Pavement cells and the topology puzzle

Abstract

D'Arcy Thompson emphasised the importance of surface tension as a potential driving force in establishing cell shape and topology within tissues. Leaf epidermal pavement cells grow into jigsaw-piece shapes, highly deviating from such classical forms. We investigate the topology of developing Arabidopsis leaves composed solely of pavement cells. Image analysis of around 50,000 cells reveals a clear and unique topological signature, deviating from previously studied epidermal tissues. This topological distribution is established early during leaf development, already before the typical pavement cell shapes emerge, with topological homeostasis maintained throughout growth and unaltered between division and maturation zones. Simulating graph models, we identify a heuristic cellular division rule that reproduces the observed topology. Our parsimonious model predicts how and when cells effectively place their division plane with respect to their neighbours. We verify the predicted dynamics through in vivo tracking of 800 mitotic events, and conclude that the distinct topology is not a direct consequence of the jigsaw piece-like shape of the cells, but rather owes itself to a strongly life history-driven process, with limited impact from cell-surface mechanics.

Minimisation of surface energy drives apical epithelial organisation and gives rise to Lewis’ law

“…Importantly, the puzzle shape emerges only after cells have stopped dividing and a contiguous lattice with defined neighbour numbers has already formed, which can no longer change because of rigid cell walls [22]. Accordingly, puzzle cells in plants still follow Lewis' law [23].…”

Cellular perspectives for improving mesophyll conductance

“…At the subcellular scale, there has been a focus on lobes as an effective means to increase exposed mesophyll cell area for CO 2 uptake, with a high degree of lobing being linked to high g m (Sage and Sage, ). The formation of lobes in plant cells has been most intensively studied in the leaf epidermis where intricate jig‐saw puzzle forms are common and which, due to their position on the leaf surface, are relatively easy to visualize (Carter et al , ; Sapala et al , ). A series of elegant papers has revealed changes in the cytoskeleton (tubulin/actin) at the neck of lobes, with differential distribution of cell wall epitopes along cell perimeter being produced, which set up local gradients of stress/strain along the cell wall perimeter, resulting in local outgrowth (lobes) (Sampathkumar et al , ).…”

The Receptor Kinase BRI1 promotes cell proliferation in Arabidopsis by phosphorylation- mediated inhibition of the growth repressing peptidase DA1

“…Argon laser excitation wavelength was 514nm and fluorescence emission between 520-600nm was collected. Data was analysed using the Leaf Analysis Toolkit software [51] . Gaussian projection was used on Z-stacks to identify fluorescence from the epidermal layer, to accommodate leaf curvature and to reduce bleed-through from underlying tissues.…”