Plant Physiology Preview
Published on December 18, 2003; 10.1104/pp.103.031039
Received July 29, 2003
Returned for revision September 5, 2003
Accepted October 17, 2003
Salicylic Acid Is an Uncoupler and Inhibitor of Mitochondrial Electron Transport
Christel Norman , Katharine A. Howell , A. Harvey Millar , James M. Whelan , and David A. Day *
Plant Molecular Biology Group, Biochemistry and Molecular Biology, School of Biomedical and Chemical Sciences, and School of Plant Biology, Faculty of Natural and Agricultural Sciences, The University of Western Australia, 35 Stirling Highway, Crawley 6009, Western Australia, Australia
* Corresponding author; email: dday{at}cyllene.uwa.edu.au.
The effect of salicylic acid (SA) on respiration and mitochondrial function was examined in tobacco (Nicotiana tabacum) suspension cell cultures in the range of 0.01 to 5 mM. Cells rapidly accumulated SA up to 10-fold of the externally applied concentrations. At the lower concentrations, SA accumulation was transitory. When applied at 0.1 mM or less, SA stimulated respiration of whole cells and isolated mitochondria in the absence of added ADP, indicating uncoupling of respiration. However, at higher concentrations, respiration was severely inhibited. Measurements of ubiquinone redox poise in isolated mitochondria suggested that SA blocked electron flow from the substrate dehydrogenases to the ubiquinone pool. This inhibition could be at least partially reversed by re-isolating the mitochondria. Two active analogs of SA, benzoic acid and acetyl-SA, had the same effect as SA on isolated tobacco mitochondria, whereas the inactive p-hydroxybenzoic acid was without effect at the same concentration. SA induced an increase in Aox protein levels in cell suspensions, and this was correlated with an increase in Aox1 transcript abundance. However, when applied at 0.1 mM, this induction was transient and disappeared as SA levels in the cells declined. SA at 0.1 mM also increased the expression of other SA-responsive genes, and this induction was dependent on active mitochondria. The results indicate that SA is both an uncoupler and an inhibitor of mitochondrial electron transport and suggest that this underlies the induction of some genes by SA. The possible implications of this for the interpretation of SA action in plants are discussed.
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