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Precision positioning with peptides

Nature volume 522, pages 424425 (25 June 2015) | Download Citation

Two related peptides compete for binding to the same receptor to regulate the spacing of cells on the lower surfaces of leaves. This discovery highlights the complexity of cell signalling in plants. See Article p.439

Being fixed in position, plants must be able to respond to a multitude of environmental and developmental inputs over appropriate time frames. To do this, they use organic molecules such as auxin or ethylene, as well as signalling molecules analogous to those used in animals, including peptides (short strings of amino acids) and hormones. But plant peptide signalling pathways, particularly interactions between peptides and their receptor proteins, are poorly understood. In this issue, Lee et al.1 (page 439) define a plant signalling pathway in which two peptides compete for binding to one receptor, exerting opposing effects on the development of tiny openings called stomata on the lower surfaces of leaves.

Stomata regulate the passage of oxygen, carbon dioxide and water vapour in and out of the leaf. These pores are surrounded by two guard cells, which mediate stomatal opening and closing in response to the time of day, to changes in the environment or to physical changes in the plant itself. Guard cells originate from precursors called protodermal cells. Protodermal cells can either proliferate to give rise to pavement cells, which make up the protective epidermis covering the surface of the leaf, or differentiate into a meristemoid mother cell (MMC), a progenitor of the guard cell. MMCs divide asymmetrically, one daughter cell becoming a meristemoid, the other becoming a stomatal-lineage ground cell, a progenitor that can either differentiate into pavement cells or, through a 'spacing division', give rise to a second, satellite meristemoid cell. Meristemoids then undergo asymmetric divisions, and finally differentiate into pairs of guard cells that are evenly distributed between pavement cells (Fig. 1). But what governs these cell-fate decisions?

Figure 1: Orchestrating stomatal development.
Figure 1

During leaf development, most protodermal cells develop into pavement cells, which line the underside of leaves. But a few can undergo differentiation and asymmetric division to form meristemoid cells and stomatal lineage ground cells (SLGCs), which together give rise to the guard cells that enclose stomata — pores on the surface of the leaf. Meristemoids, SLGCs and protodermal cells all express the receptor protein ERECTA (ER). ER activation by the peptide EPF2, which is secreted from cells that have already become meristemoids, suppresses the meristemoid–guard-cell lineage in adjacent cells. By contrast, the peptide Stomagen, which is produced in the overlying mesophyll cell layer, inhibits activation of ER and so promotes guard-cell differentiation. Lee et al.1 report that EPF2 and Stomagen compete for binding to ER, to regulate the even spacing of guard cells between pavement cells.

Mutations in genes encoding receptor proteins of the ERECTA (ER) family cause a loss of control over stomatal spacing, leading to the development of leaves with unevenly spaced stomata. The severity of this trait is further influenced by mutations in an ER co-receptor, TOO MANY MOUTHS (TMM), demonstrating that ER-family signalling is a key regulator of stomatal development. ER-family receptors are activated by EPIDERMAL PATTERNING FACTOR 1 (EPF1) and EPF2, peptides that exert different, but overlapping, effects on stomatal development. By signalling through the receptor ER-LIKE 1 (ERL1), EPF1 orients stomatal spacing and prevents differentiation into guard cells, whereas EPF2–ER signalling restricts the formation of this lineage at an earlier stage. Both receptors exert their effects by activating an intracellular signalling cascade called the MAPK pathway (reviewed in ref. 2).

In contrast to EPF1 and EPF2, the EPF-like peptide Stomagen promotes stomatal development by inducing guard-cell differentiation3. Lee et al. set out to investigate how these related peptides could exert such dramatically opposing effects. The authors found that the altered stomatal differentiation that occurs in plants harbouring mutant forms of the genes encoding ER, ERL1 or TMM was not affected by the addition of Stomagen. This suggests that Stomagen, like EPF1 and EPF2, acts through ER-family receptors.

Lee and colleagues then provided extensive genetic evidence to support this idea. By inhibiting or overexpressing the gene encoding Stomagen, the authors showed that misexpression of the peptide interferes with all signalling pathways mediated by the ER family. Next, using sophisticated genetic and in vitro biochemical experiments, they confirmed that Stomagen actively competes with EPF2 for ER, the two peptides binding to the receptor with similar affinities. Finally, the researchers showed that Stomagen could not activate MAPK signalling. They propose that binding of Stomagen to ER-family receptors actually prevents MAPK signal transduction.

These results provide evidence that a finely balanced system of closely related activating and inhibitory peptides locally modulates the signalling pathways required for proper stomatal spacing in the plant epidermis (Fig. 1). One uncertainty in this model is the similarity in the dissociation constants (a measure of the binding strength between two proteins) of EPF2–ER and Stomagen–ER. This implies that massive changes in the local concentration of one ligand, or a large adjustment in the ligand's local receptor sensitivity, would be needed to induce a change in stomatal patterning. Which mechanism is used in physiological conditions is an issue that clearly needs to be addressed.

A competitive inhibition mechanism provides precise control of cellular spacing, analogous to the 'lateral inhibition' mechanism that regulates the spacing of animal cells. It is now imperative to determine whether similar mechanisms operate over time to generate repetitive differentiation events periodically during plant development. For example, systems such as the CLE40–CLV1–ACR4 signalling pathway, which regulates stem-cell maintenance in the growing tips and roots of plants4, might use a similar combination of activators and inhibitors. Future studies should also analyse whether local changes in the levels of particular peptide combinations could weave a 3D pattern of locally activating and inhibitory signalling conditions.

The results of the current study can be put in the larger context of plant signalling pathways — which includes different combinations of ligands, receptors and co-receptors — acting in conjunction with local changes in signalling pathways mediated by organic molecules. Furthermore, because there is evidence for a direct connection between plant steroid signalling and the stomatal pathway5, yet another level of signalling seems plausible. A picture emerges in which almost every cell in a plant tissue can be exposed to a precisely defined set of signals. This new concept in plant spatial control should now be tested in other settings.

Notes

References

  1. 1.

    et al. Nature 522, 439–443 (2015).

  2. 2.

    & Annu. Rev. Plant Biol. 63, 591–614 (2012).

  3. 3.

    et al. Nature 463, 241–244 (2010).

  4. 4.

    et al. Curr. Biol. 23, 362–371 (2013).

  5. 5.

    et al. Nature Cell Biol. 14, 548–554 (2012).

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  1. Sacco de Vries is in the Department of Biochemistry, Wageningen University, Wageningen 6703 HA, the Netherlands.

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Correspondence to Sacco de Vries.

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https://doi.org/10.1038/nature14535

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