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Zinc-Dependent Protection of Tobacco and Rice Cells From Aluminum-Induced Superoxide-Mediated Cytotoxicity.

Lin C, Hara A, Comparini D, Bouteau F, Kawano T - Front Plant Sci (2015)

Bottom Line: Earlier studies suggested that lack of zinc often results in ROS-mediated oxidative damage to plant cells.In the present study, the effect of Zn(2+) on Al(3+)-induced superoxide generation in the cell suspension cultures of tobacco (Nicotiana tabacum L., cell-line, BY-2) and rice (Oryza sativa L., cv.Obtained results indicated that presence of Zn(2+) at physiological concentrations can protect the cells by preventing the Al(3+)-induced superoxide generation and cell death.

View Article: PubMed Central - PubMed

Affiliation: Faculty of Environmental Engineering and Graduate School of Environmental Engineering, The University of Kitakyushu , Kitakyushu, Japan.

ABSTRACT
Al(3+) toxicity in growing plants is considered as one of the major factors limiting the production of crops on acidic soils worldwide. In the last 15 years, it has been proposed that Al(3+) toxicity are mediated with distortion of the cellular signaling mechanisms such as calcium signaling pathways, and production of cytotoxic reactive oxygen species (ROS) causing oxidative damages. On the other hand, zinc is normally present in plants at high concentrations and its deficiency is one of the most widespread micronutrient deficiencies in plants. Earlier studies suggested that lack of zinc often results in ROS-mediated oxidative damage to plant cells. Previously, inhibitory action of Zn(2+) against lanthanide-induced superoxide generation in tobacco cells have been reported, suggesting that Zn(2+) interferes with the cation-induced ROS production via stimulation of NADPH oxidase. In the present study, the effect of Zn(2+) on Al(3+)-induced superoxide generation in the cell suspension cultures of tobacco (Nicotiana tabacum L., cell-line, BY-2) and rice (Oryza sativa L., cv. Nipponbare), was examined. The Zn(2+)-dependent inhibition of the Al(3+)-induced oxidative burst was observed in both model cells selected from the monocots and dicots (rice and tobacco), suggesting that this phenomenon (Al(3+)/Zn(2+) interaction) can be preserved in higher plants. Subsequently induced cell death in tobacco cells was analyzed by lethal cell staining with Evans blue. Obtained results indicated that presence of Zn(2+) at physiological concentrations can protect the cells by preventing the Al(3+)-induced superoxide generation and cell death. Furthermore, the regulation of the Ca(2+) signaling, i.e., change in the cytosolic Ca(2+) ion concentration, and the cross-talks among the elements which participate in the pathway were further explored.

No MeSH data available.


Related in: MedlinePlus

A model for Al3+-induced signaling leading to oxidative cell death and its inhibition by Zn2+ in model plant cells. Knowledge from present experiments using the aequorin-expressing cell lines of tobacco (BY-2) were strengthened by previously reported models. As suggested in the cells of Arabidopsis thaliana (Kunihiro et al., 2011), SA signaling pathway is activated in the downstream of ROS such as O2•– (and possibly of calcium signaling). The loop of ROS-stimulated the SA signaling and expression of NADPH oxidase which produces further ROS, may eventually lead to development of cell death. Zinc may block the loop by interfering the NADPH oxidase-catalyzed ROS production similarly to the model for lanthanide-induced oxidative burst and cell death in tobacco cells (Kawano et al., 2002). Arrows indicate the stimulation and the T-shaped lines indicate the steps inhibited by agent indicated. The numbers and the symbol “C” in small brackets next to arrows or T-shaped lines denote the source of knowledge, namely; C, data confirmed here; 1, Kawano et al. (2003a; BY-2 cells); 2, Kawano et al. (2004; BY-2 cells); 3, Lin et al. (2005; BY-2 cells); 4, Kunihiro et al. (2011; Arabidopsis thaliana); 5, Kawano et al. (2002; BY-2 cells); 6, Kawano et al. (1998; BY-2 cells); 7, Kawano et al. (2013; review on higher plants).
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Figure 9: A model for Al3+-induced signaling leading to oxidative cell death and its inhibition by Zn2+ in model plant cells. Knowledge from present experiments using the aequorin-expressing cell lines of tobacco (BY-2) were strengthened by previously reported models. As suggested in the cells of Arabidopsis thaliana (Kunihiro et al., 2011), SA signaling pathway is activated in the downstream of ROS such as O2•– (and possibly of calcium signaling). The loop of ROS-stimulated the SA signaling and expression of NADPH oxidase which produces further ROS, may eventually lead to development of cell death. Zinc may block the loop by interfering the NADPH oxidase-catalyzed ROS production similarly to the model for lanthanide-induced oxidative burst and cell death in tobacco cells (Kawano et al., 2002). Arrows indicate the stimulation and the T-shaped lines indicate the steps inhibited by agent indicated. The numbers and the symbol “C” in small brackets next to arrows or T-shaped lines denote the source of knowledge, namely; C, data confirmed here; 1, Kawano et al. (2003a; BY-2 cells); 2, Kawano et al. (2004; BY-2 cells); 3, Lin et al. (2005; BY-2 cells); 4, Kunihiro et al. (2011; Arabidopsis thaliana); 5, Kawano et al. (2002; BY-2 cells); 6, Kawano et al. (1998; BY-2 cells); 7, Kawano et al. (2013; review on higher plants).

Mentions: Previously, we have propose a model that Al3+ plays dual roles acting for and against the Ca2+ influx, by releasing O2•– and by inhibiting the Ca2+ channel(s), respectively (Kawano et al., 2003a). Al3+-dependent distortion in calcium signaling in plant cells can be dissected into two opposing modes of Al3+ actions, viz., (i) stimulation of ROS-responsive calcium channels via induction of O2•– and (ii) inhibition of calcium channels. At low Al3+ concentrations, the ROS-responsive Ca2+ influx potency is high but the driving force (due to ROS) is not sufficient. At high Al3+concentrations, the Ca2+ influx-driving force is at sufficient level but the channel’s Ca2+ permeability is low. This effect is showed in Figure 7B, where [Ca2+]c elevation could be manifested only in the range of Al3+ concentration in which the two opposing effects eventually compromise (Kawano et al., 2003a). Zn2+ hardly blocks the calcium influx in model plant cells unless the event of interest is dependent on the ROS generating events (Figure 8). Therefore, we view here that Zn2+ might target only the earlier phase of Al3+ action involved in induction of O2•– as illustrated in Figure 9.


Zinc-Dependent Protection of Tobacco and Rice Cells From Aluminum-Induced Superoxide-Mediated Cytotoxicity.

Lin C, Hara A, Comparini D, Bouteau F, Kawano T - Front Plant Sci (2015)

A model for Al3+-induced signaling leading to oxidative cell death and its inhibition by Zn2+ in model plant cells. Knowledge from present experiments using the aequorin-expressing cell lines of tobacco (BY-2) were strengthened by previously reported models. As suggested in the cells of Arabidopsis thaliana (Kunihiro et al., 2011), SA signaling pathway is activated in the downstream of ROS such as O2•– (and possibly of calcium signaling). The loop of ROS-stimulated the SA signaling and expression of NADPH oxidase which produces further ROS, may eventually lead to development of cell death. Zinc may block the loop by interfering the NADPH oxidase-catalyzed ROS production similarly to the model for lanthanide-induced oxidative burst and cell death in tobacco cells (Kawano et al., 2002). Arrows indicate the stimulation and the T-shaped lines indicate the steps inhibited by agent indicated. The numbers and the symbol “C” in small brackets next to arrows or T-shaped lines denote the source of knowledge, namely; C, data confirmed here; 1, Kawano et al. (2003a; BY-2 cells); 2, Kawano et al. (2004; BY-2 cells); 3, Lin et al. (2005; BY-2 cells); 4, Kunihiro et al. (2011; Arabidopsis thaliana); 5, Kawano et al. (2002; BY-2 cells); 6, Kawano et al. (1998; BY-2 cells); 7, Kawano et al. (2013; review on higher plants).
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Figure 9: A model for Al3+-induced signaling leading to oxidative cell death and its inhibition by Zn2+ in model plant cells. Knowledge from present experiments using the aequorin-expressing cell lines of tobacco (BY-2) were strengthened by previously reported models. As suggested in the cells of Arabidopsis thaliana (Kunihiro et al., 2011), SA signaling pathway is activated in the downstream of ROS such as O2•– (and possibly of calcium signaling). The loop of ROS-stimulated the SA signaling and expression of NADPH oxidase which produces further ROS, may eventually lead to development of cell death. Zinc may block the loop by interfering the NADPH oxidase-catalyzed ROS production similarly to the model for lanthanide-induced oxidative burst and cell death in tobacco cells (Kawano et al., 2002). Arrows indicate the stimulation and the T-shaped lines indicate the steps inhibited by agent indicated. The numbers and the symbol “C” in small brackets next to arrows or T-shaped lines denote the source of knowledge, namely; C, data confirmed here; 1, Kawano et al. (2003a; BY-2 cells); 2, Kawano et al. (2004; BY-2 cells); 3, Lin et al. (2005; BY-2 cells); 4, Kunihiro et al. (2011; Arabidopsis thaliana); 5, Kawano et al. (2002; BY-2 cells); 6, Kawano et al. (1998; BY-2 cells); 7, Kawano et al. (2013; review on higher plants).
Mentions: Previously, we have propose a model that Al3+ plays dual roles acting for and against the Ca2+ influx, by releasing O2•– and by inhibiting the Ca2+ channel(s), respectively (Kawano et al., 2003a). Al3+-dependent distortion in calcium signaling in plant cells can be dissected into two opposing modes of Al3+ actions, viz., (i) stimulation of ROS-responsive calcium channels via induction of O2•– and (ii) inhibition of calcium channels. At low Al3+ concentrations, the ROS-responsive Ca2+ influx potency is high but the driving force (due to ROS) is not sufficient. At high Al3+concentrations, the Ca2+ influx-driving force is at sufficient level but the channel’s Ca2+ permeability is low. This effect is showed in Figure 7B, where [Ca2+]c elevation could be manifested only in the range of Al3+ concentration in which the two opposing effects eventually compromise (Kawano et al., 2003a). Zn2+ hardly blocks the calcium influx in model plant cells unless the event of interest is dependent on the ROS generating events (Figure 8). Therefore, we view here that Zn2+ might target only the earlier phase of Al3+ action involved in induction of O2•– as illustrated in Figure 9.

Bottom Line: Earlier studies suggested that lack of zinc often results in ROS-mediated oxidative damage to plant cells.In the present study, the effect of Zn(2+) on Al(3+)-induced superoxide generation in the cell suspension cultures of tobacco (Nicotiana tabacum L., cell-line, BY-2) and rice (Oryza sativa L., cv.Obtained results indicated that presence of Zn(2+) at physiological concentrations can protect the cells by preventing the Al(3+)-induced superoxide generation and cell death.

View Article: PubMed Central - PubMed

Affiliation: Faculty of Environmental Engineering and Graduate School of Environmental Engineering, The University of Kitakyushu , Kitakyushu, Japan.

ABSTRACT
Al(3+) toxicity in growing plants is considered as one of the major factors limiting the production of crops on acidic soils worldwide. In the last 15 years, it has been proposed that Al(3+) toxicity are mediated with distortion of the cellular signaling mechanisms such as calcium signaling pathways, and production of cytotoxic reactive oxygen species (ROS) causing oxidative damages. On the other hand, zinc is normally present in plants at high concentrations and its deficiency is one of the most widespread micronutrient deficiencies in plants. Earlier studies suggested that lack of zinc often results in ROS-mediated oxidative damage to plant cells. Previously, inhibitory action of Zn(2+) against lanthanide-induced superoxide generation in tobacco cells have been reported, suggesting that Zn(2+) interferes with the cation-induced ROS production via stimulation of NADPH oxidase. In the present study, the effect of Zn(2+) on Al(3+)-induced superoxide generation in the cell suspension cultures of tobacco (Nicotiana tabacum L., cell-line, BY-2) and rice (Oryza sativa L., cv. Nipponbare), was examined. The Zn(2+)-dependent inhibition of the Al(3+)-induced oxidative burst was observed in both model cells selected from the monocots and dicots (rice and tobacco), suggesting that this phenomenon (Al(3+)/Zn(2+) interaction) can be preserved in higher plants. Subsequently induced cell death in tobacco cells was analyzed by lethal cell staining with Evans blue. Obtained results indicated that presence of Zn(2+) at physiological concentrations can protect the cells by preventing the Al(3+)-induced superoxide generation and cell death. Furthermore, the regulation of the Ca(2+) signaling, i.e., change in the cytosolic Ca(2+) ion concentration, and the cross-talks among the elements which participate in the pathway were further explored.

No MeSH data available.


Related in: MedlinePlus