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Nitrite-driven anaerobic ATP synthesis in barley and rice root mitochondria

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Abstract

Mitochondria isolated from the roots of barley (Hordeum vulgare L.) and rice (Oryza sativa L.) seedlings were capable of oxidizing external NADH and NADPH anaerobically in the presence of nitrite. The reaction was linked to ATP synthesis and nitric oxide (NO) was a measurable product. The rates of NADH and NADPH oxidation were in the range of 12–16 nmol min−1 mg−1 protein for both species. The anaerobic ATP synthesis rate was 7–9 nmol min−1 mg−1 protein for barley and 15–17 nmol min−1 mg−1 protein for rice. The rates are of the same order of magnitude as glycolytic ATP production during anoxia and about 3–5% of the aerobic mitochondrial ATP synthesis rate. NADH/NADPH oxidation and ATP synthesis were sensitive to the mitochondrial inhibitors myxothiazol, oligomycin, diphenyleneiodonium and insensitive to rotenone and antimycin A. The uncoupler FCCP completely eliminated ATP production. Succinate was also capable of driving ATP synthesis. We conclude that plant mitochondria, under anaerobic conditions, have a capacity to use nitrite as an electron acceptor to oxidize cytosolic NADH/NADPH and generate ATP.

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Abbreviations

AOX:

Alternative oxidase

COX:

Cytochrome c oxidase

DPI:

Diphenyleneiodonium

ETC:

Electron transport chain

FCCP:

Carbonylcyanide-p-trifluoromethoxyphenylhydrazone

Hb:

Hemoglobin

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Acknowledgments

We thank Werner M. Kaiser for his cooperation and helpful suggestions. This work was supported by the Natural Sciences and Engineering Research Council of Canada and Genome Canada (to R.D.H.).

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Authors and Affiliations

  1. Department of Plant Science, University of Manitoba, Winnipeg, Manitoba, R3T 2N2, Canada

    Maria Stoimenova, Abir U. Igamberdiev & Robert D. Hill

  2. Julius-von-Sachs-Institut fur Biowissenschaften, Lehrstuhl Botanik 1, Julius-von-Sachs-Platz 2, 97082, Würzburg, Germany

    Kapuganti Jagadis Gupta

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  1. Maria Stoimenova
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  2. Abir U. Igamberdiev
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  3. Kapuganti Jagadis Gupta
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  4. Robert D. Hill
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Correspondence to Robert D. Hill.

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Stoimenova, M., Igamberdiev, A.U., Gupta, K.J. et al. Nitrite-driven anaerobic ATP synthesis in barley and rice root mitochondria. Planta 226, 465–474 (2007). https://doi.org/10.1007/s00425-007-0496-0

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