Out of the Niche: A Bird's-Eye View of the Molecular Networks Controlling Root Stem Cells

Abstract

The capacity of plants to generate new organs and tissues throughout their life cycle depends on the activity of the stem cells contained in meristematic tissues. Plant stem cells are organized in small, clustered populations referred to as stem cell niches. In addition to generating new undifferentiated cells, stem cell niches also provide the positional information that maintains stem cell self-renewal properties and controls the non-cell-autonomous differentiation of surrounding tissues. In this review, we aim to analyze and discuss the most recent literature describing the molecular mechanism controlling the activity and the organization of the stem cell niche in the root of the model plant Arabidopsis thaliana (L.) Heynh. In particular, we will focus on the complex molecular regulatory networks that control the balance between stemness and differentiation in distal stem cells, as well as the maintenance of the mitotically inactive state of the quiescent center.

Keywords: differentiation; distal stem cell; hormones; proliferation; quiescent center; root apical meristem; stem cell niche; transcription factors.

Figure 2

Complex regulation of SCN maintenance. Schematic representation depicting the regulatory links among the main molecular networks governing SCN maintenance and DSC fate. Colored boxes represent specific stem cell compartments to display both cell-autonomous and non-cell-autonomous regulatory steps; see text for details. Blue arrows, positive regulation; black lines, negative regulation; ball-end connectors, protein–protein interactions. Hormone inputs are indicated in red; non-cell-autonomous inputs are depicted with dashed arrows/lines. SI, stele initials; QC, quiescent center; CSC; columella stem cells; CSCD, Columella stem cell daughters.

Figure 1

The SCN in Arabidopsis thaliana. (A) Structure of the SCN, depicted by overlying cell type-specific colors over a Confocal Laser Scanning Microscopy image depicting a propidium iodide-stained meristem from a 5-day-old wild-type root. SI, stele initials; CEI, cortex/endodermis initials; QC, quiescent center; ELI, epidermis/lateral root cap initials; CSC; columella stem cells. (B) Graphical representation of formative divisions and lineages of the root stem cells. Initials are color coded as in (A); daughter cells are depicted in darker tones compared to their respective initials. Dashed lines represent the orientation of cell division planes for each initial. Black dashes, first division plane; red dashes, second division plane in CEI and ELI. The image is a higher magnification detail of (A). (C) Cycles of proliferative (yellow arrows) and differentiative (orange arrows) phases in CSCs displayed in 5-day-old wild-type roots stained with Lugol’s solution and imaged under Nomarski optics upon chloral hydrate clearing. (i) A single layer of CSCs (light green arrowhead) is contained between the QC (yellow arrowhead) and differentiated columella cells (dark green arrowhead); (ii) CSCs start dividing to give rise to CSCDs (asterisk); (iii) when all the columella initials have divided, the formation of a double-layered structure of CSC-like cells can be observed; (iv) CSCDs start differentiating, ultimately restoring the conformation observed in (i). (D) The QC acts as a reservoir of stem cells in cases of extreme differentiation of CSCs. The image shows an RAM where CSC differentiation was induced by altering local auxin gradients with naphtylphtalamic acid treatments (10 μM, 5 days). Notice QC divisions (asterisks) adjacent to differentiated columella cells marked by purple staining of starch granules using Lugol’s solution. Scale bars, 20 μm.