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Identification of superoxide production by Arabidopsis thaliana aldehyde oxidases AAO1 and AAO3

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Abstract

Plant aldehyde oxidases (AOs) have gained great attention during the last years as they catalyze the last step in the biosynthesis of the phytohormone abscisic acid by oxidation of abscisic aldehyde. Furthermore, oxidation of indole-3-acetaldehyde by AOs is likely to represent one route to produce another phytohormone, indole-3-acetic acid, and thus, AOs play important roles in many aspects of plant growth and development. In the present work we demonstrate that heterologously expressed AAO1 and AAO3, two prominent members of the AO family from Arabidopsis thaliana, do not only generate hydrogen peroxide but also superoxide anions by transferring aldehyde-derived electrons to molecular oxygen. In support of this, superoxide production has also been found for native AO proteins in Arabidopsis leaf extracts. In addition to their aldehyde oxidation activity, AAO1 and AAO3 were found to exhibit NADH oxidase activity, which likewise is associated with the production of superoxide anions. According to these results and due to the fact that molecular oxygen is the only known physiological electron acceptor of AOs, the production of hydrogen peroxide and/or superoxide has to be considered in any physiological condition in which aldehydes or NADH serve as substrate for AOs. In this respect, conditions such as natural senescence and stress-induced stomatal movement, which both require simultaneously elevated levels of abscisic acid and hydrogen peroxide/superoxide, are likely to benefit from AOs in two ways, namely by formation of abscisic acid and by concomitant formation of reactive oxygen species.

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Abbreviations

ABA:

Abscisic acid

AO:

Aldehyde oxidase

DCIP:

2,6-dichloroindophenol

DPI:

Diphenylene iodonium

FAD:

Flavin adenine dinucleotide

HRP:

Horseradish peroxidase

Moco:

Molybdenum cofactor

MTT:

3[4,5-dimethylthiazol-2-yl]-2,5-diphenyltetrazolium-bromide

PMS:

Phenazine methosulfate

P. pastoris :

Pichia pastoris

SOD:

Superoxide dismutase

XDH:

Xanthine dehydrogenase

XTT:

2,3-bis-(2-methoxy-4-nitro-5-sulfophenyl)-2H-tetrazolium-5-carboxanilide sodium salt

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Acknowledgments

We are grateful to Victoria Michael and Marion Kay (TU Braunschweig) for excellent technical assistance. This work was supported by the Deutsche Forschungsgemeinschaft (DFG grant Bi 1075/2-1 to FB).

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  1. Maryam Zarepour

    Present address: Department of Pediatrics, Child and Family Research Institute, University of British Columbia, 950 West 28th Ave., Vancouver, BC, V5Z 4H4, Canada

Authors and Affiliations

  1. Department of Plant Biology, Braunschweig University of Technology, Humboldtstrasse 1, 38106, Braunschweig, Germany

    Maryam Zarepour, Moritz Wilch, Ute Nieländer & Florian Bittner

  2. Institute of Organic Chemistry, Braunschweig University of Technology, 38023, Braunschweig, Germany

    Kristina Simon & Thomas Lindel

  3. Department of Biological Sciences, Tokyo Metropolitan University, Hachioji, Tokyo, 192-0397, Japan

    Tomokazu Koshiba

  4. Dormancy and Adaptation Research Unit, RIKEN Plant Science Center, Yokohama, Kanagawa, 230-0045, Japan

    Mitsunori Seo

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Zarepour, M., Simon, K., Wilch, M. et al. Identification of superoxide production by Arabidopsis thaliana aldehyde oxidases AAO1 and AAO3. Plant Mol Biol 80, 659–671 (2012). https://doi.org/10.1007/s11103-012-9975-1

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