Functional Mitochondrial Complex I Is Required by Tobacco Leaves for Optimal Photosynthetic Performance in Photorespiratory Conditions and during Transients

• Published in: Plant physiology (Bethesda) 2003-01, Vol.131 (1), p.264-275
• Main Authors: Dutilleul, Christelle, Simon Driscoll, Gabriel Cornic, De Paepe, Rosine, Foyer, Christine H., Noctor, Graham
• Format: Article
• Language: English
• Subjects: Amino Acid Oxidoreductases - metabolism; Bioenergetics and Photosynthesis; Biological and medical sciences; Carbon dioxide; Carbon Dioxide - pharmacology; Cell Respiration - physiology; Darkness; Electron Transport - genetics; Electron Transport - physiology; Electron Transport Complex I; Fundamental and applied biological sciences. Psychology; Genotypes; Glycine - metabolism; Glycine Dehydrogenase (Decarboxylating); Irradiance; Leaves; Light; Malate Dehydrogenase (NADP+); Malate Dehydrogenase - metabolism; Metabolism; Mitochondria; Mitochondria - metabolism; Mutants; Mutation; NADH, NADPH Oxidoreductases - metabolism; Nicotiana - genetics; Nicotiana - metabolism; Oxidation; Oxidation-Reduction; Oxygen - metabolism; Photorespiration; Photosynthesis; Photosynthesis - drug effects; Photosynthesis - physiology; Photosynthesis - radiation effects; Photosynthesis, respiration. Anabolism, catabolism; Photosynthetic Reaction Center Complex Proteins - genetics; Photosynthetic Reaction Center Complex Proteins - metabolism; Plant Leaves - genetics; Plant Leaves - metabolism; Plant physiology and development; Plants; Respiration; Ribulose-Bisphosphate Carboxylase - metabolism
• ISSN: 0032-0889; 1532-2548
• DOI: 10.1104/pp.011155

The importance of the mitochondrial electron transport chain in photosynthesis was studied using the tobacco (Nicotiana sylvestris) mutant CMSII, which lacks functional complex I. Rubisco activities and oxygen evolution at saturating CO2 showed that photosynthetic capacity in the mutant was at least as high as in wild-type (WT) leaves. Despite this, steady-state photosynthesis in the mutant was reduced by 20% to 30% at atmospheric CO2 levels. The inhibition of photosynthesis was alleviated by high CO2 or low O2. The mutant showed a prolonged induction of photosynthesis, which was exacerbated in conditions favoring photorespiration and which was accompanied by increased extractable NADP-malate dehydrogenase activity. Feeding experiments with leaf discs demonstrated that CMSII had a lower capacity than the WT for glycine (Gly) oxidation in the dark. Analysis of the postillumination burst in CO2 evolution showed that this was not because of insufficient Gly decarboxylase capacity. Despite the lower rate of Gly metabolism in CMSII leaves in the dark, the Gly to Ser ratio in the light displayed a similar dependence on photosynthesis to the WT. It is concluded that: (a) Mitochondrial complex I is required for optimal photosynthetic performance, despite the operation of alternative dehydrogenases in CMSII; and (b) complex I is necessary to avoid redox disruption of photosynthesis in conditions where leaf mitochondria must oxidize both respiratory and photorespiratory substrates simultaneously.