A coupled mechano-biochemical framework for root meristem morphogenesis

Abstract

Understanding how an independent organ develops from the stem cell populations in the process called morphogenesis is a pressing challenge in developmental biology and medicine. Plants build up new organs such as roots to adjust their bodies to dynamic changes in the environment, thereby providing a tractable model to address this challenge. Here, we combined empirical data with advanced computer modeling techniques to build a mechanistic cell-based framework for the morphogenesis of the plant root. Our framework relies on experimentally supported design principles underlying the multi-layered feedback between tissue mechanics, cell growth, and directional cell-to-cell transport of growth regulator auxin. Model simulations reconstruct experimentally-observed patterns of anisotropic growth, auxin distribution, and cell polarity, as well as several root phenotypes caused by chemical, mechanical, or genetic perturbations. Furthermore, our model provides new insights into mechanisms of sustained root growth and cell polarity establishment. This work reveals that mobile auxin signal feeds back on cell polarity and growth mechanics to instruct the morphogenesis of an independent organ.

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

“…It has been shown that cortical microtubules align with maximal tensile stress in plant tissues ( Hamant et al, 2019 ), indicating the existence of a feedback loop which reinforces the cell anisotropy against principal stress directions ( Figure 1A ). Surprisingly, it has been suggested that even isotropic growth could generate anisotropic patterns as a result of differential growth rates between adjacent tissues ( Kennaway et al, 2011 ; Marconi et al, 2021 ). Other studies have also hypothesized the existence of morphogen-driven growth polarity fields ( Mansfield et al, 2018 ).…”

“…The marginal patterning of the leaf blade is the result of the combined action of a local growth activator (red) and a growth suppressor (blue). (C) Computational model of radicle emergence (adapted from Marconi et al, 2021 ). This simulation reproduces the embryonic emergence of the root meristem of Arabidopsis .…”

“…Organ growth follows the combined action of cell elongation, cell division, and tissue mechanics. Note that the organ maintains a distinct anisotropic form through the self-organization of cortical microtubules despite each single cell being expanded by uniform turgor pressure (see Marconi et al, 2021 for details).…”

“…Root growth is regulated by auxin which flows through the inner tissues toward the tip, where it accumulates creating a maximum, and it is later refluxed back through the outer tissues ( Kepinski and Leyser, 2005 ). The mechanisms behind root growth have been studied and tested in-silico using several computational models ( Grieneisen et al, 2007 ; Fozard et al, 2013 ; Bassel et al, 2014 ; Jensen and Fozard, 2015 ; Marconi et al, 2021 ).…”

“…At the same time, using the cell complex it was possible to recreate the complete 4D map of early Arabidopsis embryo development including all successive cell division events ( Yoshida et al, 2014 ). Similarly, the cell complex was chosen as the base structure for the simulation of root emergence and development in a comprehensive model combining mechanical and biochemical signals ( Marconi et al, 2021 ).…”