A system-level mechanistic explanation for asymmetric stem cell fates: Arabidopsis thaliana root niche as a study system

Elena R Álvarez-Buylla,Diego Ornelas-Ayala,Adriana Garay-Arroyo,Mónica L García-Gómez,María De La Paz Sánchez,Berenice García-Ponce

doi:10.1038/s41598-020-60251-8

Abstract

Asymmetric divisions maintain long-term stem cell populations while producing new cells that proliferate and then differentiate. Recent reports in animal systems show that divisions of stem cells can be uncoupled from their progeny differentiation, and the outcome of a division could be influenced by microenvironmental signals. But the underlying system-level mechanisms, and whether this dynamics also occur in plant stem cell niches (SCN), remain elusive. This article presents a cell fate regulatory network model that contributes to understanding such mechanism and identify critical cues for cell fate transitions in the root SCN. Novel computational and experimental results show that the transcriptional regulator SHR is critical for the most frequent asymmetric division previously described for quiescent centre stem cells. A multi-scale model of the root tip that simulated each cell’s intracellular regulatory network, and the dynamics of SHR intercellular transport as a cell-cell coupling mechanism, was developed. It revealed that quiescent centre cell divisions produce two identical cells, that may acquire different fates depending on the feedback between SHR’s availability and the state of the regulatory network. Novel experimental data presented here validates our model, which in turn, constitutes the first proposed systemic mechanism for uncoupled SCN cell division and differentiation.

Highlights

Asymmetric divisions maintain long-term stem cell populations while producing new cells that proliferate and differentiate
In this article we hypothesize that a mechanism like this is behind the asymmetric divisions at the root stem cell niche (SCN) of Arabidopsis thaliana (“Arabidopsis” )
We used a complex-systems approach to identify the signals that could be critical for the asymmetric SC divisions in the root stem cell niches (SCN), and studied the cell-fate decisions during SC divisions as a dynamic process resulting from the feedback between the intracellular regulatory network underlying cell fate and an extracellular signal that reshapes the attractor landscape, and cell fate

Summary

Introduction

Asymmetric divisions maintain long-term stem cell populations while producing new cells that proliferate and differentiate. We used a complex-systems approach to identify the signals that could be critical for the asymmetric SC divisions in the root SCN, and studied the cell-fate decisions during SC divisions as a dynamic process resulting from the feedback between the intracellular regulatory network underlying cell fate and an extracellular signal that reshapes the attractor landscape, and cell fate. It is reasonable to think that the spatial context in which the QC progeny is found after a periclinal division could be providing molecular cues that guide their posterior fate: to remain as a QC cell or to differentiate into one of the initial cells To identify such signals we used an updated version of a published mathematical model of the gene regulatory network underlying cell fate decisions at the root SCN (Fig. 1c)[53]. Our computational analysis predicted that variations in the activity of SHORTROOT (SHR) within the daughter cells of a QC cell division could explain the biased production of columella initials

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