Free-radical-induced mutation vs redox regulation: Costs and benefits of genes in organelles

The prokaryotic endosymbionts that became plastids and mitochondria contained genes destined for one of three fates. Genes required for free-living existence were lost. Most genes useful to the symbiosis were transferred to the nucleus of the host. Some genes, a small minority, were retained within the organelle. Here we suggest that a selective advantage of movement of genes to the nucleus is decreased mutation: plastids and mitochondria have high volume-specific rates of redox reactions, producing oxygen free radicals that chemically modify DNA. These mutations lead to synthesis of modified electron carriers that in turn generate more mutagenic free radicals—the “vicious circle” theory of aging. Transfer of genes to the nucleus is also advantageous in facilitating sexual recombination and DNA repair. For genes encoding certain key components of photosynthesis and respiration, direct control of gene expression by redox state of electron carriers may be required to minimize free radical production, providing a selective advantage of organelle location which outweighs that of location in the nucleus. A previous proposal for transfer of genes to the nucleus is an economy of resources in having a single genome and a single apparatus for gene expression, but this argument fails if any organellar gene is retained. A previous proposal for the retention of genes within organelles is that certain proteins are organelle-encoded because they cannot be imported, but there is now evidence against this view. Decreased free radical mutagenesis and increased sexual recombination upon transfer to the nucleus together with redox control of gene expression in organelles may now account for the slightly different gene distributions among nuclei, plastids, and mitochondria found in major eukaryote taxa. This analysis suggests a novel reason for uniparental inheritance of organelles and the evolution of anisogametic sex, and may also account for the occurrence of nitrogen fixation in symbionts rather than in nitrogen-fixing organelles. Correspondence to: J.F. Allen