Pollen Cell Wall Patterns Form from Modulated Phases

The ornately geometric walls of pollen grains have inspired scientists for decades. We show that the evolved diversity of these patterns is entirely recapitulated by a biophysical model in which an initially uniform polysaccharide layer in the extracellular space, mechanically coupled to the cell membrane, phase separates to a spatially modulated state. Experiments reveal this process occurring in living cells. We observe that in ∼10% of extant species, this phase separation reaches equilibrium during development such that individual pollen grains are identical and perfectly reproducible. About 90% of species undergo an arrest of this process prior to equilibrium such that individual grains are similar but inexact copies. Equilibrium patterns have appeared multiple times during the evolution of seed plants, but selection does not favor these states. This framework for pattern development provides a route to rationalizing the surface textures of other secreted structures, such as cell walls and insect cuticle. [Display omitted] •A single physical theory accounts for pollen cell wall pattern diversity•Pollen patterns form by primexine phase separation coupled to membrane undulations•This process reaches equilibrium in some taxa; most patterns form in kinetic arrest•Arrested patterns evolve more rapidly than equilibrated patterns A biophysical model explains the non-equilibrium phase-separation properties in polysaccharides that form distinct, characteristic patterns on the surface of pollen grains across the diversity of plants.