundamental role in plant development. This polar auxin transport relies on the PIN auxin exporters, whose polarization at the plasma membrane determines the overall direction of auxin flow. Hence, PIN polarization is crucial for development, but its evolution during the rise of developmental complexity in land plants remains unclear. Here, we investigated the evolution of PIN trafficking and polarization by comparing two model bryophytes, Physcomitrella patens and Marchantia polymorpha, with the angiosperm model Arabidopsis thaliana. All examined PINs show a conserved auxin export function, which is reflected by comparable bryophytic growth defects in overexpression lines. In bryophytes, bryophytic PINs polarize to filamentous apices, while Arabidopsis PINs distribute symmetrically on the membrane with additional intracellular puncta. In the Arabidopsis root epidermis, bryophytic PINs show no defined polarity. Pharmacological interference revealed a strong cytoskeleton dependence of bryophytic but not Arabidopsis PIN polarization, which, in contrast, strongly relies on Brefeldin A-sensitive trafficking. The divergence of PIN polarization and trafficking is also observed within the bryophyte clade and between tissues in individual species. These results collectively reveal a divergence of PIN trafficking and polarity mechanisms throughout land plant evolution and suggest co-evolution of PIN sequence-based and cell-based polarity mechanisms.