Abstract
Pollen provides an excellent system to study pattern formation at the single-cell level. Pollen surface is covered by the pollen wall exine, whose deposition is excluded from certain surface areas, the apertures, which vary between the species in their numbers, positions, and morphology. What determines aperture patterns is not understood. Arabidopsis thaliana normally develops three apertures, equally spaced along the pollen equator. However, Arabidopsis mutants whose pollen has higher ploidy and larger volume develop four or more apertures. To explore possible mechanisms responsible for aperture patterning, we developed a mathematical model based on the Gierer-Meinhardt system of equations. This model was able to recapitulate aperture patterns observed in the wild-type and higher-ploidy pollen. We then used this model to further explore geometric and kinetic factors that may influence aperture patterns and found that pollen size, as well as certain kinetic parameters, like diffusion and decay of morphogens, could play a role in formation of aperture patterns. In conjunction with mathematical modeling, we also performed a forward genetic screen in Arabidopsis and discovered two mutants with aperture patterns that had not been previously observed in this species but were predicted by our model. The macaron mutant develops a single ring-like aperture, matching the unusual ring-like pattern produced by the model. The doughnut mutant forms two pore-like apertures at the poles of the pollen grain. Further tests on these novel mutants, motivated by the modeling results, suggested the existence of an area of inhibition around apertures that prevents formation of additional apertures in their vicinity. This work demonstrates the ability of the theoretical model to help focus experimental efforts and to provide fundamental insights into an important biological process.
Highlights
The process of cell morphogenesis often depends on the ability of cells to form distinct domains of plasma membrane and precisely target deposition of extracellular materials
One of the most prominent patterns on the pollen surface is formed by apertures, the regions that lack deposition of the pollen wall exine and develop at precise locations which often vary between the species
We developed a mathematical model that aims to explore the mechanisms responsible for the aperture patterning in the pollen of the model plant Arabidopsis
Summary
The process of cell morphogenesis often depends on the ability of cells to form distinct domains of plasma membrane and precisely target deposition of extracellular materials. Pollen grains are surrounded by a complex extracellular structure, exine, that can assemble into thousands of elaborate, species-specific patterns, which make the pollen surface one of the most diverse structures found in nature [1,2,3]. These patterns are formed by precisely depositing exine at certain areas of the pollen surface and by preventing or reducing its deposition at other sites. Apertures are critical for pollen viability and function, as they often serve as portals through which pollen tubes exit during germination and as architectural details that help the pollen accommodate volume changes in response to changing hydration levels [5,6,7,8,9]
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