Shaping the Organ: A Biologist Guide to Quantitative Models of Plant Morphogenesis

Abstract

Organ morphogenesis is the process of shape acquisition initiated with a small reservoir of undifferentiated cells. In plants, morphogenesis is a complex endeavor that comprises a large number of interacting elements, including mechanical stimuli, biochemical signaling, and genetic prerequisites. Because of the large body of data being produced by modern laboratories, solving this complexity requires the application of computational techniques and analyses. In the last two decades, computational models combined with wet-lab experiments have advanced our understanding of plant organ morphogenesis. Here, we provide a comprehensive review of the most important achievements in the field of computational plant morphodynamics. We present a brief history from the earliest attempts to describe plant forms using algorithmic pattern generation to the evolution of quantitative cell-based models fueled by increasing computational power. We then provide an overview of the most common types of “digital plant” paradigms, and demonstrate how models benefit from diverse techniques used to describe cell growth mechanics. Finally, we highlight the development of computational frameworks designed to resolve organ shape complexity through integration of mechanical, biochemical, and genetic cues into a quantitative standardized and user-friendly environment.

A coupled mechano-biochemical model for cell polarity guided anisotropic root growth

“…To model the pure growth mechanics at a single-cell resolution, we used these meshes at the start of each simulation. We implemented the organ growth framework based on Position-based Dynamics (PBD), a modeling technique adapted from computer graphics ( Müller et al, 2007 ; Marconi and Wabnik, 2021a ; Marconi and Wabnik, 2021b , Figure 1—figure supplement 2A ). PBD approximates physical forces using a set of growth constraints ( Müller et al, 2007 ).…”

Stiffness transitions in new walls post-cell division differ between Marchantia polymorpha gemmae and Arabidopsis thaliana leaves

“…When cell divisions follow the shortest path or maximum stress direction, the resulting lower stress in neighboring cells promotes a more uniform growth dynamics. Currently, in studies of plant morphogenesis, cell division is often modeled as the appearance of a new edge with either the same or stiffer properties than the surrounding ones ( 29 , 30 ). This implementation is based on the assumption that cell wall deposition occurs instantaneously and that the new wall will possess the same or stiffer properties as the surrounding ones at the end of the division process.…”

Computer models of cell polarity establishment in plants

“…It is quite possible that each of these models is correct in specific situations and what is needed is a unifying system that averages over those models’ predictions and proposes a comprehensive solution capable of fitting different types of observations from cell polarization events. Computer models have become an indispensable tool for researchers to investigate biological phenomena ( Marconi and Wabnik 2021 ). With the help of additional experimental data and new computer modeling techniques, researchers will have more powerful tools at their disposal to investigate cell polarity and its consequences (see “Outstanding Questions Box”).…”