Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells
TL;DR: Activation of Ca2+-permeable channels in the plasma membrane of Arabidopsis guard cells by hydrogen peroxide indicates that ABA-induced H2O2 production and the H 2O 2-activated Ca2-activated channels are important mechanisms for A BA-induced stomatal closing.
Abstract: Drought is a major threat to agricultural production. Plants synthesize the hormone abscisic acid (ABA) in response to drought, triggering a signalling cascade in guard cells that results in stomatal closure, thus reducing water loss. ABA triggers an increase in cytosolic calcium in guard cells ([Ca2+]cyt) that has been proposed to include Ca2+ influx across the plasma membrane. However, direct recordings of Ca2+ currents have been limited and the upstream activation mechanisms of plasma membrane Ca2+ channels remain unknown. Here we report activation of Ca2+-permeable channels in the plasma membrane of Arabidopsis guard cells by hydrogen peroxide. The H2O2-activated Ca2+ channels mediate both influx of Ca2+ in protoplasts and increases in [Ca2+]cyt in intact guard cells. ABA induces the production of H2O2 in guard cells. If H2O2 production is blocked, ABA-induced closure of stomata is inhibited. Moreover, activation of Ca2+ channels by H2O2 and ABA- and H2O2-induced stomatal closing are disrupted in the recessive ABA-insensitive mutant gca2. These data indicate that ABA-induced H2O2 production and the H2O2-activated Ca2+ channels are important mechanisms for ABA-induced stomatal closing.
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TL;DR: The mechanisms of ROS generation and removal in plants during development and under biotic and abiotic stress conditions are described and the possible functions and mechanisms for ROS sensing and signaling in plants are compared with those in animals and yeast.
Abstract: Several reactive oxygen species (ROS) are continuously produced in plants as byproducts of aerobic metabolism. Depending on the nature of the ROS species, some are highly toxic and rapidly detoxified by various cellular enzymatic and nonenzymatic mechanisms. Whereas plants are surfeited with mechanisms to combat increased ROS levels during abiotic stress conditions, in other circumstances plants appear to purposefully generate ROS as signaling molecules to control various processes including pathogen defense, programmed cell death, and stomatal behavior. This review describes the mechanisms of ROS generation and removal in plants during development and under biotic and abiotic stress conditions. New insights into the complexity and roles that ROS play in plants have come from genetic analyses of ROS detoxifying and signaling mutants. Considering recent ROS-induced genome-wide expression analyses, the possible functions and mechanisms for ROS sensing and signaling in plants are compared with those in animals and yeast.
9,908 citations
Cites background from "Calcium channels activated by hydro..."
...ABA-stimulated ROS accumulation induced stomatal closure via activation of plasma membrane calcium channels (99)....
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...In the gca2mutant, ABA increased ROS production, but H 2O2-induced calcium channel activation and stomatal closure were absent in the mutant (99)....
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TL;DR: Key steps of the signal transduction pathway that senses ROIs in plants have been identified and raise several intriguing questions about the relationships between ROI signaling, ROI stress and the production and scavenging ofROIs in the different cellular compartments.
9,395 citations
TL;DR: In Arabidopsis, a network of at least 152 genes is involved in managing the level of ROS, and this network is highly dynamic and redundant, and encodes ROS-scavenging and ROS-producing proteins.
4,902 citations
TL;DR: The generation, sites of production and role of ROS as messenger molecules as well as inducers of oxidative damage are described and the antioxidative defense mechanisms operating in the cells for scavenging of ROS overproduced under various stressful conditions of the environment are described.
Abstract: Reactive oxygen species (ROS) are produced as a normal product of plant cellular metabolism. Various environmental stresses lead to excessive production of ROS causing progressive oxidative damage and ultimately cell death. Despite their destructive activity, they are well-described second messengers in a variety of cellular processes, including conferment of tolerance to various environmental stresses. Whether ROS would serve as signaling molecules or could cause oxidative damage to the tissues depends on the delicate equilibrium between ROS production, and their scavenging. Efficient scavenging of ROS produced during various environmental stresses requires the action of several nonenzymatic as well as enzymatic antioxidants present in the tissues. In this paper, we describe the generation, sites of production and role of ROS as messenger molecules as well as inducers of oxidative damage. Further, the antioxidative defense mechanisms operating in the cells for scavenging of ROS overproduced under various stressful conditions of the environment have been discussed in detail.
4,012 citations
Cites background from "Calcium channels activated by hydro..."
...ABA induced H2O2 is an essential signal in mediating stomatal closure to reduce water loss through the activation of calcium-permeable channels in the plasma membrane [77]....
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...[77] Z....
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TL;DR: Recent advances in elucidating the role of root exudates in interactions between plant roots and other plants, microbes, and nematodes present in the rhizosphere are described.
Abstract: The rhizosphere encompasses the millimeters of soil surrounding a plant root where complex biological and ecological processes occur. This review describes recent advances in elucidating the role of root exudates in interactions between plant roots and other plants, microbes, and nematodes present in the rhizosphere. Evidence indicating that root exudates may take part in the signaling events that initiate the execution of these interactions is also presented. Various positive and negative plant-plant and plant-microbe interactions are highlighted and described from the molecular to the ecosystem scale. Furthermore, methodologies to address these interactions under laboratory conditions are presented.
3,674 citations
References
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01 Jun 1997
TL;DR: Emerging data indicate that the oxidative burst reflects activation of a membrane-bound NADPH oxidase closely resembling that operating in activated neutrophils, which underlies the expression of disease-resistance mechanisms.
Abstract: Rapid generation of superoxide and accumulation of H2O2 is a characteristic early feature of the hypersensitive response following perception of pathogen avirulence signals. Emerging data indicate that the oxidative burst reflects activation of a membrane-bound NADPH oxidase closely resembling that operating in activated neutrophils. The oxidants are not only direct protective agents, but H2O2 also functions as a substrate for oxidative cross-linking in the cell wall, as a threshold trigger for hypersensitive cell death, and as a diffusible signal for induction of cellular protectant genes in surrounding cells. Activation of the oxidative burst is a central component of a highly amplified and integrated signal system, also involving salicylic acid and perturbations of cytosolic Ca2+, which underlies the expression of disease-resistance mechanisms.
3,203 citations
"Calcium channels activated by hydro..." refers background in this paper
...001), indicating that physiological H 2 O 2 concentration...
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TL;DR: It is shown that inoculation of Arabidopsis leaves with avirulent Pseudomonas syringae induces secondary oxidative bursts in discrete cells in distant tissues, leading to low-frequency systemic micro-HRs.
1,129 citations
"Calcium channels activated by hydro..." refers methods in this paper
...To assess whether H 2 O 2 is involved in ABA signalling, we blocked the production of reactive oxygen species (ROS) using diphenylene iodonium chloride (DPI), an inhibitor of NADPH oxidase...
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TL;DR: It is shown here that aequorin can be reconstituted in transformed plants and that it reports calcium changes induced by touch, cold-shock and fungal elicitors, which could be valuable for determining the role of calcium in intracellular signalling processes in plants.
Abstract: Methods for measuring plant cytoplasmic calcium using microelectrodes or microinjected fluorescent dyes are associated with extensive technical problems, so measurements have been limited to single or small groups of cells in tissue strips or protoplasts. Aequorin is a calcium-sensitive luminescent protein from the coelenterate Aequorea victoria (A. forskalea) which is formed from apoaequorin, a polypeptide of relative molecular mass approximately 22,000, and coelenterazine, a hydrophobic luminophore. Microinjected aequorin has been widely used for intracellular calcium measurement in animal cells, but its use in plants has been limited to exceptionally large cells. We show here that aequorin can be reconstituted in transformed plants and that it reports calcium changes induced by touch, cold-shock and fungal elicitors. Reconstituted aequorin is cytoplasmic and nonperturbing; measurements can be made on whole plants and a calcium indicator can be constituted in every viable cell. Now that apoaequorin can be targeted to specific organelles, cells and tissues, with the range of coelenterazines with differing calcium sensitivities and properties available, this new method could be valuable for determining the role of calcium in intracellular signalling processes in plants.
1,114 citations
"Calcium channels activated by hydro..." refers background in this paper
...Note that distinct elicitor-induced [Ca 2+ ] cyt elevation components have been implicated both before and after H 2 O 2 production, indicating that more than one Ca 2+ channel might contribute to this respons...
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TL;DR: Calcium as a Ubiquitous Signal in Plants uses a network of signal transduction pathways to conduct developmental programs, obtain nutrients, control their metabolism, and cope with their environment.
Abstract: ### Calcium as a Ubiquitous Signal in Plants
All living cells use a network of signal transduction pathways to conduct developmental programs, obtain nutrients, control their metabolism, and cope with their environment. A major challenge for cell biologists is to understand the “language” of
973 citations
"Calcium channels activated by hydro..." refers background in this paper
...Together these studies indicate that the H 2 O 2 activation of the plasma membrane Ca 2+ channel characterized here may represent central signalling components in plants, which integrate several stress signal transduction pathways that are known to cause [Ca 2+ ] cyt elevation...
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TL;DR: The cumulative data suggest that systemic wound signals that induce PG activity and H2O2 are widespread in the plant kingdom and that the response may be associated with the defense of plants against both herbivores and pathogens.
Abstract: Hydrogen peroxide (H2O2) generated in response to wounding can be detected at wound sites and in distal leaf veins within 1 hr after wounding. The response is systemic and maximizes at about 4–6 hr in both wounded and unwounded leaves, and then declines. The timing of the response corresponds with an increase in wound-inducible polygalacturonase (PG) mRNA and enzyme activity previously reported, suggesting that oligogalacturonic acid (OGA) fragments produced by PG are triggering the H2O2 response. Systemin, OGA, chitosan, and methyl jasmonate (MJ) all induce the accumulation of H2O2 in leaves. Tomato plants transformed with an antisense prosystemin gene produce neither PG activity or H2O2 in leaves in response to wounding, implicating systemin as a primary wound signal. The antisense plants do produce both PG activity and H2O2 when supplied with systemin, OGA, chitosan, or MJ. A mutant tomato line compromised in the octadecanoid pathway does not exhibit PG activity or H2O2 in response to wounding, systemin, OGA, or chitosan, but does respond to MJ, indicating that the generation of H2O2 requires a functional octadecanoid signaling pathway. Among 18 plant species from six families that were assayed for wound-inducible PG activity and H2O2 generation, 14 species exhibited both wound-inducible PG activity and the generation of H2O2. Four species, all from the Fabaceae family, exhibited little or no wound-inducible PG activity and did not generate H2O2. The time course of wound-inducible PG activity and H2O2 in Arabidopsis thaliana leaves was similar to that found in tomato. The cumulative data suggest that systemic wound signals that induce PG activity and H2O2 are widespread in the plant kingdom and that the response may be associated with the defense of plants against both herbivores and pathogens.
807 citations
"Calcium channels activated by hydro..." refers methods in this paper
...To assess whether H 2 O 2 is involved in ABA signalling, we blocked the production of reactive oxygen species (ROS) using diphenylene iodonium chloride (DPI), an inhibitor of NADPH oxidase...
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