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How plant cells sense the outside world through hydrogen peroxide

The discovery of a sensor that detects hydrogen peroxide at the surface of a cell provides insights into the mechanisms by which plant cells perceive and respond to environmental stress.
Christine H. Foyer is in the School of Biosciences, College of Life and Environmental Sciences, University of Birmingham, Edgbaston B15 2TT, UK.
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Chemically reactive, oxygen-containing molecules called reactive oxygen species (ROS) are central to cell function. Plant cells generate various ROS, including hydrogen peroxide (H2O2), which has a key role in cell signalling. It is produced in an extracellular space between the plasma membrane and cell wall called the apoplast, in response to a range of factors, including stressors, plant hormones such as abscisic acid, and physical or chemical changes outside the cell1. But whether and how this extracellular H2O2 (eH2O2) is sensed at the cell surface is unknown. Writing in Nature, Wu et al.2 identify the first known cell-surface H2O2 receptor in plants.

The apoplast and cell wall act as a dynamic interface between plant cells and the outside world, with all its threats, challenges and opportunities. Some eH2O2 moves from the apoplast into the cytoplasm through channel proteins called aquaporins3. However, unlike the cytoplasm, the apoplast contains relatively few molecules that counteract oxidation1 — and so ROS, including H2O2, can survive for much longer in the apoplast than in the cytoplasm. This is a compelling reason to suspect that there is a sensor for eH2O2 in the apoplast.

Although little is known about the initial target of eH2O2, the consequences of its production are much better defined4. It is clear that eH2O2 triggers an influx of calcium ions (Ca2+) into the cell, which then leads to the systemic transmission of signals between cells in waves, activating processes such as pathogen resistance or acclimation to stress across the entire plant5. In addition, eH2O2 signals regulate the polarized growth of pollen tubes and root hairs6, and control the opening and closing of stomata3 — pores on the outer layer of the leaf formed by two guard cells. Stomata enable the free passage of molecules such as carbon dioxide and oxygen into the plant when open, and can close to prevent water loss from the plant.

Wu et al. set out to identify cell-surface receptors for eH2O2 that trigger Ca2+ signalling, using a ‘forward’ genetic-screen approach. They treated seeds of the plant Arabidopsis thaliana with a chemical that induces DNA mutations, then screened the resulting plants to identify mutants that showed low Ca2+ influxes in response to H2O2. They named these mutant plants hydrogen-peroxide-induced Ca2+ increases 1 (hpca1).

The authors then identified the HPCA1 protein. They report that HPCA1 is a membrane-spanning enzyme of a protein family known as leucine-rich repeat (LRR) receptor kinases. The group also showed that HPCA1 has two special pairs of cysteine (Cys) amino-acid residues in its extracellular domain. The thiol groups of Cys residues are known7 to be a target for oxidation by H2O2. The authors demonstrate that the presence of eH2O2 leads to oxidation of the extracellular Cys residues of HPCA1 in guard cells. This modification activates HPCA1’s intracellular kinase activity, triggering Ca2+-channel activation and Ca2+ influx, followed by stomatal closure (Fig. 1).

Figure 1 | The HPCA1 protein. Wu et al.2 have identified the first extracellular sensor of hydrogen peroxide (H2O2) in plants, HPCA1. The protein has an intracellular kinase enzyme domain, and an extracellular domain that protrudes into the apoplast — the compartment between a plant cell’s plasma membrane and the cell wall. HPCA1 has two special pairs of cysteine (Cys) amino-acid residues. The authors demonstrate that H2O2 oxidizes thiol groups (not shown) on these residues, forming sulfenic acid (SOH; not shown) and disulfide bonds. This oxidation triggers a conformational change and kinase activity, which, through unknown mechanisms, lead to the opening of calcium-ion (Ca2+) channels and Ca2+ influx into the cell, triggering intrinsic and systemic signalling pathways.

In the absence of eH2O2, the hpca1 seedlings showed no differences from wild-type seedlings. However, their guard cells were less sensitive to eH2O2 than were those of the wild-type seedlings, showing lower than wild-type levels of Ca2+ influx in response to eH2O2. HPCA1 is therefore required to convert the eH2O2 signal into a physiological response. Moreover, the abscisic acid-dependent production of eH2O2 by guard cells was defective in the hpca1 mutants. Of note, the function of HPCA1 in eH2O2 signalling was not limited to guard cells, and the authors provided evidence that eH2O2 signalling helps to transmit environmental signals to the nucleus of various cell types to regulate gene expression.

Oxidation of Cys by H2O2 leads to the formation of a sulfenic acid (SOH), which is at the heart of reduction–oxidation (redox) signalling. Sulfenic acids are rather unstable intermediates that can be further oxidized to sulfinic (SO2H) and sulfonic (SO3H) acid, or can undergo ‘exchange reactions’ to form disulfide bonds. For HPCA1 to function properly as a receptor for eH2O2, the Cys oxidation process must be readily reversible, re-forming thiol residues that can be oxidized again. However, the factors that mediate reduction of the oxidized HPCA1 are unknown. One candidate is a membrane-bound electron-transport system, such as the one that reduces an oxidized form of the antioxidant molecule ascorbic acid in the apoplast8. Membrane-bound and apoplastic thioredoxin-like proteins are also putative candidates, given that thioredoxin is a well-characterized reducing agent for oxidized Cys residues of proteins.

Wu and colleagues have uncovered a receptor-kinase-mediated eH2O2 sensing mechanism that does not resemble any known eH2O2 receptors or sensors reported in other organisms. Nonetheless, HPCA1 might be part of a much wider portfolio of sensors used by plants to perceive and respond to environmental changes through ROS signals. The identification of such receptors has proved challenging, not least because likely candidates are members of very large protein families. Sophisticated screens, such as that used by Wu et al., will be required to tease out the family members that have ROS sensing and signalling roles. Once these sensors have been identified, it should be relatively easy to manipulate their properties to produce model plants and crops that have, for example, increased or depressed sensitivity to environmental H2O2 signals, and so show altered tolerance to environmental threats.

Stomatal closure is not regulated just by H2O2; it is also a response to elevated atmospheric CO2 levels3,9. It will be intriguing to see how proteins such as HPCA1 function in redox signalling networks that are likely to prepare plants for life in a future high-CO2 world. High CO2 levels can stimulate photosynthesis and depress photorespiration; changes in the photosynthesis:respiration ratio have a wide-ranging impact on cellular redox balance, because photorespiration generates a molecule of H2O2 in one organelle, the peroxisome, for every oxygen molecule assimilated in another organelle, the chloroplast, during photosynthesis. Perhaps other H2O2 sensors act together with HPCA1 to transmit organelle-specific redox messages to the nucleus, along with messages from the external face of the plasma membrane.

Nature 578, 518-519 (2020)

doi: 10.1038/d41586-020-00403-y

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