Abstract
Growth extent and direction determine cell and whole-organ architecture. How they are spatio-temporally modulated to control size and shape is not well known. Here we tackled this question by studying the effect of brassinosteroid (BR) signalling on the structure of the root meristem. Quantification of the three-dimensional geometry of thousands of individual meristematic cells across different tissue types showed that the modulation of BR signalling yields distinct changes in growth rate and anisotropy, which affects the time that cells spend in the meristem and has a strong impact on the final root form. By contrast, the hormone effect on cell volume was minor, establishing cell volume as invariant to the effect of BR. Thus, BR has the highest effect on cell shape and growth anisotropy, regulating the overall longitudinal and radial growth of the meristem, while maintaining a coherent distribution of cell sizes. Moving from single-cell quantification to the whole organ, we developed a computational model of radial growth. The simulation demonstrates how differential BR-regulated growth between the inner and outer tissues shapes the meristem and thus explains the non-intuitive outcomes of tissue-specific perturbation of BR signalling. The combined experimental data and simulation suggest that the inner and outer tissues have distinct but coordinated roles in growth regulation.
Highlights
Plant morphogenesis is determined by the rate of growth and its directionality[1]
Using the root meristem as the model organ and BR signalling as one of these factors, our work established the key role of BR as a controller of cellular growth directionality from the onset of cell production, while cell volume was still stable
We linked geometry at the cellular scale to radial meristem growth, and we propose a model in which BR signalling controls radial growth via interaction with tissue-specific mechanical constraints
Summary
Understanding morphogenesis control requires a multiscale analysis of the factors involved. We linked geometry at the cellular scale to radial meristem growth, and we propose a model in which BR signalling controls radial growth via interaction with tissue-specific mechanical constraints. The results from the model suggest that the mechanical properties of the different tissues of the root meristem are not uniform, and that the inner and outer tissues must have differential regulation of growth. The short and wide meristem phenotype of bri[1] can be interpreted as a trade-off between longitudinal and radial growth, as observed upon tissue-specific perturbations of BR signalling and as supported by our finding that cell volume is relatively unchanged. Our experimental data and simulation propose a plausible model for how tissue-specific decoding of BR signalling at the cell level drives mechanical changes This probably controls growth anisotropy and shapes the root meristem
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