In developing leaves, the rate and polarity of epidermal cell expansion influences the overall shape of the organ. Antagonistic hormone signaling pathways can either increase or decrease cell expansion rate. The mechanisms by which fields of relatively flat and mechanically-coupled pavement cells morph into lobed and highly interdigitated cells has been analyzed for decades, and the number of proposed explanatory models continues to grow. Here the combined approaches of genetics, multivariate live cell imaging, and finite element (FE) mechanical modeling provided insight into how cellular and biomechanical interactions operate across wide spatial scales to pattern tissue morphogenesis. A small local bias in the persistence of transfacial microtubules templates oriented cellulose synthesis in the tough outer wall. The resulting local bias in wall and growth anisotropy generate nanometer scale shape distortions that initiate lobe formation. Realistic FE models of cell clusters were used to predict subcellular patterns of cell wall mechanical stress. The tensile stress patterns predicted the location, orientation, and persistence of microtubules both at cellular scales and at finer scales that could explain lobe initiation. A cell autonomous cell lobing system was developed to clearly show that wall stress-dependent patterning of microtubules initiates symmetry breaking. These results provide unique insights into the morphogenetic power of subsets of microtubules, and how they respond to mechanical signals that initiate and maintain polarized tissue morphogenesis.
Coauthors: Samuel Belteton – Purdue University;Wenlong LI – U. Nebraska-Lincoln;Makoto Yanagisawa – U. Wisc Madison;Margaret Szymanski – Purdue University;Faezeh Hatam – U. Nebraska-Lincoln;Joseph Turner – U. Nebraska-Lincoln