Abstract
In most eukaryotes, organellar genomes are transmitted preferentially by the mother, but the reasons underlying this fundamental biological principle are far from being understood. It is believed that biparental inheritance promotes competition between the cytoplasmic organelles and allows the spread of selfish cytoplasmic elements. Those can be, for example, fast replicating chloroplasts (plastids) that are incompatible with the hybrid nuclear genome and therefore maladaptive.
Here we show, that plastid competition is a metabolic phenotype determined by extremely rapidly evolving regions in the plastid genome of the evening primrose Oenothera. Polymorphisms in repeats of the regulatory region of accD (the only plastid-encoded subunit of the acetyl-CoA carboxylase, which catalyzes the first step of lipid biosynthesis), are responsible for the differences in competitive behavior of different plastid genotypes. These cytoplasmic drive loci change lipid synthesis and consequently lipid profiles of the plastid envelope membrane. This most likely determines plastid division and/or turn-over rates and hence competitiveness. Since plastid competition can result in uniparental inheritance (through elimination of the “weak” plastid) or biparental inheritance (when two similarly “strong” plastids are transmitted), this work uncovers for the first time a genetic determinant of organelle inheritance.