Abstract
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.
Highlights
The development of an organ from a primordium typically involves two types of processes: increase in cell number through division, and change in tissue shape and size through growth
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
During the first time interval imaged (Fig 1A, 0–14 h), division competence was restricted to the basal half of the leaf, with a distal limit of about 150 μm
Summary
The development of an organ from a primordium typically involves two types of processes: increase in cell number through division, and change in tissue shape and size through growth. How these processes are coordinated in space and time is unclear. Spatiotemporal regulation could act on both growth and division (dual control), with cross talk between them. Distinguishing between these possibilities is challenging because growth and division typically occur in a context in which the tissue is continually deforming. Plant development presents a tractable system for addressing such problems because cell rearrangements make little or no contribution to morphogenesis, simplifying analysis [2]
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