Skip to main content

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

Abstract

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.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

References

  1. Asard H, Barbaro R, Trost P, Bérczi A (2013) Cytochromes b561: ascorbate-mediated trans-membrane electron transport. Antioxid Redox Signal 19:1026–1035

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  2. Askerlund P, Larsson C (1991) Transmembrane electron transport in plasma membrane vesicles loaded with an NADH-generating system or ascorbate. Plant Physiol 96:178–1184

    Article  Google Scholar 

  3. Bailly C, El-Maarouf-Bouteau H, Corbineau F (2008) From intracellular signaling networks to cell death: the dual role of reactive oxygen species in seed physiology. C R Biol 331:806–814

    CAS  Article  PubMed  Google Scholar 

  4. Baxter A, Mittler R, Suzuki N (2014) ROS as key players in ROS stress signaling. J Exp Bot 65:1229–1240

    CAS  Article  PubMed  Google Scholar 

  5. Bérczi A, Møller IM (2000) Redox enzymes in the plant plasma membrane and their possible roles. Plant, Cell Environ 23:1287–1302

    Article  Google Scholar 

  6. Beyer RE, Segura-Aguilar J, Di Bernardo S, Cavazzoni M, Fato R, Fiorentini D, Galli MC, Setti M, Landi L, Lenaz G (1996) The role of DT-diaphorase in the maintenance of the reduced antioxidant form of coenzyme Q in membrane systems. PNAS 93:2528–2532

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  7. Costa A, Barbaro MR, Sicilia F, Preger V, Krieger-Liszkay A, Sparla F, De Lorenzo G, Trost P (2015) AIR12, a b-type cytochrome of the plasma membrane of Arabidopsis thaliana is a negative regulator of resistance against Botrytis cinerea. Plant Sci 233:32–43

    CAS  Article  PubMed  Google Scholar 

  8. Dietz KJ, Turkan I, Krieger-Liszkay A (2016) Redox- and reactive oxygen species-dependent signaling into and out of the photosynthesizing chloroplast. Plant Physiol 171:1541–1550

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  9. Fry SC (1998) Oxidative scission of plant cell wall polysaccharides by ascorbate-induced hydroxyl radicals. Biochem J 332:507–515

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  10. Gibson SW, Todd CD (2015) Arabidopsis AIR12 influences root development. Physiol Mol Biol Plants 21:479–489

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  11. Gibson SW, Conway AL, Zheng Z, Uchacz TM, Taylor TM, Todd CD (2012) Brassica carinata CIL1 mediates extracellular ROS production during auxin- and ABA-regulated lateral root development. J Plant Biol 22:361–372

    Article  Google Scholar 

  12. Heyno E, Mary V, Schopfer P, Krieger-Liszkay A (2011) Oxygen activation at the plasma membrane: relation between superoxide and hydroxyl radical production by isolated membranes. Planta 234:35–45

    CAS  Article  PubMed  Google Scholar 

  13. Heyno E, Alkan N, Fluhr R (2013) A dual role for plant quinone reductases in host-fungus interaction. Physiol Plant 149:340–353

    CAS  PubMed  Google Scholar 

  14. Kruk J, Strzałka K, Schmid GH (1994) Antioxidant properties of plastoquinol and other biological prenylquinols in liposomes and solution. Free Radic Res 21:409–416

    CAS  Article  PubMed  Google Scholar 

  15. Laskowski MJ, Dreher KA, Gehring MA, Abel S, Gensler AL, Sussex IM (2002) FQR1, a novel primary auxin-response gene, encodes a flavin mononucleotide-binding quinone reductase. Plant Physiol 128:578–590

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  16. Lefebvre B, Furt F, Hartmann MA, Michaelson LV, Carde JP, Sargueil-Boiron F, Rossignol M, Napier JA, Cullimore J, Bessoule JJ, Mongrand S (2007) Characterization of lipid rafts from Medicago truncatula root plasma membranes: a proteomic study reveals the presence of a raft-associated redox system. Plant Physiol 144:402–418

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  17. Lüthje S, Van Gestelen P, Cordoba-Pedregosa MC, Gonzalez-Reyes JA, Asard H, Villalba JM, Böttger M (1998) Quinones in plant plasma membranes—a missing link? Protoplasma 205:43–51

    Article  Google Scholar 

  18. Lüthje S, Möller B, Perrineau FC, Wöltje K (2013) Plasma membrane electron pathways and oxidative stress. Antioxid Redox Signal 18:2163–2183

    Article  PubMed  Google Scholar 

  19. Mayhew SG (1999) The effects of pH and semiquinone formation on the oxidation–reduction potentials of flavin mononucleotide. Euro J Biochem 265:698–702

    CAS  Article  Google Scholar 

  20. Menckhoff M, Lüthje S (2004) Transmembrane electron transport in sealed and NAD(P)H-loaded right-side-out plasma membrane vesicles isolated from maize (Zea mays L.) roots. J Exp Bot 55:1343–1349

    CAS  Article  PubMed  Google Scholar 

  21. Müller K, Linkies A, Vreeburg RA, Fry SC, Krieger-Liszkay A, Leubner-Metzger G (2009) In vivo cell wall loosening by hydroxyl radicals during cress seed germination and elongation growth. Plant Physiol 150:1855–1865

    Article  PubMed  PubMed Central  Google Scholar 

  22. Nakagawa K, Hirota Y, Sawada N, Yuge N, Watanabe M, Uchino Y, Okuda N, Shimomura Y, Suhara Y, Okano T (2010) Identification of UBIAD1 as a novel human menaquinone-4 biosynthetic enzyme. Nature 468:117–121

    CAS  Article  PubMed  Google Scholar 

  23. Nanda AK, Andrio E, Marino D, Pauly N, Dunand C (2010) Reactive oxygen species during plant-microorganism early interactions. J Integr Plant Biol 52:195–204

    CAS  Article  PubMed  Google Scholar 

  24. Nowicka B, Kruk J (2010) Occurrence, biosynthesis and function of isoprenoid quinones. Biochim Biophys Acta 1797:1587–1605

    CAS  Article  PubMed  Google Scholar 

  25. Oja V, Savchenko G, Jakob B, Heber U (1999) pH and buffer capacities of apoplastic and cytoplasmic cell compartments in leaves. Planta 209:239–249

    CAS  Article  PubMed  Google Scholar 

  26. O’Leary BM, Neale HC, Geilfus CM, Jackson RW, Arnold DL, Preston GM (2016) Early changes in apoplast composition associated with defense and disease in interactions between Phaseolus vulgaris and the halo blight pathogen Pseudomonas syringae Pv. phaseolicola. Plant Cell Environ. doi:10.1111/pce.12770

    PubMed  PubMed Central  Google Scholar 

  27. Oracz K, Karpiński S (2016) Phytohormones signaling pathways and ROS involvement in seed germination. Front Plant Sci 7:864. doi:10.3389/fpls.2016.00864

    PubMed  PubMed Central  Google Scholar 

  28. Picco C, Scholz-Starke J, Festa M, Costa A, Sparla F, Trost P, Carpaneto A (2015) Direct recording of trans-plasma membrane electron currents mediated by a member of the cytochrome b561 family of soybean. Plant Physiol 169:986–995

    Article  PubMed  PubMed Central  Google Scholar 

  29. Preger V, Tango N, Marchand C, Lemaire SD, Carbonera D, Di Valentin M, Costa A, Pupillo P, Trost P (2009) Auxin-responsive genes AIR12 code for a new family of plasma membrane b-type cytochromes specific to flowering plants. Plant Physiol 150:606–620

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  30. Radjendirane V, Joseph P, Lee YH, Kimura S, Klein-Szanto AJ, Gonzalez FJ, Jaiswal AK (1998) Disruption of the DT diaphorase (NQO1) gene in mice leads to increased menadione toxicity. J Biol Chem 273:7382–7389

    CAS  Article  PubMed  Google Scholar 

  31. Richards SL, Wilkins KA, Swarbreck SM, Anderson AA, Habib N, Smith AG, McAinsh M, Davies JM (2015) The hydroxyl radical in plants: from seed to seed. J Exp Bot 66:37–46

    CAS  Article  PubMed  Google Scholar 

  32. Riegel B, Smith P, Schweitzer CE (1940) The oxidation-reduction potential of vitamin K. J Am Chem Soc 62:992

    CAS  Article  Google Scholar 

  33. Savchenko G, Wiese C, Neimanis S, Hedrich R, Heber U (2000) pH regulation in apoplastic and cytoplasmic cell compartments of leaves. Planta 211:246–255

    CAS  Article  PubMed  Google Scholar 

  34. Schopfer P, Plachy C, Frahry G (2001) Release of reactive oxygen intermediates (superoxide radicals, hydrogen peroxide, and hydroxyl radicals) and peroxidase in germinating radish seeds controlled by light, gibberellin, and abscisic acid. Plant Physiol 125:1591–1602

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  35. Schopfer P, Liszkay A, Bechtold M, Frahry G, Wagner A (2002) Evidence that hydroxyl radicals mediate auxin-induced extension growth. Planta 214:821–828

    CAS  Article  PubMed  Google Scholar 

  36. Schopfer P, Heyno E, Drepper F, Krieger-Liszkay A (2008) Naphthoquinone-dependent generation of superoxide radicals by quinone reductase isolated from the plasma membrane of soybean. Plant Physiol 147:864–878

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  37. Sparla F, Tedeschi G, Pupillo P, Trost P (1999) Cloning and heterologous expression of NAD(P)H:quinone reductase of Arabidopsis thaliana, a functional homologue of animal DT-diaphorase. FEBS Lett 463:382–386

    CAS  Article  PubMed  Google Scholar 

  38. Thein M, Michalke W (1988) Bisulfite interacts with binding sites of the auxin-transport inhibitor N-1-naphthylphthalamic acid. Planta 176:343–350

    CAS  Article  PubMed  Google Scholar 

  39. Trost P, Bonora P, Scagliarini S, Pupillo P (1995) Purification and properties of NAD (P)H: (quinone acceptor) oxidoreductase of sugarbeet cells. Eur J Biochem 234:452–458

    CAS  Article  PubMed  Google Scholar 

  40. Trost P, Foscarini S, Preger V, Bonora P, Vitale L, Pupillo P (1997) Dissecting the diphenylene iodonium-sensitive NAD(P)H: quinone oxidoreductase of zucchini plasma membrane. Plant Physiol 114:737–746

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  41. van Oostende C, Widhalm JR, Basset JC (2008) Detection and quantification of vitamin K1 quinol in leaf tissues. Phytochemistry 69:2457–2462

    Article  PubMed  Google Scholar 

  42. Wrzaczek M, Brosché M, Kangasjärvi J (2013) ROS signaling loops—production, perception, regulation. Curr Opin Plant Biol 16:575–582

    CAS  Article  PubMed  Google Scholar 

Download references

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.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Anja Krieger-Liszkay.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 414 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

Keywords

  • Arabidopsis thaliana
  • Germination
  • Plasma membrane
  • Reactive oxygen species