Plasticity and robustness of pattern formation in the model diatom Phaeodactylum tricornutum

Abstract

Understanding the morphogenesis of mineralized structures found in shells, bones, teeth, spicules and plant cell walls is difficult because of the complexities underlying biomineralization, and the requirement of accurate models for pattern formation. Here, we investigated the spatial and temporal development of siliceous structures found in a model diatom species, Phaeodactylum tricornutum, for which the entire genome has been sequenced and transformation is routine. Analyses of pattern formation revealed that the process of silicification starts from a 'pi-like' structure that controls the spatial organization of a sternum upon which regular instabilities are initiated and developed. Detailed analyses also demonstrate that morphogenesis of silica is nonuniform. We also tested the sensitivity of pattern formation to perturbation of proton pumps, and found that selective inhibitors of H(+)-V-ATPases affect silica biomineralization both quantitatively and qualitatively. Morphometric analyses of valves purified from isogenic populations of cells show that the morphometric noise of several traits is under exquisite regulation, explaining why the overall valve pattern is reproducibly maintained. Altogether our analyses demonstrate that silica morphogenesis is a robust but nonuniform process, and allow us to propose a model for the dynamic growth of materials within a spatially controlled geometry.