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

Abstract

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.

Unraveling the Tapestry of Networks Involving Reactive Oxygen Species in Plants

“…Proteins that function to reduce NAD(P) to NAD(P)H or alter the level of ATP were found to be essential for plant tolerance to oxidative stress (Chai et al, 2006;Valderrama et al, 2006;Marino et al, 2007;Noctor et al, 2007;Rodriguez et al, 2007;Vidal et al, 2007). These reports strengthen the link between ROS scavenging and metabolism and demonstrate that proper regulation of ROS requires reducing power that can be supplied by photosynthesis, respiration, and/or different carbon utilization pathways.…”

“…Allan and Fluhr, 1997) and supports a model in which multiple sources of ROS production are involved in the response of plants to pathogen or insect interactions. Interestingly, ROS accumulation in response to elicitation was observed in nuclei (Ashtamker et al, 2007), chloroplasts , and mitochondria (Vidal et al, 2007). In addition, the distribution of iron within the different subcellular compartments was linked to ROS production and activation of plant defenses during the oxidative burst (G. .…”

Remodeled Respiration in ndufs4 with Low Phosphorylation Efficiency Suppresses Arabidopsis Germination and Growth and Alters Control of Metabolism at Night

“…3F). It has been previously reported in the CMSII mutant that external NADH dehydrogenase activity as well as AOX capacity are increased in isolated mitochondria (Sabar et al, 2000), even though the in vivo flux through the AOX was not increased (Vidal et al, 2007). An increased capacity could be explained by an increased activity or a larger pool of the proteins analyzed.…”

The Pentatricopeptide Repeat GeneOTP43Is Required fortrans-Splicing of the Mitochondrialnad1Intron 1 inArabidopsis thaliana

“…This mutant carries a mitochondrial deletion in the nad7 gene encoding a 40-kD subunit of Complex I (Pla et al, 1995). The mutant plants develop slowly, exhibit conditional male sterility, and have no detectable Complex I, increased amounts and activity of AOX, and multiple perturbations to primary metabolism (Gutierres et al, 1997(Gutierres et al, , 1999Lelandais et al, 1998;Sabar et al, 2000;Dutilleul et al, 2003aDutilleul et al, , 2003bDutilleul et al, , 2005Pineau et al, 2005;Priault et al, 2006aPriault et al, , 2006bVidal et al, 2007). A second Complex I mutant has been described from maize (Karpova and Newton, 1999).…”