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BIOENERGETICS AND PHOTOSYNTHESIS

Reactive Oxygen Species Production by Potato Tuber Mitochondria Is Modulated by Mitochondrially Bound Hexokinase Activity¹

Instituto de Bioquímica Médica, Programa de Biofísica e Bioquímica Celular and Programa de Biologia Molecular e Biotecnologia, Universidade Federal do Rio de Janeiro, Laboratório de Bioenergética e Fisiologia Mitochondrial, Cidade Universitária, Rio de Janeiro 21941–590, Brazil

Potato tuber (Solanum tuberosum) mitochondria (PTM) have a mitochondrially bound hexokinase (HK) activity that exhibits a pronounced sensitivity to ADP inhibition. Here we investigated the role of mitochondrial HK activity in PTM reactive oxygen species generation. Mitochondrial HK has a 10-fold higher affinity for glucose (Glc) than for fructose (K_MGlc = 140 µM versus K_MFrc = 1,375 µM). Activation of PTM respiration by succinate led to an increase in hydrogen peroxide (H₂O₂) release that was abrogated by mitochondrial HK activation. Mitochondrial HK activity caused a decrease in the mitochondrial membrane potential and an increase in oxygen consumption by PTM. Inhibition of Glc phosphorylation by mannoheptulose or GlcNAc induced a rapid increase in H₂O₂ release. The blockage of H₂O₂ release sustained by Glc was reverted by oligomycin and atractyloside, indicating that ADP recycles through the adenine nucleotide translocator and F₀F₁ATP synthase is operative during the mitochondrial HK reaction. Inhibition of mitochondrial HK activity by 60% to 70% caused an increase of 50% in the maximal rate of H₂O₂ release. Inhibition in H₂O₂ release by mitochondrial HK activity was comparable to, or even more potent, than that observed for StUCP (S. tuberosum uncoupling protein) activity. The inhibition of H₂O₂ release in PTM was two orders of magnitude more selective for the ADP produced from the mitochondrial HK reaction than for that derived from soluble yeast (Saccharomyces cerevisiae) HK. Modulation of H₂O₂ release and oxygen consumption by Glc and mitochondrial HK inhibitors in potato tuber slices shows that hexoses and mitochondrial HK may act as a potent preventive antioxidant mechanism in potato tubers.

² These authors contributed equally to the article.

The author responsible for the distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Antonio Galina (galina{at}bioqmed.ufrj.br).

www.plantphysiol.org/cgi/doi/10.1104/pp.108.129247

^* Corresponding author; e-mail galina{at}bioqmed.ufrj.br.

Received September 3, 2008; accepted December 15, 2008; published December 24, 2008.