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Exogenous Nitric Oxide Confers Tolerance to Cr(VI) in Maize (Zea mays L.) Seedlings by Modulating Endogenous Oxido-Nitrosative Events

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Abstract

The use of exogenous compounds such as ‘gasotransmitter’ molecules is a well-established agronomic strategy to improve the crop tolerance to environmental stresses. In this current work, when Cr (200 µM) was combined with the nitric oxide (NO) generator sodium nitroprusside SNP, 500 µM) there was a suppression of metal-induced alterations in embryo growth. Exogenous NO produced by SNP reduced the accumulation of toxic hydrogen peroxide and methylglyoxal and stress-linked proline in Cr-treated seedlings. Chromium increased thiol and S-nitrosothiol levels but this was restored to control levels by SNP, in spite of a competing NO reaction leading to increase of S-nitrosoglutathione content. However, added complexity was indicated by addition of arginine analogue N (ω)-nitro-L-arginine methyl ester (L-NAME, 500 µM) in the germinating medium to suppress endogenous NO production. This suppressed endogenous NO production but superoxide dismutase (SOD) was suppressed not enhanced in Cr + L-NAME treatments. In addition, Cr + L-NAME significantly decreased the content of spermidine and spermine in epicotyls as compared to Cr treatment alone. Similarly, exposure to Cr + SNP decreased spermidine and spermine levels in both radicles and epicotyls. This is important as polyamines have been suggested as route for NO production. Thus, our observations suggest that exogenous NO mitigates Cr-induced damage and confers seedling tolerance to Cr through suppression of NADPH oxidase activity and increased GSNO contents. This may act to prevent an excess of methylglyoxal and hydrogen peroxide. However, the reduction in polyamine mediated cellular NO generation could also promote increased viability under Cr stress.

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Abbreviations

GSNO:

S-nitrosoglutathione

GSNOR:

S-nitrosoglutathione reductase

L-NAME:

Nω-Nitro-L-arginine methyl ester

MG:

Methylglyoxal

NO:

Nitric oxide

O2· :

Superoxide radicals

Pas:

Polyamines

Pro:

Proline

RNS:

Reactive nitrogen species

ROS:

Reactive oxygen species

SOD:

Superoxide dismutase

SNO:

S-nitrosothiols

SNP:

Sodium nitroprusside

Spd:

Spermidine

Spm:

Spermine

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Acknowledgements

This work was financially supported by the Tunisian Ministry of Higher Education, Scientific Research (LR18ES38) and Technology and the Institute of Biological, Environmental and Rural Sciences, Aberystwyth University, UK (Grant to Oussama Kharbech). The authors wish to thank Ms Helen Clare Phillips and Dr. Manfred Beckmann for their technical support and assistance in FIE-HRMS and LC-ES/MS.

Funding

This work was supported by Abdelilah Chaoui Ministère de l’Enseignement Supérieur et de la Recherche Scientifique (LR18ES38), Oussama Kharbech Technology and the Institute of Biological, Environmental and Rural Sciences, Aberystwyth University, united kingdom.

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Authors

Contributions

OK performed the experiments and wrote the manuscript. MBM helped in data analysis. AC helped in designing the experiment. LAJM and WD revised and improved the final version. All authors approved the manuscript.

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Correspondence to Oussama Kharbech.

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All authors declare that they have no conflict of interest.

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Handling Editor: Durgesh Kumar Tripathi.

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Kharbech, O., Massoud, M.B., Chaoui, A. et al. Exogenous Nitric Oxide Confers Tolerance to Cr(VI) in Maize (Zea mays L.) Seedlings by Modulating Endogenous Oxido-Nitrosative Events. J Plant Growth Regul 41, 1773–1785 (2022). https://doi.org/10.1007/s00344-021-10411-5

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  • DOI: https://doi.org/10.1007/s00344-021-10411-5

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