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NO and H2O2 contribute to SO2 toxicity via Ca2+ signaling in Vicia faba guard cells

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Abstract

NO and H2O2 have been implicated as important signals in biotic and abiotic stress responses of plants to the environment. Previously, we have shown that SO2 exposure increased the levels of NO and H2O2 in plant cells. We hypothesize that, as signaling molecules, NO and H2O2 mediate SO2-caused toxicity. In this paper, we show that SO2 hydrates caused guard cell death in a concentration-dependent manner in the concentration range of 0.25 to 6 mmol L−1, which was associated with elevation of intracellular NO, H2O2, and Ca2+ levels in Vicia faba guard cells. NO donor SNP enhanced SO2 toxicity, while NO scavenger c-PTIO and NO synthesis inhibitors l-NAME and tungstate significantly prevented SO2 toxicity. ROS scavenger ascorbic acid (AsA) and catalase (CAT), Ca2+ chelating agent EGTA, and Ca2+ channel inhibitor LaCl3 also markedly blocked SO2 toxicity. In addition, both c-PTIO and AsA could completely block SO2-induced elevation of intracellular Ca2+ level. Moreover, c-PTIO efficiently blocked SO2-induced H2O2 elevation, and AsA significantly blocked SO2-induced NO elevation. These results indicate that extra NO and H2O2 are produced and accumulated in SO2-treated guard cells, which further activate Ca2+ signaling to mediate SO2 toxicity. Our findings suggest that both NO and H2O2 contribute to SO2 toxicity via Ca2+ signaling.

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Acknowledgments

We thank Dr. Hong Wang (Monell Chemical Senses Center, USA) for her careful and critical reading of our manuscript. This study was supported by the National Natural Science Foundation of China (Grant No. 30470318, No. 30870454, and No. 31371868), the Research Fund for the Doctoral Program of Higher Education of China (Grant No. 20070108007 and No. 20121401110007), and the Research Project Supported by Shanxi Scholarship Council of China (Grant No. 2009022 and No. 2012013).

Author information

Correspondence to Huilan Yi.

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The authors declare that they have no conflict of interest.

Additional information

Responsible editor: Yi-ping Chen

Electronic supplementary material

Suppl. Fig. 1

I Effect of SO2 hydrates on permeability of the guard cell plasma membrane of V. faba. II Esterase activity in V. faba leaves exposed to SO2 hydrates. Different letters between treatments indicate significant differences (P<0.05). Same letter indicates no significant difference (P>0.05). (DOC 43 kb)

Suppl. Fig. 2

The combination of NO scavenger c-PTIO and H2O2 scavenger AsA blocked SO2-caused death of V. faba guard cells. Different letters between treatments indicate significant differences (P<0.05). Same letter indicates no significant difference (P>0.05). (DOC 28 kb)

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Cite this article

Yi, M., Bai, H., Xue, M. et al. NO and H2O2 contribute to SO2 toxicity via Ca2+ signaling in Vicia faba guard cells. Environ Sci Pollut Res 24, 9437–9446 (2017). https://doi.org/10.1007/s11356-017-8612-6

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Keywords

  • Vicia faba guard cell
  • SO2
  • Cytotoxicity
  • Nitric oxide
  • H2O2
  • Ca2+