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Nitric oxide contributes to copper tolerance by influencing ROS metabolism in Arabidopsis

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Abstract

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Nitric oxide improves copper tolerance via modulation of superoxide and hydrogen peroxide levels. This reflects the necessity of a well-coordinated interplay between NO and ROS during stress tolerance.

Abstract

Copper (Cu) excess causes toxicity and one probable consequence of this is the disturbance of cell redox state maintenance, inter alia, by reactive oxygen- (ROS) and nitrogen species (RNS). The objective of this paper was to examine the role of nitric oxide (NO) in Cu stress tolerance and its relationship with ROS in Arabidopsis. In agar-grown seedlings, concentration-dependent Cu accumulation was observed. The 5 μM Cu resulted in reduced cell viability in the NO overproducing nox1 and gsnor1-3 root tips compared to the wild-type (WT). In contrast, 25 and 50 μM Cu caused higher viability in these mutants, while in the NO-lacking nia1nia2 lower viability was detected than in the WT. The exogenous NO donor enhanced cell viability and scavenging endogenous NO decreased it in Cu-exposed WT seedlings. Besides, SNP in nia1nia2 roots led to the improvement of viability. The ascorbic acid-deficient mutants (vtc2-1, vtc2-3) possessing slightly elevated ROS levels proved to be Cu sensitive, while miox4 showing decreased ROS production was more tolerant to Cu than the WT. In nox1 and gsnor1-3, Cu did not induce superoxide formation, and H2O2 accumulation occurred only in the case of NO deficiency. Based on these, under mild stress NO intensifies cell injury, while in the case of severe Cu excess it contributes to better viability. ROS were found to be responsible for aggravation of Cu-induced damage. NO alleviates acute Cu stress via modulation of O ·−2 and H2O2 levels reflecting the necessity of a well-coordinated interplay between NO and ROS during stress tolerance.

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Acknowledgments

We thank Prof. Dr. G. F. E. Scherer (University of Hannover, Germany) for supplying the NR double mutant nia1nia2 seeds and Dr. Christian Lindermayr (Helmholtz Zentrum München, Germany) for supplying the gsnor1-3 seeds. Nox1 seeds were kindly provided by Professor Yikun He (Capital Normal University, Beijing, China). We also thank Dr. Laura Zsigmond (University of Szeged, Hungary) for the kind gift of vtc2-1, vtc2-3 and miox4 seeds, respectively. The authors wish to thank “Scientia Amabilis Foundation for Hungarian Plant Physiology” for the financial support. This work was supported by the Hungarian Scientific Research Fund (grant no. OTKA PD100504). We acknowledge HURO/0901/147/2.2.2 SZETISA1. Project for the ICP-MS instrumental background. This research was realized in the frames of TÁMOP 4.2.4. A/2-11-1-2012-0001 “National Excellence Program – Elaborating and operating an inland student and researcher personal support system”. The project was subsidized by the European Union and co-financed by the European Social Fund.

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  1. Department of Plant Biology, Faculty of Science and Informatics, University of Szeged, Szeged, Hungary

    Andrea Pető, Nóra Lehotai, Gábor Feigl, Nóra Tugyi, Attila Ördög, Katalin Gémes, Irma Tari, László Erdei & Zsuzsanna Kolbert

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  1. Andrea Pető
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Correspondence to Zsuzsanna Kolbert.

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Communicated by Q. Zhao.

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Pető, A., Lehotai, N., Feigl, G. et al. Nitric oxide contributes to copper tolerance by influencing ROS metabolism in Arabidopsis . Plant Cell Rep 32, 1913–1923 (2013). https://doi.org/10.1007/s00299-013-1503-5

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