Extracellular ATP Induces Nitric Oxide Production in Tomato Cell Suspensions

Foresi, Noelia; Laxalt, Ana M.; Tonón, Claudia Virginia; Casalongué, Claudia Anahí; Lamattina, Lorenzo

doi:10.1104/pp.107.106518

Cited by 86 publications

(75 citation statements)

References 24 publications

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“…More recently, the plasma membrane NADPH oxidase RBOHC (for respiratory burst oxidase homolog C) was shown to be required for extracellular ATPinduced ROS production in Arabidopsis primary roots (Demidchik et al, 2009). Extracellular ATP also stimulates the production of nitric oxide in tomato (Solanum lycopersicum) culture cells and in Salvia miltiorrhiza hairy roots (Foresi et al, 2007;. These reports suggest that extracellular ATP signals across the plasma membrane by triggering elevation in [Ca 2+ ] cyt , which activates the production of downstream messengers.…”

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confidence: 84%

Extracellular Nucleotides Elicit Cytosolic Free Calcium Oscillations in Arabidopsis

et al. 2010

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Extracellular ATP induces a rise in the level of cytosolic free calcium ([Ca 2+ ] cyt ) in plant cells. To expand our knowledge about the function of extracellular nucleotides in plants, the effects of several nucleotide analogs and pharmacological agents on [Ca 2+ ] cyt changes were studied using transgenic Arabidopsis (Arabidopsis thaliana) expressing aequorin or the fluorescence resonance energy transfer-based Ca 2+ sensor Yellow Cameleon 3.6. Exogenously applied CTP caused elevations in [Ca 2+ ] cyt that displayed distinct time-and dose-dependent kinetics compared with the purine nucleotides ATP and GTP. The inhibitory effects of antagonists of mammalian P2 receptors and calcium influx inhibitors on nucleotide-induced [Ca 2+ ] cyt elevations were distinct between CTP and purine nucleotides. These results suggest that distinct recognition systems may exist for the respective types of nucleotides. Interestingly, a mutant lacking the heterotrimeric G protein Gb-subunit exhibited a remarkably higher [Ca 2+ ] cyt elevation in response to all tested nucleotides in comparison with the wild type. These data suggest a role for Gb in negatively regulating extracellular nucleotide signaling and point to an important role for heterotrimeric G proteins in modulating the cellular effects of extracellular nucleotides. The addition of extracellular nucleotides induced multiple temporal [Ca 2+ ] cyt oscillations, which could be localized to specific root cells. The oscillations were attenuated by a vesicletrafficking inhibitor, indicating that the oscillations likely require ATP release via exocytotic secretion. The results reveal new molecular details concerning extracellular nucleotide signaling in plants and the importance of fine control of extracellular nucleotide levels to mediate specific plant cell responses.The calcium ion, Ca 2+

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confidence: 84%

Extracellular Nucleotides Elicit Cytosolic Free Calcium Oscillations in Arabidopsis

et al. 2010

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“…Several roles have been attributed to extracellular ATP (eATP) and NO in plants, ranging from cell viability to pathogen defence and cell death. [2][3][4] NO production stimulated by eATP was shown in tomato suspension cells, 5 hairy roots of Salvia miltiorrhiza 6 as well as in algae. 7 Reichler et al 8 showed that the intersection of eATP signaling and NO via the cellular messenger cGMP regulates pollen germination and pollen tube growth in Arabidopsis.…”

Section: Linking Signaling Pathways To Gain Understanding On the Regumentioning

confidence: 99%

Extracellular ATP and nitric oxide signaling pathways regulate redox-dependent responses associated to root hair growth in etiolated Arabidopsis seedlings

Terrile

Tonón

Iglesias

et al. 2010

Plant Signaling & Behavior

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Addendum to: Tonón C, Terrile MC, Iglesias MJ, Lamattina L, Casalongué C. Extracellular ATP, nitric oxide and superoxide act coordinately to regulate hypocotyl growth in etiolated Arabidopsis seedlings. J Plant Physiol 2010; 167:540-546; PMID: 19962212; DOI: 10.1016 DOI: 10. /j.jplph.2009. E xtracellular ATP (eATP) and nitric oxide (NO) have emerged as crucial players in plant development, stress responses and cell viability. Glutathione (GSH) is an abundant reducing agent with proposed roles in plant growth, development and stress physiology. In a recent publication, we demonstrated that eATP and NO restore hypocotyl elongation of etiolated Arabidopsis seedlings treated with GSH. Here it is reported that exogenous ATP also restores root hair growth suggesting a role for ATP and NO in the regulation of redox balance associated to specific processes of plant morphogenesis. A tentative model integrating redox-, eATPand NO-signaling pathways during root hair growth in Arabidopsis seedlings is presented. Linking Signaling Pathways to Gain Understanding on the Regulation of Morphological Processes in PlantsThe first living organisms evolved under reducing conditions a long time before the environment became oxidizing due to oxygen produced by photosynthesis. As a consequence, the most fundamental signaling pathways were initially adapted to reducing conditions. Plants, as sessile organisms have taken advantage of the regulatory mechanisms evolved on a changing redox-status and nowadays they are strongly dependent of environmental redox conditions. An efficient redox control together with other signaling mechanisms cooperates to maintain the steady-state redox homeostasis in plant cell. In this scenario, two small signaling molecules such as ATP and NO have a very ancient origin and are involved in cell redox physiology. 1,2 ATP and NO play diverse biological functions in phylogenetically distant species. Intracellular ATP is the major source of energy for cellular reactions. However, ATP also acts as a signaling molecule at the extracellular face of the plasma membrane in animals as well as in plants. 3 NO is an important regulatory molecule in eukaryotes. Several roles have been attributed to extracellular ATP (eATP) and NO in plants, ranging from cell viability to pathogen defence and cell death.2-4 NO production stimulated by eATP was shown in tomato suspension cells, 5 hairy roots of Salvia miltiorrhiza 6 as well as in algae. 7 Reichler et al. 8 showed that the intersection of eATP signaling and NO via the cellular messenger cGMP regulates pollen germination and pollen tube growth in Arabidopsis. Thus, the biochemical and molecular mechanisms underlying eATP and NO signaling pathways in plants have just begun to emerge. Lately, we have described an interconnection between eATP, NO and redox system during hypocotyl elongation in etiolated Arabidopsis seedlings. 9It was demonstrated that a fine-tuning of redox balance and endogenous NO level is associated to eATP action. Therefore, these findings open a new w...

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“…Nitric oxide is now also established as a product of extracellular purine nucleotide perception. Nitric oxide evolution by plants has been observed on application of extracellular ATP or extracellular ADP and linked to influx of Ca 2+ or production of phosphatidic acid (Foresi et al, 2007;Wu and Wu, 2008;Reichler et al, 2009;Clark et al, 2010b;Sueldo et al, 2010;Tonó n et al, 2010).…”

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Receptor-Like Activity Evoked by Extracellular ADP in Arabidopsis Root Epidermal Plasma Membrane

et al. 2011

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Extracellular purine nucleotides are implicated in the control of plant development and stress responses. While extracellular ATP is known to activate transcriptional pathways via plasma membrane (PM) NADPH oxidase and calcium channel activation, very little is known about signal transduction by extracellular ADP. Here, extracellular ADP was found to activate net Ca 2+ influx in roots of Arabidopsis (Arabidopsis thaliana) and transiently elevate cytosolic free Ca 2+ in root epidermal protoplasts. An inward Ca 2+ -permeable conductance in root epidermal PM was activated within 1 s of ADP application and repeated application evoked a smaller current. Such response speed and densitization are consistent with operation of equivalents to animal ionotropic purine receptors, although to date no equivalent genes for such receptors have been identified in higher plants. In contrast to ATP, extracellular ADP did not evoke accumulation of intracellular reactive oxygen species. While high concentrations of ATP caused net Ca 2+ efflux from roots, equivalent concentrations of ADP caused net influx. Overall the results point to a discrete ADP signaling pathway, reliant on receptor-like activity at the PM. Extracellular purine nucleotides have been shown to be involved in the regulation of plant cell viability, membrane permeability, immunity, symbiosis, stress responses, and growth

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Extracellular ATP Induces Nitric Oxide Production in Tomato Cell Suspensions

Cited by 86 publications

References 24 publications

Extracellular Nucleotides Elicit Cytosolic Free Calcium Oscillations in Arabidopsis

Extracellular Nucleotides Elicit Cytosolic Free Calcium Oscillations in Arabidopsis

Extracellular ATP and nitric oxide signaling pathways regulate redox-dependent responses associated to root hair growth in etiolated Arabidopsis seedlings

Receptor-Like Activity Evoked by Extracellular ADP in Arabidopsis Root Epidermal Plasma Membrane

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