A computational framework for 3D mechanical modeling of plant morphogenesis with cellular resolution

PLoS Comput Biol. 2015 Jan 8;11(1):e1003950. doi: 10.1371/journal.pcbi.1003950. eCollection 2015 Jan.

Abstract

The link between genetic regulation and the definition of form and size during morphogenesis remains largely an open question in both plant and animal biology. This is partially due to the complexity of the process, involving extensive molecular networks, multiple feedbacks between different scales of organization and physical forces operating at multiple levels. Here we present a conceptual and modeling framework aimed at generating an integrated understanding of morphogenesis in plants. This framework is based on the biophysical properties of plant cells, which are under high internal turgor pressure, and are prevented from bursting because of the presence of a rigid cell wall. To control cell growth, the underlying molecular networks must interfere locally with the elastic and/or plastic extensibility of this cell wall. We present a model in the form of a three dimensional (3D) virtual tissue, where growth depends on the local modulation of wall mechanical properties and turgor pressure. The model shows how forces generated by turgor-pressure can act both cell autonomously and non-cell autonomously to drive growth in different directions. We use simulations to explore lateral organ formation at the shoot apical meristem. Although different scenarios lead to similar shape changes, they are not equivalent and lead to different, testable predictions regarding the mechanical and geometrical properties of the growing lateral organs. Using flower development as an example, we further show how a limited number of gene activities can explain the complex shape changes that accompany organ outgrowth.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis / growth & development
  • Computational Biology / methods*
  • Computer Simulation
  • Flowers / cytology
  • Flowers / growth & development
  • Models, Biological*
  • Plant Cells / physiology
  • Plant Development / physiology*

Grants and funding

This work was funded by the grants ANR FlowerModel, GeneShape, ANR/BBSRC EraSysBio+ ISam to JC JT CG, Inria Project Lab Morphogenetics to JT CG, European ERCs to JT and AB, ANR Institute of Computational Biology (IBC) to FB, BG and CG. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.