Role of turgor-pressure induced boundary tension in the maintenance of the shoot apical meristem of Arabidopsis thaliana

Author:

Michael Christian123ORCID,Banwarth-Kuhn Mikahl124,Rodriguez Kevin1567,Ta Calvin-Khang8,Roy-Chowdhury Amit9,Chen Weitao12,Venugopala Reddy G.1567,Alber Mark12ORCID

Affiliation:

1. Interdisciplinary Center for Quantitative Modeling in Biology, University of California, Riverside, CA 92521, USA

2. Department of Mathematics, University of California, Riverside, CA 92521, USA

3. Department of Microbiology and Immunology, University of Michigan, Ann Arbor, MI, 48109, USA

4. Department of Mathematics, Cal State East Bay, Hayward, CA 94542, USA

5. Department of Botany and Plant Sciences, University of California, Riverside, CA 92521, USA

6. Center for Plant Cell Biology, University of California, Riverside, CA 92521, USA

7. Institute for Integrative Genome Biology, University of California, Riverside, CA 92521, USA

8. Department of Computer Science and Engineering, University of California, Riverside, CA 92521, USA

9. Department of Electrical and Computer Engineering, University of California, Riverside, CA 92521, USA

Abstract

In plants, the robust maintenance of tissue structure is crucial to supporting its functionality. The multi-layered shoot apical meristem (SAM) of Arabidopsis, containing stem cells , is an approximately radially symmetric tissue whose shape and structure is maintained throughout the life of the plant. In this paper, a new biologically calibrated pseudo-three-dimensional (P3D) computational model of a longitudinal section of the SAM is developed. It includes anisotropic expansion and division of cells out of the cross-section plane, as well as representation of tension experienced by the SAM epidermis. Results from the experimentally calibrated P3D model provide new insights into maintenance of the structure of the SAM epidermal cell monolayer under tension and quantify dependence of epidermal and subepidermal cell anisotropy on the amount of tension. Moreover, the model simulations revealed that out-of-plane cell growth is important in offsetting cell crowding and regulating mechanical stresses experienced by tunica cells. Predictive model simulations show that tension-determined cell division plane orientation in the apical corpus may be regulating cell and tissue shape distributions needed for maintaining structure of the wild-type SAM. This suggests that cells' responses to local mechanical cues may serve as a mechanism to regulate cell- and tissue-scale patterning.

Funder

National Science Foundation

Publisher

The Royal Society

Subject

Biomedical Engineering,Biochemistry,Biomaterials,Bioengineering,Biophysics,Biotechnology

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