Pollen grains are known for their impressive variety of species-specific, microscale surface patterning. Despite having similar biological developmental steps, pollen grain surface features are remarkably geometrically varied. Previous work suggests that a physical process may drive this pattern formation and that the observed diversity of patterns can be explained by viewing pollen pattern development as a phase transition to a spatially modulated phase. Several studies have shown that the polysaccharide material of plant cell walls undergoes phase separation in the absence of cross-linking stabilizers of the mixed phase. Here we show experimental evidence that phase separation of the extracellular polysaccharide material (primexine) during pollen cell development leads to a spatially modulated phase. The spatial pattern of this phase-separated primexine is also mechanically coupled to the undulation of the pollen cell membrane. The resulting patterned pools of denser primexine form the negative template of the ultimate sites of sporopollenin deposition, leading to the final micropattern observed in the mature pollen. We then present a general physical model of pattern formation via modulated phases. Using analytical and numerical techniques, we find that most of the pollen micropatterns observed in biological evolution could result from a physical process of modulated phases. However, an analysis of the relative rates of transitions from states that are equilibrated to or from states that are not equilibrated suggests that while equilibrium states of this process have occurred throughout evolutionary history, there has been no particular evolutionary selection for symmetric, equilibrated states.
Publications related to this project:
Radja A, Horsley EM, Lavrentovich MO, and Sweeney AM. (2019). Pollen cell wall patterns form from modulated phases. Cell. In Press.
Lavrentovich MO, Horsley EM, Radja A, Sweeney AM, and Kamien RD. (2016). First-order patterning transitions on a sphere as a route to cell morphology. PNAS. 113 (19) 5189-5194.
Liu JQ, Radja A, Gao Y, Yin R, Sweeney AM, and Yang S. (2020). Mimicry of a biophysical pathway leads to diverse pollen-like surface patterns. PNAS.
Butterfly Wing Scale Formation
It is known that butterfly wings can shed water droplets in a preferred direction, that they are extremely water repellant, and that they use unconventional ways to generate lift and maneuver. In some butterflies, these structures are simultaneously responsible for wing iridescence. Similarly, pollen’s ability to generate lift so it can move from one plant to the next during pollination and its management of wet and dry states are crucial to reproductive success. By studying the development and mechanical origins of these microstructures, we hope to better understand how they generate such properties and to gain insight into control of material microstructure more generally. The morphology of adult wing scales is well-studied but, to date, there is little data regarding the mechanics involved in the genesis of their famous and characteristic microarchitecture. Passive buckling of the developing cuticle leading to microstructural development has been proposed by Ghiradella and Locke; they calculated that cuticulin may buckle with a periodicity similar to that observed for lamellae on ridges, but did not explain other hierarchical aspects of these structures (Ghiradella, 1974). Therefore, the origin of causative mechanical stresses remains poorly described; ultimately these prior models are insufficient to explain the shape and nested hierarchical detail of the mature scales.