Why plants make puzzle cells, and how their shape emerges

Author:

Sapala Aleksandra1ORCID,Runions Adam12ORCID,Routier-Kierzkowska Anne-Lise1,Das Gupta Mainak13,Hong Lilan45,Hofhuis Hugo1,Verger Stéphane6ORCID,Mosca Gabriella1,Li Chun-Biu7ORCID,Hay Angela1,Hamant Olivier6ORCID,Roeder Adrienne HK45ORCID,Tsiantis Miltos1,Prusinkiewicz Przemyslaw2,Smith Richard S1ORCID

Affiliation:

1. Department of Comparative Development and Genetics, Max Planck Institute for Plant Breeding Research, Cologne, Germany

2. Department of Computer Science, University of Calgary, Calgary, Canada

3. Department of Microbiology and Cell Biology, Indian Institute of Science, Bangalore, India

4. Weill Institute for Cell and Molecular Biology, Cornell University, Ithaca, United States

5. School of Integrative Plant Science, Section of Plant Biology, Cornell University, Ithaca, United States

6. Laboratoire Reproduction et Développement des Plantes, Université de Lyon, ENS de Lyon, UCBL, INRA, CNRS, Lyon, France

7. Department 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.

Funder

Swiss National Science Foundation

Bundesministerium für Bildung und Forschung

Human Frontier Science Program

European Commission

Natural Science and Engineering Research Council of Canada

European Research Council

Max Planck Society

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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