The nucleocytoplasmic conflict, a driving force for the emergence of plant organellar RNA editing.

RNA editing challenges the central dogma of molecular biology by changing the genetic information at the transcript level. In plant organelles, RNAs are modified by deamination of some specific cytosine residues, but the origin of this process remains puzzling. Different from the generally accepted neutral model to explain the emergence of RNA editing in plant organelles, we propose a new hypothesis based on the nucleocytoplasmic conflict theory. We assume that mutations in organellar genomes arose first and spread into the population provided they increased the transmission of their own maternally inherited genome. RNA editing appeared subsequently as a nuclear-encoded correction mechanism to restore the transmission of the nuclear genome. In plants, a well-known consequence of the nucleocytoplasmic conflict is cytoplasmic male sterility (CMS) which is counteracted by the emergence of fertility restorer genes (Rf) belonging to the pentatricopeptide repeat (PPR) protein family. Interestingly, RNA-editing deficiency can lead to CMS, and it now clearly appears that PPR proteins are major players in RNA editing. This striking similarity between the mechanisms of fertility restoration and RNA editing can be explained if both reactions are the consequence of the same driving force, the nucleocytoplasmic conflict. Similarly, the prevalence of RNA editing in eukaryotic organellar genomes could also be a consequence of the genetic antagonism between organellar and nuclear genomes.