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Abstract Highly polarized cotton fibre cells that develop from the seed coat surface are the foundation of a multi-billion-dollar international textile industry. The unicellular trichoblast emerges as a hemispherical bulge that is efficiently converted to a narrower and elongated shape that extends for about 2 weeks before transitioning into a cellulose-generating machine. The polarized elongation phase employs an evolutionarily conserved microtubule-cellulose synthase control module that patterns the cell wall and enables highly anisotropic diffuse growth. As the multi-scale interactions and feedback controls among cytoskeletal systems, morphologically potent cell wall properties, and a changing cell geometry are uncovered, opportunities emerge to engineer architectural traits. However, in cotton, such efforts are hampered by insufficient knowledge about the underlying control mechanisms. For example, fibre diameter is an important trait that is determined during the earliest stages of development, but the basic growth mode and the mechanisms by which cytoskeletal and cell wall systems mediate fibre tapering are not known. This paper combines multiparametric and multiscale fibre phenotyping and finite element computational modelling of a growing cell to discover an evolutionarily conserved tapering mechanism. The actin network interconverts between two distinct longitudinal organizations that broadly distributes organelles and likely enables matrix secretion patterns that maintain cell wall thickness during growth. Based on plausible finite element models and quantitative analyses of the microtubule cytoskeleton, tapering and anisotropic growth is programmed by a constricting apical microtubule depletion zone and highly aligned microtubules along the fibre shaft. The finite element model points to a central role for tensile forces in the cell wall to dictate the densities and orientations of morphologically potent microtubules that pattern the cell wall. 

Abstract Mechanical properties, size and geometry of cells, and internal turgor pressure greatly influence cell morphogenesis. Computational models of cell growth require values for wall elastic modulus and turgor pressure, but very few experiments have been designed to validate the results using measurements that deform the entire thickness of the cell wall. New wall material is synthesized at the inner surface of the cell such that full-thickness deformations are needed to quantify relevant changes associated with cell development. Here, we present an integrated, experimental–computational approach to analyze quantitatively the variation of elastic bending behavior in the primary cell wall of living Arabidopsis (Arabidopsis thaliana) pavement cells and to measure turgor pressure within cells under different osmotic conditions. This approach used laser scanning confocal microscopy to measure the 3D geometry of single pavement cells and indentation experiments to probe the local mechanical responses across the periclinal wall. The experimental results were matched iteratively using a finite element model of the experiment to determine the local mechanical properties and turgor pressure. The resulting modulus distribution along the periclinal wall was nonuniform across the leaf cells studied. These results were consistent with the characteristics of plant cell walls which have a heterogeneous organization. The results and model allowed the magnitude and orientation of cell wall stress to be predicted quantitatively. The methods also serve as a reference for future work to analyze the morphogenetic behaviors of plant cells in terms of the heterogeneity and anisotropy of cell walls.