Why plants make puzzle cells, and how their shape emerges

Aleksandra Sapala1 Adam Runions1,2 Anne-Lise Routier-Kierzkowska1 Mainak Das Gupta1,3 Lilan Hong4,5 Hugo Hofhuis1 Stéphane Verger6 Gabriella Mosca1 Chun-Biu Li7 Angela Hay1 Olivier Hamant6 Adrienne HK Roeder4,5 Miltos Tsiantis1 Przemyslaw Prusinkiewicz2 Richard S Smith1
1Department of Comparative Development and Genetics, Max Planck Institute for Plant Breeding Research, Cologne, Germany
2Department of Computer Science, University of Calgary, Calgary, Canada
3Department of Microbiology and Cell Biology, Indian Institute of Science, Bangalore, India
4Weill Institute for Cell and Molecular Biology, Cornell University, Ithaca, United States
5School of Integrative Plant Science, Section of Plant Biology, Cornell University, Ithaca, United States
6Laboratoire Reproduction et Développement des Plantes, Université de Lyon, ENS de Lyon, UCBL, INRA, CNRS, Lyon, France;
7Department of Mathematics, Stockholm University, Stockholm, Sweden

Abstract

The shape and function of plant cells are often highly interdependent. The puzzle-shaped cells that appear in the epidermis of many plants are a striking example of a complex cell shape, however their functional benefit has remained elusive. We propose that these intricate forms provide an effective strategy to reduce mechanical stress in the cell wall of the epidermis. When tissue-level growth is isotropic, we hypothesize that lobes emerge at the cellular level to prevent formation of large isodiametric cells that would bulge under the stress produced by turgor pressure. Data from various plant organs and species support the relationship between lobes and growth isotropy, which we test with mutants where growth direction is perturbed. Using simulation models we show that a mechanism actively regulating cellular stress plausibly reproduces the development of epidermal cell shape. Together, our results suggest that mechanical stress is a key driver of cell-shape morphogenesis.

Reference

Aleksandra Sapala, Adam Runions, Anne-Lise Routier-Kierzkowska, Mainak Das Gupta, Lilan Hong, Hugo Hofhuis, Stéphane Verger, Gabriella Mosca, Chun-Biu Li, Angela Hay, Olivier Hamant, Adrienne HK Roeder, Miltos Tsiantis, Przemyslaw Prusinkiewicz, and Richard S Smith. Why plants make puzzle cells, and how their shape emerges. eLife, 7:e32794, Feb 2018.

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