Spatiotemporal coordination of cell division and growth during organ morphogenesis

Fox, Samantha; Southam, Paul; Pantin, Florent; Kennaway, Richard; Robinson, Sarah Jane; Castorina, Giulia; Sánchez-Corrales, Yara E.; Sablowski, Robert; Chan, Jordi; Grieneisen, Verônica; Marée, Athanasius F. M.; Bangham, J. Andrew; Coen, Enrico (2018). Spatiotemporal coordination of cell division and growth during organ morphogenesis. PLoS biology, 16(11), e2005952. Public Library of Science 10.1371/journal.pbio.2005952

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A developing plant organ exhibits complex spatiotemporal patterns of growth, cell division, cell size, cell shape, and organ shape. Explaining these patterns presents a challenge because of their dynamics and cross-correlations, which can make it difficult to disentangle causes from effects. To address these problems, we used live imaging to determine the spatiotemporal patterns of leaf growth and division in different genetic and tissue contexts. In the simplifying background of the speechless (spch) mutant, which lacks stomatal lineages, the epidermal cell layer exhibits defined patterns of division, cell size, cell shape, and growth along the proximodistal and mediolateral axes. The patterns and correlations are distinctive from those observed in the connected subepidermal layer and also different from the epidermal layer of wild type. Through computational modelling we show that the results can be accounted for by a dual control model in which spatiotemporal control operates on both growth and cell division, with cross-connections between them. The interactions between resulting growth and division patterns lead to a dynamic distributions of cell sizes and shapes within a deforming leaf. By modulating parameters of the model, we illustrate how phenotypes with correlated changes in cell size, cell number, and organ size may be generated. The model thus provides an integrated view of growth and division that can act as a framework for further experimental study.

Author summary
Organ morphogenesis involves two coordinated processes: growth of tissue and increase in cell number through cell division. Both processes have been analysed individually in many systems and shown to exhibit complex patterns in space and time. However, it is unclear how these patterns of growth and cell division are coordinated in a growing leaf that is undergoing shape changes. We have addressed this problem using live imaging to track growth and cell division in the developing leaf of the mustard plant Arabidopsis thaliana. Using subsequent computational modelling, we propose an integrated model of leaf growth and cell division, which generates dynamic distributions of cell size and shape in different tissue layers, closely matching those observed experimentally. A key aspect of the model is dual control of spatiotemporal patterns of growth and cell division parameters. By modulating parameters in the model, we illustrate how phenotypes may correlate with changes in cell size, cell number, and organ size.

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