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Plant responses to extracellular nucleotides: Cellular processes and biological effects.

Jeter CR, Roux SJ - Purinergic Signal. (2006)

Bottom Line: Extracellular ATP can also induce the production of reactive oxygen species and stimulate an increase in the mRNA levels of a number of stress- and calcium-regulated genes, suggesting a role for nucleotide-based signaling in plant wound and defense responses.Furthermore, the growth and development of plants can also be altered by the application of external ATP.Recent studies are only beginning to uncover the complexities of plant signaling networks activated in response to extracellular ATP and how these might interact to affect plant physiological processes.

View Article: PubMed Central - PubMed

Affiliation: Science Park-Research Division, Department of Carcinogenesis, The University of Texas MD Anderson Cancer Center, Smithville, TX, 78957, USA.

ABSTRACT
Higher plants exhibit cellular responsiveness to the exogenous application of purine nucleotides in a manner consistent with a cell-cell signaling function for these molecules. Like animals, plants respond to extracellular ATP, ADP, and stable analogues (e.g., ATPgammaS and ADPbetaS) by increasing the cytoplasmic concentration of calcium. Agonist substrate specificity and concentration dependency suggest receptor mediation of these events, and, although the identity of the plant receptor is currently unknown, pharmacological analysis points to the involvement of a plasma membrane-localized calcium channel. Extracellular ATP can also induce the production of reactive oxygen species and stimulate an increase in the mRNA levels of a number of stress- and calcium-regulated genes, suggesting a role for nucleotide-based signaling in plant wound and defense responses. Furthermore, the growth and development of plants can also be altered by the application of external ATP. Recent studies are only beginning to uncover the complexities of plant signaling networks activated in response to extracellular ATP and how these might interact to affect plant physiological processes.

No MeSH data available.


Transgenic apo-aequorin-expressing Arabidopsis display calcium transients in response to exogenously applied ATP. A Typical response of excised roots to 3 µM ATP, measured in a recording solution containing either 10 or 0.1 mM CaCl2, 2 mM MES, pH 5.7 and 4 µg/ml of the coelenterazine luminophore cofactor. B Typical response of whole seedlings to 500 µM ATP, 50 mM MES (buffer only), and 0.666 M mannitol. R indicates resting calcium levels. (From Demidchik et al. [27] and Jeter et al. [29].)
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Fig1: Transgenic apo-aequorin-expressing Arabidopsis display calcium transients in response to exogenously applied ATP. A Typical response of excised roots to 3 µM ATP, measured in a recording solution containing either 10 or 0.1 mM CaCl2, 2 mM MES, pH 5.7 and 4 µg/ml of the coelenterazine luminophore cofactor. B Typical response of whole seedlings to 500 µM ATP, 50 mM MES (buffer only), and 0.666 M mannitol. R indicates resting calcium levels. (From Demidchik et al. [27] and Jeter et al. [29].)

Mentions: To further evaluate the extracellular signaling activities of nucleotide derivatives, two independent studies utilizing aequorin-expressing Arabidopsis were performed nearly in parallel, one focusing on roots [27] and the other on whole seedlings [28, 29]. These results have verified that exogenous application of either ATP, ADP, or, importantly, a variety of poorly hydrolysable stable analogs can indeed significantly increase the [Ca2+] in plant cells. Demidchik et al. [27] utilized excised roots from adult plants bathed in a recording solution containing 10 mM CaCl2, 2 mM MES and Tris buffered to pH 5.7 and nicely demonstrated the induction of a strong calcium transient (up to µM levels, compared to resting levels of approximately 100 nM) in response to agonist concentrations ranging from µM to mM (Figure 1A). They also documented the substrate specificity of the response (e.g., the application of UTP had minimal effects, and AMP was ineffective). Furthermore, in spite of the heterogenous nature of the tissue responding, the plotted response curves revealed dose-dependency and an apparent saturation of the response, suggesting receptor mediation [27]. Pharmacological analysis with potential antagonists also showed that the response was sensitive to the calcium channel blocker gadolinium (Gd3+), as well as the P2-receptor antagonists suramin and PPADS (pyridoxal phosphate-6-azo-(benzene-2,4-disulfonic acid)) (Figure 2A). The authors interpreted these effects as being consistent with an influx of calcium from the plant ECM through a channel in the plasma membrane.Figure 1


Plant responses to extracellular nucleotides: Cellular processes and biological effects.

Jeter CR, Roux SJ - Purinergic Signal. (2006)

Transgenic apo-aequorin-expressing Arabidopsis display calcium transients in response to exogenously applied ATP. A Typical response of excised roots to 3 µM ATP, measured in a recording solution containing either 10 or 0.1 mM CaCl2, 2 mM MES, pH 5.7 and 4 µg/ml of the coelenterazine luminophore cofactor. B Typical response of whole seedlings to 500 µM ATP, 50 mM MES (buffer only), and 0.666 M mannitol. R indicates resting calcium levels. (From Demidchik et al. [27] and Jeter et al. [29].)
© Copyright Policy
Related In: Results  -  Collection

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Fig1: Transgenic apo-aequorin-expressing Arabidopsis display calcium transients in response to exogenously applied ATP. A Typical response of excised roots to 3 µM ATP, measured in a recording solution containing either 10 or 0.1 mM CaCl2, 2 mM MES, pH 5.7 and 4 µg/ml of the coelenterazine luminophore cofactor. B Typical response of whole seedlings to 500 µM ATP, 50 mM MES (buffer only), and 0.666 M mannitol. R indicates resting calcium levels. (From Demidchik et al. [27] and Jeter et al. [29].)
Mentions: To further evaluate the extracellular signaling activities of nucleotide derivatives, two independent studies utilizing aequorin-expressing Arabidopsis were performed nearly in parallel, one focusing on roots [27] and the other on whole seedlings [28, 29]. These results have verified that exogenous application of either ATP, ADP, or, importantly, a variety of poorly hydrolysable stable analogs can indeed significantly increase the [Ca2+] in plant cells. Demidchik et al. [27] utilized excised roots from adult plants bathed in a recording solution containing 10 mM CaCl2, 2 mM MES and Tris buffered to pH 5.7 and nicely demonstrated the induction of a strong calcium transient (up to µM levels, compared to resting levels of approximately 100 nM) in response to agonist concentrations ranging from µM to mM (Figure 1A). They also documented the substrate specificity of the response (e.g., the application of UTP had minimal effects, and AMP was ineffective). Furthermore, in spite of the heterogenous nature of the tissue responding, the plotted response curves revealed dose-dependency and an apparent saturation of the response, suggesting receptor mediation [27]. Pharmacological analysis with potential antagonists also showed that the response was sensitive to the calcium channel blocker gadolinium (Gd3+), as well as the P2-receptor antagonists suramin and PPADS (pyridoxal phosphate-6-azo-(benzene-2,4-disulfonic acid)) (Figure 2A). The authors interpreted these effects as being consistent with an influx of calcium from the plant ECM through a channel in the plasma membrane.Figure 1

Bottom Line: Extracellular ATP can also induce the production of reactive oxygen species and stimulate an increase in the mRNA levels of a number of stress- and calcium-regulated genes, suggesting a role for nucleotide-based signaling in plant wound and defense responses.Furthermore, the growth and development of plants can also be altered by the application of external ATP.Recent studies are only beginning to uncover the complexities of plant signaling networks activated in response to extracellular ATP and how these might interact to affect plant physiological processes.

View Article: PubMed Central - PubMed

Affiliation: Science Park-Research Division, Department of Carcinogenesis, The University of Texas MD Anderson Cancer Center, Smithville, TX, 78957, USA.

ABSTRACT
Higher plants exhibit cellular responsiveness to the exogenous application of purine nucleotides in a manner consistent with a cell-cell signaling function for these molecules. Like animals, plants respond to extracellular ATP, ADP, and stable analogues (e.g., ATPgammaS and ADPbetaS) by increasing the cytoplasmic concentration of calcium. Agonist substrate specificity and concentration dependency suggest receptor mediation of these events, and, although the identity of the plant receptor is currently unknown, pharmacological analysis points to the involvement of a plasma membrane-localized calcium channel. Extracellular ATP can also induce the production of reactive oxygen species and stimulate an increase in the mRNA levels of a number of stress- and calcium-regulated genes, suggesting a role for nucleotide-based signaling in plant wound and defense responses. Furthermore, the growth and development of plants can also be altered by the application of external ATP. Recent studies are only beginning to uncover the complexities of plant signaling networks activated in response to extracellular ATP and how these might interact to affect plant physiological processes.

No MeSH data available.