The radish Ogura fertility restorer impedes translation elongation along its cognate CMS-causing mRNA

Significance Nucleo-cytoplasmic male sterilities (CMS) are two-component genetic systems in which mitochondria-encoded male sterility transcripts are controlled through the action of nuclear-encoded restorer-of-fertility proteins. Fertility restorers most often impact the accumulation of CMS transcripts. In this analysis, we demonstrate that fertility restoration in the Ogura system from radish operates through a specific blockade of ribosome progression along the orf138 CMS transcript. Our analysis reveals that CMS transcripts can be controlled at the translational level, a discovery that will be instrumental to produce custom synthetic fertility restorers. The control of messenger RNA (mRNA) translation has been increasingly recognized as a key regulatory step for gene control, but clear examples in eukaryotes are still scarce. Nucleo-cytoplasmic male sterilities (CMS) represent ideal genetic models to dissect genetic interactions between the mitochondria and the nucleus in plants. This trait is determined by specific mitochondrial genes and is associated with a pollen sterility phenotype that can be suppressed by nuclear genes known as restorer-of-fertility (Rf). In this study, we focused on the Ogura CMS system in rapeseed and showed that reversion to male sterility by the PPR-B fertility restorer (also called Rfo) occurs through a specific translation inhibition of the mitochondria-encoded CMS-causing mRNA orf138. We also demonstrate that PPR-B binds within the coding sequence of orf138 and acts as a ribosome blocker to specifically impede translation elongation along the orf138 mRNA. Rfo is the first recognized fertility restorer shown to act this way. These observations will certainly facilitate the development of synthetic fertility restorers for CMS systems in which efficient natural Rfs are lacking.