Both endogenous processes and exogenous physical and chemical sources generate deoxyribonucleic acid (DNA) damage in the nucleus and organelles of living cells. To prevent deleterious effects, damage is balanced by repair pathways. DNA repair was first documented for the nuclear compartment but evidence was subsequently extended to the organelles. Mitochondria and chloroplasts possess their own repair processes. These share a number of factors with the nucleus but also rely on original mechanisms. Base excision repair remains the best characterized. Repair is organized with the other DNA metabolism pathways in the organelle membrane-associated nucleoids. DNA repair in mitochondria is a regulated, stress-responsive process. Organelle genomes do not encode DNA repair enzymes and translocation of nuclear-encoded repair proteins from the cytosol seems to be a major control mechanism. Finally, changes in the fidelity and efficiency of mitochondrial DNA repair are likely to be involved in DNA damage accumulation, disease and aging. The present review successively addresses these different issues.

Despite constant threat of oxidative damage, sequence drift in mitochondrial and chloroplast DNA usually remains very low in plant species, indicating efficient defense and repair. Whereas the antioxidative defense in the different subcellular compartments is known, the information on DNA repair in plant organelles is still scarce. Focusing on the occurrence of uracil in the DNA, the present work demonstrates that plant mitochondria possess a base excision repair (BER) pathway. In vitro and in organello incision assays of double-stranded oligodeoxyribonucleotides showed that mitochondria isolated from plant cells contain DNA glycosylase activity specific for uracil cleavage. A major proportion of the uracil–DNA glycosylase (UDG) was associated with the membranes, in agreement with the current hypothesis that the DNA is replicated, proofread and repaired in inner membrane-bound nucleoids. Full repair, from uracil excision to thymidine insertion and religation, was obtained in organello following import of a uracil-containing DNA fragment into isolated plant mitochondria. Repair occurred through single nucleotide insertion, which points to short-patch BER. In vivo targeting and in vitro import of GFP fusions showed that the putative UDG encoded by the At3g18 630 locus might be the first enzyme of this mitochondrial pathway in Arabidopsis thaliana.

Expression of the gdh2 gene encoding the alpha-subunit of mitochondrial glutamate dehydrogenase depends on redox state of the mitochondrial electron transport chain. Treatment of Arabidopsis thaliana cell suspension with antimycin A, a respiratory chain complex III inhibitor, resulted in an increase in gdh2 transcripts within 2 h. Inhibition of complex I by rotenone did not influence the transcript level, but treatment with potassium cyanide, a complex IV inhibitor, also increased the transcript content. Thus, gdh2 gene expression obviously responds to changes in the respiratory chain segment localized between complexes I and III. Lack of activation of gene expression after treatment of a cell suspension with hydrogen peroxide and the prooxidant paraquat and results of experiments with antioxidants suggest that gdh2 gene expression is not associated with increased content of reactive oxygen species generated during inhibition of the electron transport chain. Protein phosphorylation by serine/threonine protein kinases is the essential step required for signal transduction into nucleus resulting in the induction of gdh2 expression.