A Case for Distributed Control of Local Stem Cell Behavior in Plants

Abstract

The root meristem has a centrally located group of mitotically quiescent cells, to which current models assign a stem cell organizer function. However, evidence is emerging for decentralized control of stem cell activity, whereby self-renewing behavior emerges from the lack of cell displacement at the border of opposing differentiation gradients. We term this a "stagnation" model due to its reliance on passive mechanics. The position of stem cells is established by two opposing axes that reciprocally control each other's differentiation. Such broad tissue organization programs would allow plants, like some animal systems, to rapidly reconstitute stem cells from non-stem-cell tissues.

Figure 1. Anatomy of the root meristem and stem cell niche

The diagram on the right shows the stereotypical contributions of stem cells, or initials, to specialized cell types, which form cell files in the root. The initials surround and directly contact the QC.

Figure 2. The dual poles controlling differentiation within the distal cells

At the upper position, WOX5 exerts influence from the QC by moving toward the tip and inhibiting differentiation in the CSCs. There, WOX5 recruits co-repressors TOPLESS/TOPLESS-RELATED (TPL/TPR) and HISTONE DEACETYLASE 19 (HDA19) to repress the differentiation-promoting factor, CDF4. At the tipward position of columella cells, CLE40 inhibits WOX5 expression and promotes differentiation through receptor kinases CLAVATA1 (CLV1) and ARABIDOPSIS CRINKLY4 (ACR4).

Figure 3. Mechanisms that mediate long-distance control of growth and differentiation from two opposing signaling domains

The distal axis (QC, columella, and LRC) regulates both cell division and differentiation gradients by long-distance influence (e.g., RGFs and miR396). The proximal axis (radial cell files) has top-down influence, setting the position of the QC, the upper-most cell of the distal axis, through SCR/SHR and ROW1. These factors influence distal axis division and differentiation through QC factors and potentially other long distance mechanisms to affect columella identity (not shown).

Figure 4. Alternative models of stem cell regulation

In a central organizer model, signals from QC regulate stem cell behavior in all cells that contact it by means of a short range signal. In the dual axis model, opposing growth axes, which regulate each other’s division and differentiation gradients, displace their cells in opposite directions. Cells at the border of the opposing growth axes are not displaced by their neighbors whose daughters are pushed out of place in the opposite direction. These border cells behave as stem cells simply because they are not pushed away, a passive mechanism. Such a mechanism can result in bi-directional and radiating growth without a central organizer of division patterns.