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Peptide signal alerts plants to drought

It is thought that plants sense water availability in the soil as a way of anticipating drought. The identification of a peptide expressed when water is scarce offers a chance to unravel the underlying molecular mechanism.
Alexander Christmann is in the Department of Plant Sciences, Technical University of Munich, 5354 Freising, Germany.
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Erwin Grill is in the Department of Plant Sciences, Technical University of Munich, 5354 Freising, Germany.
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Because plants cannot move to escape unfavourable conditions, they must continuously monitor environmental cues to survive when conditions change. Plants can sense interactions with other organisms, such as bacteria, and can monitor light conditions across the spectrum, from ultraviolet to far red. The molecular mechanisms that facilitate those capacities are well understood. But how plants sense drought, cold and salt has remained an enigma1. In a paper in Nature, Takahashi et al.2 report the identification of a peptide that is generated in response to a water deficit in plants.

Drought, cold or salty conditions can affect a plant’s water status. Such conditions result in the synthesis3 of the hormone abscisic acid (ABA), which can regulate the plant’s water levels. Stomatal pores in leaves enable plants to take up the carbon dioxide required for photosynthesis, but water vapour can escape through them. ABA can trigger a reduction in how fully stomatal pores are opened4, helping to conserve water.

The molecular basis of the link between water deficit and the induction of ABA synthesis has been a mystery. Using the plant Arabidopsis thaliana as a model system, Takahashi and colleagues investigated whether members of the CLE family of secreted peptides might have a role in this process. There are more than 30 members of this family, and they are generated by an enzyme-mediated cleavage event. These peptides are involved in diverse biological processes5. For example, CLAVATA3 controls the fate of stem cells, and TDIF regulates the formation of the vasculature, the water-transport tissues of plants6.

Takahashi et al. tested 27 CLE peptides for their ability to stimulate ABA synthesis, which is known7 to occur in the vasculature in response to drought. Enzymes called NCEDs cleave a carotenoid precursor molecule in the pathway that gives rise to ABA, and the expression of the gene NCED3 is induced by drought3. The authors administered CLE peptides to the roots of plants, and monitored whether this treatment induced NCED3 in leaves. They found that, at low levels of peptide application, only CLE25 was active in regulating NCED3 expression. CLE25 treatment resulted in an increase in ABA levels and a decrease in stomatal opening. The CLE25 gene was rapidly expressed in roots in response to drought, and CLE25-deficient mutant plants failed to induce NCED3 expression in response to dehydration. The formation of CLE25 in the root or shoot was enough to induce NCED3 in response to dehydration.

The authors tested groups of receptors known to recognize CLE peptides, and identified the receptor proteins BAM1 and BAM3 as being necessary for CLE25-induced responses. A series of grafting experiments clarified how this system works. If roots containing mutations in both the BAM1 and BAM3 genes were grafted to wild-type shoots, the application of CLE25 to the plant’s roots led to NCED3 expression in the shoot. However, if the plant was a graft between wild-type roots and shoots that had mutations in both the BAM1 and BAM3 genes, NCED3 was not expressed in the shoot in response to root application of CLE25.

These results are consistent with a model in which CLE25 expressed in the roots can travel to the leaves and bind to BAM1 or BAM3 (Fig. 1). The authors confirmed this pattern of CLE25 mobility by using a mass-spectrometry technique to identify CLE25 peptides that had travelled from the root to the leaf. Little is known about how CLE peptides travel within the plant, and not all such peptides travel as far as CLE25: CLAVATA3 moves only a few layers of cells8, for example.

Figure 1 | A peptide aids a plant’s response to drought. In drought3, plants generate the hormone ABA, which can help to regulate plant water levels using processes such as the closure of stomatal pores4, through which water escapes from leaves. However, the steps that occur between a plant sensing drought and the production of ABA were previously unknown. Using the plant Arabidopsis thaliana, Takahashi et al.2 report that the peptide CLE25 is activated in response to drought and is a mobile signal, moving from the roots to the leaves. The authors propose BAM1 and BAM3 proteins as receptors for CLE25, and their results indicate that interactions of CLE25 with these receptors leads to expression of the carotenoid-cleaving enzyme NCED3. The action of this enzyme generates an ABA precursor molecule3, which is converted to the active ABA signal, facilitating changes that help the plant to cope with a water shortage.

Takahashi and colleagues’ findings open up potential avenues for determining the long-sought molecular events that occur when a water deficit is initially sensed. The steps leading to CLE25 expression in response to dehydration are unknown, and their discovery would shed light on this matter. And many questions remain about how CLE25 levels are regulated. How does the presumed cleavage of CLE25 occur? Chemical modifications to CLE25, including the hydroxylation of proline amino-acid residues and possibly the addition of sugar groups, might be crucial for its activity5. Whether such modifications are necessary for the function of CLE25 in the drought-sensing process should be investigated.

The molecular mechanism of CLE25 action might be evolutionarily conserved in other plants. The results of Takahashi and colleagues suggest that the CLE25 peptide is generated by the enzymatic cleavage of a precursor protein that generates a 12-amino-acid peptide. In our own analysis of gene sequences, we note that the sequence of this CLE25 peptide in A. thaliana is identical to that of many other species, including beet (Beta vulgaris), poplar (Populus trichocarpa), rice (Oryza sativa) and maize (corn; Zea mays).

Previous analysis9 revealed that water deficit can result in tension in the vasculature that can serve as a signal for ABA induction. Transport of CLE25 from the roots to the leaves is likely to be much slower than the immediate relay of this tension cue. Whether this cue and CLE25 act together or independently needs to be addressed. BAM1 and BAM3 are linked to the maintenance of meristem structures, which contain stem cells, and to vasculature development10. Whether these receptors use the same signalling pathways for those developmental processes as the ones used in this drought response also awaits further analysis.

The authors’ identification of this role for CLE25 provides an intriguing insight into the regulatory interaction network that plants use to optimize their performance and viability under drought conditions. Water deficit is the major limiting factor for crop yields, and an improved understanding of the molecular strategies used by plants to cope with this environmental challenge11 might reveal ways of boosting crop resilience and ensuring stability in the future.

Nature 556, 178-179 (2018)

doi: 10.1038/d41586-018-03872-4

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