PerspectivePlant Science

Oscillating Roots

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Science  10 Sep 2010:
Vol. 329, Issue 5997, pp. 1290-1291
DOI: 10.1126/science.1195572

During embryo formation in higher plants, only a rudimentary body forms, consisting of an embryonic root, a stem, and a limited number of leaves. The rest of the plant, including its extensive network of branching roots and stems, is derived from two populations of stem cells at the tips (meristems) of the embryonic root and shoot. The developmental mechanisms that control this branching, however, have been unknown. On page 1306 of this issue, Moreno-Risueno et al. (1) demonstrate that cyclic expression of genes in root meristems can generate the elaborate network of branching roots that anchors the plant and provides it with essential nutrients.

Two possible routes to roots.

Left: Nondifferentiated cells (white) start to oscillate following an internal clock. When the differentiation front (purple) reaches these cells, they stop oscillating. Depending on the phase of the cycle when the cell stops oscillating, it will be competent (red)—capable of forming lateral roots—or not (blue). Right: The same result could be produced if competent cells (red) inhibit newer, adjacent cells from becoming competent. Note: Circles represent in principle groups of cells.

The work of Moreno-Risueno et al. rests on previous observations suggesting that genes in cells close to the meristem show an oscillating sensitivity to the plant hormone auxin and could be involved in determining the locations where roots branch laterally (2, 3). To investigate this idea, they used a promoter, DR5, that appears to be sensitive to auxin levels, with a luciferase gene that “lights up” when activated; this coupling allowed the researchers to detect changes in DR5 activity in real time. They observed that expression of DR5 pulsed rhythmically about every 6 hours in a zone a short distance from the root tip. This activity, however, seems to represent just the tip of an iceberg, as an analysis of gene expression levels in this so-called oscillation zone (OZ) showed massive changes affecting almost 3500 genes that fluctuated in or out of phase with DR5.

The picture that emerges is as follows: As the root meristem continuously produces undifferentiated cells as it grows, the OZ follows behind the tip at a more or less fixed distance. When new cells enter the OZ, the gene network starts to oscillate until the cells exit the zone and enter differentiation. A cell that exits the OZ during a certain phase of the oscillation cycle will be competent, or capable of forming lateral roots.

This scenario, where changes in gene expression depend on the internal “clock” of every cell, is very different from what has been proposed for pattern formation at the shoot meristem. Here, competent cells appear to inhibit branching in adjacent cells. Changes in gene expression at the shoot apex, therefore, seem to depend on signaling between cells. The root scenario, however, is intriguingly similar to the one proposed for the formation of somites (body segments) in vertebrates (4, 5). Cells of the presomitic mesoderm also show oscillating gene expression, involving genes of the Notch and Wnt signaling pathways. These oscillations are translated into spatial arrangements of segment boundaries, through a process implicating a gradient of the growth factor Fgf8, which decreases in more anterior cells where the differentiation process takes place. As growth continues at the tail end of the embryo, cells exit from the anterior end and cease oscillating, probably because the concentration of Fgf8 declines with the increasing distance from the tail bud. Depending on the phase of the oscillation cycle in which the cells become arrested, they switch on different sets of genes, marking them as the front or back end of the next somite. These oscillations are called the clock, and the moving differentiation front is called the wavefront; somite patterning thus depends on a clock-and-wavefront mechanism.

There seems to be, however, an important difference between the animal and plant systems. In a typical vertebrate, an individual cell will go through several oscillations. In a chicken, for instance, certain cells will sense up to 12 fluctuations before differentiation occurs (5). In contrast, the number of oscillations in the OZ of the root seems much more restricted. The study's figure does not provide cellular-level resolution, but known growth dynamics (6) suggest that, in the root, a single cell nucleus (or its descendants) will spend only a couple of hours in the OZ. This implies that it could go through as little as a single fluctuation between entering and leaving the OZ. If this is true, the genetic clock could tick several times in vertebrates, but just once in the root. This single fluctuation could be based on a vertebrate-like clock-and-wavefront system. Other mechanisms, however, could also generate a single fluctuation. For example, a scenario where more mature cells send signals back to cells in the OZ would produce a similar pattern (see the figure). To determine the exact mechanism, it will be important to define the number of oscillations every cell experiences. Because the root is readily accessible, such an analysis at the cellular level should be much easier to achieve than in animal systems.

Another question is whether auxin alone is responsible for the observed oscillations. Although the DR5 promoter is often considered to be a sensor of auxin levels, Moreno-Risueno et al. show that other auxin-responsive genes, such as IAA19, do not fluctuate in a similar manner. This observation implies that the fluctuations in DR5 activity do not necessarily depend on equivalent fluctuations in auxin. Unfortunately, it is currently impossible to visualize auxin directly, so it is difficult to determine to what extent changes in DR5 activity depend on hormone fluctuations alone. The results, however, strongly suggest that the competence to react to auxin is important, as is the cell's final response (7).

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