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Mitochondria/nuclear signaling of alternative oxidase gene expression occurs through distinct pathways involving organic acids and reactive oxygen species

  • Physiology and Biochemistry
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Abstract

Cultured cells of tobacco (Nicotiana tabacum L. cv Petit Havana) were used to investigate signals regulating the expression of the “model” nuclear gene encoding the alternative oxidase (AOX) (AOX1), the terminal oxidase of the mitochondrial alternative respiratory pathway. Several conditions shown to induce AOX1 mRNA accumulation also result in an increase in cellular citrate concentrations, suggesting that citrate and/or other tricarboxylic acid (TCA) cycle intermediates may be important signal metabolites. In addition, mitochondrial reactive oxygen species (ROS) production has recently been shown to be a factor mediating mitochondria-to-nucleus signaling for the expression of AOX1. We found that the exogenously supplied TCA cycle organic acids citrate, malate and 2-oxoglutarate caused rapid and dramatic increases in the steady-state level of AOX1 mRNA at low, near physiological concentrations (0.1 mM). Furthermore, an increase in AOX1 induced by the addition of organic acids occurs independently of mitochondrial ROS formation. Our results demonstrate that two separate pathways for mitochondria-to-nucleus signaling of AOX1 may exist, one involving ROS and the other organic acids.

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Abbreviations

AA:

Antimycin A

AOX:

Alternative oxidase

AOX1 :

Nuclear gene encoding alternative oxidase

AP:

Alternative pathway

CP:

Cytochrome pathway

DCF:

Dichlorofluorescein

H2DCF-DA:

2′,7′Dichlorofluorescein diacetate

KCN:

Potassium cyanide

MFA:

Monofluoroacetate

ROS:

Reactive oxygen species

SA:

Salicylic acid

SHAM:

Salicylhydroxamic acid

TCA:

Tricarboxylic acid

TOR:

Target of rampamycin

TTC:

2,3,5-Triphenyltetrazolium chloride

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Acknowledgements

The authors wish to thank Roxy L. Nickels for technical assistance. This research was supported, in part, by a United States Department of Energy grant DEFG0291ER20021 and National Science Foundation grant IBM 0110768. G. R. G. was supported, in part, by a postdoctoral fellowship and research grant from the Natural Sciences and Engineering Research Council of Canada (NSERC). A. R. V. acknowledges support from the Ronald E. McNair Post-Baccalaureate Achievement Program at Michigan State University.

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Authors and Affiliations

  1. Department of Plant Sciences, University of Saskatchewan, Saskatoon, SK, Canada, S7N 5A8

    G. R. Gray

  2. Department of Biology, The University of Western Ontario, London, ON, Canada, N6A 5B7

    D. P. Maxwell

  3. US Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, MI, USA, 48824-1312

    A. R. Villarimo & L. McIntosh

  4. Departments of Biochemistry and Molecular Biology, Michigan State University, East Lansing, MI, USA, 48824-1312

    L. McIntosh

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  1. G. R. Gray
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  2. D. P. Maxwell
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  3. A. R. Villarimo
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  4. L. McIntosh
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Correspondence to G. R. Gray.

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Communicated by H. Wang

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Gray, G.R., Maxwell, D.P., Villarimo, A.R. et al. Mitochondria/nuclear signaling of alternative oxidase gene expression occurs through distinct pathways involving organic acids and reactive oxygen species. Plant Cell Rep 23, 497–503 (2004). https://doi.org/10.1007/s00299-004-0848-1

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  • DOI: https://doi.org/10.1007/s00299-004-0848-1

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