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Cadmium uncouples mitochondrial oxidative phosphorylation and induces oxidative cellular stress in soybean roots

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Abstract

Cadmium (Cd) inhibits soybean root growth, but its exact mode of action is still not completely understood. We evaluated the effects of Cd on growth, mitochondrial respiration, lipid peroxidation, total phenols, glutathione, and activities of lipoxygenase (LOX), superoxide dismutase (SOD), and catalase (CAT) in soybean roots. In primary roots, Cd stimulated KCN-insensitive respiration and KCN-SHAM-insensitive respiration, indicating the involvement of the alternative oxidase (AOX) pathway, while it decreased KCN-sensitive respiration, suggesting an inhibition of the cytochrome oxidase pathway (COX). In isolated mitochondria, Cd uncoupled the oxidative phosphorylation since it decreased state III respiration (coupled respiration) and ADP/O and respiratory control ratios, while it increased state IV respiration (depletion of exogenously added ADP). The uncoupling effect increased extramitochondrial LOX activity, lipid peroxidation, and oxidized and reduced glutathione, which induced an antioxidant response with enhanced SOD and CAT activities. In brief, our findings reveal that Cd acts as an uncoupler of the mitochondrial oxidative phosphorylation in soybean roots, disturbing cellular respiration and inducing oxidative cellular stress.

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Acknowledgements

A. Finger-Teixeira sincerely thanks the Brazilian Council for Scientific and Technological Development (CNPq) for providing a scholarship. R. Marchiosi, E.L. Ishii-Iwamoto, W.D. dos Santos, and O. Ferrarese-Filho are research fellows of CNPq. The authors would like to thank Isabela de Carvalho Contesoto for her indispensable assistance in further analyses on phenolics and glutathione.

Funding

This study was financed by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brasil (CAPES) – Finance Code 001.

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OFF and ELII conceptualized the study together with ALT. ALT, EMPC, RPC, and ARS performed all biochemical experiments. ALT, EMPC, RM, WDS, and OFF analyzed the data and co-wrote the manuscript. All authors read and approved the final manuscript.

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Correspondence to Osvaldo Ferrarese-Filho.

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The authors declare no competing interests.

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Responsible editor: Gangrong Shi

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Finger-Teixeira, A., Ishii-Iwamoto, E.L., Marchiosi, R. et al. Cadmium uncouples mitochondrial oxidative phosphorylation and induces oxidative cellular stress in soybean roots. Environ Sci Pollut Res 28, 67711–67723 (2021). https://doi.org/10.1007/s11356-021-15368-2

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  • DOI: https://doi.org/10.1007/s11356-021-15368-2

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