Developmental biology

Roots respond to an inner calling

In plant roots, patterning of two types of water-conducting xylem tissue is determined by a signalling system that involves the reciprocal dance of a mobile transcription factor and mobile microRNAs.

Reciprocal signalling over tissue boundaries is a well-known developmental feature in fruitfly embryos. Surprisingly, a similar mechanism seems to apply in the plant root, as described by Carlsbecker and colleagues on page 316 of this issue1.

In fruitflies, the anterior and posterior parasegments, pre-specified by transcription factors, communicate and stabilize their boundaries using short-range signals carried by Hedgehog and Wingless — small secreted proteins originating from one parasegment and perceived by the neighbouring one. These signals help to consolidate their own expression at boundaries created by earlier patterning systems. Moreover, they create new short-range patterns with the boundary as an 'organizing centre'2. This strategy makes sense in the context of groups of cells that can move relative to one another, and that need to translate positional information encoded in a cell nucleus into cellular positional information — as in the fly embryo.

Carlsbecker et al.1 show that reciprocal signalling operates in the root of the model plant Arabidopsis thaliana, in which, in contrast to animals, cell positions are stable. The authors reveal how a mobile transcription factor and mobile microRNAs perform an intimate reciprocal dance to consolidate cell identities at the boundary between the inner vascular tissue of the plant and the surrounding cell layers.

The vascular tissue of plants consists of branched networks in leaves and separated strands in stems. But in the root, the tissue takes on the relatively simple organization of one central cylinder containing water-conducting xylem elements arranged in arches, which separate the nutrient-conducting phloem elements. The narrow Arabidopsis root has only a single xylem axis in which the conducting cells specialize into central metaxylem (with pitted cell walls) and peripheral protoxylem (with spiral cell walls). It was shown previously that the transcription factor SHORT ROOT (SHR), which is expressed in the central cylinder but is unable to efficiently influence nuclear activity there, travels from cell to cell, ultimately leaving the central cylinder and ending up in the surrounding cell layer3. There, a system that uses the physical partner and downstream target of SHR, SCARECROW (SCR), as well as other proteins, leads to efficient nuclear uptake of SHR and activation of a transcriptional pathway that specifies this cell layer as endodermis4,5,6(Fig. 1a).

Figure 1: Reciprocal signalling across a tissue boundary.
figure1

This side view of concentric tissue layers of a root depicts a two-way signalling mechanism responsible for tissue patterning. a, SHORT ROOT (SHR) transcription factor (red) is synthesized in the central vascular tissue. It moves across the boundary, depicted by thicker lines, to the next layer, where it enters the cell nuclei (red dots) and specifies endodermis identity. b, c, Summary of the results of Carlsbecker and colleagues1. b, Assisted by other proteins, the nuclear SHR activates the transcription of microRNAs (dark green), specifically miR165/6, and their effect spreads, as shown in light green. c, In the vascular tissue, messenger RNA of the PHABULOSA (PHB) transcription factor is downregulated by the microRNAs in a dose-dependent manner: low levels of PHB specify metaxylem (dark blue), and high levels specify protoxylem (light blue).

Carlsbecker et al.1 show that this act of inside-out signalling sets up a signalling pathway targeted outside-in. SHR binds directly to and activates a set of microRNA genes, with the aid of its helper protein SCR, resulting in endodermis-specific production of these small RNAs. Recently, the mobility of a member of an unrelated class of small RNA, known as tasiRNAs, has been implicated in establishing polarity during leaf development, providing a precedent for the involvement of at least one class of mobile small RNA in plant pattern formation7.

Carlsbecker et al. demonstrate that the endodermis-expressed microRNAs act in cells inside this layer to repress the messenger RNA levels of the PHABULOSA (PHB) transcription factor (Fig. 1b). In a series of elegant genetic experiments using mutant plants, they show that PHB and its family members direct xylem development in a dose-dependent fashion, specifying central metaxylem at low levels and peripheral protoxylem at high levels. This is a neat demonstration of the deployment of a two-way signalling system for specifying cell type (Fig. 1c).

A theoretical advantage of two-way signalling systems is that they allow signals to pattern cell types with different affinities across boundaries, hence creating signal gradients with a peak at one end. This 'broken symmetry' around the signalling source is caused by the different pre-patterns around the boundary. In the case of Wingless and Hedgehog in fly embryos, the ability to respond to the signals is confined to different sides of the boundary by differential regulation of the signal-response pathways, determined by pre-patterning factors. In Arabidopsis roots, the response pathway to SHR is constrained by a capture mechanism that is present only in the outer cell layers5,6. In turn, the response pathway to the microRNAs is confined to the inner layers because this is the expression domain of the PHB target and its family members. Again, pre-patterns select the domain of response to be confined to one of two tissue compartments.

In the case of flies, the resulting distribution of signalling molecules can lead to morphogenetic gradients that instruct several cell-fate decisions. The mutant analyses presented by Carlsbecker et al.1 indicate that PHB and related genes are not only required for a binary choice between xylem fates, but have a broader role in the specification of vascular cell identities. Future research should nail down whether the endodermis-derived microRNAs regulate other aspects of vascular differentiation by acting on PHB and related factors through a gradient distribution. Such work may establish whether, in plants, microRNAs can act as bona fide morphogen gradients.

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Scheres, B. Roots respond to an inner calling. Nature 465, 299–300 (2010). https://doi.org/10.1038/465299a

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