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Role of the NAD(P)H quinone oxidoreductase NQR and the cytochrome b AIR12 in controlling superoxide generation at the plasma membrane

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Main conclusion

The quinone reductase NQR and the b-type cytochrome AIR12 of the plasma membrane are important for the control of reactive oxygen species in the apoplast.

AIR12 and NQR are two proteins attached to the plant plasma membrane which may be important for generating and controlling levels of reactive oxygen species in the apoplast. AIR12 (Auxin Induced in Root culture) is a single gene of Arabidopsis that codes for a mono-heme cytochrome b. The NADPH quinone oxidoreductase NQR is a two-electron-transferring flavoenzyme that contributes to the generation of O •−2 in isolated plasma membranes. A. thaliana double knockout plants of both NQR and AIR12 generated more O •−2 and germinated faster than the single mutant affected in AIR12. To test whether NQR and AIR12 are able to interact functionally, recombinant purified proteins were added to plasma membranes isolated from soybean hypocotyls. In vitro NADH-dependent O •−2 production at the plasma membrane in the presence of NQR was reduced upon addition of AIR12. Electron donation from semi-reduced menadione to AIR12 was shown to take place. Biochemical analysis showed that purified plasma membrane from soybean hypocotyls or roots contained phylloquinone and menaquinone-4 as redox carriers. This is the first report on the occurrence of menaquinone-4 in eukaryotic photosynthetic organisms. We propose that NQR and AIR12 interact via the quinone, allowing an electron transfer from cytosolic NAD(P)H to apoplastic monodehydroascorbate and control thereby the level of reactive oxygen production and the redox state of the apoplast.

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Acknowledgements

We thank Pierre Sétif, I2BC CEA Saclay, for critical reading of the manuscript and Sébastien Thomine, I2BC Gif-sur-Yvette for his help with growing Arabidopsis. This work was supported by ERC.KBBE.2012.1.1-01 (EcoSeed-311840) to C. B. and A. K.-L.

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Authors and Affiliations

  1. Institut de Biologie Intégrative de la Cellule (I2BC), IBITECS, CEA, CNRS, Univ Paris-Sud, Université Paris-Saclay, 91198, Gif-sur-Yvette, France

    Catherine Biniek & Anja Krieger-Liszkay

  2. Biochemie der Pflanzen, Ruhr-Universität Bochum, Universitätsstr. 150, 44801, Bochum, Germany

    Eiri Heyno

  3. Department of Plant Physiology and Biochemistry, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Gronostajowa 7, 30-387, Kraków, Poland

    Jerzy Kruk

  4. Department of Pharmacy and Biotechnology, University of Bologna, Via Irnerio 42, 40126, Bologna, Italy

    Francesca Sparla & Paolo Trost

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  1. Catherine Biniek
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  2. Eiri Heyno
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Correspondence to Anja Krieger-Liszkay.

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Biniek, C., Heyno, E., Kruk, J. et al. Role of the NAD(P)H quinone oxidoreductase NQR and the cytochrome b AIR12 in controlling superoxide generation at the plasma membrane. Planta 245, 807–817 (2017). https://doi.org/10.1007/s00425-016-2643-y

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