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Lack of Respiratory Chain Complex I Impairs Alternative Oxidase Engagement and Modulates Redox Signaling during Elicitor-Induced Cell Death in Tobacco

^a Laboratoire Mitochondries et Métabolisme, Institut de Biotechnologie des Plantes, Unité Mixte de Recherche, Centre National de la Recherche Scientifique 8618, Université Paris Sud, 91 405 Orsay, France
^b Grup de Recerca en Biologia de les Plantes en Condicions Mediterrànies, Departament de Biologia, Universitat de les Illes Balears, 07122 Palma de Mallorca, Spain
^c Department of Cell and Organism Biology, Lund University, Sölvegatan 35B, SE-223 62 Lund, Sweden
^d Crop Performance and Improvement Division, Rothamsted Research, Harpenden, Herts, AL5 2 JQ, United Kingdom

¹ To whom correspondence should be addressed. E-mail rosine.de-paepe{at}u-psud.fr; fax 33-1-69-15-3425.

Alternative oxidase (AOX) functions in stress resistance by preventing accumulation of reactive oxygen species (ROS), but little is known about in vivo partitioning of electron flow between AOX and the cytochrome pathway. We investigated the relationships between AOX expression and in vivo activity in Nicotiana sylvestris and the complex I–deficient CMSII mutant in response to a cell death elicitor. While a specific AOX1 isoform in the active reduced state was constitutively overexpressed in CMSII, partitioning through the alternative pathway was similar to the wild type. Lack of correlation between AOX content and activity indicates severe metabolic constraints in nonstressed mutant leaves. The bacterial elicitor harpin N_Ea induced similar timing and extent of cell death and a twofold respiratory burst in both genotypes with little change in AOX amounts. However, partitioning to AOX was increased twofold in the wild type but remained unchanged in CMSII. Oxidative phosphorylation modeling indicated a twofold ATP increase in both genotypes. By contrast, mitochondrial superoxide dismutase activity and reduced forms of ascorbate and glutathione were higher in CMSII than in the wild type. These results demonstrate genetically programmed flexibility of plant respiratory routes and antioxidants in response to elicitors and suggest that sustained ATP production, rather than AOX activity by itself or mitochondrial ROS, might be important for in planta cell death.

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